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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(4): 1149-1163, October-December 2021 (Published Oct. 26, 2021)

Time partitioning among neotropical frugivorous bats:

effects of phylogeny, body size, and abundance

Manuel Francisco Cano

; https://orcid.org/0000-0002-0238-1762

Oscar E. Murillo-García

; https://orcid.org/0000-0001-5040-7894

1. Grupo de Ecología Animal, Departamento de Biología, Universidad del Valle, Cali, Valle del Cauca, Colombia;

manuel.cano@correounivalle.edu.co (*Correspondence), oscar.murillo@correounivalle.edu.co

Received 18-VI-2021. Corrected 20-IX-2021. Accepted 13-X-2021.

ABSTRACT

Introduction: Resource partitioning by promoting coexistence is essential to determine species richness and

composition in natural communities. However, the partitioning of time has been questioned as a mechanism that

promotes the coexistence of ecologically similar species.

Objective: To determine the importance of the partitioning of time as a mechanism that promotes coexistence,

we compared the activity patterns of tropical frugivorous bats.

Methods: We captured bats with mist nets from sunset to sunrise in three study sites (tropical dry forest, wet

forest, and rainforest) to calculate activity patterns of the species using Kernel density estimation. We used the

superposition coefficient (Δ

) to compare activity patterns between (1) bat assemblages of study sites, (2) fru-

givorous species in the same site, and (3) populations of the same species among different sites. To determine

whether the overlap in the activity patterns was related to the ecological similarity of species, we evaluated the

association between Δ

and similarity in abundances and body mass and phylogenetic closeness.

Results: We found geographical variations in the overall activity patterns of the assemblages of the three locali-

ties. Likewise, we found variations in activity patterns between species at each study site and between popula-

tions in different study sites. Overlap in activity patterns tended to decrease as species were phylogenetically

more closely related and similar in abundance and body size.

Conclusions: Our results provide empirical support for the role of temporal segregation in activity patterns as a

mechanism that promotes the coexistence of ecologically similar species in nature.

Key words: competition; niche overlapping; temporal segregation; ecological segregation; ecologically similar

species; species coexistence.

Cano, M. F., & Murillo-García, O. E. (2021). Time partitioning

among neotropical frugivorous bats: effects of phylogeny,

body size, and abundance. Revista de Biología Tropical,

69(4), 1149-1163. https://doi.org/10.15517/rbt.v69i4.47487

https://doi.org/10.15517/rbt.v69i4.47487

Interspecific interactions are essential to

determine species richness and composition in

natural communities (Chase & Leibold, 2003;

Colorado-Zuluaga, 2015; Diamond, 1975). In

particular, competition is considered a critical

interaction since its reduction or avoidance

promotes resource partitioning of ecological-

ly similar species (Holt, 2001; Klatt et al.,

2015). Thus, temporal and spatial segregation

of ecologically similar species can result from

the effect of interspecific competition, which

may have ecological and evolutionary implica-

tions by constituting a mechanism that allows

coexistence between species and, so, affect-

ing the structure of biological communities

(Kronfeld-Schor & Dayan, 2003). The remov-

al of an ecologically similar species leads

to changes in the temporal activity patterns

VERTEBRATE BIOLOGY

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and habitat use of competing species (Ziv et

al., 1993), suggesting temporal segregation;

however, it is considered less common than

dietary specialization and spatial segregation

(Schoener, 1974). Consequently, the ecological

significance of segregation in temporal activ-

ity to facilitate the coexistence of species is

still controversial (Zeppelini et al., 2017), and

this segregation is usually associated with the

circadian rhythms of species (Kronfeld-Schor

& Dayan, 2003).

The temporal activity patterns of species

can vary across their geographic ranges in

response to biotic and abiotic factors (Vieira

et al., 2017). In small mammals, the degree of

flexibility in the temporal activity pattern is

associated with predation risk, so species with

a higher predation risk tend to have less flex-

ible activity patterns (Halle & Stenseth, 2000).

Besides, abiotic factors (such as temperature,

precipitation, and photoperiod) tend to influ-

ence the activity patterns of certain groups of

organisms (Kronfeld-Schor & Dayan, 2003;

Vieira et al., 2017), with different effects and

magnitudes depending on the animal group

(Vieira et al., 2017). Variations in the daily

activity patterns of species between locations

possibly reflect fluctuations in food availability

or foraging strategies (O’Donnell, 2010; Vieira

et al., 2017). Due to the multiple factors that

can influence the temporal activity of species,

assessing the importance of temporal segrega-

tion as a mechanism of coexistence requires

understanding spatial and temporal variation in

activity patterns of ecologically diverse groups.

