American Society of Mammalogists

Diet and Abundance of the Bat Sturnira lilium (Chiroptera) in a Brazilian Montane Atlantic Forest Author(s): Marco A. R. Mello, Elisabeth K. V. Kalko and Wesley R. Silva Source: Journal of Mammalogy, Vol. 89, No. 2 (Apr., 2008), pp. 485-492 Published by: American Society of Mammalogists Stable URL: http://www.jstor.org/stable/25145118 . Accessed: 18/02/2014 08:51
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Journal ofMammalogy,

89(2):485-492,

2008

DIET AND ABUNDANCE OF THE BAT STURNIRALILIUM (CHIROPTERA) IN A BRAZILIAN MONTANE ATLANTIC FOREST
Marco A. R. Mello,* Elisabeth K. V. Kalko, and Wesley R. Silva em Ecologia, Instituto de Biologia, Universidade Estadual de Campinas, Programa de Pos-Graduacao 13083-970, Campinas, Sao Paulo, Brazil (MARM) Institute of Experimental Ecology, University of Ulm, Albert-Einstein Allee 11, 89069 Ulm, Germany (MARM, EKVK) de Zoologia, Universidade Estadual de Campinas, Laboratorio de lnteracbes Vertebrados-Plantas, Departamento 13083-970, Campinas, Sao Paulo, Brazil (WRS) de Botdnica, Universidade Federal de Sao Carloes, Rod. Washington Luis, KM.235, Present address of MARM: Departmento 13565-905 Sao Paulo, SP, Brazil

We

in amontane studied variations in diet and abundance of the bat Sturnira lilium (Chiroptera: Phyllostomidae) Atlantic Forest, in order to investigate if patterns in this habitat differ from those in the better-studied lowlands. The diet of S. lilium was assessed based on fecal samples, whereas possible variations in abundance were and linked variability in air temperature to fruit documented based on capture success. We also monitored production of Solanaceae, the main food of S. lilium. Bats fed exclusively on fruits, mostly on Solanaceae and
occasionally on Piperaceae and Cecropiaceae. S. lilium was mostly absent in the area during the colder months,

suggesting that they might migrate to lower and hence warmer elevations. Absence of the bats was not related to a distinct decline in availability of fruit of Solanaceae because fruit production was not related to temperature. We conclude that in tropical montane systems, abundance of some frugivorous bats might be affected more by air temperature than by food availability. Furthermore, we reinforce the idea that preserving elevational gradients
is a crucial aspect for the conservation of migratory montane species. rain

Key words: Stenodermatinae

climate,

frugivory,

migration,

forest,

plant-animal

interactions,

populations,

forest,

seasonality,

bats represent the 2nd largest order of mammals, Worldwide, with more than 1,100 recognized species (Simmons 2005).
In Brazil, they constitute one-third of the mammal fauna

S.

lilium

is generally

dominated

by

fruits

of

the family

Solanaceae.

(Marinho-Filho
members of the

and Sazima
subfamily

1998). Among
feed

phyllostomids,
almost exclu

Stenodermatinae

sively on fruits and constitute important seed dispersers of many tropical trees and shrubs (Fleming and Sosa 1994). The bat, Sturnira lilium (E. Geoffroy St.-Hilaire, yellow-shouldered in the 1810), is one of the most abundant stenodermatines It has a broad distribution and occurs from Mexico Neotropics. to northern Argentina, including the Lesser Antilles (Simmons et al. (2002) list 28 plant families and 76 2005). Geiselman plant species as food for S. lilium throughout its geographical range. In spite of this overall variety, the diet of individual

Although there is extensive literature on the diet of S. lilium in tropical lowlands (e.g., Bizerril and Raw 1997; Caceres and et al. 2002; Giannini Moura 2003; Fleming 1986; Geiselman Mello and Vasconcellos-Neto Uieda 1999; 2006; 1985), of the feeding habits of this species in montane knowledge forests is poor. Montane systems are characterized by different
environmental conditions compared to lowland forests, in par

ticular higher seasonality, which is expressed by lower temper atures and often also by lower food availability (Mantovani in diet are thought to lead to 2001). Seasonal differences altitudinal movements of bats, as observed for instance by Giannini (1999), who studied the diet of S. lilium across an elevational gradient in Argentina. Furthermore, some phyllos tomids may not be able to tolerate lower temperatures as well as other bats such as vespertilionids and rhinolophids that save to lower their energy (torpor). regularly body temperature This, 485 in turn, might affect the distribution and abundance of

Correspondent:

marmello@gmail.com

2008 American

Society

of Mammalogists

www.mammalogy.org

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486 JOURNAL OF MAMMALOGY

600 -| ?-? C 500 ez-irainfall (study)r 25 1=1 rainfall (average)q* ?temperature (study)2-? p]_ v ? ?temperature (average)? ^ ^

Vol.

