Seasonal environments, episodic density ... - Springer Link

Biodivers Conserv (2012) 21:267–279 DOI 10.1007/s10531-011-0182-1 ORIGINAL PAPER

Seasonal environments, episodic density compensation and dynamics of structure of chiropteran frugivore guilds in Paraguayan Atlantic forest Richard D. Stevens • Heidi N. Amarilla-Stevens

Received: 26 April 2011 / Accepted: 19 October 2011 / Published online: 30 October 2011 Ó Springer Science+Business Media B.V. 2011

Abstract Seasonal environmental variation experienced in the subtropics may contribute substantially to dynamics of community structure. This is particularly true for Neotropical bats because the geographic terminus of most families occurs there. Paraguayan Atlantic forest provides an ideal opportunity to evaluate effects of seasonality on structure of communities; it exhibits notable spatial and seasonal environmental variation and lies near the edge of the geographic distribution of most tropical bat species occurring there. We examined seasonality of bat populations and communities as well as correspondence to seasonal environmental conditions in eastern Paraguay. Most species exhibited lower abundances in the cool than in the warm season. Nonetheless, magnitude of differences was species-specific. Accordingly, highly significant differences between warm and cool seasons existed regarding species composition, evenness and diversity. Moreover, consistent with competition theory, magnitude of positive correlation between morphological distance and abundance and hence degree of structure was greater in the cool than warm season. Across the New World, seasonality assumes various forms (i.e. cold winters, dry and wet seasons) suggesting that better understanding of mechanistic bases of bat community structure in general may come from seasonal perspectives. Keywords Bat assemblage Bat community Competition Frugivory Null model Seasonality

Introduction In both the southern and northern hemispheres, taxa of tropical affinity extend into the subtropics, at least on a seasonal basis. Subtropical and temperate environs may provide relatively harsh climates for tropical taxa (Wiens and Donoghue 2004), at least during

R. D. Stevens (&) H. N. Amarilla-Stevens Department of Biological Sciences, Louisiana State University, Baton Rouge, LA 70803, USA e-mail: [email protected]

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Biodivers Conserv (2012) 21:267–279

certain portions of the year. In particular, seasonality of temperature and solar radiation becomes pronounced at higher latitudes which translates into seasonal variation in primary productivity and ultimately changes in food resources available for consumers (MacArthur 1972). Such seasonal environments may induce changes in abundance as well as spatial and temporal distribution of taxa. For example, many bat species migrate to more favorable environments (Fleming and Eby 2003) or utilize torpor to overcome colder temperatures or reductions in resource levels that are associated with seasonality (Speakman and Thomas 2003). New World bats are primarily of tropical affinity. Eight of nine families have a primarily Neotropical distribution and a supposed tropical origin (Koopman 1994; Stevens 2004; Teeling et al. 2005; Lim 2009). Nonetheless, the distribution of some species in most of these Neotropical families extends at least into the subtropics and even to relatively high latitudes in the temperate zone. For example, of the 134 species of Phyllostomidae that occur in South America, 37 have distributions that extend beyond 23.5° latitude into the subtropics (Gardner 2007). Toward the edge of their distribution at higher latitudes, many of these tropical taxa likely experience environmental conditions far from optimum. Accordingly, seasonal environmental variability may be even more taxing to the persistence of tropical species within subtropical communities and seasonality alone may cause substantive differences in the composition and structure of communities between seasons. In systems where seasonality represents an important component of environmental variation, seasonal perspectives may provide added insight into the tight linkage between pattern and process at the community level. The country of Paraguay has a central position on the continent of South America, in particular at the intersection of the tropics and subtropics as well as a number of biomes such as Gran Chaco, Cerrado, Pantanal and Atlantic forest. Such heterogeneity can create very dynamic bat assemblages (Fahr and Kalko 2011) and those in this region are quite variable (Willig et al. 2000), responding to aspects of land use (Gorresen and Willlig 2004), as well as environmental (Stevens et al. 2007), spatial (Presley et al. 2009) and biogeographic (Lopez-Gonzalez 2004) processes. Paraguayan Atlantic forest offers an ideal setting to examine effects of seasonal subtropical environments on structure of bat communities comprising tropical bats. Much of Atlantic forest is buffered from climatic extremes due to its disproportionately coastal distribution (Oliveira-Filho and Fontes 2000). Nonetheless, continental effects due to the interior position of Paraguay within South America produce considerable temperature seasonality on a yearly basis (Prohaska 1976). The cool season is markedly colder than the warm season with typically a few days a year of frost and freezing temperatures (Sanchez 1973; Hill et al. 1994; Hill and Hurtado 1996). Much of the Atlantic forest is semi-deciduous, and many tree species exhibit strong seasonal phenological patterns and even drop their leaves during the cool season (Morellato et al. 1989; Morellato et al. 2000; Marques et al. 2004). This is especially true in interior Atlantic forest of Paraguay (Stutz de Ortega 1986). Whether groups of consumers exhibit similar seasonal patterns as does the flora in interior Atlantic Forest remains unclear. Herein, we examine seasonality of bat communities from Atlantic forest of Paraguay from two distinct perspectives. First, we examine seasonal differences in abundance, species composition and diversity of communities. If bats are differentially responding to seasonal climates, then aspects of community structure should exhibit seasonality as well. Thus, we examined seasonal differences in the degree to which models of competitively induced deterministic structure characterize these communities.

