Abstract
Complex animal–plant interactions are present in the Neotropical bat family Phyllostomidae. Many of these interactions are still unknown, mainly due to the paucity of information available on the diet and habits of these species. The wrinkle-faced bat, Centurio senex , has been always considered as an enigmatic species. However, emerging evidence has partially elucidated the feeding ecology of this bat, confirming adaptations to consume hard food items. In addition to this information, here we show evidence of the predation of the seeds of Sideroxylon capiri (Sapotaceae) by C. senex . Bats employed principally deep unilateral bites to process the seeds. Our observations show that endocarp hardness has important implications on the ecological interaction between C. senex and S. capiri , due to the bats inability to puncture seeds with harder endocarps, causing an alternation between predation and dispersal of seeds. Nutritional rewards could be related to the predatory behavior documented. However, additional information is needed to clarify seed predation and seed dispersal patterns that exist between the 2 species.
Complejas interacciones planta-animal existen en la familia de murciélagos neotropicales Phyllostomidae. Muchas de estas interacciones continúan desconocidas, principalmente debido a la escasez de información disponible sobre la dieta y hábitos de estas especies. El murciélago de cara arrugada, Centurio senex , ha sido siempre considerada una especie enigmática. No obstante, evidencia emergente ha dilucidado parcialmente la ecología de alimentación de este murciélago, confirmando adaptaciones para el consumo de alimentos duros. Adicionalmente a esta información, aquí presentamos evidencias de la depredación de semillas de Sideroxylon capiri (Sapotaceae) por parte de C. senex . Los murciélagos emplean principalmente mordiscos profundos unilaterales para procesar las semillas. Nuestras observaciones muestran que la dureza del endocarpio tiene importantes implicaciones sobre la interacción ecológica entre C. senex y S. capiri , debido a la incapacidad de los murciélagos de perforar las semillas con endocarpios más duros, causando una alternancia entre la depredación y la dispersión de las semillas. Recompensas nutricionales podrían estar involucradas en el comportamiento predatorio documentado. No obstante, información adicional es necesaria para esclarecer los patrones de depredación y dispersión de semillas entre estas dos especies.
Phyllostomidae is one of the most diverse families of mammals in the Neotropics, including about 58 genera and at least 204 species ( Solari and Martínez-Arias 2014 ). These bats exhibit outstanding diversification in many aspects of their biology, including roosting ecology and feeding habits. Other examples include the variation in cranial morphology and musculature plus behavioral strategies to modulate bite force associated with functional and behavioral specializations for processing many type of foods ( Dumont 1999 , 2003 ; Santana and Dumont 2009 ; Santana et al. 2012 ). Within the family Phyllostomidae, there is a continuum of variation from species with long, narrow rostrums like Musonycteris harrisoni (nectarivorous species) to those with short, broad rostrums such as species of the genus Artibeus (fruit-eating species— Wetterer et al. 2000 ; Nogueira et al. 2009 ; Santana et al. 2010 ; Dumont et al. 2011 ).
In the order Chiroptera, durophagous species are those that can access hard fruits or hard insects and vertebrates ( Santana et al. 2012 ). Consuming these kinds of foods is related to a number of specific traits like large body size (Pteropodidae) or specialized morphology (i.e., skulls with high bite force production; Phyllostomidae— Aguirre et al. 2003 ; Dumont 2003 ; Freeman and Lemen 2007 ; Santana et al. 2012 ). In the case of hard fruit eaters, it has been proposed recently that this capacity could be advantageous ( Dumont et al. 2009 ), allowing some species to acquire food items not available to other bats. One example is the case of Neotropical bats of the genus Chiroderma ( Nogueira and Peracchi 2003 ; Nogueira et al. 2005 ) that are able to process and digest fig seeds (in addition to the pulp). This case represents a new feeding strategy in bats ( Nogueira and Peracchi 2003 ) and is related to an improvement in the nutrient gain (especially protein and fat) available in the fruits ( Wagner et al. 2015 ).