However, partitioning of time among species

has been less studied than spatial partitioning.

Bats are highly diverse, abundant, and

ecologically important in tropical forests; thus,

understanding their activity patterns can help

unravel the mechanisms that determine the

local diversity of assemblages. Temporal activ-

ity patterns are known for some species of Neo-

tropical bats (Brown, 1968; Rocha et al., 2020;

Zeppelini et al., 2017), vary spatially, and are

influenced by the availability of resources:

vegetation structure, nectar availability, energy

requirements, and activity patterns of their

preys (Kunz, 1973; Rothenwöhrer et al., 2011).

For insectivorous bats, the temporal variation in

activity patterns is related to the temporal dis-

tribution of insects (Hagen & Sabo, 2014; Kue-

nzi & Morrison, 2003; Speakman et al., 2000).

For canopy frugivores, there are regulatory fac-

tors of the activity patterns as climatic seasons

and lunar cycles, mainly associated with full

moon nights (Lang et al., 2005; Santos-Moreno

et al., 2010; Zeppelini et al., 2019) and several

unpredictable factors such as precipitation and

environmental disturbance (López-González et

al., 2012; Milne et al., 2005). However, despite

the high local richness of bats, time partitioning

as a mechanism structuring bat assemblages

remains poorly studied.

Neotropical frugivorous bats, in particular,

are a rich local guild with a high potential for

niche overlap and interspecific competition,

resulting from a close phylogenetic relationship

since all species belong to the Phyllostomidae

family. Thus, studying Neotropical frugivorous

bats’ activity patterns can help to understand

the mechanisms that allow the coexistence of

species in highly diverse assemblages. For bats

of Carolliinae subfamily, differences in noctur-

nal activity among closely related have been

reported (Bonaccorso et al., 2007; Delaval et

al., 2005). Besides, base on a high spatial over-

lap on foraging sites, the differences in mean

emergence time among Carollia castanea y C.

brevicauda seem to avoid competition and sug-

gests the existence of exploitative competition

between them (Bonaccorso et al., 2007). How-

ever, comparisons of activity patterns between

pairs of closely related species have concluded

that the activity peaks of fruit bats have not

evolved to reduce competition between them

(Aguiar & Marinho-Filho, 2004; Zeppelini et

al., 2017). Hence, empirical studies are needed

to fully understand the importance of segrega-

tion in temporal activity as a mechanism that,

by reducing competition, promotes coexistence

in bat assemblages.

To understand the importance of time

partitioning for the coexistence of ecologi-

cally similar species, we studied the temporal

activity patterns of assemblages of Neotropical

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frugivorous bats in three ecosystems (tropical

dry forest, wetforest, and rainforest). We com-

pared the degree of overlap in temporal activity

at different levels: A) Community, contrasting

assemblages between study areas; B) inter-

specific, comparing species inside each of the

assemblages; and C) intra-specific, comparing

the same species between study areas. We

compared temporal activity by estimating the

degree of overlap in hourly activity between

species pairs. Additionally, we evaluated the

association between the degree of overlap in

temporal activity and the differences in body

size, abundance, and phylogenetic relationship

at each site. We predict that: (1) the temporal

overlap between assemblages of bats will be

low, indicating that temporal activity patterns

will be different between assemblages due to

adjusting of species to contrasting local envi-

ronmental and biotic conditions between sites

(O’Donnell, 2010; Vieira et al., 2017; Vilella

et al., 2020); (2) in each site, the overlap in

temporal activity of species will decrease as

species are more similar in size, abundance, or

phylogenetically (Castro-Arellano & Lacher,

2009; Nagy-Reis et al., 2018) and (3) the tem-

poral overlap between populations of the same

species will be low, indicating that temporal

activity patterns of the same species will dif-

fer between sites due to adjusting of species to

contrasting local biotic and abiotic conditions

between sites (O’Donnell, 2010; Vieira et al.,

2017; Vilella et al., 2020).

MATERIALS AND METHODS

Study area: The research was carried out

in three study sites that, according to Hold-

ridge (1967), represent different life zones

in Valle del Cauca, Colombia (Fig. 1). 1) El

Vínculo Regional Natural Park (3°50’12” N &

76°17’58” W): A protected fragment of tropical

dry forest of 83 ha (Funagua, 2010) with wood-

ed areas in different stages of natural regenera-

tion such as intervened primary forest (Bp-i),

secondary forest (Bs), and scrub (M) (Cadelo-

Cabrera & Parra-Valencia, 2007). El Vínculo

has altitudes between 997 and 1 150 m above

sea level (m.a.s.l.), an average temperature of

25 °C, and an annual rainfall of 1 380 mm.

