anystyle 1.1.0 → 1.2.0
Sign up to get free protection for your applications and to get access to all the features.
- checksums.yaml +5 -5
- data/HISTORY.md +9 -0
- data/lib/anystyle.rb +2 -0
- data/lib/anystyle/document.rb +61 -127
- data/lib/anystyle/feature/line.rb +23 -8
- data/lib/anystyle/feature/ref.rb +4 -4
- data/lib/anystyle/finder.rb +4 -4
- data/lib/anystyle/normalizer/locale.rb +17 -6
- data/lib/anystyle/normalizer/names.rb +1 -1
- data/lib/anystyle/page.rb +50 -0
- data/lib/anystyle/refs.rb +244 -0
- data/lib/anystyle/support/finder.mod +5972 -3461
- data/lib/anystyle/support/finder.txt +94 -72
- data/lib/anystyle/support/parser.mod +12876 -12387
- data/lib/anystyle/utils.rb +49 -5
- data/lib/anystyle/version.rb +1 -1
- data/res/finder/bb132pr2055.ttx +20 -20
- data/res/finder/bb408gp7470.ttx +3919 -0
- data/res/finder/bb599nz4341.ttx +5 -5
- data/res/finder/bb725rt6501.ttx +5 -5
- data/res/finder/bc605xz1554.ttx +40 -40
- data/res/finder/bd040gx5718.ttx +15 -15
- data/res/finder/bd413nt2715.ttx +46 -46
- data/res/finder/bf668vw2021.ttx +7 -7
- data/res/finder/bg495cx0468.ttx +19 -19
- data/res/finder/bg599vt3743.ttx +6 -6
- data/res/finder/bg608dx2253.ttx +3 -3
- data/res/finder/bh410qk3771.ttx +23 -23
- data/res/finder/bh989ww6442.ttx +33 -33
- data/res/finder/bj581pc8202.ttx +2 -2
- data/res/parser/core.xml +47 -0
- data/res/parser/gold.xml +59 -8
- metadata +6 -4
- data/res/finder/bb550sh8053.ttx +0 -18660
data/lib/anystyle/utils.rb
CHANGED
@@ -25,18 +25,23 @@ module AnyStyle
|
|
25
25
|
scrub(transliterate(string)).downcase
|
26
26
|
end
|
27
27
|
|
28
|
+
def nnum(string, symbol = '#')
|
29
|
+
string.unicode_normalize.gsub(/\d/, symbol)
|
30
|
+
end
|
31
|
+
|
28
32
|
def page_break?(string)
|
29
33
|
string =~ /\f/
|
30
34
|
end
|
31
35
|
|
32
36
|
def display_width(string)
|
33
|
-
display_chars(string).
|
37
|
+
display_chars(string).length
|
34
38
|
end
|
35
39
|
|
36
40
|
def display_chars(string)
|
37
41
|
string
|
38
42
|
.gsub(/\p{Mn}|\p{Me}|\p{Cc}/, '')
|
39
43
|
.gsub(/\p{Zs}/, ' ')
|
44
|
+
.rstrip
|
40
45
|
end
|
41
46
|
|
42
47
|
def count(string, pattern)
|
@@ -44,7 +49,7 @@ module AnyStyle
|
|
44
49
|
end
|
45
50
|
|
46
51
|
def indent(token)
|
47
|
-
display_chars(token)
|
52
|
+
display_chars(token)[/^(\s*)/].length
|
48
53
|
end
|
49
54
|
|
50
55
|
def strip_html(string)
|
@@ -53,11 +58,13 @@ module AnyStyle
|
|
53
58
|
end
|
54
59
|
end
|
55
60
|
|
56
|
-
module
|
61
|
+
module PDFUtils
|
57
62
|
module_function
|
58
63
|
|
59
|
-
def pdf_to_text(path,
|
60
|
-
%x{pdftotext #{
|
64
|
+
def pdf_to_text(path, **opts)
|
65
|
+
text = %x{pdftotext #{pdf_opts(path, **opts).join(' ')} "#{path}" -}
|
66
|
+
raise "pdftotext failed with error code #{$?.exitstatus}" unless $?.success?
|
67
|
+
text.force_encoding(opts[:encoding] || 'UTF-8')
|
61
68
|
end
|
62
69
|
|
63
70
|
def pdf_info(path)
|
@@ -69,6 +76,43 @@ module AnyStyle
|
|
69
76
|
def pdf_meta(path)
|
70
77
|
%x{pdfinfo -meta -isodates "#{path}"}
|
71
78
|
end
|
79
|
+
|
80
|
+
def pdf_page_size(path)
|
81
|
+
pdf_info(path)['Page size'].scan(/\d+/)[0, 2].map(&:to_i)
|
82
|
+
end
|
83
|
+
|
84
|
+
private
|
85
|
+
|
86
|
+
def pdf_opts(path, layout: true, encoding: 'UTF-8', **opts)
|
87
|
+
[
|
88
|
+
layout ? '-layout' : '',
|
89
|
+
opts[:crop] ? pdf_crop(path, opts[:crop]) : '',
|
90
|
+
'-eol unix',
|
91
|
+
"-enc #{encoding}",
|
92
|
+
'-q'
|
93
|
+
]
|
94
|
+
end
|
95
|
+
|
96
|
+
def pdf_crop(path, args)
|
97
|
+
(x, y, w, h) = case args.length
|
98
|
+
when 1
|
99
|
+
[args[0], args[0], -args[0], -args[0]]
|
100
|
+
when 2
|
101
|
+
[args[0], args[1], -args[0], -args[1]]
|
102
|
+
when 4
|
103
|
+
args
|
104
|
+
else
|
105
|
+
raise "invalid crop option: #{args}"
|
106
|
+
end
|
107
|
+
|
108
|
+
if w < 0 || h < 0
|
109
|
+
(width, height) = pdf_page_size(path)
|
110
|
+
w = width - x + w if w < 0
|
111
|
+
h = height - y + h if h < 0
|
112
|
+
end
|
113
|
+
|
114
|
+
"-x #{x} -y #{y} -W #{w} -H #{h}"
|
115
|
+
end
|
72
116
|
end
|
73
117
|
|
74
118
|
extend Utils
|
data/lib/anystyle/version.rb
CHANGED
data/res/finder/bb132pr2055.ttx
CHANGED
@@ -241,7 +241,7 @@ blank |
|
|
241
241
|
|
|
242
242
|
|
|
243
243
|
meta | ix
|
244
|
-
|
244
|
+
title | Chapter 1
|
245
245
|
blank |
|
246
246
|
title | Introduction
|
247
247
|
blank |
|
@@ -261,8 +261,8 @@ blank |
|
|
261
261
|
text | The reason Bernanke took such a public stand defending the Fed’s independence
|
262
262
|
| is simple: central bank independence is widely seen as a necessary condition for the
|
263
263
|
| attainment of economic and financial stability. Thus, Bernanke and central bankers
|
264
|
-
|
265
|
-
|
264
|
+
meta | 1
|
265
|
+
text | Text of full statement is available at http://www.federalreserve.gov/newsevents/speech/
|
266
266
|
| bernanke20100203a.htm.
|
267
267
|
blank |
|
268
268
|
|
|
@@ -293,8 +293,8 @@ text | everywhere have a substantial interest in promoting the idea tha
|
|
293
293
|
| thereby ignoring the crucial role that central banks play as lenders of last resort.
|
294
294
|
| Other studies have taken a more targeted approach in studying the impact of
|
295
295
|
| politics on policymaking at the Fed by asking whether or not monetary policy becomes
|
296
|
-
|
297
|
-
|
296
|
+
meta | 2
|
297
|
+
text | For a review of the literature investigating this relationship, see Eijffinger and de Haan (1996).
|
298
298
|
| Bade and Parkin (1988), Alesina (1988), Grilli, Masciandaro and Tabellini (1991), Cukierman, Web
|
299
299
|
| and Neyapti (1992), Alesina and Summers (1993), Eijffinger, Van Rooij and Schaling (1996), Berger,
|
300
300
|
| De Haan and Eijffinger (2001), and Keefer and Stasavage (2003), among others, provide additional
|
@@ -389,7 +389,7 @@ blank |
|
|
389
389
|
text | to remain insulated from external political pressure is imperfect.
|
390
390
|
| I conclude in Chapter 5 by discussing the implications of my findings and mapping
|
391
391
|
| out some research projects that are natural extensions of this work.
|
392
|
-
|
392
|
+
title | Chapter 2
|
393
393
|
blank |
|
394
394
|
title | The Politics Behind the Federal
|
395
395
|
| Reserve’s Structure
|
@@ -1208,8 +1208,8 @@ text | Paired Paired
|
|
1208
1208
|
| Republican 6 34 0 3 1 44
|
1209
1209
|
| Progressive 1 0 0 0 0 1
|
1210
1210
|
| Total 54 34 3 3 1 95
|
1211
|
-
|
1212
|
-
|
1211
|
+
meta | 19
|
1212
|
+
text | This small group of midwesterners, led by Lindberg, opposed any sort of central bank.
|
1213
1213
|
meta | CHAPTER 2. THE POLITICS BEHIND THE FED’S STRUCTURE 35
|
1214
1214
|
blank |
|
1215
1215
|
|
|
@@ -2744,9 +2744,9 @@ text | Table 2.11: Partisan Preferences in 19
|
|
2744
2744
|
| R2 Edward non-eastern B Horizontal cost of moving away from their
|
2745
2745
|
| Vreeland bankers desired level of centralization
|
2746
2746
|
| Key: A = politicized central bank
|
2747
|
-
|
2747
|
+
| B = decentralized, private bank with autonomous branches
|
2748
2748
|
| C = centralized bank controlled by Wall Street
|
2749
|
-
|
2749
|
+
meta | CHAPTER 2. THE POLITICS BEHIND THE FED’S STRUCTURE 86
|
2750
2750
|
blank |
|
2751
2751
|
|
|
2752
2752
|
|
|
@@ -2765,7 +2765,7 @@ blank |
|
|
2765
2765
|
|
|
2766
2766
|
text | Figure 2.14: Could the Banking Act have Passed Had the Composition of Congress
|
2767
2767
|
| Not Changed Between 1913 and 1935?
|
2768
|
-
|
2768
|
+
title | Chapter 3
|
2769
2769
|
blank |
|
2770
2770
|
title | The Fed as a Political Agent: How
|
2771
2771
|
| Partisan Central Bankers Allow
|
@@ -3079,7 +3079,7 @@ blank |
|
|
3079
3079
|
|
|
3080
3080
|
title | 3.2 Do We Know if There is a Political Business
|
3081
3081
|
blank |
|
3082
|
-
|
3082
|
+
title | Cycle in Monetary Policy?
|
3083
3083
|
blank |
|
3084
3084
|
text | Most studies assessing the presence of a political business cycle in monetary policy
|
3085
3085
|
| have decided against pursuing this more fine-grained, individual-level analysis and
|
@@ -3628,8 +3628,8 @@ text | partisan identity by using information from press reports at the
|
|
3628
3628
|
| four are Independents, and five are Republicans. The remaining 15 are not able to be
|
3629
3629
|
| identified, since they either are (or were) not a registered voter or are not included in
|
3630
3630
|
| the Catalist voter file that I have access to through my university’s subscription.34
|
3631
|
-
|
3632
|
-
|
3631
|
+
meta | 33
|
3632
|
+
text | Other studies using Catalist for data on voter registrations include Ansolabehere and Hersh
|
3633
3633
|
| (2012), Hersh and Nall (2013), and Peterson (2014).
|
3634
3634
|
meta | 34
|
3635
3635
|
text | The subscription is for only a subset of the entire Catalist national voter file.
|
@@ -4363,7 +4363,7 @@ meta | Note: p<0.1; p<0
|
|
4363
4363
|
blank |
|
4364
4364
|
|
|
4365
4365
|
text | Figure 3.5: Power Analysis: Democratic Elections’ Effect on FOMC Republicans
|
4366
|
-
|
4366
|
+
title | Chapter 4
|
4367
4367
|
blank |
|
4368
4368
|
title | The Role of Politics in the Federal
|
4369
4369
|
| Reserve’s Lending during the
|
@@ -4874,8 +4874,8 @@ text | officials expending their legislative resources on issues unrela
|
|
4874
4874
|
| respondence (i.e., letters) issued between the board and Congress pertaining to the
|
4875
4875
|
| Fed’s emergency lending during the financial crisis.19
|
4876
4876
|
| The over 3,300 pages that were released included 69 letters from congresspersons
|
4877
|
-
|
4878
|
-
|
4877
|
+
meta | 16
|
4878
|
+
text | This point is even more true if the campaign contributions are made to politicians that are never
|
4879
4879
|
| even elected to office. After all, a firm can make a campaign contribution for many reasons, not just
|
4880
4880
|
| to try to influence the Fed’s lending.
|
4881
4881
|
meta | 17
|
@@ -5891,8 +5891,8 @@ blank |
|
|
5891
5891
|
|
|
5892
5892
|
|
|
5893
5893
|
|
|
5894
|
-
|
5895
|
-
|
5894
|
+
text | (c) Political Entity: Letter Writers
|
5895
|
+
meta | CHAPTER 4. THE ROLE OF POLITICS IN THE FED’S LENDING 184
|
5896
5896
|
blank |
|
5897
5897
|
|
|
5898
5898
|
|
|
@@ -5957,7 +5957,7 @@ text | Figure 4.3: Financial Covariates’ Marginal Effects on Income
|
|
5957
5957
|
| AIC used by Stata 3709.097 3705.628 3702.708 3705.485 3699.858 3696.849 3698.747
|
5958
5958
|
meta | CHAPTER 4. THE ROLE OF POLITICS IN THE FED’S LENDING
|
5959
5959
|
| 186
|
5960
|
-
|
5960
|
+
title | Chapter 5
|
5961
5961
|
blank |
|
5962
5962
|
title | Conclusion
|
5963
5963
|
blank |
|
@@ -0,0 +1,3919 @@
|
|
1
|
+
title | FUNCTIONAL TRAIT MEDIATION OF PLANT-ANIMAL INTERACTIONS:
|
2
|
+
| EFFECTS OF DEFAUNATION ON PLANT FUNCTIONAL DIVERSITY IN A
|
3
|
+
| NEOTROPICAL FOREST
|
4
|
+
blank |
|
5
|
+
|
|
6
|
+
|
|
7
|
+
|
|
8
|
+
text | A DISSERTATION
|
9
|
+
| SUBMITTED TO THE DEPARTMENT OF BIOLOGY
|
10
|
+
| AND THE COMMITTEE ON GRADUATE STUDIES
|
11
|
+
| OF STANFORD UNIVERSITY
|
12
|
+
| IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF
|
13
|
+
| DOCTOR OF PHILOSOPHY
|
14
|
+
blank |
|
15
|
+
|
|
16
|
+
|
|
17
|
+
|
|
18
|
+
text | Erin Leigh Kurten
|
19
|
+
| August 2010
|
20
|
+
| © 2010 by Erin Leigh Kurten. All Rights Reserved.
|
21
|
+
| Re-distributed by Stanford University under license with the author.
|
22
|
+
blank |
|
23
|
+
|
|
24
|
+
|
|
25
|
+
text | This work is licensed under a Creative Commons Attribution-
|
26
|
+
| Noncommercial 3.0 United States License.
|
27
|
+
| http://creativecommons.org/licenses/by-nc/3.0/us/
|
28
|
+
blank |
|
29
|
+
|
|
30
|
+
|
|
31
|
+
|
|
32
|
+
text | This dissertation is online at: http://purl.stanford.edu/bb408gp7470
|
33
|
+
blank |
|
34
|
+
|
|
35
|
+
|
|
36
|
+
|
|
37
|
+
meta | ii
|
38
|
+
text | I certify that I have read this dissertation and that, in my opinion, it is fully adequate
|
39
|
+
| in scope and quality as a dissertation for the degree of Doctor of Philosophy.
|
40
|
+
blank |
|
41
|
+
text | Rodolfo Dirzo, Primary Adviser
|
42
|
+
blank |
|
43
|
+
|
|
44
|
+
|
|
45
|
+
text | I certify that I have read this dissertation and that, in my opinion, it is fully adequate
|
46
|
+
| in scope and quality as a dissertation for the degree of Doctor of Philosophy.
|
47
|
+
blank |
|
48
|
+
text | Peter Vitousek
|
49
|
+
blank |
|
50
|
+
|
|
51
|
+
|
|
52
|
+
text | I certify that I have read this dissertation and that, in my opinion, it is fully adequate
|
53
|
+
| in scope and quality as a dissertation for the degree of Doctor of Philosophy.
|
54
|
+
blank |
|
55
|
+
text | David Ackerly
|
56
|
+
blank |
|
57
|
+
|
|
58
|
+
|
|
59
|
+
|
|
60
|
+
text | Approved for the Stanford University Committee on Graduate Studies.
|
61
|
+
| Patricia J. Gumport, Vice Provost Graduate Education
|
62
|
+
blank |
|
63
|
+
|
|
64
|
+
|
|
65
|
+
|
|
66
|
+
text | This signature page was generated electronically upon submission of this dissertation in
|
67
|
+
| electronic format. An original signed hard copy of the signature page is on file in
|
68
|
+
| University Archives.
|
69
|
+
blank |
|
70
|
+
|
|
71
|
+
|
|
72
|
+
|
|
73
|
+
meta | iii
|
74
|
+
title | Preface
|
75
|
+
| Dissertation Abstract
|
76
|
+
text | This dissertation examines how terrestrial vertebrates, as seed dispersers, seed
|
77
|
+
| predators and herbivores, influence plant functional trait composition in tropical forests and
|
78
|
+
| thereby diversity. I conducted this work in the Barro Colorado National Monument (BCNM)
|
79
|
+
| in Central Panama, where a long term mammal exclosure experiment has been ongoing, and in
|
80
|
+
| neighboring Parque Nacional Soberanía (PNS), which together with the BCNM forms a
|
81
|
+
| defaunation gradient driven by hunting.
|
82
|
+
| I first comprehensively review what is known about how the loss of vertebrates in
|
83
|
+
| tropical forests alters plant-animal interactions, plant demography, and plant diversity.
|
84
|
+
| Defaunation consistently lowers primary dispersal and creates a seed shadow that is more
|
85
|
+
| dense around the parent tree and less dense at sites farther away. However, it also often
|
86
|
+
| lowers seed predation by rodents, and as a consequence, species with rodents as seed predators
|
87
|
+
| and dispersers often benefit from defaunation. While demographic and diversity responses
|
88
|
+
| tend to be more mixed, a few consistent trends emerge. Community dominance tends to
|
89
|
+
| increase in response to defaunation. Often, plants with particular functional traits or abiotic or
|
90
|
+
| unhunted dispersal agents are favored by defaunation.
|
91
|
+
| I next examined how community-level functional trait composition shifts in seedling
|
92
|
+
| communities (Chapter 2) and sapling communities (Chapter 3) which have experienced
|
93
|
+
| exclosure from terrestrial mammals. Seedling communities in exclosures had higher median
|
94
|
+
| seed mass than paired plots open to the mammal community, but treatments did not differ in
|
95
|
+
| their leaf traits (leaf mass per area and laminar toughness) or wood density. In contrast to the
|
96
|
+
| seedling community, the sapling community did show significant shifts toward higher specific
|
97
|
+
| leaf area and lower leaf toughness in response to herbivore exclosure, primarily due to an
|
98
|
+
| increased dominance of species with those traits, and secondarily due to differences in the
|
99
|
+
blank |
|
100
|
+
|
|
101
|
+
|
|
102
|
+
meta | iv
|
103
|
+
text | species present in each treatment type. These data, combined with data from PNS, also
|
104
|
+
| suggest that hunting results in community mean wood density in seedling communities, due to
|
105
|
+
| a disproportionate number of high wood density species relying on hunted animals for their
|
106
|
+
| seed dispersal.
|
107
|
+
| Finally, I investigated the seed size response to changes in mammal abundance by
|
108
|
+
| measuring vertebrate seed predation rates in a protected and hunted forest (Chapter 4). I
|
109
|
+
| found that in central Panama, seed mass does not correlate well with either body size of the
|
110
|
+
| seed predator, or vertebrate seed predation rates. I suggest that rather than formulate seed
|
111
|
+
| predation rates as a linear function of seed predator abundance, these interactions may be
|
112
|
+
| better modeled as threshold-dependent processes.
|
113
|
+
blank |
|
114
|
+
|
|
115
|
+
text | This work suggests that terrestrial vertebrates play an underappreciated role in maintaining
|
116
|
+
| plant diversity and that pan-tropical levels of unsustainable hunting may indirectly lead to
|
117
|
+
| losses of plant biodiversity.
|
118
|
+
blank |
|
119
|
+
|
|
120
|
+
|
|
121
|
+
|
|
122
|
+
meta | v
|
123
|
+
title | Acknowledgments
|
124
|
+
text | My deep gratitude goes to my two advisors, Rodolfo Dirzo and David Ackerly, for giving me
|
125
|
+
| the flexibility and support to pursue this work. Rodolfo’s generosity as a teacher and advisor,
|
126
|
+
| and his tireless contributions to teaching, research and conservation, both at Stanford and
|
127
|
+
| internationally, are a great inspiration to me. I am thankful to David for graciously and
|
128
|
+
| supportively allowing me to build a network of intellectual support that allowed me to
|
129
|
+
| successfully complete this journey. He has also been an excellent intellectual role model for
|
130
|
+
| me, challenging me to grapple with complexity and nuance and to confront problems from
|
131
|
+
| new perspectives.
|
132
|
+
| Joe Wright has been a generous and supportive mentor and collaborator throughout
|
133
|
+
| my time at the Smithsonian Tropical Research Institute, and some of this work would not have
|
134
|
+
| been possible without his contributions. Peter Vitousek contributed many insightful
|
135
|
+
| suggestions throughout the course of this work as a committee member, and his service
|
136
|
+
| activities, from facilitating collaboration among scientists in Hawaii, to the First Nations’
|
137
|
+
| Futures Program, have also inspired me. I also thank Fio Micheli for her enthusiasm as a
|
138
|
+
| committee member and for helping me frame my work in a broader context. Walter Carson
|
139
|
+
| very generously permitted me to work on the long-term mammal exclosure experiment he
|
140
|
+
| established in the Barro Colorado National Monument in Panama and shared with me his
|
141
|
+
| long-term datasets.
|
142
|
+
| The communities at Stanford, Berkeley and STRI were essential in shaping my
|
143
|
+
| graduate school experience. At Stanford, Will Cornwell, Nathan Kraft, Virginia Maztek,
|
144
|
+
| Steve Allison, Stephen Porder, Katie Amatangelo, Jen Funk, Camila Donatti, and Mauro
|
145
|
+
| Galetti provided helpful feedback and support throughout the various stages of my work.
|
146
|
+
| Doug Turner was an essential help in analyzing leaf nutrients, both for chapter three, and work
|
147
|
+
| not included in this thesis. Alex Royo, Allen Herre, Scott Magnan, Liza Comita, Mike Tobin,
|
148
|
+
blank |
|
149
|
+
|
|
150
|
+
meta | vi
|
151
|
+
text | Patrick Jansen, Noelle Beckman, Roland Kays, Jackie Willis, Stephan Schnitzer generously
|
152
|
+
| shared their advice and knowledge of the field site with me, improving the feasibility and
|
153
|
+
| execution of this work.
|
154
|
+
| Many thanks go to the botanists at BCI. Without their assistance, this work would not
|
155
|
+
| have been possible. Andrés Hernández, Oldemar Valdes, David Brassfield, and Osvaldo
|
156
|
+
| Calderón were always happy to help me identify whatever leaf, fruit, seed, or flower I
|
157
|
+
| brought to their office. Andrés and Oldemar in particular taught me most of what I know
|
158
|
+
| about the BCI flora.
|
159
|
+
| Many paid and volunteer field and lab assistants helped to make this work possible.
|
160
|
+
| Lissie Jiménez helped immensely with the collection and processing of the thousands of
|
161
|
+
| leaves collected for Chapter three. Ana Patricia Calderón and Rousmery Bethancourt
|
162
|
+
| contributed many early mornings conducting mammal transect surveys. Clare Sherman was
|
163
|
+
| such a dedicated help in the lab and fieldwork for chapter 4, that I sometimes had to remind
|
164
|
+
| her to take a break and have some fun. Susan Rebellon helped with the pilot studies for
|
165
|
+
| chapter four, and also with leaf sample processing at Stanford. Gaspar Bruner, Karen
|
166
|
+
| Kapheim, Adam Roddy, and David Bethancourt, helped me recover (most of) my leaf
|
167
|
+
| samples after they were destroyed in a freezer accident.
|
168
|
+
| I would also like to thank staff at Stanford and STRI who helped make the logistical
|
169
|
+
| aspects of this work easier. The competence of Pam Hung, Oris Acevedo, Belkys Jiménez,
|
170
|
+
| Orelis Arosemana, and Marcela Paz made them a pleasure to work with. The Falconer library
|
171
|
+
| and copy staff, as well as Allen Smith, did their best to get me the literature I needed, despite
|
172
|
+
| STRI’s rigorous firewall. Valerie Kiszka and Jennifer Mason helped with countless
|
173
|
+
| administrative tasks and advice during my time as a student at Stanford.
|
174
|
+
blank |
|
175
|
+
|
|
176
|
+
|
|
177
|
+
|
|
178
|
+
meta | vii
|
179
|
+
title | Contents
|
180
|
+
text | Preface iv
|
181
|
+
| Acknowledgements vi
|
182
|
+
| List of tables ix
|
183
|
+
| List of figures x
|
184
|
+
blank |
|
185
|
+
text | Introduction………………………………………………………………………... 1
|
186
|
+
| 1 Contemporaneous defaunation and cascading effects on tropical forests…...… 3
|
187
|
+
| Introduction…………………………………………………………………. 3
|
188
|
+
| Scope of Review……………………………………………………………. 4
|
189
|
+
| Methodology………………………………………………………………... 5
|
190
|
+
| Plant-animal interactions………………………………………………….... 7
|
191
|
+
| Seed dispersal……………………………………………………….... 7
|
192
|
+
| Seed Predation………………………………………………………… 14
|
193
|
+
| Herbivory & Trampling…………………………………………….… 17
|
194
|
+
| Plant Demography……………………………………………………….…. 17
|
195
|
+
| Recruitment…………………………………………………………… 17
|
196
|
+
| Seedling survival……………………………………………………… 19
|
197
|
+
| Standing abundance……………………………………………….….. 20
|
198
|
+
| Linking Dispersal and Seedling Recruitment………………………… 22
|
199
|
+
| Community Diversity….…………………………………………………… 24
|
200
|
+
| Seedling density………………………………………………………. 24
|
201
|
+
| Diversity……………………………………………………………… 24
|
202
|
+
| Plant Functional Groups……………………………………………… 25
|
203
|
+
| What is defaunation? ………………………………………………………. 27
|
204
|
+
| Heterogeneity Among Studies……………………………………………… 28
|
205
|
+
| Conclusions……………………………………………………………….… 29
|
206
|
+
| Appendix 1.1……………………………………………………………..… 30
|
207
|
+
blank |
|
208
|
+
text | 2 Reduced seed dispersal as a consequence of hunting lowers community-level
|
209
|
+
| wood density in a Neotropical forest ……………………………………… 35
|
210
|
+
| Abstract…………………………………………………………………… 35
|
211
|
+
| Introduction……………………………………………………………..…. 36
|
212
|
+
blank |
|
213
|
+
|
|
214
|
+
meta | viii
|
215
|
+
text | Methods…………………………………………………………………… 38
|
216
|
+
| Results…………………………………………………………………….. 41
|
217
|
+
| Discussion………………………………………………………………… 45
|
218
|
+
| Acknowledgments………………………………………………………….. 49
|
219
|
+
blank |
|
220
|
+
text | 3 Terrestrial mammalian herbivores influence the distribution of defense and
|
221
|
+
| nutrient traits in a Neotropical forest………………………………………….. 51
|
222
|
+
| Abstract………………………..…………………………………………… 51
|
223
|
+
| Introduction…………………………………………………………………. 52
|
224
|
+
| Methods……………………..……………………………………………… 54
|
225
|
+
| Results……………………..……………………………………………….. 56
|
226
|
+
| Discussion……………..…………………………………………………… 61
|
227
|
+
| Acknowledgments………………………………………………………….. 65
|
228
|
+
blank |
|
229
|
+
text | 4 Hunting does not alter seed predation rates as a function of seed size in a
|
230
|
+
| Neotropical forest……………………………………………………………… 67
|
231
|
+
| Abstract…………………………………………………………………..… 67
|
232
|
+
| Introduction………………………………………………………………... 68
|
233
|
+
| Methods…………………………………………………………………..… 72
|
234
|
+
| Results………………………………………………………………………. 76
|
235
|
+
| Discussion………………………………………………………………..… 81
|
236
|
+
| Conclusion…………………………………………………………………... 86
|
237
|
+
| Acknowledgments………………………………………………………….. 86
|
238
|
+
blank |
|
239
|
+
text | Bibliography………………………………………………………………………. 87
|
240
|
+
blank |
|
241
|
+
|
|
242
|
+
|
|
243
|
+
|
|
244
|
+
title | List of Tables
|
245
|
+
text | 3.1 The number of species and stems for which traits were measured………….. 57
|
246
|
+
| 3.2 R2 values for pair-wise correlations between species mean trait values ……... 57
|
247
|
+
| 3.3 Effect of species and exclosure on variation in leaf toughness……….. 61
|
248
|
+
| 4.1 Mean fresh seed masses of study species……………………………... 75
|
249
|
+
blank |
|
250
|
+
|
|
251
|
+
|
|
252
|
+
|
|
253
|
+
meta | ix
|
254
|
+
title | List of Figures
|
255
|
+
text | 1.1 Primary seed dispersal in defaunated sites relative to non-defaunated
|
256
|
+
| sites…………………………………………………………………… 9
|
257
|
+
| 1.2 Differences in seed caching in defaunated sites relative to non-
|
258
|
+
| defaunated sites……………………………………………………… 10
|
259
|
+
| 1.3 Changes in seedling distribution as a consequence of defaunation…… 13
|
260
|
+
| 1.4 Differences in vertebrate seed predation rates as a consequence of
|
261
|
+
| defaunation……………………………………………………………. 16
|
262
|
+
| 1.5 Differences in invertebrate seed predation rates as a consequence of
|
263
|
+
| defaunation……………………………………………………………. 17
|
264
|
+
| 1.6 Plant recruitment responses to defaunation for seedlings and saplings.. 19
|
265
|
+
| 1.7 Seedling survival in defaunated sites relative to non-defaunated sites.. 20
|
266
|
+
| 1.8 Differences in seedling densities in defaunated sites relative to non-
|
267
|
+
| defaunated sites……………………………………………………….. 22
|
268
|
+
| 1.9 Community-level herb densities in defaunation forest comparisons
|
269
|
+
| and mammal exclosure experiments………………………………….. 24
|
270
|
+
| 1.10 Differences in species richness, dominance, and diversity for
|
271
|
+
| defaunation forest comparisons and mammal exclosure experiments... 26
|
272
|
+
| 2.1 Vertebrate activity in open and exclosure plots……………………….. 41
|
273
|
+
| 2.2 Proportion of seedlings by dispersal mode class in open and exclosure 42
|
274
|
+
| treatments……………………………………………………………..
|
275
|
+
| 2.3 Proportion of seedlings by life form class in open and exclosure 42
|
276
|
+
| treatments……………………………………………………………..
|
277
|
+
| 2.4 Median seed mass is significantly higher in exclosures……………… 43
|
278
|
+
| 2.5 Effects of exclosure and hunting on community median wood density. 44
|
279
|
+
| 2.6 Associations between dispersal agents and species wood specific
|
280
|
+
| gravity………………………………………………………………… 45
|
281
|
+
| 3.1 Changes in plot-level trait means, unweighted by species abundance... 58
|
282
|
+
| 3.2 Abundance-weighted, plot-level trait means in open and exclosure
|
283
|
+
| plots…………………………………………………………………… 59
|
284
|
+
| 3.3 Intraspecific differences in species’ mean leaf toughness……………. 60
|
285
|
+
| 4.1 Model of how seed predation should vary with seed mass as a
|
286
|
+
| function of defaunation intensity…………………………………….. 71
|
287
|
+
| 4.2 Map of Lake Gatun study area……………………………………….. 73
|
288
|
+
| 4.3 Animal abundances in BCI and PNS in 2008………………………… 77
|
289
|
+
blank |
|
290
|
+
meta | x
|
291
|
+
text | 4.4 Seed predation rates as a function of seed size……………………….. 78
|
292
|
+
| 4.5 Number of palm seed cached in BCI and PNS………………………... 79
|
293
|
+
| 4.6 Identity of species removing seeds…………………………………… 80
|
294
|
+
| 4.7 Published studies examining seed predation of large-seeded palms….. 85
|
295
|
+
blank |
|
296
|
+
|
|
297
|
+
|
|
298
|
+
|
|
299
|
+
meta | xi
|
300
|
+
| 1
|
301
|
+
blank |
|
302
|
+
|
|
303
|
+
|
|
304
|
+
|
|
305
|
+
title | Introduction
|
306
|
+
text | Tropical forests are among the most biodiverse ecosystems on the planet. Many
|
307
|
+
| mechanisms have been proposed to explain the maintenance of that diversity,
|
308
|
+
| including negative distance- or density- dependent mortality, niche partitioning, and
|
309
|
+
| neutral processes. However, little attention has been paid to the role vertebrate
|
310
|
+
| consumers play in maintaining tropical diversity. Evidence from defaunated tropical
|
311
|
+
| forests suggests that these animals play a critical role in diversity maintenance
|
312
|
+
| (Chapter 1). This dissertation examines how terrestrial vertebrates, as seed dispersers,
|
313
|
+
| seed predators and herbivores, influence plant community composition in tropical
|
314
|
+
| forests and thereby levels of diversity. Specifically, I used plant functional traits as a
|
315
|
+
| lens through which to observe changes in seedling and sapling communities, identify
|
316
|
+
| which guilds of consumers were responsible for the changes, and elucidate trait-
|
317
|
+
| mediated mechanisms for the observed change. This work suggests that terrestrial
|
318
|
+
| vertebrates play an underappreciated role in maintaining plant diversity and that pan-
|
319
|
+
| tropical levels of unsustainable hunting may indirectly lead to losses of plant
|
320
|
+
| biodiversity.
|
321
|
+
| I first examined how community-level functional trait composition shifts in
|
322
|
+
| seedling communities which have been protected from terrestrial mammals (Chapter
|
323
|
+
| 2). I conducted this work in the Barro Colorado National Monument in Central
|
324
|
+
| Panama, where a long term mammal exclosure experiment was established in 1993-
|
325
|
+
| 94, and where terrestrial mammals are relatively abundant. I found that seedling
|
326
|
+
| communities in exclosures did not differ in their dispersal mode or in the relative
|
327
|
+
| abundance of free standing and climbing growth forms, as may be expected in an
|
328
|
+
| experiment that did not manipulate primary dispersal agents. Seedling communities in
|
329
|
+
| exclosures had higher median seed mass than paired plots open to the mammal
|
330
|
+
| community, but treatments did not differ in their leaf traits (leaf mass per area and
|
331
|
+
meta | 2 INTRODUCTION
|
332
|
+
blank |
|
333
|
+
|
|
334
|
+
text | laminar toughness) or wood density. These results were validated with similar data
|
335
|
+
| from a defaunation gradient in the same region of Central Panama. One key contrast
|
336
|
+
| to the exclosure, however, was that seedling communities in defaunated sites had a
|
337
|
+
| higher representation of species with abiotic dispersal modes, lianas, and species with
|
338
|
+
| lower wood densities, which is consistent with the fact that primary dispersers are
|
339
|
+
| impacted by hunting.
|
340
|
+
| I next examined the sapling community in the exclosure experiment to evaluate
|
341
|
+
| the effects of herbivores specifically, and to identify the relative contributions of
|
342
|
+
| altered species present, abundance, and trait expression to the differences in functional
|
343
|
+
| trait composition observed (Chapter 3). In contrast to the seedling community, the
|
344
|
+
| sapling community did show significant shifts toward higher leaf nitrogen and lower
|
345
|
+
| leaf toughness in response to herbivore exclosure, primarily due to an increased
|
346
|
+
| dominance of species with those traits, and secondarily due to differences in the
|
347
|
+
| species present in each treatment type. Interestingly, I also found evidence that
|
348
|
+
| intraspecific differences in leaf traits were also contributing minorly to changes in
|
349
|
+
| community mean leaf toughness, though whether this is the result of differential
|
350
|
+
| mortality among genotypes or microhabitats, or a plastic response to decreased
|
351
|
+
| mammalian herbivory is unknown.
