The Science of Nature (2018) 105:29

https://doi.org/10.1007/s00114-018-1556-y

ORIGINAL PAPER

Fruit traits and temporal abundance shape plant-frugivore interaction

networks in a seasonal tropical forest
Michelle Ramos-Robles 1,2 & Wesley Dáttilo 3 & Cecilia Díaz-Castelazo 1 & Ellen Andresen 4

Received: 27 February 2018 / Revised: 17 March 2018 / Accepted: 20 March 2018

# Springer-Verlag GmbH Germany, part of Springer Nature 2018

Abstract
Interactions between fleshy fruited plants and frugivores are crucial for the structuring and functioning of biotic communities,
particularly in tropical forests where both groups are diverse and play different roles in network organization. However, it remains
poorly understood how different groups of frugivore species and fruit traits contribute to network structure. We recorded
interactions among 28 plant species and three groups of frugivores (birds, bats, and non-flying mammals) in a seasonal forest
in Mexico to determine which species contribute more to network structure and evaluate the importance of each species. We also
determined whether fruit abundance, water content, morphology traits, and fruiting phenology are related to network parameters:
the number of interactions, species contribution to nestedness, and species strength. We found that plants did not depend on a
single group of frugivores, but rather on one species of each group: the bird Pitangus sulphuratus, the bat Sturnira parvidens, and
the non-flying mammal Procyon lotor. The abundance, size, and water content of the fruits were significantly related to the
contribution to nestedness, number of interactions, and species strength index of plant species. Tree species and birds contributed
mainly to the nested structure of the network. We show that the structure of plant-frugivore networks in this seasonal forest is non-
random and that fruit traits (i.e., abundance, phenology, size, and water content) are important factors shaping plant-frugivore
networks. Identification of the key species and their traits that maintain the complex structure of species interactions is therefore
fundamental for the integral conservation of tropical forests.

Keywords Frugivorous animals . Network metrics . Nestedness . Phenology . Species strength

