BlOTROPlCA 32(1): 174-184 2000

A Comparison of the Phyllostomid Assemblages in Undisturbed Neotropical Forest and in Forest Fragments of a Slash-and-Burn Farming Mosaic in Peten, Guatemala’

Mark D. Schulze*, Nathaniel E. Seavy3,and David F. Whitacre The Peregrine Fund, 566 West Flying Hawk Lane, Boise, Idaho 83709, U.S.A.

ABSTRACT Using mist nets, we compared phyllostomid bat ensembles of continuous mature forest in Tikal National Park, Guatemala, and of forest fragments in the nearby farming landscape. Of 20 species captured, 13 were shared between treatments, 4 were unique to continuous forest, and 3 were unique to forest fragments. Dominance-diversity curves were similar for the two treatments except that lilium comprised 43 percent of captures in the forest fragments, resulting in greater dominance there. Capture rates (and presumably relative abundance) differed significantly between continuous forest and forest fragments, both in terms of species and feeding guilds. Sturnia lilium and Dermanura sp. were captured significantly more often in forest fragments than in continuous forest, whereas jamaicensis, A. Izturatus, and Centurio senex were taken significantly more often in continuous forest. Large frugivores accounted for a higher proportion of total captures in conrinuous forest than in forest fragments, whereas small frugivores showed the opposite pattern. By their abundances, perspicilkzta and S. lilium are indicators of forest disturbance. The relative abundances of large frugivores, which feed on large fruits of mature forest trees, and small frugivores, which fced on small-fruited plants occurring in early succession, are an indicator of forest disturbance. Other groups, such as large insect- and vertebrate-eating , because of their low capture rates, are impractical as indicators for rapid assessment of forest disturbance based on mist netting, but may prove especially vulnerable to forest fragmentation.

RESUMEN Usando redes de neblina, comparamos las comunidades de murcidagos phyllost6midos de bosque maduro continuo en Parque Nacional Tikal, Guatemala, y en bosques remanentes en el paisaje agricola en la vecindad. De 20 especies capturadas, 13 eran en comGn en 10s dos hhbitat, 4 eran irnicas a1 bosque continuo, ,y 3 a 10s bosques remanentes. Curvas de dominancia-diversidad eran similar en las dos muestras falto que Sturnira blzum contribuy6 43 percent de las capturas en 10s fragmentos de bosque, resultando en mayor dominancia alli. Tasas de captura (y se presuma la ahundaticia relativa) eran significativamente diferente en bosque continuo y en bosques remanentes, tanto en numero de especies que en gremios tr6ficos. S. lilium y Dermanura sp. fueron capturadas m6s comhnmente en 10s astilleros qiic en bosque continuo, mientras Artibeus jamaicenris, A. lituratus, y Centurio senex se capturaron con mayor frecuencia cn bosque continuo que en 10s fragmentos. Frugivoros mayores tenian tasas de captura significativamente mayores en bosque continuo que cn 10s astilleros, mientras 10s frugivoros menores demostraron el rev& Por su abundancia, Carollia perspicillata y S. lilium sirven como indicadores de disturbio del bosque. Otro indicador Gtil del disturbio del bosque parece ser la abundancia relativa de 10s frugivoros mayores que se alimentan de 10s frutos grandes de especies de drboles caracteristicos de bosque maduro, y de 10s frugivoros menores que se alimentan de las plantas con frutas pcqueiias que ocurren en las etapas iniciales de la sucesi6n. Aunque son dificiles para estudiar, las especies de murcit- lagos “carnivoros” puedan ser especialmente vulnerables a la fragmentaci6n del bosque.

Key words: bat; Cbiroptera; community composition; disturbance; forest; fragmentation; habitat; indicator species; Neo- tropical; pbyllostomid.

IN MANY PARTS OF CEN’rIL4L AMERICA, SHIFTING CUL- farmers make intrusions into the fringes of remain- TIVATION is a major land use and a dominant agent ing large tracts of forest, the landscape becomes of deforestation. Conversion of forest to farmland increasingly fragmented and eventually is converted generally occurs in piecemeal fashion; as colonizing to a mosaic of small crop (usually corn) fields, fal- low fields in various stages of succession, and rem- ’ Received 30 December 1997; revision accepted 27 Oc- nant patches of mature forest. With time, these tober 1998. forest fragments become increasingly degraded by Current address: Department of Biology, Pennsylvania various human uses, fire, increased treefall rates, State University, University Park, Pennsylvania 16802, U.S.A. and invasion by disturbance-adapted plants (cj Current address: 17142 Lemolo Shore Drive N.E., Laurance 1997, Viana et al. 1997). Despite such I’oulsbo, Washington 98370, U.S.A. degradation, these patches are often the only refu-