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Methods Study sites Study sites were located in two forest reserves (Reserva Natural del Bosque Mbaracayu´ and Yaguarete´ forests). Both occur in the Alto Parana Atlantic forest ecoregion (NT0150 ecoregion delineation of Olson et al. 2001). Climate is seasonal and subtropical with distinct warm (October–April) and cool (May–September) seasons that are characterized by marked temperature differences (Hill and Hurtado 1996; Hill et al. 1994). Low temperatures of -3°C are not uncommon in winter with several days of hard frost annually. Annual precipitation ranges between 1,500 and 1,700 mm from west to east (Hayes 1995), and is characterized by considerable inter-annual variation (Hill and Hurtado 1996). More detailed descriptions are in Stevens et al. (2004). Reserva Natural del Bosque Mbaracayu´ is located approximately 30 km east of Ygatimı´ in the Department of Canindeyu´ (24°07.690 S, 55°30.340 W) at an elevation of 250 m (Willig et al. 2000). Mbaracayu´ comprises approximately 65,000 ha and is bisected by the Jejui-mi River. Although the reserve includes mesophytic broadleaf tall, medium, and short forests, tall forest is most common. The five most common plant species at this site were Sorocea bonblandii, Campomanesia xanthocarpa, Chrysophyllum gonocarpum, Myrciaria bapoleti and Balfourodendron reidelianum (Keel et al. 1993). Yaguarete´ forests is located approximately 40 km east of Santa Rosa de Lima in the Department of San Pedro (23°48.500 S, 56°07.680 W), at an elevation of approximately 250 m (Willig et al. 2000). This private reserve was established to operate an economically viable but environmentally sound and sustainable timber management and wildlife conservation program. Ostensibly, harvest of trees was light; only a portion of the property was logged selectively on a 40-year rotation scheme (Yaguarete´ Forests LDC 1996). Yaguarete´ Forests occupies approximately 16,000 ha. This site is embedded in a transition zone between the Amambay and Central Paraguay phytogeographic regions defined by Keel et al. (1993), and the property is characterized by mesic tree species of low stature, although some tall–dry forest habitats dominated by peroba (Aspidosperma polyneuron) occur as well (Yaguarete´ Forests LDC 1996). Grassland-savanna habitats (campos cerrados) interdigitate with these forested habitats, enhancing spatial heterogeneity. Accordingly, 66% of the site was forested and 34% comprised natural grassland and riparian habitats. The five most common plant species in rank abundance in the overstory were M. bapoleti, C. gonocarpum, Coutarea hexandra, Sweetia elegans, and Dendropanex cuneatus, whereas the five most common species in the understory were Coussarea platyphylla, S. bondplandii, Fagara naranjillo, C. hexandra, and S. elegans (Jin and Oren 1997). Bats were collected by mist-netting from January 1997 through February 1998. In total 36,815 and 42,047 net hours of effort were employed at Yaguarete´ and Mbaracayu´, respectively. Between five and 10 locations at each of the two study sites were visited monthly and sampled for one night each. All habitats were sampled proportionally to their extent. In general, 10 standard mist nets (3 by 12 m, 1.5 in mesh) were erected on roads, trails and in open areas along edges of emergent vegetation each night. All nets were monitored from just prior to dusk for at least 4 h, and frequently (25% of nights) until dawn the next morning. Nets were checked hourly; bats were sacrificed and prepared as standard museum specimens or released after identification. Herein, we analyze seasonal differences in the most species rich group of New World leaf-nosed bats (Phyllostomidae), frugivores, that are represented by the subfamilies Carolliinae and Stenodermatinae. In addition, Glossophaga soricina consumed much fruit at both sites (28 of 33 individuals possessed