|
352
|
+
| Finally, I investigated the seed size response to changes in mammal abundance
|
353
|
+
| by measuring vertebrate seed predation rates in a protected and hunted forest (Chapter
|
354
|
+
| 4). I aimed to both test a model of how seed predation rates should vary with seed size
|
355
|
+
| and defaunation intensity, and potentially clarify discrepancies in community level
|
356
|
+
| seed-size responses to hunting at different sites. I found that in central Panama, seed
|
357
|
+
| mass does not correlate well with either body size of the seed predator, or vertebrate
|
358
|
+
| seed predation rates. In fact, I found little difference in seed predation rates between
|
359
|
+
| the protected and hunted forests, despite large differences in key seed predators such
|
360
|
+
| as peccaries and agoutis. I suggest that rather than formulate seed predation rates as a
|
361
|
+
| linear function of seed predator abundance, these interactions may be better modeled
|
362
|
+
| as threshold-dependent processes.
|
363
|
+
meta | 3
|
364
|
+
blank |
|
365
|
+
|
|
366
|
+
|
|
367
|
+
|
|
368
|
+
title | Chapter 1
|
369
|
+
blank |
|
370
|
+
title | Contemporaneous defaunation and
|
371
|
+
| cascading effects on tropical forests
|
372
|
+
| Erin. L. Kurten, Mauro Galetti
|
373
|
+
blank |
|
374
|
+
|
|
375
|
+
title | INTRODUCTION
|
376
|
+
blank |
|
377
|
+
text | Large bodied vertebrates have been subject to human hunting for millennia. At
|
378
|
+
| the end of the Pleistocene, a diversity of large mammals became extinct worldwide,
|
379
|
+
| with human overhunting likely being one of the major drivers (Barnosky et al. 2004).
|
380
|
+
| The extinction of mammoth, giant sloths, giant kangaroos, giant deer, and many more
|
381
|
+
| megafauna in such a short time likely changed the structure and composition of their
|
382
|
+
| associated plant communities (Zimov et al. 1995, Guimares et al. 2008, Johnson
|
383
|
+
| 2009).
|
384
|
+
| The extinction of large vertebrates is not a phenomenon restricted to the past,
|
385
|
+
| but rather continues in the present day. While scientists still debate what caused the
|
386
|
+
| Pleistocene megafaunal extinction (Alroy 2001; de Vivo & Carmignotto 2004; Koch
|
387
|
+
| & Barnosky 2006; Webb 2008), there is little doubt that human activities are
|
388
|
+
| resposible for threatening the persistence of approximately 22 percent of all mammal
|
389
|
+
| and 12 percent of all bird species in the world today (Pimm et al. 2006). Particularly
|
390
|
+
| in tropical forests, animal populations are currently in decline due to both
|
391
|
+
meta | 4 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
392
|
+
blank |
|
393
|
+
|
|
394
|
+
|
|
395
|
+
text | unsustainable hunting and habitat fragmentation throughout Asia (Corlett 2007),
|
396
|
+
| Africa (Fa & Brown 2009) and Latin America (Peres & Palacios 2007).
|
397
|
+
| Whether changes in vegetation structure and composition have occurred as a
|
398
|
+
| result of the extinction of the megafauna or climate change in the past, the effects of
|
399
|
+
| comtemporaneous defaunation on vegetation is measurable. In many parts of the
|
400
|
+
| tropics, plants have lost their major seeds dispersers, seed predators, and herbivores,
|
401
|
+
| likely altering plant demography, spatial distribution, genetic diversity and selection
|
402
|
+
| on seed and plant defense traits within species, with cascading effects on community
|
403
|
+
| composition and diversity.
|
404
|
+
blank |
|
405
|
+
title | SCOPE OF REVIEW
|
406
|
+
blank |
|
407
|
+
text | Because the animals most vulnerable to defaunation, as well as their less vulnerable
|
408
|
+
| competitors, interact with plants as seed dispersers, seed predators, seedling predators,
|
409
|
+
| and herbivores, contemporaneous defaunation is likely to disrupt plant-vertebrate
|
410
|
+
| interactions. Several papers have outlined in detail how species interactions and plant
|
411
|
+
| communities are likely to change as a consequence of these disruptions (Wright 2003,
|
412
|
+
| Dirzo et al. 2007, Muller-Landau 2007). Disruptions of seed dispersal are likely to
|
413
|
+
| have negative effects on plant recruitment by preventing individuals from escaping
|
414
|
+
| distance-dependent and density-dependent mortality (sensu Janzen 1970, Connell
|
415
|
+
| 1971). Reduced seed dispersal may also prevent light-demanding species, or species
|
416
|
+
| with other specific environmental requirements, from reaching sites favorable for
|
417
|
+
| recruitment (Muller-Landau 2007, Brodie et al. 2009). Changes in seed predation,
|
418
|
+
| seedling predation, and herbivory may have positive or negative effects on species
|
419
|
+
| recruitment by altering seed and seedling survival (Wright 2003, Dirzo et al. 2007,
|
420
|
+
| Muller-Landau 2007). Changes in seed predation and seedling predation may have
|
421
|
+
| further indirect benefits for invertebrate seed predators and herbivores.
|
422
|
+
| Overall, the net effect of defaunation on plant diversity has been hypothesized
|
423
|
+
| to be negative (Wright 2003, Muller-Landau 2007) This is both because it is thought
|
424
|
+
| that species experiencing reduced seed dispersal will not persist if they cannot escape
|
425
|
+
meta | 5
|
426
|
+
blank |
|
427
|
+
|
|
428
|
+
|
|
429
|
+
text | distance-dependent or density-dependent mortality, and because seed predators and
|
430
|
+
| herbivores will not suppress populations of competitively dominant species.
|
431
|
+
| Here we synthesize what is currently known about the indirect effects of
|
432
|
+
| defaunation on tropical plants, in the context of hunting, forest fragmentation, and
|
433
|
+
| animal exclosure. We divide our analysis into three sections, addressing effects on
|
434
|
+
| plant-animal interactions, population demography, and community diversity. Our first
|
435
|
+
| goal was to evaluate the extent to which the hypothesized changes mentioned above
|
436
|
+
| are supported by empirical evidence. Our second goal was to focus on plant species
|
437
|
+
| or community responses that show mixed responses to defaunation, and try to clarify
|
438
|
+
| why such variability may exist. Our third goal was to identify areas of study which
|
439
|
+
| have received little attention and warrant future attention.
|
440
|
+
blank |
|
441
|
+
|
|
442
|
+
title | METHODOLOGY
|
443
|
+
blank |
|
444
|
+
|
|
445
|
+
text | IDENTIFICATION OF STUDIES Here we summarize literature in the field as of 2009.
|
446
|
+
| We identified studies primarily by searching literature databases for publications on
|
447
|
+
| aspects of plant ecology with a “defaunation” or “hunting” component. We
|
448
|
+
| supplemented this collection with other studies cited in that literature, as well as
|
449
|
+
| unpublished theses of which we had knowledge. In total, thirty-seven studies
|
450
|
+
| comprise the quantitative portion of this review (Appendix 1).
|
451
|
+
blank |
|
452
|
+
|
|
453
|
+
text | STANDARDIZATION OF RESPONSE VARIABLES FOR COMPARISON Together, the
|
454
|
+
| variation in study design, defaunation intensities compared, species studied, and
|
455
|
+
| response variables measured introduce too much heterogeneity to conduct a formal
|
456
|
+
| meta-analysis of responses (Hedges & Olkin 1985). Yet, we have attempted to present
|
457
|
+
| a review which is quantitative rather than qualitative. We have done so by calculating
|
458
|
+
| effect sizes for each response variable. The effect size estimator we use here is the
|
459
|
+
| percent difference in the response variable reported between defaunated and non-
|
460
|
+
| defaunated sites as follows:
|
461
|
+
| ோವ ିோಿವ
|
462
|
+
| Effect size = ∗ 100,
|
463
|
+
| ோಿವ
|
464
|
+
meta | 6 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
465
|
+
blank |
|
466
|
+
|
|
467
|
+
|
|
468
|
+
text | where RD and RND are the magnitudes of the response variables in the defaunated and
|
469
|
+
| non-defaunated sites, respectively. In cases where the denominator, RND, was zero, we
|
470
|
+
| used the smallest possible non-zero value for RND (e.g. one seed, in the case of
|
471
|
+
| absolute seed dispersal). When the minimum possible response could not be inferred
|
472
|
+
| (e.g., a percent abundance), we conservatively estimated the effect size as 100 percent.
|
473
|
+
| For example, where size class data were reported, sapling to seedling ratios were
|
474
|
+
| calculated to allow for comparison of recruitment rates across studies.
|
475
|
+
| When studies reported response variables from multiple defaunated or non-
|
476
|
+
| defaunated sites, the data were averaged to derive a single value for defaunated and
|
477
|
+
| non-defaunated states. In studies of defaunation gradients, data on the abundance or
|
478
|
+
| presence-absence of vertebrate species relevant to the study, as well as the authors’
|
479
|
+
| categorical characterizations of the relative levels of defaunation were used to define
|
480
|
+
| sites as “defaunated” or “non-defaunated” for purposes of comparison. In these cases,
|
481
|
+
| sites experiencing the lowest levels of defaunation were often grouped with “no
|
482
|
+
| defaunation” sites, while sites showing medium to high levels of defaunation
|
483
|
+
| comprised the “defaunated” sites.
|
484
|
+
blank |
|
485
|
+
|
|
486
|
+
text | QUANTIFICATION OF DEFAUNATION INTENSITY We attempted to compare effects as a
|
487
|
+
| function of defaunation intensity. We restricted these analyses to Neotropical sites
|
488
|
+
| (70% of studies) because more extensive and comparative data on vertebrate
|
489
|
+
| communities was reported for this region. We selected twelve genera of mammalian
|
490
|
+
| frugivores, granivores, and browsers that differ in body mass and sensitivity to
|
491
|
+
| defaunation pressures: Tapir, Tayassu, Pecari, Odocoileus, Mazama, Ateles, Allouata,
|
492
|
+
| Cebus, Agouti, Dasyprocta, Sciurus and Proechimys. These genera are wide-ranging
|
493
|
+
| in the Neotropics, though the particular species may vary. Because some studies did
|
494
|
+
| not report animal abundances or densities, but rather species presence or absence, we
|
495
|
+
| calculated the degree of defaunation for each site as the percent of focal genera that
|
496
|
+
| appeared to be locally extirpated in that site, though present historically.
|
497
|
+
meta | 7
|
498
|
+
blank |
|
499
|
+
|
|
500
|
+
|
|
501
|
+
text | SEED SIZE DATA In several cases, the perturbations in plant-animal interactions as a
|
502
|
+
| consequence of defaunation are hypothesized to vary as a function of seed size. We
|
503
|
+
| therefore attempted to rank species by seed size in order to present the data in a way
|
504
|
+
| that would address these hypotheses. In most cases, either seed mass or seed length
|
505
|
+
| was reported. In the case of Celtis durandii, one Astrocaryum species and one
|
506
|
+
| unspecified Dipteryx species for which seed sizes were not reported, an approximate
|
507
|
+
| seed size was estimated by assigning that species the value of a congeneric species
|
508
|
+
| from another site. Species for which both length and mass were reported were used to
|
509
|
+
| approximate a relative size rank for the species for which only mass or length were
|
510
|
+
| reported. Alternatively, we could have used published seed mass-seed length
|
511
|
+
| correlations to estimate missing size parameters and used one measure of seed size to
|
512
|
+
| assign size ranks. However, this would generally change the positions of only a few
|
513
|
+
| species with unusual seed mass-to-seed length proportions (e.g. Gustavia superba),
|
514
|
+
| and we felt that those species were better assigned a rank by considering the size
|
515
|
+
| parameters in the context of the plant-animal interaction and the natural history of that
|
516
|
+
| species.
|
517
|
+
blank |
|
518
|
+
title | PLANT-ANIMAL INTERACTIONS
|
519
|
+
blank |
|
520
|
+
|
|
521
|
+
title | Seed dispersal
|
522
|
+
text | Seed dispersal is thought to promote plant recruitment in tropical forests by facilitating
|
523
|
+
| escape from natural enemies (Janzen 1970, Connell 1971) and by helping species with
|
524
|
+
| particular environmental requirements for germination and survival (e.g. light-
|
525
|
+
| demanding species) reach favorable microhabitats (Muller-Landau 2007). Seed
|
526
|
+
| dispersal establishes the spatial distribution and diversity of species in the seed and
|
527
|
+
| seedling banks.
|
528
|
+
| A single seed can be dispersed multiple times by different agents. Here we
|
529
|
+
| refer to primary seed dispersal as physical removal from the parent tree and deposition
|
530
|
+
| on the ground. Primary seed dispersal can be performed by biotic agents such as
|
531
|
+
| primates, bats, and birds, or by abiotic agents such as wind. Once a seed has dispersed
|
532
|
+
| from the parent tree, it may still disperse further. This we refer to here as secondary
|
533
|
+
meta | 8 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
534
|
+
blank |
|
535
|
+
|
|
536
|
+
|
|
537
|
+
text | dispersal. We focus on secondary dispersal by biotic agents such as rodents, though in
|
538
|
+
| some circumstances, water and gravity may also facilitate dispersal on the ground.
|
539
|
+
blank |
|
540
|
+
|
|
541
|
+
text | PRIMARY SEED DISPERSAL Seed dispersal by biotic agents should decrease as
|
542
|
+
| defaunation intensity increases and the abundance of seed dispersers is reduced. This
|
543
|
+
| should affect large-seeded species to a disproportionate degree for two reasons. First,
|
544
|
+
| their predominate dispersal agents tend to be larger-bodied, and therefore more
|
545
|
+
| vulnerable to defaunation (Peres & van Roosmalen 2002, Holbrook & Loiselle 2009).
|
546
|
+
| There also appears to be less redundancy of seed dispersal agents for large-seeded
|
547
|
+
| species, relative to smaller-seeded species (Peres & van Roosmalen 2002, Nuñez-Iturri
|
548
|
+
| et al. 2008, Donatti et al. 2009). When seed dispersal has been directly measured,
|
549
|
+
| either as the quantity of seeds removed by primary dispersers such as birds or
|
550
|
+
| primates, or as the proportion of seed crop removed from a parent tree, seed dispersal
|
551
|
+
| is lower in defaunated forests in almost all cases examined (Fig. 1.1). The magnitude
|
552
|
+
| of the decrease appears to be moderately correlated with seed size.
|
553
|
+
| It is important to keep in mind that tropical seed mass distributions span more
|
554
|
+
| than seven orders of magnitude (I.J. Wright et al. 2007). The species reported here
|
555
|
+
| represent only the very upper range of that distribution and were generally selected for
|
556
|
+
| study because they were most likely to show dispersal declines. Almost nothing is
|
557
|
+
| known about how hunting alters biotic dispersal across the broader range of seed sizes
|
558
|
+
| (Muller-Landau 2007).
|
559
|
+
| Two studies examining how perturbations of bird communities affect the
|
560
|
+
| dispersal of smaller-seeded species (< 1 cm fruit diameter) have shown contrasting
|
561
|
+
| results. Dispersal of Bocageopsis multiflora in defaunated sites was actually more than
|
562
|
+
| 2-fold higher than in non-defaunated sites (Fig. 1.1). The cause of this increase is
|
563
|
+
| unknown, but has been suggested to result from an increase in the relative abundance
|
564
|
+
| of generalist, frugivorous birds in highly fragmented sites (Cramer et al. 2007). In the
|
565
|
+
| case of Celtis durandii, a decrease in avian forest specialists that was not compensated
|
566
|
+
| for by forests generalists appears to be responsible for in an overall decrease in seed
|
567
|
+
| dispersal (Kirika et al. 2008).
|
568
|
+
meta | 9
|
569
|
+
blank |
|
570
|
+
|
|
571
|
+
|
|
572
|
+
|
|
573
|
+
text | Genus & Source
|
574
|
+
| Large (Community), Tonga (26)
|
575
|
+
| Leptonychia, Tanzania (9)
|
576
|
+
| Dipteryx, Costa Rica (19)
|
577
|
+
| Duckeodendron, Brazil (10)
|
578
|
+
| Carapa, Costa Rica (19)
|
579
|
+
| Attalea, Panama (36)
|
580
|
+
| Gustavia, Panama (3)
|
581
|
+
| Astrocaryum, Panama (36)
|
582
|
+
| Antrocaryon, Cameroon (35)
|
583
|
+
| Virola, Panama (3)
|
584
|
+
| Choerospondias, Thailand (7)
|
585
|
+
| Pouteria, Brazil (2)
|
586
|
+
| Pourouma, Brazil (2)
|
587
|
+
| Virola, Ecuador (20)
|
588
|
+
| Euterpe, Brazil (14)
|
589
|
+
| Bocageopsis, Brazil (10)
|
590
|
+
| Small Celtis, Uganda (22)
|
591
|
+
| -100 -50 0 50 100 150
|
592
|
+
| % Difference in Seeds Dispersed
|
593
|
+
blank |
|
594
|
+
|
|
595
|
+
text | FIGURE 1.1 Seed dispersal is lower in defaunated sites relative to non-defaunated
|
596
|
+
| sites in almost all cases. Species are ranked by seed size, with Leptonychia being
|
597
|
+
| largest (11.15 cm long) and Bocageopsis and Celtis being smallest (< 1 cm long).
|
598
|
+
| Numbers in parentheses denote the study number in Appendix 1.
|
599
|
+
blank |
|
600
|
+
text | SEED CACHING A special case of seed dispersal is the caching of seeds in the ground
|
601
|
+
| by scatter-hoarding rodents. While individual cached seeds may be predated at a later
|
602
|
+
| time, seeds that are not subsequently recovered are afforded protection from
|
603
|
+
| invertebrate seed predators. For some species, such as large seeded palms with
|
604
|
+
| specialist bruchid beetle seed predators, seed survival is heavily dependent upon seed
|
605
|
+
| caching by rodents.
|
606
|
+
meta | 10 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
607
|
+
blank |
|
608
|
+
|
|
609
|
+
|
|
610
|
+
text | In most cases, seed caching was higher in defaunated sites relative to non-
|
611
|
+
| defaunated sites (Fig. 1.2). This is likely due to the fact that the rodents primarily
|
612
|
+
| responsible for seed caching in these forests, agoutis (Dasyprocta spp.) and squirrels
|
613
|
+
| (Sciurus spp.) may actually benefit from a reduction in the abundance of predators and
|
614
|
+
| larger-bodied competitors at low to medium levels of defaunation (Wright 2003, Dirzo
|
615
|
+
| et al. 2007, Peres & Palacios 2007). Therefore, while defaunation may have a
|
616
|
+
| negative effect on primary dispersal, this negative effect often does not extend to
|
617
|
+
| secondary seed dispersal by terrestrial rodents.
|
618
|
+
blank |
|
619
|
+
|
|
620
|
+
text | Genus & Source
|
621
|
+
| Large Carapa, Costa Rica (18)
|
622
|
+
| Attalea, Panama (24)
|
623
|
+
| Astrocaryum, Panama (24)
|
624
|
+
| Lechthis, Costa Rica (18)
|
625
|
+
| Pentaclethra, Costa Rica (18)
|
626
|
+
| Astrocaryum, Brazil (17)
|
627
|
+
| Astrocaryum, Brazil (13)
|
628
|
+
| Minquartia, Costa Rica (21)
|
629
|
+
| Hymenaea, Venezuela (4)
|
630
|
+
| Welfia, Costa Rica (18)
|
631
|
+
| Otoba, Costa Rica (18)
|
632
|
+
| Virola, Costa Rica (18)
|
633
|
+
| Clarisia, Costa Rica (11)
|
634
|
+
| Small Virola, Costa Rica (11)
|
635
|
+
blank |
|
636
|
+
text | -200 -100 0 100 200 300 400 500
|
637
|
+
| % Difference in Seeds Cached
|
638
|
+
blank |
|
639
|
+
|
|
640
|
+
text | FIGURE 1.2 Differences in seed caching rates in defaunated sites relative to non-
|
641
|
+
| defaunated sites. Species are ranked by size, with Carapa being the largest (20 g) and
|
642
|
+
| Virola the smallest (2 g). Absence of bar indicates no difference. Numbers in
|
643
|
+
| parentheses denote the study number in Appendix 1.
|
644
|
+
meta | 11
|
645
|
+
blank |
|
646
|
+
|
|
647
|
+
|
|
648
|
+
text | Defaunation gradients in Venezuela and Brazil were exceptions to the trend of
|
649
|
+
| higher seed caching rates in defaunated forests (Asquith et al. 1999, Galetti et al.
|
650
|
+
| 2006). In both of these cases, the defaunated sites were small fragments in which
|
651
|
+
| agoutis were virtually absent. Consistent with the loss of this important terrestrial
|
652
|
+
| seed disperser, seed caching in defaunated sites was lower than in non-defaunated sites
|
653
|
+
| in these studies (Fig. 1.2). Squirrels do not compensate for the loss of agoutis (Donatti
|
654
|
+
| et al. 2009).
|
655
|
+
| In contrast to primary dispersal, no relationship between seed size and
|
656
|
+
| differences in caching rates were apparent between defaunated and non-defaunated
|
657
|
+
| sites. This may again be due to the fact that agoutis are capable of handling large
|
658
|
+
| seeds and fruits much larger than their relatively small gape size might suggest.
|
659
|
+
| Therefore, in the Neotropics secondary dispersal of larger-seeded species may occur
|
660
|
+
| despite some degree of defaunation, provided that agoutis persist in the site.
|
661
|
+
| Smaller-bodied scatter-hoarding rodents, such as squirrels, exist in Africa and
|
662
|
+
| Asia, however to our knowledge, there is no functional equivalent to the agouti in
|
663
|
+
| Paleotropical forests. The larger Paleotropical rodents that do exist, such as
|
664
|
+
| Cricetomys species, are larder-hoarding rodents that tend to take seeds to burrows
|
665
|
+
| where they will not survive (Guedje et al. 2003). Therefore, the seed dispersal
|
666
|
+
| “buffer” that agoutis provide in the Neotropics is less likely to be present in other
|
667
|
+
| systems.
|
668
|
+
blank |
|
669
|
+
|
|
670
|
+
text | SPATIAL DISTRIBUTION OF SEEDS AND SEEDLINGS The spatial distribution of seeds
|
671
|
+
| and seedlings on the forest floor can also be an indicator of changes in seed dispersal.
|
672
|
+
| In particular, if seed dispersal is lower in defaunated forests, one would expect to find
|
673
|
+
| a greater proportion of seeds or seedlings undispersed under parent trees relative to
|
674
|
+
| what is observed in non-defaunated forests. Likewise, one would expect to see fewer
|
675
|
+
| seeds or seedlings at distances away from parent trees relative to non-defaunated
|
676
|
+
| forests. Indeed for many species, seed or seedling numbers under parent trees were 2-
|
677
|
+
| to 12-fold higher in defaunated sites relative to non-defaunated sites, and were lower
|
678
|
+
meta | 12 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
679
|
+
blank |
|
680
|
+
|
|
681
|
+
|
|
682
|
+
text | away from parent trees (Fig. 1.3). These patterns are consistent with the loss of biotic
|
683
|
+
| dispersal agents.
|
684
|
+
| One notable exception is Hymenaea on land-bridge islands in Venezuela.
|
685
|
+
| Hymenaea shows the highest increases in seed pods remaining under parent trees in
|
686
|
+
| sites without agoutis relative to sites with agoutis. However, it is one of the few cases
|
687
|
+
| in which seedling densities are actually lower under parent trees in defaunated forests
|
688
|
+
| (Fig.1.3). This is not due to distance or density dependent mortality effects as
|
689
|
+
| mediated by specialist invertebrates or pathogens (Janzen 1970, Connell 1971).
|
690
|
+
| Rather, Hymenaea relies on agoutis to open its seed pods so that seeds may germinate.
|
691
|
+
| In sites lacking agoutis, the seeds cannot escape the seed pod, and seedling densities
|
692
|
+
| are correspondingly low (Asquith et al. 1999).
|
693
|
+
| One study estimated changes in dispersal distances with defaunation. Cramer
|
694
|
+
| et al. (2007) reported a 60 percent and 80 percent decrease in mean and maximum
|
695
|
+
| dispersal distances respectively for the large-seeded Duckeodendron cestroides in
|
696
|
+
| defaunated fragments, relative to continuous forest. In the same study, the smaller-
|
697
|
+
| seeded Bocageopsis multiflora mean and maximum dispersal distances were not
|
698
|
+
| significantly different. This suggests that large-seeded species may become more
|
699
|
+
| spatially aggregated in defaunated forests. Those plant species requiring special
|
700
|
+
| microhabitats for germination and recruitment (e.g. light gaps) may have greater
|
701
|
+
| difficultly reaching suitable sites. Meanwhile, smaller seeded species may be less
|
702
|
+
| affected.
|
703
|
+
meta | 13
|
704
|
+
blank |
|
705
|
+
|
|
706
|
+
text | Genus & Source
|
707
|
+
| Large Choerospondias, Thailand (7)
|
708
|
+
| Leptonychia, Tanzania (9) Under Parent
|
709
|
+
| Balanites, Gabon (5)
|
710
|
+
| Attalea, Panama (37)
|
711
|
+
| Attalea, Panama (37)
|
712
|
+
| Attalea, Panama (36)
|
713
|
+
| Dysoxylum, India (31)
|
714
|
+
| Chisocheton, India (31)
|
715
|
+
| Astrocaryum, Panama (36)
|
716
|
+
| Hymenaea, Venezuela (5)
|
717
|
+
| Polyalthia, India (31)
|
718
|
+
| Hymenaea, Venezuela (4)
|
719
|
+
| Syagrus, Brazil (1)
|
720
|
+
| Small Antrocaryon, Cameroon (35)
|
721
|
+
| -250 0 250 500 750 1000 1250 1500 2350 2600
|
722
|
+
| Large Attalea, Panama (37)
|
723
|
+
| Attalea, Panama (37) Away From
|
724
|
+
| Attalea, Panama (36) Parent
|
725
|
+
| Astrocaryum, Panama (36)
|
726
|
+
| Duckeodendron, Brazil (10)
|
727
|
+
| Dysoxylum, India (31)
|
728
|
+
| Chisocheton, India (31)
|
729
|
+
| Polyalthia, India (31)
|
730
|
+
| Small Bocageopsis, Brazil (10)
|
731
|
+
blank |
|
732
|
+
text | Seeds -100 -50 0 50 100 150 250 300 350
|
733
|
+
| Seedlings % Difference in Seed or Seedling Abundance
|
734
|
+
blank |
|
735
|
+
text | FIGURE 1.3 The number or proportion of seeds or seedlings is generally higher
|
736
|
+
| immediate vicinity of parent trees and generally lower away from parent trees, in
|
737
|
+
| defaunated sites relative to non-defaunated sites. Species are ordered by seed size.
|
738
|
+
| Numbers in parentheses denote the study number in Appendix 1.
|
739
|
+
blank |
|
740
|
+
|
|
741
|
+
|
|
742
|
+
text | COMPENSATION AMONG DISPERSAL AGENTS An important question regarding seed
|
743
|
+
| dispersal in tropical forests is whether a decrease in dispersal by the principle dispersal
|
744
|
+
| agent may be compensated for by other dispersal agents. Comparisons of primate
|
745
|
+
| diets suggest that smaller species of primates only disperse a nested subset of the plant
|
746
|
+
| species that are dispersed by larger primates. Even when co-occurring dispersers
|
747
|
+
meta | 14 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
748
|
+
blank |
|
749
|
+
|
|
750
|
+
|
|
751
|
+
text | appear to have significant dietary overlap on the basis of species consumed, a
|
752
|
+
| quantitative diet analysis reveals that dispersers differ in the fruit species that make up
|
753
|
+
| the major portion of their diets (Poulsen et al. 2002). This suggests that even
|
754
|
+
| dispersers with diet overlap may not compensate for one another. Similarly, among
|
755
|
+
| frugivores that feed on Virola, alternative dispersers do not shift their diet preferences
|
756
|
+
| enough to compensate for the loss of the principle dispersers (Holbrook & Loiselle
|
757
|
+
| 2009).
|
758
|
+
| Decreases in primary seed dispersal summarized here (Fig. 1.1) suggest that
|
759
|
+
| this lack of compensation among primary dispersal agents may be fairly general, at
|
760
|
+
| least for larger-seeded species. There are no studies that directly investigate the
|
761
|
+
| degree to which an increase in secondary dispersal by terrestrial vertebrates (e.g. Fig
|
762
|
+
| 1.2) may compensate for reduced dispersal by birds and primates. However, in cases
|
763
|
+
| where species have lost their primary dispersal agent, the number of seeds and
|
764
|
+
| seedlings remaining under adult trees in defaunated sites is often higher than in non-
|
765
|
+
| defaunated sites (Fig. 1.3). These data provide indirect evidence that, at least in the
|
766
|
+
| cases studied, terrestrial seed dispersers do not fully compensate for loss of principle
|
767
|
+
| avian and primate dispersers. It is possible, however, that terrestrial dispersers are
|
768
|
+
| partially compensating for the loss of other dispersers, and that the observed changes
|
769
|
+
| in seed and seedling densities under and away from parents would be even more
|
770
|
+
| extreme in the absence of terrestrial dispersal.
|
771
|
+
blank |
|
772
|
+
title | Seed Predation
|
773
|
+
blank |
|
774
|
+
text | PRE-DISPERSAL SEED PREDATION Beckman and Muller-Landau (2007) investigated
|
775
|
+
| effects of defaunation on pre-dispersal seed predation for two species of contrasting
|
776
|
+
| seed size in central Panama. They found that pre-dispersal seed predation by
|
777
|
+
| mammals was significantly lower in the defaunated sites for the larger-seeded
|
778
|
+
| Oneocarpus mapora. Authors did not observe mammalian pre-dispersal seed
|
779
|
+
| predation of small-seeded Cordia bicolor. Pre-dispersal seed predation by insects
|
780
|
+
| between sites was not significantly different for either species.
|
781
|
+
meta | 15
|
782
|
+
blank |
|
783
|
+
|
|
784
|
+
|
|
785
|
+
text | POST-DISPERSAL SEED PREDATION After primary dispersal, seeds may be predated
|
786
|
+
| upon by terrestrial mammals such as rodents, peccaries, pigs and deer. The majority of
|
787
|
+
| studies comparing seed predation rates between defaunated and non-defaunated sites
|
788
|
+
| have performed manipulative experiments, setting out arrays of seeds and monitoring
|
789
|
+
| the fates of those seeds. However a few studies of species with slowly decomposing
|
790
|
+
| endocarps have looked at “standing” rates of seed predation in the field (Wright et al.
|
791
|
+
| 2000, Wright & Duber 2001, Galetti et al. 2006). In 22 of the 31 cases, seed predation
|
792
|
+
| rates were lower in defaunated sites, while in nine cases, seed predation rates were
|
793
|
+
| higher (Fig. 1.4).
|
794
|
+
| In a conceptual model, larger-seeded species were hypothesized to experience
|
795
|
+
| higher seed predation rates in moderately defaunated forests relative to non-
|
796
|
+
| defaunated forests (Dirzo et al. 2007). At severe intensities of defaunation, however,
|
797
|
+
| large-seeded species were hypothesized to experience lower seed predation rates,
|
798
|
+
| relative to sites with moderate to no defaunation. These changes in seed predation
|
799
|
+
| rates were posited to be in response to changes in the abundance of seed predators of
|
800
|
+
| medium body size.
|
801
|
+
| Using our estimates of defaunation intensity for Neotropical sites, we
|
802
|
+
| examined how differences in seed predation rates for different plant species varied
|
803
|
+
| with defaunation intensity. These empirical data do not generally support the
|
804
|
+
| hypothesis that seed predation of larger seeds in moderately defaunated sites is higher
|
805
|
+
| than non-defauanted sites, while being lower in highly defaunated sites. (Fig. 1.4).
|
806
|
+
| Among the largest-seeded species studied, seed predation increased and decreased in
|
807
|
+
| about the same number of cases across all levels of defaunation examined.
|
808
|
+
| The conceptual model also hypothesized that seed predation rates of smaller
|
809
|
+
| seeded species would increase monotonically with increasing defaunation intensity, as
|
810
|
+
| small rodents experienced release from competition and predation. However
|
811
|
+
| empirical data suggest that seed predation rates are generally lower for smaller-seeded
|
812
|
+
| species in defaunated sites, regardless of defaunation intensity (Fig. 1.4).
|
813
|
+
meta | 16 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
814
|
+
blank |
|
815
|
+
|
|
816
|
+
|
|
817
|
+
text | 250
|
818
|
+
blank |
|
819
|
+
|
|
820
|
+
|
|
821
|
+
|
|
822
|
+
text | % Difference in Seed Predation
|
823
|
+
| 200
|
824
|
+
blank |
|
825
|
+
text | 150
|
826
|
+
blank |
|
827
|
+
text | 100
|
828
|
+
blank |
|
829
|
+
text | 50
|
830
|
+
blank |
|
831
|
+
text | 0
|
832
|
+
blank |
|
833
|
+
text | -50
|
834
|
+
blank |
|
835
|
+
text | -100
|
836
|
+
| 0.0 20.0 40.0 60.0 80.0 100.0 120.0
|
837
|
+
blank |
|
838
|
+
text | Defaunation Intensity in Defaunated Site
|
839
|
+
blank |
|
840
|
+
|
|
841
|
+
text | FIGURE 1.4 Differences in seed predation rates as a function of the intensity of
|
842
|
+
| defaunation in the defaunated sites. Circle sizes indicate the relative seed size of the
|
843
|
+
| plant species.
|
844
|
+
blank |
|
845
|
+
text | INVERTEBRATE SEED PREDATION It has been suggested that a reduction in vertebrate
|
846
|
+
| seed predation may benefit invertebrate seed predators in two ways. First,
|
847
|
+
| invertebrates experience a release from competition for seed resources (Muller-Landau
|
848
|
+
| 2007). Secondly, larvae developing in seeds may experience decreased mortality due
|
849
|
+
| to the reduction of seed predation by vertebrates (Silvius 2002). Through these
|
850
|
+
| mechanisms, defaunation may lead to higher abundances of invertebrates, and thereby
|
851
|
+
| higher rates of invertebrate seed predation.
|
852
|
+
| Few studies have investigated how defaunation indirectly alters invertebrate
|
853
|
+
| seed predation rates. Consistent with expectation, bruchid beetle seed predation of
|
854
|
+
| palms was higher in defaunated sites for every species investigated (Fig. 1.5).
|
855
|
+
| However, in most cases, the absolute increase in invertebrate seed predation rates only
|
856
|
+
| partially compensated for the decreases in vertebrate seed predation (Wright et al.
|
857
|
+
| 2000, Wright & Duber 2001, but see Galetti et al. 2006).
|
858
|
+
meta | 17
|
859
|
+
blank |
|
860
|
+
|
|
861
|
+
|
|
862
|
+
text | Genus & Source
|
863
|
+
| Attalea, Panama (37)
|
864
|
+
| Attalea, Panama (36)
|
865
|
+
| Astrocaryum, Brazil (17)
|
866
|
+
| Astrocaryum, Panama (36)
|
867
|
+
| Syagrus, Brazil (1)
|
868
|
+
| Syagrus, Brazil (1)
|
869
|
+
| 0 500 1000 1500
|
870
|
+
| % Difference in Invertebrate
|
871
|
+
| Seed Predation
|
872
|
+
| FIGURE 1.5 Seed predation rates by invertebrates for four species of palms are
|
873
|
+
| higher in defaunated sites relative to non-defaunated sites. Species are ranked by
|
874
|
+
| size, with Attalea being the largest and Syagrus the smallest. Numbers in parentheses
|
875
|
+
| denote the study number in Appendix 1.
|
876
|
+
blank |
|
877
|
+
|
|
878
|
+
title | Herbivory & Trampling
|
879
|
+
blank |
|
880
|
+
|
|
881
|
+
text | Few observational studies have evaluated differences in herbivory or trampling as a
|
882
|
+
| consequence of defaunation. Dirzo & Miranda (1991) an absence of vertebrate
|
883
|
+
| herbivory in Los Tuxtlas, a defaunated site. Alves-Costa (2004) categorized herbivory
|
884
|
+
| of the palm Syagrus romanzoffiana into classes by percent damage and also found that
|
885
|
+
| the frequency individuals experiencing little to no herbivory was 66% higher in
|
886
|
+
| defaunated sites.
|
887
|
+
| Mortality by trampling has not been evaluated for live seedlings in the context
|
888
|
+
| of defaunation, however trampling has been evaluated with seedling models. In
|
889
|
+
| Bolivia, “trampling” of seedling models by vertebrates was 75 percent lower in
|
890
|
+
| defaunated forests (Roldán and Simonetti 2001).
|
891
|
+
blank |
|
892
|
+
|
|
893
|
+
title | POPULATION DEMOGRAPHY
|
894
|
+
blank |
|
895
|
+
|
|
896
|
+
text | RECRUITMENT Reduced seed dispersal in defaunated forests has been hypothesized
|
897
|
+
| to have negative impacts on plant recruitment by preventing individuals from escaping
|
898
|
+
| distance-dependent and density dependent mortality (Muller-Landau 2007).