174 Bats in Forest Fragments 175 gia within the agricultural mosaic for spe- Forest fragments may play a critical role in bi- cies dependent on mature forest. For example, otic conservation of tropical agricultural landscapes Whitacre et al. (1995) found that 47 percent of the (e.g., Gascon 1993, Schelhas & Greenberg 1996, forest bird species sampled in PetCn, Guatemala, Turner & Corlett 1996, Laurance & Bierregaard were associated with mature forest, and were not 1997). Documenting patterns of relative species found in substantial numbers in even the oldest abundance in continuous forest and in the farming second-growth vegetation (30 yr) of the area. Sim- landscape is a first step to understanding the con- ilarly, Brosset et al. (1996) found that phyllostomid servation potential of this dynamic and fragmented bat species richness declined in deforested areas of landscape. Despite great interest in the potential French Guiana and that many forest-dwelling bat use of bats as indicators for ecological integrity of species were less abundant in, or absent from, de- forest, few studies have focused on the use of forest forested areas. fragments by Neotropical bat species. The one Studies of the effects of habitat fragmentation study which we are aware of that has focused on on bird, insect, and assemblages have bats in Neotropical forest fragments (Estrada et al. shown that some groups of species are highly sen- 1993) did not compare directly the communities sitive to fragmentation and patch size (Bierregaard of bats using forest fragments to those in contin- & Lovejoy 1989, Klein 1989, Bierregaard et al. uous forest. Previous researchers (Fenton et al. 1992, Bierregaard & Stouffer 1997, Lynam 1997). 1992, Wilson et al. 1996) have found that phyl- Fragmentation-sensitive species are typically habitat lostomids are good indicators of habitat alteration specialists with an aversion to crossing habitat (primarily deforestation), as this family contains a boundaries (Quintela 1985; Klein 1989; Laurance high diversity of species and feeding guilds and in- 1990, 1994). Some forest vertebrates even avoid cludes a large number of forest-associated species. clearings as small as 20 m (Bierregaard & Lovejoy The degree of habitat specificity and the impact of 1988, Burnett 1992, Goosem 1997). The effective human disturbance on patterns of habitat use are isolation of forest remnants, and thereby the im- not known for most bat species (Fenton 1997). pact of fragmentation on animal populations, de- Our objective was to compare the phyllostomid pends heavily on the nature of the matrix habitat community in a large area of continuous, mature (Lynam 1997, Malcolm 1997, Tocher et al. 1997). tropical forest inside Tikal National Park to that of Many , including bat species (Fenton fragmented forest within an agricultural mosaic ad- 1993, readily cross open areas, and forest remnants jacent to the park. may not represent islands for these species (Lynam 1997, Tocher et al. 1997); however, frequent use MATERIALS AND METHODS of forest trails by phyllostomid bats traveling to foraging sites (Tuttle 1976) and reduced activity of STUDYAm.--This study was conducted in and ad- some species under bright moonlit conditions may jacent to Tikal National Park in the lowlands of indicate a preference for the cover of forest canopy. Guatemala’s Pettn Department. The area is classi- Habitat degradation associated with patch size fied as subtropical moist (Holdridge et al. 1971) or and intensity of forest use by humans may reduce tropical semi-deciduous forest (Pennington & Sa- significantly (for some species) the utility of forest rukhan 1968), receiving an average of 1350 mm patches within the slash-and-burn mosaic (Laur- of rainfall annually and typically experiencing a ance 1997, Lynam 1997). Degradation of forest pronounced dry season between February and fragments-changes in forest structure and tree June. Peak flowering occurs in the dry season, with species composition-tends to vary inversely with peak fruit availability at the end of the dry and fragment size, an increasing percentage of the forest beginning of the rainy season (Ramirez 1996; M. patch being affected by edge effects in smaller Vhsquez, pers. comm.; M. Schulze, pers. obs.; see patches (Lovejoy et al. 1986, Bierregaard et al. Frankie et al. 1974 and Heideman 1989 for other 1992). Moreover, in our study area, smaller forest Neotropical sites). fragments often occur in areas where agricultural Tikal National Park is a large area (576 km2) activities have a longer history and higher intensity; of relatively undisturbed forest, contiguous with hence size and edge effects may be confounded by much larger areas of similarly pristine or little-al- time and distance of isolation, and nature of the tered forest within the Maya Biosphere Reserve to surrounding matrix. Such covariation makes it dif- the east, west, and north. Throughout this large ficult to identify causal agents responsible for spe- forested area (>1 million ha), localized selective cies’ occurrence patterns. logging of mahogany (Swietenia macrophylla) and 176 Schulze, Seavy, and Whitacre some Spanish cedar (Cedrela mexicana) has been has been found to be the most effective