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either seeds or fruit pulp in their stomachs, Stevens ‘‘personal observation’’). This has been noted in other parts of Atlantic forest (Pedro and Taddei 2002) and for this reason this species was treated as a frugivore in these analyses. We used average minimum temperature each month to characterize seasonality. Data on average minimum temperature were obtained from http://www.climate-charts.com on 16 September 2010. Data were generated for the World Meteorological Organization (WMO), processed by the National Climatic Data Center (NCDC), and obtained from the National Oceanic and Atmospheric Administration (NOAA) from NOAA Global Climate Normals 1961–1990. To estimate seasonality of the region we compiled data from three different NOAA weather stations: (1) Asuncion (Station PY86218, 25°150 S, 57°310 W), (2) ciudad del Este (PY86248, 25°270 S, 54°360 W), (3) concepcion (PY86134, 23°260 S, 57°260 W). We used UPGMA to identify natural clusters of months based on minimum temperature that could be used to delineate warm season and cold season samples. UPGMA was conducted in SPSS (V.10). We expected that species-specific changes in abundance would characterize a seasonal difference in species composition. We conducted a Chi-square test (Sokal and Rohlf 1995) of independence to evaluate the hypothesis that species composition (i.e. number of individuals per species) was independent of season or in other words not statistically different between warm and cool seasons. Analyses were conducted for each site separately. Marginal totals were treated as unconstrained. For Mbaracayu´ data, G. soricina and Vampyressa pusilla and for Yaguarete´ data for G. soricina, V. pusilla and Chiroderma doriae were combined so as to increase the magnitude of expected values past 5. We predicted that diversity and evenness would decrease from the warm to the cool season because those species that can best tolerate the seasonal difference would disproportionately be represented in the cool season. To evaluate significant differences in species diversity and evenness at each site between warm and cool season samples we used the randomization procedures of Solow (1993). We characterized diversity and evenness with the appropriate Shannon index (Pielou 1975). Then we determined the difference in these metrics between warm and cool samples; this represented the test statistic for the analysis. We then compared this observed difference to a distribution of 10,000 random differences to evaluate significance. To generate a random difference, we joined all individuals from both warm and cool samples into the same pool. Then we randomly allocated individuals to warm and cool samples until the total for each sample equaled the original total of the empirical data. We then determined the number of individuals of each species in each sample, calculated a diversity or evenness index and determined the random difference between warm and cool seasons. Once this was conducted 10,000 times, we determined the position of the observed difference relative to the distribution of random differences to obtain a two-tailed P value expressing how non random was the observed difference. We also examined seasonal differences in the degree of deterministic community structure by examining differences in how nonrandom was community composition based on a null model. In particular, we examined differences in the degree of density compensation (Stevens and Willig 2000a, b; Tello et al. 2008) between warm and cool seasons at each site. We predicted that if resources become more limiting in the cool season then community structure would be more nonrandom than in the warm season. Within bat communities, morphology, in particular attributes that reflect size, is a powerful predictor of resource use (Findley 1973; Findley 1976; Stevens and Willig 1999; Dumont 2004). Competition theory predicts that when morphology reflects resource use, species that are morphologically similar will experience greater competitive interaction than those that are