89,

No. 2

- 20 *

15 400 - ^^^

^\
>? 300 ^^*C^^ -i ~

?^^^ s n

i '
t'

plants of the bats. S. lilium is very abundant at Sede de Pesquisa (Passos et al. 2003). Data collection.?Our study site is characterized by a relatively dry and cold season between April and September (winter), and a relatively rainy and hot season between October (summer; see Fig. 1). During our study, rainfall averaged a total of 176.2 mm per month and varied from a minimum of 3.3 mm (August 2004) to a maximum of 507.9 mm (January 2005); monthly air temperature averaged 16.8?C and ranged from 12.6?C (June 2004) to 19.7?C (January 2005). Minimum temperatures yielded values as low as 0?C (July 2003). Variations in rainfall and air temperature were correlated with the long-term monthly means that had been recorded in the area for the last 7 years, indicating that the year of our study did not deviate from the long-term average (rainfall: r2 = 0.76, P < 0.001; temperature: r2 = 0.85, P < 0.001). We followed guidelines for animal care and use approved by the American Society of Mammalogists (Gannon et al. 2007). In order to capture bats we used a standardized protocol consisting of a set of 10 nylon mist nets (7 x 3 m; Ecotone, and March Inc., Sopot, Poland) opened for 6 h after sunset on 3 (from October to December 2003) or 2 (from March 2004 to February 2005) consecutive (Mello nights over a total of 15 months 2006). Netting sites were distributed rather evenly across the study area, covering about 400 ha (for a detailed map, please see Mello [2006]). We always sampled during the dark phases of the moon (1st quarter and new moon) to reduce possible effects of lunarphobic behavior of bats. We did not sample during nights with strong rain. At the beginning of the study, we selected a total of 20 fixed netting positions. The nets were set at distances of about 30 m on the trails dissecting the study area.We always changed net positions between the 1st and 2nd netting night in each month to minimize bias caused by net of the nets were positioned near known shyness. One-half patches of plants that bore bat fruits, that is, Cecropiaceae, Moraceae, Piperaceae, and Solanaceae (Fleming 1986) and the other one-half at sites without such plants to avoid over estimations of the proportion of those plants in the fecal samples. All captured bats were marked with individually num bered aluminum wing bands (A. C. Hughes, Inc., Middlesex, United Kingdom). We used 2 keys (Emmons and Feer 1997; Vizotto and Taddei 1973) for identification of bats. There were 2 species of Sturnira in the area. S. lilium was much more abundant than S. tildae, which was seldom captured (n = 2?Mello 2006). We used the morphological characters proposed by different authors (Gannon et al. 1989; Goodwin and Greenhall 1961; Simmons and Voss 1998) for identification, including forearm and shape of the cusps length, form of the lower maxilla, of the molars and the lower incisors. The identification of some specimens was confirmed by Marcelo R. Nogueira (Universidade Estadual do Norte Fluminense, Brazil). We also recorded a standard set of demographic data from all captured individuals including sex, age, reproductive condition, and
body mass.

r-n n 1 I 100

2 200 -

'

c n

-10 1* S

rk 1 _n n

n .

s i p-i 'n "i ' ' ' "5 S [1

? Jl

Jlllillll,
Fig. 1.?Monthly (?C) and

JllllartnilillJllllllllL'
Time variation in our study in total area. We for rainfall present (mm) data and average air

temperature period (study)

from

the sampling

the average

the past

7 years

(average).

in the highlands and probably limit their pres phyllostomids ence to the warmest months (Speakman and Thomas 2003). We focused on the composition and temporal variability of the diet of S. lilium and on its variation in abundance in a selected area of the Brazilian montane Atlantic Forest. We asked whether the diet of S. lilium in the highlands is similar to the diet observed in the lowlands, with fruits of as the main component. We expected temporal Solanaceae variation in the diet and abundance of S. lilium because of stronger seasonality in the study area, mainly caused by dif ferences in air temperature at higher elevations, which could affect food availability for the bats as well as their thermo regulatory abilities.