|
899
|
+
| Empirically, plant recruitment has been reported either in terms of new seedlings
|
900
|
+
meta | 18 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
901
|
+
blank |
|
902
|
+
|
|
903
|
+
|
|
904
|
+
text | entering the population in a determined length of time, or as the ratio of juvenile plants
|
905
|
+
| to seedlings. Authors could define seedlings variously as first year germinants or by
|
906
|
+
| size class. In about half of cases, recruitment was about 2-fold higher in defaunated
|
907
|
+
| forests than in non-defaunated forests, both for seedlings and saplings (Fig. 1.6). In
|
908
|
+
| the other half of cases, recruitment is lower in defaunated forests.
|
909
|
+
| There have been virtually no investigations into why recruitment rates change.
|
910
|
+
| The variation in changes in recruitment do not seem to be consistently related to the
|
911
|
+
| degree of defaunation across studies, loss of particular dispersers or loss of particular
|
912
|
+
| seed predators. Changes in vertebrate seedling predation and herbivory, as well as
|
913
|
+
| distance and density dependent mortality as mediated by invertebrate herbivores and
|
914
|
+
| pathogens (Janzen 1970, Connell 1971), can be responsible for altered seedling
|
915
|
+
| recruitment. However, no studies have recorded herbivory rates or causes of plant
|
916
|
+
| mortality, so no definitive data exists on how each of these mechanisms contribute to
|
917
|
+
| the changes in recruitment observed. One study of Syagrus found that sapling
|
918
|
+
| recruitment near the parent tree was slightly lower in defaunated forests, while
|
919
|
+
| recruitment far from the parent tree was more than 2-fold higher in defaunated forests
|
920
|
+
| (Alves-Costa 2004). This may be because non-vertebrate natural enemies are more
|
921
|
+
| than compensating for the loss of vertebrate herbivores near the parent trees, but not at
|
922
|
+
| far distances, for this species. However, no data exist with which to evaluate this
|
923
|
+
| explanation.
|
924
|
+
| It is also possible, in some cases, that differences in recruitment are not
|
925
|
+
| actually due to defaunation. In some studies of seedling recruitment, only one
|
926
|
+
| defaunated site and one non-defaunated site were compared. This opens the
|
927
|
+
| possibility that some differences in recruitment were due to other environmental
|
928
|
+
| factors that vary across the landscape, such as precipitation or edaphic conditions. The
|
929
|
+
| driver of defaunation is another potential source of variation. In some cases, hunting
|
930
|
+
| was the cause of defaunation, altering primarily the animal community. However in
|
931
|
+
| other studies fragmentation or a combination of fragmentation and hunting was the
|
932
|
+
| cause of defaunation. As fragmentation alters many aspects of the microclimate, it is
|
933
|
+
| possible that changes in seedling recruitment are due to the effects of fragmentation on
|
934
|
+
meta | 19
|
935
|
+
blank |
|
936
|
+
|
|
937
|
+
|
|
938
|
+
text | microclimate, rather than or in addition to the effects of a reduction in herbivore
|
939
|
+
| abundance.
|
940
|
+
blank |
|
941
|
+
|
|
942
|
+
text | Genus & Source
|
943
|
+
| Attalea, Panama (36) Seedlings
|
944
|
+
| Dipteryx, Peru/Panama (34)
|
945
|
+
| Astrocaryum, Brazil (17)
|
946
|
+
| Astrocaryum, Panama (36)
|
947
|
+
| Syagrus, Brazil (1)
|
948
|
+
| Saplings
|
949
|
+
| (Community), Malaysia (31)
|
950
|
+
| Leptonychia, Tanzania (9)
|
951
|
+
| Balanites, Gabon (5)
|
952
|
+
| Astrocaryum, Brazil (17)
|
953
|
+
| Syagrus (near), Brazil (1)
|
954
|
+
| Syagrus (far), Brazil (1)
|
955
|
+
| -100 0 100 200 300 400 500
|
956
|
+
| % Difference in Recruitment
|
957
|
+
blank |
|
958
|
+
|
|
959
|
+
text | FIGURE 1.6 Plant recruitment does not respond consistently to defaunation across
|
960
|
+
| species for either seedlings or saplings. Numbers in parentheses denote the study
|
961
|
+
| number in Appendix 1.
|
962
|
+
blank |
|
963
|
+
|
|
964
|
+
text | SEEDLING SURVIVAL As with recruitment, responses of seedling survival to
|
965
|
+
| defaunation are quite variable (Fig. 1.7). Asquith et al. (1997) found that differences
|
966
|
+
| in seedling survival could vary among species within the same study system. Survival
|
967
|
+
| was lowest on highly defaunated islands in Lake Gatun, Panama for two of the three
|
968
|
+
| species tested. Exclosure experiments verified that spiny rats, free of competition
|
969
|
+
| from larger mammals, reach population sizes 10-fold greater on these islands relative
|
970
|
+
| to the non-that sites (Adler 1996), and are responsible for the increased mortality. The
|
971
|
+
| third species, which did not show a difference in survival between sites, Virola
|
972
|
+
| surinamensis, experienced 100% mortality at both defaunated and non-defaunated
|
973
|
+
| sites (Asquith et al. 1997).
|
974
|
+
| Differences in survival rates can also be variable within a species in the same
|
975
|
+
| region, likely due to differences in the defaunation intensities being compared. Two
|
976
|
+
meta | 20 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
977
|
+
blank |
|
978
|
+
|
|
979
|
+
|
|
980
|
+
text | studies have compared the survival of Gustavia superba in defaunated sites in the
|
981
|
+
| Lake Gatun region of central Panama. In one case, the defaunated site was hunted
|
982
|
+
| relative to the non-defaunated site, but the animal community was not so impoverished
|
983
|
+
| as to lead to a competitive release of small rodents. In that study, G. superba had
|
984
|
+
| higher survival rates in the defaunated sites. However, when the defaunated sites were
|
985
|
+
| islands with only high populations of spiny rats present, survival of G. superba was
|
986
|
+
| lower in the defaunated site. This difference in the degree of defaunation intensity
|
987
|
+
| evaluated in the two studies, and compensatory changes in abundance of non-hunted
|
988
|
+
| species, are likely to account for the contrasting responses in seedling survival, and
|
989
|
+
| illustrate that changes in seedling survival as a consequence of defaunation may not
|
990
|
+
| change monotonically.
|
991
|
+
blank |
|
992
|
+
|
|
993
|
+
text | Genus & Source
|
994
|
+
| Dipteryx, Panama (3)
|
995
|
+
| Gustavia, Panama (3)
|
996
|
+
| Dipteryx, Peru/Panama (33)
|
997
|
+
| Syagrus, Brazil (1)
|
998
|
+
| Virola, Panama (3)
|
999
|
+
| Gustavia, Panama (32)
|
1000
|
+
| Pentaclethra, Costa Rica (18)
|
1001
|
+
| -75 -50 -25 0 25 50 75 100 125
|
1002
|
+
| % Difference in Seedling Survival
|
1003
|
+
blank |
|
1004
|
+
|
|
1005
|
+
text | FIGURE 1.7 Seedling survival does not show consistent changes as a consequence of
|
1006
|
+
| defaunation, even within sites (e.g. study 4) or species (e.g. Gustavia superba in
|
1007
|
+
| Panama). Numbers in parentheses denote the study number in Appendix 1.
|
1008
|
+
blank |
|
1009
|
+
|
|
1010
|
+
text | STANDING ABUNDANCE Seedling densities do not respond uniformly to defaunation.
|
1011
|
+
| Species that are dispersed and predated upon by scatterhoarding rodents tend to
|
1012
|
+
| increase in abundance in defaunated sites (Fig. 1.8). Likewise the increase in seedling
|
1013
|
+
| abundance of the elephant dispersed Balanites wilsoniana, despite reduced seed
|
1014
|
+
| dispersal, was attributed to low seed and seedling predation in the defaunated site
|
1015
|
+
meta | 21
|
1016
|
+
blank |
|
1017
|
+
|
|
1018
|
+
|
|
1019
|
+
text | (Babweteera et al. 2007). Meanwhile, species that are bird dispersed have lower
|
1020
|
+
| abundances in non-defaunated sites.
|
1021
|
+
| These data suggest, for species which are rodent dispersed and predated, any
|
1022
|
+
| increases in distance-dependent or density-dependent mortality by invertebrates or
|
1023
|
+
| pathogens, as a consequence of reduced dispersal, do not compensate for reductions in
|
1024
|
+
| vertebrate seed and seedling predation, resulting in a net increase in survival for these
|
1025
|
+
| species. The same does not appear to be true for bird dispersed species, although there
|
1026
|
+
| is no theoretical reason why these species should not experience high reductions in
|
1027
|
+
| vertebrate seed predation.
|
1028
|
+
| All studies involving rodent dispersed species were conducted on palm species,
|
1029
|
+
| most of which are preferred food species for agoutis, a dominant Neotropical seed
|
1030
|
+
| predator. More studies in Neotropical forests are required to determine if these
|
1031
|
+
| species are unique in experiencing a net benefit from defaunation, or if other species
|
1032
|
+
| preyed upon by agoutis also increase in abundance in defaunated sites. These studies
|
1033
|
+
| should include species that have birds or primates as their primary dispersal agents.
|
1034
|
+
| In contrast to the rodent-dispersed palms, little is known about the seed
|
1035
|
+
| predators of the bird-dispersed species studied. However, at least two of the three
|
1036
|
+
| studies of bird-dispersed species were conducted in Paleotropical forests with different
|
1037
|
+
| assemblages of seed predators. Studies of vertebrate seed and seedling predation in
|
1038
|
+
| the Paleotropics may determine whether differences observed between rodent-
|
1039
|
+
| dispersed species and bird-dispersed species may be due to differences in the seed and
|
1040
|
+
| seedling predator community, rather than differences between species with different
|
1041
|
+
| dispersal agents per se.
|
1042
|
+
meta | 22 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
1043
|
+
blank |
|
1044
|
+
|
|
1045
|
+
text | Genus & Source
|
1046
|
+
| Astrocaryum, Brazil (17) Rodent Dispersed
|
1047
|
+
| Dipteryx, Peru (33)
|
1048
|
+
| Syagrus, Brazil (1)
|
1049
|
+
| Astrocaryum, Bolivia (29)
|
1050
|
+
| Syagrus, Brazil (1)
|
1051
|
+
| Attalea, Panama (36)
|
1052
|
+
| Attalea, Panama (37)
|
1053
|
+
| Astrocaryum, Panama (36)
|
1054
|
+
blank |
|
1055
|
+
text | Bird Dispersed
|
1056
|
+
| Chisocheton, India (31)
|
1057
|
+
| Polyalthia, India (31)
|
1058
|
+
| Dysoxylum, India (31)
|
1059
|
+
| Euterpe, Brazil (14)
|
1060
|
+
| Leptonychia, Tanzania (9)
|
1061
|
+
| -100 0 100 200 300
|
1062
|
+
| Elephant Dispersed
|
1063
|
+
| Balanites, Gabon (5)
|
1064
|
+
| -400 0 400 800 1200
|
1065
|
+
| % Difference in Seedling Densities
|
1066
|
+
| FIGURE 1.8 Differences in seedling densities in defaunated sites relative to non-
|
1067
|
+
| defaunated sites. Numbers in parentheses denote the study number in Appendix 1.
|
1068
|
+
blank |
|
1069
|
+
|
|
1070
|
+
text | LINKING DISPERSAL AND SEEDLING RECRUITMENT It is clear, by several measures,
|
1071
|
+
| that seed dispersal decreases as a consequence of defaunation (Figs. 1.1 & 1.3), though
|
1072
|
+
| effects on seed caching are variable (Fig. 1.2). What is less clear is whether decreased
|
1073
|
+
| dispersal translates to decreases in plant recruitment. Investigators focusing on
|
1074
|
+
| decreased seed dispersal as a consequence of defaunation often suggest that decreased
|
1075
|
+
| dispersal will result in decreases in seed and seedling survival and plant recruitment.
|
1076
|
+
| This is because undispersed seeds are assumed to be unable to escape distance-
|
1077
|
+
| dependent and/or density-dependent mortality (Janzen 1970, Connell 1971).
|
1078
|
+
| However, there are several problems with this assumption. First, there are
|
1079
|
+
| many species for which distance- and/or density-dependent mortality have not been
|
1080
|
+
| detected (Hyatt et al. 2003, Uriarte et al. 2005). Secondly, spatial data on seedling
|
1081
|
+
| densities also show that reduced seed dispersal does not generally lead to great
|
1082
|
+
| decreases in seedling abundances under parent trees in defaunated forests (Fig. 1.3).
|
1083
|
+
| This suggests that though seed and seedling mortality may be higher under parent
|
1084
|
+
meta | 23
|
1085
|
+
blank |
|
1086
|
+
|
|
1087
|
+
|
|
1088
|
+
text | trees, the higher number of seeds that fall below the parent tree in defaunated forests
|
1089
|
+
| compensate for this higher mortality and seedling densities under parent trees remain
|
1090
|
+
| relatively similar to those observed in non-defaunated forests. Finally, as seen above,
|
1091
|
+
| vertebrate seed and seedling predation rates may also vary with defaunation (Figs. 1.4
|
1092
|
+
| & 1.5). Seedling density data suggest that reduced rates of vertebrate seed predation
|
1093
|
+
| result in increased survival rates that more than compensate for any increases in
|
1094
|
+
| distance-dependent or density-dependent mortality by non-vertebrates, at least for
|
1095
|
+
| rodent-dispersed species and species like B. wilsoniana (Fig. 1.6). Taken together,
|
1096
|
+
| these data suggest that the assumed negative effects of reduced seed dispersal on plant
|
1097
|
+
| recruitment as a consequence of hunting may not be general, but rather manifest
|
1098
|
+
| themselves only in species which (1) experience strong natural enemy-mediated,
|
1099
|
+
| negative density-dependent mortality (2) rely exclusively upon a few, large-bodied,
|
1100
|
+
| hunted vertebrates for seed dispersal, and (3) do not experience a demographic benefit
|
1101
|
+
| of reduced seed predation by rodents with increasing defaunation intensity.
|
1102
|
+
| Interestingly, there are few studies that actually investigate changes in
|
1103
|
+
| dispersal and seedling recruitment simultaneously in a single species. In the case of
|
1104
|
+
| the large seeded palm Attalea butyracea in Central Panama, seed dispersal is reduced
|
1105
|
+
| in defaunated forests (Wright & Duber 2001). In addition, the intensity of bruchid
|
1106
|
+
| beetle seed predation does increase with proximity to the parent tree, and the effect
|
1107
|
+
| intensifies with defaunation. However, increased bruchid beetle seed predation did
|
1108
|
+
| not fully compensate for the decrease in vertebrate seed predation associated with the
|
1109
|
+
| defaunation, and seedling densities of the palm were higher in defaunated sites,
|
1110
|
+
| despite the decrease in seed dispersal.
|
1111
|
+
| Brodie et al. (2009) modeled the effects of decreased dispersal on seedling
|
1112
|
+
| recruitment for Choerospondias axillaris in Thailand and did find evidence that
|
1113
|
+
| decreased dispersal would translate to decreased recruitment in this species. However
|
1114
|
+
| this was because defaunation deprived C. axillaris of favorable regeneration sites,
|
1115
|
+
| since C. axillaris seems to depend on light gaps for regeneration and could not
|
1116
|
+
| disperse to gaps without its vertebrate disperser (Brodie et al. 2009). It was not a
|
1117
|
+
| consequence of distance-dependent or density-dependent mortality.
|
1118
|
+
meta | 24 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
1119
|
+
blank |
|
1120
|
+
|
|
1121
|
+
|
|
1122
|
+
title | COMMUNITY DIVERSITY
|
1123
|
+
blank |
|
1124
|
+
|
|
1125
|
+
text | SEEDLING DENSITY Seedling or herb density at the community level is consistently
|
1126
|
+
| higher where exclosure experiments (Ickes et al. 2001, Royo & Carson 2005) or
|
1127
|
+
| defaunation due to hunting and fragmentation (Dirzo & Miranda 1991) completely
|
1128
|
+
| eliminate vertebrate herbivory (Fig. 1.9). Interestingly, at many moderately
|
1129
|
+
| defaunated sites, community seedling densities are lower, relative to non-defaunated
|
1130
|
+
| sites. It may be that terrestrial herbivores initially increase in abundance as a
|
1131
|
+
| consequence of a release from predation, and perhaps competition. However,
|
1132
|
+
| decreased seedling densities at the community level are in contrast to higher seedling
|
1133
|
+
| densities of many individual species in defaunated sites (Fig. 1.8). This discrepancy
|
1134
|
+
| further highlights the need to understand how defaunation alters plant recruitment
|
1135
|
+
| across a broader range of species, and to reconcile changes in recruitment at the
|
1136
|
+
| species level with changes at the community-level.
|
1137
|
+
| Site & Source
|
1138
|
+
| Uganda (8) Forest comparison
|
1139
|
+
| Uganda (8) Exclosure study
|
1140
|
+
| Panama (38)
|
1141
|
+
| Bolivia (29)
|
1142
|
+
| Panama (30)
|
1143
|
+
| Peru (27)
|
1144
|
+
| Malaysia (21)
|
1145
|
+
| Panama (30)
|
1146
|
+
| Malaysia (21)
|
1147
|
+
| Mexico (12)
|
1148
|
+
| -100 -50 0 50 100 150
|
1149
|
+
| % Difference in Seedling Density
|
1150
|
+
blank |
|
1151
|
+
|
|
1152
|
+
text | FIGURE 1.9 Community level seedling and herb densities generally increase in
|
1153
|
+
| cases of high defaunation but decrease in others. Numbers in parentheses denote the
|
1154
|
+
| study number in Appendix 1.
|
1155
|
+
blank |
|
1156
|
+
|
|
1157
|
+
text | DIVERSITY Several short-term exclosure studies have shown that species richness
|
1158
|
+
| initially increases with herbivore removal (Fig. 1.10a). However, this appears to be an
|
1159
|
+
| effect of increased stem densities increasing the likelihood that rare species will be
|
1160
|
+
| present inside the exclosures. In an exclosure experiment in Panama, rare herbs
|
1161
|
+
meta | 25
|
1162
|
+
blank |
|
1163
|
+
|
|
1164
|
+
|
|
1165
|
+
text | increased 2-fold (Royo & Carson 2005) (Fig. 1.10b). However, defaunation also
|
1166
|
+
| appears to increase species dominance as well (Fig. 1.10b). Diversity indices appear
|
1167
|
+
| to mask the changes in community composition that occur in exclosure experiments,
|
1168
|
+
| because the effects of increased species richness and increased dominance tend to
|
1169
|
+
| cancel each other out, such that exclosures show only small decreases in indices of
|
1170
|
+
| diversity.
|
1171
|
+
| In forest comparisons, species richness was generally lower. Unlike short-term
|
1172
|
+
| exclosure experiments, defaunated forests have experienced decades of defaunation,
|
1173
|
+
| likely allowing competitively dominant plant species to outcompete rarer and less
|
1174
|
+
| dominant species, reducing diversity. Consistent with this hypothesis, species
|
1175
|
+
| dominance was higher in the cases that reported it (Fig. 1.10b). Responses in diversity
|
1176
|
+
| indices were mixed (Fig. 1.10c), again suggesting that these indices may be less
|
1177
|
+
| informative than directly evaluating changes in species richness and dominance.
|
1178
|
+
blank |
|
1179
|
+
|
|
1180
|
+
text | PLANT FUNCTIONAL GROUPS Nuñez-Iturri et al. (2007, 2008) and Wright et al.
|
1181
|
+
| (2007) both found little difference in total species richness between defaunated and
|
1182
|
+
| non-defaunated sites. However, the lack of differences in species richness belied
|
1183
|
+
| important changes in plant community composition. Species with abiotic or unhunted,
|
1184
|
+
| biotic dispersal agents consistently show higher abundance in hunted sites (Wright et
|
1185
|
+
| al. 2007, Nuñez-Iturri et al. 2008, Terborgh et al. 2008). In contrast, species dispersed
|
1186
|
+
| by game animals show decreased abundance in defaunated sites. Consistent with this
|
1187
|
+
| finding, lianas, which tend to be abiotically dispersed (Hardesty & Muller-Landau
|
1188
|
+
| 2005, Wright et al. 2007), were higher in relative abundance in defaunated sites in
|
1189
|
+
| central Panama (Wright et al. 2007).
|
1190
|
+
meta | 26 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
1191
|
+
blank |
|
1192
|
+
|
|
1193
|
+
text | Site & Source A Site & Source B
|
1194
|
+
| Mexico (12) Panama (30)
|
1195
|
+
| (game) Peru (28) Brazil (1)
|
1196
|
+
| (game) Peru (27) Panama (30)
|
1197
|
+
| Uganda (8) Panama (30)
|
1198
|
+
| Peru (28) Mexico (12)
|
1199
|
+
| Uganda (8) 100 200 500 600 700
|
1200
|
+
| 0
|
1201
|
+
| Bolivia (29) % Difference Species Dominance
|
1202
|
+
| Bolivia (29)
|
1203
|
+
| Site & Source C
|
1204
|
+
| Panama (38)
|
1205
|
+
| Mexico (12)
|
1206
|
+
| Peru (27)
|
1207
|
+
| Malaysia (21)
|
1208
|
+
| Malaysia (21)
|
1209
|
+
| Colombia (25)
|
1210
|
+
| Panama (30)
|
1211
|
+
| Panama (38)
|
1212
|
+
| (abiotic) Peru (28)
|
1213
|
+
| -80 -40 0 40
|
1214
|
+
| (non-game) Peru (27) % Difference in Diversity
|
1215
|
+
| Colombia (25)
|
1216
|
+
| (abiotic) Peru (27)
|
1217
|
+
blank |
|
1218
|
+
text | -75 -50 -25 0 25 50 75 Forest comparison
|
1219
|
+
| % Difference Species Richness Exclosure study
|
1220
|
+
blank |
|
1221
|
+
text | FIGURE 1.10 Diversity responses to defaunation. (a) species richness, (b) species
|
1222
|
+
| dominance, and (c) species diversity (Shannon-Weiner, Simpson, or Fisher’s α
|
1223
|
+
| indices). Peruvian richness differences are generally for groups with different dispersal
|
1224
|
+
| agents; dominance for the Panama study is similarly for subsets of common and rare
|
1225
|
+
| herbs. Numbers in parentheses denote the study number in Appendix 1.
|
1226
|
+
blank |
|
1227
|
+
|
|
1228
|
+
text | The studies found important differences in community seed mass responses.
|
1229
|
+
| In Peru, the relative abundance of large seeded species was lower in defaunated sites,
|
1230
|
+
| while in Panama, the community mean seed mass was higher in defaunated sites
|
1231
|
+
| (Wright et al. 2007, Nuñez-Iturri et al. 2008). The discrepancy appears to be due to
|
1232
|
+
| differences in faunal communities between Peru and Panama. In the Peruvian study,
|
1233
|
+
| defaunation greatly reduces populations of large primate dispersers, while not greatly
|
1234
|
+
| affecting the relatively low populations of seed predators such as agoutis. In contrast,
|
1235
|
+
| defaunation in Panama, defaunation greatly reduces agouti populations, but does not
|
1236
|
+
| greatly affect seed dispersal by large primates, as these animals are rare or absent even
|
1237
|
+
| in the non-defaunated sites.
|
1238
|
+
| Studies of the effects of defaunation effects on other functional traits are rare.
|
1239
|
+
| Both a forest comparison study in Panama and an exclosure study in Panama found
|
1240
|
+
meta | 27
|
1241
|
+
blank |
|
1242
|
+
|
|
1243
|
+
|
|
1244
|
+
text | that community median leaf mass per area and leaf laminar toughness in the seedling
|
1245
|
+
| community did not change in response to defaunation (Ch. 2). However, saplings (40-
|
1246
|
+
| 100 cm) in the exclosure experiment did have lower community mean leaf toughness,
|
1247
|
+
| and higher community mean leaf nitrogen relative to controls (Ch. 3). Wood density
|
1248
|
+
| was the only functional trait that had different responses to defaunation in the forest
|
1249
|
+
| comparison and exclosure studies. This is likely due to the fact that primary dispersal
|
1250
|
+
| is altered in the forest comparison, but not in the exclosure study (Ch. 2).
|
1251
|
+
blank |
|
1252
|
+
|
|
1253
|
+
title | WHAT IS DEFAUNATION?
|
1254
|
+
text | The heterogeneity in response to defaunation, particularly at the level of plant
|
1255
|
+
| population dynamics and community composition, suggest that more precision is
|
1256
|
+
| needed in characterizing exactly what is meant by defaunation, including its drivers
|
1257
|
+
| and the effects on the particular mammal community being studied. Among the
|
1258
|
+
| studies reported there, there was variation in the levels of defaunation in both “non-
|
1259
|
+
| defaunated” and “defaunated” forests across studies. In some cases, sites with similar
|
1260
|
+
| species compositions would be considered “non-defaunated” in one study, and
|
1261
|
+
| “defaunated” in another.
|
1262
|
+
| Unfortunately, terms such as “hunted”, “fragmented,” or “disturbed” are
|
1263
|
+
| usually used to classify sites into treatments, but do not correspond to a specific
|
1264
|
+
| change in a vertebrate community. This problem could be addressed by reporting a
|
1265
|
+
| robust characterization of the vertebrate community. Often, studies did not actually
|
1266
|
+
| report differences in either abundances of key species (e.g. a particular seed disperser)
|
1267
|
+
| or the vertebrate community as a whole. In other cases, the presence or absence of
|
1268
|
+
| species were reported, but not animal abundances. Reporting presence/absence data
|
1269
|
+
| will not capture situations in which animals such as rodents or smaller primates
|
1270
|
+
| actually increase in population size as defaunation reduces the predation and
|
1271
|
+
| competition they experience. In other cases, a species may be present, but in such rare
|
1272
|
+
| numbers so as to be functionally extinct.
|
1273
|
+
| Though estimating animal abundances is labor-intensive, we suggest that
|
1274
|
+
| further clarity and progress in understanding the effects of defaunation on plant
|
1275
|
+
meta | 28 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
1276
|
+
blank |
|
1277
|
+
|
|
1278
|
+
|
|
1279
|
+
text | communities will rely on exactly this level of precision in characterizing sites used in
|
1280
|
+
| comparative studies.
|
1281
|
+
blank |
|
1282
|
+
|
|
1283
|
+
title | HETEROGENEITY AMONG STUDIES
|
1284
|
+
blank |
|
1285
|
+
|
|
1286
|
+
text | Understanding the heterogeneity and sources of potential bias in the studies examined
|
1287
|
+
| here is important both for understanding the limitations and generality of the data, as
|
1288
|
+
| well as identifying areas for further research. Research on effects of defaunation on
|
1289
|
+
| plants has predominantly focused on Neotropical mammals. Over 70 percent of
|
1290
|
+
| studies were conducted in the Neotropics, while only 15 percent and 10 percent of
|
1291
|
+
| studies were conducted in Africa and Asia respectively, with the remaining 5 percent
|
1292
|
+
| conducted in Australia and Polynesia. As this review has demonstrated, responses to
|
1293
|
+
| defaunation can be quite variable even within the Neotropics, where faunal
|
1294
|
+
| communities are relatively similar. More studies in the Paleotropics are needed to
|
1295
|
+
| understand how plant responses to defaunation in these forests may differ from those
|
1296
|
+
| observed in Neotropical forests.
|
1297
|
+
| Only 15 percent of studies reported effects of avian defaunation, with the
|
1298
|
+
| remainder examining effects of mammalian defaunation. Many of those studies
|
1299
|
+
| focused on rodents and/or primates. Despite the fact that many of the larger
|
1300
|
+
| vertebrates such as peccaries, pigs, deer, tapir and elephants are most vulnerable to
|
1301
|
+
| defaunation, only a few studies investigated the effects of losing these animals from
|
1302
|
+
| the community. Future studies should seek to understand the impacts of losing
|
1303
|
+
| relatively understudied groups of vertebrates, as well as understanding how losses of
|
1304
|
+
| dispersers, seed predators, and herbivores may synergize.
|
1305
|
+
| It is also important to note that forest comparisons generally had low
|
1306
|
+
| replication. The majority of studies only had one non-defaunated site, and sometimes
|
1307
|
+
| only one defaunated site. We suggest that a better understanding of patterns and
|
1308
|
+
| mechanisms could come from increasing the number of study sites examined, and
|
1309
|
+
| including a range of defaunation intensities within a single study, with better
|
1310
|
+
| quantification of the differences in vertebrate communities. We suspect that many of
|
1311
|
+
meta | 29
|
1312
|
+
blank |
|
1313
|
+
|
|
1314
|
+
|
|
1315
|
+
text | the interactions and patterns discussed in this review do not vary linearly with animal
|
1316
|
+
| abundance, but rather, change in a step-wise or threshold dependent manner as key
|
1317
|
+
| interaction partners are removed from a system. Studying gradients of defaunation
|
1318
|
+
| intensity would allow scientists to better elucidate the levels of defaunation at which
|
1319
|
+
| changes in key interactions occur, and perhaps allow for the reconciliation of
|
1320
|
+
| discrepancies in responses among studies.
|
1321
|
+
blank |
|
1322
|
+
|
|
1323
|
+
title | CONCLUSIONS
|
1324
|
+
blank |
|
1325
|
+
|
|
1326
|
+
text | It is now well documented that larger-seeded species experience reduced dispersal,
|
1327
|
+
| and increased aggregation around parent trees as a result of defaunation. However the
|
1328
|
+
| overall consequences for species recruitment appear variable. More work is required
|
1329
|
+
| to link reduced dispersal to subsequent stages of the seedling recruitment process to
|
1330
|
+
| determine whether reduced dispersal poses a general threat to the persistence of large-
|
1331
|
+
| seeded species. Responses to defaunation at the community level are also variable,
|
1332
|
+
| and future studies should work to reconcile the changes observed that the species
|
1333
|
+
| interaction or population levels with changes in composition at the community level.
|
1334
|
+
meta | 30 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
1335
|
+
blank |
|
1336
|
+
|
|
1337
|
+
|
|
1338
|
+
text | APPENDIX 1.1 Reference information and raw data for response variables for studies
|
1339
|
+
| referenced in figures. Ndef = value for non-defaunated site(s); Def = Value for
|
1340
|
+
| defaunated site(s); % ∆ = Percent change from non-defaunated site to defaunated site.