Fig. 1. Study area showing sampling sites. Dry forest (El Vínculo Regional Park), wet forest (Pericos Community Reserve),

and rainforest (Bachué Reserve).

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2) Pericos Natural Reserve (3°50’39” N &

76°47’22” W): A community-managed reserve

that contains an extensive area of wet forest

(440 ha) in the Choco Biogeographic region,

on the Western slope of the Western mountain

range of the Andes. The reserve is located in

the Dagua river basin at 500 m.a.s.l., has a high

annual rainfall of above 5 000 mm, and temper-

atures above 24 °C (Funagua, 2010). 3) Bachué

Nature Reserve (3°19’50” N & 76°39’15” W):

A private reserve of 2 000 ha of rainforest with

intervened primary and secondary forest areas

in the Tropical Andes region. It is located in

the Farallones de Cali National Natural Park

buffer zone at 1 800 m.a.s.l., at the confluence

of the Pato and Pance rivers. The temperature

varies from 16 to 24 °C and has an annual rain-

fall between 2 000 and 3 000 mm (Fundación

Farallones, 2013).

Sampling method: We sampled bats

between July and October 2018 using mist

nets. Each study site was sampled once at

nighttime for a total sampling of 44 nights: 15

nights at the Vínculo and Pericos and 14 nights

at Bachué. To determine the activity patterns

of the frugivorous bats, we captured specimens

using ten mist-nets (2.5 × 12 m) for a total

of 158 400 m

-net/h in the localities: 54 000

-net/h in Vínculo and Pericos, and 50 400

-net/h in Bachué.

The mist nets were deployed in areas suit-

able for bat captures, such as forest clearings,

trails, and water sources. We relocated them

every two nights to include the variation in

vegetation cover of each locality. The nets were

checked hourly, from 18:00 to 6:00 h, due to

the low catch rates of individuals. However,

in case of rain, intervals of net checking were

shorter, or nets were closed. We kept all cap-

tured individuals in cloth bags and classified

them taxonomically using a field guide from

South America (Díaz et al., 2016). Addition-

ally, the weight of each individual was recorded

and considered as a surrogate of body size.

To avoid pseudo-replication, individuals were

marked with haircuts in the lower dorsal region

(close to the uropatagium). Finally, we fed

individuals with fruit compote before being

released. The study was covered by the permit

for the sampling and handling of wild animals

1 070 (28/08/2015) issue by National Authority

for Environmental Licenses (ANLA) to Uni-

versidad del Valle. All applicable international,

national, and institutional guidelines for the

care and use of animals were followed.

Data analysis: We used the distribution

that describes the probability of capture within

any particular hourly interval of the day to

characterize the temporal activity patterns.

Thus, we used the probability density func-

tion, calculated with the Kernel method of the

overlap R-package (Meredith & Ridout, 2017),

to describe activity patterns. First, we calcu-

lated the activity pattern for each assemblage

of frugivorous bats (by adding all the capture

data from a given site) and for each species at

each locality. For analysis, we only considered

species with at least ten records. Posteriorly,

we quantified the extent of overlap between

the correspondent estimated distributions of

two assemblages or species to compare activ-

ity patterns. The overlapping coefficient (Δ

)

quantifies the area of overlap between pairs

of density curves and is recommended for

small sample sizes (less than 50 records per

species) (Meredith & Ridout, 2014). So, we

used Δ

to quantify the differences in hourly

activity between assemblages or species. This

coefficient varies between 0 (no overlap) and

1 (complete overlap) (Linkie & Ridout, 2011;

Meredith & Ridout, 2017). Finally, we gener-

ated 95 % confidence intervals for ∆1 using

the Bootstrap method from 1 000 repetitions

(Meredith & Ridout, 2014). Then, we used

these confidence intervals to determine wheth-

er activity patterns were different (between

assemblages and populations of species in

various sites) or whether temporal segregation

was present (between species at each site).

Between sympatric species of genus Carollia,

the early emergence of 14 min for the small

species (C. castanea) is enough to foraging,

avoiding competition with the more dominant

and larger species (C. brevicauda) (Bonaccorso

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et al., 2007). Thus, we considered differences

or temporal segregation when the upper levels

of confidence intervals for the overlap index

were less than 0.9, indicating that the activity

patterns diverged by at least 10 %.

To determine whether the overlap in the

activity patterns was related to the ecological

similarity of species, we evaluated the associa-

tion between Δ

and similarity in abundances

and body mass and phylogenetic closeness.