rapid sam- the most significant habitat modification. Because pling technique for phyllostomid bats (Kunz & densities of target trees are low, direct logging im- Kurta 1988, Fenton etal. 1992). Capture rates pre- pacts are light, and the logged forest is essentially sumably correlate positively, although not necessar- indistinguishable from unlogged forest except for ily closely, with the number of bats of a given spe- lower densities of large mahoganies and the pres- cies moving through or foraging at the netted sites. ence of occasional stumps and old logging roads. We did not document roosting or movement pat- The agricultural frontier abuts the southern terns, and some phyllostomids forage widely and boundary of the park, where three small commu- far from roost sites (Morrison 1978, Bonaccorso nities are located in a north-south line along the 1979, Fleming & Heithaus 1986, Fleming 1988, only paved road in the region. The landscape here Fenton 1997); hence a capture simply denoted the is highly fragmented by cattle pasture, cornfields, presence of an individual and did not indicate in and successional vegetation, mostly 1-10 years old. what way the site was used. We assume, however, Forest fragments differ in size from less than one that many bats captured were foraging or traveling to hundreds of hectares, with small fragments of 1 to foraging sites. to 20 ha being most common. Forest remnants are Initial experimentation with mist netting along scattered through the landscape and generally are transects randomly situated in the forest understory isolated from other fragments by young succession- yielded prohibitively low capture rates: less than al vegetation or pasture. one bat per 16 net-hours. We therefore limited Deforestation ofien follows a nonrandom pattern sampling in both treatments to major trails and with productive agricultural areas most prone to clear- roads beneath closed canopy-human modifica- ing (Dale & Pearson 1997); likewise, at Tikal, a large tions frequently used as flyways by phyllostomids proportion of forest fragments occupy hilltops with (Tuttle 1976). We recognize a potential bias in fa- upland dry forest (Schulze & Whitacre in press), with vor of species using these pathways for foraging or swales between preferentially farmed land. Use of for- travel, particularly for frugivorous and nectarivo- est fragments by local people is frequent, mainly con- rous species (cf: Palmeirim & Etheridge 1985). We, sisting of extracting firewood and building materials, however, believe this bias to be similar for the two hunting, and collecting several palm species and other treatments. Each mist-net array consisted of four plant products. More damaging activities include to six nets (six was the target number, but high opening of fragments to cattle grazing and cutting capture rates forced net closures on some nights) branches of the tree Brosimum alicdctrum for cattle spaced along a 500-m segment of a major trail or and mule forage. Fires frequently spread from adja- small road, with each net crossing these flyways. cent pastures and fields to forest fragments (M. Schul- Mist netting began 20 minutes after sunset and ze, pers. obs.; 4 Laurance 1997, Lynam 1997), ac- continued for two to three hours. Sampling effort celerating the process of degradation, killing both can- was 15.3 t 3.8 (SD) net-hours per site in Tikal opy and understory plants, increasing light penetra- and 16.1 t 3.9 (SD) net-hours in the fragments tion to the understory, and shifting the species (Table 1). composition of the understory (4 Holdsworth & Bats were identified to species with the exception Uhl 1997), and eventually the canopy, toward ag- of Ghssopbaga and Dmnura (species could not be gressive, light-demanding plant species (e.g., Pipe. reliably distinguished), measured for forearm length, spp., Sebdctiana longicmpis, Dendropandlc arborem, and marked dorsally with an indelible marking pen Cecropia peltata). Degree of degradation of forest frag- to prevent recording any individual more than once ments, as judged qualitatively through comparison of at a site. A total of 440 phyllostomid bats was cap- forest structure and tree species composition during tured in continuous, mature forest in Tikal, and 461 an initial survey, appeared to show an inverse rela- in the forest fragments outside the park. tionship to fragment size (M. Schulze, pers. obs.). After the first two Tikal sites, which were sam- pled more than a month prior to initiation of sam- METIiom-Mist-net samples of bats were taken at pling in the fragmented landscape, no sample from 11 sites within Tikal and in 7 forest fragments dur- a given treatment was taken more than ten days ing the dry season (February-June) of 1994; sam- apart from a sample of the other treatment to con- pling of intact forest and forest fragment sites was trol for any potential seasonal variation in capture alternated to control for possible seasonal effects. probabilities. Because of the potential bias in the We sampled using 35-mm mesh, 12-m mist nests early Tikal samples and the higher overall sampling set from the ground to 2.5 m height. Mist netting intensity in this treatment, we omitted these sam- Bats in Forest Fragments 177

