Ambient temperature is more important than food
availability in explaining reproductive timing of the
bat Sturnira lilium (Mammalia: Chiroptera) in a
montane Atlantic Forest
M.A.R. Mello, E.K.V. Kalko, and W.R. Silva
Abstract: Reproduction of bats is determined by a suite of endogenous and exogenous factors. Among exogenous influen-
ces, special attention has been given to the influence of food availability. However, in highland forests, severe decreases
in temperature during the cold and dry season may also play an important role. In the present study we tested the influence
of ambient temperature and food availability on the timing of reproduction in the frugivorous bat Sturnira lilium
(E. Geoffroy, 1810). We conducted a 15-month mist-netting sampling in a mountain area of the Brazilian Atlantic Forest
during which time we assessed the bats? diet through fecal samples, monitored fruit production of the main food plants,
and recorded variations in ambient temperature. Sturnira lilium fed almost exclusively on Solanaceae. Similarly to the low-
lands, reproduction was bimodal, but reproductive season tended to be shorter in the highlands and peaked in the warmer
months of the year. Overall, 44% to 53% of the reproductive pattern was explained by variations in ambient temperature,
while the relationship with food availability was nonsignificant. We conclude that variations in ambient temperature in
tropical mountains may be a stronger selection pressure than food availability in determining reproductive timing of bats.
Re?sume? : La reproduction des chauves-souris est de?termine?e par une se?rie de facteurs endoge`nes et exoge`nes. Parmi les
facteurs exoge`nes, on a porte? une attention particulie`re a` l?influence de la disponibilite? de nourriture. Cependant, dans les
fore?ts des terres hautes, les grandes chutes de tempe?rature durant la saison froide et se`che peuvent aussi jouer un ro?le im-
portant. Dans notre recherche, nous testons l?influence de la tempe?rature ambiante et de la disponibilite? de la nourriture
sur le calendrier de la reproduction chez la chauve-souris frugivore Sturnira lilium (E. Geoffroy, 1810). Nous avons fait
une e?chantillonnage pendant 15 mois dans une re?gion montagneuse de la Fore?t atlantique bre?silienne; nous avons de?ter-
mine? le re?gime alimentaire des chauves-souris par pre?le`vement de fe`ces, suivi la production de fruits des principales
plantes nourricie`res et enregistre? les variations de la tempe?rature ambiante. Sturnira lilium se nourrit presque exclusive-
ment de Solanaceae. Comme dans les basses terres, la reproduction est bimodale, mais la saison de reproduction tend a`
e?tre plus courte dans les terres hautes et elle atteint un sommet durant les mois plus chauds de l?anne?e. Les variations de
la tempe?rature ambiante expliquent globalement 44 % a` 53 % du patron de reproduction, alors que la relation avec la dis-
ponibilite? de nourriture n?est pas significative. Nous en concluons que dans les montagnes tropicales, les variations de la
tempe?rature ambiante peuvent exercer une pression de se?lection plus grande que la disponibilite? de nourriture dans la de?-
termination du calendrier de reproduction des chauves-souris.
[Traduit par la Re?daction]
Introduction
Bats (Mammalia: Chiroptera) are highly diverse world-
wide including Brazil (Simmons 2005), where they consti-
tute one third of the country?s mammal species (Marinho-
Filho and Sazima 1998). They have an unusual combination
of life-history characteristics (Barclay and Harder 2003).
Most bats are small compared with other mammals (<50 g)
but are long-lived, as some individuals in the temperate zone
have been recorded to live more than 40 years. They are
also slow-breeding, mostly with one or two offspring a
year, which makes every reproductive season very important
(Barclay and Harder 2003). A variety of factors are regarded
as determinants of reproductive timing, including endo-
genous causes, especially the hormonal cycle (Klose et al.
2006), and exogenous causes, represented mainly by diet,
food availability, day length, rainfall, and temperature
(Kunz 1982; Handley et al. 1991; Kalko 1998; Arlettaz et
al. 2001; Barclay et al. 2004).