For this, we calculated matrices of similarity in

activity patterns (Δ

), differences in body mass

and abundance, and phylogenetic distance for

each pair of species at each site. We calculated

the abundance matrix based on the differences

in captures between species from the same

locality, the body size matrix based on the dif-

ference in average body mass between each

pair of species, and the phylogenetic matrix

based on the patristic distances (index of phy-

logenetic distance) between species pairs using

a phylogeny of Noctilionoidea superfamily

(Rojas et al., 2016), which includes more than

90 % of genera and 76 % of the superfamily

species. Finally, to determine the degree of

association of the temporal overlap matrix with

the matrices of abundance, body size, and phy-

logenetics, we performed Mantel tests using the

vegan package (Oksanen et al., 2017) in the R

programming language (R Core Team, 2017).

RESULTS

A total of 21 species (350 individuals) of

frugivorous bats were captured. The highest

species richness was found in the site of wet

forest (Pericos: 13 species), followed by the

site of rainforest (Bachué: 10 species), and the

site of dry forest (El Vínculo: 7 species). Fru-

givorous bats of the genera Carollia and Arti-

beus obtained the highest number of records

in the wet forest and dry forest sites, while

those of genus Sturnira were dominant in the

rainforest site. Small frugivorous bats, such as

those of genus Vampyressa, had a low number

of captures (Table 1).

TABLE 1

Species richness and abundance of frugivorous bats

in El Vínculo (dry forest), Pericos (wet forest),

and Bachué (rainforest) study sites

Species (sp. / spp.)

Locality

El Vínculo Pericos Bachué

Artibeus aequatorialis

0 16 0

Artibeus jamaicensis

0 3 0

Artibeus lituratus

26 0 2

Artibeus planirostris

22 0 0

Carollia brevicauda

3 16 50

Carollia castanea

0 27 1

Carollia perspicillata

10 16 1

Dermanura anderseni

0 0 8

Dermanura Phaeotis

1 16 0

Dermanura sp 1

3 0 0

Dermanura sp 2

0 12 0

Enchistenes hartii

0 0 2

Platyrrhinus chocoensis

0 3 0

Platyrrhinus dorsalis

0 7 1

Rhinophylla alethina

0 21 0

Sturnira bogotensis

0 0 20

Sturnira erythromos

0 0 2

Sturnira koopmanhilli

0 1 0

Sturnira ludovici

0 0 41

Sturnira parvidens

0 0 2

Uroderma convexum

10 1 0

Vampyressa thyone

0 6 0

Total 75 145 135

The activity patterns of assemblages of

frugivorous bats were variable among sites.

The assemblage at the dry forest showed a

bimodal pattern, with activity peaks during the

first two hours after sunset and the last two

hours before sunrise (Fig. 2A). On the other

hand, the activity patterns of the wet forest

and rainforest assemblages were unimodal,

with a peak of activity during the first hours

of the night and a gradual decrease in activity

(Fig. 2B, Fig. 2C) respectively. The observed

overlap coefficients (∆1) in hourly activity was

lower between the sites with unimodal activity

pattern than between them and the site with

bimodal pattern: Wet forest – dry forest (∆1 =

0.675, IC = 0.555-0.751) , wet forest – rainfor-

est (∆1 = 0.791, IC = 0.612-0.838) and dry for-

est - rainforest (∆1 = 0.588, IC = 0.444-0.652).

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The overlap in temporal activity patterns

between sympatric species of frugivorous bats

(Table 2) was high and variable. At the dry

forest of El Vínculo, the observed overlap

coefficients (∆1) in hourly activity were on

average 0.76 ± 0.06 with a difference greater

than 10 % for all pairs of species (upper level

of confidence intervals less than 0.9); except

for Carollia perspicillata and Artibeus lituratus

(Table 2).

At the wet forest of Pericos, the observed

overlap coefficients were on average 0.70

± 0.16, with 20 out of the 27 comparisons

between species differing by more than 10 %

(confidence intervals with values lower than

0.9) (Table 3). This difference was especially

marked between Rhinophylla alethina and Car-

ollia castanea since the confidence interval for

∆1 was the lowest (∆1 = 0.530, IC = 0.359-

0.800) (Table 3), indicating a difference of

Fig. 2. Estimates of activity patterns overlap for frugivorous bat assemblages between different ecosystems: Dry forest (El

Vínculo Regional Park), wet forest (Pericos Community Reserve), and rainforest (Bachué Reserve). Comparison between A.

Wet forest and dry forest B. Wet forest and rainforest C. Rainforest and dry forest. The shaded area represents the overlap

coefficient (∆1).

TABLE 2

Mean hourly overlap (95 % confidence interval) in temporal activity between the most abundant species

of frugivorous bats in a dry forest (El Vínculo Regional Park)

Species (sp.)