Here, we present evidence of the seed predation by the wrinkle-faced bat Centurio senex , supporting the hypothesis proposed by Dumont et al. (2009) , that the exceptional cranial design and bite force of this species could reflect the ability to consume hard food items. Additionally, we analyze the ecological interaction between C. senex and the plant Sideroxylon capiri in 2 contrasting bat–plant interactions: seed predation and seed dispersal.
M aterials and M ethods
Study species.
Centurio senex ( Gray 1842 ) is a medium-sized bat (body mass: 17.44±0.53g, n = 6), family Phyllostomidae, subfamily Stenodermatinae ( Figs. 1a and 1b ). Its geographic distribution extends from Mexico through Northern South America to Trinidad and Tobago ( Snow et al. 1980 ). This species is generally uncommon or rare ( LaVal and Rodríguez-Herrera 2002 ; Reid 2009 ), however, it can be abundant and common during limited periods of time in certain localities ( Dumont et al. 2009 ). Information about the diet of Centurio is scarce; the few records suggest that, like other stenodermatines, it is highly frugivorous ( Goodwin and Greenhall 1961 ; Gardner 1977 ; Herrera et al. 1998 ). Field observations have confirmed a frugivorous diet, in the wild, C. senex eats fruits of Spondias radlkoferi (Anacardiaceae— Bonaccorso 1979 ), Drypetes lateriflora (Putranjivaceae— Snow et al. 1980 ), Ficus sp. (Moraceae— Gardner 1977 ), Guettarda foliacea (Rubiaceae— Giannini and Kalko 2004 ), Vitex mollis (Lamiaceae— Ramírez-Pulido and López-Forment 1979 ; Ceballos and Oliva 2005 ), Maclura tinctoria (Moraceae— Dumont et al. 2009 ), and most recently S. capiri (Sapotaceae— Madrid-López et al. 2013 ). Centurio have a peculiar and derived cranial morphology, with an extremely short and wide skull ( Goodwin and Greenhall 1961 ) that generates high bite forces ( Dumont et al. 2009 ) in comparison to other frugivores of similar size ( Madrid-López et al. 2013 ). Recently, some researchers have proposed that these unique characteristics of C. senex are related to the consumption of hard food items when other resources are limited ( Dumont et al. 2009 ). No strong evidence with fruits of native species had supported this hypothesis. However, Madrid-López et al. (2013) reported for the 1st time strong and quantitative evidence of the presence of a hard native fruit ( S. capiri ) in the diet of C. senex , the hardest reported until now. Like other frugivorous bats of the Phyllostomidae family, it has also been proposed that C. senex can act as a seed disperser of some plant species ( Madrid-López et al. 2013 ).
Centurio senex holding (a) and eating (b) a seed of Sideroxylon capiri . Detailed of the predated seeds (c) and remains (d).
Sideroxylon capiri (A.DC.) Pittier is a tropical tree up to 40 m of the family Sapotaceae that occurs in deciduous and semideciduous forests, gallery forests, and evergreen forests within its distribution ( Chavarría et al. 2001 ). It ranges from Mexico to Panamá, Trinidad and Tobago and Granada ( Chavarría et al. 2001 ; García and Di Stefano 2004 ). In Costa Rica, S. capiri is distributed principally in the dry and deciduous forest (northern and central parts— Villalobos-Barrantes et al. 2015 ) and is a threatened and an economically important timber species ( Jiménez 1999 ; Villalobos-Barrantes et al. 2015 ). The fruits of S. capiri have an ellipsoid or globose shape ( Fig. 2a ), the epicarp has a high puncture resistance (2.23±0.28 newtons [N]— Madrid-López et al. 2013 ), and the mesocarp is soft and juicy. The length, width, and mass of these fruits ( n = 20) varies between 30 and 50mm (24.32±0.28mm), 18 and 22mm (20.48±0.21mm), and 3 and 7g (5.34±0.16g), respectively. Each fruit contains a single ovoid-shaped seed ( Figs. 2b and 2c ; García and Di Stefano 2004 ; Jiménez 1999 ; Poveda and Sánchez 1999 ) with the approximate dimensions of 17.81±0.45mm length; 14.08±0.14mm width; and a mass of 1.63±0.08g ( n = 20).