Introduction
Communicated by: Sven Thatje
Electronic supplementary material The online version of this article
Interactions between plants and frugivorous animals play an
(https://doi.org/10.1007/s00114-018-1556-y) contains supplementary important role in the diversification, structure, and functioning
material, which is available to authorized users. of ecosystems (Traveset and Richardson 2014). In tropical
ecosystems, a high percentage (70–90%) of woody plants
* Michelle Ramos-Robles depend on interactions with animals in order to complete their
ramosrobles.m@gmail.com life cycle (Farwig and Berens 2012). Fleshy fruits are an im-
portant component of the diet of a wide diversity of frugivo-
1
Red de Interacciones Multitróficas, Instituto de Ecología, A. C., rous animals (Fleming and Kress 2013), and seed dispersal in
Antigua Carretera a Coatepec No. 351, El Haya, 91070 Xalapa, Ver, the majority of fleshy fruited plants takes place through a
Mexico
variety of animals belonging to different taxa and/or function-
2
Present address: Centro de Investigación en Biodiversidad y al groups, which may contribute differently to the final estab-
Conservación, Universidad Autónoma del Estado de Morelos,
62209 Cuernavaca, Mor, Mexico
lishment of plants (Schupp et al. 2010). For instance, different
3
groups of frugivores can have a complementary role in the
Red de Ecoetología, Instituto de Ecología, A. C., Xalapa, Antigua
Carretera a Coatepec No. 351, El Haya, 91070 Xalapa, Ver, Mexico
seed dispersal process (e.g., birds and bats; Sarmento et al.
4
2014), since birds and bats display behavioral differences
Instituto de Investigaciones en Ecosistemas y Sustentabilidad,
Universidad Nacional Autónoma de México, Antigua Carretera a
and a low dietary overlap (Mello et al. 2011).
Pátzcuaro No.8701, Ex Hacienda de San José de la Huerta, Interspecific interactions form complex assemblages of
58190 Morelia, Mich, Mexico species, which can be represented as interaction networks
29 Page 2 of 11
(Bascompte and Jordano 2007; Rohr et al. 2014). In general,
the structure of plant-frugivore networks shows a nested pat-
tern, characterized by a few generalist species interacting with
a large subset of species from another guild or trophic level
(Bascompte and Jordano 2006). These characteristics confer
great robustness to secondary extinctions and promote the
long-term coexistence and persistence of species within an
environment (Bastolla et al. 2009; Tylianakis et al. 2010).
Species level metrics allow us to identify the functional im-
portance of each species (Schleuning et al. 2015). In mutual-
istic networks, a few generalist species contribute significantly
to the nested pattern and thus exert an important influence on
the whole system (Guimarães et al. 2011). However, very few
studies have identified the frugivorous species that most con-
tribute to the nested pattern (Vidal et al. 2014). Moreover,
some species are more important than others in terms of de-
pendence on their counterparts (i.e., species strength;
Bascompte and Jordano 2007). Here, we understand species
strength as the importance of the species in terms of an eco-
logical function (in this case, frugivory). Therefore, identifi-
cation of species with important ecological functions and that
act to maintain network structure is fundamental in terms of
conservation, particularly in view of the crisis of faunal loss
(i.e., defaunation; sensu Dirzo and Miranda 1991; Ceballos
et al. 2015) and thus the imminent loss of interactions.
Recent studies have addressed the relationships between
species traits and their influence on network structure and
functioning of ecosystems (Dehling et al. 2016; Muñoz et al.
2017). Traits such as abundance are determinant in species
interaction probability, since the most abundant species tend
to interact more among themselves than with less abundant
species (Vázquez et al. 2007; Dáttilo et al. 2014). For exam-
ple, the number of available fruits (i.e., plant crop size) can
influence the success of fruit removal and thus seed dispersion
(Ortiz-Pulido et al. 2006). Another important issue to consider
is that of temporal dynamics, such as the phenological patterns
of species that act to modulate interactions between plants and
animals, since not all plant species with a high nutritional
quality are available simultaneously and this may influence
animal foraging decisions (Blendinger et al. 2016).
Plant species morphology (e.g., fruit or seed size) limits the
variety of frugivores that can consume them, since only large-
bodied frugivores have a sufficiently wide gape to ingest large
seeds and transport them over long distances (Galetti et al.
2013; Donoso et al. 2017). The lack of trait-matching between
species affects plant-frugivore interactions and thus plant re-
cruitment (Dehling et al. 2016). However, trait-matching seed
size studies have focused mainly on plant-bird interactions
(e.g., Dehling et al. 2014, 2016; Muñoz et al. 2017).
Inclusion of other frugivore groups (e.g., mammals) and other
fruit variables, such as abundance or temporal availability,
would significantly improve our understanding of frugivory.
In addition, the chemical traits of fruits determine the diet of
Sci Nat (2018) 105:29
many frugivorous species; for example, the pulp of fleshy
fruits provides water, lipids, carbohydrates, and
micronutrients to the frugivores (Schupp et al. 2010; Galetti
et al. 2011; Blendinger et al. 2016). Specifically, the water
available in fruit pulp is an important resource for frugivores
in seasonal habitats (Herrera 1982). There is no doubt regard-
ing the importance of species traits in plant-frugivore interac-
tions (Dehling et al. 2014, 2016), but it is necessary to evaluate
these interactions with multiple groups of frugivores in order
to reach comprehensive and unbiased conclusions.
In this study, we investigate which frugivorous species are
important in terms of maintaining network structure and
which fruit traits are linked to the structure of the plant-
frugivore networks, by considering the whole community of
frugivores (i.e., birds, bats, and non-flying mammals) in a
seasonal forest in Mexico. Our main objective was to under-
stand how different species of plants and frugivorous animals
contribute to the network structure and which fruit traits influ-
ence the organization of such interactions. We sought to an-
swer the following specific questions: (i) which group of fru-