Artibeus lituratus Artibeus planirostris Carollia perspicillata Uroderma convexum

Artibeus lituratus

1 0.708 (0.452-0.850) 0.878 (0.500-0.907) 0.748 (0.408-0.862)

Artibeus planirostris

1 0.714 (0.366-0.851) 0.766 (0.391-0.882)

Carollia perspicillata

1 0.737 (0.325-0.847)

Uroderma convexum

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TABLE 3

Mean hourly overlap (95 % confidence interval) in temporal activity between the most abundant species

of frugivorous bats in a wet forest (Pericos Community Reserve)

Species (sp.)

Artibeus

aequatorialis

Carollia

brevicauda

Carollia

castanea

Carollia

perspicillata

Dermanura

sp. 2

Dermanura

phaeotis

Platyrrhinus

dorsalis

Rhinophylla

allethina

Artibeus aequatorialis

1 0.765

(0.442-0.907)

0.684

(0.427-0.882)

0.731

(0.400-0.879)

0.644

(0.442-0.880)

0.884

(0.517-0.937)

0.654

(0.250-0.855)

0.548

(0.313-0.813)

Carollia brevicauda

1 0.686

(0.454-0.891)

0.792

(0.471-0.919)

0.713

(0.396-0.896)

0.835

(0.477-0.938)

0.668

(0.250-0.866)

0.751

(0.490-0.925)

Carollia castanea

1 0.782

(0.545-0.922)

0.868

(0.528-0.917)

0.690

(0.435-0.888)

0.680

(0.332-0.879)

0.534

(0.359-0.800)

Carollia perspicillata

1 0.833

(0.458-0.917)

0.773

(0.438-0.899)

0.642

(0.273-0.853)

0.615

(0.386-0.855)

Dermanura sp. 2

1 0.677

(0.327-0.868)

0.685

(0.327-0.868)

0.570

(0.418-0.890)

Dermanura phaeotis

1 0.616

(0.235-0.851)

0.604

(0.347-0.863)

Platyrrhinus dorsalis

1 0.564

(0.200-0.814)

Rhinophylla allethina

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more than 20 % in the activity patterns of these

two species. This marked segregation between

the activity patterns of both species is because

the peak activity of R. alethina occurs around

21:00 h, when the activity of C. castanea has

decreased (Fig. 3).

Finally, at the rainforest of Bachué, the

average overlap coefficient was 0.67 ± 0.11,

with differences greater than 10 % between the

two species of Sturnira (S. bogotensis and S.

ludovici) and between them and C. brevicauda

(Table 4). The overlap was particularly lower

between S. bogotensis and S. ludovici (∆1 =

0.456, IC = 0.269-0.677). The activity of S.

bogotensis is restricted to the first four hours

at night (18:00-22:00 h), while S. ludovici

increases after 21:00 h and remains relatively

constant until before dawn (Fig. 4).

We found contrasting activity patterns

between populations of the same species from

different locations. For Carollia perspicillata,

we found a difference greater than 10 % in tem-

poral activity between Pericos and El Vínculo

populations (Δ

= 0.695, CI = 0.415-0.896),

with El Vínculo individuals exhibiting a second

activity peak just before the dawn that was not

observed in Pericos (Fig. 5A). However, Carol-

lia brevicauda´s activity patterns did not differ

between Pericos and Bachué (Δ

= 0.800, CI

= 0.498-0.924), with both populations having

higher activity at the beginning of the night and

a gradual decrease after (Fig. 5B).

We found evidence for an association

between the temporal overlap and traits related

to ecological similarity in some sites with high

effect sizes indicating moderate to strong cor-

relations (R > 0.64) but no significant due to

Fig. 3. Estimates of activity patterns overlap for R.

alethina y C. castanea in the site of wet forest (Pericos

Community Reserve). The shaded area represents the

overlap coefficient (∆1).

Fig. 4. Estimates of activity patterns overlap for S.

bogotensis and S. Ludovici in the site of rainforest

(BachuéReserve). The shaded area represents the overlap

coefficient (∆1).

Fig. 5. Estimates of activity patterns overlap for frugivorous

bats between localities. A. C. perspicillata in wet forest

(Pericos Community Reserve) and dry forest (El Vínculo

Regional Park). B. C. brevicauda wet forest (Pericos

Community Reserve) and rainforest (BachuéReserve). The

shaded area represents the overlap coefficient (∆

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the small sample sizes involved in the tests.

