2008 mello et al. diet and abundance of the bat sturnia lilium

American Society of Mammalogists

Diet and Abundance of the Bat Sturnira lilium (Chiroptera) in a Brazilian Montane AtlanticForestAuthor(s): Marco A. R. Mello, Elisabeth K. V. Kalko and Wesley R. SilvaSource: Journal of Mammalogy, Vol. 89, No. 2 (Apr., 2008), pp. 485-492Published by: American Society of MammalogistsStable URL: http://www.jstor.org/stable/25145118 .

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Journal of Mammalogy, 89(2):485-492, 2008

DIET AND ABUNDANCE OF THE BAT STURNIRA LILIUM (CHIROPTERA) IN A BRAZILIAN MONTANE

ATLANTIC FOREST Marco A. R. Mello,* Elisabeth K. V. Kalko, and Wesley R. Silva

Programa de Pos-Graduacao em Ecologia, Instituto de Biologia, Universidade Estadual de Campinas, 13083-970, Campinas, Sao Paulo, Brazil (MARM) Institute of Experimental Ecology, University of Ulm, Albert-Einstein Allee 11, 89069 Ulm, Germany (MARM, EKVK) Laboratorio de lnteracbes Vertebrados-Plantas, Departamento de Zoologia, Universidade Estadual de Campinas, 13083-970, Campinas, Sao Paulo, Brazil (WRS)

Present address of MARM: Departmento de Botdnica, Universidade Federal de Sao Carloes, Rod. Washington Luis, KM.235, 13565-905 Sao Paulo, SP, Brazil

We studied variations in diet and abundance of the bat Sturnira lilium (Chiroptera: Phyllostomidae) in a montane

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

documented based on capture success. We also monitored and linked variability in air temperature to fruit

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 species.

Key words: climate, frugivory, migration, montane forest, plant-animal interactions, populations, rain forest, seasonality,

Stenodermatinae

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

(Marinho-Filho and Sazima 1998). Among phyllostomids, members of the subfamily Stenodermatinae feed almost exclu

sively on fruits and constitute important seed dispersers of

many tropical trees and shrubs (Fleming and Sosa 1994). The

yellow-shouldered bat, Sturnira lilium (E. Geoffroy St.-Hilaire,

1810), is one of the most abundant stenodermatines in the

Neotropics. It has a broad distribution and occurs from Mexico

to northern Argentina, including the Lesser Antilles (Simmons

2005). Geiselman et al. (2002) list 28 plant families and 76

plant species as food for S. lilium throughout its geographical range. In spite of this overall variety, the diet of individual

* Correspondent: [email protected]

? 2008 American Society of Mammalogists

www.mammalogy.org

S. lilium is generally dominated by fruits of the family Solanaceae.

Although there is extensive literature on the diet of S. lilium

in tropical lowlands (e.g., Bizerril and Raw 1997; Caceres and

Moura 2003; Fleming 1986; Geiselman et al. 2002; Giannini

1999; Mello 2006; Uieda and Vasconcellos-Neto 1985),

knowledge of the feeding habits of this species in montane

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

2001). Seasonal differences in diet are thought to lead to

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

regularly lower their body temperature to save energy (torpor).

This, in turn, might affect the distribution and abundance of

485



486 JOURNAL OF MAMMALOGY Vol. 89, No. 2

600 -| ez-i rainfall (study) r 25 1=1 rainfall (average) q* ?-? ?temperature (study) 2-? C 500 -

p]_ a ? v ?temperature (average) ? ^ ^

- 20 *

15 400 - ̂ ^^ ^\ ?^^^ i ?

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

s n '

1* c n t' -10 S 2 200 - n

' Jl ? - r-n n 1 rk n p-i 'n "i i s

I 100 - 1 _n n . [1 ' ' ' "5

S

Jlllillll, JllllartnilillJllllllllL'

Time

Fig. 1.?Monthly variation in total rainfall (mm) and average air

temperature (?C) in our study area. We present data from the sampling

period (study) and the average for the past 7 years (average).

phyllostomids in the highlands and probably limit their pres 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 Solanaceae as the main component. We expected temporal 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 Intervales, we worked in Sede de Pesquisa

(24?16'24.7"S, 48?25'00.6"W), located 850 m above sea level, 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

temperatures reaching ?4?C during the coldest months in 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

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 and March (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, 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 nights over a total of 15 months (Mello 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

shyness. One-half of the nets were positioned near known

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

length, form of the lower maxilla, and shape of the cusps 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.