givores contributes most to the nested pattern of the network?
(ii) do plant species have a higher dependence on a particular
group of frugivores? and (iii) which fruit traits are related to
the parameters of the plant-frugivore network? We quantified
the number of fruits removed by each frugivorous species on
each fruiting plant and measured fruit abundance, water con-
tent, morphological traits, and fruiting phenology. We studied
whether interaction strength varied among different taxa of
frugivorous species. Given the functional complementarity
of the frugivorous groups, we hypothesized that certain spe-
cies in each guild would play a greater role in the structure of
the network. We also hypothesized that plant species with
more temporal abundance and smaller fruits are important to
network structure, due to the fact that species with long
fruiting periods have higher temporal availability and are thus
available for consumption by a greater variety of frugivores.
Methods
Study system
The study was conducted at La Mancha Center for Coastal
Research (CICOLMA) in the state of Veracruz, Mexico, in a
protected area of seasonal forest on the Gulf of Mexico coast
(19°35′ 25 N and 96°22′49 W, 0–50 m a.s.l.). Maximum and
minimum temperatures are 36 and 16 °C, respectively, with
mean annual temperature ranging from 22 to 26 °C. Mean
annual rainfall is between 1200 and 1500 mm (García
1981). The rainy season occurs between June and
September, while the dry season occurs from December to
May. Northerly cold fronts are common from November to
February and are characterized by lower temperatures, mild
Sci Nat (2018) 105:29
occasional rains, and strong winds (Castillo and Carabias
1982). The CICOLMA covers 83.29 ha and features at least
eight vegetation types (Travieso-Bello 2000). This environ-
mental heterogeneity favors species diversity and thus the di-
versity of plant-animal interactions (Martínez et al. 2006). Our
study encompassed four vegetation types: semi-deciduous
forest, flooded deciduous forest, coastal dunes, and secondary
forest (20 years of age).
At the study site and in its surroundings, 108 bird species
have been reported to include fruit in their diet (Ortiz-Pulido
et al. 2000), as well as 13 frugivorous bats (Phyllostomidae;
Saldaña-Vázquez et al. 2010) and 14 frugivorous non-flying
mammals (NFM), which are the group most affected by hu-
man disturbance (Morales Mávil and Guzmán 1994).
Recording interactions between plants and frugivores
Between April 2014 and May 2015, we carried out 12
samplings, one per month (19 ± 2.6 days per sampling).
In each sampling, we recorded all interactions between
plant species bearing fleshy fruits and three groups of
frugivores (birds, bats, and NFM). We established one
transect of variable length in each of four vegetation
types, with transect length proportional to the area cov-
ered by each vegetation type (semi-deciduous forest,
1338 m; flooded deciduous forest, 511 m; coastal dunes,
808 m; secondary forest, 1595 m). We did not aim to
compare these vegetation types, but rather to obtain a
representative sample of our study site. We used four
sampling methods to register interactions: focal observa-
tions (birds), mist net trapping (birds and bats), camera
trapping (NFM), and transects for scat collection (NFM).
In all cases, the number of fruits consumed was used as a
quantitative metric of the intensity or strength of the in-
teraction (sensu Bascompte and Jordano 2007) between a
frugivorous species and the plant species consumed.
Focal observations During each sampling, we walked the
length of each transect once, from dawn to 11:00 h and from
16:00 h to sunset (mean effort of 6.8 h ± 0.09 per transect), for
a total sampling effort of 531 observation hours. We focused
on species with endozoochorous syndrome, using observation
periods of 10–15 min for each species bearing ripe fruits. We
considered an interaction to have occurred when a bird species
was observed feeding on the fruits of a given plant species.
Observations were carried out using binoculars (Bushnell
10X42) and a digital photographic camera Canon
(PowerShot SX50 HS). We identified bird species with the
help of field guides (Peterson and Chalif 1989; Howell and
Webb 1995) and expert ornithologists. The number of fruits
consumed (i.e., interaction intensity) was quantified directly
during the observations.
Page 3 of 11 29
Camera traps We used 14 night vision cameras (LTL Acorn
6210MC), orientated towards fruiting plants and/or sites
where the presence of animal droppings had been previously
observed. Each camera was active for a period of 15 to
30 days, depending on the activity recorded at each site.
Total sampling effort (total number of cameras multiplied by
total sampling days; Medellín et al. 2006) was 4240 trap-days.
We identified mammal species with the help of reference
guides (Aranda 2000). We considered a plant-frugivore inter-
action to have occurred when a photo and/or video showed an
animal species feeding on the focal fruits.
Mist nets In each vegetation type, we used six mist nets (12 ×
2.5 m) for capturing birds. The nets were set on 1 day in each
vegetation type at each of the samplings and were active from
dawn to noon and from 16:00 h to sunset (a total of 8 h), with a
total sampling effort of 2496 net-hours for the entire study. To
collect fecal samples, we kept each captured bird in a fabric
sack with a metal mesh bottom for a period of 30 min (Heleno
et al. 2010).
To capture bats, we followed the same mist-netting proto-
col as that employed for the birds, except that the nets were set
from 20:00 h until 03:00 h, for a total sampling effort of 2184
net-hours. We identified species using specialized guides
(Medellín et al. 2008). Under each mist net, we placed a
12 × 1 m plastic sheet on the forest floor to collect defecated
seeds (Galindo-González et al. 2009). Bats that had not defe-
cated while in the net were placed inside a fabric sack for 10 to
30 min in order to collect the feces.
Transects for the collection of NFM scats To locate scats, we
conducted systematic walks along the four transects described
above, as well as intensive searches at open sites, on top of
logs and rocks and at the base of trees (Peredo et al. 2013).
Total sampling effort consisted of 86.5 search hours. Seeds
found in scats were dried for 12–24 h and then identified by
consulting existing collections for the study area.
For seed identification (focal observation and fecal sam-