Regarding reproductive timing, bat populations are char-
acterized by four basic patterns (Fleming et al. 1972): con-
tinuous reproduction throughout the year, a single
reproductive season a year, two or more well-defined repro-
ductive seasons a year, and no clearly defined reproductive
Received 2 June 2008. Accepted 2 February 2009. Published on
the NRC Research Press Web site at cjz.nrc.ca on 26 February
2009.
M.A.R. Mello.1 Departamento de Bota?nica, Universidade
Federal de Sa?o Carlos, Rodovia Washington Lu??s,
Km. 235, 13565-905, Sa?o Carlos, SP, Brazil.
E.K.V. Kalko. Institute of Experimental Ecology, University of
Ulm, Albert Einstein Allee 11, 89069 Ulm, Germany;
Smithsonian Tropical Research Institute, Balboa, Panama.
W.R. Silva. Departamento de Zoologia, Universidade
Estadual de Campinas, Cidade Universitaria Zeferino Vaz,
s/n UNICAMP, 13083-970, Campinas, SP, Brazil.
1Corresponding author (e-mail: marmello@gmail.com).
239
Can. J. Zool. 87: 239?245 (2009) doi:10.1139/Z09-010 Published by NRC Research Press
pattern. Differences in those patterns have been linked
mainly to differences in diet and temporal availability of
food (Crichton and Krutzsch 2000). Whereas ambient tem-
perature is well known to influence reproductive pattern of
bats in the temperate zone (Crichton and Krutzsch 2000), it
may also be more important in the tropics than previously
thought (Mello et al. 2004).
In the Neotropics, fruit-eating leaf-nosed bats are a very
interesting study group, because they feed on an easily-
trackable resource, fruits, making the monitoring of food
availability much less difficult than for instance in insect-
eating bats (Kunz 1988). This permits linkage of seasonal
variation in food over time with reproductive seasonality,
thus allowing accurate assessment of the relative strength of
this and other exogenous factors such as ambient tempera-
ture. Thus far, our knowledge on the reproductive ecology
of frugivorous leaf-nosed bats is still limited, encompassing
only a few species, which is remarkable little given the high
diversity and ecological importance of this group (Zorte?a
2003; Mello et al. 2004; Klose et al. 2006).
We selected one of the most widespread and common
neotropical bat species (Simmons 2005), the stenodermatine
little yellow-shouldered bat (Sturnira lilium (E. Geoffroy,
1810)), as an example to better understand the relationship
between reproduction and exogenous factors, namely food
availability and ambient temperature. Members of the sub-
family Stenodermatinae feed almost exclusively on fruits,
encompassing 28 plant families and 83 plant species that
have been listed as food for S. lilium (Mello et al. 2008a).
This species has a strong preference for fruits of the family
Solanaceae, which represent usually over 80% of its diet
(Mello et al. 2008a). Despite this preference, S. lilium can
be considered a generalist to some degree, because local
population feed on a great number of Solanaceae species
(Mello et al. 2008a). Sturnira lilium seems to follow the bi-
modal reproductive pattern of stenodermatines and phyllos-
tomids in general (Handley et al. 1991). However, most
studies on S. lilium have been conducted in tropical low-
lands, and little is known about the ecology of this species
in montane regions (Mello et al. 2008b). It is known that,
on average, plant diversity and abundance is lower in high-
lands if compared with lowlands of the Atlantic Forest
(Mantovani 2001), thus it is reasonable to suppose that food
availability for frugivorous leaf-nosed bats may be lower in
highlands.