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different. Density compensation is a change in population density in response to competition with other species. Species that are similar to others in the community will experience greater competitive effects and thus lower abundance whereas species that are different will experience less competitive effects and higher abundance. Density compensation can be identified by a correlation between morphological distance and abundance that is more positive than that predicted by a null model. We conducted the null model described in Stevens and Willig (2000a, b) to estimate significant density compensation. Size is an important trophic characteristic of frugivorous bats (Bonaccorso 1978; Stevens and Willig 1999) and we characterized distances among species based on differences in forearm length. First we calculated the Spearman rank-correlation (Sokal and Rohlf 1995) between the distance of a species to all others based on forearm length and its abundance. This correlation coefficient represented the test statistic for the analysis. We then permuted abundances among species. Next we calculated the spearman rank-correlation coefficient for the randomized data. We repeated this 1,000 times to yield a distribution of randomized correlation coefficients. We then determined a P value describing how non-random the original correlation was (measured by the test statistic) by determining what proportion of the distribution of random coefficients was larger than the test statistic. P values based on such a null model are only approximate because they subsample only a certain number of all possible random combinations (often an infinite number). Thus, there is variation in P values from simulation to simulation that reflects random variation based on subsampling (Koehler et al. 2009). We used this variation to examine significant differences between warm and cool season samples in the degree of density compensation. We repeated the density compensation null model 1,000 times for the warm season and 1,000 times for cool season and created two distributions of P values. If warm and cool season samples simply reflect random variates of the same underlying distribution of P values then they should form a single distribution when simulations are conducted a large number of times. In contrast, if the P value for the cool season comes from a different distribution than the P value for the warm season, when simulations are conducted a large number of times the two different seasons should form two different distributions. Distributions were compared and if they did not overlap by more than 5% we concluded a significant difference between the warm and cool seasons in degree of density compensation.

Results A clear seasonal pattern of minimum temperature existed in Paraguayan Atlantic forest. Cluster analysis identified the largest difference between warm months of October through April and cool months of May through September (Fig. 1). Warm and cool seasons represented two distinct clusters. Bats exhibited strong seasonal differences as well. At both sites, when species were absent they were always absent from the cool season sample (Fig. 2). Artibeus planirostris and G. soricina were absent from Yaguarete´ and V. pusilla was absent from both sites during the cool season. The latter two species were relatively rare and it is difficult to determine whether they truly were absent in the winter time or just reduced to such a low density that they were virtually undetectable. Total numbers of captures were much greater during the warm than cool season (Fig. 2). More bats were caught at Mbaracayu´ than Yaguarete´, but this was primarily due to a difference in numbers caught during the warm season. Species composition was highly significantly different

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between seasons at each site (Mbaracayu´: V2 = 37.48, P = 0.0006, df = 6; Yaguarete´: X2 = 258.97, P \ 0.0001, df = 7). Single degree of freedom contrasts indicated that changes in abundance of A. lituratus, Sturnira lilium and Platyrrhinus lineatus were the primary contributors to this difference at Mbaracayu´ and these species plus Pygoderma bilobiatum were most different between seasons at Yaguarete´. Significant seasonal differences also exist in terms of diversity and evenness (Table 1). At both sites, diversity and evenness were higher during the cool season than during the warm season. Degree of density compensation was typically weak. For Mbaracayu´ there was no correlation between morphological distance and abundance for the cool season (r = 0.00, Pave = 0.518) and negative but nonsignificant correlation for the warm season (r = -0.144, Pave = 0.642). In contrast, at Yaguarete´, this correlation was positive and significant in the cool season (r = 0.643, Pave = 0.069) and barely positive for the warm season (r = 0.006, Pave = 0.496). Seasonal differences at both sites in the degree of density compensation were highly significant (Fig. 3). At both sites, the P value describing degree of nonrandomness of the relationship between morphology and abundance was significantly lower in the cool season than in the warm season. This was especially true at Yaguarete´, where the correlation was positive and significant in the cool season and barely positive and nonsignificant in the warm season.

