ArticlePDF Available

Overfishing disrupts an ancient mutualism between frugivorous fishes and plants in Neotropical wetlands

Authors:

Figures

Content may be subject to copyright.
Overshing disrupts an ancient mutualism between frugivorous shes
and plants in Neotropical wetlands
Sandra Bibiana Correa
a
, Joisiane K. Araujo
b
, Jerry M.F. Penha
b
,CatiaNunesdaCunha
b
,
Pablo R. Stevenson
c
,JillT.Anderson
a,
a
Department of Genetics, Odum School of Ecology, University of Georgia, 120 Green St., Athens, GA 30602, USA
b
Instituto de Biociências, Universidade Federal de Mato Grosso, Ave. Fernando Correia 2367, Cuiabá, MT, Brazil
c
Departamento de Ciencias Biológicas, Universidad de los Andes, Carrera 1 No. 18A-12,Bogotá, Colombia
abstractarticle info
Article history:
Received 7 May 2015
Received in revised form 13 June 2015
Accepted 14 June 2015
Available online xxxx
Keywords:
Seed dispersal
Defaunation
Flooded forest
Flooded savannah
Amazon
Pantanal
Defaunation is disrupting plantanimal interactions worldwide. The overhunting of frugivores disrupts seed
dispersal and diminishesplant regeneration, yet investigations of frugivoreoverexploitation neglect anancient
guild: fruit-eating sh. For nearly ve decades, Neotropical frugivorous shes have been intensively harvested.
These shing activities have reduced population sizes of some species by up to 90% and have likely altered
populations to younger, smaller individuals. Here we evaluate potential ecological consequences of overshing
frugivores for seed dispersal and recruitment dynamics. We analyzed dietary data from seven fruit-eating sh
species in Amazonian and Pantanal wetlands to test the hypothesis that seed dispersal effectiveness increases
with sh size within and across species. Relative to small individuals, larger sh dispersed large numbers of
seeds of a higher diversity of plants and a greater range of seed sizes. For some seed species, dispersal by larger
sh augmented germination success, relative to seeds dispersed by smaller shes. Large Piaractus mesopotamicus
in the Pantanal disperse seeds of 27% more speciesthan shes under the minimum size limit for this shery.Our
results indicate that the ongoing overexploitation of multiple frugivorous sh species coulddepress the quantity
and diversity of seeds dispersed, as well as the quality of seed dispersal in wetland habitats that extend over 15%
of the area of South America.
© 2015 Elsevier Ltd. All rights reserved.
1. Introduction
The disruption of pollination and seed dispersal mutualisms directly
affects plant reproductive success and threatens biodiversity (Aslan
et al., 2013; Dirzo et al., 2014; Valiente-Banuet et al., 2015). The vast
majority of plants rely on animals to disperse their genes and progeny
(Jordano, 2000; Ollerton et al., 2011). Forexample, vertebrate frugivores
disperse the seeds of 7095% of woody plant species in tropical forests
(e.g., Jordano, 2000). Seed dispersal sets the initial template of plant dis-
tribution in the landscape, shapes the pool of interacting plant species,
and potentially facilitates species coexistence through competition/
colonization tradeoffs (Howe and Smallwood, 1982; Seidler and
Plotkin, 2006).
Frugivorous vertebrates are overhunted in tropical forests across the
globe, which reduces plant recruitment, alters plant species composi-
tion, diminishes biodiversity, and causes numerous indirect changes to
communities (Caughlin et al., 2015; Markl et al., 2012; Poulsen et al.,
2013). As hunters prefer big prey, overharvesting is particularly
problematic for large-seeded plant species, which require seed dispersal
by sizable frugivores (Caughlin et al., 2015; Efom et al., 2014). Local
extinction of large frugivores can even induce rapid evolutionary changes
in seed size (Galetti et al., 2013). A burgeoning body of work evaluates the
ecological repercussions of hunting frugivores (Aslan et al., 2013), but
neglects the largest clade of vertebrates: sh.
Worldwide, over 275 species of sh consume fruits and disperse
seeds; of these, at least 150 inhabit South American wetlands (Horn
et al., 2011), where they disperse seeds of at least 566 plant species
from 82 families (Correa et al., 2015). Neotropical wetlands extend
across eight countries and the three largest South American river basins
(Amazon, Orinoco, and ParanáParaguay), occupying at least 15% of
the continent (Junk and Piedade, 2010). Fruiting is synchronized with
the annual ood, lasting up to seven months, and many fruits and
seeds exhibit adaptations for dispersal by water (hydrochory) or sh
(ichthyochory; Ferreira et al., 2010; Kubitzki and Ziburski, 1994).
During lengthy ooded seasons, shes spend ~87% of their time in
oodplain habitats (Anderson et al., 2011) where seeds can germinate
after oodwaters recede (Ferreira et al., 2010).
Globally, selective harvesting of sh concentrates on large individ-
uals, inducing changes in population structure by favoring the survival
of smaller shes that reproduce earlier (Allan et al., 2005; Palkovacs,
Biological Conservation 191 (2015) 159167
Corresponding author: Tel.: +1 706 542 0853.
E-mail address: jta24@uga.edu (J.T. Anderson).
http://dx.doi.org/10.1016/j.biocon.2015.06.019
0006-3207/© 2015 Elsevier Ltd. All rights reserved.
Contents lists available at ScienceDirect
Biological Conservation
journal homepage: www.elsevier.com/locate/bioc
2011). A shery-induced reduction in body size of frugivorous species
would have profound effects on plant regeneration if larger shes are
better seed dispersers than smaller shes (Anderson et al., 2011;
Correa et al., 2015; Galetti et al., 2008; Kubitzki and Ziburski, 1994).
Large Neotropical frugivorous shes are prized in commercial, subsis-
tence, and recreational sheries, and are threatened by ongoing overex-
ploitation (Isaac and Rufno, 1996; Peixer et al., 2007). Frugivorous
shes are heavily consumed in the Amazon, Orinocoand Pantanal, con-
tributingto food security andeconomic growth (Barthem and Goulding,
2007; Mateus et al., 2004; Rodriguez et al., 2007). Intensive commercial
sheries developed in the 1970s across the Amazon and Pantanal with
the introduction of nylon gill nets and large capacity freezer rooms
(Mateus et al., 2004; Santos and Santos, 2005). By the early 1990s,
stocks of Colossoma macropomum in the Central Amazon were already
overexploited (Isaac and Rufno, 1996) and commercial and recrea-
tional shing activities have reduced population sizes of Piaractus
mesopotamicus in the Pantanal by 90% (Albuquerque et al., 2012;
Peixer et al., 2007). In addition to population declines, overshing likely
has shifted body size of these species to smaller individuals that repro-
duce earlier (Palkovacs, 2011), however the lack of basin-wide continu-
ous historic shery statistics (Mateus et al., 2004; Rufno, 2008)hinders
our ability to assess changes in population structure of overexploited
populations. Striking population declines in other large species such as
catshes have shifted shing pressure to under-exploited stocks of
large frugivorous shes in remote locations (Agudelo et al., 2012;
Albuquerque et al., 2012; Mateus et al., 2004; Reinert and Winter,
2002). Small- and medium-sized frugivorous sh species are also inten-
sively exploited in the Amazon and Pantanal (Mateus et al., 2004;
Santos and Santos, 2005). These species are heavily consumed by river-
ine people; therefore, a large portion of the capture is not accounted for
in commercial shery statistics, leading to an underestimation of the
real shing pressure (Castello et al., 2013).
Here, we examine the ecological consequences of overshing in two
expansive and diverse Neotropical wetlands: the Pantanal and the
Amazon. In both regions, we predict that the largest shes disperse
more seeds of a greater diversity of plant species, and that large-
bodied sh species are among the primary vectors of dispersal for
plant species with big seeds (e.g., Stevenson, 2011). Additionally, we
examine size-dependent shifts in seed predation, testing the prediction
that larger shes depredate fewer seeds than smaller individuals. In a
preliminary analysis, Correa et al. (2015) found that smaller shes had
a greater probability of destroying seeds than larger shes across
three species of Brycon, presumably because big shes are more adept
at swallowing eshy fruits entire. Finally, we tested whether seed
germination success increases with sh size in a greenhouse experiment.
Overexploitation could fundamentally alter shfruit interactions
from high quality seed dispersal by large shes to greater rates of seed
predation by smaller shes.
2. Materials AND Methods
2.1. Study areas
2.1.1. Brazilian Pantanal
Spanning over 160 000 km
2
, the Pantanal is one of the largest
tropical wetlands in the world (Junk and Nunes da Cunha, 2005). We
conducted our study in the SESC Pantanal Private Natural Heritage
Reserve (1063 km
2
;16°3051S, 56°2238W; Fig. 1b) in the northern
Pantanal. The Pantanal Reserve constitutes a mosaic of seasonally
ooded savannas with small patches of semi-deciduous mono-
dominant forests of cambará (Vochysia divergens, Vochysiaceae) and
gallery forests. Tree diversity in forests is low (up to 10 species with
dbh N10 cm per 0.1 ha; Arieira et al., 2011)andtheooding regime is
moderate (2 m depth for 5 months annually, Junk and Nunes da
Cunha, 2005).