|
1341
|
+
blank |
|
1342
|
+
|
|
1343
|
+
text | No Reference Site Response Variable Ndef Def %∆
|
1344
|
+
| 1 Alves-Costa (2004) Brazil Diaspores predated (%) 31.2 12.6 -60
|
1345
|
+
| 1 Alves-Costa (2004) Brazil Insect seed predation (near) 10.7 23.4 119
|
1346
|
+
| 1 Alves-Costa (2004) Brazil Insect seed predation (far) 1.6 24.2 1376
|
1347
|
+
| 1 Alves-Costa (2004) Brazil Seed density 0.16 0.18 8
|
1348
|
+
| 1 Alves-Costa (2004) Brazil Seedlings under parent 0.06 0.72 1187
|
1349
|
+
| 1 Alves-Costa (2004) Brazil Juvenile:Seedling (near) 2.33 1.16 -50
|
1350
|
+
| 1 Alves-Costa (2004) Brazil Juvenile:Seedling (far) 2.65 9.51 259
|
1351
|
+
| 1 Alves-Costa (2004) Brazil Seedling density 26.8 46.8 75
|
1352
|
+
| 1 Alves-Costa (2004) Brazil No. species/No. plants 0.23 0.14 -37
|
1353
|
+
| 1 Alves-Costa (2004) Brazil Frequency of low herbivory 24.1 40.0 66
|
1354
|
+
| 1 Alves-Costa (2004) Brazil No. new plants 41.2 118.4 187
|
1355
|
+
| 1 Alves-Costa (2004) Brazil Seedling mortality (%) 40.1 42.7 6
|
1356
|
+
| 2 Andresen (2003) Brazil % Pouteria seeds buried 40 32.5 -19
|
1357
|
+
| 2 Andresen (2003) Brazil % Pourouma seeds buried 36 19 -47
|
1358
|
+
| 3 Asquith et al. (1997) Panama Seed removal 0.01 0.05 900
|
1359
|
+
| 3 Asquith et al. (1997) Panama Seedling survival 0.21 0.07 -69
|
1360
|
+
| 3 Asquith et al. (1997) Panama Seed removal 0.01 0.08 700
|
1361
|
+
| 3 Asquith et al. (1997) Panama Seed dispersal 0.56 0.24 -58
|
1362
|
+
| 3 Asquith et al. (1997) Panama Seedling survival 0.49 0.22 -56
|
1363
|
+
| 3 Asquith et al. (1997) Panama Seed removal 0.00 0.00 0
|
1364
|
+
| 3 Asquith et al. (1997) Panama Seed dispersal 0.54 0.19 -65
|
1365
|
+
| 3 Asquith et al. (1997) Panama Seedling survival 0.00 0.00 0
|
1366
|
+
| 4 Asquith et al. (1999) Venezuela Pod removal 1.00 0.14 -86
|
1367
|
+
| 4 Asquith et al. (1999) Venezuela Seed removal 0.92 0.60 -35
|
1368
|
+
| 4 Asquith et al. (1999) Venezuela Seed caching 0.17 0.00 -100
|
1369
|
+
| 4 Asquith et al. (1999) Venezuela Seed density under parent 4.0 100.0 2400
|
1370
|
+
| 4 Asquith et al. (1999) Venezuela Seedling density under parent 22.0 1.8 -92
|
1371
|
+
| 5 Babweteera et al. (2007) Gabon Juvenile density 85 1169 1275
|
1372
|
+
| 5 Babweteera et al. (2007) Gabon Sapling:Seedling 0.21 0.00 -98
|
1373
|
+
| 5 Babweteera et al. (2007) Gabon Pole:Seedling 0.08 0.01 -92
|
1374
|
+
| 5 Babweteera et al. (2007) Gabon Prob. Juvenile's under conspecific 58.0 89.0 53
|
1375
|
+
| 6 Beckman & Muller-Landau (2007) Panama Primary seed removal 42.0 24.1 -43
|
1376
|
+
| 6 Beckman & Muller-Landau (2007) Panama Predispersal seed predation 55.0 25.0 -55
|
1377
|
+
| 6 Beckman & Muller-Landau (2007) Panama Secondary seed removal 0.0 10.6 100
|
1378
|
+
| 6 Beckman & Muller-Landau (2007) Panama Primary seed removal 21.6 14.6 -32
|
1379
|
+
| 6 Beckman & Muller-Landau (2007) Panama Predispersal seed predation 7.0 7.0 0
|
1380
|
+
| 6 Beckman & Muller-Landau (2007) Panama Predispersal seed predation 20.0 0.0 -100
|
1381
|
+
| 6 Beckman & Muller-Landau (2007) Panama Secondary seed removal 80.0 10.8 -87
|
1382
|
+
| 7 Brodie et al. (2009) Thailand Proportion fruits under adults 0.19 0.68 252
|
1383
|
+
| 7 Brodie et al. (2009) Thailand Seeds dispersed 0.15 0.01 -91
|
1384
|
+
| 8 Chapman & Onderdonk (1998) Uganda Seedling density, non-valley sites 12.5 5.5 -56
|
1385
|
+
| 8 Chapman & Onderdonk (1998) Uganda Seedling richness, non-valley sites 5.0 3.1 -39
|
1386
|
+
| 8 Chapman & Onderdonk (1998) Uganda Seedling density, valley bottom 2.5 1.3 -50
|
1387
|
+
meta | 31
|
1388
|
+
blank |
|
1389
|
+
|
|
1390
|
+
|
|
1391
|
+
text | 8 Chapman & Onderdonk (1998) Uganda Seedling richness, valley bottom 1.3 1.0 -23
|
1392
|
+
| 9 Cordeiro and Howe (2003) Tanzania Seed dispersal 12.8 3.0 -76
|
1393
|
+
| Proportion indiv under adults
|
1394
|
+
| 9 Cordeiro and Howe (2003) Tanzania (<10 m) 57.3 88.5 54
|
1395
|
+
| 9 Cordeiro and Howe (2003) Tanzania Juvenile:Seedling 0.4 0.3 -27
|
1396
|
+
| 9 Cordeiro and Howe (2003) Tanzania Seedling abundance 163.7 96.7 -41
|
1397
|
+
| 10 Cramer et al. (2007) Brazil Seeds dispersed 48.0 16.0 -67
|
1398
|
+
| 10 Cramer et al. (2007) Brazil Seeds dispersed 5.0 12.0 140
|
1399
|
+
| 10 Cramer et al. (2007) Brazil Ave. dispersal distance 7.5 3.0 -60
|
1400
|
+
| 10 Cramer et al. (2007) Brazil Ave. dispersal distance 23.0 18.0 -22
|
1401
|
+
| 10 Cramer et al. (2007) Brazil Max. dipersal distance 20.0 4.0 -80
|
1402
|
+
| 10 Cramer et al. (2007) Brazil Max. dipersal distance 17.0 18.0 6
|
1403
|
+
| 10 Cramer et al. (2007) Brazil Seeds away from parent 27.0 1.0 -96
|
1404
|
+
| 10 Cramer et al. (2007) Brazil Seeds away from parent 8.0 6.0 -25
|
1405
|
+
| 11 DeMattia et al. (2004) Costa Rica Seeds destroyed 100.0 93.6 -6
|
1406
|
+
| 11 DeMattia et al. (2004) Costa Rica Seeds destroyed 68.8 65.6 -5
|
1407
|
+
| 11 DeMattia et al. (2004) Costa Rica Seeds destroyed 100.0 84.1 -16
|
1408
|
+
| 11 DeMattia et al. (2004) Costa Rica Seeds destroyed 31.2 15.6 -50
|
1409
|
+
| 11 DeMattia et al. (2004) Costa Rica Seeds destroyed 93.8 75.0 -20
|
1410
|
+
| 11 DeMattia et al. (2004) Costa Rica Seeds destroyed 28.0 12.2 -57
|
1411
|
+
| 11 DeMattia et al. (2004) Costa Rica Seeds destroyed 18.5 24.5 33
|
1412
|
+
| 11 DeMattia et al. (2004) Costa Rica Seeds cached 25.0 3.1 -88
|
1413
|
+
| 11 DeMattia et al. (2004) Costa Rica Seeds cached 3.07 9.22 200
|
1414
|
+
| 12 Dirzo & Miranda (1991) Mexico Herbivory 0.27 0.00 -100
|
1415
|
+
| 12 Dirzo & Miranda (1991) Mexico Seedling density 22.6 52.8 134
|
1416
|
+
| 12 Dirzo & Miranda (1991) Mexico Seedling species richness 6.65 2.30 -65
|
1417
|
+
| 12 Dirzo & Miranda (1991) Mexico Seedling diversity 3.71 1.07 -71
|
1418
|
+
| 12 Dirzo & Miranda (1991) Mexico Seedling species dominance 14.0 2.0 -86
|
1419
|
+
| 13 Donatti et al. (2009) Brazil Seeds predated 0.18 0.03 -83
|
1420
|
+
| 13 Donatti et al. (2009) Brazil Seeds cached 0.33 0.13 -61
|
1421
|
+
| 14 Fadini et al. (2009) Brazil Seed dispersal 1.6 0.9 -42
|
1422
|
+
| 14 Fadini et al. (2009) Brazil Seed predation 99.7 7.4 -93
|
1423
|
+
| 14 Fadini et al. (2009) Brazil Seedling density 1000 80 -92
|
1424
|
+
| 15 Farwig et al. (2006) Kenya seed removal 0.97 1.57 62
|
1425
|
+
| 16 Fleury & Galetti (2006) Brazil Seed predation 15.8 48.0 203
|
1426
|
+
| 16 Fleury & Galetti (2006) Brazil Seed predation 15.8 0.0 -100
|
1427
|
+
| 17 Galetti et al. (2006) Brazil Seed predation (%) 6.9 0.3 -96
|
1428
|
+
| 17 Galetti et al. (2006) Brazil Seed caching (%) 12.2 3.4 -72
|
1429
|
+
| 17 Galetti et al. (2006) Brazil Seed predation (%) 38.4 2.0 -95
|
1430
|
+
| 17 Galetti et al. (2006) Brazil Seed predation (%) 34.4 69.6 102
|
1431
|
+
| 17 Galetti et al. (2006) Brazil Seedling density 148.2 34.5 -77
|
1432
|
+
| 17 Galetti et al. (2006) Brazil Seedling:Adult 6.96 0.35 -95
|
1433
|
+
| 17 Galetti et al. (2006) Brazil Sapling:Seedling 1.98 10.07 409
|
1434
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed removal 0.41 0.13 -67
|
1435
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed removal 0.31 0.37 20
|
1436
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed removal 0.88 0.94 7
|
1437
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed removal 0.59 0.91 56
|
1438
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed removal 0.66 0.88 33
|
1439
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed removal 0.87 0.38 -56
|
1440
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed removal 0.98 0.40 -59
|
1441
|
+
meta | 32 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
1442
|
+
blank |
|
1443
|
+
|
|
1444
|
+
|
|
1445
|
+
text | 18 Guariguata et al. (2000) Costa Rica Secondary seed predation 0.41 0.13 -67
|
1446
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed predation 0.31 0.37 20
|
1447
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed predation 0.77 0.91 18
|
1448
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed predation 0.55 0.91 64
|
1449
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed predation 0.57 0.78 38
|
1450
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed predation 0.73 0.38 -48
|
1451
|
+
| 18 Guariguata et al. (2000) Costa Rica Secondary seed predation 0.95 0.40 -58
|
1452
|
+
| 18 Guariguata et al. (2000) Costa Rica Seed caching 0.00 0.00 0
|
1453
|
+
| 18 Guariguata et al. (2000) Costa Rica Seed caching 0.00 0.00 0
|
1454
|
+
| 18 Guariguata et al. (2000) Costa Rica Seed caching 0.03 0.11 300
|
1455
|
+
| 18 Guariguata et al. (2000) Costa Rica Seed caching 0.01 0.03 400
|
1456
|
+
| 18 Guariguata et al. (2000) Costa Rica Seed caching 0.10 0.09 -7
|
1457
|
+
| 18 Guariguata et al. (2000) Costa Rica Seed caching 0.00 0.13 100
|
1458
|
+
| 18 Guariguata et al. (2000) Costa Rica Seed caching 0.00 0.03 100
|
1459
|
+
| 18 Guariguata et al. (2000) Costa Rica Tertiary seed removal/predation 0.50 0.81 63
|
1460
|
+
| 18 Guariguata et al. (2000) Costa Rica Tertiary seed removal/predation 1.00 0.80 -20
|
1461
|
+
| 18 Guariguata et al. (2000) Costa Rica Tertiary seed removal/predation 1.00 1.00 0
|
1462
|
+
| 18 Guariguata et al. (2000) Costa Rica Seedling survival 0.00 0.07 100
|
1463
|
+
| 19 Guariguata et al. (2002) Costa Rica Seeds dispersed 0.11 0.03 17
|
1464
|
+
| 19 Guariguata et al. (2002) Costa Rica Seeds dispersed 0.00 0.02 -67
|
1465
|
+
| 20 Holbrook & Loiselle (2009) Ecuador Seeds removed (primary) 89.4 66.8 -25
|
1466
|
+
| 21 Ickes, K., et al. 2001. Malaysia Seedlings 75.5 117.5 56
|
1467
|
+
| 21 Ickes, K., et al. 2001. Malaysia Sapling density 107.1 142.3 33
|
1468
|
+
| 21 Ickes, K., et al. 2001. Malaysia Mortality 10.0 8.7 -13
|
1469
|
+
| 21 Ickes, K., et al. 2001. Malaysia Recruits 14.9 48.8 228
|
1470
|
+
| 21 Ickes, K., et al. 2001. Malaysia Species richness 50.6 55.7 10
|
1471
|
+
| 21 Ickes, K., et al. 2001. Malaysia Diversity 45.8 39.7 -13
|
1472
|
+
| 21 Ickes, K., et al. 2001. Malaysia Liana proportion of stems 25.9 30.5 18
|
1473
|
+
| 22 Kirika et al. (2008) Uganda Seed dispersal 14124 3714 -74
|
1474
|
+
| 23 Kurten (2010a) Panama seed mass 0.21 0.32 58
|
1475
|
+
| 23 Kurten (2010a) Panama SLA 20.0 22.4 12
|
1476
|
+
| 23 Kurten (2010a) Panama Leaf toughness 1.49 1.49 0
|
1477
|
+
| 23 Kurten (2010a) Panama Wood density 0.65 0.64 -2
|
1478
|
+
| 24 Kurten (2010b) Panama Secondary seed predation 0.50 0.81 63
|
1479
|
+
| 24 Kurten (2010b) Panama Secondary seed predation 0.90 0.85 -5
|
1480
|
+
| 24 Kurten (2010b) Panama Secondary seed predation 0.53 0.11 -79
|
1481
|
+
| 24 Kurten (2010b) Panama Secondary seed predation 0.00 0.00 0
|
1482
|
+
| 24 Kurten (2010b) Panama Seed caching 1.16 1.33 15
|
1483
|
+
| 24 Kurten (2010b) Panama Seed caching 0.83 1.16 40
|
1484
|
+
| 25 Lizcano (2006) Colombia Richness 8.02 11.24 40
|
1485
|
+
| 25 Lizcano (2006) Colombia Shannon Index 0.82 0.75 -9
|
1486
|
+
| 26 McConkey & Drake (2006) Tonga Seed dispersal 0.34 0.03 -90
|
1487
|
+
| 27 Nuñez-Iturri et al. (2007) Peru Sapling richness - total 47.4 50.4 6
|
1488
|
+
| 27 Nuñez-Iturri et al. (2007) Peru Sapling richness -large mammal 16.6 7.8 -53
|
1489
|
+
| 27 Nuñez-Iturri et al. (2007) Peru Sapling richness - nongame 27.1 36.6 35
|
1490
|
+
| 27 Nuñez-Iturri et al. (2007) Peru Sapling richness - abiotic 3.70 6.00 62
|
1491
|
+
| 27 Nuñez-Iturri et al. (2007) Peru Sapling density - total 78.3 90.0 15
|
1492
|
+
| 27 Nuñez-Iturri et al. (2007) Peru Sapling density -large mammal 26.8 11.3 -58
|
1493
|
+
| 27 Nuñez-Iturri et al. (2007) Peru Sapling density - nongame 45.5 67.8 49
|
1494
|
+
meta | 33
|
1495
|
+
blank |
|
1496
|
+
|
|
1497
|
+
|
|
1498
|
+
text | 27 Nuñez-Iturri et al. (2007) Peru Sapling density - abiotic 5.91 10.98 86
|
1499
|
+
| 28 Nuñez-Iturri et al. (2008) Peru Species richness (primate disp) 1.60 0.60 -63
|
1500
|
+
| 28 Nuñez-Iturri et al. (2008) Peru Species richness (abiotic disp) 1.40 1.80 29
|
1501
|
+
| 28 Nuñez-Iturri et al. (2008) Peru Species richness 145 100 -31
|
1502
|
+
| 28 Nuñez-Iturri et al. (2008) Peru Density (primate disp) 1.90 0.90 -53
|
1503
|
+
| 28 Nuñez-Iturri et al. (2008) Peru Density (abiotic) 3.60 11.30 214
|
1504
|
+
| 29 Roldan & Simonetti (2001) Bolivia Seed predation 0.43 0.64 49
|
1505
|
+
| 29 Roldan & Simonetti (2001) Bolivia Trampling survival 0.78 0.90 15
|
1506
|
+
| 29 Roldan & Simonetti (2001) Bolivia Seedling density 4.21 3.92 -7
|
1507
|
+
| 29 Roldan & Simonetti (2001) Bolivia Species richness 35.0 34.0 -3
|
1508
|
+
| 29 Roldan & Simonetti (2001) Bolivia Seedling spp:Adult spp 0.61 0.59 -5
|
1509
|
+
| 29 Roldan & Simonetti (2001) Bolivia Seedling composition 4.21 3.92 -7
|
1510
|
+
| 30 Royo & Carson (2005) Panama Species richness 16.8 13.1 -22
|
1511
|
+
| 30 Royo & Carson (2005) Panama Herb Density 1.21 1.19 -2
|
1512
|
+
| 30 Royo & Carson (2005) Panama Density dominants 0.42 0.35 -17
|
1513
|
+
| 30 Royo & Carson (2005) Panama Density rare 0.34 0.16 -53
|
1514
|
+
| 30 Royo & Carson (2005) Panama Cover 7.90 5.90 -25
|
1515
|
+
| 30 Royo & Carson (2005) Panama Cover of dominants 2.65 1.50 -43
|
1516
|
+
| 31 Sethi & Howe (2009) India Total seedlings 2.55 0.76 -70
|
1517
|
+
| 31 Sethi & Howe (2009) India Seedlings under parent 0.37 0.60 64
|
1518
|
+
| 31 Sethi & Howe (2009) India Seedlings away from parent 2.19 0.16 -93
|
1519
|
+
| 31 Sethi & Howe (2009) India Total seedlings 2.17 0.81 -62
|
1520
|
+
| 31 Sethi & Howe (2009) India Seedlings under parent 0.99 0.35 -65
|
1521
|
+
| 31 Sethi & Howe (2009) India Seedlings away from parent 1.18 0.46 -61
|
1522
|
+
| 31 Sethi & Howe (2009) India Total seedlings 4.16 0.81 -80
|
1523
|
+
| 31 Sethi & Howe (2009) India Seedlings under parent 2.96 0.58 -81
|
1524
|
+
| 31 Sethi & Howe (2009) India Seedlings away from parent 1.20 0.24 -80
|
1525
|
+
| 32 Sork (1987) Panama Secondary seed predation 0.94 0.41 -56
|
1526
|
+
| 32 Sork (1987) Panama seedling survival 0.69 0.97 42
|
1527
|
+
| Peru/
|
1528
|
+
| 33 Terborgh & Wright (1994) Panama Seed predation 0.35 0.82 136
|
1529
|
+
| Peru/
|
1530
|
+
| 33 Terborgh & Wright (1994) Panama Seedling density 38.3 29.3 -23
|
1531
|
+
| Peru/
|
1532
|
+
| 33 Terborgh & Wright (1994) Panama Seedling recruitment 0.25 0.96 276
|
1533
|
+
| Peru/
|
1534
|
+
| 33 Terborgh & Wright (1994) Panama Seedling mortality 0.20 0.29 43
|
1535
|
+
| 34 Terborgh et al. (2008) Peru Recruit. Bird dispersed 0.23 0.24 4
|
1536
|
+
| 34 Terborgh et al. (2008) Peru Recruit. Bat dispersed 0.10 0.11 16
|
1537
|
+
| 34 Terborgh et al. (2008) Peru Recruit. Lg. primate dispersed 0.25 0.19 -24
|
1538
|
+
| Recruit. Sm. arboreal mammal
|
1539
|
+
| 34 Terborgh et al. (2008) Peru dispersed 0.33 0.24 -26
|
1540
|
+
| Recruit. Terrestrial mammal
|
1541
|
+
| 34 Terborgh et al. (2008) Peru dispersed 0.04 0.02 -50
|
1542
|
+
| 34 Terborgh et al. (2008) Peru Recruit. Wind disp. 0.05 0.17 278
|
1543
|
+
| 35 Wang et al. (2007) Cameroon Diaspore under adult 10.0 50.0 400
|
1544
|
+
| 35 Wang et al. (2007) Cameroon Seed dispersal 0.98 0.58 -41
|
1545
|
+
| 36 Wright et al. (2000) Panama Seed predation 90.8 47.7 -47
|
1546
|
+
| 36 Wright et al. (2000) Panama Seed predation 0.03 0.34 1033
|
1547
|
+
| 36 Wright et al. (2000) Panama Seed density under parent 180 2749 1427
|
1548
|
+
| 36 Wright et al. (2000) Panama Seed density away from parent 2.65 1.79 -32
|
1549
|
+
| 36 Wright et al. (2000) Panama Prop. seeds dispersed 0.93 0.39 -58
|
1550
|
+
meta | 34 CHAPTER 1: CASCADING EFFECTS OF DEFAUNATION ON TROPICAL PLANTS
|
1551
|
+
blank |
|
1552
|
+
|
|
1553
|
+
|
|
1554
|
+
text | 36 Wright et al. (2000) Panama Seedling density 0.0 0.0 300
|
1555
|
+
| 36 Wright et al. (2000) Panama Seedlings:Adult 11.0 28.9 163
|
1556
|
+
| 36 Wright et al. (2000) Panama Seed predation 91.7 21.7 -76
|
1557
|
+
| 36 Wright et al. (2000) Panama Seed predation 0.1 0.3 460
|
1558
|
+
| 36 Wright et al. (2000) Panama Seed density under parent 910 1290 42
|
1559
|
+
| 36 Wright et al. (2000) Panama Seed density away from parent 4.4 2.8 -37
|
1560
|
+
| 36 Wright et al. (2000) Panama Prop. seeds dispersed 0.9 0.1 -93
|
1561
|
+
| 36 Wright et al. (2000) Panama Seedling density 0.1 0.2 129
|
1562
|
+
| 36 Wright et al. (2000) Panama Seedlings:Adult 113.8 92.5 -19
|
1563
|
+
| 37 Wright et al. (2001) Panama Seed density under parent tree 24.6 35.7 46
|
1564
|
+
| 37 Wright et al. (2001) Panama Seed density away from parent 0.9 0.2 -81
|
1565
|
+
| tree
|
1566
|
+
| 37 Wright et al. (2001) Panama Seedling density under parent 0.0 0.1 282
|
1567
|
+
| Seedling density away from
|
1568
|
+
| 37 Wright et al. (2001) Panama parent 0.0 0.1 282
|
1569
|
+
| 37 Wright et al. (2001) Panama Seedling density (total) 0.0 0.1 282
|
1570
|
+
| 37 Wright et al. (2001) Panama Seed predation-rodents 0.8 0.4 -46
|
1571
|
+
| 37 Wright et al. (2001) Panama Seed predation-bruchid 0.1 0.4 266
|
1572
|
+
| 38 Wright et al. (2007) Panama Community mean seed mass 90 100 11
|
1573
|
+
| 38 Wright et al. (2007) Panama Prop. seedlings (hunted disperser) 0.7 0.4 -40
|
1574
|
+
| 38 Wright et al. (2007) Panama Prop. seedlings (unhunted 0.2 0.4 75
|
1575
|
+
| disperser)
|
1576
|
+
| 38 Wright et al. (2007) Panama Proportion lianas 0.1 0.4 150
|
1577
|
+
| 38 Wright et al. (2007) Panama Seedling density 15.2 9.4 -38
|
1578
|
+
| 38 Wright et al. (2007) Panama Seedling Richness 70.7 69.8 -1
|
1579
|
+
| 38 Wright et al. (2007) Panama Seedling S-W Diversity 2.6 3.2 23
|
1580
|
+
meta | 35
|
1581
|
+
blank |
|
1582
|
+
|
|
1583
|
+
|
|
1584
|
+
|
|
1585
|
+
title | Chapter 2
|
1586
|
+
blank |
|
1587
|
+
text | Reduced seed dispersal as a
|
1588
|
+
| consequence of hunting lowers
|
1589
|
+
| community-level wood density in a
|
1590
|
+
| Neotropical forest
|
1591
|
+
| Authors: Erin L. Kurten, S. Joseph Wright, Andrés Hernandéz , Walter P. Carson
|
1592
|
+
blank |
|
1593
|
+
title | Abstract
|
1594
|
+
blank |
|
1595
|
+
text | Defaunation alters interactions between plants and their seed dispersers and predators,
|
1596
|
+
| and is sometimes associated with decreased diversity at the community level. A more
|
1597
|
+
| cryptic plant response to defaunation is an altered distribution of life histories and
|
1598
|
+
| functional traits in the community. In this study, we censused 12,769 seedlings in a
|
1599
|
+
| long-term terrestrial mammal exclosure experiment (LTEE) in Central Panama to
|
1600
|
+
| examine how vertebrate seed dispersers and seed predators shape relative abundances
|
1601
|
+
| of species classified by dispersal mode, growth forms, seed mass, leaf mass per area
|
1602
|
+
| (LMA), leaf toughness, and wood density. We then compared exclosure results with
|
1603
|
+
| data from a natural comparison of 38,250 seedlings in nearby hunted and unhunted
|
1604
|
+
| sites. The exclosure experiment excludes terrestrial seed predators and herbivores but
|
1605
|
+
| not seed dispersers such as primates, birds, and bats. In contrast, the hunting
|
1606
|
+
meta | 36 CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
|
1607
|
+
blank |
|
1608
|
+
|
|
1609
|
+
|
|
1610
|
+
text | comparison reduces the abundance of all three groups. We tested the hypotheses that
|
1611
|
+
| (1) where seed dispersal is disrupted, species with unhunted dispersal modes, and
|
1612
|
+
| lianas, which are abiotically dispersed, are favored, (2) where seed predation is
|
1613
|
+
| reduced, larger-seed plant species are favored, and (3) where herbivory is reduced,
|
1614
|
+
| species with lower LMA, leaf toughness, and wood density are favored. Consistent
|
1615
|
+
| with our expectations, dispersal-driven changes in the relative abundance of growth
|
1616
|
+
| forms or dispersal mode classes were not observed in the terrestrial mammal exclosure
|
1617
|
+
| experiment, while higher median seed mass as a consequence of reduced seed
|
1618
|
+
| predation was observed. In contrast to our hypothesis, leaf functional traits did not
|
1619
|
+
| differ as a consequence of defaunation either in the forest comparison or in the LTEE.
|
1620
|
+
| Interestingly, wood density responses differed between our two experiments. Species
|
1621
|
+
| dispersed by mammals and large birds had significantly higher mean wood density
|
1622
|
+
| than wind dispersed species, suggesting that seed dispersal, rather than seedling
|
1623
|
+
| herbivory, may mediate decreases in community median wood density in hunted
|
1624
|
+
| forests.
|
1625
|
+
blank |
|
1626
|
+
title | Introduction
|
1627
|
+
blank |
|
1628
|
+
text | Over-hunting has caused severe declines, and even local extirpations, of hunted
|
1629
|
+
| wildlife populations in tropical forests throughout Latin America (Peres & Palacios
|
1630
|
+
| 2007), Africa (Fa & Brown 2009), and Asia (Corlett 2007). Defaunation perturbs
|
1631
|
+
| plant interactions with the frugivores, granivores, and herbivores that play critical
|
1632
|
+
| roles in establishing the composition and spatial distribution of seedlings in tropical
|
1633
|
+
| forest seedling banks. Reduced seed dispersal in hunted forests results in higher
|
1634
|
+
| proportions of undispersed seeds under parent trees of species reliant on hunted biotic
|
1635
|
+
| dispersal agents (Wright & Duber 2001, Cordiero & Howe 2003, Babweteera et al
|
1636
|
+
| 2007, Sethi & Howe 2009). Vertebrate seed predation rates may increase or decrease,
|
1637
|
+
| depending on the severity of defaunation and the size of the seeds and seed predators
|
1638
|
+
| affected (Guariguata et al. 2000, Galetti et al. 2006, Dirzo et al. 2007). Vertebrate
|
1639
|
+
| herbivory rates can also be drastically reduced (Dirzo and Miranda 1991). The net
|
1640
|
+
| effect of these perturbations can be the loss of plant diversity (Dirzo and Miranda
|
1641
|
+
meta | 37
|
1642
|
+
blank |
|
1643
|
+
|
|
1644
|
+
|
|
1645
|
+
text | 1991, Chapman & Onderdonk 1998), with up to 66% of species failing to recruit in the
|
1646
|
+
| most extreme case documented.
|
1647
|
+
| Other important changes may also be occurring in the plant community even if
|
1648
|
+
| species richness is unaffected. Species with hunted dispersal agents, such as primates
|
1649
|
+
| or large birds, consistently decrease in abundance in hunted forests, while species with
|
1650
|
+
| abiotic or unhunted dispersal agents increase (Wright et al. 2007b, Nuñez-Iturri et al.
|
1651
|
+
| 2008, Terborgh et al. 2008). Lianas, the majority of which are abiotically dispersed in
|
1652
|
+
| this forest (Hardesty & Muller-Landau 2005), also increase in abundance in hunted
|
1653
|
+
| sites (Wright et al. 2007b). Where dispersal of large, primate-dispersed seeds is
|
1654
|
+
| disrupted by local extirpation of ateline monkeys, the relative abundance of those plant
|
1655
|
+
| species is lower than in sites where ateline monkeys are present (Nuñez-Iturri et al.
|
1656
|
+
| 2008). In sites where hunting decreases rodent seed predator populations, the median
|
1657
|
+
| seed mass of the seedling community is higher than in unhunted sites (Wright et al.
|
1658
|
+
| 2007b).
|
1659
|
+
| In this study, our first goal was to move beyond investigations of dispersal
|
1660
|
+
| mode classes and seed mass to examine the effect of defaunation on other functional
|
1661
|
+
| traits. Lower abundances of browsers and other seedling predators in hunted sites
|
1662
|
+
| should lead to reduced vertebrate herbivory and seedling predation. Leaf mass per
|
1663
|
+
| unit area (LMA), low leaf laminar toughness (hereafter referred to as “toughness”),
|
1664
|
+
| and wood density are correlated with palatability to vertebrates or seedling survival
|
1665
|
+
| (Wardle et al. 2002, Alvarez-Clare & Kitajima 2007). We hypothesized that species
|
1666
|
+
| with low leaf area per unit mass, low leaf laminar toughness, and lower wood density
|
1667
|
+
| should be favored in hunted sites.
|
1668
|
+
| A weakness of many forest comparison studies in defaunation work is that they
|
1669
|
+
| lack replication of hunted and unhunted forests. Even when there is replication,
|
1670
|
+
| differences in climate, soils, forest age, fragmentation or other anthropogenic factors
|
1671
|
+
| may covary with hunting intensity in comparative studies, making it difficult to
|
1672
|
+
| attribute the patterns observed to hunting alone. Therefore, a second goal of this study
|
1673
|
+
| was to validate results from forest comparisons with data from a long-term exclosure
|
1674
|
+
| experiment (LTEE). We conducted this study in Central Panama, where a hunting
|
1675
|
+
meta | 38 CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
|
1676
|
+
blank |
|
1677
|
+
|
|
1678
|
+
|
|
1679
|
+
text | defaunation gradient has been previously documented (Wright et al. 2007b). Within
|
1680
|
+
| the unhunted, protected sites, a terrestrial mammal exclosure experiment has been
|
1681
|
+
| ongoing for the past fifteen years (Royo & Carson 2005).
|
1682
|
+
| Because hunting typically disrupts multiple plant-animal interactions
|
1683
|
+
| simultaneously, it can be difficult to determine the relative influence of lost seed
|
1684
|
+
| dispersers, seed predators, or herbivores on resulting seedling communities in
|
1685
|
+
| comparative studies. A third goal of this study was to improve the extent to which
|
1686
|
+
| changes in the seedling community could be attributed to changes in particular
|
1687
|
+
| interactions. Unlike the hunted forest comparison, our LTEE excludes terrestrial seed
|
1688
|
+
| predators and herbivores from exclosure plots, but does not alter the abundance of
|
1689
|
+
| primary dispersal agents such as primates and most large birds. By comparing results
|
1690
|
+
| between the forest comparison and exclosure approaches, we can identify which
|
1691
|
+
| changes in the seedling community are due to changes in seed dispersal and which are
|
1692
|
+
| due to changes in seed or seedling predation. .
|
1693
|
+
| We predicted that seedling communities in exclosures would have higher
|
1694
|
+
| median seed massas a consequence of lower seed predation, consistent with the forest
|
1695
|
+
| comparison (Wright et al. 2007). In contrast to the forest comparison experiment, we
|
1696
|
+
| predicted the LTEE would not show differences in the relative abundances of dispersal
|
1697
|
+
| mode classes or growth forms. We expected that median LMA, toughness and wood
|
1698
|
+
| density would be lower in exclosure plots relative to paired plots open to terrestrial
|
1699
|
+
| mammals, and in hunted forests relative to unhunted forests, as a consequence of
|
1700
|
+
| reduced herbivory.
|
1701
|
+
blank |
|
1702
|
+
|
|
1703
|
+
title | Methods
|
1704
|
+
blank |
|
1705
|
+
|
|
1706
|
+
text | Study sites. The Barro Colorado National Monument (BCNM) is a group of islands
|
1707
|
+
| and mainland peninsulas located in Lake Gatun in the Republic of Panama. Because
|
1708
|
+
| of forest guard patrol and researcher presence, activity of poachers is virtually
|
1709
|
+
| nonexistent on Barro Colorado Island (BCI) itself and is highly reduced on Gigante
|
1710
|
+
| (GIG) and other peninsulas. The Parque Nacional Soberanía (PNS) is a protected area
|
1711
|
+
meta | 39
|
1712
|
+
blank |
|
1713
|
+
|
|
1714
|
+
|
|
1715
|
+
text | contiguous with the BCNM, which is not actively patrolled. Intensity of poaching
|
1716
|
+
| within the PNS varies with accessibility, but is much greater than within the BCNM
|
1717
|
+
| (Wright et al. 2000).
|
1718
|
+
blank |
|
1719
|
+
|
|
1720
|
+
text | Exclosure experimental design. Between late-1993 and mid-1994, eight pairs of
|
1721
|
+
| fenced, exclosure plots and open, control plots were established within the BCNM
|
1722
|
+
| (Royo & Carson 2005). Paired fenced and unfenced plots are 30 m x 45 m and are
|
1723
|
+
| approximately 5 m apart. Exclosure fences are constructed of 12.7 x 12.7 cm
|
1724
|
+
| galvanized steel fencing 2.2 m tall and buried 0.25 m deep. A secondary 1.3 x 1.3 cm
|
1725
|
+
| mesh surrounds the lower 70 cm and also extends 0.25 m below ground. Twenty-
|
1726
|
+
| eight 0.5 x 0.5 m subplots were established in each of the 16 plots in a stratified
|
1727
|
+
| random fashion to census seedlings. To avoid fence effects, no subplots were
|
1728
|
+
| established within a 5-7 m buffer zone of a plot edge. Within each subplot, each plant
|
1729
|
+
| less than 50 cm in height was tagged, measured, and identified. Seedling census data
|
1730
|
+
| were collected in 2006.
|
1731
|
+
blank |
|
1732
|
+
|
|
1733
|
+
text | Exclosure effectiveness. To assess differences in the animal communities between
|
1734
|
+
| open and exclosure treatments, Reconyx RC-55 infrared cameras (Reconyx, Inc.,
|
1735
|
+
| Holmen, WI) were used to monitor mammal activity in the 16 plots between August
|
1736
|
+
| and October 2008. Each plot was monitored at 6-7 locations, for a total of 41 camera
|
1737
|
+
| trap days per plot. A camera trigger was counted as a new “visit” if (1) it was a
|
1738
|
+
| different species than the prior trigger, or (2) if 60 minutes had elapsed between
|
1739
|
+
| triggers (Di Bitetti et al. 2008). We chose this method of quantification because
|
1740
|
+
| unmarked individuals of most mammals in this community cannot be distinguished by
|
1741
|
+
| photograph, and because this measure of activity likely describes animal impact on
|
1742
|
+
| each plot more accurately than abundance. Because it was difficult to accurately
|
1743
|
+
| count individuals for social animals such as peccaries (Tayassu tajacu) and coatis
|
1744
|
+
| (Nasua narica), activity by these species was analyzed as the number of visits by
|
1745
|
+
| social groups rather than visits by individuals.
|
1746
|
+
meta | 40 CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
|
1747
|
+
blank |
|
1748
|
+
|
|
1749
|
+
|
|
1750
|
+
text | Hunting intensity comparison. At 9 protected sites (BCNM) and 11 intensely hunted
|
1751
|
+
| sites (PNS), all adult trees larger than 20 cm diameter at breast height (dbh) within a 1
|
1752
|
+
| ha plot were mapped and identified by Condit et al. (2002) and Wright et al. (2007b).
|
1753
|
+
| Between June and December 2004, all woody plants less than 50 cm tall in an 8 x 8 m
|
1754
|
+
| subplot were censused by Wright et al. (2007b). Seedling plots were at the center of
|
1755
|
+
| each tree plot, or as close as possible in three plots in which tree falls occurred
|
1756
|
+
| between adult and seedling censuses. A total of 38250 individuals comprising 312
|
1757
|
+
| identified species were recorded (Wright et al. 2007b).
|
1758
|
+
blank |
|
1759
|
+
|
|
1760
|
+
text | Plant traits. Wright et al. (2010) determined life history traits, dry seed mass, leaf
|
1761
|
+
| mass per area (LMA), laminar toughness, and wood density for species in central
|
1762
|
+
| Panama. In this study, dry seed mass was measured as endosperm plus embryo mass
|
1763
|
+
| after oven drying to constant mass at 60ºC. Leaf mass per unit area was measured on
|
1764
|
+
| shade leaves as the mass of a standard-sized leaf disc after oven drying to constant
|
1765
|
+
| mass at 60ºC divided by the area of the disc. Laminar toughness was measured as the
|
1766
|
+
| force necessary to cut across a leaf, perpendicular to the midvein (Lucas et al. 2000).
|
1767
|
+
| Wood specific gravity, or mass after drying at 100ºC per unit volume, was used as the
|
1768
|
+
| unit of wood density. Data on dispersal agents have been assembled from published
|
1769
|
+
| studies and long-term personal observations.
|
1770
|
+
blank |
|
1771
|
+
|
|
1772
|
+
text | Analyses. We used a MANOVA to test whether mammal activity differed between
|
1773
|
+
| open and control plots for each vertebrate species observed. Paired t-tests were used
|
1774
|
+
| to test for differences in the relative abundance of growth forms, dispersal mode
|
1775
|
+
| classes, and functional traits. For the hunting comparison, an ANCOVA was used to
|
1776
|
+
| determine whether the correspondence of functional traits between seedling and adult
|
1777
|
+
| communities differed with hunting. Statistical analyses were performed with SYSTAT
|
1778
|
+
| © 11.0 (Richmond, CA, U.S.A.) and R version 2.7.2 (R Development Core Team,
|
1779
|
+
| 2008).
|
1780
|
+
meta | 41
|
1781
|
+
blank |
|
1782
|
+
|
|
1783
|
+
|
|
1784
|
+
title | Results
|
1785
|
+
blank |
|
1786
|
+
|
|
1787
|
+
text | EXCLOSURE EFFECTIVENESS. Fenced plots excluded non-climbing, terrestrial
|
1788
|
+
| granivores and herbivores from exclosures, including agoutis (Dasyprocta punctata),
|
1789
|
+
| paca (Agouti paca), deer (Mazama Americana and Odocoileus virginianus), and
|
1790
|
+
| peccaries (T. tajacu) (Fig. 1). Most climbing animals appeared to be undeterred by the
|
1791
|
+
| exclosure treatment. Spiny rats (Proechimys steerei) showed higher activity in
|
1792
|
+
| exclosures than controls, perhaps responding to a lack of competition for food, greater
|
1793
|
+
| cover, or a reduction in ocelet abundance (Felis pardalis) in the exclosures. Most
|
1794
|
+
| birds were not affected by the exclosures, a notable exception being tinamous, which
|
1795
|
+
| are seed predators (Erand et al. 1991).
|
1796
|
+
blank |
|
1797
|
+
|
|
1798
|
+
text | 0
|
1799
|
+
| Agouti ***
|
1800
|
+
blank |
|
1801
|
+
text | 0 20 40 60 80 100
|
1802
|
+
blank |
|
1803
|
+
text | Anteater
|
1804
|
+
| 0
|
1805
|
+
| Armadillo
|
1806
|
+
| 0
|
1807
|
+
| Capuchin
|
1808
|
+
| Coati†
|
1809
|
+
| 0
|
1810
|
+
| Deer
|
1811
|
+
| 0
|
1812
|
+
| Mouse
|
1813
|
+
| 0
|
1814
|
+
| Ocelot *
|
1815
|
+
| Opposum
|
1816
|
+
| 0
|
1817
|
+
| *
|
1818
|
+
| Paca **
|
1819
|
+
| 0
|
1820
|
+
| Peccary† **
|
1821
|
+
| 0
|
1822
|
+
| Rabbit
|
1823
|
+
| Spiny Rat
|
1824
|
+
| Squirrel
|
1825
|
+
blank |
|
1826
|
+
text | 0
|
1827
|
+
| Tinamou
|
1828
|
+
| Birds (other)
|
1829
|
+
blank |
|
1830
|
+
text | 0 2 4 6 8 10 12 14
|
1831
|
+
| Visits/plot
|
1832
|
+
blank |
|
1833
|
+
|
|
1834
|
+
|
|
1835
|
+
|
|
1836
|
+
text | FIGURE 2.1. Total visits per plot by species for control plots (dark grey) and exclosure
|
1837
|
+
| plots (light grey). Zeros denote no individuals observed in exclosures. *** p < 0.001,
|
1838
|
+
| ** p < 0.01, * p < 0.05, p < 0.1; † groups, not individuals
|
1839
|
+
meta | 42 CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
|
1840
|
+
blank |
|
1841
|
+
|
|
1842
|
+
|
|
1843
|
+
|
|
1844
|
+
text | DISPERSAL AGENTS & LIFEFORMS. A total of 12,769 seedlings of 322 species were
|
1845
|
+
| recorded in the 2006 LTEE seedling census. Of those, dispersal agents were known
|
1846
|
+
| for 247 species (76.7%) and 12575 stems (98.5%), and growth form was known for
|
1847
|
+
| 241 species (74.8%) and 12468 stems (97.6%). Consistent with our expectations,
|
1848
|
+
| there was no difference in the proportions of seedlings with different dispersal agents
|
1849
|
+
| (hunted: t = 1.161, P = 0.2651; unhunted t = 1.861, P = 0.089) (Fig. 2) or growth
|
1850
|
+
| forms (free-standing: t = 1.7131, P = 0.1096) (Fig. 3) in the LTEE.