We studied the feeding habits of S. lilium by analyzing fecal

samples, which we collected directly from bats captured in mist



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

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 a monthly basis. In addition, we also assessed the phenology of the Piperaceae and Cecropiaceae that also are consumed

by S. lilium to determine if their fruits were available during the same seasons as Solanaceae. For other plant families, we

considered 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

provided by Jorge I. Tamashiro (Universidade Estadual de

Campinas), Rafael Fernando da Silva Possette (Embrapa Florestas), Osmar Ribas, and Gerdt Hatschbach (Museu Botanico Municipal de Curitiba). Vouchers of the studied

plant species were deposited in the collections of the

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

given by Zar (1996), and used the software packages SYSTAT

9.0 (regular statistics; SYSTAT Software, Inc., San Jose,

California) and Oriana 2.0 (circular statistics; Kovach Com

puting Systems, Anglesy, United Kingdom) for calculations. Percent data were arcsine transformed before being used in

statistical tests.

We collected data on average air temperature (?C) and total

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

calculated as the total number of captures divided by the total

capture effort (captures h_1 m-2) in each month. Although capture success is not equivalent to total population size, it

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 in relative abundance. We then tested

the relationship between capture success and temperature, and

between capture success and fruit production of Solanaceae

by nonlinear regressions.

We 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 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

(Zar 1996). To test the hypothesis of a relationship between

consumption (percentage in fecal samples) and production

(average individual 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 whose seeds were actually observed in the fecal samples.

Results

We captured a total of 477 bats including recaptures,

representing 15 species. Thirteen species were members of the

family Phyllostomidae and 2 species belonged to the family Vespertilionidae. The number of species corresponds to about

40% of all bat species recorded for the park (n = 34?Mello

2006). Overall capture success at our study site in the highland was much lower (11.5 x 10-3 captures h_1 m-2) compared to

studies in the lowlands of the Atlantic Forest areas (e.g., 37.3 x

10~3 captures h_1 m-2?Mello 2002).

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 significantly and positively related to air

temperature (model: y =

x366, n = 12, r2 =

0.37, P = 0.03;

Fig. 3). However, contrary to initial expectation, there was no




80% j -production of Solanaceae j 0.03 ^

-o-consumption of Solanaceae o ? ^j" _ -^capturesuccess ,--'' . / \ ?

i? \ / Jf\ 1 ?. \ ^' * \ A T

?'02 ? 2 \ /' \ y\ *

8 40% I a / ? A \ MS i A / A >/\\ / s *20% t / \ '' / \ A \\ \ s

v_I "?^K- s 0% -I-1-1? I? -T~ I ?I-1-1-1-1?o?I-1- 0.00

Time

Fig. 2.?Monthly variation in capture success of Sturnira lilium

in the study area, fruit production of Solanaceae, and consumption

of those fruits by bats. The line for consumption of Solanaceae is

interrupted, because we obtained no fecal samples of S. lilium during

this time.

association between capture success and fruit availability

expressed as average individual fruit crop of Solanaceae

(model: y =

0.02x204, n = 12, r2 =

0.16, P = 0.19).

To describe the diet of S. lilium, we analyzed 96 fecal

samples. Nineteen samples contained exclusively soft parts of

fruits (pulp) that we could not assign reliably to a particular

plant family. Those samples were thus excluded from further

calculations. Seventy-seven fecal samples contained seeds, and

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

(unidentified seeds that differ in morphology) in the feces of

T r?-0.41,p = 0.03

E

Ifi 0.015-1

m

Ui / en 0.010+ / a> / o / " / V) /

CD /

2 0.005-L / Q- / CO / o y

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

0 5 10 15 20

Average minimum air temperature (?C)

Fig. 3.?Relationship between average air temperature (?C) and

capture success of Sturnira lilium (captures h-1 m~2) by month.