2.1.2. Colombian Amazon
The lowlands of the Amazon River and its tributaries contain vast
expanses of seasonally ooded forests. Amazonian oodplains cover
approximately 250000 km
2
, constituting the largest wetland on earth
(Junk, 1993). We sampled the lower Caquetá River (1°1632S, 69°43
50W; Fig. 1a), where the oodplain supports a continuous, relatively
undisturbed evergreen forest with high tree diversity (up to 54species
with dbh N10 cm per 0.1 ha; Duivenvoorden, 1996) that oods up to
9mdepthfor6monthsannually(Rodriguez, 1991).
2.2. Fish sampling
To sample frugivorous shes of varying sizes, we baited hooks of
different sizes with ripe local fruits, as well as with dough made of
cooked manioc our and articial fruit avors, and shed with pole
and line. In the Amazon, hooks were also suspended from vegetation
in the ooded forest and monitored hourly (Correa and Winemiller,
2014), which is not feasible in the Pantanal due to abundant Caiman
populations. Our sampling selectively captures fruit-eating sh species
(Correa and Winemiller, 2014). Immediately after removal from the
hook, we euthanized shes with Tricaine methanesulfonate (MS-222).
We recorded species identity, standard length (SLlength from the tip
of the snout to the posterior end of the hypural bones, excluding the
caudal n), weight, and mouth gape of the sh, and collected stomach
and intestinal samples by dissection. This research complies with
animal use guidelines (AUP# 2194-100789-011314).
In the Pantanal, we sampled shes in four habitats (river channels,
savannas, mono-dominant and gallery forests) during the ooding
season of 2014 (FebruaryMay) for a total of n= 374 individuals of
four species (Serrasalmidae: P. mesopotamicus,n=217,1459 cm SL;
Mylossoma duriventre,n= 50, 1121 cm SL; Myloplus tiete,n=40,
1116 cm SL. Characidae: Brycon hilarii,n=67, 1136 cm SL; Fig. 2).
In the Amazon, we sampled shes in three oodplain forest habitats
(river channels, islands within the river channel, and oodplain
channels) during the peak ooding (JuneAugust 2014) for a total of
n= 285 individuals of four species(Serrasalmidae: Myloplus torquatus,
n=69,1228 cm SL; M. duriventre,n=34,1527 cm SL. Characidae:
Brycon amazonicus,n= 52, 2335 cm SL; Brycon melanopterus,n=
130, 1227 cm SL; Fig. 2). These sample sizes exclude shes with
empty digestive tracts (n= 20 in the Pantanal and n= 6 in the Ama-
zon). Fish nomenclature follows Reis et al. (2003).
2.3. Diet estimation
We separated stomach (excluding bait) and intestinal contents into
food categories (intact seeds, masticated seeds, and fruit pulp), calculat-
ed the volume of each category by water displacement, and identied
and quantied intact seeds. Intact seeds pass through the digestive
system undamaged, and are likely viable, whereas masticated seeds
are destroyed during consumption and digestion. We measured length
and width of at least 3 intact seeds per taxa when possible.
To assess the number of species fruiting during the ooded season,
we established 100 m long × 10 m wide transects in all sampled habitat
types: savanna (n= 3), mono-dominant (n= 3) and gallery forest
(n= 4) in the Pantanal; and oodplain forest parallel (n=5)andper-
pendicular to the rivers' edge (n= 3) and along oodplain channels
(n= 2) in the Amazon. Biweekly, we recorded the number of plants
per species with ripe and immature fruits. Botanical vouchers were de-
posited at the Herbarium of the Universidade Federal de Mato Grosso,
Cuiabá, Brazil and the Colombian Amazon Herbarium (COAH),
Colombia. Plant nomenclature follows Angiosperm Phylogeny Group
and Tropicos (http://www.tropicos.org).
We tested the hypothesis that seed dispersal effectiveness increases
with sh size within and across sh species using four metrics of
dispersal quality and quantity: (1) proportion of intact to total seed
matter (the probability of dispersing rather than destroying seeds),
160 S.B. Correa et al. / Biological Conservation 191 (2015) 159167
(2) number of seeds, (3) seed species richness, and (4) seed size. We
modeled these response variables as a function of individual sh body
size (SL), sh species, and the size by species interaction. When the
interaction was non-signicant, we removed it. We analyzed these
four response variables separately because of differentstatistical distri-
butions, and sites separately because of differences in sh and plant
species compositions between the Pantanal and Amazon. We adjusted
probability values for multiple tests of the same dataset (Pantanal vs.
Amazon) using the Benjamin and Hochberg (1995) correction. Models
were implemented in R (version 3.1.2).
To test if the probability of dispersing seeds increases with sh size,
we calculated the proportion of seeds that were intact in the digestive
tract of each sh relative to total seed matter (intact seed volume:
intact + masticated seed volume), which is directly related to the
probability of seed predation (seed predation = 1 seed dispersal).
Fishes with entirely masticated seeds had values of 0, whereas shes
with entirely intact seeds had values of 1. We limited this analysis to
shes with seed matter (intact ormasticated) in their digestive contents
(n=325shes of 4 species inthe Pantanal, and 261 shes of 4 species
in the Amazon). We implemented zero-one inated beta models in
GAMLSS (version 4.3-1 Rigby and Stasinopoulos, 2005) with the BEINF
family to test the proportion of intact seeds as a function of sh size
(SL), sh species, and the interaction. Zero-one inated beta regression
analyzes proportions as a mixture of Bernoulli and beta distributions,
and is the only approach currently capable of accommodating propor-
tional data that include values of 0 and 1, i.e., on the interval [0,1].
These models simultaneously estimate 3 parameters: (1) the probabili-
ty that this proportion has a valueof 0 (nu); (2) the expected value for
the beta component (values between 0 and 1, mu); and (3) the proba-
bility that this proportion has a value of 1 (tau). If larger shes are better
seed dispersers, we expect negative relationships between sh size and
nu (the probability that digestive contents contained 0 intact seeds),
and positive relationships between sh size and mu (proportions
between 0 and 1) and tau (probability that digestive contents contained
only intact seeds).
We then restricted the datasets to individuals with intact seeds in
their digestive contents to assess the quantity and quality of dispersal
among shes serving as seed dispersers (n=229shes of 4 species in
the Pantanal, and 157 shes of 4 species in the Amazon). The number
of intact seeds in sh digestive tracts was modeled with a quasipoisson
regression, which tted the data better than a Poisson model given
overdispersion in the dataset. We analyzed seed species richness with
Fig. 1. Map of the study sites. (a) RíoCaquetá, Amazonas,Colombia, Northwestern Amazonia. Samplingwas conducted betweenthe conuence with the Río Mirití (A) and the oodplain
forest below the Córdoba rapids (B). (b) Reserva Particular do Patrimônio Natural (RPPN) SESC Pantanal, Mato Grosso, Brazil, Northern Pantanal. Sampling was conducted in Riozinho
(C) and the Rio Cuiabá (D). Dark green areas in (b) are monodominant forests of Vochysia divergens. Satellite images were retrieved from ESRI. (For interpretation of the references to
color in this gure legend, the reader is referred to the web version of this article.)
161S.B. Correa et al. / Biological Conservation 191 (2015) 159167
a Poisson regression of the number of seed species present in individual
gut contents. Finally, since gape size constrains the size of the seeds that
a frugivore can consume (Wheelwright, 1985), we hypothesized that
large shes are unique vectors of dispersal for the biggest seeds. We
calculated the size (length × width) of the largest intact seed in the
digestive tract of each sh to estimate the upper bound of seed sizes
that a sh can consume. Mouth gape was tightly correlated with body
length (R
2
=0.89,F
1,526
=4092,pb0.0001) across our 7 sh species;
therefore, we used sh size as a proxy for gape size to test the hypothesis
that the size of dispersed seeds increases with sh size. Since large shes
can swallow both small and large seeds, heterogeneity in seed size
increased with sh size in our datasets; therefore, we conducted a
generalized least squares regression in which variance in seed size is
proportional to sh size (Zuur et al., 2009) in the R package nlme
(version 3.1-118, Pinheiro et al., 2014).
2.4. Germination experiment
To test whether shes enhance germination, we conducted a
greenhouse experiment comparing seeds removed from sh digestive
tracts vs. local control seeds without fruit pulp. Removing the pulp
from control seeds tested if (1) sh consumption increases germination
success via scarication, in which case gut-processed seeds should have
a greater probability of germinating than control seeds or (2) sh
consumption inuences germination simply by eliminating fruit pulp,
in which case gut-processed seeds should have equivalent germination
success as control seeds (Traveset et al., 2008). We randomly planted
individual seeds of the most abundant species in sh diets at each
site (Pantanal: 11 species, total n= 1660; Amazon: 5 species, total
n= 746; see Appendix A for additional details) into pots with 40, 60
or 80 mL of soil, depending on seed size. Pots were lled with commer-
cial potting soil for forest plants (Pantanal) or local forest soil that was
sieved to remove seeds and large debris (Amazon). Trays were housed
in a screened greenhouse (50% shade) at each eld site. We monitored
seeds for germination daily (Pantanal: 8 months, Amazon: 6 months)
and watered as needed.
We conducted a logistic regression to test the effects of seed species,
treatment (de-pulped control seeds vs. gut treatment by sh) and
their interaction on germination success in separate analyses for
the Pantanal and Amazon datasets (Proc Logistic, SAS ver. 9.3). Owing
to quasi-separation of data points, we used a penalized likelihood
method (Firth, 1993). A second logistic regression examined
whether germination success of seeds processed by sh increased
with sh size.