ples), fruits from all plant species were collected along the
transects used for focal observations (see above) in order to
develop a reference guide with photographs of ripe fruit and to
record seed numbers per fruit. We estimated the number of
fruits consumed per animal by extrapolating from information
about the number of seeds contained in the fruit of each spe-
cies (M. Ramos-Robles, unpublished data).
Fruit traits
We measured fruit abundance, water content, morphological
traits, and fruiting phenology of each fruiting plant species.
From at least five individuals of each plant species observed in
interaction with frugivores, we randomly collected a total of
30 fruits and recorded the following variables: fresh fruit
29 Page 4 of 11
weight (g), dry fruit weight (g), fruit diameter (mm), fruit
length (mm), seed diameter (mm), fruit water content (%),
and life form (i.e., tree, shrub, or liana).
During each sampling, we estimated fruit abundance and
also made observations along the same transects (see above),
but defining a fixed width of 8 m, for a total sampled area of
1.7 ha. To estimate fruit abundance (F), we used a mature fruit
abundance index (Saracco et al. 2004) in which one of the
following categories was assigned to each fruiting individual:
1 = 1–10 fruits, 2 = 11–100 fruits, 3 = 101–1000 fruits, 4 =
1001–10,000 fruits, and 5 = > 10,000 fruits. We then calculat-
ed the mean values of these categories. The number of fruiting
individuals of each species (I) was estimated as the total num-
ber of individuals fruiting per sampling. To reduce bias, esti-
mations of visual abundance were conducted by the same
observer.
In addition to evaluating the fruiting phenology for each
plant species, we calculated the relative fruiting duration (D),
as the proportion of samples with mature fruits for each spe-
cies, relative to the total number of samplings. Finally, by
combining these basic variables (F, I, and D), we calculated
the following fruiting indices that consider the abundance and
fruiting phenology of each plant species:
& Index ID: the number of fruiting individuals (I) multiplied
by the relative duration of fructification (D).
& Index FD: the mean fruit abundance category (F) multi-
plied by the relative duration of fructification (D).
& Index FDI: the mean fruit abundance category (F) multi-
plied by the relative duration of fructification (D) and the
number of fruiting individuals (I).
& Index Frel: for each sampling, the number of fruits of each
species was divided by the total number of fruits of all
species. The overall average was then calculated for each
plant considering all samplings.
Data analyses
Data pertaining to the four types of vegetation were
pooled and considered as a single functional unit since
the animals move freely among them (Ortiz-Pulido et al.
2000). In order to evaluate sampling completeness, we
generated nonparametric species richness estimators
(Chao1, Jack1, Jack2, Bootstrap) to determine the ap-
proximate total number of frugivores and interactions.
An average of the four estimators was used as a measure
of the Btrue^ species richness (Posa and Sodhi 2006),
sinc e no sing le m etho d is cons id ered the best
(Chiarucci et al. 2003). All estimates were calculated
using the function Bspecpool^ of the Bvegan^ package
(version 1.15-2, J. Oksanen).
Sci Nat (2018) 105:29
Based on the plant-frugivore interactions recorded, we built
an adjacency matrix A, in which aij = number of fruits of plant
species (j) consumed by frugivore species (i) such that aij = 0
when no interaction between species j and i was recorded. We
then calculated different metrics (number of interactions,
nested contribution, and species strength) to describe the
structure of the plant-frugivore network.
In order to identify non-random interaction patterns, we
estimated nestedness using the NODF metric (Almeida-Neto
et al. 2008) in the software program ANINHADO (Guimarães
and Guimarães 2006). NODF values for the whole network
ranged from 0 (non-nested) to 100 (perfectly nested). To ver-
ify the significance of nestedness, we tested the empirical
values against null distributions of these values. In this case,
we computed 1000 simulated networks generated by the Null
Model II (Bascompte et al. 2003). In this null model, the
probability of occurrence of an interaction is proportional to
the number of interactions of both animal and plant species
(interaction richness).
Since our network was significantly nested (see
BResults^ section), we explored the relative contributions
of plants, birds, bats, and NFM to the nested pattern of the
network. We estimated the extent of nested contribution
(Nc), in which the interactions of plant or animal species
increase or decrease the overall network nestedness, and
compared this to our random expectations, following
Saavedra et al. (2011). Positive values of cni indicate a
greater contribution of species i to the nested structure
than would be expected by chance.
For each pair of interacting plant and animal species,
there are two estimates of mutual dependence (defined
in two adjacency matrices P and A): the dependence
dPij of plant species i on animal species j (i.e., the
fraction of all animal visits accounted for by this partic-
ular animal species) and the dependence dAji of animal
species j on plant species i (i.e., the fraction of all visits
by this animal species to this particular plant species;
Bascompte et al. 2006). The dependence value of a spe-
cies has a maximum of 1 if it relies only on a single
partner. Based on these dependences, we estimated spe-
cies strength, which is the sum of dependencies of each
species across all of its partners (counterpart); species
strength quantifies the importance of a given species to
the assemblage of species in the other trophic level with
which it interacts. We calculated species strength for the
animals to determine if a particular animal species or
group (birds, bats, and NFM) interacts more with the
plants. We also calculated this index for plants, in order
to assess whether the species strength of a plant species
is associated with fruit traits (abundance, water content,
morphological traits, and fruiting phenology). Network
metrics were computed with the bipartite package
(Dormann et al. 2009).
Sci Nat (2018) 105:29
In addition, to determine the position of the plant and fru-
givore species in the network, a central core-periphery analy-
sis was conducted using the equation
 