Fig. 1 Monthly variation in average minimum temperature for three meteorological stations in eastern Paraguay (above). Cluster analysis identified two main groups of months based on minimum temperature (below). These groups herein are considered to represent the warm and cool season

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Fig. 2 Histograms depicting differences between warm (black) and cool (grey) seasons in terms of abundance of bats at Mbaracayu´ and Yaguarete´. Asterisks indicate statistically significant differences between seasons of individual bat species based on a single degree of freedom Chi-square test. Figure to the left illustrates seasonal differences in numbers of individuals captured across all species per net hour at both sites. In figures to the right, above row indicates differences in the absolute number of individuals captured per species whereas figures below indicate differences based on relative abundance

Table 1 Seasonal differences in diversity and evenness at Mbaracayu´ and Yaguarete´ in Paraguayan Atlantic forest Site

Measure

Warm season

Cool season

Difference

Mbaracayu´

Diversity

1.13

1.26

0.13

Evenness

0.55

0.65

0.10

0.006

Diversity

1.06

1.23

0.17

\0.001

Evenness

0.46

0.63

0.17

\0.001

Yaguarete´

P value 0.004

Discussion Climate and frugivorous bats exhibit considerable seasonality in Paraguayan Atlantic forest. Relative to warm summers, cooler winters are associated with fewer bats, more even frugivore ensembles, and greater structure that is more consistent with predictions from competition theory. Perhaps as interesting are the species specific differences that underlie the overall seasonal differences at the community level. Not all species contributed equally to the overall seasonal difference. A. lituratus exhibited the largest change, decreasing from the warm to the cool season. Carollia persipicillata and A. fimbriatus exhibited no significant change related to season. Moreover, P. bilabiatum and S. lilium increased in abundance while others decreased, at least at Yaguarete´.

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Fig. 3 Histograms depicting differences between warm (black) and cool (grey) seasons in terms of degree of structure of the frugivore guild at Mbaracayu´ and Yaguarete´. Height of each bar in each histogram corresponds to the number of P values generated from the 1,000 iterations of the null model conducted on each seasons data. Each histogram represent the distribution of P values for a particular season and site combination. If warm and cool season P values come from the same distribution then they should form one single distribution. If P values for both seasons are statistically different then cool and warm seasons should form two distributions. Lack of overlap between histograms indicates that they are statistically different

Seasonal bat communities from interior Atlantic forest Although decreases in temperature and productivity may be the ultimate cause of seasonality of bats in this system (Mello et al. 2008), much of the species-specific seasonal variation may be due to proximal fluctuations in resource availability (Ortencio Filho et al. 2010). For example, A. lituratus, a specialist of Ficus and Cecropia spp. (Muller and dos Reis 1992; Sipinski and dos Reis 1995; Mikich 2002; Passos et al. 2003; Aguiar and Marinho-Filho 2007) exhibited the largest seasonal difference. Frugivores that specialize on fruits that are more variable seasonally may fluctuate more than species that rely on a constant resource (Aguirre et al. 2003; Mello 2009). Thus, which of the two main fruiting syndromes (‘big bang’ or ‘‘cornucopia’’, Gentry 1974) for tropical fruit producing plants is