Fig. 2. Variation in body size across species in local assemblages of frugivorous sh species in the Pantanal (MtMyloplus tiete,MdMylossoma duriventre,BhBrycon hilarii, and
PmPiaractus mesopotamicus) and Amazon (MdMylossoma duriventre,MtqMyloplus torquatus,BmBrycon melanopterus, and BaBrycon amazonicus). Photographs represent the
largest adult individuals per species captured during the study, except for Piaractus mesopotamicus (largest individual: 59 cm SL) and Mylossoma duriventre in the Amazon (largest
individual: 27 cm SL). SLstandard length. Photos by S.B. Correa and J.K. Araujo.
162 S.B. Correa et al. / Biological Conservation 191 (2015) 159167
3. Results
We found 42938 intact seeds of 53 species in the digestive tracts
of 229 individual shes in the Pantanal and 150624 intact seeds of
70 species in the digestive tracts of 163 shes in the Amazon (see
Appendix B for additional details). Fishes dispersed 52% and 14% of
the eshy-fruited plant species recorded during vegetation transects
in the Pantanal and Amazon, respectively (Appendix C). However,
several seed species found intact in sh guts were not observed in
the vegetation transects (Pantanal: 11 species, Amazon: 54 species;
Appendix BC), suggesting that these highly mobile shes may have
consumed fruits in distant wetlands (Anderson et al., 2011). A single
sh carried up to 3554 (mean seed length and width =
5.5 mm × Proc Logistic, SAS 4.8 mm; sh size: 40.5 cm SL) and 8386
(mean seed length and width = 4.4 mm × 2.0 mm; sh size: 23 cm
SL) seeds in its digestive tract, in the Pantanal and Amazon, respectively.
Fish-dispersed seeds ranged in size from 0.8 mm × 0.6 mm (Banara
arguta, Flacourtiaceae) to 40.7 mm × 19.6 mm (Couepia uiti,
Chrysobalanaceae) in the Pantanal, and 0.6 mm × 0.5 mm (Ficus sp.
Moraceae) to 27.1 mm × 11.9 mm (Pouteria sp., Sapotaceaceae) in the
Amazon. In the Pantanal and Amazon, shes dispersed 10 and 12 large-
seeded species (N10 mm wide, Stevenson, 2011), respectively.
3.1. Seed dispersal effectiveness
Concordant with predictions, the probability of dispersing intact
seeds increased with body size (see Appendix D for full model results).
We observed the expected negative relationship between sh size and
the probability a sh destroyed all consumed seeds (nu) fortwo species:
a 1 cm increase in sh standard length decreased the odds of complete
seed mastication (nu)by6.6%forP. mesopotamicus in the Pantanal (95%
CI: 2.6, 10.3; padjusted for multiple tests = 0.008) and by 28.0% for
B. melanopterus in the Amazon (95% CI: 9.1, 43.0; adjusted p=0.028).
Furthermore, we observed the expected positive relationship between
sh size and mu [volume of intact to total seeds on the interval (0,1)]
for three species: a 1 cm increase in sh standard length increased the
odds of seed dispersal (mu)by2.7%forP. mesopotamicus in the Pantanal
(95% CI: 0.74%, 4.77%; adjusted p= 0.031; Fig. 3a) and by 58.0%
for B. amazonicus in the Amazon (95% CI: 11.3%, 125.4%; adjusted
p=0.035, Fig. 3b). M. torquatus followed a similar overall pattern
(Fig. 3c), but the p-value was non-signicant after correctionfor multi-
ple tests (raw p= 0.034, adjusted p=0.081).
The abundance, species richness and size of dispersed seeds in-
creased with sh size in both wetlands. In the Pantanal, larger shes dis-
persed more seeds (Fig. 4a, Appendix E) irrespective of sh species
(SL × species, F
3,221
. = 0.65, p= 0.59). In the Amazon, a 1 cm increase
in standard length increased the number of intact seeds by 1.18 (95%
CI: 1.02, 1.35; p= 0.026) for M. torquatus (Fig. 4b), but there was no re-
lationship between sh size and intact seed abundance for
B. amazonicus,B. melanopterus and M. duriventre (SL × species,
F
3,149
= 4.76, adjusted p= 0.021). In both wetlands, the species rich-
ness of dispersed seeds increased with sh size (Fig. 4c, d; Appendix
E), independent of sh species (SL × species, Pantanal: F
3,221
= 0.11,
p=0.95;Amazon:F
1,149
=1.79,p= 0.15), as did the size of dispersed
seeds (Fig. 4e, f; Appendix E; SL × species, Pantanal: F
3,221
=0.71,p=
0.55; Amazon: F
3,149
= 0.85, p=0.47).
In the Pantanal, the effect of treatment (de-pulped control seeds vs.
gut treatment by sh) on germination success differed across seed spe-
cies (seed species × treatment: χ
2
=32.96,p= 0.048; Appendix F). For
8 of 11 seed species, there was no difference in germination success be-
tween seed treatments. For B. arguta (Flacourtiaceae), control seeds
were more likely to germinate than those dispersed by B. hilarii.For
Duroia duckei (Rubiaceae) and Mouriri guianensis (Melastomataceae),
control seeds had higher germination success than those dispersed
by P. mesopotamicus, but not those dispersed by other sh species
(Appendix F). When we analyzed the effect of sh size on germination
success of sh-ingested seeds, we found that larger shes increased
the odds of germination for four out of 11 seed species (Fig. 5,sh
size × seed species: χ
2
= 29.95, p= 0.001; Appendix GH), and there
was no relationship between germination success and sh size for the
remaining 7 species.
In the Amazon, germination success differed between seed species
(χ
2
= 23.04, p= 0.0001), but did not differ between seed treatment
(gut passage by various sh species vs. control seeds: χ
2
= 5.07,
p= 0.17). Nor did we nd evidence for a seed species by treatment
interaction (χ
2
=4.79,p= 0.44; Appendix F); therefore, in the
Amazon, shes neither enhance nor depress seed germination success
relative to seeds removed from fruit pulp manually. However, when
we assessed the effect of sh size on germination of sh-ingested
Fig. 3. Proportion of dispersedseeds [volume of intact to total seeds on the interval (01),
mu] modeled as a function of sh size (SLstandard length). Pantanal: (a) Piaractus
mesopotamicus. Amazon: (b) Brycon amazonicus, and (c) Myloplus torquatus.
163S.B. Correa et al. / Biological Conservation 191 (2015) 159167
seeds, we found that a 1 cm increase in standard length enhanced the
odds of germination by 16.7% (95% CI: 431%, χ
2
= 6.9, p= 0.009;
Fig. 6). This effect held across seed species, as we found no signicant
interaction between sh size and seed species (sh size × seed species:
χ
2
=5.92,p=0.21).
4. Discussion
Seed dispersal effectiveness increased with sh body size in two
distinct regions with different ora, fauna and landscape features. At
any given time, shes hadaccess to multiple species of fruits of variable
morphologies (Appendix B). In addition, the species composition of
fruits changed across the season in both regions; fruits available to sh-
es captured early in the season were different from those available to
shes captured late in the season (Correa et al., in prep.). Despite the
variability in the diets of individual sh sampled in different habitats
at different times, we found remarkably consistent results in the
Pantanaland Amazon: relative to small individuals, bigger shes masti-
cated a lower proportion of the seeds they consume, instead dispersing
larger numbers of intact seeds of a greater plant diversity and of a wider
range of seed-sizes.
Furthermore, big shes enhanced germination success across
multiple seed species. Frugivores inuence the probability of seed
germination by removing the pulp and/or scarifying the seed coat
Fig. 4. Abundance, diversity and maximum size of intact seeds dispersed by shes in two Neotropical wetlands(Pantanal: a, c, e; Amazon: b, d, f) modeled as a function of sh size
(SLstandard length). pvalues were corrected for multiple comparisons per data set. Black bars represent the range of body sizes per species of individuals included in the analyses.
Species codes follow those in Fig. 2.
164 S.B. Correa et al. / Biological Conservation 191 (2015) 159167
(Traveset et al., 2008). In our study, ingestion by shes did not augment
or inhibit germination for most seed species relative to manually de-
pulped seeds, suggesting that sh consumption inuences germination
simply by eliminating fruit pulp. However, germination success of
multiple seed species increased with sh size. This positive relationship
between germination success and sh size could be related to longer
retention time in larger intestinal tracts, as intestinal length increases
with sh body size in all of our focal sh species except M. tiete
(R
2
=0.91,F
13,444
=341.4,pb0.0001). Laboratory experiments feeding
seeds of various species to shes of different body sizes could help elu-
cidate possible physical or chemical changes to seed coats in response to
longer retention times (Pollux, 2011; Traveset et al., 2008).
Effective seed dispersal enhances seedling recruitment and directly
contributes to plant community structure (Jordano, 2000; Wang and
Smith, 2002). Most studies assessing seed dispersal effectiveness focus
on birds and mammals (Schupp et al., 2010) as these are the classic
model systems for endozoochorous seed dispersal (Fleming and Kress,
2013). Only relatively recently have empiricists turned their attention
to quantifying seed dispersal effectiveness of frugivorous shes.