Materials

and Methods

Time frame and study area.?We collected data for a total of 36 nights in 15 monthly sessions from October 2003 to February 2005, except January and February 2004, when we could not reach the study area because of logistical problems. The study took place at the state park Parque Estadual Inter vales (hereafter Intervales, approximately 50,000 ha) in the Ribeirao Grande municipality, Sao Paulo State, southeastern Brazil. Intervales and 3 neighboring preserved areas form the Continuo Ecologico de Paranapiacaba, which represents the largest continuous remnant of the Atlantic Forest in Brazil. Within in Sede de Pesquisa Intervales, we worked located 850 m above sea level, (24?16'24.7"S, 48?25'00.6"W), the highest research base of the park. We worked in an area of approximately 400 ha, where we monitored bats and plants simultaneously. The climate of the region is classified as humid subtropical (Mantovani 2001), with average temperatures of 22?C during the warmest months, and absolute minimum in temperatures reaching ?4?C during the coldest months winter. Annual total rainfall averages approximately 2,000 mm. The main vegetation at Sede de Pesquisa is classified as Montane Atlantic Forest (Mantovani 2001). The flora of this region is well known based on a recent inventory (Passos et al. 2003) that greatly facilitated the identification of the food

studied the feeding habits of S. lilium by analyzing fecal samples, which we collected directly from bats captured inmist

We

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April 2008

MELLO ET AL.?DIET

AND ABUNDANCE

OF STURNIRA LILIUM 487

nets using small Eppendorf tubes and from individuals that we kept for at least 1 h in clean cloth bags. Each sample from each individual was collected separately, and then stored frozen at
a temperature of about 0?C. For analysis, each sample was 1st

allowed us, in conjunction with a standardized capture protocol that aimed at minimizing sampling bias caused by lunarphobic
behavior of the bats, or net-shyness, or both to assess the gen

eral pattern of variation

the relationship between

in relative abundance. We
capture success and

then tested
and

put in a fine-meshed sieve and carefully rinsed with water to separate the seeds from the pulp and other materials. Seeds were 1st classified to family (97% of all seeds), and in most cases also to genus (70% of all seeds). In 65% of all cases we identified seeds to species based on a reference collection of the study area started by Passos et al. (2003). We marked all trees of Solanaceae found along the trails in the study area in a 5-m band on both sides of the trail, totaling 70 individuals of 13 species, and documented their phenology on amonthly basis. In addition, we also assessed the phenology of the Piperaceae and Cecropiaceae that also are consumed were available during to lilium determine if their fruits S. by
the same seasons as Solanaceae. For other plant families, we

temperature,

between
by nonlinear

capture

success

and fruit production

of Solanaceae

regressions.

identified food items found in fecal samples and summarized their frequency of consumption by S. lilium. To address possible temporal variation in diet, we pooled dietary data of S. lilium on a monthly basis as the percentage of samples that contained seeds of identified plant families. We tested for differences in the overall proportion of each plant family in the fecal samples with a chi-square test for the entire
data set, and for monthly variation with a G-test.

We

general patterns described by Leiner (2005). We distinguished between inactive, flowering, fruiting, flowering/ fruiting. Furthermore, we counted total number of flowers and fruits (ripe and unripe) on individual plants that could be clearly observed (86%) or made estimates for individual plants that were difficult to fully observe (14%), following the method proposed by Korine et al. (2000). Identification of plants was (Universidade Estadual de provided by Jorge I. Tamashiro Rafael Fernando da Silva Possette Campinas), (Embrapa Osmar and Gerdt Hatschbach Ribas, Florestas), (Museu Botanico Municipal de Curitiba). Vouchers of the studied in the collections of the plant species were deposited Laboratorio de Interacoes Vertebrados-Plantas (Universidade Estadual de Campinas, Brazil) and "Museu Botanico Munici pal de Curitiba" (Curitiba, Brazil).
Data analysis.?We based our statistical analyses on those

considered

We monitored the phenology of food plants by assessing the status of each population as the percentage of adult individuals producing fruits on a monthly basis. We tested the relationship
between fruit production, average air temperature, and total

rainfall by multiple linear regressions. To determine whether fruit production was randomly distributed or was bound to a specific season, we used Rayleigh's circular test, which
analyzes the concentration of observations in particular months

test the hypothesis of a relationship between consumption (percentage in fecal samples) and production individual (average crop) of fruits of all Solanaceae, we used a logarithmic model (see "Results" for details), as proposed by Mello et al. (2004a). In this regression analysis, we limited our analysis to the species of Solanaceae that dominated the diet of S. lilium by including only phenological data of plant species (Zar 1996). To
whose seeds were actually observed in the fecal samples.