We found a positive and marginally significant

association of temporal overlap (Δ

) with abun-

dance (R = 0.647, P = 0.166) and body mass

(R = 0.657, P = 0.083) in El Vinculo, and with

phylogenetic distance in Bachué (R = 0.829, P=

0.083) (Table 5). On the other hand, we did not

find associations of temporal overlap with body

mass, abundance, or phylogenetic similarity in

the assemblage of Pericos. Thus, these results

indicate that species similar in abundance, size,

and phylogenetic history tend to have less over-

lap in activity patterns.

DISCUSSION

We found differences in the temporal

activity pattern of frugivorous bats assemblag-

es among sites, revealed by a difference greater

than 10 % in activity patterns of assemblages.

We also found differences in activity patterns

between species in each locality and popula-

tions of the same species among sites. Finally,

we found that species similar in abundance,

size, and phylogenetic history, tend to have less

overlap in activity patterns. Consequently, our

results suggest that (1) local biotic and abiotic

conditions may influence variation in the activ-

ity patterns between assemblages and popula-

tions of the same species, and (2) ecologically

similar species tend to present less overlap in

their activity patterns. Thus, our results provide

empirical support for the role of segregation in

temporal activity as a mechanism that allows

the coexistence of ecologically similar species.

We obtained a low capture rate of phyl-

lostomid bats that contrasts with studies in

other Neotropical sites (La Val, 1970), but it

is consistent with previous studies at Reserva

Pericos (Zapata-Mesa et al., 2017) and El Vin-

culo (Velásquez-Roa & Murillo-García, 2019)

and in another wet forest at similar altitude on

the Western Andes of Colombia (Ferro-Muñoz

et al., 2018). As we expected, the assemblages

of frugivorous bats showed spatial variations

in their activity patterns. Given the high energy

cost and predation risk implicit in bat flight

(Erkert, 1982; Norberg et al., 1993), the eco-

logical tendency is to minimize foraging time

(Howe, 1979). On the other hand, frugivo-

res could require more time to satisfy their

daily energetic requirements than other trophic

TABLE 4

Mean hourly overlap (95 % confidence interval) in temporal activity between the most abundant species

of frugivorous bats in a rainforest (Bachué Reserve)

Species (sp.)

Carollia

brevicauda

Dermanura

cf. anderseni

Sturnira

bogotensis

Sturnira

ludovici

Carollia brevicauda

1 0.764 (0.474-0.930) 0.666 (0.472-0.863) 0.741 (0.560-0.89)

Dermanura cf. Anderseni

1 0.694 (0.339-0.900) 0.718 (0.354-0.915)

Sturnira bogotensis

1 0.456 (0.269-0.677)

Sturnira ludovici

TABLE 5

Summary of Mantel test applied to assemblages of frugivorous bats comparing effects of abundance, body mass,

and phylogenetic distance into temporal segregation estimated by the hourly overlap in the temporal activity

Locality

Abundance Body mass Phylogenetic distance

R P-value R P-value R P-value

Vínculo

0.647 0.166 0.657 0.083

0.085 0.5

Pericos -0.344 0.866 -0.037 0.638 -0.354 0.874

Bachué -0.058 0.485 0.486 0.167

0.829 0.083

The correlations with marginally significant associations are highlighted in bold.

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guilds since their food can have a higher pro-

portion water and indigestible materials (Erk-

ert, 1982; Thomas, 1984). Bats spend most of

the daytime in shelters, a period in which they

do not feed, so they are expected to leave their

shelters early in the night to solve this situation

of energy stress (Aguiar et al., 2014; Ortêncio

Filho et al., 2010). The frugivorous bats of the

three assemblages showed the highest activity

during the first hours of the night. This pat-

tern is widely documented in neotropical bats

and can result from synergistic factors (Erkert,

1982; Marinho Filho & Sazima, 1989; Pedro

& Taddei, 2002; Verde et al., 2018). In this

sense, the activity time, which initiates with

the emergence from shelters, is also influenced

by the diet of the species and the shelter’s

proximity to food sources (Ortêncio Filho et

al., 2010). With an activity peak early in the

night, the unimodal pattern observed in Pericos

and Bachué is characteristic of frugivorous spe-

cies (De Souza & Marinho-filho, 2004; Erkert,

1982; Ramirez-Pulido & Armella, 1987). How-

ever, frugivorous bats at El Vínculo showed a

bimodal pattern of activity, which peaks just

after sunset and before sunrise. The availability

of food sources can be low in El Vínculo since

it is a small fragment of tropical dry forest,

which could probably force frugivorous bats

to perform a second feeding trip to supply

their daily energy requirement. Alternatively,

variations in activity between assemblages may

correspond to species responses to differences

between study sites in other ecological factors,

such as vegetation coverage, luminosity, etc.

