2007. Proceedings of the Indiana Academy of Science 116(l):66-70

ACTIVITY PATTERNS IN A CAPTIVE COLONY OF JAMAICAN FRUIT , JAMAICENSIS

1 2 Jennifer J. Tung and Karen E. Francl : Department of Biological Sciences, University of Notre Dame, Notre Dame, Indiana 46556 USA

ABSTRACT. We examined activity patterns of a captive colony of Jamaican fruit bats {Artibeus ja- maicensis) using an Anabat II echolocation detection system and visual observations. Results showed that this colony, subjected to a light-reversal circadian cycle (darkness ca. 1000-2000 h daily), adjusted its activity patterns to maximize activity during dark hours. Major activities, including flying and feeding, were most frequent shortly after dark hours began, and roosting alternately increased throughout the dark time blocks. Additionally, captive behavior appeared to follow expected patterns of natural populations; they fed away from the source of food and preferred to roost in smaller groups rather than in large ones. We, therefore, provide quantitative evidence that captive colonies may be useful in elucidating the behav- iors of natural populations.

Keywords: Artibeus jamaicensis, behavior, circadian activity, echolocation

Jamaican fruit bats (Phyllostomidae: Arti- equates to ca. 2000-2200 h during summer beus jamaicensis) are leaf- nosed bats whose months. Additionally, they found that activity native range includes Brazil, , peaked around midnight (ca. 2-4 h after dusk) Antilles, Trinidad, Tobago, Key West, and and activity was less predictable and more from central Mexico south to Bolivia. This sporadic in remaining dark hours (Fenton & species tends to roost in caves, rock over- Kunz 1977). Whether this species follows a hangs, rock fissures, buildings, hollow trees, similar pattern of activity in captivity is un- and self-made leaf tents (Gorog 1999). Pri- known. marily frugivorous with a specialty in figs (Fi- The roosting behavior of wild colonies has cus spp.), Jamaican fruit bats also feed on focused on caves, in which a harem-like social mangos (Mangifera spp.), avocados (Persea hierarchy exists. Typically, one dominant americana), bananas (Musa spp.), and espave male roosts with 2—14 females (Kunz et al. nuts (Anacardium excelsum; Morrison 1978; 1983; Ortega & Arita 1999), but larger groups Castro Arellano This species Ortega & 2001). of up to 20 individuals may form if subdom- often transports fruit to night roosts for feed- inant males are present. Outside of harems, ing, acting as influential dispersers of tropical fruit bats may roost individually or in small fruits (Gorog 1999). Often referred to as clusters (Ortega & Arita 1999). Given the typ- "whispering bats," Jamaican fruit bats emit ically skewed sex ratio in captive fruit bat col- three low-intensity FM pulses used primarily onies, as well as limitation for space, it is un- for obstacle avoidance while flying or perch- known whether these group sizes will be as ing (Heffner et al. 2003). A series of 40-60 large or as socially structured in captivity as kHz pulses usually precedes a 60-110 kHz in the wild. harmonic, followed by pulses at 30-33 kHz Altered fruit bat activity with respect to (Novick 1963). changes in light pattern is a generally accepted Fenton & Kunz (1977) found that wild pop- conjecture (Erkert 1978). However, the extent ulations of Jamaican fruit bats were most ac- of change in behavioral activity has rarely tive during the first hours after dusk, which been quantified (e.g., Erkert & Kracht 1978; Marimuthu 1984). To quantify how a captive 1 Current address Bard Hall, Columbia Univer- colony of Jamaican fruit bats has acclimated sity, Mailbox #B 232, 50 Haven Avenue, New York, New York 10032 USA. to a complete light-reversal, we utilized an 2 Current address: Biology Department, Radford Anabat II detection system (Titley Electronics, University, Radfoul, Virginia 24142 USA. Australia) to record echolocation calls in 24 h