k i −k mean
Gc ¼
σk
where ki is the average number of links of frugivore species i,
kmean is the average number of links for all frugivore species in
the network, and σk is the standard deviation of the number of
links for all frugivore species in the network (Dáttilo et al.
2013). In this analysis, species with values of Gc > 1 present
a large number of interactions (or links) and constitute the
central core of highly connected species. Conversely, values
of Gc < 1 denoted species with a small number of interactions
or links, which constitute the network periphery.
We measured a total of 10 fruit variables (supplementary
Table S1). However, these variables were highly correlated
and eliminated from the analyses. The criterion by which to
decide which variables were to be eliminated was the variance
inflation factor (VIF < 3; Zuur et al. 2010), which estimates to
what extent the variance of the estimated regression coeffi-
cients has increased, in comparison to a context in which
prediction variables are not linearly related. For subsequent
analyses, we used fruit length, seed width, water content, the
number of fruiting individuals (I), and the index FD.
We tested whether the network metrics (response variables:
number of interactions, Nc, and species strength) calculated
for plant species were related to plant traits (predictor vari-
ables: fruit length, seed diameter, water content, number of
fruiting individuals (I), and index FD) using generalized linear
models (GLM). We began with a full model, then constructed
various models with different combinations of explanatory
variables, with the final model selected according to the low-
est AICc (Akaike’s information criterion) value, where the
ΔAICc value < 2 between models. For the models, a
Gaussian type error distribution was used (Zuur et al. 2009)
with the packages MASS Survey, Design and AER. All sta-
tistical analyses were carried out using R version 3.3.0 (R
Core Team 2014, http://www.r-project.org).
Results
A total of 3156 interactions were recorded between 28
plant species (18 families) and 58 frugivorous species
(22 families). Of the total number of interactions ob-
served, 81% involved birds (18 families), 12% bats (1
family), and 7% were non-flying mammals (3 families;
Fig. 1, supplementary Table S2). The average of estima-
tors indicated that we recorded 74% of the frugivorous
species and 59% of the plant-frugivore interactions.
Page 5 of 11 29
We found that the mutualistic network was significantly
nested (observed matrix, NODF = 38.81; simulated matrices,
NODF = 22.96 ± 1.92; P < 0.05). The species that most con-
tributed to the nestedness were the trees Bursera simaruba
and Ficus obtusifolia and the bird Pitangus sulphuratus
(Fig. 2). Similarly, the plants contributed more to the nested
pattern among trophic levels. We also found that five plant
species and 14 frugivorous species presented negative values
that decreased the nested pattern (i.e., specialized or idiosyn-
cratic interactions), for example, the bat species Carollia
perspicillata with Piper sp., or the interactions of opportunis-
tic species, such as the bird Quiscalus mexicanus interacting
with Chrysobalanus icaco (supplementary Table S2).
The central core-periphery analysis showed that only four
plant species were part of the central core network:
B. simaruba, F. obtusifolia, Ficus cotinifolia, and Nectandra
salicifolia (supplementary Table S2). In the case of the frugi-
vores, only birds formed part of the core and nine species in
particular: Dumetella carolinensis, Megarynchus pitangua,
Melanerpes aurifrons, Myiozetetes similis, Ortalis vetula,
Pitangus sulphuratus, Tangara abbas, Tityra semifasciata,
and Turdus grayi (supplementary Table S2). In general, the
species strength of animal groups showed low mean values
(< 1). However, there were species with high values (1.8–3) in
each of the groups: the bird species P. sulphuratus,
Patagioenas flavirostris, Tyrannus tyrannus, and
D. carolinensis (the last two are migratory); the bat Artibeus
jamaicensis; and the raccoon (NFM) Procyon lotor (Fig. 3,
supplementary Table S2). On the other hand, the plants that
showed the highest species strength values (1.7–8) were the
trees B. simaruba and F. obtusifolia (supplementary Table S2).
Regarding the fruit traits, we found that the shrub
C. icaco and the mistletoe Phoradendron quadrangulare
were those with the longest (27.7 mm) and shortest
(4.5 mm) fruit lengths, respectively; C. icaco and
F. cotinifolia presented the highest (16.6 mm) and lowest
(0.7 mm) seed diameters, respectively, while Chiococca
alba and B. simaruba presented the highest (92%) and low-
est (27%) fruit water content values, respectively (supple-
mentary Table S1). Chiococca alba presented the highest
number of fruiting individuals (92; supplementary
Table S1). When analyzing network parameters in terms
of the relationship between response variables obtained for
the plants (species strength, number of interactions, and
nestedness contribution) and predictor variables (fruit
traits), we found that species strength had a negative rela-
tionship with fruit length and with water content, but a pos-
itive relationship with fruit abundance (index FD; Table 1).
With respect to the number of interactions and nestedness
contribution, these metrics showed higher values for species
with smaller fruits and lower water content. Finally, the
species that showed the highest values of index FD contrib-
uted most to the nested network pattern (Table 1).
29 Page 6 of 11
Fig. 1 Plant-frugivore interaction network at the La Mancha Coastal
Research Center (CICOLMA). Nodes represent plants, birds, bats, and
non-flying mammals. The width of links and nodes corresponds to the
intensity of the interaction. Black circles indicate species that are part of
Discussion
One of the main contributions of this study was identification
of the fruit traits (abundance, size, water content, and phenol-