|
1851
|
+
meta | 1.0
|
1852
|
+
blank |
|
1853
|
+
|
|
1854
|
+
|
|
1855
|
+
|
|
1856
|
+
text | Hunted Mixed Unhunted
|
1857
|
+
| 0.8
|
1858
|
+
| Proportion of seedlings
|
1859
|
+
blank |
|
1860
|
+
text | 0.6
|
1861
|
+
| 0.4
|
1862
|
+
| 0.2
|
1863
|
+
| 0.0
|
1864
|
+
blank |
|
1865
|
+
|
|
1866
|
+
|
|
1867
|
+
|
|
1868
|
+
text | Open Excl Open Excl Open Excl
|
1869
|
+
blank |
|
1870
|
+
text | Treatment by Disperser
|
1871
|
+
| FIGURE 2.2. Proportion of seedlings by dispersal mode class is not significantly
|
1872
|
+
| different between treatments in exclosure experiment.
|
1873
|
+
| 1.0
|
1874
|
+
blank |
|
1875
|
+
|
|
1876
|
+
|
|
1877
|
+
|
|
1878
|
+
text | Climbing Free Standing
|
1879
|
+
| Proportion of seedlings
|
1880
|
+
blank |
|
1881
|
+
text | 0.8
|
1882
|
+
| 0.6
|
1883
|
+
| 0.4
|
1884
|
+
| 0.2
|
1885
|
+
| 0.0
|
1886
|
+
blank |
|
1887
|
+
|
|
1888
|
+
|
|
1889
|
+
|
|
1890
|
+
text | Open Excl Open Excl
|
1891
|
+
blank |
|
1892
|
+
text | Treatment by Growth form
|
1893
|
+
blank |
|
1894
|
+
text | FIGURE 2.3. Proportion of seedlings by life form is not significantly different
|
1895
|
+
| between treatments in exclosure experiment.
|
1896
|
+
meta | 43
|
1897
|
+
blank |
|
1898
|
+
|
|
1899
|
+
|
|
1900
|
+
|
|
1901
|
+
text | SEED MASS. In the LTEE, seed dry mass was known for 166 (51.6 %) of species and
|
1902
|
+
| 10866 (85.1%) of stems. Exclosures removed all but the smallest seed predators. The
|
1903
|
+
| reduction in agouti activity was particularly dramatic (Fig. 4). Consistent with these
|
1904
|
+
| findings, as well as results from the forest comparison (Wright et al. 2007b), median
|
1905
|
+
| seed mass was 44% higher in exclosure plots, relative to controls (t = 2.315, P =
|
1906
|
+
| 0.02261).
|
1907
|
+
blank |
|
1908
|
+
text | 250
|
1909
|
+
| Diaspore Dry mass (mg)
|
1910
|
+
blank |
|
1911
|
+
text | 200
|
1912
|
+
| 150
|
1913
|
+
| 100
|
1914
|
+
blank |
|
1915
|
+
|
|
1916
|
+
|
|
1917
|
+
|
|
1918
|
+
text | Open Excl
|
1919
|
+
blank |
|
1920
|
+
|
|
1921
|
+
text | Treatment
|
1922
|
+
blank |
|
1923
|
+
text | FIGURE 2.4. (A) Median seed mass is significantly higher in exclosures (p <
|
1924
|
+
| 0.02261).
|
1925
|
+
blank |
|
1926
|
+
|
|
1927
|
+
text | LEAF TRAITS. LMA and laminar toughness were known for 11,173 stems (87.5%)
|
1928
|
+
| and 10,904 stems (85.4%) respectively in the LTEE, and for 33,839 stems (87.5 %)
|
1929
|
+
| and 29,962 stems (77.5 %) respectively in the hunting experiment. Exclosure and
|
1930
|
+
| hunting treatments were expected to reduce the number of terrestrial vertebrate
|
1931
|
+
| seedling predators in a way analogous to seed predators. A reduction in vertebrate
|
1932
|
+
| herbivores was expected to favor species with low LMA and small laminar toughness.
|
1933
|
+
| Contrary to expectation, neither the exclosure nor the hunting experiment showed
|
1934
|
+
| significant differences in median LMA or laminar toughness, nor was there a
|
1935
|
+
| significant difference between protected and hunted sites when the correspondence
|
1936
|
+
meta | 44 CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
|
1937
|
+
blank |
|
1938
|
+
|
|
1939
|
+
|
|
1940
|
+
text | between seedling and adult communities was evaluated by ANCOVA (data not
|
1941
|
+
| shown).
|
1942
|
+
blank |
|
1943
|
+
|
|
1944
|
+
text | WOOD DENSITY. Adult wood specific gravity was known for 208 species (64.6% %)
|
1945
|
+
| and 11,620 stems (91.0 %) in the LTEE, and for 239 species (63.2 %) and 28,488
|
1946
|
+
| stems (73.3 %) in the hunting experiment. Stem tissue density is strongly positively
|
1947
|
+
| correlated with seedling survival in this forest (Alvarez-Clare & Kitajima 2007). If
|
1948
|
+
| greater stem tissue densities confer a protective effect against herbivores, we would
|
1949
|
+
| expect higher wood density species to be favored in open plots relative to exclosures,
|
1950
|
+
| and protected sites relative to hunted sites. Median wood densities were greatly
|
1951
|
+
| reduced in hunted site seedling communities, relative to both protected site seedling
|
1952
|
+
| communities (pooled variance t=3.86, P = 0.0011, one-tailed test) (Fig. 5a), and their
|
1953
|
+
| surrounding adult communities (F1,18 = 16.2, p < 0.001) (Fig. 5b). However, the
|
1954
|
+
| LTEE showed no differenced in median wood density (t = 0.024, P = 0.49) (Fig. 5a).
|
1955
|
+
| 0.65
|
1956
|
+
| Wood density of tree seedlings (g/cm3)
|
1957
|
+
| 0.65
|
1958
|
+
| Wood Specific Gravity (g/cm3)
|
1959
|
+
blank |
|
1960
|
+
|
|
1961
|
+
|
|
1962
|
+
|
|
1963
|
+
text | A B
|
1964
|
+
| Exclosure Hunting
|
1965
|
+
| 0.60
|
1966
|
+
| 0.60
|
1967
|
+
blank |
|
1968
|
+
|
|
1969
|
+
|
|
1970
|
+
|
|
1971
|
+
text | 0.55
|
1972
|
+
| 0.55
|
1973
|
+
blank |
|
1974
|
+
|
|
1975
|
+
|
|
1976
|
+
|
|
1977
|
+
text | 0.50
|
1978
|
+
blank |
|
1979
|
+
|
|
1980
|
+
text | 0.45
|
1981
|
+
| 0.50
|
1982
|
+
blank |
|
1983
|
+
|
|
1984
|
+
|
|
1985
|
+
|
|
1986
|
+
text | 0.45 0.50 0.55 0.60 0.65
|
1987
|
+
| Open Excl Protect Hunt Wood density of canopy trees (g/cm3)
|
1988
|
+
| Treatment
|
1989
|
+
blank |
|
1990
|
+
text | FIGURE 2.5. (A) Median wood density is not significantly different between treatments in the
|
1991
|
+
| exclosure experiment (p = 0.0238), but is significantly lower in hunted sites relative to
|
1992
|
+
| protected sites (p = 0.0011). White and grey boxes indicate analogous treatments (B) Seedling
|
1993
|
+
| median wood density is lower than adult median wood density for tree species in hunted sites
|
1994
|
+
| (dark circles) but not in protected sites (light triangles) (F1,18 = 16.2, p < 0.001). The dashed
|
1995
|
+
| line represents is the 1:1 line at which adult and seedling communities have the same median
|
1996
|
+
| values.
|
1997
|
+
blank |
|
1998
|
+
|
|
1999
|
+
text | We tested whether differences in primary dispersal may be responsible for the
|
2000
|
+
| discrepancy in wood density responses, as it was for differences in dispersal mode and
|
2001
|
+
| growth form. We used an ANOVA to compare mean wood densities across dispersal
|
2002
|
+
meta | 45
|
2003
|
+
blank |
|
2004
|
+
|
|
2005
|
+
|
|
2006
|
+
text | mode classes. Interestingly, species with unhunted dispersal agents had significantly
|
2007
|
+
| lower mean wood density than either species with hunted dispersal modes, or species
|
2008
|
+
| dispersed by agents in both categories (ANOVA, F2, 277, p = 0.0017) (Fig. 6a).
|
2009
|
+
| Specifically, wind dispersed species had significantly lower wood densities compared
|
2010
|
+
| to both mammal and large bird dispersed species (ANOVA, F6, 461, p = 0.0057) (Fig.
|
2011
|
+
| 6b).
|
2012
|
+
blank |
|
2013
|
+
|
|
2014
|
+
text | 0.7
|
2015
|
+
| 1.0
|
2016
|
+
| Mean Wood Specific Gravity (g/cm3)
|
2017
|
+
blank |
|
2018
|
+
|
|
2019
|
+
|
|
2020
|
+
|
|
2021
|
+
text | B
|
2022
|
+
blank |
|
2023
|
+
|
|
2024
|
+
|
|
2025
|
+
|
|
2026
|
+
text | Mean Wood Specific Gravity (g/cm3)
|
2027
|
+
| A a
|
2028
|
+
| a
|
2029
|
+
| b 0.6 ab
|
2030
|
+
| a
|
2031
|
+
| ab
|
2032
|
+
| a ab
|
2033
|
+
| 0.8
|
2034
|
+
blank |
|
2035
|
+
|
|
2036
|
+
|
|
2037
|
+
|
|
2038
|
+
text | ab b
|
2039
|
+
| 0.5
|
2040
|
+
| 0.6
|
2041
|
+
blank |
|
2042
|
+
|
|
2043
|
+
|
|
2044
|
+
|
|
2045
|
+
text | 0.4
|
2046
|
+
| 0.4
|
2047
|
+
blank |
|
2048
|
+
|
|
2049
|
+
|
|
2050
|
+
|
|
2051
|
+
text | 0.3
|
2052
|
+
| 0.2
|
2053
|
+
blank |
|
2054
|
+
|
|
2055
|
+
|
|
2056
|
+
|
|
2057
|
+
text | 0.2
|
2058
|
+
| 0.0
|
2059
|
+
blank |
|
2060
|
+
|
|
2061
|
+
|
|
2062
|
+
|
|
2063
|
+
text | 0.1
|
2064
|
+
blank |
|
2065
|
+
text | Hunted Mixed Unhunted 0.0
|
2066
|
+
| Bat Bird L.Bird Explo Mam Water Wind
|
2067
|
+
| Dispersal Mode Class
|
2068
|
+
| Dispersal Agent
|
2069
|
+
blank |
|
2070
|
+
|
|
2071
|
+
|
|
2072
|
+
|
|
2073
|
+
text | FIGURE 2.6. (A) Species with unhunted dispersal agents have lower WSGs. (B)
|
2074
|
+
| Wind dispersed species have significantly lower mean wood density than both
|
2075
|
+
| mammal and large bird dispersed species. Bars with same letter were not
|
2076
|
+
| significantly different in post hoc comparisons.
|
2077
|
+
blank |
|
2078
|
+
|
|
2079
|
+
title | Discussion
|
2080
|
+
blank |
|
2081
|
+
|
|
2082
|
+
title | Hunting, vertebrate abundance, and plant functional diversity
|
2083
|
+
blank |
|
2084
|
+
|
|
2085
|
+
text | This study demonstrates that hunting effects change in the seedling community of
|
2086
|
+
| tropical forests primarily by perturbing biotic seed dispersal and vertebrate seed
|
2087
|
+
| predation. Increases in lianas and reductions in species with hunted biotic dispersal
|
2088
|
+
| agents were observed in the hunting experiment, where primary dispersers were
|
2089
|
+
| reduced (Wright et al. 2007b), but not in the LTEE, where primary dispersers were not
|
2090
|
+
| manipulated (Figs. 2 and 3). Activity of seed predators was dramatically reduced in
|
2091
|
+
| the LTEE, and here we observed increases in median seed mass (Fig. 4). This result is
|
2092
|
+
meta | 46 CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
|
2093
|
+
blank |
|
2094
|
+
|
|
2095
|
+
|
|
2096
|
+
text | consistent with larger-seed species experiencing an escape from vertebrate seed
|
2097
|
+
| predation (Dirzo et al., 2007), and lends strong support to the view that changes in
|
2098
|
+
| seed predator abundance are responsible for the increases in median seed mass
|
2099
|
+
| observed in hunted forests relative to protected forests (Wright et al. 2007b).
|
2100
|
+
| Leaf traits showed no differences in both the LTEE and the hunting
|
2101
|
+
| experiment. This suggests that the reduction of vertebrate herbivores by hunting does
|
2102
|
+
| not have a strong impact on changes in seedling community composition at early
|
2103
|
+
| stages of plant recruitment.
|
2104
|
+
| Wood density responses to herbivore reduction differed between the
|
2105
|
+
| LTEE and hunting experiment. The likeliest explanation for the discrepancy is that, as
|
2106
|
+
| with differences in dispersal mode and growth form responses between our
|
2107
|
+
| experiments, differences in wood density responses are dispersal-driven. To test this
|
2108
|
+
| post hoc hypothesis, we evaluated whether dispersal mode classes differ in their mean
|
2109
|
+
| wood densities. Consistent with our hypothesis that experimental differences in wood
|
2110
|
+
| density responses are due to differences in dispersal, wood density was significantly
|
2111
|
+
| lower for species with unhunted dispersal agents than for species having either hunted
|
2112
|
+
| dispersal agents, or a combination of the two (Fig. 6).
|
2113
|
+
| In contrast to the hunting experiment, the LTEE shows higher spiny rat activity
|
2114
|
+
| in the defaunated treatment. As spiny rats are known to be significant seedling
|
2115
|
+
| predators in the absence of other competitors (Asquith et al. 1997), it is also possible
|
2116
|
+
| that they may be compensating for the reduction in other seedling predators inside the
|
2117
|
+
| exclosures. However several lines of evidence contradict this putative explanation.
|
2118
|
+
| First, if spiny rats were compensating for other herbivores inside the exclosure
|
2119
|
+
| as in the study of Asquith et al. (1997), we would expect overall seedling densities to
|
2120
|
+
| be similar in open and exclosure plots, but instead, seedling densities in exclosures are
|
2121
|
+
| about 2-fold higher than in open plots (data not shown). The herbivory study on
|
2122
|
+
| islands which indicated that spiny rats alone can achieve seedling predation rates as
|
2123
|
+
| high as communities with relatively intact mammal fauna were conducted on islands
|
2124
|
+
| in which spiny rat densities are among the highest rodent densities ever documented
|
2125
|
+
| (Adler 1996), but our study does not replicate these high densities. In addition,
|
2126
|
+
meta | 47
|
2127
|
+
blank |
|
2128
|
+
|
|
2129
|
+
|
|
2130
|
+
text | herbivory by spiny rats cannot explain why wood density responses differ between
|
2131
|
+
| experiments, but leaf traits did not.
|
2132
|
+
blank |
|
2133
|
+
|
|
2134
|
+
text | Our evidence for a link between seed dispersal and community wood density is
|
2135
|
+
| an interesting result because Brodie and Gibbs (2009) recently proposed that
|
2136
|
+
| reductions in seed dispersal as a consequence of defaunation may result in shifts in
|
2137
|
+
| mean wood density at the community level. However, the mechanism that they
|
2138
|
+
| proposed assumed that seed mass was positively correlated with wood density across
|
2139
|
+
| species in tropical forests, which is true neither generally, nor for our site specifically
|
2140
|
+
| (Wright et al. 2010). Here we show that dispersal likely mediates changes in
|
2141
|
+
| community wood density distributions via an alternative mechanism, namely that low
|
2142
|
+
| and high wood density plant species are disportionately associated with dispersal
|
2143
|
+
| mode agents that are favored and disfavored respectively by hunting.
|
2144
|
+
blank |
|
2145
|
+
|
|
2146
|
+
text | Implications of defaunation for carbon sequestration in tropical forests.
|
2147
|
+
blank |
|
2148
|
+
|
|
2149
|
+
text | Our results suggest that there may be important links between hunting,
|
2150
|
+
| frugivore abundance, and the ability of future tropical forests to sequester carbon.
|
2151
|
+
| Disruption of seed dispersal by game animals has the potential to alter the ability of
|
2152
|
+
| forests to store carbon by (1) decreasing the abundance of trees relative to lianas
|
2153
|
+
| (Wright et al. 2007b), and (2) shifting wood density distributions in the community
|
2154
|
+
| toward lower wood density species (Fig 5a).
|
2155
|
+
| Higher liana relative abundance may reduce carbon storage at the ecosystem
|
2156
|
+
| level in two ways. Lianas compete with trees for light, displace tree leaf mass (Kira &
|
2157
|
+
| Ogawa 1971), and lower tree growth. One recent study from Amazonia estimated
|
2158
|
+
| that above ground competition from lianas was responsible for reductions in tree
|
2159
|
+
| growth that reduced carbon sequestration by the equivalent of 0.25 Mg C ha-1 yr-1 (van
|
2160
|
+
| der Heijden & Phillips, 2009). Growth of the lianas themselves amounted to 0.07 Mg
|
2161
|
+
| C ha-1 yr-1, which did not compensate for reductions in tree growth. The authors
|
2162
|
+
meta | 48 CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
|
2163
|
+
blank |
|
2164
|
+
|
|
2165
|
+
|
|
2166
|
+
text | therefore estimated that competition from lianas reduced carbon sequestration at the
|
2167
|
+
| ecosystem level by net amount of 0.18 Mg C ha-1 yr-1 or 71%.
|
2168
|
+
| The consequences of lowering community mean wood density for carbon
|
2169
|
+
| storage depend on the relationship between wood density and tree volume in a
|
2170
|
+
| particular forest. Three Panamanian forests in the region, including BCI, exhibit a
|
2171
|
+
| weak, but negative relationship between plot mean wood density and plot biomass
|
2172
|
+
| (Stegen et al. 2009). This suggests that the reduction in community wood density in
|
2173
|
+
| our study site may actually lead to higher forest biomass, and partially compensate for
|
2174
|
+
| any reduction resulting from the relative reduction in free-standing stems. However,
|
2175
|
+
| forests exhibiting positive wood density-biomass relationships could experience a
|
2176
|
+
| decrease in carbon sequestration potential under the same scenario of reduced plot
|
2177
|
+
| wood density.
|
2178
|
+
| The phenomenon of over-hunting in tropical forests is widespread and severe.
|
2179
|
+
| If the changes in carbon storage potential represented by shifting seedling
|
2180
|
+
| communities in this study are as wide-spread as over-hunting itself, the potential
|
2181
|
+
| impact may be great. However, many questions must be answered before we can
|
2182
|
+
| understand the magnitude of the impact that hunting may have on the ability of
|
2183
|
+
| tropical forests to sequester carbon.
|
2184
|
+
| First, to our knowledge, this is the first study demonstrating that tropical tree
|
2185
|
+
| wood densities are associated with dispersal mode classes, and in a way that would
|
2186
|
+
| respond to hunting. Studies investigating the generality of this association would
|
2187
|
+
| represent the first step in predicting whether the changes observed in our site would
|
2188
|
+
| apply pan-tropically. Secondly, here we report changes in the seedling community,
|
2189
|
+
| but better models of forest dynamics are needed to understand the extent to which
|
2190
|
+
| those changes will propagate to the adult community. Third, how lianas alter carbon
|
2191
|
+
| storage at the ecosystem level is poorly understood, and in particular we do not
|
2192
|
+
| understand how liana competition with trees varies as a function of liana abundance.
|
2193
|
+
| Finally, as noted by Stegen et al. (2009), there are many unanswered questions
|
2194
|
+
| pertaining to how changes in wood density distributions translate to changes in
|
2195
|
+
| biomass at the plot level.
|
2196
|
+
meta | 49
|
2197
|
+
blank |
|
2198
|
+
|
|
2199
|
+
|
|
2200
|
+
text | Hunting is not the only cause of defaunation. Frugivores, granivores, and
|
2201
|
+
| herbivores may also decrease in abundance as a result of habitat fragmentation and
|
2202
|
+
| loss (Asquith et al. 1999, Galetti et al. 2006, Terborgh et al. 2006, Cramer et al.
|
2203
|
+
| 2007). As with hunting, decreases in abundance with intensity of habitat loss
|
2204
|
+
| disproportionately affect larger-bodied animals. Therefore, even in the absence of
|
2205
|
+
| hunting, other sources of defaunation may be expected to have similar indirect effects
|
2206
|
+
| on plant community functional trait composition and ecosystem services in tropical
|
2207
|
+
| forests.
|
2208
|
+
blank |
|
2209
|
+
|
|
2210
|
+
title | Acknowledgements
|
2211
|
+
blank |
|
2212
|
+
|
|
2213
|
+
text | We extend our gratitude to the Autoridad Nacional del Ambiente (ANAM) for
|
2214
|
+
| permitting us to conduct research within the Parque Nacional Soberanía. David
|
2215
|
+
| Brassfield, Didimo Ureña, and Joana Balbuena conducted the seedling censuses in the
|
2216
|
+
| hunting experiment. A competitive research grant from the Smithsonian Tropical
|
2217
|
+
| Research Institute funded seedling censuses in hunted and protected forests. The
|
2218
|
+
| Smithsonian Tropical Research Institute, the U.S. Department of Defence Legacy
|
2219
|
+
| Fund, and the U.S. Agency for International Development funded canopy tree
|
2220
|
+
| censuses at hunted and protected forests. NSF grant DEB 9527729 funded the LTEE.
|
2221
|
+
| NSF DEB-0808338, the Theresa Heinz Environmental Scholars program, and the
|
2222
|
+
| STRI short-term fellowship program provided support to E. Kurten.
|
2223
|
+
| 50 CHAPTER 2: CONSEQUENCES OF HUNTING FOR SEED DISPERSAL AND WOOD DENSITY
|
2224
|
+
meta | 51
|
2225
|
+
blank |
|
2226
|
+
|
|
2227
|
+
|
|
2228
|
+
|
|
2229
|
+
title | Chapter 3
|
2230
|
+
blank |
|
2231
|
+
title | Terrestrial mammalian herbivores
|
2232
|
+
| influence the distribution of defense
|
2233
|
+
| and nutrient traits in a Neotropical
|
2234
|
+
| forest
|
2235
|
+
| Erin. L. Kurten, Walter P. Carson
|
2236
|
+
blank |
|
2237
|
+
title | ABSTRACT
|
2238
|
+
blank |
|
2239
|
+
text | Mammalian herbivores are known to be important regulators of plant community
|
2240
|
+
| composition in tropical savannas and temperate systems. However, their impact on
|
2241
|
+
| tropical communities beyond their impact as seedling predators has remained largely
|
2242
|
+
| unexplored, perhaps because of the assumed importance of insect herbivory for
|
2243
|
+
| tropical plants beyond the seedling stage. In this study, we censused 35,069 saplings
|
2244
|
+
| in a long-term terrestrial mammal exclosure experiment in Central Panama to
|
2245
|
+
| determine whether mammalian herbivores had the ability to regulate the abundances
|
2246
|
+
| of species differing in wood density, specific leaf area (SLA), leaf toughness, and leaf
|
2247
|
+
| nitrogen. We found that community mean leaf toughness decreased in exclosures over
|
2248
|
+
| time, while community mean leaf nitrogen increased. These differences were
|
2249
|
+
| primarily due to an increased abundance of species possessing favored traits, rather
|
2250
|
+
| than species turnover as a consequence of herbivore exclusion. No community-level
|
2251
|
+
| differences were observed for mean wood density or specific leaf area. We also found
|
2252
|
+
meta | 52 CHAPTER 3: EFFECTS OF MAMMALIAN HERBIVORES ON SAPLING TRAITS
|
2253
|
+
blank |
|
2254
|
+
|
|
2255
|
+
|
|
2256
|
+
text | that intraspecific leaf toughness was lower in exclosures. Our results suggest that
|
2257
|
+
| mammalian herbivores are important for shaping plant functional trait distributions
|
2258
|
+
| well beyond the seedling stage, and that their effects on the sapling community are
|
2259
|
+
| distinct from their effects on the seedling community.
|
2260
|
+
blank |
|
2261
|
+
|
|
2262
|
+
title | INTRODUCTION
|
2263
|
+
blank |
|
2264
|
+
text | Mammalian herbivores are known to be important top-down regulators of plant
|
2265
|
+
| community composition in many ecosystems (Olff & Ritchie 1998, Parker et al.
|
2266
|
+
| 2006). In tropical forests, mammals are recognized as significant seedling predators
|
2267
|
+
| (Barone and Coley 1996). However their importance as herbivores in later stages of
|
2268
|
+
| plant recruitment has been less studied.
|
2269
|
+
| One study in peninsular Malaysia found that native pigs (Sus scrofa) uproot or
|
2270
|
+
| snap 500 saplings per female pig in their reproductive nest building (Ickes et al. 2001).
|
2271
|
+
| Experimental exclusion of pigs resulted in sapling density increasing by 32 percent,
|
2272
|
+
| relative to open controls in just two years (Ickes et al. 2001). Lizcano (2006) excluded
|
2273
|
+
| large mammalian herbivores, including mountain tapir (Tapirus pinchaque) and
|
2274
|
+
| brocket deer (Mazama spp.), in montane tropical forests in Columbia and discovered a
|
2275
|
+
| 2-fold increase in understory plant biomass in two years.
|
2276
|
+
| These two studies found higher species richness in exclosures, as may be
|
2277
|
+
| expected with higher stem densities, but no differences in species diversity indices.
|
2278
|
+
| The discrepancy between species richness and species diversity indices is explained by
|
2279
|
+
| the fact that species dominance often increases in mammal exclosures as well. The
|
2280
|
+
| positive and negative influences of increased species richness and dominance
|
2281
|
+
| respectively on the diversity index of an exclosure community can cancel each other
|
2282
|
+
| out, leading to the diversity index of an exclosure community being similar to that of a
|
2283
|
+
| control community.
|
2284
|
+
| In other ecosystems, herbivore exclosure not only results in changes in plant
|
2285
|
+
| density and diversity, but also in plant functional trait composition. This is because,
|
2286
|
+
| although mammals are generalist herbivores relative to many insects, they still exhibit
|
2287
|
+
| diet preferences. In one temperate forest, browsers selected species lower in defense
|
2288
|
+
meta | 53
|
2289
|
+
blank |
|
2290
|
+
|
|
2291
|
+
|
|
2292
|
+
text | compounds (e.g. leaf phenolics, condensed tannins, fiber, lignin) (Wardle et al. 2002),
|
2293
|
+
| and in a sub-humid grassland, grazers preferred taller-growing species (Diaz et al.
|
2294
|
+
| 2001).
|
2295
|
+
| However, at the community level, evolutionary history and present day
|
2296
|
+
| intensity of herbivory interact with diet preferences to produce mixed effects on
|
2297
|
+
| functional trait composition. In cases where species have evolved naïve of
|
2298
|
+
| mammalian herbivores, introduced browsers change species composition in favor of
|
2299
|
+
| species with lower average tissue quality (Wardle et al. 2002). The same occurs in
|
2300
|
+
| intensely grazed grasslands (Chaneton et al. 1988). In cases where plant communities
|
2301
|
+
| have evolved with mammalian herbivores, herbivory results in communities of species
|
2302
|
+
| with higher average tissue quality, both in the presence of native herbivores
|
2303
|
+
| (McNaughton 1985), as well as domestic herbivores that are not grazing at intensive
|
2304
|
+
| levels (Cingolani et al. 2002).
|
2305
|
+
| In contrast to other ecosystems, mammals in tropical forests are perceived to
|
2306
|
+
| be relatively unimportant herbivores. Mammals are responsible for about one quarter
|
2307
|
+
| of all herbivory in tropical forests. As generalists, they are perceived to have less of a
|
2308
|
+
| selective influence in shaping plant community composition and plant anti-herbivore
|
2309
|
+
| defense than specialist invertebrate herbivores (Coley and Barone 2003). However,
|
2310
|
+
| tropical forest mammals are important seedling predators. Therefore, the primary aim
|
2311
|
+
| of this study was to test whether mammalian herbivores could indeed have effects on
|
2312
|
+
| plant functional trait composition in tropical forests similar to those seen in temperate
|
2313
|
+
| forests by influencing the composition of the younger cohorts of the plant community.
|
2314
|
+
| We conducted this study in the Barro Colorado National Monument in central
|
2315
|
+
| Panama, where a terrestrial mammal exclosure experiment has been ongoing for the
|
2316
|
+
| past fifteen years (Royo & Carson 2005). We predicted that if mammalian herbivores
|
2317
|
+
| were important for determining sapling functional trait distributions, exclosure would
|
2318
|
+
| favor species that are faster growing (typically species with low wood density and
|
2319
|
+
| high specific leaf area, or SLA), less defended (low leaf toughness) and which have
|
2320
|
+
| higher nutrient leaves (higher leaf nitrogen). Our second goal was to evaluate the
|
2321
|
+
| hypothesis that differences in traits between treatments developed both as a
|
2322
|
+
meta | 54 CHAPTER 3: EFFECTS OF MAMMALIAN HERBIVORES ON SAPLING TRAITS
|
2323
|
+
blank |
|
2324
|
+
|
|
2325
|
+
|
|
2326
|
+
text | consequence of species turnover as well as increases in abundance of favored species
|
2327
|
+
| already common to both treatments.
|
2328
|
+
| A final goal of this study was to examine whether the traits of the species
|
2329
|
+
| themselves changed intraspecifically with mammal exclusion. In temperate systems,
|
2330
|
+
| changes in mammalian herbivory induce changes in photosynthetic rates (Oleksyn et
|
2331
|
+
| al. 1998, Nabeshima et al. 2001), photosynthetic efficiency (Retuerto et al. 2004), leaf
|
2332
|
+
| toughness (Shimazaki & Miyashita 2002). In tropical savanna, megaherbivores
|
2333
|
+
| influence the concentrations of condensed tannins in Acacia (Ward & Young 2002).
|
2334
|
+
| Though herbivory rates in tropical forests are much higher overall in comparison to
|
2335
|
+
| temperate forests (Coley & Barone 1996), suggesting that perhaps constitutive anti-
|
2336
|
+
| herbivore defenses should be ubiquitous. However, several tropical species alter their
|
2337
|
+
| defense in response to herbivory, and it has been suggested that the lack of more
|
2338
|
+
| tropical examples of plasticity in defense are due to lack of study rather than
|
2339
|
+
| biological differences between temperate and tropical plants (Karban & Baldwin
|
2340
|
+
| 1997). We therefore examined whether the defense trait we examined, leaf toughness,
|
2341
|
+
| may decrease intraspecifically in response to mammal exclusion.
|
2342
|
+
blank |
|
2343
|
+
|
|
2344
|
+
title | METHODS
|
2345
|
+
blank |
|
2346
|
+
|
|
2347
|
+
text | Study sites. The forest in Central Panama surrounding Lake Gatun is semi-deciduous
|
2348
|
+
| moist forest. We conducted our experiment on Barro Colorado Island (BCI) and on
|
2349
|
+
| the Gigante Peninsula, within the Barro Colorado National Monument (BCNM). The
|
2350
|
+
| BCI has relatively high abundances of vertebrate herbivores affected by mammal
|
2351
|
+
| exclosure, compared to other Neotropical forests, including deer (Mazama Americana
|
2352
|
+
| and Odocoileus virginianus), collared peccary (Tayassu tajacu), agoutis (Dasyprocta
|
2353
|
+
| punctata), pacas (Agouti paca), rabbits (Silvilagus brasiliensis). This is due to a
|
2354
|
+
| combination of factors, including a lack of resident large felines on the island,
|
2355
|
+
| protection from poaching, and other environmental factors. Tapir (Tapirus bairdii) are
|
2356
|
+
| also present on BCI, but are rare.
|
2357
|
+
meta | 55
|
2358
|
+
blank |
|
2359
|
+
|
|
2360
|
+
|
|
2361
|
+
text | Exclosure experimental design. Between late-1993 and mid-1994, eight pairs of
|
2362
|
+
| fenced, exclosure plots and open, control plots were established within the BCNM
|
2363
|
+
| (Royo & Carson 2005). Four pairs of plots are on (BCI) and the remaining four pairs
|
2364
|
+
| are on the mainland Gigante Penninsula. Fenced and unfenced plots are 30 m x 45 m
|
2365
|
+
| and are approximately 5 m apart. Exclosure fences are constructed of 12.7 x 12.7 cm
|
2366
|
+
| galvanized steel fencing 2.2 m tall and buried 0.25 m deep. A secondary 1.3 x 1.3 cm
|
2367
|
+
| mesh surrounds the lower 70 cm and also extends 0.25 m below ground. A 5-7 m
|
2368
|
+
| buffer zone at the plot edge, and bisecting the plot, allowed for access and the
|
2369
|
+
| avoidance of fence effects. Exclosures excluded the species mentioned above, but did
|
2370
|
+
| not exclude climbing mammals such as squirrels and spiny rats, nor did they exclude
|
2371
|
+
| arboreal mammals such as monkeys (Fig. 2.1). Monitoring data suggest that birds
|
2372
|
+
| were not altered by the exclosures, with the possible exception of tinamous (Fig. 2.1).
|
2373
|
+
| Though tortoises occur on our study site and are likely to be excluded by the fences,
|
2374
|
+
| they are small and rare, and generally not considered to have an effect on our study
|
2375
|
+
| results.
|
2376
|
+
blank |
|
2377
|
+
text | Plant censuses. In 1994 and 2003, all woody juveniles (“saplings”) taller than 40 cm
|
2378
|
+
| or larger than 3 mm diameter at 20 cm in height and not in the buffer zone were
|
2379
|
+
| identified, measured and marked.
|
2380
|
+
blank |
|
2381
|
+
|
|
2382
|
+
text | Plant traits. We sampled leaves from up to six individual saplings of each tree
|
2383
|
+
| species in each of the eight plots occurring on BCI. Specific leaf area was measured
|
2384
|
+
| on shade leaves of saplings as the fresh lamina area divided by the mass of a whole
|
2385
|
+
| leaf with petiole after oven drying to constant mass at 60ºC (Cornelissen et al. 2003).
|
2386
|
+
| Leaf samples were dried at 65ºC, ground using a ball grinder, and analyzed on an
|
2387
|
+
| NA1500 elemental analyzer (Carlo Erba Instruments, Italy) for total N and C. Leaf
|
2388
|
+
| toughness was measured as the force necessary to punch a 3mm diameter hole the leaf
|
2389
|
+
| lamina with a force gauge, avoiding leaf veins to the extent possible (Sagers &Coley
|
2390
|
+
| 1995). Wright and colleagues (2007b) determined dry seed mass and adult tree wood
|
2391
|
+
| specific gravity (2010) for both free standing species and lianas in central Panama.
|
2392
|
+
meta | 56 CHAPTER 3: EFFECTS OF MAMMALIAN HERBIVORES ON SAPLING TRAITS
|
2393
|
+
blank |
|
2394
|
+
|
|
2395
|
+
|
|
2396
|
+
text | Analyses. Trait correlations were conducted to assess whether traits in this study were
|
2397
|
+
| orthogonal to one another, and thus likely to respond independently to herbivory.
|
2398
|
+
| Community mean trait values were calculated in three ways. First, we calculated the
|
2399
|
+
| grand means of the traits at the species level, and used these species means to
|
2400
|
+
| determine the average trait value of the species occurring in each plot. We next
|
2401
|
+
| repeated this analysis, but weighted the species’ trait means by species’ abundances in
|
2402
|
+
| the plots. Finally, we calculated species trait means separately for exclosure and open
|
2403
|
+
| communities, and recalculated the abundance-weighted plot means using these
|
2404
|
+
| treatment-specific species trait values.
|
2405
|
+
| Linear mixed models were used to evaluate whether changes in community
|
2406
|
+
| mean trait values over time differed between treatments. Exclosure and time were
|
2407
|
+
| treated as fixed factors and the exclosure-control pair were treated as a random factor
|
2408
|
+
| nested within time. Our experiment tested for an exclosure-time interaction, and
|
2409
|
+
| significance values reported here refer to that interaction. All analyses were conducted
|
2410
|
+
| in R (R Development Core Team, 2008).