Table 1.?Diet composition of Sturnira lilium based on fecal

samples. Fecal samples that contained only pulp or other unidentifiable

material were excluded (n =

21).

No. %

Morphospecies Family Species samples samples

s.01 Solanaceae Solanum granulosoleprosum 31 41

s.07 Solanaceae Unidentified 8 11

p.01 Piperaceae Piper gaudichaudianum 5 7

s.21 Solanaceae Solanum sanctae-katharinae 4 5



c.02 Cecropiaceae Cecropia glaziovii 2 3

p.04 Piperaceae Piper corintoanum 2 3

p.05 Piperaceae Piper hoehnei 2 3

s.03 Solanaceae Vassobia breviflora 2 3

s.13 Solanaceae Aureliana fasciculata 2 3


p.02 Piperaceae Piper sp. 1 1




s.ll Solanaceae Unidentified 1 1


s.23 Solanaceae Solanum capsicum 1 1

s.27 Solanaceae Solanaceae 1 1

s.28 Solanaceae Aureliana sp. 2 11

Subtotals Solanaceae 63 84

Piperaceae 10 13

Cecropiaceae 2 3

Total 75

Pulp and other plant material 21

S. lilium, including Solanaceae, Piperaceae, and Cecropiaceae

(Table 1). S. lilium fed mostly on fruits of Solanaceae, which

represented 84% of all seed samples (n = 96, x2 = 94.92,

P < 0.001). Bats also ate Piperaceae, which were present in 13% of all samples with seeds, and to a lesser extent also

consumed Cecropiaceae (3%). Among the identified Solana

ceae, Solanum granulosoleprosum was consumed most fre

quently (40% of all samples) by S. lilium. The proportions of

each plant family in the diet of the bats varied among months

(n = 96, G = 66.66, P = 0.019; Table 2). However, Solanaceae

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 number of plant species than during the dry season (Table 2).

In the phenological part of our study, we monitored 13

species of Solanaceae, 3 of which did not produce fruits during 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

(Table 3). Despite the extended fruiting season, fruit produc tion of Solanaceae was characterized by peaks (Solanaceae:

Rayleigh's Z = 17,081.78, P < 0.001; Piperaceae: Z =

1,009.63, P < 0.001). Fruit production of Solanaceae was

negatively related to air temperature (standardized partial co

efficient of the multiple regression [b'] = ?0.659, P = 0.034)




Table 2.?Monthly variation in the diet of Sturnira lilium, represented as the number of fecal samples that contained the species of plant

indicated (cells without numbers were zeros). Seeds that could not be identified to genus are represented as morphospecies of Piperaceae (p.02) or

Solanaceae (all others). All fecal samples contained only 1 kind of seed.

Oct. Nov. Dec. No Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb.

Species 2003 2003 2003 sampling 2004 2004 2004 2004 2004 2004 2004 2004 2004 2004 2005 2005

Cecropiaceae Period with

Cecropia glaziovii 1 sampling, but

Piperaceae almost no

Piper gaudichaudianum captures of 13

p.02 1 S. lilium

Piper corintoanum 1

Piper hoehnei 2

Solanaceae

Aureliana fasciculata 1 1

Aureliana sp. 2

Solanum capsicum 1

Solanum granulosoleprosum 7 10 1 6 5

Solanum sanctae-katharinae 1 111

Vassobia breviflora 2

s.05 1

s.06 1 1 1

s.07 2 5 1

s.08 1

s.09 1 11

s.10 1

s.ll 1

s.12 1

s.26 1 1

s.27 1

Total 9 13 16 ? 25 0 000068802

but it was 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

(model: y = 1.06 + 0.32 x In x, n = 1, r2 = 0.29, P = 0.20;

Fig. 4).

Discussion

Based on our observations and including extensive literature

surveys, we suggest that fruits of Solanaceae are the most im

portant food source for S. lilium in lowland as well as in high land habitats. We propose that low winter temperatures may

force bats to migrate to the warmer lowlands, because S. lilium

may not tolerate well the very low temperatures during this season. Here we discuss some implications of those patterns

observed.