Sideroxylon capiri freshly fruit (a), intact seeds with different levels of endocarp formation (b, c), and cross section of a seed showing the details of the endocarp and endosperm (d). Arrow indicates the side of the seed where the bats start to bite and penetrate.
Study site and data collection.
On January 2014, we studied C. senex at the water hole “Guayacán,” located in Palo Verde National Park, Bagaces, Guanacaste, Costa Rica (10°21′4.48′′N; 85°19′54.7′′W, 22 m). The study site is one of the remnants of the tropical dry forest life zone in Costa Rica ( Holdridge 1967 ) and is characterized by semideciduous forest. Bats were captured over a 1-week period using mist nets settled at the ground level around the water hole. Nets were opened at 18:30h and checked at 10–20min intervals until midnight (00:00h). All C. senex captured during the sampling period were placed in individual cloth holding bags and transported to the Organization for Tropical Studies station approximately 500 m from the netting site; other species were released immediately. We handled all animals in accordance with guidelines approved by the American Society of Mammalogists ( Sikes et al. 2011 ). At the end of field experiments, specimens of bats were collected and deposited at the Museo de Zoología, Universidad de Costa Rica (1 female: UCR #4524 and 1 female: UCR #4526).
Feeding behavior.
Based on recent findings that have confirmed the presence of S. capiri fruits in the diet of C. senex ( Madrid-López et al. 2013 ) and taking advantage of the availability of bats and fruits from fruiting trees of this plant species at the study site, we offered to the animals the fruits of S. capiri in order to film and describe the feeding behavior of this rare species of bat. Surprisingly, after the consumption of the fleshy part of the 1st fruit offered to 1 individual, we noted that the bat also started to feed on the seeds. Since this was an uncommon behavior and a poorly documented event in Chiroptera, we decided to record the bats’ feeding behavior on fruits and seeds of S. capiri (see Supplementary Data ). Individual bats were housed for approximately 1h in a single mesh cage (length: 107.5cm, wide: 57.5cm, and high: 58cm). This was to acclimate the animals to the cage and give them time to process any food recently ingested in the wild. Bats were filmed 2 consecutive nights for approximately 6h per night, using a digital camera with video option (Nikon Coolpix P510) and a low-level white spotlight.
We quantified our data from observations of the bats feeding from 2 parts of the fruits of S. capiri : (1) the fleshy part (see Supplementary Data ) and (2) the seeds (see Supplementary Data ). The fleshy parts were composed of epicarp (outermost layer) and mesocarp (middle layer; Fig. 2a ). The seeds were composed of endocarp (inner layer surrounding the reproductive parts of the seeds) and endosperm (inner and nutritive tissue of the seed; Fig. 2d ). In this sense, information on the processing time of the food and the number of bites and chews used to process a mouthful of food was obtained from each bite sequence documented in the videos. We defined as a bite sequence, each successful trial to eat a mouthful of food, including since the initial and subsequent bites used to remove a portion of fleshy part or seed, the time expended chewing the portion removed, until the moment that bats let drop the wad of dry fiber or initiate the sequence again. Additionally, following previous studies ( Dumont 1999 ; Dumont and O’Neal 2004 ), we classified each biting event in 1 of the 4 descriptive categories available. Categories are related, as described in Dumont (1999) , with the location of bites and the number of teeth involved, and are the following: shallow unilateral bites, shallow bilateral bites, deep unilateral bites, and deep bilateral bites. Shallow bites were those that involved canine and incisor teeth, meanwhile deep bites involved premolar and molar teeth. On the other hand, unilateral bites use either the left or right toothrow and bilateral bites uses both left and right teeth simultaneously ( Dumont 1999 ).
Seed hardness.