ogy) that shape plant-frugivore interactions in a seasonal for-
est in Mexico. Frugivory was higher in plant species with
small (< 14 mm), low water content fruits and long temporal
abundance (index FD). In addition, unlike most studies of
plant-frugivore networks, we included the three main groups
of frugivores present in the tropical ecosystems (i.e., birds,
bats, and NFM). In general, we found that our plant-
frugivore network exhibited a nested pattern of species inter-
actions. In this study, birds and plants contributed more to the
nestedness than bats and NFM. This is to be expected, con-
sidering that birds constitute the most abundant and diverse
group in the frugivorous community in our study area
(Ramos-Robles et al. 2016).
Our results show that three tree species with small seeds
(e.g., Bursera simaruba, Ficus obtusifolia, and F. cotinifolia)
were important to the structure and contributed substantially to
the nested pattern of the network (e.g., Vidal et al. 2014). These
species attract a great variety of frugivores from different guilds
with the capacity to consume large amounts of fruit (David
et al. 2015; Muñoz et al. 2017). Several studies have shown
the importance of these plant genera for the maintenance of
Sci Nat (2018) 105:29
the generalist central core of the network. The names of species are coded
as follows: plants (Pl), birds (B), bats (Ba), and non-flying mammals
(NFM). See supplementary material S2 for full species names
many frugivorous species in the neotropics (e.g., Janzen
1979; Fleming and Kress 2013; Almazán-Núñez et al. 2015).
Recent studies have highlighted that only a few species
tend to contribute strongly to the nested network pattern and
that these may play an important role in the long-term conser-
vation of interactions (Rohr et al. 2014; Pawar 2014). Another
important characteristic of these plant species is the individual
asynchronous fruiting (Scott and Martin 1984) and this may
guarantee food availability almost all year round, in contrast to
those species with synchronic fructification (Janzen 1979).
Other studies of plant-frugivore networks have reported that
plant species with long fructification periods play an impor-
tant role in network structuring (Donatti et al., 2011; Vidal
et al. 2014). Bursera and Ficus trees are considered Bkeystone
resources,^ since they have a strong positive effect on ani-
mals, maintaining high abundances at the population level,
as well as high diversity and community structure and ecosys-
tem functioning (Terborgh 1986; Diaz-Martin et al. 2014).
Species abundance and animal behavior are important traits
related to network structure (Vázquez et al. 2009; Dáttilo et al.
2013). In our study, we found that abundant bird species and
habitat generalists (e.g., Pitangus sulphuratus and
Megarynchus pitangua; Ortiz-Pulido et al. 2000) contributed
strongly to the nested pattern. Moreover, these bird species
exhibited territorial behavior (e.g., they were competitively
Sci Nat (2018) 105:29
Fig. 2 Contribution of plant and frugivore species to the nested structure
of the network at the La Mancha Coastal Research Center (CICOLMA). a
Species are organized in decreasing order according to their contribution
to nested structure (supplementary material S2). b Contribution to
nestedness by taxonomic group of the species that integrate the plant-
frugivore mutualistic network. Values for individual species (circles),
the median (central line), and extreme values (bars) are presented
superior and/or aggressive; M. Ramos-Robles, personal ob-
servations), being more central in the network structure.
Fig. 3 Species strength of
frugivores in plant-frugivore
interactions at the La Mancha
Coastal Research Center
(CICOLMA). Values for
individual species (circles), the
median (central line), and extreme
values (bars) are presented
Page 7 of 11 29
On the other hand, we identified an idiosyncratic interac-
tion between two species, which only interact with each other
(Guimarães and Guimarães 2006) and thus decrease the
nested pattern of a network (Atmar and Patterson 1993).
This interaction occurred between the shrub Chrysobalanus
icaco (Chrysobalanaceae) and the opportunistic bird
Quiscalus mexicanus; this shrub species is characterized by
large fruits and seeds, while the bird species is adapted to
disturbed and urbanized environments (Christensen 2000).
This is important since, according to our data, bigger fruits
imply fewer interactions and are less frequently consumed by
the frugivorous community (e.g., Muñoz et al. 2017). In ad-
dition, we recorded a specialized interaction between the
Seba’s short-tailed bat (Carollia perspicillata) and plants of
the genus Piper. This bat species has been previously recog-
nized as a Piper specialist disperser (Fleming 1988; Thies
et al. 1998). In this context, it is important to determine wheth-
er a frugivore species could replace the seed dispersal service
of plants that have lost their local dispersers. We therefore
consider that the identification of idiosyncratic and specialized
interactions can have important implication in terms of the
conservation and management of tropical forest.
In general, none of the three groups of frugivores presented
a particularly strong relationship (species strength) with
plants, since certain species in each group had a high value
of species strength, e.g., the resident bird P. sulphuratus and
the two migratory birds Tyrannus tyrannus and Dumetella
carolinensis, the bat Sturnira parvidens, and the NFM
Procyon lotor. These frugivore species may have implications
for the survival of the plant species with which they interact,
given their abundance and behavior. For example, the great
kiskadee (P. sulphuratus) uses different types of vegetation in
the landscape, promoting connectivity among fragments and
facilitating the gene flow of plant species (Ortiz-Pulido et al.
2000; Díaz Vélez et al. 2015). Moreover, migratory birds are
29 Page 8 of 11 Sci Nat (2018) 105:29