given by Zar (1996), and used the software packages SYSTAT 9.0 (regular statistics; SYSTAT Software, Inc., San Jose, and Oriana 2.0 California) (circular statistics; Kovach Com United for calculations. puting Systems, Anglesy, Kingdom)
Percent statistical We data were arcsine transformed before being used in tests. collected data on average air temperature (?C) and total

Results captured a total of 477 bats including recaptures, representing 15 species. Thirteen species were members of the and 2 species belonged to the family family Phyllostomidae We
Vespertilionidae. The number of

rainfall (mm) daily and pooled them on a monthly basis (total sum for rainfall and daily mean for temperature) to describe variations in climate in the area and to link them to the data on both bats and plants. We used simple linear correlations to determine whether the climate data from our study period followed the yearly average from the last 7 years. We further tested the relationship between temperature, rainfall, and fruit production with multiple linear regressions. Our total netting effort was 41,580 h/m2, calculated as the total amount of square meters of nets (each net was 21 m2) opened each night multiplied by the total number of hours worked in the entire study, following Straube and Bianconi (2002). This permits comparisons between studies that used
different sizes and numbers of mist nets. Capture success was

40% of all bat species 2006). Overall capture was much lower (11.5 studies in the lowlands
10~3 captures h_1

recorded for the park (n = 34?Mello success at our study site in the highland x 10-3 captures h_1 m-2) compared to of the Atlantic Forest areas (e.g., 37.3 x
2002).

species

corresponds

to about

m-2?Mello

Sturnira lilium was the dominant species and represented 70% of all captures (n = 333 captures, including 27 re captures). Capture success of S. lilium varied strongly between months. It averaged 7.46 x 10~3 ? 6.64 x 10~3 captures h~l m-2 (SD) with a maximum of 19.84 x 10"3 captures h_1 m-2 and a minimum of no captures (Fig. 2). We obtained 3 peaks with regard to capture success, 1 at the beginning of the dry season (April), the 2nd at the end of the dry season (September), and the 3rd in the middle of the rainy season (December). During the coldest months, S. lilium was either not captured at all or in very low numbers. The variation in capture success was and positively related to air significantly
temperature Fig. (model: y = x366, to n = initial 12, r2 = 0.37, P there = was 0.03; no 3). However, contrary expectation,

calculated as the total number of captures divided by the total in each month. Although capture effort (captures h_1 m-2) capture success is not equivalent to total population size, it

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488
80% j ^ -production ofSolanaceae j 0.03 -o-consumptionofSolanaceae o ? . / _ ^j" -^capturesuccess ,--''

JOURNAL OF MAMMALOGY

Vol.

89,
of composition that contained = (n 21).

No.

Table \? samples. material

1.?Diet Fecal were

Sturnira only pulp

lilium

based

on

fecal

i?

i A *20% t/ \
0% -I-1-1?

8 40% I

a/

^' ?. \ 2\/' ?

Jf\ *
\

\A y\*

1 ?'02 ?

samples excluded

or other

unidentifiable

No. Morphospecies s.01 s.07 p.01 s.21 s.06 s.09 c.02 Family Solanaceae Solanaceae Piperaceae Solanaceae Solanaceae Solanaceae Cecropiaceae Piperaceae Piperaceae Solanaceae Solanaceae Solanaceae Piperaceae Solanaceae Solanaceae Solanaceae Solanaceae Solanaceae Solanaceae Solanaceae Solanaceae Subtotals Species Solanum granulosoleprosum Unidentified 8 11 Piper gaudichaudianum Solanum sanctae-katharinae Unidentified Unidentified 3 4 3 4 2 3 2 3 2 3 2 3 7 samples 31 5 4

% samples 41

/ ''