We used a mechanical force gauge (Chatillon DPPH100, Berwyn, Pennsylvania) to compare the hardness of the endocarp of several S. capiri seeds. Seed hardness was defined as the force necessary to pierce the endocarp of the seeds with a point of approximately 0.5mm 2 . Seeds were classified into 2 contrasting categories according to the stage of formation of the endocarp: early stages ( Fig. 2b ) and advanced stages ( Fig. 2c ). Hardness always was measured at the side of the seeds used by the bats to penetrate the endocarp (see position of arrow in Fig. 2b ).
Data analysis.
Visual inspections of the 95% confidence intervals from boxplots ( Chambers et al. 1983 ) were used to examine differences between the number of bites and chews employed by bats while processing the fleshy part and the seeds of S. capiri fruits. Additionally, to compare the endocarp hardness of both categories established, we performed a nonparametric analysis (Kruskal–Wallis rank sum test). All numerical results reported in the text are means and SE . Statistical analyses were conducted using R ( R Development Core Team 2015 ).
R esults
We captured 2 adult females C. senex during our sampling period at Palo Verde National Park on January 2014. For both females, we documented 8 independent epicarp–mesocarp consumptions and 8 independent predatory attempts on seeds of S. capiri ( Fig. 1 ). Six of the predatory attempts were successful and 2 failed. We were only able to film 2 events for each part of the fruit, because the other events occurred when we were not filming. Failed predatory attempts were also filmed.
Processing time spent by bats in the fleshy part of the fruits was in average 94.5±3.5min ( n = 2 fruits). For the seeds, bats spent about 14.2±1.7min ( n = 2 seeds). Feeding behavior of C. senex on fruits and seeds of S. capiri was similar to that described by Dumont et al. (2009) for M. tinctoria fruits. Individual bats held the fruit with their forelimbs and thumb claws ( Figs. 1a and 1b ), used numerous bites to remove a mouthful ( Fig. 3a ) and chewed the food several times ( Fig. 3b ) to obtain a bolus of dry fiber which was discarded ( Fig. 1d ).
Median (quartiles and range) of the number of bites (a) and chews (b) used by Centurio senex to remove and process a mouthful of the fleshy part of the fruit and a mouthful of seed of Sideroxylon capiri . Notches represent 95% confidence intervals around the median. Data are based on repeated measurements of the 2 individuals recorded.
Analysis of biting behavior showed that C. senex used principally deep unilateral bites to process both parts of the S. capiri fruits ( Table 1 ). Deep bilateral and shallow bilateral bites showed low frequencies of use during the consumption of fleshy parts; nevertheless, their frequency increased during seed consumption. Finally, shallow unilateral bites were presented in similar frequencies for both parts of the fruit ( Table 1 ).
Biting behavior of a female Centurio senex during epicarp–mesocarp and seed consumption of Sideroxylon capiri . mean ± SE of percentages of bite types.
| Part of the fruit | n | Bite sequences (total) | Shallow bilateral | Shallow unilateral | Deep bilateral | Deep unilateral |
|---|---|---|---|---|---|---|
| Epicarp–Mesocarp | 1 | 60 | 0.36±0.00 | 9.42±0.48 | 0.90±0.00 | 89.31±0.68 |
| Seed | 1 | 58 | 2.53±0.40 | 9.39±1.27 | 12.40±0.68 | 75.66±0.91 |
| Part of the fruit | n | Bite sequences (total) | Shallow bilateral | Shallow unilateral | Deep bilateral | Deep unilateral |
|---|---|---|---|---|---|---|
| Epicarp–Mesocarp | 1 | 60 | 0.36±0.00 | 9.42±0.48 | 0.90±0.00 | 89.31±0.68 |
| Seed | 1 | 58 | 2.53±0.40 | 9.39±1.27 | 12.40±0.68 | 75.66±0.91 |
Biting behavior of a female Centurio senex during epicarp–mesocarp and seed consumption of Sideroxylon capiri . mean ± SE of percentages of bite types.