Table 1 Effects of network metrics of plant traits of 28 fleshy fruited plant species from the plant-frugivore network. We report estimates from
plant species in CICOLMA. Network metrics: number of interactions, the single best model, as well as the standard error (S.E.). *P < 0.05;
species strength, and contribution to nestedness were estimated for each **P < 0.01; ***P < 0.001; ns, no significant effects

Predictor Number of interactions Species strength Nested contribution

Estimate S.E. t P Estimate S.E. t P Estimate S.E. t P

Intercept 25.00 5.56 4.49 *** 5.47 2.67 2.04 ns 3.93 0.94 4.15 ***
Fruit length (mm) − 0.50 0.12 − 4.00 *** − 0.16 0.06 − 2.71 * − 0.09 0.02 − 4.52 ***
Seed width (mm) 0.49 0.36 1.36 ns 0.290 0.17 1.68 ns 0.04 0.06 0.65 ns
Water content (%) − 0.25 0.06 − 3.95 *** − 0.08 0.03 − 2.76 * − 0.04 0.01 − 3.71 **
Individual fruiting 0.08 0.05 1.37 ns 0.01 0.02 0.65 ns 0.01 0.01 1.66 ns
Index FD1 3.37 1.71 1.97 ns 2.99 0.82 3.63 ** 0.86 0.29 2.97 **
1
Considers fruit abundance and the duration of fructification throughout the sampling year