Although the tropics are often regarded as stable environ-
ments with low seasonality and nearly constant food avail-
ability (Ricklefs and Wikelski 2002), variations in some
factors, especially ambient temperature, may have ecologi-
cally important consequences (Speakman and Thomas 2003;
Mello et al. 2004). Palearctic and Nearctic bat species are
well adapted to a wider range of decreases in ambient tem-
perature if compared with tropical bar species (Speakman
and Thomas 2003). As an example, in the case of moderate
drops in temperature, species such as trawling Daubenton?s
bats (Myotis daubentonii (Kuhl, 1817)) temporarily increase
food intake, form larger aggregations in nursery colonies,
and reduce the use of torpor to prioritize reproductive de-
mands during colder seasons (Dietz and Kalko 2006). Other
temperate species like European free-tailed bats (Tadarida
teniotis (Rafinesque, 1814)) may achieve a stronger drop in
body temperature and hibernate (Arlettaz et al. 2000). How-
ever, their neotropical counterparts differ in thermoregula-
tory strategies and do not cope well with severe drops in
environmental temperature (Speakman and Thomas 2003).
When faced with low temperatures during winter, leaf-nosed
bats like S. lilium can only resort to suboptimal strategies
such as facultative hypothermia (Audet and Thomas 1997)
or probably migration (Mello et al. 2008b). Therefore, tak-
ing into account that S. lilium does not cope well with big
drops in temperature, and that this bat species is able to
feed on a wide range of fruits (even considering the prefer-
ence for Solanaceae) and even other items like pollen and
nectar, environmental temperature may be more important
than food availability in determining reproductive timing of
frugivorous leaf-nosed bats in highlands of the Atlantic For-
est. This is a reasonable hypothesis, because even during
seasons of overall fruit scarcity, especially during winter,
there are always some fruits and flower products available,
thus the diet limitation is less important than the temperature
limitation.
Thus, considering that (i) our study population of S. lilium
lives in a montane region with a severe winter by subtropi-
cal standards, (ii) this species does not cope well with low
temperatures, and (iii) that ambient temperature may be im-
portant in determining reproductive timing (Mello et al.
2004), our objective was to test the hypothesis that S. lilium
exhibits a relatively short reproductive season compared
with patterns observed for the same species in the tropical
lowlands. We expected the main reproductive peak of S. lil-
ium to occur during summer, when temperatures are
warmer, so that recruitment and weaning of juveniles, two
very costly activities, would take place when it is easier to
maintain normothermic body temperatures. Furthermore, we
predicted that the typical bimodal reproductive pattern usu-
ally documented for stenodermatine bats would be less
marked or even unimodal in our study area, because of the
harsh climatic seasonality that may force bats to reproduce
within a shorter time window.
Materials and methods
Time frame and study area
Fieldwork was conducted during 15 monthly sample peri-
ods from October 2003 to February 2005 (except January
and February 2004) in the protected area Parque Estadual
Intervales (hereafter Intervales), Sa?o Paulo state, southeast-
ern Brazil. Intervales is part of the ??Paranapiacaba Ecologi-
cal Continuum??, which comprises more than 100 000 ha and
is the largest continuous remnant of Atlantic Forest in Bra-
zil, one of the hotspots of the International Union for the
Conservation of Nature and Natural Resources (Myers et al.
2000).
Inside the park, we chose the area known as Sede de Pes-
quisa (24816?24.7@S, 48825?00.6@W). This area is located
850 m above sea level and represents the highest elevation
in the park. The climate of this region is classified as tem-
perate humid (Mantovani 2001). Mean temperatures of
22 8C during the warmest months (October?March), and
during the coldest months absolute minimum temperatures
may reach ?4 8C during the colder months (April?September)
in the highlands. There are 1?5 days of frost each year. At
240 Can. J. Zool. Vol. 87, 2009
Published by NRC Research Press
Sede de Pesquisa, the main vegetation consists of montane
Atlantic Forest (Mantovani 2001).
Sturnira lilium is the most abundant bat species in the
area (Passos et al. 2003). Extensive inventories of the local
flora, as well as reference collections for seeds found in the
feces of bats and birds, are available (Passos et al. 2003).
For other aspects of the ecology of S. lilium in the area see
Mello (2006) and Mello et al. (2008a, 2008b).