Previous studies of three of the largest frugivorous sh species in the
Neotropics found that big P. mesopotamicus disperse a greater number
of intact seeds of a common palm in the Pantanal (Galetti et al., 2008),
that the volume of intact seeds increased with body size for
C. macropomum and P. brachypomus in the Peruvian Amazon, and
passage through guts of adult C. macropomum accelerated seed germi-
nation for a common pioneer tree in Amazonian ooded forests
(Anderson et al., 2009). Here, we demonstrate that these patterns,
observed in a handful of population-level studies, can scale to local
communities of frugivorous shes containing small- and large-sized
Fig. 5. Germination probabilitymodeled as a function of sh size(SLstandardlength) for four plantspecies dispersedby shes in the Pantanal: (a) Banaraarguta,(b)Cayaponiapodantha,
(c) Eugenia inundata, and (d) Passiora cf. edulis.
Fig. 6. Germinationprobability modeledas a function of sh size (SLstandard length)for
ve plant species dispersed by shes in the Amazon. The ve species are shown in one
panel because the sh size by seed species interaction was non-signicant.
165S.B. Correa et al. / Biological Conservation 191 (2015) 159167
species. Within and across small- to large-sized sh species, large
individuals are better seed dispersers.
4.1. Consequences of overharvesting frugivorous shes
Big frugivores are key components of seed dispersal networks in
tropical wetlands because of their consumption of large numbers of
fruits, their long seed-retention times, extensive movement patterns,
and unique ability to disperse large-seeded species (Anderson et al.,
2011; Galetti et al., 2008; Kitamura, 2011; Stevenson et al., 2014;
Woodward et al., 2005; Wotton and Kelly, 2012). Given that large sh
species are the main target of commercial shing operations (Allan
et al., 2005), overexploitation of large frugivorous shes likely has pro-
found implications for the recruitment of large-seeded canopy species
and the maintenance of diversity in wetland forests. For example, in
our study, large P. mesopotamicus in the Pantanal disperse 27% more
seed species than individuals under the minimum size limit for this sh-
ery (total length = 45 cm). Simulation models suggest that the loss of
large-mammal seed dispersers from Thai forests depressed survival
and growth atmultiple life stages of a canopy tree species, and reduced
population viability (Caughlin et al., 2015). Population declines of forest
elephants in the Congo eliminated seedling recruitment for 12 species
of elephant-dependent large seeded-trees due to increased predation
of undispersed seeds (Beaune et al., 2013). Finally, in western Amazonia,
intact forests with large-bodied primates had higher seedling diversity
and better recruitment of medium- and large-seeded canopy species
relative to overhunted sites (Stevenson, 2011).
In our study, the probability of seed predation decreased with sh
size for P. mesopotamicus,B. melanopterus and B. amazonicus, and we
observed a non-signicant trend in that direction for M. torquatus.
Such size-dependent shifts in seed predation could be difcult to reverse
if commercial sheries induce evolutionary changes in frugivorous sh
populations to smaller individuals that mature early (Palkovacs, 2011).
Overshing could change the nature of fruitsh relationships from
primarily mutualistic to increasingly antagonistic with negative
consequences for plant community structure and diversity. Trees in
Amazonian ooded forest typically do not form seed banks, as their
seeds germinate shortly after the water recedes (Ferreira et al., 2010).
Plant communities with negligible seed banks are particularly susceptible
to increased seed predation, which diminishes seedling recruitment
(Vaz Ferreira et al., 2011).
Our study also demonstrates that larger shes arecapable of dispers-
ing seeds of a broader range of sizes than smaller shes (Fig. 4e, f). Gape
size limits the size of seeds a frugivore can consume and disperse
(Wheelwright, 1985), which means that large primates and birds
are typically the primary vectors of dispersal for large-seeded plant
species in terrestrial systems (Kitamura, 2011; Stevenson, 2011).
P. mesopotamicus is the biggest frugivorous shes in the Pantanal. It
can achieve more than ve times the length of reproductive adults of
M. tiete (15 cm SL), the smallest frugivorous species therein (Fig. 2).
The size of the largest seed (M. guianensis: 7.6 mm × 5.6 mm) dispersed
by M. tiete, is merely 8% of the size of the largest seed (C. uiti:
40.7 mm × 19.6 mm) dispersed by P. mesopotamicus. Within assem-
blages of frugivorous shes, adults of the largest sh species disperse
suites of seed species that are unavailable to smaller individuals of
those sh species and to adults of smaller sh species.
Mutualistic interactions between frugivorous shes and tropical
plants date back to the Late Cretaceous (~ 70 Ma) in South America
(Correa et al., 2015; Thompson et al., 2014), which coincides with the
radiation of angiosperms (Berendse and Scheffer, 2009), and pre-dates
most bird- and mammalfruit interactions (Correa et al., 2015).
Knowledge of how seed dispersal services of shes compare with
those of non-aquatic frugivores in wetlands is rather limited, although
observations from one sh species in the Pantanal suggest that shes
disperse a different suite of species (Donatti et al., 2011). If indeed,
shes, birds and mammals disperse different seed species, the loss of
one or several key frugivorous shes may not be mitigated by the
remaining frugivore groups (e.g., Efom et al., 2014).
4.2. Conclusions
Through a comprehensive multi-system, multi-species study of the
role of sh size on seed dispersal, we documented that the quality and
quantity of seed dispersal increases with body size within and across
sh species. Larger individuals disperse a greater number of viable
seeds of a higher diversity of plants, and are unique vectors of dispersal
for big seeds. As shes of varying size classes differ in their seed dispers-
al services, we predict that small shes will not be able to maintain seed
dispersal in wetlands if populations of large shes continue to decline.
Future empirical studies on recruitment dynamics and spatial aggrega-
tion of sh-dispersed seed species in areas with intact sh populations
vs. overshed areas should be conducted to test the consequences of
seed dispersal limitation for plant population viability (e.g., Caughlin
et al., 2015). Overexploitation of fruit-eating shes could disrupt an an-
cient mutualism, potentially leading to declines in plant recruitment
success and diversity in wetlands that rely on fruit-eating shes. To
conserve wetland plant communities, we need to protect not just
the habitat, but the interactions that occur within that habitat. Plant
species composition could change dramatically in oodplain forests if
overshing removes the shes that provide the greatest seed dispersal
quantity and quality. Although minimum legal capture sizes have
been established to preserve reproductive potential, this management
strategy does not consider the role of these shes in wetland plant
regeneration. A scientically robust management plan that preserves
larger individuals, such as maximum size thresholds (e.g., Pierce,
2010), can help safeguard a key ecosystem process.
Acknowledgments
We thank Jessika Sanabria, Tafnys Hadassa, Érika de-Faria, Pedro
de-Anunciaçao, Ademar, Rodrigo Brandāo, Lázaro Ramos, Anderson
Alvarenga, Ivo Brandāo, Oilton de-Moraes, Márcio Correa, Jhon
Patarroyo, Margarita Roa, Jarvis Rodriguez and Benedicto Neira for eld
assistance. We thank Fernando Barbosa, Helio Ferreira, Norida Canchala
and Dairon Cárdenas for plant identications and Ivonne Vargas for
seed identications. We thank Tainá F.D. Rodrigues (Universidade Feder-
al de Mato Grosso) for preparing the map. We thank Seth Wenger,
Thomas Pendergast, Mauro Galetti, and two anonymous reviewers for
valuable comments on a previous draft. Permits for this research were
granted by the Chico Mendes Institute of Biodiversity Conservation,
Brazil (License# 42085-1) and the National Authority of Environmental
Licenses, Colombia (Act# 1177 to Universidad de los Andes). We thank
the Eppley Family Foundation, SESC Pantanal, the University of South
Carolina, and the University of Georgia for support of this research.
Equipment donated by IdeaWild (to S.B.C.) was used in this research.
Appendix A. Supplementary data
Supplementary data to this article can be found online at http://dx.
doi.org/10.1016/j.biocon.2015.06.019.
References
Agudelo, E., Bonilla, C.A., Gomez, G.A., Salvino, H., Trujillo, D.L., 2012. Evolución de las
longitudes corporales para la pesquería comercial de bagres en la amazonía
colombiana.Rev.Colomb.Amazón.5,176195.
Albuquerque, S.P., Catella, A.C., Campos, F.L.d.R., Santos, D.C.d., 2012. Sistema de Controle
da Pesca de Mato Grosso do Sul SCPESCA/MS 17-2010. EMBRAPA, Corumbá, MS.
Allan, J.D., Abell, R., Hogan, Z., Revenga, C., Taylor, B.W., Welcomme, R.L., Winemiller, K.,
2005. Overshing of inland waters. Bioscience 55, 10411051.
Anderson, J.T., Saldaña-Rojas, J., Flecker, A.S., 2009. High-quality seed dispersal by
fruit-eating shes in Amazonian oodplain habitats. Oecologia 161, 279290.
Anderson,J.T., Nuttle, T., Saldaña-Rojas, J.S., Pendergast,T.H., Flecker, A.S.,2011. Extremely
long-distance seed dispersal by an overshed Amazonian frugivore. Proc. R. Soc.
Lond. Ser. B Biol. Sci. 278, 33293335.
166 S.B. Correa et al. / Biological Conservation 191 (2015) 159167
Arieira, J., Karssenberg, D., de Jong, S.M., Addink, E.A., Couto, E.G., Nunes da Cunha, C.,
Skøien, J.O., 2011. Integrating eld sampling, geostatistics and remote sensing to
map wetland vegetation in the Pantanal, Brazil. Biogeosciences 8, 667686.
Aslan, C., Zavaleta, E., Tershy, E.S., Croll, B., D., 2013. Mutualism disruption threatens
global plant biodiversity: a systematic review. PLoS ONE 8 (e66993).