Our results revealed an entirely frugivorous diet for S. lilium.

This is in accordance with most other studies of this species (see a wide list of case studies in Geiselman et al. [2002]).

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

(Fleming 1988), may meet its nutritional requirements by

feeding only on fruits. Although we cannot exclude the pos

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

may allow S. lilium to meet all its energetic and nitrogen needs.

Fruits of Solanaceae were the main food of S. lilium.

Piperaceae and Cecropiaceae also were consumed, albeit to a

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).

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

ple, if the bats reacted opportunistically to fruit abundance, they 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

(Bonaccorso and Gush 1987; Fleming 1986; Giannini 1999;

Hernandez-Conrique et al. 1997). Fruits of other plant families

may supplement energetic or mineral needs or both of S. lilium

when the fruit crop of Solanaceae is low. The relationship between S. lilium and the Solanaceae seems to be as strong as is

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




Table 3.?Fruiting phenology of Solanaceae and Piperaceae in the study area. Numbers inside parentheses after names of species represent

sample sizes. Cells without numbers are months when monitored plants were not producing fruits. Plants of the Solanaceae were permanently

marked, whereas plants of Piperaceae were randomly sampled each month. For further explanation see "Materials and Methods." Species whose

seeds were observed in fecal samples of Sturnira lilium during this study are marked with an asterisk (*).

Mar. Apr. May Jun. Jul. Aug. Sep. Oct. Nov. Dec. Jan. Feb.

Species (n) 2004 2004 2004 2004 2004 2004 2004 2004 2004 2004 2005 2005

Solanaceae

Aureliana cf. fasciculata (1)* 100% 100%

Aureliana sp. 1 (13) 23% 8% 8% 8% 15%

Aureliana sp. 3 (1) 100%

Solarium granulosoleprosum (22)* 5% 45% 59% 68% 68% 5%

Solarium phyllosepalum (11) 9% 9% 27% 18%

Solarium sanctae-katharinae (3)* 33% 67% 67% 33% 33%

Solarium variabile (14) 21% 14% 7% 7% 7% 36% 29% 36% 21%

Vassobia breviflora (3)* 33% 33% 100% 33%

Piperaceae

Piper gaudichaudianum (10)* 50% 46% 33% 64% 100% 71% 10%

Piper hispidum (10) 14% 12% 33% 21% 7% 7% 23%

Piper mosenii (10) 50% 86%

Contrary to our expectation that fruit consumption of

Solanaceae by S. lilium should be positively related to fruit

production, this relationship was not significant. The main 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

results that most of the bats might migrate temporarily to

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

1.20 -I

S>

o

=5

.E 0.80 -

0) CO <D

O CO

I o (/> m- 0.40

-

O

42 3

? r2 = 0.29, p

= 0.20

o.oo -I- -,-.-1

0.00 0.40 0.80 1.20

% Individuals of Solanaceae producing fruits

Fig. 4.?Relationship between consumption rate of Solanaceae

fruits by Sturnira lilium, expressed as percentage of samples that

contained seeds of this family, by month (percents are arcsine

transformed), and fruit production of Solanaceae, expressed as

proportion of plants producing fruits each month.

tropical or temperate environments are likely to conduct

seasonal migrations. Further evidence for possible elevational

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 in montane forests, because

bat fruits were more abundant during the cold, dry season when

most S. lilium appeared to leave the area. Compared to the

tropical lowlands, temperatures are much lower during the

cold season, with an average minimum temperature of 12?C.

Occasionally, temperatures even drop as low as ?4?C. Low

temperatures over longer periods of time probably affect S. lilium negatively, because small fruit-eating bats have in

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

heat (Fleming and Eby 2003). The influence of air temperature on the demography of

tropical bats is probably much larger than previously thought. There is increasing evidence that reproduction in small phyllo stomids is related to air temperature, because, for example,

C. perspicillata tends to peak its reproductive activity during warmer months independent of resource levels (Mello et al.

2004b). As a reaction to low air temperatures, bats may

undergo "facultative hypothermia" or torpor (see Dietz and

Kalko 2006; Speakman and Thomas 2003). They save energy

by temporarily lowering their body temperature. This strategy also is known for phyllostomids (Audet and Thomas 1997).