Data collection
The staff at Intervales? meteorological station provided us
with data on ambient temperature. We did not include rain-
fall because its influence is reflected indirectly in fruit avail-
ability (Mello et al. 2004). Variation in climate followed the
general trend of the previous 7 years (Mello et al. 2008a).
Capture and handling of bats were carried out in accord-
ance to guidelines for animal care and use approved by the
American Society of Mammalogists (Gannon and Sikes
2007). We captured bats on a monthly basis in two consec-
utive nights, using 10 nylon mist nets (7 m  3 m, mesh
36 mm; Ecotone, Inc., Sopot, Poland). Nets were set on
trails and dirt roads at a minimum distance of 30 m and
kept open for 6 h after local sunset. Every 30 min we
checked nets for bats. Between capture and release bats
were kept in individual cloth bags for 1?4 h, so we could
get fecal samples for dietary analysis. Bats were banded
with aluminum rings with individual markings (A.C. Hughes
Inc., Middlesex, England), always using ring sizes that were
30% larger than the bat?s forearm diameter to minimize in-
juries. We identified the bat species with a combination of
keys (Vizotto and Taddei 1973; Gannon et al. 1989; Em-
mons and Feer 1997; Simmons and Voss 1998). Marcelo R.
Nogueira (Universidade Estadual do Norte Fluminense) con-
firmed the identification of two voucher specimens (one
male and one female). We followed Kunz (1988) in estimat-
ing age of bats, considering juveniles to be those with at
least one unossified epiphysis in the bones of wing fingers
and adults to be those with all epiphyses ossified. We used
external characters to determine reproductive condition of
adult bats. Females were classified into five categories ac-
cording to the status of the nipples (hair cover, color, and
size) and the presence of a palpable embryo following Kunz
(1988): 1, inactive; 2, pregnant; 3, lactating; 4, pregnant and
lactating; 5, postlactating. Males were categorized according
to the position of their testes, either inside the abdomen or
inside the scrotum. Because the position of the testes may
vary according to other effects as well (i.e., fear, cold tem-
peratures), we also documented the condition of the males?
shoulder glands, which were either active (bright reddish,
sticky fur around glands with a strong, terpentine-like smell)
or inactive following Gannon et al. (1989). Males were as-
signed as ??reproductive??, considering both testes and
shoulder gland condition. Age was estimated using the
method proposed by Kunz (1988), based on the ossification
of the digital epiphyses.
We investigated the feeding habits of S. lilium by analyz-
ing fecal samples, which we collected directly from 96 bats
captured in mist nets using small plastic vials and from indi-
viduals that we kept for 1?4 h inside clean cloth bags.
Seventy individual Solanaceae of 13 species were marked
and monitored on a monthly basis to estimate food availabil-
ity for S. lilium (Mello et al. 2008a).
Data analysis
Data on climate were analyzed on a monthly basis (Mello
et al. 2008a). Total netting effort during our study was
41 580 hm2 (total area of nets opened multiplied by the total
number of hours sampled) following Straube and Bianconi
(2002). We characterized the reproductive status of the pop-
ulation of S. lilium on a monthly basis as the proportion of
females and males in each reproductive class in relation to
total numbers of captures of adult females and males in the
respective month. We tested the relationship between ambi-
ent temperature, fruit production of Solanaceae, and propor-
tions of reproductive females and males using simple
nonlinear regressions (model: y = axb). We chose this geo-
metric model because we predicted that the response of bats
to the variation in ambient temperature should be nonlinear,
first exhibiting a fast increase in reproductive activity when
temperature increases and then reaching a plateau when the
percentage of reproductive females approaches the maxi-
mum of 100%.
We identified seeds from 96 fecal samples and pooled di-
etary data of S. lilium on a monthly basis as the percentage
of samples for each plant family to assess possible temporal
variation in diet (for details on dietary analysis see Mello et
al. 2008a). Concerning phenology of food plants, we as-
sessed the status of each population of Solanaceae species
as the percentage of adult individuals producing fruits on a
monthly basis (details in Mello et al. 2008a). We based our
statistical analyses on Zar (1996), and used SPSS version
16.0 (SPSS Inc., Chicago, Illinois, USA) for regular statis-
tics and Oriana version 2.0 (Kovach Computing Services,
Anglesey, Wales) for circular statistics in our calculations.