TABLE 1. Characteristics, sampling effort, and sample sizesfor mist-netting sites in forestfragments and continuousforest, Pet& Guatemah.

Distance from Forest fragment continuous Fragment size Sampling effort Capture total (site no.-name) forest (km) (ha) (net-hours) (no. of indivs.) 1-Quemadal Road 5 3-4 8.5 9 2-Parcela Pajaritos 6 8-10 19.5 35 3-Terry 8 ca 5 20.5 47 4-Invisible Stump 4 ca 10 17.0 40 5-“Danto” Woods 6 50-100 18.0 94 6-Rodolfo 6 ca 15 12.5 84 7-Dave’s Paradise 10 200 16.6 158 Tikal forest transect Nearest Tikal Sampling effort Capture total (site no-name) transect (km) (net-hours) (no. of indivs.) *--Chasis Quemado, I 0.8 12.5 12 *-Complejo P, I 0.4 13.0 23 1-Temple IV 1 12 15 2-Brecha Anabela, I 1.5 13.5 16 3-Brecha Anabela, I1 1.5 12 7 4-Chasis Quemado, I1 0.8 13.5 25 5-Naranjal 21.0 36 (,-Temple VI 2 19.5 86 7-Compejo P, I1 0.4 22.5 112 8-Curva Peligrosa 5 13.0 58 9-Nat’s gravel pit 2 13.3 56 * Asterisks indicate two Tikal sites omitted from analyses.

ples from analyses (omitting these sites did not sub- samples; all captures at Tikal were used, excluding stantially affect species composition or proportional sites 1 and 2, and a random sample of 403 was abundances). selected from the 461 captures in forest fragments. Seven forest fragments were studied: five be- Species richness and composition were compared tween ca 8 and 20 ha, one between 50 and 100 between treatments. The observed Jaccard?s simi- ha, and one ca 200 ha (Table 1). All forest frag- larity index (Krebs 1989) for the two treatments ments sampled were within 4 to 10 km of an im- was compared to a simulated distribution of indices mense tract (thousands of km2) of continuous for- based on the null hypothesis of no treatment effect, est. Although we examined differences between using resampling with random assignment of tran- large (>50 ha) and small (<20 ha) fragments, most sects to treatments (Mooney & Duvall 1993). comparisons considered all seven fragments collec- Abundance distributions were compared between tively as the fragmented treatment; the nine sites treatments in two ways. A Kolmogorov-Smirnov within Tikal National Park comprised the contin- two-sample test (Sokal & Rohlf 1981) was used to uous forest treatment. Overall sampling effort was compare the total distributions and a G-test (op. roughly comparable, but not equal, between treat- cit.) was employed (R x C with the ten lowest ranks ments, with 155.8 net-hours at Tikal (of which grouped into two classes to achieve expected cell 130.3 were used in analyses) and 112.6 in forest totals of at least five for all cells). The latter test fragments. High variability in capture rates and was used to focus on the abundances of the seven sampling effort between nights within treatments first-ranked species per treatment, in which relative and an increase in capture rates through the study abundances were sampled most adequately. In ad- period led us to focus primarily on the proportional dition, observed rank-abundance distributions for composition of total captures per treatment (CJ To- each treatment were compared (Kolmogorov-Smir- keshi 1993) rather than on absolute number of nov test) to expected values calculated from the captures per net array or per net-hour. broken-stick (MacArthur 1957, 1960) and geo- We analyzed the data in several ways. First, data metric series models (Tokeshi 1990). were grouped by treatment and 403 captures se- We distinguished three feeding guilds: frugi- lected from each treatment to provide equally sized vores, nectarivores, and animal-eating bats, includ- 178 Schulze, Seavy, and Whitacre

TABLE 2. Total and proportional capture rates of phyllostomid bat species in continuous and japented forest samples, Pet&, Guatemala."