|
2411
|
+
blank |
|
2412
|
+
title | RESULTS
|
2413
|
+
blank |
|
2414
|
+
text | SPECIES TRAITS Functional traits were measured for 38.5-76.4 percent of species in
|
2415
|
+
| the experiment and 58.8-91.6 percent of stems in the experiment (Table 3.1). Traits
|
2416
|
+
| correlations were largely not significant, with the exceptions of SLA-leaf toughness
|
2417
|
+
| and SLA-leaf nitrogen (Table 3.2). However, the correlation coefficients for these two
|
2418
|
+
| relationships were still low (r2 = 0.325 and r2 = 0.231 respectively), and our results did
|
2419
|
+
| not show these trait pairs responding in a coordinated fashion (Fig. 3.1 & 3.2).
|
2420
|
+
meta | 57
|
2421
|
+
blank |
|
2422
|
+
|
|
2423
|
+
text | TABLE 3.1. The number of species and stems for which traits were measured.
|
2424
|
+
blank |
|
2425
|
+
text | No. Spp % Spp No. Stems % Stems
|
2426
|
+
| Total 369 - 35,069 -
|
2427
|
+
| Wood specific gravity 282 76.4 32,113 91.6
|
2428
|
+
| Specific Leaf Area 154 41.7 23,342 66.6
|
2429
|
+
| Leaf Toughness 152 41.2 23,322 66.5
|
2430
|
+
| Leaf Nitrogen 142 38.5 20,633 58.8
|
2431
|
+
blank |
|
2432
|
+
|
|
2433
|
+
text | TABLE 3.2. R2 values for pair-wise correlations between species mean trait
|
2434
|
+
| values evaluated in this study. The sign in parenthesis denotes whether the
|
2435
|
+
| relationship was positive or negative. All correlations are significant (p <
|
2436
|
+
| 0.001).
|
2437
|
+
blank |
|
2438
|
+
text | Wood specific gravity SLA Toughness
|
2439
|
+
| SLA 0.031 (-)
|
2440
|
+
| Toughness 0.004 (-) 0.325 (-)
|
2441
|
+
| Nitrogen 0.11 (-) 0.231 (+) 0.081 (-)
|
2442
|
+
blank |
|
2443
|
+
|
|
2444
|
+
|
|
2445
|
+
|
|
2446
|
+
text | EFFECTS OF SPECIES OCCURRENCE In 1993, approximately 87 percent of species
|
2447
|
+
| occurring in the experiment were present in both treatments. In 2003, 75 percent of
|
2448
|
+
| species occurring in the experiment were present in both treatments. Therefore, when
|
2449
|
+
| we averaged the trait means of the species occurring in each plot, we observed that the
|
2450
|
+
| changes in plot trait means over time did not differ between treatments for any of the
|
2451
|
+
| traits measured (Fig. 3.1).
|
2452
|
+
meta | 58 CHAPTER 3: EFFECTS OF MAMMALIAN HERBIVORES ON SAPLING TRAITS
|
2453
|
+
blank |
|
2454
|
+
|
|
2455
|
+
|
|
2456
|
+
|
|
2457
|
+
text | Wood Specific Gravity (g/cm3)
|
2458
|
+
| 0.60 22
|
2459
|
+
| 1994 2003 1994 2003
|
2460
|
+
blank |
|
2461
|
+
|
|
2462
|
+
|
|
2463
|
+
|
|
2464
|
+
text | Mean SLA (mg/mm2)
|
2465
|
+
| 0.59 21
|
2466
|
+
| 0.58 20
|
2467
|
+
| 0.57 19
|
2468
|
+
| 0.56 18
|
2469
|
+
| 0.55 17
|
2470
|
+
| 0.54 16
|
2471
|
+
| Open Excl Open Excl Open Excl Open Excl
|
2472
|
+
| A Treatment B Treatment
|
2473
|
+
| Mean Leaf Toughness (g/mm2)
|
2474
|
+
blank |
|
2475
|
+
|
|
2476
|
+
|
|
2477
|
+
|
|
2478
|
+
text | 34
|
2479
|
+
| 1994 2003 2.6 1994 2003
|
2480
|
+
| Mean % Leaf Nitrogen
|
2481
|
+
| 33
|
2482
|
+
| 2.4
|
2483
|
+
| 32
|
2484
|
+
| 2.2
|
2485
|
+
| 31
|
2486
|
+
| 2.0
|
2487
|
+
| 30
|
2488
|
+
| 1.8
|
2489
|
+
| 29
|
2490
|
+
| 1.6
|
2491
|
+
| 28
|
2492
|
+
| Open Excl Open Excl Open Excl Open Excl
|
2493
|
+
| C Treatment D Treatment
|
2494
|
+
blank |
|
2495
|
+
text | FIGURE 3.1. Changes in plot-level trait means, not weighted by species
|
2496
|
+
| abundance, did not differ significantly between treatments for (A) wood
|
2497
|
+
| density, (B) SLA, (C) leaf toughness or (D) leaf nitrogen.
|
2498
|
+
blank |
|
2499
|
+
text | EFFECTS OF SPECIES ABUNDANCE Stem densities increased by 46% in exclosures
|
2500
|
+
| from 1994 to 2003, but did not increase in open plots (data not shown). When we
|
2501
|
+
| averaged the trait means of the species occurring in each plot, and weighted traits by
|
2502
|
+
| species abundance, we did observe differences between treatments for some traits.
|
2503
|
+
| We predicted that exclosures would favor species with lower wood density, lower
|
2504
|
+
| SLA, lower leaf toughness, and higher leaf nitrogen. We did not see significant
|
2505
|
+
| differences between treatments in wood density (Fig. 3.2A) or SLA (Fig. 3.2B).
|
2506
|
+
| However, changes in leaf toughness (Fig. 3.2C) and leaf nitrogen (Fig. 3.D) over time
|
2507
|
+
| were significantly different between treatments. Consistent with our expectations,
|
2508
|
+
| exclosures had lower community mean leaf toughness and higher community mean
|
2509
|
+
meta | 59
|
2510
|
+
blank |
|
2511
|
+
|
|
2512
|
+
|
|
2513
|
+
text | leaf nitrogen in 2003, relative to open plots. However these differences did not exist
|
2514
|
+
| when the experiment was initiated in 1994 (Fig. 3.2 C & D).
|
2515
|
+
blank |
|
2516
|
+
|
|
2517
|
+
|
|
2518
|
+
text | Wood Specific Gravity (g/cm3)
|
2519
|
+
| 0.60 24
|
2520
|
+
| 1994 2003 1994 2003
|
2521
|
+
blank |
|
2522
|
+
|
|
2523
|
+
|
|
2524
|
+
|
|
2525
|
+
text | Mean SLA (mg/mm2)
|
2526
|
+
| 0.59 22
|
2527
|
+
| 0.58 20
|
2528
|
+
| 0.57 18
|
2529
|
+
| 0.56 16
|
2530
|
+
| 0.55 14
|
2531
|
+
| 0.54 12
|
2532
|
+
| Open Excl Open Excl Open Excl Open Excl
|
2533
|
+
| A Treatment B Treatment
|
2534
|
+
| Mean Leaf Toughness (g/mm3)
|
2535
|
+
blank |
|
2536
|
+
|
|
2537
|
+
|
|
2538
|
+
|
|
2539
|
+
text | 38 2.6
|
2540
|
+
| 1994 2003 Mean % Leaf Nitrogen 1994 2003
|
2541
|
+
| 36 2.4
|
2542
|
+
| * *
|
2543
|
+
| 34 2.2
|
2544
|
+
| 32 2.0
|
2545
|
+
| 30 1.8
|
2546
|
+
blank |
|
2547
|
+
text | 28 1.6
|
2548
|
+
blank |
|
2549
|
+
text | 26 1.4
|
2550
|
+
| Open Excl Open Excl Open Excl Open Excl
|
2551
|
+
| C Treatment D Treatment
|
2552
|
+
blank |
|
2553
|
+
|
|
2554
|
+
text | FIGURE 3.2. Changes in abundance-weighted, plot-level trait means did not
|
2555
|
+
| differ significantly between treatments for (A) wood density or (B) SLA, but
|
2556
|
+
| did differ significantly between treatments for (C) leaf toughness and (D) leaf
|
2557
|
+
| nitrogen. (* p = 0.06 , time x treatment interaction)
|
2558
|
+
blank |
|
2559
|
+
|
|
2560
|
+
text | INTRASPECIFIC DIFFERENCES IN LEAF TRAITS Because we sampled leaf traits in both
|
2561
|
+
| open and exclosure plots, we could examine how intraspecific differences in trait
|
2562
|
+
| means contributed to the differences between treatments at the community level. For
|
2563
|
+
| one trait, leaf toughness, we found that determining species trait means separately for
|
2564
|
+
| open and exclosure treatments, and using those treatment-specific species trait means
|
2565
|
+
| to calculate plot-level means, resulted in an enhanced difference between treatments at
|
2566
|
+
meta | 60 CHAPTER 3: EFFECTS OF MAMMALIAN HERBIVORES ON SAPLING TRAITS
|
2567
|
+
blank |
|
2568
|
+
|
|
2569
|
+
|
|
2570
|
+
text | the plot-level in the later time point (Fig. 3.3), relative to using grand trait means for
|
2571
|
+
| species (Fig. 3.2C).
|
2572
|
+
blank |
|
2573
|
+
text | 38
|
2574
|
+
blank |
|
2575
|
+
|
|
2576
|
+
|
|
2577
|
+
text | Mean Leaf Toughness (g/mm2)
|
2578
|
+
| 1994 2003
|
2579
|
+
| 36
|
2580
|
+
| 34 *
|
2581
|
+
| 32
|
2582
|
+
| 30
|
2583
|
+
| 28
|
2584
|
+
| 26
|
2585
|
+
| Open Excl Open Excl
|
2586
|
+
| Treatment
|
2587
|
+
blank |
|
2588
|
+
text | FIGURE 3.3. Intraspecific differences in species’ mean leaf toughness between
|
2589
|
+
| open and exclosure plots increase the difference in treatment-level mean leaf
|
2590
|
+
| toughness in 2003. (* p = 0.004, time x treatment interaction)
|
2591
|
+
blank |
|
2592
|
+
text | For species having at least two leaf samples from each treatment type, 61.8%
|
2593
|
+
| of species had lower leaf toughnesses in exclosures relative to controls (binomial test,
|
2594
|
+
| N = 76, p = 0.025). This bias was even stronger when the sample was limited to
|
2595
|
+
| species with treatment mean toughnesses based on at least eight leaf samples, with
|
2596
|
+
| 73.9% of species having lower leaf toughnesses in exclosures (binomial test, N = 23,
|
2597
|
+
| p = 0.017).
|
2598
|
+
| Because sample sizes among species and between treatments was unbalanced,
|
2599
|
+
| a MANOVA approach could not be taken to assess whether treatment means within a
|
2600
|
+
| species were significantly different. Therefore, using the latter subset of species
|
2601
|
+
| above, a two-way ANOVA was applied. The association of exclosure treatment with
|
2602
|
+
| lower mean leaf toughness with species was also significant using this approach
|
2603
|
+
| (Table 3.3).
|
2604
|
+
meta | 61
|
2605
|
+
blank |
|
2606
|
+
|
|
2607
|
+
|
|
2608
|
+
text | TABLE 3.3. Effect of species and exclosure on variation in leaf
|
2609
|
+
| toughness. N = 23 species, each of which had at least eight leaf
|
2610
|
+
| toughness samples from each of the two treatment types.
|
2611
|
+
blank |
|
2612
|
+
text | Effect df SS MS F p
|
2613
|
+
| Species 22 207.4 9.425 165.2 < 0.001
|
2614
|
+
| Exclosure 1 0.305 0.305 5.352 0.021
|
2615
|
+
| Species x Exclosure 22 1.292 0.059 1.029 0.425
|
2616
|
+
| Residuals 604 34.467 0.057
|
2617
|
+
blank |
|
2618
|
+
|
|
2619
|
+
|
|
2620
|
+
title | DISCUSSION
|
2621
|
+
blank |
|
2622
|
+
text | Regulation of plant functional trait composition by mammalian herbivores
|
2623
|
+
| In this study, we demonstrate that terrestrial mammals influence understory functional
|
2624
|
+
| trait distributions in tropical forests. They do so primarily by suppressing populations
|
2625
|
+
| of species with traits that are correlated with high nutrition and low defense.
|
2626
|
+
| Consistent with our predictions that reduced herbivory should favor species with low
|
2627
|
+
| defense and high nutrient content, community mean leaf toughness decreased over
|
2628
|
+
| time in exclosures over time (Fig. 3.2C), and community mean leaf nitrogen increased
|
2629
|
+
| in exclosures over time (Fig 3.2D), while open control plots did not show equivalent
|
2630
|
+
| changes.
|
2631
|
+
| Wood density is associated with seedling survival in the presence of herbivores
|
2632
|
+
| in this forest (Alvarez-Claire & Kitajima 2007, 2009). Browsers and grazers have also
|
2633
|
+
| been shown to select species with higher SLA in other systems (Wardle et al. 2002,
|
2634
|
+
| Cingolani et al. 2002). However, neither of these traits changed in response to
|
2635
|
+
| mammal exclosure. This could be because, at the sapling stage in tropical forests, the
|
2636
|
+
| low light conditions of the forest understory also favor low SLA, high wood density
|
2637
|
+
| species and perhaps this environmental factor constrains the community response to
|
2638
|
+
| herbivory with respect to those traits.
|
2639
|
+
| We did not find that changes in functional traits at the community-level were
|
2640
|
+
| the result of divergences in species presence-absence between exclosure and open
|
2641
|
+
| plots. The sapling community established prior to the imposition of the exclosure
|
2642
|
+
| treatments, and therefore two treatments started out with very similar communities.
|
2643
|
+
meta | 62 CHAPTER 3: EFFECTS OF MAMMALIAN HERBIVORES ON SAPLING TRAITS
|
2644
|
+
blank |
|
2645
|
+
|
|
2646
|
+
|
|
2647
|
+
text | Over longer time scales, competitively dominant species may outcompete less
|
2648
|
+
| competitive species in the exclosure treatment, resulting in lower species richness,
|
2649
|
+
| particularly of species which are better defended but slower growing. However, we
|
2650
|
+
| did not observe decreases in species richness in the time-frame of this experiment
|
2651
|
+
| (data not shown).
|
2652
|
+
| Seed and seedling predators are also excluded from the exclosure communities.
|
2653
|
+
| Therefore, it is reasonable to question whether the effects we observed are due
|
2654
|
+
| exclusively to herbivore exclusion. Two lines of evidence allow us to attribute our
|
2655
|
+
| results to herbivores. First, long-term studies of seedling growth in central Panama
|
2656
|
+
| suggest that all individuals in this size class established before the experimental
|
2657
|
+
| treatments were imposed (S.J. Wright, pers. comm.). Therefore, saplings in both
|
2658
|
+
| treatments should have been exposed to the same seed and seedling predation agents.
|
2659
|
+
| Consistent with the assumption that saplings established prior to exclusion of
|
2660
|
+
| seed and seedling predators, community mean seed mass does not differ between
|
2661
|
+
| treatments for the sapling community (data not shown). This is in contrast to the
|
2662
|
+
| seedlings in the exclosure communities, which did establish under conditions of seed
|
2663
|
+
| and seedling predator exclusion, and as a result have higher community mean seed
|
2664
|
+
| mass than seedlings in open control communities (Fig. 2.4).
|
2665
|
+
| These two lines of evidence suggest that exclusion of seed and seedling
|
2666
|
+
| predators are not responsible for the exclosure effects observed in the sapling
|
2667
|
+
| community, leaving only herbivory as a possible explanation.
|
2668
|
+
blank |
|
2669
|
+
|
|
2670
|
+
title | Intraspecific differences in leaf toughness
|
2671
|
+
text | The majority of species in the experiment showed lower mean leaf toughness inside
|
2672
|
+
| the exclosure, relative to open plots. When these intraspecific differences in species
|
2673
|
+
| leaf toughness were accounted for (Fig. 3.3), treatment differences in plot level leaf
|
2674
|
+
| toughness in 2003 were 66 percent larger than when a grand mean for the species leaf
|
2675
|
+
| toughness was applied (Fig. 3.2C). This result suggests that in the case of leaf
|
2676
|
+
| toughness, the trait values measured for juvenile tropical plants may vary with the
|
2677
|
+
| degree of herbivory experienced.
|
2678
|
+
meta | 63
|
2679
|
+
blank |
|
2680
|
+
|
|
2681
|
+
|
|
2682
|
+
text | There are several possible explanations for the intraspecific divergence in leaf
|
2683
|
+
| toughness. First, it is possible that, within species, genotype or environment produces
|
2684
|
+
| variation in leaf toughness, and individuals with lower leaf toughness survive at a
|
2685
|
+
| lower rate in open plots than in exclosures . Support for this mechanism can be found
|
2686
|
+
| in studies of insect herbivory on plant genotypes which differ in their expression of
|
2687
|
+
| qualitative defense traits (Kessler & Baldwin, 2001, Silfer et al. 2009).
|
2688
|
+
| An alternative explanation is that plants are relaxing their investment in
|
2689
|
+
| mechanical defenses when they no longer experience mammalian herbivory.
|
2690
|
+
| Hundreds of plant species are known to increase investment in defense when exposed
|
2691
|
+
| to herbivory, and subsequently attenuate that defense when herbivory levels are lower
|
2692
|
+
| (Karban & Baldwin 1997). However few studies have documented reduced
|
2693
|
+
| investment in defense upon reduction of mammalian herbivory. In Acacia
|
2694
|
+
| drepanolobium decreases in spine length or spinescence are detectable after 22 months
|
2695
|
+
| (Young & Okello 1998), decreases in condensed tannin concentrations are detectable
|
2696
|
+
| after 24-36 months (Ward & Young 2002) and reduced investment in indirect defenses
|
2697
|
+
| occur within several years (Huntzinger et al. 2004).
|
2698
|
+
| Regardless of the mechanism, the fact that mammalian herbivores may play a
|
2699
|
+
| role in altering leaf toughness intraspecifically in tropical plants is unexpected. Insects
|
2700
|
+
| are thought to be responsible for three quarters of herbivory in tropical forests, and
|
2701
|
+
| also the source of the strongest selection pressures plants receive to develop anti-
|
2702
|
+
| herbivore defenses in this system (Barone & Coley 2002). The experimental plots in
|
2703
|
+
| which we measured leaf toughness did not manipulate insects, and it is plausible that
|
2704
|
+
| plants in both treatments could have experience high rates of invertebrate herbivory,
|
2705
|
+
| and therefore shown no attenuation in defense traits. Yet, it appears that insect
|
2706
|
+
| herbivores could not compensate for mammalian herbivores in maintaining high
|
2707
|
+
| intraspecific leaf toughness when mammals were excluded.
|
2708
|
+
blank |
|
2709
|
+
|
|
2710
|
+
title | Implications for tropical defaunation
|
2711
|
+
text | In many temperate forests, populations of native or introduced large
|
2712
|
+
| mammalian herbivores are not regulated in a top-down fashion by predators. As a
|
2713
|
+
meta | 64 CHAPTER 3: EFFECTS OF MAMMALIAN HERBIVORES ON SAPLING TRAITS
|
2714
|
+
blank |
|
2715
|
+
|
|
2716
|
+
|
|
2717
|
+
text | result, these communities currently experience intense levels of herbivory, low rates of
|
2718
|
+
| plant recruitment and often decreases in species richness and diversity (Wardle et al.
|
2719
|
+
| 2002, Rooney 2001). However, tropical forests are undergoing the opposite
|
2720
|
+
| perturbation. Throughout the tropics, mammalian herbivores are being unsustainably
|
2721
|
+
| hunted (Peres & Palacios 2007, Corlett 2007, Fa & Brown 2009). Preferred game
|
2722
|
+
| species of animals are often large-bodied herbivores, such as elephants, tapir, pigs,
|
2723
|
+
| peccaries and deer.
|
2724
|
+
| Understanding how and why such perturbations in herbivore abundance alter
|
2725
|
+
| plant species diversity and functional composition will help conservation biologists
|
2726
|
+
| identify potential interventions to conserve plant species threatened indirectly by
|
2727
|
+
| defaunation. However, because most studies examining changes in functional
|
2728
|
+
| diversity have been conducted in temperate forests, where the perturbation
|
2729
|
+
| experienced by plant communities is increased rates of herbivory, little empirical data
|
2730
|
+
| exists with which to evaluate how tropical forests may respond to decreased rates of
|
2731
|
+
| herbivory by native herbivores as a consequence of defaunation.
|
2732
|
+
| The biomass of terrestrial mammalian herbivores in tropical forests is quite
|
2733
|
+
| low, relative to other ecosystems (Bodmer 1989, Leigh et al. 1982). In addition,
|
2734
|
+
| insects are thought to account for approximately 75 percent of overall herbivory in
|
2735
|
+
| tropical forests. Taken together, these data might suggest that observed reductions in
|
2736
|
+
| terrestrial mammalian herbivore populations in tropical forests may not have large
|
2737
|
+
| impacts on sapling community composition. However, this study demonstrates
|
2738
|
+
| reduced herbivory as a consequence of tropical defaunation is likely to cause an
|
2739
|
+
| increase in dominance of sapling species with higher leaf nitrogen and lower leaf
|
2740
|
+
| toughness. Leaves with higher leaf nitrogen and lower concentrations of defense
|
2741
|
+
| compounds typically have higher decomposition rates. Therefore, it is conceivable
|
2742
|
+
| that if changes in the sapling community propagate to alter canopy composition,
|
2743
|
+
| defaunation may alter nutrient cycling in tropical forests.
|
2744
|
+
meta | 65
|
2745
|
+
blank |
|
2746
|
+
|
|
2747
|
+
|
|
2748
|
+
title | ACKNOWLEDGEMENTS
|
2749
|
+
blank |
|
2750
|
+
text | D. Ackerly, L. Curran, R. Dirzo and P. Vitousek provided constructive criticism which
|
2751
|
+
| improved this work. The Smithsonian Tropical Research Institute granted permission
|
2752
|
+
| to conduct this work, and provided logistical support. D. Turner provided assistance
|
2753
|
+
| with leaf nitrogen analysis. J. Wright provided seed mass and wood density data.
|
2754
|
+
| Many thanks go to L. Jimenez, C. Sarmiento, S. Rebellon, A. Calderón, R.
|
2755
|
+
| Bethancourt for help in the field and lab. A. Hernandez and O. Valdes provided
|
2756
|
+
| indispensible help with species identification. NSF DEB-0808338, the Theresa Heinz
|
2757
|
+
| Environmental Scholars program, and the STRI short-term fellowship program
|
2758
|
+
| provided support to E. Kurten.
|
2759
|
+
| 66 CHAPTER 3: EFFECTS OF MAMMALIAN HERBIVORES ON SAPLING TRAITS
|
2760
|
+
meta | 67
|
2761
|
+
blank |
|
2762
|
+
|
|
2763
|
+
|
|
2764
|
+
|
|
2765
|
+
title | Chapter 4
|
2766
|
+
blank |
|
2767
|
+
text | Hunting does not alter seed
|
2768
|
+
| predation rates as a function of seed
|
2769
|
+
| size in a Neotropical forest
|
2770
|
+
| Erin L. Kurten
|
2771
|
+
blank |
|
2772
|
+
title | ABSTRACT
|
2773
|
+
blank |
|
2774
|
+
text | This study tested the hypothesis that vertebrate seed predation rates vary with seed
|
2775
|
+
| size and with hunting intensity in tropical forests, corresponding to direct impacts of
|
2776
|
+
| hunting on vertebrate species of differing size classes. Seed fate of seeds from species
|
2777
|
+
| with mean fresh seed masses ranging from 0.002 to 62.4 g was compared between a
|
2778
|
+
| protected and nearby hunted forest in central Panama. Transect survey data verified
|
2779
|
+
| that higher hunting intensity corresponded with lower abundances of key mammalian
|
2780
|
+
| seed predators. Seed arrays of a subset of species were monitored with camera traps
|
2781
|
+
| to verify the identities of animals responsible for seed removal. In this system, there
|
2782
|
+
| was only weak support for a relationship between seed predation rates and seed size,
|
2783
|
+
| and no evidence that this relationship changed at high hunting intensity. There was
|
2784
|
+
| also no evidence that seed predator body size varied with seed size, as agoutis
|
2785
|
+
| (Dasyprocta punctata) were responsible for most of the verified removal for five plant
|
2786
|
+
| species examined, ranging from 1.95 to 62.4 g in fresh seed mass.
|
2787
|
+
meta | 68 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
2788
|
+
blank |
|
2789
|
+
|
|
2790
|
+
|
|
2791
|
+
title | INTRODUCTION
|
2792
|
+
blank |
|
2793
|
+
text | Overharvesting of bushmeat is a pervasive threat to biodiversity across the tropics (Fa
|
2794
|
+
| & Peres 2001, Peres & Palacios 2007, Corlett 2007). This defaunation not only
|
2795
|
+
| directly lowers vertebrate abundance in hunted forests, but initiates trophic cascades
|
2796
|
+
| which perturb the plant, insect, and pathogen communities as well. Preferred game
|
2797
|
+
| species of animals are usually large-bodied vertebrates, such as ateline monkeys, tapir,
|
2798
|
+
| peccary and deer, as well as large birds, and in some cases reptiles, in the context of
|
2799
|
+
| Neotropical forests. Understanding how and why such cascading perturbations alter
|
2800
|
+
| species diversity and functional composition in the plant community is important for
|
2801
|
+
| understanding the role mammals play in maintaining the diversity of tropical forests,
|
2802
|
+
| as well as identify potential interventions to conserve plant species threatened by the
|
2803
|
+
| negative indirect effects of defaunation.
|
2804
|
+
| Several studies have documented reduced seed dispersal as a consequence of
|
2805
|
+
| hunting in tropical forests, particularly for larger-seed species (e.g. Wright et al. 2000,
|
2806
|
+
| Guariguata et al. 2000, Guariguata et al. 2002, Galetti et al. 2006, Wang et al. 2007,
|
2807
|
+
| Brodie et al. 2009, Fadini et al. 2009, Holbrook & Loiselle 2009). These studies
|
2808
|
+
| suggest that reduced dispersal should result in reduced recruitment of large-seeded
|
2809
|
+
| species, in particular those that rely on large-bodied mammals vulnerable to hunting
|
2810
|
+
| for their seed dispersal (Peres & van Roosmalen 2002, Nuñez-Iturri et al. 2008,
|
2811
|
+
| Terborgh et al. 2008).
|
2812
|
+
| However, in most cases, reduced dispersal due to hunting has not been
|
2813
|
+
| explicitly linked to subsequent reductions in seedling recruitment. While one study
|
2814
|
+
| modeled the potential reduction in seedling recruitment, based on estimates of reduced
|
2815
|
+
| dispersal to and differential survival in different microhabitats (Brodie et al. 2009),
|
2816
|
+
| only one set of studies of which I am aware measured seed dispersal, seed predation,
|
2817
|
+
| and seedling recruitment for the same species in both protected and hunted sites
|
2818
|
+
| (Wright et al. 2000, Wright & Duber 2001). Wright and colleagues (2000, 2001)
|
2819
|
+
| focused on two large-seeded palm species, members of genera which are widespread
|
2820
|
+
| in the Neotropics. They found seed dispersal to be indeed reduced, and seedling
|
2821
|
+
| densities near parent trees to be higher, as one would predict to be associated with
|
2822
|
+
meta | 69
|
2823
|
+
blank |
|
2824
|
+
|
|
2825
|
+
|
|
2826
|
+
text | hunting. However, contrary to what has been hypothesized in the seed dispersal
|
2827
|
+
| literature, recruitment of Attalea and Astrocaryum palms was actually higher in the
|
2828
|
+
| hunted sites (Wright et al. 2000, 20001). The reason for this unexpected increase in
|
2829
|
+
| recruitment was that hunting reduced the intensity of vertebrate seed predation, and
|
2830
|
+
| this reduction was not fully compensated for by invertebrates. (Cramer et al. 2003)
|
2831
|
+
| suggested a similar reduction in seed predation was responsible for higher recruitment
|
2832
|
+
| of the African species Balanites wilsoniana in defaunated sites, despite lower dispersal
|
2833
|
+
| by elephants, however seed predation rates were never measured (Babweteera et al.
|
2834
|
+
| 2007).
|
2835
|
+
| It is clear from this example that a better understanding of the consequences of
|
2836
|
+
| hunting for seed predation is necessary for providing context to the studies
|
2837
|
+
| documenting reduced seed dispersal. In studies which have measured seed predation
|
2838
|
+
| in sites with differing intensities of hunting, rates of vertebrate seed predation have
|
2839
|
+
| often been lower in hunted sites (Terborgh & Wright 1994, Wright et al. 2000, Wright
|
2840
|
+
| & Duber 2001, Guariguata 2000, Beckman & Muller-Landau 2007, but see Roldán &
|
2841
|
+
| Simonetti 2001).
|
2842
|
+
| Even less clear is how perturbations in seed predation rates as a consequence
|
2843
|
+
| of hunting may vary with seed size. Because larger-seeded species are expected to
|
2844
|
+
| disproportionately experience reduced seed dispersal, understanding how seed
|
2845
|
+
| predation changes with hunting across a range of seed sizes is important for
|
2846
|
+
| understanding whether or not the potentially negative demographic consequences of
|
2847
|
+
| reduced seed dispersal of larger-seeded species is intensified, maintained, or
|
2848
|
+
| compensated for by alterations in seed predation across species (Stoner et al. 2007).
|
2849
|
+
| However, most studies which have measured seed predation rates under various
|
2850
|
+
| hunting regimes have focused on one or two plant species (e.g. Terborgh & Wright
|
2851
|
+
| 1994, Wright et al. 2000, Roldán & Simonetti 2001, Wright & Duber 2001, Galetti et
|
2852
|
+
| al. 2006, Beckman & Muller-Landau 2007, Donatti et al. 2009). Due to the variation
|
2853
|
+
| in location, mammal community composition, and degree of defaunation in the sites
|
2854
|
+
| studied, these data cannot be directly compared to assess how seed predation rates
|
2855
|
+
| change with defaunation intensity as a function of seed size. Guariguata and
|
2856
|
+
meta | 70 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
2857
|
+
blank |
|
2858
|
+
|
|
2859
|
+
|
|
2860
|
+
text | colleagues (2000) measured seed predation rates of seven species, but focused
|
2861
|
+
| primarily on small-seeded timber species. .
|
2862
|
+
| In 2007, Dirzo and colleagues published a model of how vertebrate seed
|
2863
|
+
| predation could be expected to vary with seed size and intensity of vertebrate
|
2864
|
+
| defaunation in tropical forests (Fig. 4.1). At low levels of hunting, vulnerable, large-
|
2865
|
+
| bodied animals drastically decrease in abundance or become locally extirpated. In
|
2866
|
+
| response to this competitive release, as well as a likely reduction in predation by
|
2867
|
+
| felines, medium-sized seed predators initially become more abundant, until they
|
2868
|
+
| become the primary game species at moderate levels of hunting. At the highest
|
2869
|
+
| intensities of defaunation, even medium-sized seed predators have become rare. Small
|
2870
|
+
| rodents increase steadily with increasing hunting intensity, as they experience a
|
2871
|
+
| reduction in competition and predation.
|
2872
|
+
| In this model, predation intensity of larger-seeded species mirrors the changes
|
2873
|
+
| in abundance of medium-bodied seed predators (e.g. 4-20 kg body mass in
|
2874
|
+
| Neotropical communities), while predation of smaller-seeded species increases as
|
2875
|
+
| small bodied seed predator (< 1 kg) biomass increases. As a result, the relative
|
2876
|
+
| proportion of larger and smaller seeds comprising the seedling bank is expected to
|
2877
|
+
| shift as defaunation intensity increases. This model was important for clarifying how
|
2878
|
+
| seed predation is likely to vary by seed-size, and how this relationship is dependent
|
2879
|
+
| upon the defaunation context.
|
2880
|
+
meta | 71
|
2881
|
+
blank |
|
2882
|
+
|
|
2883
|
+
text | Large vertebrates
|
2884
|
+
| A
|
2885
|
+
blank |
|
2886
|
+
|
|
2887
|
+
text | Seed predator Biomass
|
2888
|
+
| Mid-sized vertbrates
|
2889
|
+
| Small rodents
|
2890
|
+
blank |
|
2891
|
+
text | BCI
|
2892
|
+
| PNS
|
2893
|
+
| C No Def.
|
2894
|
+
blank |
|
2895
|
+
|
|
2896
|
+
|
|
2897
|
+
|
|
2898
|
+
text | Seed predation Intensity
|
2899
|
+
| High Def.
|
2900
|
+
blank |
|
2901
|
+
|
|
2902
|
+
|
|
2903
|
+
|
|
2904
|
+
text | B Large Seeds
|
2905
|
+
| Seed predation Intensity
|
2906
|
+
blank |
|
2907
|
+
|
|
2908
|
+
text | Small Seeds
|
2909
|
+
blank |
|
2910
|
+
|
|
2911
|
+
|
|
2912
|
+
|
|
2913
|
+
text | Small La rge
|
2914
|
+
| Seed Size
|
2915
|
+
blank |
|
2916
|
+
|
|
2917
|
+
|
|
2918
|
+
text | None Moderate High
|
2919
|
+
| Defaunation Intensity
|
2920
|
+
| FIGURE 4.1. Model of how seed predation should vary with seed
|
2921
|
+
| mass as a function of defaunation intensity in a Neotropical forest
|
2922
|
+
| (modified from Dirzo et al. 2007). (A) Changes in large, medium and
|
2923
|
+
| small vertebrate seed predator abundance with increasing defaunation
|
2924
|
+
| intensity. The approximate positions of BCI and PNS along the
|
2925
|
+
| defaunation gradient shown here are based on mammal transect
|
2926
|
+
| surveys. (B) Seed predation intensity of large and small seeded species
|
2927
|
+
| on a biomass basis is correlated with the abundance of medium- and
|
2928
|
+
| small-bodied seed predators respectively. (C) As defaunation
|
2929
|
+
| intensifies, the relationship between seed predation rates and seed size
|
2930
|
+
| goes from positive to negative.
|
2931
|
+
blank |
|
2932
|
+
text | With this study, I aimed to test several assumptions and hypotheses inherent in
|
2933
|
+
| this model. The first assumption I tested was that larger-seeded species experience
|
2934
|
+
| higher seed predation intensity than smaller seeded species at all but the highest levels
|
2935
|
+
| of defaunation intensity. The second assumption of the model I tested was that larger-
|
2936
|
+
| seeded species tend to be consumed by large- and medium-bodied vertebrates.
|
2937
|
+
| Likewise, smaller-seeded species tend to be consumed by smaller-bodied vertebrates.
|
2938
|
+
| A third hypothesis implicit in the model is that at high levels of defaunation intensity,
|
2939
|
+
| where the number of large- and medium-bodied vertebrates is highly reduced, larger-
|
2940
|
+
| seeded species experience reduced seed predation, relative to less defaunated sites. A
|
2941
|
+
meta | 72 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
2942
|
+
blank |
|
2943
|
+
|
|
2944
|
+
|
|
2945
|
+
text | fourth prediction of the model is that smaller-seeded species experience increased seed
|
2946
|
+
| predation as defaunation intensity increases, as populations of small bodied vertebrates
|
2947
|
+
| increase in response to competitive release and reduced predation. There is a great
|
2948
|
+
| interest in determining the extent to which other vertebrates or natural enemies can
|
2949
|
+
| compensate for the loss of a primary seed predator.
|
2950
|
+
| To test these hypotheses, seeds of 13 species spanning the range of 0.002 to
|
2951
|
+
| 64.2 g mean fresh seed mass were monitored in arrays in both a protected forest and a
|
2952
|
+
| nearby hunted forest. Fate of seeds was monitored for four weeks. To examine
|
2953
|
+
| whether larger- and smaller-seeded species indeed had larger- and smaller-bodied
|
2954
|
+
| seed predators respectively, the seed arrays on BCI were monitored with camera traps
|
2955
|
+
| for five species ranging from 1.95 to 64.2 g fresh mean seed mass for one week, and
|
2956
|
+
| the the agents of seed removal were recorded.
|
2957
|
+
| To assess whether other vertebrates might compensate for the loss of a
|
2958
|
+
| principle seed predator, I monitored two large-seeded palm species with camera traps
|
2959
|
+
| in both sites. This allowed me to determine if and how the species of vertebrate seed
|
2960
|
+
| disperser differed between the protected and hunted sites, in particular if smaller
|
2961
|
+
| vertebrates compensated for the removal of larger vertebrates. I also recorded the
|
2962
|
+
| source of mortality for all species when seeds were killed by invertebrates and
|
2963
|
+
| pathogens, to examine whether those agents could also compensate for the loss of
|
2964
|
+
| larger bodied seed predators.