Percent data were arcsine-transformed.
Results
We captured a total of 477 bats including recaptures, rep-
resenting 15 species. This corresponds to about 40% of the
bat species that have been recorded for the park (34 species;
see Mello 2006). Sturnira lilium represented 70% of all cap-
tures (333 captures with 8% recaptures). The observed sex
ratio was biased towards females (189 females and 142
males: c2 = 6.39, p = 0.01) with little variation among
months (G = 21.61, p = 0.06).
The population of S. lilium showed a marked trend to-
wards seasonal fluctuations. Capture success varied strongly
between months, with a concentration of captures in the
middle of the rainy and warm season (October?March), es-
pecially during summer (Rayleigh?s Z = 18.58, p < 0.001)
(Fig. 1). During the cold and dry months (April?September),
S. lilium was either not captured at all or at very low num-
bers. Overall, we captured far more adults (n = 287) than
subadults (n = 25) or juveniles (n = 19), resulting in an age
structure dominated by adults (c2 = 424.48, p < 0.001). Age
structure revealed two distinct peaks of juvenile recruitment
per year, one in the middle of the rainy season and another
one between the rainy and dry seasons (Rayleigh?s Z = 7.33,
p < 0.001) (Fig. 1). This finding is in accordance with the
results on the reproductive patterns of females (Rayleigh?s
Mello et al. 241
Published by NRC Research Press
Z = 12.75, p < 0.001) (Fig. 2) and males (Rayleigh?s Z =
5.32, p = 0.005) (Fig. 3), which both exhibited a bimodal
pattern in reproduction with peaks very close to each other.
As predicted, ambient temperature explained a large por-
tion of variation in reproductive timing of females (r2 =
0.44, p = 0.02, n = 12, ) and males (r2 = 0.53, p = 0.01, n =
12, ) in contrast to fruit production that did not explain the
variation in the percentage of reproductive females (r2 =
0.04, p = 0.95, n = 12, ) or males (r2 = 0.02, p = 0.70, n =
12, ) (Fig. 4).
The diet of S. lilium was entirely frugivorous during the
study with a clear dominance of Solanaceae (Mello et al.
2008a). Although the proportions of each plant family in
the bats? diet varied during the months, fruits of Solanaceae
dominated throughout the year (detailed dietary analysis in
Mello et al. 2008a). The majority of species of Solanaceae
(9 from 12 species) revealed a steady-state strategy and con-
tinuously produced fruits over several months, with a peak
between the dry and the rainy seasons (details in Mello et
al. 2008a). Therefore, fruits of Solanaceae in general were
available during most of the year, but the largest abundance
of those fruits occurred during the beginning of the rainy
season. However, bats could choose from more Solanaceae
species during the dry season than in the rainy season.
Discussion
In our study, we confirmed our hypothesis that ambient
temperature affects reproductive seasonality of the frugivo-
rous S. lilium more than food availability in a montane re-
gion of the Atlantic Forest. Although we observed a
bimodal reproductive pattern for S. lilium as it is known
from lowland locations (Stoner 2001; De Knegt et al.
2005), reproduction was concentrated in a shorter period in
the highlands and the first (main) and the second reproduc-
Fig. 1. Monthly variation in the age structure of populations of the little yellow-shouldered bat (Sturnira lilium) in Intervales, southeastern
Brazil. ??Interval?? stands for a 2-month period when we could not carry out our sampling because of logistic problems.
Fig. 2. Monthly variation in the number of adult females of the little yellow-shouldered bat (Sturnira lilium) classified into different repro-
ductive conditions in Intervales, southeastern Brazil.