Continuous forest Forest fragments Forearm lengthb No. of captures Percent No. of captures Percent Large frugivores 180 (183) 44.7 65 (74) 16.1 Artibeus jamaicensis" 60.1 ? 2.1 75 (77) 18.6 32 (35) 7.9 A. lituratus" 69.3 i- 3.0 105 (106) 26.1 33 (39) 8.2 Small frugivores 206 (237) 51.1 331 (379) 82.1 Carollia brevicauda 39.4 i- 1.2 50 (63) 12.4 56 (68) 13.9 C. perspicillala 43.4 z 1.1 20 (24) 5.0 22 (26) 5.5 Carollia sp. (undet.) NA 3 (6) 0.7 1 (2) 0.2 Centurio sene& 42.6 2 2.2 38 (38) 9.4 20 (22) 5.0 Dermanura sp." 38.0 t 1.1 24 (28) 6.0 56 (64) 13.9 Sturnira liliumC 37.8 i 1.2 69 (76) 17.1 174 (190) 43.2 bilobatum 43.2 0 (0) 0.0 0 (1) 0.0 Varnpyressa pusilla 36.1 i 2.1 2 (2) 0.5 2 14) 0.5 Vampyrops helleri 38.3 0 (0) 0.0 0 (1) 0.0 Nectarivores 6 (8) 1.5 3 (3) 0.7 spp. 35.0 t 1.3 6 (8) 1.5 3 (3) 0.7 Animal-eating bats 11 (11) 2.7 4 (5) 1.o megalotis 34.1 0 (0) 0.0 1 (1) 0.2 Mimon cozumelae 57.3 2 0.7 2 (2) 0.5 0 (1) 0.0 M. crenulatum NA 0 (0) 0.0 1 (1) 0.2 bidens 56.5 t 0.8 2 (2) 0.5 0 (0) 0.0 7: evotis 51.4 i 0.7 1 (1) 0.2 1 (1) 0.2 Trachops cirrbosus 57.2 t 1.9 3 (3) 0.7 1 (1) 0.2 Chrotopterus auritus 83.1 1 (1) 0.2 0 (0) 0.0 Vampyrum spectrum 105.5 t 2.0 2 (2) 0.5 0 (0) 0.0 Sanguivores 0 (3) 0.0 0 0 Desmodw rotundzs 54 0 (3) 0.0 0 (0) 0.0 Total 403 (440) 100.0 403 (461) 100.0

" Capture numbers for subsamples used in most analyses are given first. Numbers in parentheses are total captures per treatment. b, i- SD. ' Treatment difference (G-test) significant at P = 0.01 after Bonferroni adjustment (k = 7 comparisons). " Treatment difference (G-test) significant at P = 0.05 after Bonferroni adjustment (k = 7 comparisons). ing foliage-gleaning insectivores and "carnivores" tation did not differ between large and small forest (i.e., species feeding on vertebrates). Forearm fragments (215 captures in five small fragments vs. length of related bat species has been shown to 252 captures in two large fragments). Single-species correlate with diet, amount of time spent feeding comparisons between treatments were conducted in second-growth forest (Fleming 199 l), foraging using G-tests on focal species captures versus all height in forests, and the size of fruits taken (Flem- other captures out of 403 per treatment; Fisher's ing 1988). We tested for such patterns by regress- exact tests gave identical results. When multiple ing mean forearm length of each frugivore species comparisons were made, we controlled tablewise on the ratio of continuous forest captures to forest type I error rates using a sequential Bonferroni pro- fragment captures. To test for differences in body cedure (Rice 1989). All statistical tests were con- size and feeding guild with respect to forest frag- ducted using SYSTAT (Wilkinson 1990). mentation, we assigned species to size classes (based on forearm lengths: small frugivores with forearm RESULTS <45 mrn; large frugivores with forearm >55 mm) and feeding guild (based on published diet infor- Our samples revealed no difference in phyllostomid mation). Total captures then were tabulated for species richness between continuous forest and for- each trophidbody size guild and a G-test (R X C) est fragments. Of 20 species captured, 13 were tak- was used to test for differences in guild represen- en in both habitats, four were unique to the con- tation between treatments. A G-test also was used tinuous forest, and three were unique to forest frag- to test the null hypothesis that bat guild represen- ments (Table 2). Hence, 65 percent of species were Bats in Forest Fragments 179