A >/\\ / \ A \\
I ?I-1-1-1-1?o?I-1-

A\

MS

s \ s
0.00

v_II? -T~

"?^K-

Time Fig. in the of those 2.?Monthly study area, fruits by because variation fruit bats. we success in capture of Solanaceae, production The line for no obtained consumption fecal samples of Sturnira lilium

p.04 p.05 s.03 s.13 is s.26 p.02 s.05 s.08 s.10 s.ll s.12 s.23 s.27 s.28

Cecropia glaziovii Piper corintoanum 2 3 Piper hoehnei Vassobia breviflora fasciculata 2 3 Unidentified Piper sp. 1 1 1 1 Unidentified Unidentified Unidentified Unidentified Unidentified Solanum 1 1 1 1 1 1 1 1 Aureliana

and of of S.

consumption Solanaceae lilium during

interrupted, this time.

association expressed
(model: y =

between capture success and fruit availability as average individual fruit crop of Solanaceae
0.02x204, n = 12, r2 = 0.16, P = 0.19).

capsicum 1 1 Solanaceae Solanaceae sp. 2 11 63 84 10 13 2 3

1 1

Aureliana

describe the diet of S. lilium, we analyzed 96 fecal soft parts of samples contained exclusively samples. Nineteen fruits (pulp) that we could not assign reliably to a particular plant family. Those samples were thus excluded from further To
calculations. Seventy-seven fecal samples contained seeds, and

Piperaceae Cecropiaceae Total 75

Pulp and other plant material

21

each sample contained only 1 kind of seed. Because we did not find any animal parts, we concluded that S. lilium fed exclu sively on fruits during our study, confirming the hypothesis of a frugivorous diet for this species. We found seeds of 22 plant species and morphospecies in the feces of (unidentified seeds that differ in morphology)

S. lilium, including Solanaceae, Piperaceae, and Cecropiaceae (Table 1). S. lilium fed mostly on fruits of Solanaceae, which = = 94.92, 96, x2 represented 84% of all seed samples (n P < 0.001). Bats also ate Piperaceae, which were present in 13% of all samples with seeds, and to a lesser extent also the identified Solana consumed Cecropiaceae (3%). Among
ceae, Solanum granulosoleprosum was consumed most fre

T E
Ifi 0.015-1

r?-0.41,p

= 0.03

quently (40% of all samples) by S. lilium. The proportions of each plant family in the diet of the bats varied among months = = 66.66, P = 0.019; Table 2). However, Solanaceae (n 96, G dominated throughout the study period and were present in more than one-half (59% ? 33% SD) of all fecal samples. During the middle of the rainy season, S. lilium fed on a higher / /
/ /

"
2 Q-

Ui en a> o
V) CD

0.010+

/
y

CO

0.005-L/ /
/

number of plant species than during the dry season (Table 2). 13 In the phenological part of our study, we monitored not fruits which did 3 of during produce species of Solanaceae, the study period. Fruit production of Solanaceae varied among months, from no fruits (0%) to high fruit production (100%) when all adult individuals of a plant species produced fruits. The majority of species of Solanaceae revealed a steady-state strategy with continuous fruit production over several months
20

o.ooo I-|--^~l-1-1 0

10

15

Average
Fig. capture

minimum air temperature

average (captures air h-1

(?C)
(?C) by month. and

between 3.?Relationship success of Sturnira lilium

temperature m~2)

(Table 3). Despite the extended fruiting season, fruit produc tion of Solanaceae was characterized by peaks (Solanaceae: = Z = 17,081.78, P < 0.001; Piperaceae: Z Rayleigh's < was of Solanaceae P Fruit 1,009.63, 0.001). production negatively related to air temperature (standardized partial co efficient of the multiple regression [b'] = ?0.659, P = 0.034)

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April 2008
Table indicated Solanaceae variation numbers All fecal Oct.

MELLO ET AL.?DIET

AND ABUNDANCE

OF STURNIRA LILIUM 489

2.?Monthly (cells without (all others).

in the diet were zeros).

of Sturnira Seeds

lilium,

that could only No

samples Nov.

contained Dec.

as the number the species of fecal that contained represented samples to genus are represented as morphospecies not be identified of Piperaceae 1 kind of seed. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec.

of plant (p.02) or

Mar.

Jan.

Feb.