less susceptible to disturbances and use abundant resources,
rarely used by resident birds, found in patches and open sites
(Mulwa et al. 2013). This could have an effect on seed dis-
persal (Jordano 1987), as has already been reported in the
study site (Ramos-Robles et al. 2016).
Among the bat species, one of the most important seed
dispersers is the northern yellow-shouldered bat (Sturnira
parvidens), which has been reported as an abundant and ef-
fective seed disperser (Mello et al. 2008). This bat species is
important for the dispersion of the plant species on which it
feeds and thus for the conservation and regeneration of eco-
systems (Mello et al. 2015). Likewise, the medium-sized op-
portunistic raccoon (P. lotor) has been reported as being high-
ly frugivorous and a disperser of the seeds of several plant
species (Cypher and Cypher 1999). We therefore infer that,
given the scarcity of medium and large frugivores in our study
region, the raccoon is replacing the function of these species in
disturbed (or defaunated) tropical forests. However, more re-
search is needed to determine whether this process is occur-
ring, as well as to evaluate the effectiveness of the raccoon as a
seed disperser. This is very important at the ecosystem level,
since larger frugivores consume a higher quantity of fruits and
disperse their seeds at greater distances, which could favor
meta-community dynamics (Donatti et al. 2011; Vidal et al.
2013). Our results suggest that the animal species that appear
to be important for plants, due to their high species strength
values, could favor the dispersal of seeds of the species they
feed on (Ruggera et al. 2016; Palacio et al. 2016). In other
studies, it has been shown that the morphological traits of
frugivore species are related to the network parameters
(Dehling et al. 2016). We have not considered these variables
in this study; however, we believe that when considering sev-
eral frugivore groups, other characteristics such as body size
may have greater relevance than gape width as previously
reported (Donatti et al. 2011).
Our results have shown that small, dry fruits are important
to the frugivorous community in a seasonal forest in Mexico.
In particular, dry fruits (i.e., rich in lipids; Stapanian 1982)
have long and asynchronous fruiting patterns (Carlo et al.
2007) and can contribute to the diet of migratory birds (e.g.,
Bursera, Nectandra; Ramos-Robles et al. 2016). In contrast,
watery fruits (i.e., high in carbohydrates; Levey et al. 1994)
have a short and synchronous fruiting period (e.g., Psychotria
erythrocarpa, Vitis bourgaeana), and their short temporal
availability could make them less important to the community
of frugivores. However, these results must be viewed with
caution since we only measured fruit water content.
Furthermore, it is possible that the plants with larger seeds at
our study site might be experiencing deficient seed dispersal
as a result of mammal defaunation. In the future, this could
lead to homogenization of plants that produce small fruits and
have a negative impact on the recruitment of other plant spe-
cies (e.g., with large fruits; Galetti et al. 2013).
In this seasonal forest, we found plant species with two
contrasting fruiting displays (1) Bmassive fruiting,^ plants that
are attractive to frugivores and consumed in relatively short
and discrete periods (e.g., Dendropanax arboreus), and (2)
Basynchronous fruiting,^ plants that are constantly consumed
by frugivores, since their fruits are almost constantly available
(e.g., Ficus spp.). Our study has shown that the plant species
with greater fruit abundance had stronger interactions with
frugivores (i.e., higher values of species strength), since they
presented longer fruiting periods and/or larger fruit crops.
Most plant-frugivore studies have analyzed individual metrics
related to fruit availability, such as fruit abundance or plant
richness (Chama et al. 2013; García et al. 2014), without con-
sidering that animals respond differently to various fruiting
strategies.
We recommend the use of resource availability estimators
that combine several fruit traits since a single variable (e.g.,
number of fruits or individuals, or the richness of species) may
incur bias and cannot explain the network patterns. In this
case, results from such networks may only lead to partial
rather than comprehensive conclusions. Tropical forests have
a great diversity of species and we therefore used four com-
plementary methods for recording interactions between the
Sci Nat (2018) 105:29
plants and frugivores. While the species of trees and birds
contributed most to the nested pattern, we have shown that
plants do not depend on a single group of frugivores. This
finding is particularly important in disturbed sites. As we dem-
onstrate here, analysis of networks allows us to determine the
functional role of the species or guilds, since these can con-
tribute differentially to the structure of the networks (Dáttilo
et al. 2016; Ramos-Robles et al. 2018).
Finally, we propose to promote reforestation with native
species that are consumed by the three frugivorous guilds.
We also consider it necessary to evaluate non-flying mammal
populations in order to design species refaunation strategies
considering their ecological function. Studies such as this pro-
vide the guidelines for evaluation of the ecological importance
of the different frugivorous guilds in regions under great an-
thropogenic pressure, such as tropical forests.
Acknowledgments We thank Antonio López-Carretero for his help in the
field and Javier Laborde for making invaluable suggestions on an early
version of this manuscript. Thanks also go to Enrique Romero for his help
with bird identification, Ángel Méndez for his help with camera trap
installation, and to all the field assistants, as well as all the personnel
working at Centro de Investigaciones Costeras, La Mancha.
Funding information This work was partially funded by the following
grants and institutions: Consejo Nacional de Ciencia y Tecnología (grant
number 234062) to R.R.M. (project number 2010-152884), SEP-
CONACYT to E. A., and Instituto de Ecología, A.C. (project number
2003011143) to CDC.
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