Number of captures was captured more commonly in forest fragments - ~- than in continuous forest (P= 0.999 X lO-’5, G 300 1- ~ - 1 = = = + Continuous forest 66.6, df l), as was Dermanura sp. (P +-Forest fragments 0.00014, G = 14.58, df = 1). In contrast, Artibeus v-Broken-stick 250 jamaicensis and A. lituratzls were more commonly 200 4 Qeometric Series 1 taken in continuous forest (P= 0.62 X 10-5 and G = 20.43; P = 0.6 X lo-“ and G = 47.26, respectively; df = I), as was Centzlrio senex (P = 0.013, G = 6.11, df = 1). After Bonferroni ad- justment, the first four species above displayed ta- blewise significance at P < 0.01, and Centurio did so at tablewise P < 0.05. 123 4 5 6 7 8 910111213 Large frugivores (Table 2) comprised a signifi- Rank abundance cantly larger proportion of captures in the contin- uous, undisturbed forest than in forest fragments; FIGURE 1. Dominance-diversity plots based on phyl- lostomid bat captures in continuous and fragmented for- small frugivores displayed the opposite pattern (G- est, Petkn, Guatemala. Plots are based on the 13 first- test using three guilds-small frugivores, large fru- ranked species in both habitats (398 captures in contin- givores, and all others-was significant: P < 0.001, uous forest; 402 in forest fragments). Expected values G = 89.8, df = 2). Not all small frugivores, how- shown for broken-stick and geometric series distributions are for continuous forest captures; those for forest frag- ever, were more common in the forest fragment ments were nearly identical. sample than in continuous forest. C. senex was sub- stantially better-represented in the continuous for- est sample (Table 2). For seven species of frugivo- rous bats, forearm length was a good predictor of shared between treatments for a Jaccard‘s coefficient the ratio of captures in continuous forest to those of 0.65. This value is within the 95 percent con- in forest fragments (linear regression: adj. R2 = fidence interval calculated by resampling under the 82.4%, P < 0.003, F,,> = 29.0), with larger bats null model of no treatment effect (2 ? SD = 0.667 having proportionally more captures in continuous 2 0.056; range = 0.550-0.750; N = 300 itera- forest than in fragments. tions). Rank-abundance distributions in the two The other guilds were represented by too few treatments did not differ overall (Kolmogorov- captures to warrant statistical testing, but one sug- Smirnov test: P = 0.73), but they did in a G-test gestive pattern was noted. Captures of large, ani- (P < 0.001, G = 40.75, df = 8) in which the mal-eating bats that include vertebrates in their diet “tail” of rare species was combined into two classes; hence, relative abundance patterns of the seven (“carnivores”; Norberg & Fenton 1988) were six first-ranked species differed between treatments. times more frequent in undisturbed forest than in Observed rank-abundance patterns differed strong- the forest fragments (Table 2). The one such spe- ly from the geometric series distribution (Kolmo- cies recorded in a forest fragment, Eachops cirrho- gorov-Smirnoff two-sample tests: P < 0.0002 and sw, is relatively small. In contrast, large, non-fru- 0.002 for continuous and fragmented forest, re- givorous bats were captured in 6 of 11 transects spectively). Neither sample departed significantly (55%) in Tikal’s continuous forest, and three large from the broken-stick distribution (Kolmogorov- carnivores (two Chrotopterus auritzls and one Vam- Smirnoff tests: P = 0.065 and 0.1 11 for continu- pymm spectrum) were captured there. ous forest and forest fragments, respectively). One Guild representation (frugivores, nectarivores, species, Sturnira lilium, accounted for 43 percent and animal-eating bats; total captures per guild as of captures in the forest fragments (Fig. l), result- a proportion of all captures) did not differ statis- ing in greater dominance there than in the contin- tically between large and small forest fragments (G- uous forest sample. test: P > 0.5, G = 3.7, df = 2), and proportional Proportional abundances of phyllostomids were abundances of the most common species were significantly different between the continuous for- equivalent in samples from small and large forest est and forest fragment samples, both in terms of fragments. Six of the seven rarest species in the individual species and feeding guilds. Based on G- forest fragment sample, however, were captured in tests, five species differed significantly in propor- the two largest fragments, both >50 ha. Moreover, tional capture rates between treatments. S. lilium the only predator of vertebrates captured in the 180 Schulze, Seavy, and Whitacre farming landscape (I:cirrhosus) was captured in the or from the “mainland source pool. Malcolm largest forest fragment sampled (ca 200 ha). (1997) hypothesized that the apparent difference in the ability of small and trophically DISCUSSION similar understory insectivorous birds to utilize