| Part of the fruit | n | Bite sequences (total) | Shallow bilateral | Shallow unilateral | Deep bilateral | Deep unilateral |
|---|---|---|---|---|---|---|
| Epicarp–Mesocarp | 1 | 60 | 0.36±0.00 | 9.42±0.48 | 0.90±0.00 | 89.31±0.68 |
| Seed | 1 | 58 | 2.53±0.40 | 9.39±1.27 | 12.40±0.68 | 75.66±0.91 |
| Part of the fruit | n | Bite sequences (total) | Shallow bilateral | Shallow unilateral | Deep bilateral | Deep unilateral |
|---|---|---|---|---|---|---|
| Epicarp–Mesocarp | 1 | 60 | 0.36±0.00 | 9.42±0.48 | 0.90±0.00 | 89.31±0.68 |
| Seed | 1 | 58 | 2.53±0.40 | 9.39±1.27 | 12.40±0.68 | 75.66±0.91 |
Visual inspection of the number of bites used by C. senex to remove a mouthful of the 2 parts of the S. capiri fruits ( Fig. 3a ) strongly suggests that, while processing seeds, bats employed significantly more bites than those used to remove a portion of epicarp–mesocarp. Approximately, individuals bit 9.2±0.67 times to remove a piece of the fleshy epicarp–mesocarp, while to take out a portion of the seed, individuals employed more bites (14.29±1.09 bites). On the other hand, when we examined the number of chews used by bats, we found that individuals chewed mouthfuls of epicarp–mesocarp significantly more times than mouthfuls of seeds ( Fig. 3b ). Centurio chew a portion of epicarp–mesocarp 31.65±1.37 times until they drop the wad of dry fiber, in contrast, seed portions are chewed fewer (19.55±1.86) times.
Seed hardness differed between both levels of endocarp formation ( H = 22.01, d.f. = 1, P ≤ 0.05; Fig. 4 ). Puncture endocarps in early stages of formation required a force of approximately 1.40±0.13 N ( n = 15), meanwhile endocarps in advanced stage of formation needed 92.7±1.93 N ( n = 15).
Median (quartiles and range) of the hardness of seeds of Sideroxylon capiri at different levels of endocarp formation. Notches represent 95% confidence intervals around the median.
D iscussion
Our results have demonstrated that the wrinkle-faced bat is able to extract, chew, and swallow S. capiri seeds at Palo Verde National Park, Guanacaste, Costa Rica. This is the 1st time that this kind of predatory event has been documented in the field for this bat species and constitutes the 2nd case of predation of a medium- to large-sized seed by bats since Bonaccorso (1979) documented the use of Anacardium excelsum seeds (Anacardiaceae) by Carollia perspicillata (Phyllostomidae). Although we only captured adult females for our observations, we expected that adult males would show a similar feeding behavior.
In S. capiri seeds, endocarp hardness is variable and is related with fruit ripeness (D. Villalobos-Chaves, Universidad de Costa Rica, pers. comm.). Fruits in an advanced stage of ripeness possess seeds with endocarps that are fully formed and consequently with high levels of hardness. In contrast, seed endocarps in early stages of formation are associated with fruits undergoing the maturing process and usually exhibit lower levels of hardness. Based on our field observations, the stage of formation of the seed when the fruit is picked influences the bat’s capacity to process them. In fact, we only recorded bats eating seeds with endocarps in early stages of formation. These kinds of seeds seem to represent less challenging items to the bats, besides requiring a puncture force below the maximum bite force reported for C. senex (10.9±0.85 N— Dumont et al. 2009 ). Seeds with endocarps in a middle stage of formation are also probably eaten considering Centurio ’s bite force. Additionally, detailed observations of the predatory events confirmed that C. senex always starts to puncture the endocarp on the opposite side of the seed hilum, which based on field observation appeared to be the most vulnerable sections of the unformed seeds (see position of arrow in Fig. 2b ). In contrast with seeds with softer endocarps, seeds with endocarps in advanced stages of formation accounted items of substantial hardness that could not be penetrated by the bats. Nevertheless, despite this hardness barrier, the predatory events on these types of seeds still occur since we documented 2 failed predatory events ( n = 2 seeds). In these observations, bats tried for several seconds to bite the seeds, however, they failed to penetrate them. Bats dropped the seeds after the failed predatory attempts. Finally, another variable possibly related to the unsuccessful attempts of the bats to predate the seeds was the slippery nature of the S. capiri propagules, property that may have caused that some bats, unintentionally, let drop some seeds. Our results have confirmed that, although C. senex possess morphological and behavioral adaptations for durophagy ( Freeman 1988 ; Dumont et al. 2009 ), limitations to process extremely hard tissues always exist.