|
2965
|
+
blank |
|
2966
|
+
|
|
2967
|
+
title | METHODS
|
2968
|
+
blank |
|
2969
|
+
|
|
2970
|
+
text | Study sites. The forest in Central Panama surrounding Lake Gatun is semi-deciduous
|
2971
|
+
| moist forest. I examined the effects of defaunation by hunting by comparing protected
|
2972
|
+
| and hunted forests in this area (Fig. 4.2). Barro Colorado Island (BCI) was chosen as
|
2973
|
+
| the protected forest site, and could be regarded as a moderately defaunated site. Due
|
2974
|
+
| to its size (15 km2), the island no longer supports white-lipped peccary, and has
|
2975
|
+
| visiting, rather than resident, jaguar (Panthera onca) and puma (Puma concolor).
|
2976
|
+
| Other large mammals, such as tapir (Tapirus bairdii) and spider monkeys (Ateles
|
2977
|
+
meta | 73
|
2978
|
+
blank |
|
2979
|
+
|
|
2980
|
+
|
|
2981
|
+
text | geoffroyi), were locally extirpated and historically reintroduced (Enders 1939,
|
2982
|
+
| Terwilliger 1978, Milton & Hopkins 2005). However today, activity of poachers is
|
2983
|
+
| virtually nonexistent on BCI due to the monitoring by forest guards and Panamanian
|
2984
|
+
| police. The last confirmed incident of poaching on BCI occurred in 1989 (Wright et
|
2985
|
+
| al. 2007). Consistent with an absence of poachers, researchers on BCI do not
|
2986
|
+
| encounter evidence of hunting, and wildlife is common to see.
|
2987
|
+
| Adjacent to the Barro Colorado National Monument (BCNM) is the Parque
|
2988
|
+
| Nacional Soberanía (PNS). PNS is a protected area, however the region of the park in
|
2989
|
+
| which the study was conducted is not actively patrolled. This is due to both fewer
|
2990
|
+
| forest guards at the park, a lack of vehicles to access the study area, which is more
|
2991
|
+
| than 20 km from the park headquarters. Consistent with a lack of protection, various
|
2992
|
+
| evidence of hunting activity was encountered while conducting this study, including
|
2993
|
+
| spent shells, campfires, litter, gun shots, hunting dogs, experimental vandalism, and in
|
2994
|
+
| one case, encountering a hunting party.
|
2995
|
+
blank |
|
2996
|
+
|
|
2997
|
+
|
|
2998
|
+
text | BCNM
|
2999
|
+
| PNS
|
3000
|
+
| trails
|
3001
|
+
blank |
|
3002
|
+
|
|
3003
|
+
|
|
3004
|
+
|
|
3005
|
+
text | N
|
3006
|
+
| 0 5 km
|
3007
|
+
blank |
|
3008
|
+
|
|
3009
|
+
text | FIGURE 4.2. Map of Lake Gatun study area in central Panama. Seed
|
3010
|
+
| predation experiments were conducted in areas demarcated by trails.
|
3011
|
+
meta | 74 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3012
|
+
blank |
|
3013
|
+
|
|
3014
|
+
|
|
3015
|
+
text | Mammal census. Diurnal mammal transect surveys were conducted from mid-August
|
3016
|
+
| to mid-December in 2008. Once per week in each site, an observer surveyed a 5 km
|
3017
|
+
| transect between the hours of 6:30 AM and 11:30 AM, walking at a speed of 1 km/hr.
|
3018
|
+
| Surveys were not conducted during rain. Observers recorded the species and age
|
3019
|
+
| (adult or juvenile) of all mammals sighted, and measured initial detection distance
|
3020
|
+
| with a Nikon ProStaff 550 range finder (Nikon Inc., Melville, NY). Because of the
|
3021
|
+
| time and difficulty involved in counting individuals in troupes of primates, these
|
3022
|
+
| species were recorded in units of groups. Because most species had few observations
|
3023
|
+
| in PNS, and the parameters that density estimators require could not be accurately
|
3024
|
+
| estimated for that site, I report animal abundances (individuals/km or groups/km),
|
3025
|
+
| rather than densities.
|
3026
|
+
meta | 75
|
3027
|
+
blank |
|
3028
|
+
|
|
3029
|
+
|
|
3030
|
+
text | TABLE 4.1. Mean fresh seed masses of study species. BCI and PNS
|
3031
|
+
| columns denotes species used in each site. Most species are free standing
|
3032
|
+
| growth forms. C. turczanninowii and T. richardii are lianas.
|
3033
|
+
| Species Family Seed mass (g) BCI PNS
|
3034
|
+
| Apeiba tibourbou Tiliaceae 0.0057 X X
|
3035
|
+
| Protium tenuifolium Burseraceae 0.18 X
|
3036
|
+
| Cupania latifolia Sapindaceae 0.19 X
|
3037
|
+
| Chamaedorea tepejilote Arecaceae 0.49 X X
|
3038
|
+
| Connorus turczanninowii Conneraceae 0.49 X
|
3039
|
+
| Thevetia ahouai Apocynaceae 1.11 X
|
3040
|
+
| Oneocarpus mapora Arecaceae 1.95 X
|
3041
|
+
| Virola surinamensis Myristicaeae 2.43 X
|
3042
|
+
| Calophyllum longifolium Clusiaceae 5.48 X
|
3043
|
+
| Astrocaryum standleyanum Arecaceae 9.84 X X
|
3044
|
+
| Gustavia superb Lecythidaceae 16.0 X
|
3045
|
+
| Attalea butyracea Arecaceae 16.2 X X
|
3046
|
+
| Tontelea richardii Celastraceae 64.2 X
|
3047
|
+
blank |
|
3048
|
+
|
|
3049
|
+
text | Seed preparation. Thirteen woody plant species ranging from 0.002 to 64.2 g mean
|
3050
|
+
| fresh seed mass were selected for this study (Table 4.1), representing 76 % of the
|
3051
|
+
| range in fresh seed mass for this area on a log scale. While these species are common
|
3052
|
+
| to both BCI and PNS, heavy insect and/or pathogen infestation of some species in
|
3053
|
+
| PNS prevented collection of viable seeds in this site. Because of protected area rules,
|
3054
|
+
| seeds could not be moved between sites. Therefore, eleven species were examined on
|
3055
|
+
| BCI and six species in PNS, with four species common to both sites, spanning almost
|
3056
|
+
| the entire range of seed size in the study.
|
3057
|
+
| Seeds appearing rotten, insect-damaged, or otherwise unviable were not
|
3058
|
+
| included in the experiment. To remove confounding effects of differing seed pulps, all
|
3059
|
+
| seeds were cleaned of pulp or mucilage. After pulp removal, mass, width and length
|
3060
|
+
| were measured for seeds of all species but Apeiba tibourbou. Apeiba seed mass for
|
3061
|
+
| BCI was previously recorded (Wright et al. 2007). A thread was attached to all but
|
3062
|
+
| the smallest seeds (A. tibourbou and P. tenuifolium), so that I could recover the seeds
|
3063
|
+
| and record their fate.
|
3064
|
+
meta | 76 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3065
|
+
blank |
|
3066
|
+
|
|
3067
|
+
|
|
3068
|
+
text | Seed predation experiment. A randomized block design was used to compare seed
|
3069
|
+
| predation rates in the two sites. Within each forest, six blocks were delineated.
|
3070
|
+
| Within each block, each species was placed on the forest floor in an array of 6-8 seeds
|
3071
|
+
| in a different random location. For G. superba on BCI and C. tepelijote in PNS, only
|
3072
|
+
| four arrays were used, as few seeds unattacked by insects were available. Because A.
|
3073
|
+
| tibourbou and P. tenuifolium, were small and not marked with thread, these species
|
3074
|
+
| were set out in shallow mesh trays with 6-8 seeds per tray. Data reported here is from
|
3075
|
+
| a total of 732 seeds.
|
3076
|
+
| Experiments were conducted between mid-July and mid-September 2009.
|
3077
|
+
| Seeds were monitored for four weeks, during which seed fate and agent of mortality
|
3078
|
+
| were recorded. Classes of seed fate were: unmoved (intact), cached, moved but not
|
3079
|
+
| buried (intact), predated by vertebrates, predated by insects, and killed by pathogens.
|
3080
|
+
| Seeds which were removed and only the thread recovered were presumed predated. .
|
3081
|
+
blank |
|
3082
|
+
|
|
3083
|
+
text | Assessment of seed predator identity. The arrays of 5 species with masses ~2 g or
|
3084
|
+
| larger were monitored with Reconyx RC-55 infrared cameras on BCI for the first
|
3085
|
+
| week. Only half of the Virola arrays were monitored due to camera limitation. In
|
3086
|
+
| addition, the arrays of two of the larger-seeded species, A. standleyanum and A.
|
3087
|
+
| butyracea were monitored in PNS. More species were not monitored in PNS due to
|
3088
|
+
| concerns over equipment loss. As a conservative assignment of seed predator identity,
|
3089
|
+
| the species of seed predator was only recorded when the removal of a marked seed
|
3090
|
+
| was clearly visible in the image. Instances of probable seed removal, but in which
|
3091
|
+
| camera angle, position of the animal, or clarity of the image prevented a clear
|
3092
|
+
| determination of the event, were not assigned to a particular animal species.
|
3093
|
+
blank |
|
3094
|
+
|
|
3095
|
+
text | Analyses. The relationships between mean seed mass and mean seed mortality in the
|
3096
|
+
| two sites was assessed via an ANCOVA, with site as the fixed factor and log-
|
3097
|
+
| transformed mean seed mass as the covariate. Differences in seed caching rates
|
3098
|
+
| between sites were evaluated with a t-test for both palm species. All analyses were
|
3099
|
+
| conducted in R (R Development Core Team, 2008).
|
3100
|
+
meta | 77
|
3101
|
+
blank |
|
3102
|
+
|
|
3103
|
+
|
|
3104
|
+
title | RESULTS
|
3105
|
+
blank |
|
3106
|
+
text | Mammal census. Diurnal mammal transect surveys, conducted from mid-August to
|
3107
|
+
| mid-December in 2008, verified differences in degree of defaunation between BCI and
|
3108
|
+
| PNS, which approximately correspond to moderate and intense degrees of defaunation
|
3109
|
+
| respectively (Fig. 4.3.)
|
3110
|
+
blank |
|
3111
|
+
|
|
3112
|
+
title | Medium-bodied
|
3113
|
+
| Dasyprocta punctata
|
3114
|
+
| Cebus capuchinus
|
3115
|
+
| Alouatta palliata
|
3116
|
+
| Species
|
3117
|
+
blank |
|
3118
|
+
|
|
3119
|
+
|
|
3120
|
+
|
|
3121
|
+
text | Large-bodied
|
3122
|
+
| Ateles geoffroyi ‡
|
3123
|
+
| Mazama americana
|
3124
|
+
| Odocoileus virginianus *
|
3125
|
+
| Pecari tajacu
|
3126
|
+
| BCI
|
3127
|
+
| Tapirus bairdii ‡ PNS
|
3128
|
+
blank |
|
3129
|
+
text | 0.0 0.2 0.4 0.6 0.8 1.0
|
3130
|
+
| Individuals per km
|
3131
|
+
blank |
|
3132
|
+
|
|
3133
|
+
text | FIGURE 4.3. Animal abundances in BCI and PNS as assessed by trail
|
3134
|
+
| census in 2008. Above are species of medium body size known to
|
3135
|
+
| maintain or increase their population density with moderate hunting,
|
3136
|
+
| but decrease with intense hunting (Peres and Palacios 2007). Below
|
3137
|
+
| are large-bodied animals that have been historically present in the sites
|
3138
|
+
| and which are known to be most vulnerable to hunting. At both BCI
|
3139
|
+
| and PNS, most large-bodied mamals are rare or locally extinct.
|
3140
|
+
| However, medium-sized mammals are highly abundant in BCI,
|
3141
|
+
| whereas they are also quite rare in PNS, indicating the two sites are
|
3142
|
+
| moderately and intensely hunted, respectively. † locally extirpated in
|
3143
|
+
| PNS; ‡ locally extirpated in BCI, reintroduced, and currently rare;
|
3144
|
+
| *present and rare at both sites, not observed in this census.
|
3145
|
+
blank |
|
3146
|
+
|
|
3147
|
+
text | Seed predation intensity. Relationships between seed mortality and seed size were
|
3148
|
+
| evaluated by ANCOVA, with site being a fixed factor. Seed mortality over all
|
3149
|
+
| species, when all sources of mortality were pooled, was not correlated with seed mass
|
3150
|
+
| (F1,13 = 1.47, p = 0.25), and this did not differ between sites (F1,13 = 0.69, p = 0.42)
|
3151
|
+
meta | 78 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3152
|
+
blank |
|
3153
|
+
|
|
3154
|
+
|
|
3155
|
+
text | (Fig. 4.4a). For the subset of species with verified vertebrate seed predation , there
|
3156
|
+
| was not significant (F1,12 = 1.45, p = 0.25) (Fig 4.4b) Apeiba, which appeared to have
|
3157
|
+
| no vertebrate seed predators at either site. was excluded from the model. ). Also,
|
3158
|
+
| contrary to the model (Fig. 4.1), the effect of site was not signficant (F1,13 = 0.11, p =
|
3159
|
+
| 0.74) (Fig. 4.4b). Mortality caused by invertebrates and fungal pathogens was
|
3160
|
+
| negatively correlated with seed mass across all species (F1,13 = 21.1, p > 0.001).
|
3161
|
+
| Again, this relationship did not differ by site (F1,13 = 0.19, p = 0.67).
|
3162
|
+
| Mortality by
|
3163
|
+
| All Sources Vertebrates Invertebrates & pathogens
|
3164
|
+
| Proportion seeds killed
|
3165
|
+
blank |
|
3166
|
+
|
|
3167
|
+
|
|
3168
|
+
|
|
3169
|
+
text | 1.0
|
3170
|
+
| A B C
|
3171
|
+
| 0.8
|
3172
|
+
blank |
|
3173
|
+
text | 0.6
|
3174
|
+
blank |
|
3175
|
+
text | 0.4
|
3176
|
+
blank |
|
3177
|
+
text | 0.2
|
3178
|
+
blank |
|
3179
|
+
text | 0.0
|
3180
|
+
| -6 -4 -2 0 2 4 -6 -4 -2 0 2 4 -6 -4 -2 0 2 4
|
3181
|
+
| BCI Log(Seed mass)
|
3182
|
+
| PNS
|
3183
|
+
| FIGURE 4.4. Seed predation rates as a function of seed size on BCI and in PNS.
|
3184
|
+
| (A) Across all species there was a negative, but non-significant, relationship
|
3185
|
+
| between seed mass and seed mortality. (B) Seed mass and vertebrate seed
|
3186
|
+
| predation were not correlated when analysis was restricted to species with verified
|
3187
|
+
| vertebrate seed predators. (Points for Apeiba slightly offset for visualization.) (C)
|
3188
|
+
| Seed mass and seed mortality by invertebrates and fungal pathogens were
|
3189
|
+
| negatively correlated (includes Apeiba). No differences were observed between
|
3190
|
+
| sites.
|
3191
|
+
blank |
|
3192
|
+
|
|
3193
|
+
text | Scatter-hoarding rodents do not just predate seeds. For two of the large seeded
|
3194
|
+
| palms, seed caching by scatter-hoarding rodents is critical for escaping seed predation
|
3195
|
+
| by bruchid beetles. I predicted that caching of Attelea and Astrocaryum would be
|
3196
|
+
| lower in the hunted site, as the primary seed caching agent, the agouti (Dasyprocta
|
3197
|
+
| punctata), was less abundant at that site (Fig. 4.3), unless compensated for by
|
3198
|
+
| squirrels. Contrary to this prediction, the number of seeds cached did not differ
|
3199
|
+
| between sites for either species (Attalea: t = -0.129, p = 0.55, one-tailed test;
|
3200
|
+
| Astrocaryum: t = -0.412, p = 0.66, one-tailed test). (Fig. 4.5). This equivalence
|
3201
|
+
meta | 79
|
3202
|
+
blank |
|
3203
|
+
|
|
3204
|
+
|
|
3205
|
+
text | between sites appears not to be due compensation by squirrels, in as far as every seed
|
3206
|
+
| caching event for which the agent could be verified by camera trap was committed by
|
3207
|
+
| an agouti (data not shown).
|
3208
|
+
blank |
|
3209
|
+
|
|
3210
|
+
text | 2.5
|
3211
|
+
blank |
|
3212
|
+
|
|
3213
|
+
text | 2.0
|
3214
|
+
blank |
|
3215
|
+
text | Seeds Cached
|
3216
|
+
| 1.5
|
3217
|
+
blank |
|
3218
|
+
|
|
3219
|
+
text | 1.0
|
3220
|
+
blank |
|
3221
|
+
|
|
3222
|
+
text | 0.5
|
3223
|
+
blank |
|
3224
|
+
|
|
3225
|
+
text | 0.0
|
3226
|
+
| BCI PNS BCI PNS
|
3227
|
+
| Attalea Astrocaryum
|
3228
|
+
| Sites by Species
|
3229
|
+
| FIGURE 4.5. Number of seeds cached per array of eight seeds for two
|
3230
|
+
| large seeded palms did not differ between BCI and PNS.
|
3231
|
+
blank |
|
3232
|
+
text | Seed predator identity. Camera trap monitoring of seeds in the first week on BCI
|
3233
|
+
| revealed D. punctata, to be the primary agent of seed removal for all species (Fig.
|
3234
|
+
| 4.6). Seed removal by spiny rats (Proechimys steerei) and squirrels (Sciurus
|
3235
|
+
| granatensis) accounted for little of the seed predation and varied by plant species (Fig.
|
3236
|
+
| 4.6). Data from BCI do not appear support the hypothesis that seed predator size is
|
3237
|
+
| correlated with seed size.
|
3238
|
+
meta | 80 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3239
|
+
blank |
|
3240
|
+
|
|
3241
|
+
|
|
3242
|
+
text | 50 50
|
3243
|
+
| Not taken
|
3244
|
+
| Unknown
|
3245
|
+
| Squirrel
|
3246
|
+
| Spiny rat 40
|
3247
|
+
| 40 Agouti
|
3248
|
+
blank |
|
3249
|
+
|
|
3250
|
+
|
|
3251
|
+
|
|
3252
|
+
text | Number of seeds
|
3253
|
+
| Number of seeds
|
3254
|
+
blank |
|
3255
|
+
|
|
3256
|
+
|
|
3257
|
+
|
|
3258
|
+
text | 30
|
3259
|
+
| 30
|
3260
|
+
blank |
|
3261
|
+
|
|
3262
|
+
text | 20
|
3263
|
+
| 20
|
3264
|
+
blank |
|
3265
|
+
|
|
3266
|
+
text | 10
|
3267
|
+
| 10
|
3268
|
+
blank |
|
3269
|
+
text | 0
|
3270
|
+
| 0
|
3271
|
+
| BCI PNS BCI PNS
|
3272
|
+
| Oneocarpus Virola Astrocaryum Attalea Tontelea
|
3273
|
+
| Attalea Astrocaryum
|
3274
|
+
| Species ranked by mass Sites by Species
|
3275
|
+
blank |
|
3276
|
+
|
|
3277
|
+
text | FIGURE 4.6. Identity of species removing seeds during first week of
|
3278
|
+
| experiment. (Left) On BCI five species ranging in mass from 1.95 g
|
3279
|
+
| (Oneocarpus) to 64.2 g (Tontelea) were primarily removed by
|
3280
|
+
| agoutis, and showed no relationship between seed size and seed
|
3281
|
+
| predator body size. (Right) Seed removal of large-seeded palms at
|
3282
|
+
| BCI and PNS. Removal of Attelea was higher in PNS, but
|
3283
|
+
| Astrocaryum removal did not differ between sites. Seed predation
|
3284
|
+
| by small mammals was higher in PNS for Attalea, and higher in BCI
|
3285
|
+
| for Astrocaryum.
|
3286
|
+
blank |
|
3287
|
+
text | A comparison of palm seed dispersal in BCI and PNS revealed that the seed
|
3288
|
+
| removal of Attelea in PNS was more than 4-fold higher in the hunted site, contrary to
|
3289
|
+
| expectation. Verified Attelea predation by D. punctata was similar in both sites, while
|
3290
|
+
| seed predation by small mammals, primarily squirrels, was much higher in the hunted
|
3291
|
+
| site. Astrocaryum removal in the first week was 100% in both sites, with confirmed
|
3292
|
+
| removals by D. punctata being slightly higher in the hunted site, and removals by P.
|
3293
|
+
| steerei being slightly higher in the protected site (Fig. 4.6).
|
3294
|
+
meta | 81
|
3295
|
+
blank |
|
3296
|
+
|
|
3297
|
+
|
|
3298
|
+
title | DISCUSSION
|
3299
|
+
blank |
|
3300
|
+
text | Hunting is a pervasive threat to biodiversity in tropical forests. Decreases in plant
|
3301
|
+
| diversity as high as 66% have been documented as an indirect consequence of hunting.
|
3302
|
+
| Yet the mechanisms by which that diversity is lost are poorly understood, as is their
|
3303
|
+
| context dependence. This study aimed to test some basic assumptions about plant-
|
3304
|
+
| seed predator interactions in the context of seed size, as well as hypotheses as to how
|
3305
|
+
| those interactions may change as a consequence of defaunation. This information is
|
3306
|
+
| useful for understanding how vertebrate seed predators shape community level
|
3307
|
+
| distributions of seed size, and to predict how and why plant community composition
|
3308
|
+
| may change with increasing hunting intensity.
|
3309
|
+
| This discussion focuses primarily on plant-seed predator interactions.
|
3310
|
+
| However, as several of the animals relevant to this discussion are also recognized to be
|
3311
|
+
| secondary seed dispersers, much of the discussion which follows is equally relevant to
|
3312
|
+
| seed dispersal.
|
3313
|
+
blank |
|
3314
|
+
|
|
3315
|
+
text | Seed size and vertebrate seed predation intensity. Overall, this study found little
|
3316
|
+
| support for the model assumption that vertebrate seed predation rates are correlated
|
3317
|
+
| with seed mass, either positively in moderately defaunated sites, or negatively in
|
3318
|
+
| highly defaunated sites. Other seed traits, as well as natural history, may be more
|
3319
|
+
| important for determining seed predation rates than seed mass per se. For instance, of
|
3320
|
+
| the three of largest seed-species in this study, the Astrocaryum and Attelea exhibited
|
3321
|
+
| the highest rates of seed removal, whereas Gustavia exhibited one of the lowest.
|
3322
|
+
| Relative to Gustavia, the palm seeds have an endosperm that is high in fat content, and
|
3323
|
+
| therefore energy rich for their weight. The rodents are well adapted to the primary
|
3324
|
+
| defense of these palms against seed predators: a woody endocarp. While the thin seed
|
3325
|
+
| coat of Gustavia would appear to make it more vulnerable to vertebrate seed
|
3326
|
+
| predators, it may exhibit chemical defenses that make them less desirable to
|
3327
|
+
| rodents(e.g. Forget 1992). Indeed, it was not uncommon on BCI and PNS to see bits
|
3328
|
+
| of Gustavia pulp with a pile of intact seeds of the forest floor, the result of agoutis
|
3329
|
+
| consuming the fruit flesh and discarding the seeds (E. Kurten, pers. obs.). However,
|
3330
|
+
meta | 82 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3331
|
+
blank |
|
3332
|
+
|
|
3333
|
+
|
|
3334
|
+
text | there are circumstances in which Gustavia seed predation has been higher (Sork 1987,
|
3335
|
+
| Forget 1992).
|
3336
|
+
| The natural history of the two palm species also make them preferable for
|
3337
|
+
| hoarding. A. standleyanum and A. butyracea germinate after 8 and 12 months
|
3338
|
+
| respectively. Therefore, they are likely to persist intact as hoarded seeds until the
|
3339
|
+
| period of low fruit availability from November through February (Foster 1982). In
|
3340
|
+
| contrast, Gustavia germinates within 1-2 weeks of fruit fall (E. Kurten, pers. obs.).
|
3341
|
+
| While the seeds remain attached to the establishing seedling for many more months,
|
3342
|
+
| seeds and cotyledons are vulnerable to consumption by other seedling predators, and
|
3343
|
+
| seed energy stores become reduced over time. By November, Gustavia seedlings are
|
3344
|
+
| no longer of interest to agoutis on BCI (Forget 1992). Therefore, in contrast to the
|
3345
|
+
| palms, Gustavia is not a species useful for provisioning rodents through the period of
|
3346
|
+
| low fruit availability.
|
3347
|
+
| Comparison of the large-seeded palm species and Gustavia illustrates how
|
3348
|
+
| variability in seed consumption by vertebrates among seeds of similar size is likely to
|
3349
|
+
| be introduced by a variety of differences in nutritive value, defense traits, and
|
3350
|
+
| germination strategy. Variation in these traits will likely cause deviations in
|
3351
|
+
| consumption rates from what may be predicted by seed size and optimal foraging
|
3352
|
+
| theory alone.
|
3353
|
+
blank |
|
3354
|
+
|
|
3355
|
+
text | Seed predator identity. Camera-based observations for five species preyed upon by
|
3356
|
+
| vertebrates showed little support for the model assumptions that the seed predator
|
3357
|
+
| body size is correlated with the size of the seed. While enclosure and exclosure
|
3358
|
+
| experiments have demonstrated that small rodents prefer small seeded species to
|
3359
|
+
| taxonomically related larger seeds, and can exert a large, and disproportionate seed
|
3360
|
+
| predation pressure on smaller seeded species (Dirzo et al. 2007, Mendoza & Dirzo
|
3361
|
+
| 2007), this study suggests that when seeds are available to the entire community of
|
3362
|
+
| potential seed predators, the importance of smaller mammals, even for relatively
|
3363
|
+
| smaller seeds, is diminished. In particular, agoutis appear to be a highly important
|
3364
|
+
| seed predator and secondary seed disperser in this system.
|
3365
|
+
meta | 83
|
3366
|
+
blank |
|
3367
|
+
|
|
3368
|
+
|
|
3369
|
+
text | There may be other circumstances, however, in which the relationship between
|
3370
|
+
| seed size and seed predator biomass may be stronger. It is notable that, despite the
|
3371
|
+
| fact that peccaries are well-documented seed predators of palms such as Astrocaryum
|
3372
|
+
| and Attelea in many parts of the Neotropics (Beck 2006), no observations of predation
|
3373
|
+
| of these two species by peccaries were observed in this study. This is likely due to the
|
3374
|
+
| fact that larger-bodied seed predators such as peccaries and brocket deer tend to
|
3375
|
+
| consume fruits and seeds under fruiting trees, where fruit and seed densities are
|
3376
|
+
| highest and foraging most efficient. In contrast, the seed arrays in this experiment best
|
3377
|
+
| mimicked the situation in which a few seeds have already been dispersed away from
|
3378
|
+
| the parent tree. Rodents such as agoutis and squirrels, will also forage under fruiting
|
3379
|
+
| trees. However, as scatter-hoarding species, they are behaviorally more likely than
|
3380
|
+
| larger seed predators to search for, find and consume small, isolated patches of seeds
|
3381
|
+
| on the forest floor.
|
3382
|
+
| In addition to dispersal context, the composition of the mammal community is
|
3383
|
+
| likely influential in determining the strength of any relationship between seed size and
|
3384
|
+
| seed disperser size. For example, in forests such as Cocha Cashu, Peru, agoutis are
|
3385
|
+
| much less abundant (Terborgh & Wright 1994), and therefore less likely to
|
3386
|
+
| demonstrate a high importance as seed predators and seed dispersers across a range of
|
3387
|
+
| species, as seen on BCI. BCI is also lacking an abundance of terrestrial vertebrates at
|
3388
|
+
| the two extremes of seed predator body size. White-lipped peccaries (T. pecari) have
|
3389
|
+
| been locally extinct for more than half a century on BCI, and tapirs are rare. At the
|
3390
|
+
| other extreme, in parts of Mexico and Belize, mice such as Peromyscus and
|
3391
|
+
| Heteromys can be significant seed predators of some species (Coates-Estrada &
|
3392
|
+
| Estrada 1988, Klinger and Rejmanek 2009), whereas rodents smaller than spiny rats
|
3393
|
+
| (P. steerii) are rare on BCI.
|
3394
|
+
blank |
|
3395
|
+
|
|
3396
|
+
text | Seed predation and defaunation. Despite large differences in abundances of key seed
|
3397
|
+
| predators such as collared peccaries and agoutis, decreased vertebrate seed predation
|
3398
|
+
| rates of larger-seeded species were not generally observed between BCI and PNS, nor
|
3399
|
+
| did smaller-seeded species generally show increases in seed predation rates in the
|
3400
|
+
meta | 84 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3401
|
+
blank |
|
3402
|
+
|
|
3403
|
+
|
|
3404
|
+
text | hunted site relative to the protected site. Rates of seed caching of large-seeded palms,
|
3405
|
+
| critical for seedling recruitment in those species, also did not differ between sites.
|
3406
|
+
| These data corroborate the work of Wright and colleagues (2001) with respect to
|
3407
|
+
| large-seeded palms, and extend it to a broader spectrum of species.
|
3408
|
+
| Rather than seed predation, and secondary seed dispersal, varying linearly with
|
3409
|
+
| agouti abundance in this system, it may be useful to consider the possibility of seed
|
3410
|
+
| predator thresholds. In particular, lower populations of agoutis as a consequence of
|
3411
|
+
| hunting may serve to decrease competition for fruit and seed resources among agoutis
|
3412
|
+
| locally, but within certain limits, may not interfere with seed dispersal and seed
|
3413
|
+
| predation rates from the perspective of the plant. However, if hunting reduces agouti
|
3414
|
+
| populations below a particular threshold in abundance, there are no longer enough
|
3415
|
+
| animals to adequately maintain levels of seed predation and dispersal.
|
3416
|
+
| Conceptualizing the disruption of plant-seed predator interactions in terms of
|
3417
|
+
| thresholds is similar to the model proposed by Galetti and colleagues (2006), in which
|
3418
|
+
| Astrocaryum seed predation rates are a sigmoidal or logistic, rather than linear,
|
3419
|
+
| function of agouti abundance. Data from two defaunation gradients suggest this may
|
3420
|
+
| be the case (Fig. 4.7). In Panama, sites with agouti densities 60%-80% lower than
|
3421
|
+
| BCI still had high rodent seed predation rates equivalent to or higher than those
|
3422
|
+
| observed on BCI, but where agouti densities were further reduced, seed predation rates
|
3423
|
+
| dropped dramatically (Wright et al. 2001). Likewise in Brazil, sites with agouti
|
3424
|
+
| abundances 80% lower than the maximum density observed still maintained agouti
|
3425
|
+
| seed predation rates approximately equal to those observed in the sites with the highest
|
3426
|
+
| agouti abundance (Donatti et al. 2009).
|
3427
|
+
meta | 85
|
3428
|
+
blank |
|
3429
|
+
|
|
3430
|
+
|
|
3431
|
+
text | 100 Above threshold
|
3432
|
+
blank |
|
3433
|
+
|
|
3434
|
+
|
|
3435
|
+
|
|
3436
|
+
text | Rodent seed predation (%)
|
3437
|
+
| Below threshold
|
3438
|
+
blank |
|
3439
|
+
text | 80
|
3440
|
+
blank |
|
3441
|
+
|
|
3442
|
+
text | 60
|
3443
|
+
blank |
|
3444
|
+
|
|
3445
|
+
text | 40
|
3446
|
+
blank |
|
3447
|
+
|
|
3448
|
+
text | 20
|
3449
|
+
blank |
|
3450
|
+
|
|
3451
|
+
text | 0
|
3452
|
+
| A B C D E
|
3453
|
+
| Literature Study
|
3454
|
+
| FIGURE 4.7. Published studies examining seed predation of
|
3455
|
+
| large-seeded palms by rodents, primarily agoutis, across
|
3456
|
+
| defaunation gradients consistently find that high rates of seed
|
3457
|
+
| predation are maintained despite reductions in agouti densities up
|
3458
|
+
| to 80% of maximum observed densities. Below this threshold,
|
3459
|
+
| seed predation rates drop 48-96%. (A) Galetti et al. (2006),
|
3460
|
+
| Astrocaryum aculeatissimum, under parent trees; (B) Donatti et
|
3461
|
+
| al. (2009), A. aculeatissimum, controlled experiment; (C) Galetti
|
3462
|
+
| et al.(2006), ), A. aculeatissimum, controlled experiment; (D)
|
3463
|
+
| Wright et al. (2000), Astrocaryum standleyanum, “dispersed”
|
3464
|
+
| seeds; (E) Wright et al. (2000), Attalea butyracea, “dispersed”
|
3465
|
+
| seeds.
|
3466
|
+
| At a community level, evidence has been found both for large, mammal- or
|
3467
|
+
| primate-dispersed species decreasing in abundance in association with hunting
|
3468
|
+
| (Nunez-Iturri et al. 2008, Terborgh et al. 2008), and community mean seed mass
|
3469
|
+
| increasing in association with hunting (Wright et al. 2007, Ch. 2). Differences in the
|
3470
|
+
| mammalian community context, in the relative levels of defaunation being compared,
|
3471
|
+
| and differences in the traits and natural histories of plant species driving the
|
3472
|
+
| community level patterns may all be contributing to such discrepancies in community
|
3473
|
+
| level response to hunting.
|
3474
|
+
meta | 86 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3475
|
+
blank |
|
3476
|
+
|
|
3477
|
+
|
|
3478
|
+
title | CONCLUSIONS
|
3479
|
+
blank |
|
3480
|
+
|
|
3481
|
+
text | Overall, this empirical test of a theoretical model (Dirzo et al. 2007) of how seed
|
3482
|
+
| predation rates should vary as a function of seed size and defaunation intensity found
|
3483
|
+
| little general support for the model. In this system, there was only weak support for a
|
3484
|
+
| relationship between seed mass and vertebrate seed predation rate, and no evidence
|
3485
|
+
| that seeds were increasingly predated upon by larger-bodied seed predators as seed
|
3486
|
+
| size increased by species. Furthermore, despite large differences in the abundances of
|
3487
|
+
| key seed predators between a hunted and protected site, no differences were seen in
|
3488
|
+
| vertebrate seed predation, or seed caching by agoutis. This work highlights the
|
3489
|
+
| importance of considering both plant natural history and mammal community context
|
3490
|
+
| when trying to predict the indirect effects of hunting on plant recruitment. It also is
|
3491
|
+
| consistent with accumulating evidence that the functional roles that seed predators and
|
3492
|
+
| seed dispersers play in tropical forests may not be linearly correlated with their
|
3493
|
+
| abundance in a system, but rather, may be threshold-dependent.
|
3494
|
+
blank |
|
3495
|
+
title | ACKNOWLEDGEMENTS
|
3496
|
+
blank |
|
3497
|
+
text | The author is grateful to the Autoridad Nacional del Ambiente (ANAM) of Panama
|
3498
|
+
| for permission to conduct work in Parque Nacional Soberanía, and to the Smithsonian
|
3499
|
+
| Tropical Research Institute (STRI) for permission to conduct this work on BCI, and
|
3500
|
+
| for providing logistical support. I would like to thank J. Wright for seed mass data
|
3501
|
+
| and advice about sites. N. Beckman also provided useful advice in the planning stages
|
3502
|
+
| of this experiment. The Fondo Peregrino–Panamá, in particular A. Muela, provided
|
3503
|
+
| logistical support at the site in the Parque Nacional Soberanía. Many thanks go to C.
|
3504
|
+
| Sherman, R. Bethancourt and R. Acosta for their hard work in the field and the lab,
|
3505
|
+
| and to S. Rebellon for help with pilot work. D. Brassfield and O. Calderón provided
|
3506
|
+
| help with species identification. I would like to thank O. Arosemena at STRI for her
|
3507
|
+
| help with permitting, and all the staff on BCI whose help made conducting this work
|
3508
|
+
| easier. R. Dirzo and C. Donatti provided comments which improved the manuscript.
|
3509
|
+
| This project was made possible with funding from NSF DEB-0808338.
|
3510
|
+
meta | 87
|
3511
|
+
blank |
|
3512
|
+
|
|
3513
|
+
|
|
3514
|
+
|
|
3515
|
+
title | Bibliography
|
3516
|
+
ref | Alroy, J. 2001. A musltispecies overkill simulation of the end-Pleistocene megafaunal
|
3517
|
+
| mass extinction. Science 292:1893-1896.
|
3518
|
+
| Ackerly, D. D., C. A. Knight, S.B. Weiss, K. Barton, K.P. Starmer. 2002. Leaf size,
|
3519
|
+
| specific leaf area and microhabitat distribution of chaparral woody plants:
|
3520
|
+
| Contrasting patterns in species level and community level analyses. Oecologia
|
3521
|
+
| 130(3): 449-457.
|
3522
|
+
| Adler, G.H. 1996. The island syndrome in isolated populations of a tropical forest
|
3523
|
+
| rodent. Oecologia. 108:694-700.