Barthem, R., Goulding, M., 2007. An Unexpected Ecosystem. The Amazon as Revealed by
Fisheries. Asociación para la Conservación de la Cuenca Amazónica (ACCA), Missouri
Botanical Garden Press, Lima.
Beaune, D., Fruth, B., Bollache, L., Hohmann, G., Bretagnolle, F., 2013. Doom of the
elephant-dependenttrees in a Congo tropical forest. For.Ecol. Manag. 295, 109117.
Benjamin, Y., Hochberg, Y., 1995. Controlling the false discovery rate: a practical and
powerful approach to multiple testing. J. R. Stat. Soc. A. Stat. Soc. 57, 289300.
Berendse, F., Scheffer, M., 2009. The angiosperm radiation revisited, an ecological
explanation for Darwin's abominable mystery. Ecol. Lett. 12, 872-885.
Castello, L., McGrath,D.G., Arantes, C.C.,Almeida, O.T., 2013. Accounting forheterogeneity
in small-scale sheries management: the Amazon case. Mar. Policy 38, 557565.
Caughlin,T.T., Ferguson, J.M., Lichstein, J.W., Zuidema, P.A.,Bunyavejchewin, S., Levey,D.J.,
2015. Loss of animal seed dispersal increases extinction risk in a tropical tree species
due to pervasive negative density dependence across life stages. Proc. R. Soc. Lond.
Ser. B Biol. Sci. 282, 20142095.
Correa, S.B., Winemiller, K.O., 2014. Niche partitioning among frugivorous shes in
response to uctuating resources in the Amazonian oodplain forest. Ecology 95,
210224.
Correa, S.B., Costa-Pereira, R.,Fleming, T.H., Goulding, M., Anderson, J.T.,2015. Neotropical
fruitsh interactions: eco-evolutionary dynamics and conservation. Biol. Rev. Camb.
Philos. Soc. http://dx.doi.org/10.1111/brv.12153.
Dirzo, R., Young, H.S., Galetti, M., Ceballos, G., Isaac, N.J., Collen, B., 2014. Defaunation in
the Anthropocene. Science 345, 401406.
Donatti, C.I., Guimaraes, P.R., Galetti, M., Pizo, M.A., Marquitti, F.M.D., Dirzo, R., 2011.
Analysis of a hyper-diverse seed dispersal network: modularity and underlying
mechanisms. Ecol. Lett. 14, 773781.
Duivenvoorden, J.F., 1996. Patterns of tree species richness in rain forests of the middle
Caquetá area, Colombia, NW Amazonia. Biotropica 28, 142158.
Efom, E.O., Birkhofer, K., Smith, H.G., Olsson, O., 2014. Changes of community
composition at multiple trophic levels due to hunting in Nigerian tropical forests.
Ecography 37, 367377.
Ferreira, C.S., Piedade, M.T.F., Oliveira-Wittmann, A.d., Franco, A.C., 2010. Plant
reproduction in the Central Amazonian oodplains: challenges and adaptations.
AoB Plants http://dx.doi.org/10.1093/aobpla/plq009.
Firth, D., 1993. Bias reduction of maximum likelihood estimates. Biometrika 80, 2738.
Fleming, T.H., Kress, W.J., 2013. The Ornaments of Life. Coevolution and Conservation in
the Tropics. The University of Chicago Press, Chicago.
Galetti, M., Donatti, C.I., Pizo, M.A., Giacomini, H.C., 2008. Big sh are the best: seed
dispersal of Bactris glaucescens by the Pacu sh (Piaractus meso potamicus)inthe
Pantanal, Brazil. Biotropica 40, 386389.
Galetti, M., Guevara, R., Côrtes, M.C., Fadini, R., Von Matter, S., Leite, A.B., Labecca, F.,
Ribeiro, T., Carvalho, C.S., Collevatti, R.G., Pires, M.M., Guimarães Jr., P.R., Brancalion,
P.H., Ribeiro, M.C., Jordano, P., 2013. Functional extinction of birds drives rapid
evolutionary changes in seed size. Science 340, 10861090.
Horn, M.H., Correa, S.B., Parolin, P., Pollux, B.J.A., Anderson, J.T., Lucas, C., Widmann, P.,
Tiju, A., Galetti, M., Goulding, M., 2011. Seed dispersal by shes in tropical and tem-
perate fresh waters: the growing evidence. Acta Oecol. 37, 561577.
Howe, H.F., Smallwood, J., 1982. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13,
201228.
Isaac, V.J., Rufno, M.L., 1996. Population dynamics of tambaqui, Colossoma macropomum
Cuvier, in the lower Amazon, Brazil.Fish. Manag. Ecol. 106, 110127.
Jordano, P., 2000. Fruits and frugivory. In: Fenner, M. (Ed.), Seeds: The Ecology of
Regeneration in Plant Communities, 2nd edition CABI International, Wallingford,
UK, pp. 125166.
Junk, W.J., 1993. Wetlands of tropical South America. In: Whigham, D.F., Dykyjová, D.,
Hejný, S. (Eds.), Wetlands of the World: Inventory, Ecology and Management Vol. I.
Springer, The Netherlands, pp. 679739.
Junk, W.J., Nunes da Cunha, C., 2005. Pantanal: a large South American wetland at a
crossroads. Ecol. Eng. 24, 391401.
Junk, W.J., Piedade, M.T.F., 2010. An introduction to South American wetland forests:
distribution, denitions and general characterization. In: Junk, W.J., Piedade, M.T.F.,
Wittmann, F., Schöngart, J., Parolin, P. (Eds.), Central Amazonian Floodplain Forests:
Ecophysiology, Biodiversity, and Sustainable Management. Springer, New York,
pp. 425.
Kitamura, S., 2011. Frugivory and seed dispersal by hornbills (Bucerotidae) in tropical
forests. Acta Oecol. 37, 531541.
Kubitzki, K., Ziburski, A., 1994. Seed dispersal in ood-plain forests of Amazonia.
Biotropica 26, 3043.
Markl, J.S., Schleuning, M., Forget, P.M., Jordano, P., Lambert, J.E., Traveset, A., Wright, S.J.,
Böhning-Gaese, K., 2012. Meta-analysis of the effects of human disturbance on seed
dispersal by animals. Conserv. Biol. 26, 10721081.
Mateus, L.A.d.F., Penha, J.M.F., Petrere, M., 2004. Fishing resources in the rio Cuiabá Basin,
Pantanal do Mato Grosso, Brazil. Neotropical Ichthyol. 2, 217227.
Ollerton, J., Winfree, R., Tarrant, S., 2011. How many owering plants are pollinated by
animals? Oikos 120, 321326.
Palkovacs, E.P., 2011. The overshing debate: an eco-evolutionary perspective. Trends
Ecol. Evol. 26, 616617.
Peixer, J., Catella, A.C., Petrere-Júnior, M., 2007. Yield per recruit of the Pacu Piaractus
mesopotamicus (Holmberg, 1887) in the Pantanal of Mato Grosso do Sul, Brazil.
Braz. J. Biol. 67, 561567.
Pierce, R.B., 2010. Long-term evaluations of length limit regulations for Northern Pike in
Minnesota. N. Am. J. Fish Manag. 30, 412432.
Pinheiro, J., Bates, D., DebRoy, S., Sarkar, D., 2014. R Development Core Team (2014).
nlme: linear and nonlinear mixed effects models. R Package Version 3.1-118.
R Foundation for Statistical Computing, Vienna.
Pollux, B.J.A., 2011. The experimental study of seed dispersal by sh (ichthyochory).
Freshw.Biol.56,197212.
Poulsen, J.R., Clark, C.J., Palmer, T.M., 2013. Ecological erosion of anAfrotropical forest and
potential consequences for tree recruitment and forest biomass. Biol. Conserv. 163,
122130.
Reinert, T.R., Winter, K.A., 2002. Sustainability of harvested Pacu (Colossoma
macropomum) populations in the northeastern Bolivian Amazon. Conserv. Biol. 16,
13441351.
Reis, R.E., Kullander, S.O., Ferraris, C.J.J. (Eds.), 2003. Check List of the Freshwater Fishes of
South and Central America. EDIPUCRS, Porto Alegre.
Rigby, R.A., Stasinopoulos, D.M., 2005. Generalized additive models for location, scale and
shape (with discussion). J. R. Stat. Soc. Ser. C Appl. Stat. 54 (part 3), 507554.
Rodriguez, C.A., 1991. Commercial Fisheries in the Lower Caqueta River. Tropenbos-
Colombia, Bogotá, D.C.
Rodriguez, M.A., Winemiller, K.O., Lewis Jr., W.M., Taphorn Baechle, D.C., 2007. The
freshwater habitats, shes, and sheries of the Orinoco River Basin. Aquat. Ecosyst.
Health Manag. 10, 140152.
Rufno, M.L., 2008. Sistema integrado de estatística pesqueira para a Amazônia. Pan-Am.
J. Aquat. Sci. 3, 193204.
Santos, G.M.d., Santos, A.C.M.d., 2005. Sustentabilidade da pesca na Amazônia. Estud.
Avançados 19, 165182.
Schupp, E.W., Jordano, P., Gomez, J.M., 2010. Seed dispersal effectiveness revisited:
a conceptual review. New Phytol. 188, 333353.
Seidler, T., Plotkin, J.B., 2006. Seed dispersal and spatial pattern in tropical trees. Public
Libr. Sci. Biol. 4, e344.
Stevenson, P.R., 2011. The abundance of large Ateline monkeys is positively associated
with the diversity of plants regenerating in Neotropical forests. Biotropica 43,
512519.