However, in contrast to other bat families such as Vespertilio nidae and Rhinolophidae, phyllostomids may be unable to

undergo long bouts of torpor (Speakman and Thomas 2003).

Alternatively, they may temporarily migrate to lower elevations

during cold seasons (Giannini 1999), as we suspect from

examination of our data on S. lilium.




This suspected elevational migration in our study area

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

endangered if the habitats are seriously altered along the

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

migrants and thus the ecological services provided by them.

This reinforces the propositions of Loiselle and Blake (1991), who were among the 1st to propose the crucial importance of

"intact" elevational gradients for migrant and resident birds

in Costa Rica.

Resumo

Nos estudamos as variacoes na dieta e na abundancia do

morcego Sturnira lilium (Chiroptera: Phyllostomidae) em uma

Mata Atlantica de montanha, a fim de investigar se os padroes neste habitat diferem das baixadas, que sao mais bem estuda

das. A dieta desta especie foi avaliada com base em amostras

fecais, enquanto que possiveis variacoes na abundancia foram

documentadas com base no sucesso de captura. Nos tambem

monitoramos e relacionamos a variabilidade na temperatura

do ar com a producao de frutos de Solanaceae, o principal alimento de S. lilium. Os morcegos se alimentaram exclusiva

mente de frutos e principalmente de Solanaceae, e ocasional

mente de Piperaceae e Cecropiaceae. S. lilium esteve quase

totalmente ausente da area durante os meses mais frios,

sugerindo que esses morcegos podem migrar para altitudes

mais baixas e, portanto, mais quentes. A ausencia dos morcegos

nao esteve relacionada com um marcado declinio na disponibi

lidade de frutos de Solanaceae, ja que a producao de frutos nao

apresentou relacao com a temperatura. Nos concluimos que, em

sistemas montanhosos tropicais, a abundancia de alguns

morcegos frugivoros pode ser mais afetada pela temperatura do ar do que pela disponibilidade de comida. Alem disso, nos

reforcamos a ideia de que preservar gradientes altitudinais e

crucial para a conservacao de especies migratorias.

Acknowledgments

We thank our colleagues at the Programa de Pos-Graduacao em

Ecologia of the Universidade Estadual de Campinas, the Institut

Experimentelle Okologie of the Universitat Ulm, Germany, and

Parque Estadual Intervales, who helped us a lot during fieldwork and

laboratory work: A. Alves, B. Oliveira, B. Buzatto, C. Meyer, E.

Paula, G. Machado, G Requena, J. Fahr, M. Gonzaga, M. Weinbeer,

N. Leiner, N. Ebigbo, P. Jordano, R. Alonso, R. Paiva, S. Spehn, and

S. Silva. M. A. R. Mello was sponsored, at different periods, by Conselho Nacional de Pesquisa e Desenvoluimento/Deutscher Aka

demischer Austauschdienst, Fundacao de Amparo a Pesquisa do

Estado de Sao Paulo (FAPESP) (02/09286-0), and Coordenacao de

Aperfeicoamento de Pessoal de Nivel Superior (290088/2004-6).

Equipment was provided by FAPESP, Bat Conservation International, and Idea Wild.

Literature Cited

Audet, D., and D. W. Thomas. 1997. Facultative hypothermia as

a thermoregulatory strategy in the phyllostomid bats, Carollia

perspicillata and Sturnira lilium. Journal of Comparative Physiol

ogy 167:146-152.

Bizerril, M. X. A., and A. Raw. 1997. Feeding specialization of two

species of bats and the fruit quality of Piper arboreum in a central

Brazilian gallery forest. Revista de Biologia Tropical 45:913-918.

Bonaccorso, F. J., and T. J. Gush. 1987. Feeding behaviour and

foraging strategies of captive phyllostomid fruit bats: an experi

mental study. Journal of Animal Ecology 56:907-920.

Caceres, N. C, and M. O. Moura. 2003. Fruit removal of a wild

tomato, Solanum granulosoleprosum Dunal (Solanaceae) by birds,

bats and non-flying mammals in an urban Brazilian environment.