Species
Cecropiaceae Cecropia Piperaceae Piper Piper gaudichaudianum corintoanum 2 1 glaziovii

2003 2003 2003

but 1 sampling,

sampling 2004 2004

Period almost no

2004
with

2004 2004 2004 2004 2004 2004 2004 2005 2005

captures p.02 1 S. lilium

13

of

Piper hoehnei Solanaceae Aureliana Aureliana Solanum Solanum Solanum Vassobia s.05 s.07 s.08 s.10 s.ll s.12 s.26 s.27 1 s.09 1 1 1 1 1 1 1

fasciculata sp. 2 capsicum 1 7 granulosoleprosum sanctae-katharinae breviflora 2

10

6 51

1 111

s.06 1 1 1 2 5 1 1 11

Total 13

16

? 0 25

000068802

not associated with rainfall (b' = ?0.183, P = 0.505). Finally, there was no relationship between fruit produc tion of Solanaceae and consumption of those fruits by S. lilium = 1.06 + 0.32 x In x, n = 1, r2 = = 0.29, P 0.20; (model: y but it was Fig. 4).

sibility of rare animalivory or nectarivory in S. lilium in our area, these habits may not be important to this species, because Herrera et al. (2001) observed experimentally that a diet of pure fruit to meet allow lilium its S. all may energetic and nitrogen needs. Fruits of Solanaceae were the main food of S. lilium.
Piperaceae and Cecropiaceae also were consumed, albeit to a

Discussion
Based surveys, on we our observations that fruits and of including Solanaceae extensive are literature the most im

suggest

portant food source for S. lilium in lowland as well

land habitats. We propose that low winter

as in high
may

much lesser degree. The dominance of Solanaceae in the diet of S. lilium has been reported for the entire geographic range of this species (Caceres and Moura 2003; Giannini 1999; Iudica and Bonaccorso 1997; Passos et al. 2003; Uieda and
Vasconcellos-Neto 1985).

temperatures

may

force bats tomigrate to the warmer lowlands, because S. lilium not tolerate well the very low temperatures during this
season. Here we discuss some implications of those patterns

observed.

Although a variety of other large fruit crops was available in our study area, the overall and monthly high proportions of Solanaceae in the diet of S. lilium indicate active selection of these fruits by the bats. For details on the phenology of other plant families, see Leiner (2005) and Mello (2006). For exam to fruit abundance, they ple, if the bats reacted opportunistically could have eaten more fruits of Piperaceae. Additional observa tions made in the wild and in food-choice experiments further support the assumption that Solanaceae is preferred by Sturnira 1987; Fleming 1986; Giannini 1999; et al. of Fruits other families 1997). Hernandez-Conrique plant may supplement energetic or mineral needs or both of S. lilium (Bonaccorso when
between

Our results revealed an entirely frugivorous diet for S. lilium. This is in accordance with most other studies of this species et al. [2002]). (see a wide list of case studies in Geiselman Additional food items, that is, insects and nectar, have been reported only in a few instances (Nowak 1994). Thomas (1984) suggested that phyllostomid frugivorous bats should supple ment their diets with insects because plants contain low protein levels. On the other hand, Delorme and Thomas (1996) observed that at least Carollia perspicillata, which supposedly eats animals (i.e., insects) more frequently than does S. lilium its nutritional requirements by 1988), may meet (Fleming on fruits. feeding only Although we cannot exclude the pos

and Gush

the fruit crop of Solanaceae

S. lilium and the Solanaceae

is low. The
seems to be as

relationship
strong as is

the case for other highly specialized bat-plant systems, that is, Carollia castanea and Piperaceae (Thies and Kalko 2004).

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490

JOURNAL OF MAMMALOGY

Vol.

89,

No.

Table sample marked, seeds

3.?Fruiting sizes. Cells whereas

of Solanaceae phenology are months without numbers were

and Piperaceae when monitored

were

plants of Piperaceae in fecal samples observed

randomly sampled of Sturnira lilium during Apr. May

in the study area. Numbers inside parentheses after names of species represent were not producing fruits. Plants of the Solanaceae plants were permanently see "Materials each month. and Methods." whose For further explanation Species this Jun. study are marked Jul. with an asterisk (*). Oct. Nov. Dec. Feb. Jan.

Mar.

Aug.

Sep.