When there is a high overlap in one of

the dimensions of the niche (for example, in

the food source), a low overlap is expected

in other dimensions (such as the foraging

schedule) (Pianka, 1974). Experimental stud-

ies have induced temporal changes of activity

in small mammals attributed to competition,

resulting in a species being restricted to a less

favorable activity time due to the influence of

the more dominant species (Ziv et al., 1993).

Likewise, previous studies have reported dif-

ferences in the temporal activity patterns of

frugivorous bats (Aguiar & Marinho-Filho,

2004; Zeppelini et al., 2017). Some authors

suggest that this difference in the temporal

activity does not result from competition (Agu-

iar & Marinho-Filho, 2004; Zeppelini et al.,

2017), even though exploitation competition

has been reported between species of Neo-

tropical frugivorous bats (Bonaccorso et al.,

2007). However, differences in activity patterns

between frugivorous bats may suggest an effect

of competition, with the early emergence of a

species to avoiding competition during forag-

ing with the more dominant and larger species

(Bonaccorso et al., 2007).

In habitats with limited resources, it is

highly probable to expect competition among

bats for the fruits available a given night

(Bonaccorso et al., 2007). Consequently, the

bats that emerge early can successfully find

food (Bonaccorso et al., 2007) since the avail-

ability of ripe fruits decreases throughout the

night; consumed fruits are not renewed on the

same night (Aguiar & Marinho-filho, 2004;

Heithaus et al., 1975). Thus, a species can

roost closer to the feeding patches or advance

its emergence time to avoid competition with

other ecologically similar species (Bonaccorso

et al., 2007). We considered that a 10 % differ-

ence in temporal activity between two species

could be enough to suggest temporal segre-

gation. In agreement with the hypothesis of

temporal segregation of resources between the

species of the same guild, we found differences

of at least 10 % in the activity patterns of pairs

of sympatric species in the three habitats; it

suggests that frugivorous bats alter their activ-

ity periods in order to reduce competition with

similar species. We found marked differences

between the activity patterns of species with

similar body mass such as C. castanea - R.

alethina in the wet forest site and between spe-

cies of the same genus such as S.ludovici - S.

bogotensis in the rainforest site.

Across the Neotropic region, there is a

high association between genera of plants and

frugivorous bats. Bats of the genus Artibeus

have an affinity for the fruits of plants of the

genus Cecropia, bats of Dermanura for Ficus,

bats Carollia for Piper, and bats of Sturnira for

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Solanum (Agnarsson et al., 2011; Estrada &

Fleming, 1986; Howell & Burch, 1974; Muller

& Reis, 1992), with species showing some

discrepancies at specific sites (Bonaccorso,

1979; Handley et al., 1991). These associations

have been previously found in our study sites

(El Vinculo: Velásquez-Roa & Murillo-Gar-

cía, 2019; Pericos: Zapata-Mesa et al., 2017),

which may reduce intergeneric competition

and explain the high overlap in the activity pat-

terns we observed inside the local assemblages.

Besides diet, vertical stratification in neotropi-

cal bats assemblages (Delaval et al., 2005;

Pereira et al., 2010; Silva et al., 2020) may be a

mechanism of spatial segregation. It can reduce

the probability of encounters between bats

foraging mainly in the canopy (i.e., Artibeus)

and the understory (i.e., Carollia, Sturnira),

reducing competition intensity. On the other

hand, foraging strategies can also promote

coexistence (Delaval et al., 2005; Soriano,

2000). Nomadic frugivores like species of Ster-

nodermatinae subfamily (except Sturnira) feed

on trees distant from each other by foraging

over large areas tracking resource availabil-

ity, whereas sedentary frugivores forage over

short distances by staying in permanent roosts

(Soriano, 2000). Therefore, the combination of

spatial and temporal segregation with behav-

ioral strategies may lead to coexistence and be

critical to determining the structure of frugivo-

rous bats’ assemblages, as has been reported

for insectivorous species (Razgour et al., 2011).

As predicted, we found an association of

temporal overlap with traits that suggest eco-

logical similarity: abundance, body size, and

phylogenetic closeness. As species differ more

in body mass and phylogenetic history, they

increase their temporal overlap, suggesting a

tendency for ecologically similar species to

segregate temporally. This effect is significant

among the most abundant species, which may

have a greater probability of interacting with

each other (Meyer & Kalko, 2008; Patterson et

al., 2003). However, we did not find these asso-

ciations for all traits in all the sites studied, sug-

gesting that the degree of ecological similarity

between species may occur through different

mechanisms or that the structuring mecha-

nisms differ between sites or ecosystems. On

the other hand, predation risk is a fundamental

aspect considering activity patterns, particular-

ly for small species such as bats. The segrega-

tion of activity times can reduce predation risk

since bat predators can detect the aggregations

of foraging bats in fruiting plants (Breviglieri

et al., 2013; Howe, 1979; Thies et al., 2006),

so visiting plants sporadically at night could

reduce the chances of being predated.