Revista Brasileira de Zoologia 20:519-522.

Delorme, M., and D. W. Thomas. 1996. Nitrogen and energy

requirements of the short-tailed fruit bat (Carollia perspicillata)'. fruit bats are not nitrogen constrained. Journal of Comparative

Physiology 166:427^134.

Dietz, M., and E. Kalko. 2006. Seasonal changes in daily torpor

patterns of free-ranging female and male Daubenton's bats (Myotis

daubentonii). Journal of Comparative Physiology 176:223-231.

Emmons, L. H., and F. Feer. 1997. Neotropical rainforest mammals:

a field guide. University of Chicago Press, Chicago, Illinois.

Fleming, T. H. 1986. Opportunism versus specialization: the evolution

of feeding strategies in frugivorous bats. Pp. 105-118 in Frugivores and seed dispersal (A. Estrada and T. H. Fleming, eds.). Dr. W.

Junk Publishers, Dordrecht, The Netherlands.

Fleming, T. H. 1988. The short-tailed fruit bat: a study in plant-animal interactions. University of Chicago Press, Chicago, Illinois.

Fleming, T. H., and P. Eby. 2003. Ecology of bat migration. Pp. 156

208 in Bat ecology (T. H. Kunz and M. B. Fenton, eds.). University

of Chicago Press, Chicago, Illinois.

Fleming, T. H., and V. J. Sosa. 1994. Effects of nectarivorous and

frugivorous mammals on reproductive success of plants. Journal of

Mammalogy 75:845-851.

Gannon, M., M. Willig, and J. Jones. 1989. Sturnira lilium.

Mammalian Species 333:1-5.

Gannon, W. L., R. S. Sikes, and the Animal Care and Use

Committee of the American Society of Mammalogists. 2007.

Guidelines of the American Society of Mammalogists for the use of

wild mammals in research. Journal of Mammalogy 88:809-823.

Geiselman, C. K., S. A. Mori, and F. Blanchard. 2002. Database

of neotropical bat/plant interactions, http://www.nybg.org/botany/

tlobova/mori/batsplants/database/dbase_frameset.htm. Accessed 15

December 2007.

Giannini, N. 1999. Selection of diet and elevation by sympatric

species of Sturnira in an Andean rainforest. Journal of Mammalogy 80:1186-1195.

Goodwin, G, and A. Greenhall. 1961. A review of the bats of

Trinidad and Tobago. Bulletin of the American Museum of Natural

History 2:187-302.

Hernandez-Conrique, D., L. Iniguez-Davalos, and J. F. Storz.

1997. Selective feeding by phyllostomid fruit bats in a subtropical montane cloud forest. Biotropica 29:376-379.

Herrera, L. G, K. A. Hobson, A. Manzo, D. Estrada, V. Sanchez

Cordero, and C. Mendez. 2001. The role of fruits and insects in the

nutrition of frugivorous bats: evaluating the use of stable isotope models. Biotropica 33:520-528.

Iudica, C. A., and F. J. Bonaccorso. 1997. Feeding of the bat,

Sturnira lilium, on fruits of Solanum riparium influences dispersal




of this pioneer tree in forests of northwestern Argentina. Studies on

Neotropical Fauna and Environment 32:4-6.

Korine, C, E. K. V. Kalko, and E. A. Herre. 2000. Fruit removal

by bats and birds from a community of strangler figs in Panama.

Oecologia 123:560-568.

Leiner, N. O. 2005. Ecologia alimentar e reprodutiva de Marmosops

paulensis (Didelphimorphia: Didelphidae) em uma area de Mata

Atlantica no sudeste de Sao Paulo. M.S. thesis, Universidade

Estadual de Campinas, Campinas, Brazil.

Loiselle, B. A., and J. G. Blake. 1991. Resource abundance and

temporal variation in fruit-eating birds and along a wet forest

elevational gradient in Costa Rica. Ecology 72:180-193.

Mantovani, W. 2001. A paisagem dinamica. Pp. 81-92 in Intervales

(C. Leonel, ed.). Fundacao para a Conservacao e a Producao

Florestal do Estado de Sao Paulo, Sao Paulo, Brazil.