Species (n)
Solanaceae Aureliana Aureliana Aureliana Solarium cf. fasciculata sp. 1 (13) sp. 3 (1)

2004

2004

2004

2004

2004

2004

2004

2004

2004

2004

2005

2005

(1)*

100% 100% 23% 8% 8% 8% 15%

100%

5% 45% 59% 68% 68% 5% (22)* granulosoleprosum 9% 9% 27% 18% Solarium phyllosepalum (11) 67% Solarium sanctae-katharinae 33% 67% 33% 33% (3)* 21% 14% 7% Solarium variabile 7% 36% 7% 29% 36% 21% (14) Vassobia Piperaceae breviflora (3)* 33% 33% 100% 33%

50% Piper gaudichaudianum(10)* 14% Piper hispidum (10) 50% Piper mosenii (10)

46% 12%

33% 33%

64% 21%

100%

71% 7%

7%

10% 23% 86%

to our expectation that fruit consumption of Contrary Solanaceae by S. lilium should be positively related to fruit this relationship was not significant. The main production, reason for this pattern is likely to be the low abundance or even absence of S. lilium in the study area during the cold season, as revealed by our monitoring program. We conclude from our most the that of bats results temporarily to might migrate warmer areas, probably to lower elevations, during the colder months of the year. This concurs with the propositions made by (Fleming and Eby 2003) that species of bats living in seasonal

tropical
seasonal

or

temperate

environments
evidence

are
for

likely
possible

to conduct
elevational

migrations.

Further

migration of Sturnira is given by Giannini (1999), who studied S. lilium in Argentina. We further conclude from our data that fruit availability appears to be less important than air temperature in determining population fluctuations of S. lilium inmontane forests, because bat fruits were more abundant during the cold, dry season when most
cold

to the S. lilium appeared to leave the area. Compared are lower much during the tropical lowlands, temperatures
season, with an average minimum even drop as temperatures of temperature as ?4?C. low 12?C. Low

1.20

-I

Occasionally,

temperatures
S. S> o =5 .E 0.80 0) CO <D O CO I lilium

over

longer
because

periods
small

of

time probably
bats have

affect
in

negatively,

fruit-eating

sufficient fat reserves that do not allow them to cope well with low air temperatures (Stones and Wiebers 1965). Therefore, those bats may be forced to migrate during cold seasons in
order to avoid expending excessive energy for production of

(/>
m- 0.40 O 42 3

heat (Fleming and Eby 2003). of The influence of air temperature on the demography than is much bats larger previously thought. tropical probably There is increasing evidence that reproduction in small phyllo
stomids is related to air temperature, because, for example,

?
o.oo -I- -,-.-1 0.00 0.40

r2 = 0.29,

= 0.20

0.80

1.20

%
Fig.

Individuals

of Solanaceae

producing

fruits

tends to peak its reproductive activity during C. perspicillata warmer months independent of resource levels (Mello et al. 2004b). As a reaction to low air temperatures, bats may or torpor (see Dietz and undergo "facultative hypothermia" Kalko 2006; Speakman and Thomas 2003). They save energy by temporarily lowering their body temperature. This strategy also is known for phyllostomids 1997). (Audet and Thomas in contrast to other bat families such as Vespertilio However, and Rhinolophidae, may be unable to phyllostomids of and Thomas 2003). bouts torpor long (Speakman undergo Alternatively, they may temporarily migrate to lower elevations during cold seasons (Giannini 1999), as we suspect from nidae
examination of our data on S. lilium.

rate of Solanaceae between consumption 4.?Relationship as percentage of samples that fruits by Sturnira lilium, expressed are arcsine of contained seeds this family, by month (percents as of Solanaceae, and fruit production transformed), expressed proportion of plants producing fruits each month.

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April 2008 This

MELLO ET AL.?DIET

AND ABUNDANCE

OF STURNIRA LILIUM 491

in our study area suspected elevational migration underlines the conservation relevance of suitable habitats along an elevational gradient. Whereas S. lilium is likely to be well protected in large parks such as Intervales, populations of S. lilium and probably other important seed dispersers may be if the habitats are seriously altered along the endangered vertical gradient. Therefore, parks that are situated mainly in montane environments need to be connected with areas in the lowlands through corridors to ensure the viability of elevational services provided by them. migrants and thus the ecological This reinforces the propositions of Loiselle and Blake (1991), who were among the 1st to propose the crucial importance of "intact" elevational in Costa Rica. gradients for migrant and resident birds

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Submitted 30 November Associate

2006. Accepted

15 July 2007.

Editor was Rodrigo A. Medellin.

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