Stevenson, P.R., Link, A., Onshuus, A., Quiroz, A.J., Velasco, M., 2014. Estimation of seed
shadows generated by Andean woolly monkeys (Lagothrix lagothricha lugens). Int.
J. Primatol. 35, 10211036.
Thompson, A.W., Betancur-R, R., López-Fernández, H., Ortí, G., 2014. A time-calibrated,
multi-locus phylogeny of piranhas, pacus, and allies (Characiformes: Serrasalmidae)
and a comparison of species tree methods. Mol. Phylogenet. Evol. 81, 242257.
Traveset, A., Rodríguez-Pérez, J., Pías, B., 2008. Seed trait changes in dispersers' guts and
consequences for germination and seedling growth. Ecology 89, 95106.
Valiente-Banuet, A., Aizen, M.A., Alcántara, J.M., Arroyo, J., Cocucci, A., Galetti, M., García,
M.B., García, D., Gómez, J.M., Jordano, P., Mendel, R., Navarro, L., Obeso, J.R., Oviedo,
R., Ramírez, N., Rey, P.J., Traveset, A., Verdú, M., Zamora, R., 2015. Beyond species loss:
the extinction of ecological interactions in a changing world. Funct. Ecol. 29, 299307.
Vaz Ferreira, A., Bruna, E.M., Vasconcelos, H.L., 2011. Seed predators limit plant
recruitment in Neotropical savannas. Oikos 120, 10131022.
Wang, B.C., Smith, T.B., 2002. Closing the seed dispersal loop. Trends Ecol. Evol. 17,
379386.
Wheelwright, N.T., 1985.Fruit size, gape width, andthe diets of fruit-eating birds. Ecology
66, 808818.
Woodward, G., Ebenman, B., Emmerson, M., Montoya, J.M., Olesen, J.M., Valido, A.,
Warren, P.H., 2005. Body size in ecological networks. Trends Ecol. Evol. 20, 402409.
Wotton, D.M., Kelly, D., 2012. Do larger frugivores move seeds further? Body size, seed
dispersal distance, and a case study of a large, sedentary pigeon. J. Biogeogr. 39,
19731983.
Zuur, A.F., Ieno, E.N., Walker, N.J., Saveliev, A.A., Smith, G.M., 2009. Mixed Effects Models
and Extensions in Ecology with R. Springer, NY.
167S.B. Correa et al. / Biological Conservation 191 (2015) 159167
... Frugivorous fish in the genus Brycon (Bryconidae) are important seed dispersers of riparian and wetland plants (Correa, Araújo, et al., 2015;Horn, 1997;Reys et al., 2009;Santos et al., 2020). Brycon, however, have a great ability to crush food due to multicuspid oral dentition (Lima, 2017). ...
... Our findings complement recent evidence demonstrating the influence of fish body size on seed dispersal effectiveness (Anderson et al., 2009;Correa, Araújo, et al., 2015;Galetti et al., 2008). As with seed dispersal, the greater number of seeds ingested by larger fish can be explained by the greater storage capacity of the gastrointestinal tract of larger animals (Galetti et al., 2008). ...
... These findings suggest that seed predation efficiency increases with fish size. In fish, mouth gape increases with body length (Correa, Araújo, et al., 2015). Thus, a bigger mouth likely is correlated with broader or denser dentition and greater biting force that may speed-up food processing. ...
Article
en Our experiment revealed unexpected behavioral strategies involved in seed predation of Mabea fistulifera by fish (Brycon cephalus), including temporal storage of seeds in the stomach followed by regurgitation and reingestion of individual seeds. Larger fish were faster at removing the seed coat and exposing the endosperm, due to precise oral manipulation of seeds. Abstract in Portuguese is available with online material Resumo pt Nosso experimento revelou estratégias comportamentais inesperadas envolvidas na predação de sementes de Mabea fistulifera por peixes (Brycon cephalus), incluindo armazenamento provisório de sementes no estômago, seguido de regurgitação e reingestão das sementes individuais. Os peixes maiores foram mais rápidos em remover o tegumento da semente e expor o endosperma devido à manipulação oral precisa das sementes.
... The length at which M. albiscopum reaches gonadal maturity is demonstrating that individuals reproduce at relatively small sizes, so this parameter could be influencing their growth rates, however, in past decades, a length of first gonadal maturity of 25.6 cm SL was reported in the Colombian Amazon (Beltrán-Hostos et al., 2001), being higher than that recorded at present study. These results show that there is probably greater fishing pressure on the resource in the Ucayali Region; several studies have described evidence that fishing exploitation is reducing length at first gonadal maturity, leading to accelerated reproduction that induces a reproductive strategy to ensure the maintenance of its population (Correa et al., 2015), a mechanism that seems to have been adopted by the fraction of the population of M. albiscopum in the Ucayali River. where the higher fishing intensity affects a reduction of maximum length and length at first gonadal maturity (Correa et al., 2015). ...
... These results show that there is probably greater fishing pressure on the resource in the Ucayali Region; several studies have described evidence that fishing exploitation is reducing length at first gonadal maturity, leading to accelerated reproduction that induces a reproductive strategy to ensure the maintenance of its population (Correa et al., 2015), a mechanism that seems to have been adopted by the fraction of the population of M. albiscopum in the Ucayali River. where the higher fishing intensity affects a reduction of maximum length and length at first gonadal maturity (Correa et al., 2015). ...
Article
Full-text available
Mylossoma albiscopum show high levels of fishing landing in Pucallpa city (Ucayali Region, Peru). Nevertheless, information available about the population and reproductive parameters and exploitation of this species, is limited. Reason that motivated the development of this research, whose basis was the analysis of information on length frequencies and biological records in the Ucayali River at 2011–2019, moreover, to attain reproductive parameters, 11005 individuals were analyzed and sampled from the main fish landing sites of Pucallpa city. Females reach the mean length at first gonadal maturity at 14 cm (1.13 years) and males at 13.6 cm (1.29 years) of total length, respectively. The equations for theoretical growth according to the von Bertalanffy are defined by Lt = 33.81*(1 − e−0.38(t−0.42)) for unsexed, Lt = 32.26*(1 − e−0.38(t−0.43)) for females and Lt = 29.93*(1 − e−0.38(t−0.44)) for males; these results allow inferring that this species has fast growing and maximum age at 7.46. Exploitation rate was estimated to be 0.61 years−1, expressing overfishing values, which would involve generating a Fishery Management Plan for its conservation and sustainability in the Ucayali Region.
... mutualism and facilitation), in which at least one species increases the fitness of another (hereafter, 'host' and 'beneficiary' species, respectively), have been observed in a wide array of organisms, including plants and animals (Holt et al. 2002, Bronstein 2015, Silknetter et al. 2020. These interactions are most influential in certain life-history stages, such as reproduction (Johnston 1994, Pendleton et al. 2012) and dispersal (Horn et al. 2011, Correa et al. 2015. Due to the nature of mutualistic/facilitative species interactions, species involved in positive interactions often exhibit strong distributional adherence at micro (< 10 m) to local habitat scales (1-10 km) (Pearson andDawson 2003, Wisz et al. 2013). ...
... Our findings have important implications for biodiversity conservation and effective ecosystem management. While it is well known that local loss of mutualistic or facilitative partners will likely cause secondary extirpations of beneficiary species (Bruno et al. 2003, Halpern et al. 2007, Correa et al. 2015, questions still remain about the role of positive biotic interactions at larger spatial scales. Our findings suggest that the loss of facilitative partners may have comparable or even greater impacts at the metapopulation level. ...
Article
Full-text available
Positive biotic interactions are recognized as important factors determining species distributions. Although effects of positive interactions have often been observed at local scales, much less is known about consequences at larger spatial scales. Here, we study nest associations of stream fishes – widespread reproductive facilitation between host (nest-builder) and beneficiary (nest associate) species in North America – as a model system to examine the role of positive interactions in determining the metapopulation level relationship between host and beneficiary species. Using regional data of fish distribution in the Midwestern US, we found that watershed-level occupancy of host species (i.e. metapopulation occupancy) remarkably increased that of nest associates. Our results illustrated that the effects of positive biotic interactions at the metapopulation level were comparable or even stronger than environmental drivers, i.e. factors that have been studied most extensively in metapopulation studies. Further, our model supported the hypothesis that the metapopulation-level relationship between hosts and nest associates was mediated by a gradient of environmental conditions: strong associations occurred under stressful habitats. This study provides insightful evidence that positive biotic interactions have larger scale consequences for distributions of organisms than previously thought. Successful biodiversity conservation may need a broader framework that appreciates the role of positive biotic interactions at larger spatial scales.
... Brycon falcatus (Bryconidae), is a member of an iconic genus of broadly distributed frugivorous fishes (from Mexico to the Rio de la Plata Basin, Argentina; Lima 2017), represented by medium-and large-sized species (16-70 cm SL) that in addition to fruits and flowers, also eat insects, other fish, and even small vertebrates (Goulding 1980;Lima 2017). Multiple Brycon species disperse seeds of diverse riparian plant species (Banack et al. 2002;Correa et al. 2015;Gomiero et al. 2008;Horn 1997;Reys et al. 2009). Brycon species typically undergo a dietary shift during ontogeny; younger fish are mostly carnivorous, while older fish are predominantly frugivorous (Drewe et al. 2004). ...