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relied upon as the primary resource by a particular species may determine that bat species seasonal dynamics and ultimately its dominance within a particular season. Indeed, Ficus and Cecropia spp. undergo ‘‘big bang’’ fruit production in which a particular plant has one large fruiting bout a year and may contribute to the strong seasonality of A. lituratus in eastern Paraguay as well as in other parts of Atlantic forest (Pedro and Taddei 2002; Passos et al. 2003; Aguiar and Marinho-Filho 2004; Ortencio Filho et al. 2010). Moreover, species such as C. perspicillata, S. lilium and P. bilabiatum (dietary information on this taxon is very scarce but it has been reported to consume steady-state fruits that continually produce fruit throughout the year such as Solanum granuloso-leprosum) that either exhibit no seasonal change or actually increase in relative abundance tend to consume ‘‘cornucopia’’ type resources such as Solanum and Piper spp. that produce fruit throughout the year (Pedro and Taddei 2002; Passos et al. 2003; Aguiar and Marinho-Filho 2004). An additional manifestation of these seasonal dynamics is change in the diversity and evenness of communities as well as in degree of deterministic structure of the trophic guild. The unexpected increase in diversity and evenness is due to the lack of dominance of A. lituratus in the cool season. Indeed, the reciprocal change in relative abundance of A. lituratus, S. lilium and P. bilabiatum also caused the correlation between abundance and morphology to be close to zero in the warm season when resources are most abundant to large and significantly positive in the cool season when resources are the least, at least at Yaguarete´. Indeed, much of this change may reflect the inability of A. lituratus to compete with other species that specialize on ‘‘cornucopia’’ type fruits. Despite the wealth of information on resource utilization by bats in other parts of Atlantic forest (Muller and dos Reis 1992; Sipinski and dos Reis 1995; Mikich 2002; Passos et al. 2003; Aguiar and Marinho-Filho 2007), to date no such data are available at these two sites. As such, the aforementioned ideas regarding effects of resource availability on bat population and community ecology in Atlantic forest of Paraguay represent working hypotheses and not causal explanations per se. Indeed, future research should more robustly examine the proximal reasons for seasonal bat dynamics in this system by simultaneously examining seasonality of environments, bats, and the availability of resources these important consumers utilize. What happens to bats during the cool season? Another important remaining question is what happens to individuals as the abundance of these species, in particular A. lituratus decreases? At least three possibilities exist: (a) They reflect deaths of individuals due to cold temperatures. (b) They reflect two subsets of the population, one that is transient and one that remains throughout the year. (c) They reflect decreased activity in the cool season of the same number of individuals in the population. The first possibility is doubtful. For example, at both sites in general the numbers of bats decreased by at least 50%. In particular, A. lituratus decreased almost 30% at Yaguarete´. It is doubtful that populations of long-lived organisms such as bats could sustain such an annual decrease due to mortality. Seasonal movements, at least of part of the population, are a possibility that warrants further investigation. Indeed, bats often exhibit local movements to track the phenology, especially fruiting, of resources (Handley et al. 1991; Estrada and Coates-Estrada 2002; Loayza and Loiselle 2008). In addition, regional movements (those of moderate distance