242 Can. J. Zool. Vol. 87, 2009
Published by NRC Research Press
tive peaks were less distinct compared with the pattern reg-
istered for other neotropical leaf-nosed bats, like carolliines
and glossophagines in the lowlands of rain forests, whose re-
productive peaks last longer (Mello and Fernandez 2000;
Zorte?a 2003; Tschapka 2005). As an example, most preg-
nant female S. lilium at a study site in the lowlands of Costa
Rica were registered in a 5-month period (Stoner 2001),
whereas pregnancy was concentrated in only 2 or 3 months
in our study area in the mountains.
The pattern of two reproductive peaks has been attributed
Fig. 3. Monthly variation in the number of adult males of the little yellow-shouldered bat (Sturnira lilium) classified into different repro-
ductive conditions in Intervales, southeastern Brazil.
Fig. 4. Relationships between the percentage of reproductive adult females and males of the little yellow-shouldered bat (Sturnira lilium),
ambient temperature (8C), and fruit production of the plant family Solanaceae (%). Percentages were arcsine-transformed.
Mello et al. 243
Published by NRC Research Press
to a postpartum estrus in New World leaf-nosed bats, where
females mate again shortly after giving birth (while they are
still nursing pups; Crichton and Krutzsch 2000). This is seen
as a strategy of a large number of tropical bat species to in-
crease the number of offspring per year from one to two per
female depending on their fitness (Cosson and Pascal 1994;
Tschapka 2005).
Our prediction of a positive relationship between temper-
ature and reproductive cycle was fully supported, as ambient
temperature explained the largest portion of reproductive
timing of females (44%) and males (53%). At high altitudes,
as in our study area, temperature is a critical factor, because
low winter temperatures may not be tolerated well as they
generate unfavorable conditions for bats like S. lilium
(Speakman and Thomas 2003; Willis et al. 2006), whose
thermoregulatory ability is not as efficient as in other groups
with a global distribution such as vespertilionids (Audet and
Thomas 1997). Interestingly, evidence accumulated that
S. lilium and probably also other fruit-eating bats may cir-
cumvent this difficulty by migrating to lower altitudes dur-
ing the coldest months (Giannini 1999; Mello et al. 2008b).
This may explain the absence or very low numbers of
S. lilium bats in highlands during winter, as they tend to re-
main abundant throughout the year in lowlands (Giannini
1999; Aguiar and Marinho-Filho 2004). It is unknown
whether S. lilium reproduces during this time in lower alti-
tudes, and this possibility should be tested in future studies.
We conclude from the short reproductive period that
S. lilium has adjusted its reproductive cycle to the specific
environmental conditions of highlands by limiting its main
reproductive activity to the short but favorable season in
summer. This supports the proposition that despite the lower
seasonality of the tropics compared with the temperate zone,
small variations in environmental factors, such as ambient
temperature, may exert rather strong pressures that force
tropical species, for instance, to adjust their reproductive
pattern. In future studies, it will be interesting to investigate
whether highland species, provided they migrate, add a third
reproductive phase. Probably, this might not happen, as the
effect of highland immigrants on lowland residents should
increase competition for food and shelter.
Acknowledgements
We thank our colleagues at Programa de Po?s-Graduac?a?o
em Ecologia of Universidade Estadual de Campinas, Institut
Experimentelle O? kologie of Universita?t Ulm, and Parque Es-
tadual Intervales, who helped us a lot during field and labo-
ratory work: Aparecido, Ariovaldo Neto, Benedito Oliveira,
Bruno Buzatto, Eliseu, Glauco Machado, Gustavo Requena,
Jakob Fahr, Joa?o Vasconcellos-Neto, Marcelo Gonzaga,
Marcelo Oliveira, Mauro Galetti, Nata?lia Leiner, Pedro Jor-
dano, Regina Alonso, Renato Paiva, and Sandra Silva.
M.A.R.M. was sponsored, at different periods, by CAPES,
FAPESP (02/09286-0), CNPq/DAAD (290088/2004-6), Bat
Conservation International, and Idea Wild.
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