Biting behavior of C. senex while feeding on S. capiri was similar between the 2 parts analyzed, and as described by Dumont et al. (2009) , bats concentrated on deep unilateral bites to process the food. Deep unilateral bites are associated with an increase in the transmission of pressure (force per unit of area) being applied to the food ( Dumont 1999 ), facilitating the efficiency to breaking down resistant food items ( Lucas and Corlett 1991 ; Strait 1993 , 1997 ). While they ate seeds, most of the time the bats processed the endosperm and endocarp together, with the production of remains of dry fiber after each bite sequence. Nevertheless meticulous observations of the video sequences also confirmed that C. senex sometimes may grasp the opened seeds in their teeth (seeds partially opened) and then using bilateral bites (especially deep bilateral) scrape out the endosperm with the help of the lower incisor and canines. When bats performed this behavior, they usually ingested a small portion of the endosperm that was chewed a very few times and then swallowed without the production of a bolus.
Like other stenodermatines, C. senex employed multiple bites and chews to remove and process, respectively, a mouthful of food ( Dumont et al. 2009 ) either of the epicarp–mesocarp or of the seed of S. capiri . In comparison to the epicarp–mesocarp consumption, we documented an increase in the number of bites and a decrease in the number of chews during seed processing. Fruit characteristics seemed to have influenced our results, because since the fleshy part of S. capiri fruits is juicy (mesocarp), an increase in chewing when eating a piece of a juicy fruit is likely related to the attempt of the bats to extract all of the available nutritive contents of the pulp ( Bonaccorso and Gush 1987 ; Dumont 1999 ). Fewer chewing movements while processing the seeds could be a result of the less juicy attributes of the endocarp -endosperm and the scrapping behavior documented, in which bats bitten small portions of the endosperm than then were swallowed quickly without being chewed. An increase in the number of bites required to remove a mouthful of seed appears to be related to the bat’s effort to access the most nutritious part, the endosperm, a task that usually requires more bites in comparison with the bites needed to remove a juicy portion of the epicarp–mesocarp. Finally, based on the few observation available about this feeding behavior in bats, it seems that mechanical limitations imposed by the seed size strongly influence the strategy adopted by the bats to consume seeds. In our case, large seeds of S. capiri were eaten in small portions obtained from each bite sequence (similar way in which the fleshy part was processed). This predatory behavior significantly differs from that reported for Chiroderma species, where small seeds of Ficus spp. (approximately 1mm) are detached from each fig bite, stocked, and accumulated in the mouth of bats and then masticated ( Nogueira and Peracchi 2003 ).
Seed predatory behaviors in bats have been associated with ecological advantages in terms of acquisition of nutrients ( Nogueira and Peracchi 2003 ). Recently, these concerns have been confirmed in the case of the hairy big-eyed bat, Chiroderma villosum , that chews and digests fig seeds in order to obtain nutritional rewards such as lipids, soluble protein, sugar, and nitrogen ( Wagner et al. 2015 ). In the case of C. senex , we have no information available about nutritional content of S. capiri seeds. Nonetheless, we consider that this feeding behavior could allow bats to increase nutrient intake per fruit and reduce predatory risk and energy invested in foraging flights ( Kalko et al. 1996 ; Nogueira and Peracchi 2003 ; Wagner et al. 2015 ). Through this predatory behavior, C. senex could be accessing a seasonally nutrient-rich food at our study site. In this context, the derived cranial morphology, the ability to produce a very strong bite, and the use of unilateral bites principally ( Dumont et al. 2009 ) represent advantageous adaptations to process hard and presumably nutrient-rich food items like seeds, conferring to C. senex benefits in niche separation from other frugivorous bats ( Madrid-López et al. 2013 ).