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between 100 and 500 km, Fleming and Eby 2003) are known for some phyllostomids but are poorly understood in tropical and subtropical systems (Fleming 1988; Newton et al. 2003). Given that both of these sites occur just outside the tropics, a regional movement of this magnitude may allow bats to enter areas that are less seasonal in terms of temperatures or resources. Nonetheless many of the taxa found in these Paraguayan communities have geographic distributions that extend farther south and into Argentina (Barquez et al. 1999). Seasonality of species composition of bats likely characterizes these communities as well (Crespo 1982). Thus, for members of these more southerly communities to move to areas with less seasonal resource distributions they would need to undergo more continental level long-distance migrations ([1,000 km, Fleming and Eby 2003). Such migrations do occur in some members of the Phyllostomidae (Ceballos et al. 1997) but are poorly understood, in particular for tropical taxa. Indeed, a simple indication would be greater genetic diversity in the warm season population (over and beyond that expected by the increase in abundance) than the cool season population. Finally, the last possibility is that of reduced movements or the use of torpor or hibernation. Simply reducing distance of movement to half could induce a perceived decrease in abundance. Similarly, if bats foraged less frequently this also could induce a change. Studier and Wilson (1970) reported that wild-caught A. jamaicensis underwent torpor at cooler temperatures. Moroever, subsequent research suggests that a number of species such as C. perspicillata and G. soricina, and Sturnira spp. undergo torpor under cold temperature and poor body condition (Audet and Thomas 1997; Soriano et al. 2002; Kelm and can Helversen 2007; Mello et al. 2008). We often caught bats in furled-closed nets left overnight. Often in the cool season bats in nets would be torpid. Phyllostomids (McNab 1976; Ceballos et al. 1997; Galindo et al. 2004) and A. lituratus (Stevens ‘‘personal observation’’) in particular, accumulate a large pad of fat in the interscapular region prior to seasons of low resource availability. Thus, in these seasonal environments phyllostomids may readily use torpor during the cool season. Implications of seasonal bat communities Seasonal differences also have implications to our understanding of bat community structure in general. In particular, studies examining the degree to which biotic interactions determine structure have focused on data that resulted from intensive, year-long or longer sampling regimes (Stevens and Willig 1999, 2000a). Such an approach combines data when biotic interactions may be potentially variable between seasons. Seasonal perspectives on bat community structure are rare (Moya et al. 2008; Mello 2009; Klingbeil and Willig 2010; Sperr et al. 2011), yet have demonstrated important biological distinctions within the year. Seasonal resource availability may be general and determined by either temperature or by seasonal precipitation regimes that occur across much of the tropics. To this end, deterministic structure may be fleeting in many situations and this may explain the paucity of support for this hypothesis in prior analyses that combine data across the entire year (Stevens and Willig 1999, 2000b; Kingston et al. 2000; Bloch et al. 2011, but also see Delaval et al. 2005; Schoeman and Jacobs 2008 for counter examples). Moreover, attempts to understand how biotic interactions structure bat communities might be improved by focusing on such seasonality and comparing degrees of structure during more productive and less productive times of the year. Acknowledgments This research was supported by grants from the American Society of Mammalogists, Grants in Aid of Research, as well as by the office of the Vice-President for Research and Graduate Studies,

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the office of Research Services, the Graduate School, Department of Biological Sciences, and the Association of Biologists at Texas Tech University. In Paraguay, the Ministe´rio de Agricultura y Ganadarıá, through the Direccion de Parques Nacionales y Vida Silvestre, the Museo Nacional de Historia Natural del Paraguay and in particular the Convention on International Trade in Endangered Species of Wild Fauna and Flora office, provided substantial logistical support. Specifically, I. G. de Fox, A. L. Aquino and O. Romero were quite helpful regarding vehicles and general logistical considerations. P. Mueller of Yaguarete´ Forests and A. Yanoski from the Fundacioń Moises Bertoni provided access to field sites as well as much logistical assistance. The Universidad Cato´lica de Nuestra Senõra de la Asuncioń provided storage and laboratory facilities. R. Baker and The Museum, Texas Tech University provided support. R. Farinã, M. Mieres, L. Gimeńez-Raidań, J. Pintos, and G. Terol provided field assistance. A. L. Aquino, S. Presley, C. Lo´pezGonza´les, R. Owen, and M. Gorresen provided invaluable insights and assistance in all stages of this project. In part, fieldwork was supported by grants (DEB-9400926, DEB 9741543, DEB 9741134) from the National Science Foundation to R. D. Owen and M. R. Willig. RDS was supported by the National Science Foundation (DEB-0535939, DEB-1020890) and the Louisiana Board of Regents (LEQSF-2006-09, NSF/LEQSF (2006)-PFUND-46, NSF (2009)-PFUND-139) during the later stages of manuscript production.

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