The study of resource partitioning

in space and time is vital to understand how

interspecific competition can allow the stable

coexistence of species with similar ecologi-

cal characteristics (Bonaccorso et al., 2007;

Schoener, 1974). Nevertheless, the effect of

time partitioning on intra-guild competition has

been poorly studied. We found that temporal

activity patterns of Neotropical frugivorous

bats are variable between assemblages, sym-

patric species, and populations of the same

species. Activity patterns respond to the inter-

action of multiple factors, ranging from the

supply of resources to interactions with other

species. The results suggest that the association

between plant and bat genera (i.e., Carollia -

Piper, Sturnira - solanum), which may reduce

intergeneric bat competition, may partially

explain the high overlap in the activity patterns

we observed. Besides, although the highest

activity is conserved at the beginning of the

night, the phylogenetic factor does not seem

to influence the conservation of the activity

patterns in bats, unlike other groups such as

rodents (Castro-Arellano & Lacher, 2009).

Finally, we found that species with similar

size, abundance, and evolutionary history dif-

ferentiate their activity patterns. Thus, our

study provides empirical support for a trend

towards temporal segregation in the activity of

ecologically similar species, which may repre-

sent a mechanism that promotes coexistence.

Consequently, our results contrast with those

pointing out that temporal activity patterns of

sympatric species do not respond to interspe-

cific competition.

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Ethical statement: the authors declare

that they all agree with this publication and

made significant contributions; that there is no

conflict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

We would like to thank to thee staff of

La Fundación Farallones, El Parque Nacional

Natural Farallones de Cali, el Instituto para

la Investigación y la Preservación del Patri-

monio Cultural y Natural del Valle del Cauca

(INCIVA) and the Medio y Alto Dagua Com-

munity Council for their logistic collaboration

and for allowing access to the sampling areas.

Thanks to Cristhian Calvache, Andrea Bernal,

Christian Cabrera, Oscar Cuellar, Julio Salinas,

Sergio Tabares, Andrés Ocampo and Alejandro

Montoya for their unconditional support during

the fieldwork. Finally, we thank the Graduate

Biology program of Universidad del Valle for

providing funds to cover publication expenses.

RESUMEN

Distribución del tiempo entre murciélagos frugívoros

neotropicales: efectos de la filogenia, el tamaño

corporal y la abundancia

Introducción: La partición de recursos es esencial para

determinar la riqueza y composición de especies en las

comunidades naturales. Sin embargo, la segregacion tem-

poral ha sido cuestionada como un mecanismo que promue-

ve la coexistencia de especies ecológicamente similares.

Objetivo: Con el fin de determinar la importancia de la

segregación en los patrones de actividad, como mecanismo

que promueve la coexistencia; se compararon los patrones

de actividad de murciélagos frugívoros neotropicales.

Métodos: Se capturaron murciélagos con redes de niebla

desde el atardecer hasta el amanecer en tres localidades

(bosque seco tropical, bosque muy húmedo y bosque

lluvioso submontano) con el fin de calcular los patrones

de actividad de las especies empleando la estimación de

densidad Kernel. Se utilizó el coeficiente de superposición

(Δ) para comparar patrones de actividad entre: (1) ensam-

blajes de murciélagos de los sitios de estudio, (2) especies

frugívoras en el mismo sitio, y (3) poblaciones de la misma

especie en diferentes sitios.

Resultados: Se encontraron variaciones geográficas en

los patrones de actividad de los ensamblajes en las tres

localidades. Asimismo, se encontraron variaciones en los

patrones de actividad entre especies en cada sitio y entre

poblaciones en diferentes sitios. Determinamos que la

superposición en los patrones de actividad disminuyó a

medida que las especies estaban más relacionadas filoge-

néticamente, similares en abundancia y tamaño corporal;

lo que sugiere una tendencia hacia la segregación temporal

de especies ecológicamente similares.

Conclusión: Estos resultados proveen apoyo empírico del

papel de la segregación temporal en los patrones de activi-

dad como un mecanismo que promueve la coexistencia de

especies ecológicamente similares en la naturaleza.

Palabras clave: competencia; traslape de nicho; segrega-

ción temporal; segregación ecológica; especies ecológica-

mente similares; coexistencia de especies.

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