At our study area, S. capiri produces huge crops of fruits during a short period of time (especially during the 1st month of dry season— García and Di Stefano 2004 ). This kind of fructification attracts large numbers of opportunistic plant visitors ( Fleming 1982 ) ranging from predators to mutualists. Many mammals, such as deer, peccaries, agoutis, monkeys, coyotes, and bats, have been observed visiting fruiting trees of S. capiri ( Di Stefano and García 2000 ; Chavarría et al. 2001 ; García and Di Stefano 2004 ), nevertheless the role of each species of visitors in the plant’s dispersal and reproduction has not been evaluated. Based on our field observations, at Palo Verde National Park, primate species (i.e., Alouatta palliata and Ateles geoffroyi ) and some bat species (i.e., Uroderma convexum , Dermanura phaeotis , Artibeus jamaicensis , and A. lituratus ) could be considered as genuine seed dispersers of this plant species, meanwhile peccaries (i.e., Pecari tajacu ) and some rodent species (e.g., Dasyprocta punctata and Liomys salvini ) act as seed predators (D. Villalobos-Chaves, Universidad de Costa Rica, pers. comm.). It is expected that due to the large amount of fruits produced by S. capiri trees, some seed predators can be tolerated as long as they are not too common in comparison with legitimate seed dispersers. In the case of C. senex , Madrid-López et al. (2013) proposed that this bat species is a genuine disperser of S. capiri . However, based on our results, individuals of C. senex can act as a seed predator or as a seed disperser depending on the hardness of the seed of each fruit selected by the individuals during foraging (chewable seeds could be consumed, while the hardest seeds could be potentially dispersed without any damage). Since most bat species are not seed predators ( Fleming and Sosa 1994 ; Nogueira and Peracchi 2003 ; Lobova et al. 2009 ), are abundant and highly mobile ( Bernard and Fenton 2003 ; Galindo-González et al. 2009 ), and can disperse large-seeded plants ( Melo et al. 2009 ), they seem to play an important role in the seed dispersal of S. capiri in the dry forest of Costa Rica.
The results of our study support the assumptions of many authors about the extreme morphology, adaptations, and feeding ecology of C. senex , as well as demonstrating that a continuum between antagonism and mutualism exists in some bat–plant interactions ( Howe and Westley 1988 ; Bronstein 2001 ; Wagner et al. 2015 ).
S upporting I nformation
The Supporting Information documents are linked to this manuscript and are available at Journal of Mammalogy online ( Supplementary Data ). The materials consist of data provided by the author that are published to benefit the reader. The posted materials are not copyedited. The contents of all supporting data are the sole responsibility of the authors. Questions or messages regarding errors should be addressed to the author.
Supplementary Data .—Video sequence of a female Centurio senex , feeding of the fleshy part (epicap–mesocarp) of a fruit of Sideroxylon capiri .
Supplementary Data .—Video sequence of a female Centurio senex , feeding of a seed (endocarp–endosperm) of Sideroxylon capiri .
A cknowledgments
We thank all the staff of the Organization for Tropical Studies in the Palo Verde National Park for all the logistical support during the fieldwork. We are also very grateful to R. K. LaVal and M. Fernández Otárola for their constructive comments on early versions of this work. Many thanks to M. Vinicio Murillo Sáenz and the laboratory of Tecnología Poscochecha of the Centro de Investigaciones Agronómicas (CIA), Universidad de Costa Rica, for their assistance and help in the seed hardness determination. Finally, for research permits and other valuables contributions, we thank I. López Nuñez of the Área de Conservación Arenal-Tempisque (ACAT), A. Jiménez Céspedes of the Área de Conservación Guanacaste (ACG), and J. Vargas Sequeira at MINAET-SINAC (Resolution No. 007-2013-SINAC).
L iterature C ited
Author notes
Associate Editor was Patrick Zollner.