the deforested matrix habitat results from a difference The most striking difference detected between un- in their perceptions of the deforested matrix. He disturbed forest and forest fragments was the high- suggested that the perceived difference in environ- er ratio of small to large frugivores in the forest ment between forest fragments and the deforested fragments (Table 2). In Brazil, Bierregaard and matrix is smaller for nocturnal vertebrates (e.g., Stouffer (1997) found that capture rates (and pre- most small mammals) than for diurnal ones (e.g., sumably populations) of many frugivorous bird most birds). Bats would be expected to display at species declined in recently isolated forest frag- least as great an ability to traverse matrix habitat ments. Although for the ten species with adequate as nocturnal quadrupedal mammals, and many spe- samples, magnitude of decline showed no clear re- cies have in fact been shown to readily cross habitat lationship to body size, these authors noted a scar- boundaries (e.g., Fleming & Heithaus 1986, Gal- city of medium-sized frugivores and a predomi- etti & Morellato 1994). nance of small frugivores moving through young The lower capture rates (and presumably num- second-growth forest. They suggested that fruits bers) of large frugivorous bats we noted in the for- available in young second growth on average may est fragments likely is related to fruit availability. be small relative to those in mature forest, and im- In our study area, we noted that during the process plied that this influences patterns of habitat use by of forest degradation by human extractive uses and frugivores. We present a similar argument that fruit fire, the abundances of light-demanding understory size may have influenced the patterns we observed species (e.g., Piper spp.) and fast-growing tree spe- among bats. We also point out that a key question cies (including but not limited to pioneer species) is: to what extent did the bats caught in forest frag- increase-a pattern that has been documented for ments live primarily in those fragments, as opposed forest fragments in other tropical areas (Laurance to ranging widely over a broader area! In this con- 1997, Viana et al. 1997, Laurance et al. 1998). nection, we hypothesize that frugivorous bats may This is accompanied by a decrease in the abun- move more freely over the fragmented landscape dance of many mature forest tree species-e.g., Bro- than many birds. simum alicastrum (coppiced for livestock forage), In previous studies of fragmented tropical land- Manilkara zapota (heavily exploited for firewood), scapes, the major determinant of the vulnerability and at times, large Ficus spp.-which serve as im- of a species or group to fragmentation appeared to portant fruit resources at Tikal (Schulze & Whit- be the ability to cross or forage within the defor- acre in press). In several of the forest fragments in ested matrix (Bierregaard & Stouffer 1997, Mal- which we sampled bats, mature forest tree species colm 1997). Hence, many bird, beetle, and primate largely had been replaced by light-demanding pi- species at Manaus, Brazil, declined in fragments oneer and canopy species, particularly Sebastiuna (Klein 1989, Bierregaard & Stouffer 1997, Did- longicuspis. Qualitative observations also revealed ham 1997), whereas small mammal and frog spe- that the understory in these degraded fragments cies richness increased and few species declined in had a high concentration of light-demanding Piper abundance (Malcolm 1997, Tocher et al. 1997). spp. (e.g., I? auritum, I? aduncum), in addition to Even for the most vulnerable bird guild in Ma- the shade-tolerant P+er spp. typically found in ma- naus-understory insectivores-regrowth of vege- ture forest understories (e.g., I! psilorachis; Schulze tation surrounding small forest fragments was & Whitacre in press). Higher densities of Piper spp. enough after five years to facilitate recolonization in disturbed habitats than in adjacent mature forest of fragments (Bierregaard & Stouffer 1997). The have been recorded in many tropical areas (Croat importance of the nature of the surrounding “ma- 1978; Opler et al. 1980; Fleming 1991) including trix” habitat is further emphasized by the finding Pettn (M. Schulze, pers. obs.). Although some that species richness and abundances of small light-demanding tree species produce relatively mammals declined dramatically within five years of large fruits amenable to consumption by large bats, isolation in small islands surrounded by water in many, such as S. longicuspis, do not. A. jamaicensis Thailand (Lynam 1997). In this situation, the ma- and A. lituratw have been found to take primarily trix habitat was hostile to small mammals, presum- fruits of canopy trees such as Ficus and Brosimum, ably resulting in limited dispersal among fragments although fruits of understory species also are taken Bats in Forest Fragments 181