|
3524
|
+
| Alvarez-Clare S. & K. Kitajima 2007. Physical defence traits enhance seedling
|
3525
|
+
| survival of Neotropical tree species. Func. Ecol. 21: 1044-1054.
|
3526
|
+
| Alvarez-Clare S. & K. Kitajima 2009.
|
3527
|
+
| Alves-Costa, C.P. 2004. Efeitos da defaunação de mamíferos herbívoros na
|
3528
|
+
| comunidade vegetal. Dissertation thesis. Instituto de Biologia, Universidade
|
3529
|
+
| Estadual de Campinas, Brazil.
|
3530
|
+
| Andresen, E. 2003. Effect of forest fragmentation on dung beetle communities and
|
3531
|
+
| functional consequences for plant regeneration. Ecography. 26: 87–97.
|
3532
|
+
| Andresen, E. and S.G.W. Laurance. 2003. Possible Indirect Effects of Mammal
|
3533
|
+
| Hunting on Dung Beetle Assemblages in Panama. Biotropica. 39(1): 141–146.
|
3534
|
+
meta | 88 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3535
|
+
blank |
|
3536
|
+
|
|
3537
|
+
|
|
3538
|
+
ref | Asquith, N. M. Wright, S.J. and M.J. Clauss. 1997. Does mammal community
|
3539
|
+
| composition control recruitment in neotropical forests? Evidence from
|
3540
|
+
| Panama. Ecology. 78(3): 941-946.
|
3541
|
+
| Asquith N.M., J. Terborgh, A.E. Arnold, and C.M. Riveros. 1999. The fruits the
|
3542
|
+
| agouti ate: Hymenaea courbaril seed fate when its disperser is absent. J. Trop.
|
3543
|
+
| Ecol. 15: 229-235.
|
3544
|
+
| Babweteera F. P. Savill and N. Brown. 2007. Balanites wilsoniana: Regeneration with
|
3545
|
+
| and without elephants. Biol. Cons. 134: 40-47.
|
3546
|
+
| Babweteera F. and N. Brown. 2009. Can remnant frugivore species effectively
|
3547
|
+
| disperse tree seeds in secondary tropical rain forests? Biodivers Conserv. 18:
|
3548
|
+
| 1611–1627.
|
3549
|
+
| Barnosky, A. D., P. L. Koch, R. S. Feranec, S. L. Wing, and A. B. Shabel. 2004.
|
3550
|
+
| Assessing the causes of Late Pleistocene extinctions on the continents. Science
|
3551
|
+
| 306: 70-75.
|
3552
|
+
| Barone, J.A. and P.D. Coley. 2002. Herbivorismo y las defensas de las plantas. Pages
|
3553
|
+
| 465-492.in M.R. Guariguata and G.H. Kattan, editors. Ecología y conservación
|
3554
|
+
| de Bosques Neotropicales. Libro Universitario Regional, Cartago, Costa Rica.
|
3555
|
+
| Beck H. and J. Terborgh. 2005. Groves versus isolates: How spatial aggregation of
|
3556
|
+
| Astrocaryum murumuru palms affects seed removal. J. Trop. Ecol. 18(2): 275-
|
3557
|
+
| 288.
|
3558
|
+
| Beck H. 2006. A review of peccary-palm interactions and their ecological
|
3559
|
+
| ramifications across the Neotropics. J. Mam., 87(3): 519–530.
|
3560
|
+
| Beckman, N.G. and H. Muller-Landau. 2007. Differential effects of hunting on pre-
|
3561
|
+
| dispersal seed predation and primary and secondary seed removal of two
|
3562
|
+
| Neotropical tree species. Biotropica 39(3): 328-339.
|
3563
|
+
| Brodie J.F., O.E. Helmy, W.Y. Brockelman, and J.L. Maron. 2009. Bushmeat
|
3564
|
+
| poaching reduces the seed dispersal and population growth rate of a mammal-
|
3565
|
+
| dispersed tree. Ecol. App. 19(4): 854–863.
|
3566
|
+
| Brodie, J.F. and H. Gibbs. 2009. Bushmeat hunting as climate threat. Science. 326:
|
3567
|
+
| 364-365.
|
3568
|
+
meta | 89
|
3569
|
+
blank |
|
3570
|
+
|
|
3571
|
+
|
|
3572
|
+
ref | Bunker, D.E. and Carson, W.P. 2005. Drought stress and tropical forests woody
|
3573
|
+
| seedlings: effect on community structure and composition. J. Trop. Ecol. 93:
|
3574
|
+
| 794-806.
|
3575
|
+
| Chaneton E.J., J.M. Facelli and R.J.C. Leon.1988. Floristic changes induced by
|
3576
|
+
| flooding on grazed and ungrazed lowland grasslands in Argentina. J. Range
|
3577
|
+
| Manag. 41(6); 495-499
|
3578
|
+
| Chapman C.A. & D.A. Onderdonk. 1998. Forests Without Primates: Primate/Plant
|
3579
|
+
| Codependency. Am. J. Primatol. 45:127–141.
|
3580
|
+
| Cingolani, A. M., G. Posse, and M.B. Collantes. 2005. Plant functional traits,
|
3581
|
+
| herbivore selectivity and response to sheep grazing in Patagonian steppe
|
3582
|
+
| grasslands. J. Ecol. 42(1): 50-59.
|
3583
|
+
| Coley, P. D. and J. A. Barone. 1996. Herbivory and plant defenses in tropical forests.
|
3584
|
+
| Ann. Rev. Ecol. Sys. 27: 305-335.
|
3585
|
+
| Condit, R., N. Pitman, E.G. Leigh Jr., J. Chave, J. Terborgh, R.B. Foster, P. Nuñez, S.
|
3586
|
+
| Aguilar, R. Valencia, G. Villa, H.C. Muller-Landau, E. Losos, S.P. Hubbell.
|
3587
|
+
| 2002. Beta-diversity in tropical forest trees. Science. 295: 666-669.
|
3588
|
+
| Connell, J. H. 1971. On the role of natural enemies in preventing competitive
|
3589
|
+
| exclusion in some marine animals and in rain forest trees. Pages 298-312 in
|
3590
|
+
| R.G. Den Boer, editor. Dynamics of numbers in populations. Proceedings of
|
3591
|
+
| the Advanced Study Institute on dynamics of numbers in populations,
|
3592
|
+
| Oosterbeck, 1971. Centre for Agricultural Publishing and Documentation,
|
3593
|
+
| Wageningen..
|
3594
|
+
| Cordiero N. and H. Howe. 2003. Forest fragmentation severs mutualism between seed
|
3595
|
+
| dispersers and an endemic African tree. PNAS. 100(24): 14052–14056.
|
3596
|
+
| Corlett, R.T. 2007. The impact of hunting on the mammalian fauna of tropical Asian
|
3597
|
+
| forests. Biotropica 39(3): 292-303.
|
3598
|
+
| Cornelissen, J.H.C., S. Lavorel, E. Garnier, S. Diaz, N. Buchmann, D.E. Gurvich, P.B.
|
3599
|
+
| Reich, H. ter Steeg, H.D. Morgan, M.G.A. van der Heijden, J.G. Pausas, and
|
3600
|
+
| H. Poorter. 2003. A handbook of protocols for standardized and easy
|
3601
|
+
| measurement of plant functional traits worldwide. Aust. J. Bot. 51: 335-380.
|
3602
|
+
meta | 90 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3603
|
+
blank |
|
3604
|
+
|
|
3605
|
+
|
|
3606
|
+
ref | Cramer J.M, R.C.G. Mesquita, G.B. Williamson. 2007. Forest fragmentation
|
3607
|
+
| differentially affects seed dispersal of large and small-seeded tropical trees.
|
3608
|
+
| Biol. Cons. 1 3 7 : 4 1 5 –4 2 3.
|
3609
|
+
| DeMattia, E.A., Curran, L.M. and B.J. Rathcke. 2004. Effects of small rodents and
|
3610
|
+
| large mammals on Neotropical seeds. Ecology. 85(8): 2161–2170.
|
3611
|
+
| DeMattia, E.A. and B.J. Rathcke. 2006. Effects of Small Rodent and Large Mammal
|
3612
|
+
| Exclusion on Seedling Recruitment in Costa Rica. Biotropica. 38(2): 196–202.
|
3613
|
+
| de Vivo, M. and A. P. Carmignotto. 2004. Holocene vegetation change and the
|
3614
|
+
| mammal faunas of South America and Africa. Journal of Biogeography
|
3615
|
+
| 31:943-957.
|
3616
|
+
| Diaz, S., I. Noy-Meir, M. Cabido. 2001. Can grazing response of herbaceous plants be
|
3617
|
+
| predicted from simple vegetative traits? J. App. Ecol. 38(3): 497-508.
|
3618
|
+
| Di Bitetti M.S., A. Paviolo, C.A. Ferrari, C. De Angelo, and Y. Di Blanco. 2008.
|
3619
|
+
| Differential responses to hunting in two sympatric species of Brocket deer
|
3620
|
+
| (Mazama americana and M. nana). Biotropica 40(5): 636-645.
|
3621
|
+
| Dirzo, R. and A. Miranda. 1991. Altered Patterns of herbivory and diversity in the
|
3622
|
+
| forest understory: A case study of the possible consequences of contemporary
|
3623
|
+
| defaunation. Pages 273-287 in P.W. Price, T.M. Lewinsohn, G.W. Fernandes,
|
3624
|
+
| & W.W. Benson, editors. Plant-Animal Interactions: Evolutionary Ecol. in
|
3625
|
+
| Tropical and Temperate Regions. John Wiley & Sons, Inc.
|
3626
|
+
| Dirzo, R., E. Mendoza, and P. Ortiz. 2007. Size-related differential seed predation in a
|
3627
|
+
| heavily defaunated Neotropical rain forest. Biotropica. 39(3): 355-362.
|
3628
|
+
| Donatti, C.I., P.R. Guimarães Jr., and M. Galetti. 2009. Seed dispersal and predation
|
3629
|
+
| in the endemic Atlantic rainforest palm Astrocaryum aculeatissimum across a
|
3630
|
+
| gradient of seed disperser abundance. Ecol. Res. DOI 10.1007/s11284-009-
|
3631
|
+
| 0601-x.
|
3632
|
+
| Erard, E., M. Théry, and D. Sabatier. 1991. Régime alimentaire de Tinamus major
|
3633
|
+
| (Tinamidae), Crax alector (Cracidae) et Psophia crepitans (Psophiidae), en
|
3634
|
+
| Forêt Guyanaise. Gibier Faune Sauvage 8: 183–210.
|
3635
|
+
meta | 91
|
3636
|
+
blank |
|
3637
|
+
|
|
3638
|
+
|
|
3639
|
+
ref | Fa J.E. and D. Brown. 2009. Impacts of hunting on mammals in African tropical
|
3640
|
+
| moise forests: a review and synthesis. Mamm. Rev. 39(4): 321-264.
|
3641
|
+
| Fa, J.E. and Peres C.A. 2001. Game vertebrate extraction in African and Neotropical
|
3642
|
+
| forests: A intercontinental comparison. In J.D. Reynolds, G.M. Mace, K.H.
|
3643
|
+
| Redford, and J.G. Robinson (Eds.) Conservation of Exploited Species.
|
3644
|
+
| Cambridge University Press, Cambridge, UK. Pages 203-241.
|
3645
|
+
| Fadini, R.F., M. Fleury, C.I. Donatti, and M. Galetti. 2008. Effects of frugivore
|
3646
|
+
| impoverishment and seed predators on the recruitment of a keystone palm.
|
3647
|
+
| Acta Oecolo. 35(2): 188-196.
|
3648
|
+
| Farwig, N. K. Böhning-Gaese, B. Bleher. 2006. Enhanced seed dispersal of Prunus
|
3649
|
+
| africana in fragmented and disturbed forests? Oecologia. 147: 238–252.
|
3650
|
+
| Fleury, M. and M. Galetti. 2006. Forest fragment size and microhabitat effects on
|
3651
|
+
| palm seed predation. Biol. Cons. 131: 1-13.
|
3652
|
+
| Forget, P.M. 1992. Seed removal and seed fate in Gustavia superb (Lecythidaceae).
|
3653
|
+
| Biotropica. 24(3): 408-414.
|
3654
|
+
| Foster, R. B. 1982. Famine on Barro Colorado Island. Pages 201–212 in Leigh,
|
3655
|
+
| E.G.,Wilson, D. M. & Rand, A. S. (eds). The ecology of a tropical forest:
|
3656
|
+
| seasonal rhythms and long-term change. Smithsonian Institution Press,
|
3657
|
+
| Washington, DC.
|
3658
|
+
| Galetti M., C.I., Donatti, C.I., A.S. Pires, P.R. Guimaraes Jr., R. Jordano. 2006. Seed
|
3659
|
+
| survival and dispersal of an endemic Atlantic forest palm: the combined effects
|
3660
|
+
| of defaunation and forest fragmentation. Bot. J. Linn. Soc. 151: 141–149.
|
3661
|
+
| Garwood, N.C. 1983. Seed Germination in a Seasonal Tropical Forest in Panama: A
|
3662
|
+
| Community Study. Ecol. Monographs 53(2): 159-181.
|
3663
|
+
| Gehring, C.A., J.E. Wolf and T.C. Theimer. 2002. Terrestrial vertebrates promote
|
3664
|
+
| arbuscular mycorrhizal fungal diversity and inoculums potential in a rain forest
|
3665
|
+
| soil. Ecol. Lett. 5: 540–548.
|
3666
|
+
| Guariguata, M.R., J.J. Rosales-Adame and B. Finegan. 2000. Seed Removal and Fate
|
3667
|
+
| in Two Selectively Logged Lowland Forests with Constrasting Protection
|
3668
|
+
| Levels. Cons. Biol. 14(4): 1046–1054.
|
3669
|
+
meta | 92 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3670
|
+
blank |
|
3671
|
+
|
|
3672
|
+
|
|
3673
|
+
ref | Guariguata, M.R., H. Arias-Le Claire and G. Jones. 2002. Tree Seed Fate in a Logged
|
3674
|
+
| and Fragmented Forest Landscape, Northeastern Costa Rica. Biotropica.
|
3675
|
+
| 34(3): 405–415.
|
3676
|
+
| Guimaraes, P. R., Jr., M. Galetti, and P. Jordano. 2008. Seed Dispersal Anachronisms:
|
3677
|
+
| Rethinking the Fruits Extinct Megafauna Ate. PLoS ONE 3:e1745.
|
3678
|
+
| Hardesty B.D. and H.C. Muller-Landau. 2005. Seed dispersal of woody plants in
|
3679
|
+
| tropical forests: concepts, examples, and future directions. Pages 267-309 in
|
3680
|
+
| D.F.R.P. Burslem, M. A. Pinard and S. E.Hartley, editors. Biotic interactions in
|
3681
|
+
| the Tropics: their role in the maintenance of species diversity. Cambridge Univ.
|
3682
|
+
| Press., New York, NY, U.S.A.
|
3683
|
+
| Harms, K. E., S. J. Wright, O. Calderon, A. Hernandez, and E.A. Herre. 2000.
|
3684
|
+
| Pervasive density-dependent recruitment enhances seedling diversity in a
|
3685
|
+
| tropical forest. Nature 404(6777): 493-495.
|
3686
|
+
blank |
|
3687
|
+
ref | Hedges L.V. and I. Olkin. (1985). Statistical Methods for Meta-Analysis. Academic
|
3688
|
+
| Press. San Diego, CA, USA.
|
3689
|
+
| Holbrook, K.M. and B.A. Loiselle. 2009. Dispersal in a Neotropical tree, Virola
|
3690
|
+
| flexuosa (Myristicaceae): Does hunting of large vertebrates limit seed
|
3691
|
+
| removal? Ecology. 90(6): 1449–1455.
|
3692
|
+
| Ickes, K., S. J. Dewalt, S. Appanah. 2001. Effects of native pigs (Sus scrofa) on
|
3693
|
+
| woody understorey vegetation in a Malaysian lowland rain forest. J. Trop.
|
3694
|
+
| Ecol. 17(2): 191-206.
|
3695
|
+
| Janzen, D. H. 1970. Herbivores and the number of tree species in tropical forests. Am.
|
3696
|
+
| Nat. 104(940): 501-528.
|
3697
|
+
| Johnson, C. N. 2009. Ecological consequences of Late Quaternary extinctions of
|
3698
|
+
| megafauna. Proceedings Of The Royal Society B-Biological Sciences
|
3699
|
+
| 276:2509-2519.
|
3700
|
+
| Kankam B.O. and W. Oduro . (2009). Frugivores and fruit removal of Antiaris
|
3701
|
+
| toxicaria (Moraceae) at Bia Biosphere Reserve, Ghana. J Trop. Ecol. 25: 201-
|
3702
|
+
| 204
|
3703
|
+
meta | 93
|
3704
|
+
blank |
|
3705
|
+
|
|
3706
|
+
|
|
3707
|
+
ref | Karban, R. and I.T. Baldwin. 1997. Induced responses to herbivory,: University of
|
3708
|
+
| Chicago Press, London, England.
|
3709
|
+
| Kira T. and H. Ogawa. 1971Assessment of primary production in tropical and
|
3710
|
+
| equatorial forests. Pages 309–321 in P. Duvigneaud, editor. Productivity of
|
3711
|
+
| Forest Ecosystems, UNESCO, Paris.
|
3712
|
+
| Kirika J.M., N. Farwig, and K. Böhning-Gaese. 2008. Effects of Local Disturbance of
|
3713
|
+
| Tropical Forests on Frugivores and Seed Removal of a Small-Seeded
|
3714
|
+
| Afrotropical Tree. Cons. Biol. 22(2): 318–328.
|
3715
|
+
| Kitajima, K. 2003. Impact of cotyledon and leaf removal on seedling survival in three
|
3716
|
+
| tree species with contrasting cotyledon functions. Biotropica 35(3): 429-434.
|
3717
|
+
| Koch, P. L. and A. D. Barnosky. 2006. Late quaternary extinctions: State of the
|
3718
|
+
| debate. Annual Review of Ecology Evolution and Systematics 37:215-250.
|
3719
|
+
| Leigh, E.G. Jr. G., Rand, and D.M. Winsor (Eds.) The Ecology of a Tropical Forest:
|
3720
|
+
| Seasonal Rhythms and Long-Term Changes, 2nd Ed. Smithsonian Institution
|
3721
|
+
| Press, Washington, D.C.
|
3722
|
+
| Lizcano, D.J. 2006. Ecology and conservation of large mammals in the Northern
|
3723
|
+
| Andes. Dissertation. Durrell Institute of Conservation and Ecology,
|
3724
|
+
| University of Kent, U.K.
|
3725
|
+
| Lucas P.W., I.M. Turner, N.J. Dominy and N. Yamashita. 2000. Mechanical defenses
|
3726
|
+
| to herbivory. Ann. Bot. 86: 913-920.
|
3727
|
+
| Mayfield, M.M., Boni, M.E., Daily G.C. and Ackerly, D.D. 2005. Species and
|
3728
|
+
| functional diversity of native and human-dominated plant communities.
|
3729
|
+
| Ecology 86(9): 2365-2372.
|
3730
|
+
| McConkey, K.M. and D.R. Drake. 2006. Flying foxes cease to function as seed
|
3731
|
+
| dispersers long before they become rare. Ecology. 87(2): 271-286.
|
3732
|
+
| McNaughton, S. J. 1985. Ecology of a grazing ecosystem: The Serengeti. Ecological
|
3733
|
+
| Monographs 55(3): 259-294.
|
3734
|
+
| Mendoza E. and R. Dirzo. 2007. Seed-size variation determines interspecific
|
3735
|
+
| differential predation by mammals in a neotropical rain forest. Oikos. 116(11):
|
3736
|
+
| 1841-1852.
|
3737
|
+
meta | 94 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3738
|
+
blank |
|
3739
|
+
|
|
3740
|
+
|
|
3741
|
+
ref | Moran C., C.P. Catterall and J. Kanowski. 2009. Reduced dispersal of native plant
|
3742
|
+
| species as a consequence of the reduced abundance of frugivore species in
|
3743
|
+
| fragmented rainforest. Biol. Cons. 142: 541-552.
|
3744
|
+
| Myers, J.A. and K. Kitajima. 2007. Carbohydrate storage enhances seedling shade
|
3745
|
+
| and stress tolerance in a neotropical forest. J. Ecol. 95: 383-395.
|
3746
|
+
| Nabeshima, E., M. Murakami, T. Hiura. 2001. Effects of herbivory and light
|
3747
|
+
| conditions on induced defense in Quercus crispula. Journal of Plant Research
|
3748
|
+
| 114(1116): 403-409.
|
3749
|
+
| Nuñez-Iturri, G. and H.F. Howe. 2007. Bushmeat and the fate of trees with seeds
|
3750
|
+
| dispersed by large primates in a lowland rain forest in Western Amazon.
|
3751
|
+
| Biotropica 39(3): 348-354.
|
3752
|
+
| Nuñez-Iturri, G., O. Olsson, H.F. Howe. 2008. Hunting reduces recruitment of
|
3753
|
+
| primate-dispersed trees in Amazonian Peru. Biol. Cons. 141: 1536-1546.
|
3754
|
+
| Oleksyn, J., P. Karolewski, M.J. Giertych, R. Zytkowiak, P.B. Reich, M.G. Tjoelker.
|
3755
|
+
| 1998. Primary and secondary host plants differ in leaf-level photosynthetic
|
3756
|
+
| response to herbivory: Evidence from Alnus and Betula grazed by the alder
|
3757
|
+
| beetle, Agelastica alni. New Phytologist 140(2): 239-249.
|
3758
|
+
| Osunkoya, O.O., J.E. Ash, A.W. Graham, and M.S. Hopkins. 1993. Growth of tree
|
3759
|
+
| seedlings in tropical rain forests of North Queensland, Australia. J. Trop. Ecol.
|
3760
|
+
| 9(1): 1-18.
|
3761
|
+
| Olff, H. and M. E. Ritchie. 1998. Effects of herbivores on grassland plant diversity.
|
3762
|
+
| Trends Ecol. Evol. 13(7): 261-265.
|
3763
|
+
| Pacheco L.F. and J.A. Simonetti. 2000. Genetic Structure of a Mimosoid Tree
|
3764
|
+
| Deprived of Its Seed Disperser, the Spider Monkey. Cons. Biol. 14(6): 1766-
|
3765
|
+
| 1755.
|
3766
|
+
| Pacheco, M.A.W. 2001. Effects of flooding and herbivores on variation in recruitment
|
3767
|
+
| of palms between habitats. J. Ecol. 89:, 358–366.
|
3768
|
+
| Parker, J.D., D.E. Burkepile, and M.E.Hay. 2006. Opposing effects of native and
|
3769
|
+
| exotic herbivores on plant invasions. Science. 311(5766): 1459-1461.
|
3770
|
+
meta | 95
|
3771
|
+
blank |
|
3772
|
+
|
|
3773
|
+
|
|
3774
|
+
ref | Peres, C. A., and M. van Roosmalen. 2002. Patterns of primate frugivory in Amazonia
|
3775
|
+
| and the Guianan shield: Implications to the demography of large-seeded plants
|
3776
|
+
| in overhunted tropical forests. Pages 407–423 in D. Levey,W. Silva, and M.
|
3777
|
+
| Galetti (Eds.). Seed dispersal and frugivory: Ecology, evolution and
|
3778
|
+
| conservation, CAB International, Oxford, UK.
|
3779
|
+
| Peres C.A. and E. Palacios. 2007. Basin-wide effects of game harvest on vertebrate
|
3780
|
+
| population densities in Amazonian Forests: Implications for animal-mediated
|
3781
|
+
| seed dispersal. Biotropica 39(3): 304-315.
|
3782
|
+
| Pimm, S., P. Raven, A. Peterson, C. H. Sekercioglu, and P. R. Ehrlich. 2006. Human
|
3783
|
+
| impacts on the rates of recent, present, and future bird extinctions. Proc Natl
|
3784
|
+
| Acad Sci U S A 103:10941-10946.
|
3785
|
+
| Pizo, M.A. and Vieira, E.M. 2004. Granivorous birds as potentially important post-
|
3786
|
+
| dispersal seed predators in a Brazilian forest fragment. Biotropica 36(3):
|
3787
|
+
| 417:423.
|
3788
|
+
| Poulsen, J. R., C. J. Clark, E. F. Connor, and T. B. Smith. 2002. Differential resource
|
3789
|
+
| use by primates and hornbills: Implications for seed dispersal. Ecology 83:
|
3790
|
+
| 228–240.
|
3791
|
+
| Rodriguez, C., E. Leoni, F. Lezama, and A. Altesor. 2003. Temporal trends in species
|
3792
|
+
| composition and plant traits in natural grasslands of Uruguay. J. of Veg. Sci.
|
3793
|
+
| 14(3): 433-440.
|
3794
|
+
| R Development Core Team. 2008. R: A language and environment for statistical
|
3795
|
+
| computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-
|
3796
|
+
| 900051-07-0, URL http://www.R-project.org.
|
3797
|
+
| Retuerto R., B. Fernandez-Lema, R. Rioloa, and J.R. Obeso. 2004. Increased
|
3798
|
+
| photosynthetic performance in holly trees infested by scale insects. Func.
|
3799
|
+
| Ecol. 18: 664-669.
|
3800
|
+
| Roldan, A.I. and J.A. Simonetti. 2001. Plant-mammal interactions in tropical Bolivian
|
3801
|
+
| forests with different hunting pressures. Cons. Bio. 15(3): 617-623.
|
3802
|
+
meta | 96 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3803
|
+
blank |
|
3804
|
+
|
|
3805
|
+
|
|
3806
|
+
ref | Royo, A. A. and W. P. Carson. 2005. The herb community of a tropical forest in
|
3807
|
+
| central Panama: dynamics and impact of mammalian herbivores. Oecologia
|
3808
|
+
| 145(1): 66-75.
|
3809
|
+
| Sagers C.L. and P.D. Coley. 1995. Benefits and costs of defense in a Neotropical
|
3810
|
+
| shrub. Ecology. 76(6) 1835-1843.
|
3811
|
+
| Sethi P. and H.F. Howe. 2009. Recruitment of Hornbill-Dispersed Trees in Hunted
|
3812
|
+
| and Logged Forests of the Indian Eastern Himalaya. Cons. Biol. 23(3): 710-
|
3813
|
+
| 718.
|
3814
|
+
| Shimazaki, A. and T. Miyashita. 2002. Deer browsing reduces leaf damage by
|
3815
|
+
| herbivorous insects through an induced response of the host plant. Ecol. Res.
|
3816
|
+
| 17(5): 527-533
|
3817
|
+
| Schipper, J. and J. S. Chanson and F. Chiozza and N. A. Cox and M. Hoffmann and V.
|
3818
|
+
| Katariya and J. Lamoreux and A. S. L. Rodrigues and S. N. Stuart and H. J.
|
3819
|
+
| Temple and J. Baillie and L. Boitani and T. E. Lacher and R. A. Mittermeier
|
3820
|
+
| and A. T. Smith and D. Absolon and J. M. Aguiar and G. Amori and N.
|
3821
|
+
| Bakkour and R. Baldi and R. J. Berridge and J. Bielby and P. A. Black and J. J.
|
3822
|
+
| Blanc and T. M. Brooks and J. A. Burton and T. M. Butynski and G. Catullo
|
3823
|
+
| and R. Chapman and Z. Cokeliss and B. Collen and J. Conroy and J. G. Cooke
|
3824
|
+
| and G. A. B. da Fonseca and A. E. Derocher and H. T. Dublin and J. W.
|
3825
|
+
| Duckworth and L. Emmons and R. H. Emslie and M. Festa-Bianchet and M.
|
3826
|
+
| Foster and S. Foster and D. L. Garshelis and C. Gates and M. Gimenez-Dixon
|
3827
|
+
| and S. Gonzalez and J. F. Gonzalez-Maya and T. C. Good and G. Hammerson
|
3828
|
+
| and P. S. Hammond and D. Happold and M. Happold and J. Hare and R. B.
|
3829
|
+
| Harris and C. E. Hawkins and M. Haywood and L. R. Heaney and S. Hedges
|
3830
|
+
| and K. M. Helgen and C. Hilton-Taylor and S. A. Hussain and N. Ishii and T.
|
3831
|
+
| A. Jefferson and R. K. B. Jenkins and C. H. Johnston and M. Keith and J.
|
3832
|
+
| Kingdon and D. H. Knox and K. M. Kovacs and P. Langhammer and K. Leus
|
3833
|
+
| and R. Lewison and G. Lichtenstein and L. F. Lowry and Z. Macavoy and G.
|
3834
|
+
| M. Mace and D. P. Mallon and M. Masi and M. W. McKnight and R. A.
|
3835
|
+
| Medellin and P. Medici and G. Mills and P. D. Moehlman and S. Molur and A.
|
3836
|
+
meta | 97
|
3837
|
+
blank |
|
3838
|
+
|
|
3839
|
+
|
|
3840
|
+
ref | Mora and K. Nowell and J. F. Oates and W. Olech and W. R. L. Oliver and M.
|
3841
|
+
| Oprea and B. D. Patterson and W. F. Perrin and B. A. Polidoro and C. Pollock
|
3842
|
+
| and A. Powel and Y. Protas and P. Racey and J. Ragle and P. Ramani and G.
|
3843
|
+
| Rathbun and R. R. Reeves and S. B. Reilly and J. E. Reynolds and C.
|
3844
|
+
| Rondinini and R. G. Rosell-Ambal and M. Rulli and A. B. Rylands and S.
|
3845
|
+
| Savini and C. J. Schank and W. Sechrest and C. Self-Sullivan and A.
|
3846
|
+
| Shoemaker and C. Sillero-Zubiri and N. De Silva and D. E. Smith and C.
|
3847
|
+
| Srinivasulu and P. J. Stephenson and N. van Strien and B. K. Talukdar and B.
|
3848
|
+
| L. Taylor and R. Timmins and D. G. Tirira and M. F. Tognelli and K.
|
3849
|
+
| Tsytsulina and L. M. Veiga and J. C. Vie and E. A. Williamson and S. A.
|
3850
|
+
| Wyatt and Y. Xie and B. E. Young. 2008. The status of the world's land and
|
3851
|
+
| marine mammals: Diversity, threat, and knowledge. Science 322:225-230.
|
3852
|
+
| Sork, V.L. 1987. Effects of predation and light on seedling establishment in Gustavia
|
3853
|
+
| superba. Ecology 68(5):1341-1350.
|
3854
|
+
| Strauss, S. Y. and A. A. Agrawal. 1999. The ecology and evolution of plant tolerance
|
3855
|
+
| to herbivory. Trends Ecol. Evol. 14(5): 179-185.
|
3856
|
+
| Stoner, K.E., K. Vulinec, S.J. Wright, and C.A. Peres. 2007. Hunting and plant
|
3857
|
+
| community dynamics in tropical forests: A synthesis and future directions.
|
3858
|
+
| Biotropica 39(3): 385–392.
|
3859
|
+
| Terborgh, J. and S.J. Wright. 1994. Effects of mammalian herbivores on plant
|
3860
|
+
| recruitment in two Neotropical forests. Ecology 75(6): 1829-1833.
|
3861
|
+
| Terborgh J., K. Feeley, M. Silman, P. Nuñez, B. Balukjian. 2006. Vegetation
|
3862
|
+
| dynamics of predator-free land-bridge islands. J. Ecol. 94: 253–263.
|
3863
|
+
| Terborgh, J., G. Nuñez-Iturri, N.C.A. Pitman, F.H. Cornejo Valverde, P. Alvarez, V.
|
3864
|
+
| Swamy, E.G. Pringle, and C.E.T. Paine. 2008. Tree recruitment in an empty
|
3865
|
+
| forest. Ecology. 89(6):1757–1768.
|
3866
|
+
| Wang, B. C., V.L. Sork, M.T. Leong, T.B. Smith. 2007. Hunting of mammals reduces
|
3867
|
+
| seed removal and dispersal of the Afrotropical tree Antrocaryon klaineanum
|
3868
|
+
| (Anacardiaceae). Biotropica 39(3): 340-347.
|
3869
|
+
meta | 98 CHAPTER 4: SEED PREDATION RATES AS A FUNCTION OF SEED SIZE AND DEFAUNATION
|
3870
|
+
blank |
|
3871
|
+
|
|
3872
|
+
|
|
3873
|
+
ref | Ward, D. and T. P. Young. 2002. Effects of large mammalian herbivores and ant
|
3874
|
+
| symbionts on condensed tannins of Acacia drepanolobium in Kenya. J. Chem.
|
3875
|
+
| Ecol. 28(5): 921-937.
|
3876
|
+
| Wardle, D. A., K. I. Bonner, and G.M. Barker. 2002. Linkages between plant litter
|
3877
|
+
| decomposition, litter quality, and vegetation responses to herbivores. Func.
|
3878
|
+
| Ecol. 16(5): 585-595.
|
3879
|
+
| Webb, C. O. and D. R. Peart. 1999. Seedling density dependence promotes
|
3880
|
+
| coexistence of Bornean rain forest trees. Ecology 80(6): 2006-2017.
|
3881
|
+
| Webb, S. 2008. Megafauna demography and late Quaternary climatic change in
|
3882
|
+
| Australia: A predisposition to extinction. Boreas 37:329-345.
|
3883
|
+
| Weiher, E. and P. Keddy. 1995. Assembly rules, null models, and trait dispersion:
|
3884
|
+
| New questions from old patterns. Oikos 74(1): 159-164.
|
3885
|
+
| Wilson, D.E., F.R. Cole, J.D. Nichols, R. Rudran, and M.S. Foster. 1996. Measuring
|
3886
|
+
| and Monitoring Biological Diversity: Standard Methods for Mammals.
|
3887
|
+
| Smithsonian Institution Press, Washington, D.C.
|
3888
|
+
| Wright, I.J, D.D. Ackerly, F. Bongers, K.E. Harms, G. Ibarra-Manriquez, M. Matinez-
|
3889
|
+
| Ramos, S.J. Mazer, H.C. Muller-Landau, H. Paz, N.C. Pitman, L. Poorter,
|
3890
|
+
| M.R. Silman, C.F. Vriesendorp, C.O. Webb, M. Westoby, S.J. Wright. 2007.
|
3891
|
+
| Relationships among ecologically important dimensions of plant trait variation
|
3892
|
+
| in seven Neotropical forests. Ann. Bot. 99: 1003-1015.
|
3893
|
+
| Wright, S.J., H. Zeballos, I. Dominguez, M.M. Gallardo, M.C. Moreno and R. Ibanez.
|
3894
|
+
| 2000. Poachers alter mammal abundance, seed dispersal, and seed predation in
|
3895
|
+
| a Neotropical forest. Cons. Bio. 14(1): 227-239.
|
3896
|
+
| Wright, S.J and H.C. Duber. 2001. Poachers and forest fragmentation alter seed
|
3897
|
+
| dispersal, seedling survival, and seedling recruitment in the palm Attalea
|
3898
|
+
| butyracea, with implications for tropical tree diversity. Biotropica 33(4):
|
3899
|
+
| 583:595.
|
3900
|
+
| Wright, S.J. 2003. The myriad consequences of hunting for vertebrates and plants in
|
3901
|
+
| tropical forests. Pers. in Plant Ecol. Evol. Sys. 6(1-2): 78-86.
|
3902
|
+
meta | 99
|
3903
|
+
blank |
|
3904
|
+
|
|
3905
|
+
|
|
3906
|
+
ref | Wright, S.J., A. Hernandéz, and R.Condit. 2007. The bush meat harvest alters seedling
|
3907
|
+
| banks by favoring lianas, large seeds and seeds dispersed by bats, birds and
|
3908
|
+
| wind. Biotropica 39(3): 363-371.
|
3909
|
+
| Wright, S.J., K. Kitajima, N.J.B. Kraft, P.B. Reich4, I.J. Wright, D.E. Bunker, R.
|
3910
|
+
| Condit, J.W. Dalling, S.J. Davies, S. Díaz, B.M.J. Engelbrecht, K.E. Harms, S.P.
|
3911
|
+
| Hubbell, C.O. Marks, Maria C. Ruiz-Jaen, C.M. Salvador and A.E. Zanne. 2010.
|
3912
|
+
| Functional traits and the growth-mortality tradeoff in tropical trees. In press.
|
3913
|
+
| Ecology. [doi:10.1890/09-2335.1]
|
3914
|
+
| Young, T. P. and B. D. Okello. 1998. Relaxation of an induced defense after exclusion
|
3915
|
+
| of herbivores: Spines on Acacia drepanolobium. Oecologia 115(4): 508-513.
|
3916
|
+
| Zimov, S. A., V. I. Chuprynin, A. P. Oreshko, F. S. Chapin, J. F. Reynolds, and M. C.
|
3917
|
+
| Chapin. 1995. Steppe-tundra transition: a herbivore-driven biome shift at the
|
3918
|
+
| end of the Pleistocene. American Naturalist 146:765-794.
|
3919
|
+
blank |
|