Article
Frugivorous fishes switch their diets seasonally in response to fluctuating food availability; a strategy that maximizes energy and nutrient intake and reduces competition for food. Kleptoparasitism is a form of competition that involves the stealing of already‐procured items, for which the host has invested energy in prey capture. We did not find previous studies on kleptoparasitism among Neotropical fish. Here we contribute the first record of kleptoparasitism among a frugivorous fish species. The matrinxã (Brycon falcatus) is a member of an iconic genus of broadly distributed frugivorous fishes. We made focal daylight underwater observations (by snorkeling) of frugivorous fish behavior in an Amazonian stream. Opportunistic feeding interactions between a school of juvenile matrinxã, (B. falcatus) and an individual of threespot leporinus (Leporinus friderici) were observed. The matrinxã stole the fruit that was captured in the substrate by the leporinus. Brycon falcatus usually lives between the middle of the water column to the surface of rivers and streams while Leporinus friderici occupies the lower portion of the water column and it actively forages close to the substrate. This suggests that stealing food from a benthic feeder is an opportunistic ecological interaction to take advantage of scarce resources during the period of food scarcity. This alternative technique of capturing fruits may be advantageous (i.e., save energy expenditures related to searching) for young matrinxã who do not eat fruit as frequently as adults. Our results reflect the trophic plasticity and foraging opportunism characteristic of most tropical freshwater fish. We believe that the hydrological period in which the observations were made, when a few trees were bearing fruit, can favor fruit stealing by Brycon falcatus.
... Intraspecific variation, such as sexual dimorphism, ontogenetic differences, or resource polymorphism, can foster individual differences in diet, microhabitat preference, foraging behavior, or other forms of resource use (reviewed in ref. 8), and the implications for community dynamics, competition, predation, demographic rates, and evolution have been reviewed comprehensively (6,9). Empirical investigations examining whether different individuals can affect the outcome of mutualistic interactions are rare, but recent studies have aimed to assess the effects of intraspecific differences related to age, sex, and genetic or morphological variation on mutualistic interactions (6,(10)(11)(12)(13)(14)(15)(16)(17). However, we lack empirical studies examining sources of variation that do not fit neatly into these categories, such as consistent intraspecific behavioral differences or personalities (18). ...
Article
Significance Mutualisms are foundational components of ecosystems and give rise to essential services such as seed dispersal and pollination. Ecologists believe that nearly every species is involved in one or more mutualisms, but it is unknown how consistent behavioral differences among individuals, or personalities, may influence an individual’s role. We scored individuals on a continuum from antagonistic to mutualistic given their contributions to the seed dispersal mutualism and found that personalities affect the extent to which individuals are mutualistic. These findings suggest a novel mechanism generating context dependence in mutualisms and underscore the need to incorporate behavioral diversity into conservation and restoration efforts.
... habitat-specific (Correa et al., 2015). Long-distance seed dispersal of dry tree species could dilute environmental effects magnifying the pattern of spatially structured environments. ...
Article
Aims Tropical dry forests are one of the most threatened ecosystems on Earth, and understanding the effects of climate on its species distributions is critical to mitigate global change impacts. Here, we assessed the impact of precipitation and dispersal limitation by natural and anthropogenic causes on phylogenetic and taxonomic beta diversity of woody plant communities. Location Cauca River Canyon in the Northwest Andean mountains, Colombia Methods We used inventory data from 160 0.02-ha plots and a phylogenetic tree to calculate phylogenetic and taxonomic beta diversity and their components (nestedness and replacement) across plots. We used Redundancy Analysis to assess the effects of precipitation, spatial distance, and connectivity (a proxy of fragmentation) to changes in beta diversity metrics and estimated each variable's relative contribution. Results We found that phylogenetic and taxonomic replacement were highly related to precipitation differences. Spatial distance and connectivity explained only a small proportion of the variance in phylogenetic and taxonomic replacement. None of the predictor variables explained phylogenetic or taxonomic nestedness. Conclusions Patterns of phylogenetic and taxonomic replacement across woody plant communities suggest that species and clades are highly specialized to particular precipitation regimes with a minor role for dispersal limitation. Both climate change and fragmentation could drastically influence the future community composition of tropical dry forests.
Article
Abnormal hydroclimatic years in the Amazon have been increasingly frequent in the last two decades, creating more prolonged droughts and severe floods. These events are expected to impact organismal phenology, including seasonal reproduction of fish. Droughts are also expected to increase fish mortality and vulnerability to fishing. However, empirical evidence on the impact of these novel conditions on fish reproduction and demography is still limited. Here, we evaluate how changes in hydrological conditions and fishing affected reproduction and demographic parameters for the 16 most common floodplain fish species in the central Amazon. We used water level data collected for 113 years together with a 19‐year dataset of fish biology, sampled monthly from a floodplain lake at the confluence of Amazon and Negro rivers. We observed a lower proportion of ripe females after long, drier low‐water and abrupt rising‐water seasons. For many species, we detected a progressive reduction in the female’s size at sexual maturity, the average size of the ripe females, and in the abundance of larger adult females. These effects were observed for both fished and non‐fished species, suggesting that the effect of the recent hydroclimatic events might be affecting most fish species. However, fished species showed a steeper decline in the average body size of ripe females, suggesting that size reduction is a combined effect of drought severity and fishing pressure. Policy implications. Our results for the proportion of females in reproduction mediated by hydrological conditions and temporal changes of demographic and life‐history parameters suggest that drought events can reduce the resilience of fish populations in the central Amazon. The increasing frequency of droughts and rapid changes in fish reproductive parameters highlight the need for conservation policies to consider the impact of droughts in addition to fisheries and habitat degradation. Our results should be taken as an early warning regarding the conservation and sustainable use of Amazon aquatic biodiversity. Conserving fish diversity and fish stocks will require substantial ecosystem management in a large portion of the Amazon floodplains and a greater enforcement of fisheries management regulations in years of predicted drought.
Chapter
Full-text available
Amazonian lowland tropical rainforests cover ~5.79 million km2. Based on geology, the Amazon lowland forest area can be divided into six regions. The Guiana Shield and Brazilian Shield (in the southern Ama- zon) are on very old, nutrient-poor soils, while the Western Amazonian regions (northern and southern) and the regions along the Amazon River are mainly built from more recent sediments of Andean origin and of variable nutrient richness. The six regions are characterized by differences in soil fertility and rain- fall, causing differences in above-ground biomass, productivity, and tree turnover. There is still intense debate concerning the total plant species richness of the the Amazon. A well-supported estimate for trees (diameter >10 cm) is 16,000 species, ~11,000 of which have been collected and described. Estimates of the total flora range from 15,000 to 55,000 species. As in much of the tropics, Fabaceae (the bean family) are the most species-rich of the major woody groups in the Amazon. South America and the Amazon are also renowned for the abundance and diversity of palms. While most ecosystem vegetation models emphasize climate and carbon production processes, these are not sufficient to understand how Amazonian forest ecosystems vary spatially. In particular, long-term observations with plots show that spatial variation in Amazonian forest biomass and stem dynamics are driven more by soil conditions than climate, while car- bon stocks are constrained as much by soil physical features and tree floristic composition as by produc- tivity. The key effects of soil on the Amazon’s ecosystem function also extend to animals and their im- portant functions, including herbivory, seed dispersal, and insect activity. Soil and geology influence Am- azonian rivers too, which are distinguished as being either white-water (carrying sediments from the An- des), clear-water (draining the ancient Shields), or black-water (draining white sand areas). The nutrients associated with each major river class strongly determine the floodplain forest ecology and species, with igapó in sediment-poor clear and black-waters, and várzea (known as tahuampa in Peru) with white, sedi- ment-rich waters. Climate impacts become stronger towards the margins, and some Amazon forests are already close to the thermal and hydrological limits of sustaining productive forest ecosystems. Amazo- nian tree mortality rates are already increasing in many intact forests, Amazonian forest composition has been affected by recent droughts, and the mortality of wet-affiliated Amazonian tree genera has increased in places where the dry season has intensified. Key areas of uncertainty include understanding the extent to which recent climate change has caused a slowing of the carbon sink in intact Amazonian forests, and whether intact forests will now lose carbon, or whether the shallow water tables and rich biodiversity of many Amazonian forests will buffer against climate change, especially in the western part of the basin.
Article
Full-text available
Neotropical Ichthyology promotes the Special Issue (SI) “Human impacts and the loss of Neotropical freshwater fish diversity” with the purpose of publishing relevant scientific articles on the current biodiversity crisis and the loss of Neotropical freshwater fishes in the Anthropocene. The SI is composed of 22 publications, being two review articles and 20 original articles. A total of 107 researchers contributed to these papers, involving 44 institutions based in Brazil and six other countries. Published articles investigated main anthropic activities and their impacts on fish diversity, with special focus on river regulation, mining, land use changes, aquaculture, and fisheries. Studies provided evidence about the loss of fish diversity in the Neotropics, including fish kill events, demographic changes, contamination, changes in assemblage structure, loss of taxonomic and functional diversity, besides the degradation of ecosystem functions and services, and the lack of effective protection and conservation. Studies were conducted in rivers, streams, lakes, and reservoirs from different Neotropical systems. The studies published in this SI represent a relevant sample of the current worrisome situation of freshwater fishes in the Neotropical region and call for urgent revision in environmental policies, management and conservation initiatives, and socioeconomic priorities.