Marinho-Filho, J. S., and I. Sazima. 1998. Brazilian bats and

conservation biology: a first survey. Pp. 282-294 in Bat biology and

conservation (T. H. Kunz and P. A. Racey, eds.). Smithsonian

Institution Press, London, United Kingdom.

Mello, M. A. R. 2002. Interacoes entre o morcego Carollia

perspicillata (Linnaeus, 1758) (Chiroptera: Phyllostomidae) e

plantas do genero Piper (Linnaeus, 1737) (Piperales: Piperaceae)

em uma area de Mata Atlantica. M.S. thesis, Universidade do

Estado do Rio de Janeiro, Rio de Janeiro, Brazil.

Mello, M. A. R. 2006. Interacoes entre o morcego Sturnira lilium

(Chiroptera: Phyllostomidae) e plantas da familia Solanaceae. Ph.D.

dissertation, Universidade Estadual de Campinas, Campinas, Brazil.

Mello, M. A. R., G. M. Schittini, P. Selig, and H. G. Bergallo.

2004a. Seasonal variation in the diet of the bat Carollia

perspicillata (Chiroptera : Phyllostomidae) in an Atlantic Forest

area in southeastern Brazil. Mammalia 68:49-55.

Mello, M. A. R., G M. Schittini, P. Selig, and H. G Bergallo. 2004b.

A test of the effects of climate and fruiting of Piper species

(Piperaceae) on reproductive patterns of the bat Carollia per

spicillata (Phyllostomidae). Acta Chiropterologica 6:309-318.

Nowak, R. M. 1994. Walker's bats of the world. Johns Hopkins

University Press, London, United Kingdom.

Passos, F. C, W. R. Silva, W. A. Pedro, and M. R. Bonin. 2003.

Frugivoria em morcegos (Mammalia, Chiroptera) no Parque

Estadual Intervales, sudeste do Brasil. Revista Brasileira de

Zoologia 20:511-517.

Simmons, N. B. 2005. Order Chiroptera. Pp. 312-529 in Mammal

species of the world: a taxonomic and geographic reference (D. E.

Wilson and D. M. Reeder, eds.). 3rd ed. Johns Hopkins University

Press, Baltimore, Maryland.

Simmons, N., and R. Voss. 1998. The mammals of Paracou, French

Guiana: a neotropical lowland rainforest fauna?part 1: bats.

Bulletin of the American Museum of Natural History 237:1-219.

Speakman, J., and D. Thomas. 2003. Physiological ecology and

energetics of bats. Pp. 430^492 in Bat ecology (T. Kunz and

M. Fenton, eds.). University of Chicago Press, Chicago, Illinois.

Stones, R. C, and J. E. Wiebers. 1965. A review of temperature

regulation in bats. American Midland Naturalist 74:155-167.

Straube, F., and G Bianconi. 2002. Sobre a grandeza e a unidade

utilizada para estimar esforco de captura com utilizagao de redes-de

neblina. Chiroptera Neotropical 8:150-152.

Thies, W., and E. K. V. Kalko. 2004. Phenology of neotropical

pepper plants and their association with their main dispersers, two

short-tailed fruit-bats, Carollia perspicillata and C castanea,

Phyllostomidae. Oikos 104:362-376.

Thomas, D. W. 1984. Fruit intake and energy budgets of frugivorous

bats. Physiological Zoology 57:457^-67.

Uieda, W., and J. Vasconcellos-Neto. 1985. Dispersao de Solanum

spp. (Solanaceae) por morcegos, na regiao de Manaus, AM, Brasil.

Revista Brasileira de Zoologia 2:449^158.

Vizotto, L. D., and V. A. Taddei. 1973. Chave para determinacao de

quiropteros brasileiros. Editora da Universidade Estadual de Sao

Paulo, Sao Jose do Rio Preto, Brazil.

Zar, J. H. 1996. Biostatistical analysis. Prentice-Hall, Upper Saddle

River, New Jersey.

Submitted 30 November 2006. Accepted 15 July 2007.

Associate Editor was Rodrigo A. Medellin.



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