(Vizquez-Yanes et al. 1975; Gardner 1977; Mor- penetration of solar radiation and decreased hu- rison 1978, 1980; Fleming 1988; Galetti & Mo- midity and foliage density (Lovejoy et al. 1986, rellato 1994). A. jamaicensis and A. lituratus also Laurance 1997) likely result in fewer sites in de- declined in abundance in deforested areas of graded forest fragments that are immune to daily French Guiana (Brossett et af. 1996), presumably temperature extremes. The combination of reduced due to changes in fruiting resources and vegetation fruit and roost availability might be expected to structure. decrease both the number of local foragers (i.e., Lower densities or absence of certain fruit trees individuals roosting in a given forest patch) and (Brosimum, Ficw, Munilkara, and Sapotaceae spp.) the number of A. jamaicensis and A. lituratus in- in forest fragments may make foraging in such ar- dividuals traveling from remote roosts to feed in a eas less rewarding for large ftugivorous bats (see given fragment. Fleming 1988 for review of major plant families Many of the smaller frugivores, particularly S. producing fruits eaten by bats). Even if density of lilium and Carollia perspicilkzta, specialize to some important fruit trees per unit area were the same degree on the relatively small fruits of Piper spp. within fragments as within continuous forest, the (Fleming 1988, Palmeirim et al. 1989), and for limited representation of fragments in the farming these bat species, food resources actually may in- landscape would dictate a lower overall fruit tree crease in density as forest fragments undergo the density than in continuous forest. Overall low den- process of degradation (i.e., as Piper spp. replace sities of fruiting trees in fragmented areas may im- more shade-toletant tree saplings and treelets). In pose high travel costs in foraging-in terms of both fact, S. lilium and C. perspicillata forage in young energy and predation risk, which is believed to ex- second-growth forest, exploiting fruit resources ert important influences on foraging movements of provided by pioneer tree and shrub species (Heit- frugivorous bats (Heithaus & Fleming 1978, Mor- haus & Fleming 1978, Brossett et al. 1996); in rison 1978, Fleming 1982). Artibeus spp. have been southeastern Peru, C. perspicilkzta was considered documented to travel 10 km from day roosts to an indicator of forest disturbance (Wilson et al. feeding sites (Fleming 1982, Fenton et al. 1992). 1996). Hence, even forest fragments too small to meet the The chief exception to the observed pattern of total food demands of one or more Artibeus indi- increased abundance of small ftugivores in dis- viduals still could be exploited by individuals that turbed forests in our study was c. senex, which had include these fragments within a broader foraging lower proportional abundance in forest fragments range. Because of the demonstrated high mobility than in continuous forest (Table 2). Similarly, at and capacity of Artibeus to cross habitat boundaries Los Twtlas, Mexico, C. senex was not found in (Fenton et al. 1992, Galetti & Morellato 1994), it highly disturbed habitats (Estrada et a/. 1993). The is unlikely that fragment size is the sole determi- limited dietary information available for this spe- nant of foraging densities. Additional factors likely cies suggests it may rely heavily on large, fleshy include the quality of forest patches and their spa- fruits (Gardner 1977, Snow et al. 1980, Nowak & tial juxtaposition, which jointly should determine Paradiso 1983). Tree species providing such fruits overall food density in the landscape as well as the (e.g., Ficw spp. and Manilkara) are typically mature costs of foraging in terms of time and energy bud- forest species; hence Centurio may be expected to gets and predation risk. respond to forest degradation in a manner similar It is currently not known to what degree roost to that of large species of Artibeus. site availability, rather than foraging habitat, limits It is possible that many of the individuals we bat behavior and population dynamics. Roost sites, captured, especially in the smaller fragments, roost- particularly the hollow tree cavities preferred for ed in other, larger forest fragments or in the con- harem roosts of A. jamaicensis (Morrison 1979), tinuous forest nearby, visiting smaller fragments may be less common in forest fragments than in only to forage. In addition, it is possible that in- undisturbed forest, as wood harvesting and in- dividuals foraging in fragments visited multiple for- creased treefall rates in fragments (Laurance 1997) est patches in a given night. Given this scenario, lead to decreased densities of the mature trees that important determinants of a species’ ability to ex- typically form such cavities. In small fragments, ploit forest fragments may include the spatial dis- sampling effects may result in lack of rate roost tribution of fragments and their proximity to rel- sites such as large, hollow trees. Availability of roost atively undisturbed forest. Hence, in a similar sites within foliage should be affected less by frag- slash-and-burn matrix that was farther from large mentation and forest degradation, but increased areas of pristine forest, one might expect the bat 182 Schulze, Seavy, and Whitacre community to differ even more strongly from that species can maintain self-sustaining populations of intact forest. there. While our results indicate that many forest- dwelling phyllostomids use forest remnants to some ACKNOWLEDGMENTS degree, it is also clear that significant differences exist among bat species in this regard. Many bat We are grateful to Tim McCarthy for help in marshaling resources for bat identification, and to M. B. Fenton, T. species, especially insectivores, were not well-sam- H. Fleming, R. Bjork, L. Kiff, and an anonymous re- pled by our methods. Large predators are some- viewer for commenting on an earlier draft. This work times predicted to be among the most sensitive in- formed part of the Peregrine Fund’s “Maya Project”; we dicators of habitat modification (Schaller & Craw- are grateful to W. Burnham, President of the Peregrine Fund, and to the Funds board of directors for their sup- shaw 1980, Terborgh 1992), and the apparent rar- port of this research. The Maya Project has received fi- ity or absence of C. auritus and I.i spectrum in the nancial support from Ruth Andres, Robert Berry, the forest fragments suggests that further research into Crystal Channel Foundation, Evie Donaldson, the Gold the effects of fragmentation on populations of these Family Foundation, the William H. and Mattie Wattis Harris Foundation, the Alfred Jurzykowski Foundation, relatively rare species is warranted. Even for species KENNETECHIUS. Windpower, the John D. and Cath- commonly caught in forest fragments, it remains erine T. MacArthur Foundation, Mill Pond Press, the Na- unknown to what extent they live within frag- tional Fish and Wildlife Foundation, the Norcross Foun- ments, versus ranging more widely. Study of move- dation, Henry and Wendy Paulson, the Pew Charitable ment patterns, residency, and population dynamics Trusts, Andres and Pilar Sada, Joe and Falinda Terteling, the U.S. Agency for International Development, the U.S. of select phyllostomid species in the slash-and-burn Man and the Biosphere ProgramlTropical Ecosystems Di- mosaic would help elucidate whether or not certain rectorate, and the Weeden Foundation.

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