Article
Full-text available
Our objective was to evaluate the effectiveness of protected areas (PAs) in the Paraná-Paraguay basin on multiple facets of ichthyofauna, both currently and in future climate change scenarios, based on reaching the 17% of conserved terrestrial and inland water defined by Aichi Target 11. Analyses were carried out vis-à-vis a distribution of 496 native species, modeling for the present and for the future, and in moderate and pessimistic scenarios of greenhouse gases. We calculated species richness, functional richness, and phylogenetic diversity, overlapping the combination of these facets with the PAs. The results indicate that the current PAs of the Paraná-Paraguay basin are not efficient in protecting the richest areas of ichthyofauna in their multiple facets. While there is a larger overlap between PAs and the richest areas in phylogenetic diversity, the values are too low (2.37%). Currently, the overlap between PAs and areas with larger species richness, functional richness, and phylogenetic diversity is only 1.48%. Although this value can increase for future projections, the values of the indices decrease substantially. The relevant aquatic environments, biological communities, and climate change should be considered as part of the systematic planning of PAs that take into consideration the terrestrial environments and their threats.
Article
Full-text available
The Floodplain Natural Resources Management Project (ProVárzea) executed by IBAMA, integrated institutions and projects that historically collecting effort and catch data, strengthened and expanded a system along of the Amazon- Solimões-river channel. This system was implemented because the institutions just had a monitoring system of fishery activity with the following characteristics: i) working with the total universe of landings on the respective colleting locals, and not estimating by samples; ii) the data were processed by a relational data bank; (iii) the original data can be interchanged in different formats; and iv) the type of information obtained were similar, and the majority of the categorical variables were standardized. The system permitted construct a common data base and realize integrated analysis about the data collected a long in 17 municipalities. The system gave information published on annual statistics bulletins and on internet, and subsided the fishery management on the region, by establishment of closing season, and mainly the fishery community co-management by fishing agreement. The system was expanded to other states, but since 2005 all collecting data system was interrupted by the end of financing.
Article
Full-text available
Frugivorous fish play a prominent role in seed dispersal and reproductive dynamics of plant communities in riparian and floodplain habitats of tropical regions worldwide. In Neotropical wetlands, many plant species have fleshy fruits and synchronize their fruiting with the flood season, when fruit-eating fish forage in forest and savannahs for periods of up to 7 months. We conducted a comprehensive analysis to examine the evolutionary origin of fish-fruit interactions, describe fruit traits associated with seed dispersal and seed predation, and assess the influence of fish size on the effectiveness of seed dispersal by fish (ichthyochory). To date, 62 studies have documented 566 species of fruits and seeds from 82 plant families in the diets of 69 Neotropical fish species. Fish interactions with flowering plants are likely to be as old as 70 million years in the Neotropics, pre-dating most modern bird-fruit and mammal-fruit interactions, and contributing to long-distance seed dispersal and possibly the radiation of early angiosperms. Ichthyochory occurs across the angiosperm phylogeny, and is more frequent among advanced eudicots. Numerous fish species are capable of dispersing small seeds, but only a limited number of species can disperse large seeds. The size of dispersed seeds and the probability of seed dispersal both increase with fish size. Large-bodied species are the most effective seed dispersal agents and remain the primary target of fishing activities in the Neotropics. Thus, conservation efforts should focus on these species to ensure continuity of plant recruitment dynamics and maintenance of plant diversity in riparian and floodplain ecosystems. © 2015 Cambridge Philosophical Society.
Article
Full-text available
Seed dispersal is known to play an important role in the ecology and evolution of plant communities, and there is ample evidence that seed dispersal by primates influences plant population dynamics in tropical forests directly. We used non-parametric statistical methods to estimate the dispersal kernels (i.e. the probability that a seed is moved at a particular distance) generated by woolly monkeys (Lagothrix lagothricha lugens) at a sub-Andean forest in Colombia and test the hypothesis that the time of feeding influences dispersal distances. We collected data on monkey ranging patterns with the aid of GPS units and obtained information on gut retention times from behavioral follows to build a model based on the kernel density estimator. Woolly monkeys drop most seeds hundreds of meters from parent trees and only a small proportion of seeds within close proximity. The time of seed ingestion had a significant effect on dispersal kernels, with seeds from fruits consumed early in the day having a greater chance of landing further away from the tree than seeds swallowed in the late afternoon. The results of this study build on previous findings suggesting that woolly monkeys have a positive effect on the fitness of plants, which may be exacerbated in mountain forests where the diversity of large frugivores is low.
Article
Full-text available
The effects of the present biodiversity crisis have been largely focused on the loss of species. However, a missed component of biodiversity loss that often accompanies or even precedes species disappearance is the extinction of ecological interactions. Here, we propose a novel model that (i) relates the diversity of both species and interactions along a gradient of environmental deterioration and (ii) explores how the rate of loss of ecological functions, and consequently of ecosystem services, can be accelerated or restrained depending on how the rate of species loss covaries with the rate of interactions loss. We find that the loss of species and interactions are decoupled, such that ecological interactions are often lost at a higher rate. This implies that the loss of ecological interactions may occur well before species disappearance, affecting species functionality and ecosystems services at a faster rate than species extinctions. We provide a number of empirical case studies illustrating these points. Our approach emphasizes the importance of focusing on species interactions as the major biodiversity component from which the ‘health’ of ecosystems depends.
Chapter
The climate of tropical South America is characterized over large areas by a high annual precipitation, varying from 1,000 mm to more than 5,000 mm per year. A pronounced seasonality in rainfall results in the periodic flooding of large areas covered by forests or savanna vegetation. Therefore, most of the wetlands in this area belong to the category of seasonal wetlands with a pronounced dry period. Flooding may occur by lateral overflow of rivers and streams or by sheet flooding due to excess rain and insufficient drainage. The floodpulse is mono-modal and predictable in the savannas and the fringing floodplains along the large rivers whereas it is polymodal and unpredictable in the floodplains along small streams. Plants and animals respond to this pulsing with a large set of morphological, anatomical, physiological, and ethological adaptations. Inspite of the physiological stress of the change between aquatic and terrestrial conditions, species diversity is comparatively high. Floodplains of tropical South America may be considered as areas of speciation, contributing to the great species diversity in the area. On the other hand, the floodpulse results in a periodic exchange of biological information between the wetlands and the drainage system, often over long distances. Therefore, many species have a wide range of distribution. Nutrient status of the wetlands varies from extremely low levels in areas flooded by nutrient-poor water (e.g. from rains or black water rivers) to high levels in the fringing floodplains of white water rivers, rich in fertile sediments and electrolytes. Consequently, productivity varies from low to very high, reaching maximum values up to 100 t dry material per hectare per year in the floodplain of the Amazon River. There is a complex exchange of nutrients and energy between the terrestrial and the aquatic phase and between the floodplains and the connected river systems. Further wetland types occur mainly along the coast of the Atlantic ocean, partly in the form of mangroves or salt marshes. Peat bogs, cushion bogs, and reed swamps occur, to a small extent, in the wet Paramos of the high Andes, salt pans occur in the dry Puna. There is no exact information about the total wetland area in tropical South America, partly due to the seasonal character of the wetlands which have been poorly studied and are often not recognized as wetlands. It is estimated, that more than 2,000,000 km2 may belong to the wetland category corresponding to about 20% of the area. In recent times, all wetland types are becoming increasingly influenced and modified by man. In floodplains agriculture and husbandry are the main anthropogenic factors, modifying natural vegetation by deforestation and use of fire for weed control. Some river-floodplains are becoming strongly affected by the construction of flood-control measures and hydroelectric power schemes. Water pollution due to the input of sediments, agro-industrial wastes, agrochemicals, and mercury is becoming a serious threat. Mangroves are probably the most endangered wetlands due to industrial pollution, colonization projects, timber extraction, and large scale fish- and shrimpcul-ture.
Article
It is shown how, in regular parametric problems, the first-order term is removed from the asymptotic bias of maximum likelihood estimates by a suitable modification of the score function. In exponential families with canonical parameterization the effect is to penalize the likelihood by the Jeffreys invariant prior. In binomial logistic models, Poisson log linear models and certain other generalized linear models, the Jeffreys prior penalty function can be imposed in standard regression software using a scheme of iterative adjustments to the data.
Article
Maximum fruiting of the trees coincides with the period of inundation, and the specific timing of diaspore release appears related to special dispersal mechanisms, dormancy, and/or requirements for germination and seedling establishment. Due to the possession of specific tissues or other devices that provide buoyancy, the diaspores of most tree species of the inundated forests are capable of floating for prolonged periods. A comparison of diaspore characteristics between hydrochorous tree species and their congeners in noninundated habitats reveals recurrent patterns: some lineages that in noninundated habitats possess dehiscent fruits with anemochorous or zoochorous seeds, in inundatable habitats switch to the production of hydrochorous seeds. Other lineages that in noninundated habitats have dehiscent fruits, in inundatable habitats switch to the production of indehiscent hydrochorous fruits. Lineages that in noninundated habitats produce indehiscent fruits remain indehiscent when switching to hydrochory in inundatable habitats. In the inundated forests virtually all diaspores that fall into the water are consumed by fish, with rates of destruction differing greatly. Most hydrochorous diaspores can be dispersed by fish, if they are not destroyed by them (facultative ichthyochory). Others depend on fish for dispersal (obligatory ichthyochory), for example, because their diaspores are very heavy and would sink to the ground under the parent tree, or because their seeds are enclosed in a hard shell from which they can be freed only by the jaws of characins. The dormancy of many kinds of seeds is probably broken by their exposure to the hypoxic conditions that prevail in still water. -from Authors