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TUNG & FRANCL—CAPTIVE BAT ACTIVITY PATTERNS 67

cycles. We supplemented this work with vi- posed to any natural daylight. Bats were fed sual observations throughout their most active chopped fruit twice daily (ca. 1030 h and hours to document specific behavioral pat- 1330 h) placed in three hanging bowls while terns. From these two methods of study, we whole bananas were hung from smaller hypothesized: 1) captive Jamaican fruit bats branches. Whole apples (Mains sppj and or- would alter their activity patterns (as docu- anges (Citrus sinensis) were also occasionally mented by echolocation calls) in response to provided on smaller branches. reverse light conditions. Specifically, they Echolocation patterns.— Bat activity was would mimic wild bat populations by mark- monitored in ten 24 h sampling periods (Sep- edly increasing activity immediately after tember 2005-April 2006) using an Anabat II lights were shut off and peak activity ca. 2-4 detector and ZCAIM unit (Titley Electronics. h after darkness had begun; 2) captive bat ac- Australia). This unit was set up in a corner of tive behavioral patterns would reflect these the enclosure, with the microphone/detector echolocation patterns; bats would fly, feed, pointed at a ca. 45° angle toward the middle vocalize, often and crawl more immediately of the enclosure to maximize call recording after lights these bats were dimmed, and ability and quality. If the Anabat system de- would roost more often in later hours; 3) cap- tected a call, it saved the call(s) in a file that tive Jamaican fruit bats would roost and feed encompassed 15 sec of elapsed time. In An- in ways similar to their wild counterparts, alook 4.9g (Corben 2003), we documented the roosting in smaller groups and feeding away time at which these data files contained qual- from the original food source. Given the lim- ity calls (>3 individual call pulses; Johnson ited space and minority of males in our cap- et al. 2002). Because of the presence of Egyp- tive colony, we expected a tendency toward tian bats in the enclosure, only calls with av- small groups or solitary individuals. However, erage frequencies >40 kHz were counted as because we could not readily distinguish Jamaican fruit bat calls (von Herbert 1985 as males from females in the enclosure, we could referenced in Holland et al. 2004). The num- not speculate on the possibilities of social hi- ber of files with documented fruit bat calls erarchies in this captive environment. was summed across 15 min periods, and the METHODS average number (with standard error) of tiles per 15 min was graphed to observe patterns Enclosure.—We studied a captive-born and across the 24 h sampling periods. -bred colony of 167 (32(5, 1359) Jamaican Behavioral observations.—Individual be- fruit bats at the Potawatomi Zoo, South Bend, haviors for colony members were observed in Indiana. Also in the exhibit were 19 Egyptian three-hour observational periods, all o\ which fruit bats (Pteropodidae: Rousettus aegyptia- fell between 1000-1700 h when it was dark cus), which is one of the few megachiropteran (and during hours in which /oo staff allowed bat species that echolocates (peak frequency access). Every 15 min. we documented the = 20-40 kHz [von Herbert 1985 as refer- number of individuals performing an\ of five enced in Holland et al. 2004]). The 5.3 m long actions: flying, feeding, vocalizing (al fre- X 3.3 m wide X 2.7 m high enclosure con- quencies < 20 kHz), crawling on the floor, tained two large horizontal plastic perches, roosting. These four four smaller plastic branches, as well as a and observations per transformed large vertical perch that spanned the height of hour were into relative activity the enclosure. The glass display window also proportions, then averaged across seven 1 h provided perching opportunities along a rim time blocks (1000-1700 h). However, we re- which butted up against the ceiling, as did air stricted statistical analyses to six blocks be- = vents in the ceiling. tween 1000-1600 h (/; 1 set of behavioral The zookeepers of the exhibit practiced re- observations between 1600-1700 h). verse-daylight conditions to maximize bat ac- Additional analyses examined bat prefer- tivity during hours of public viewing. The en- ences in feeding (at food cups v.v. aw a\ from closure was illuminated with fluorescent food cups: paired f-test) and roosting (in clus- ceiling lights from ca. 2000-1000 h every ters of >7 fruit bats. 5—7 fruit bats, or 2 — day. Due to the interior location of the exhibit fruit bats: one-way ANOVA) behaviors. All within the zoo building, the bats were not ex- statistical analyses were performed in SYS- 68 PROCEEDINGS OF THE INDIANA ACADEMY OF SCIENCE

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Figure 1 . —Anabat echolocation calls for captive Jamaican fruit bat colony, exposed to reverse daylight conditions. Plotted is average number of calls per 15-min interval (with 95% CI) for ten 24-h observation periods from September 2005-January 2006. Time interval between dotted vertical lines indicates ap- proximate hours in which bat enclosure was dark.

TAT 11.0 (Systat, Inc., Point Richmond, Cal- = 0.1 17), as well. A similar decline in feeding ifornia). was observed from the 1300 h to the 1400 h (P = 0.121). Additionally, a paired f-test RESULTS found that more bats were observed to feed We documented 18,509 Jamaican fruit bat away from food cups (x = 9.0 individuals per echolocation calls during our study, and av- observation) than at cups (x = 4.0; t = 6.667, eraged them across 15-min intervals (Fig. 1). df = 107, P < 0.001) across all time intervals. Bat activity was significantly higher in the en- Finally, bat roosting peaked during the = closure during dark hours (1000-2000 h; x 1400-h time block, which was significantly 43.2 ± 15.3) than during light hours (x - 5.1 more than roosting activity during the 1100 h ± 10.5; t = 41.4, df = 579, P < 0.001). Fur- (P = 0.001) and 1200 h (P = 0.001) time thermore, we found that the number of calls blocks. An ANOVA was used to examine per hour differed across the seven time blocks group size in roosting, and found that the three in which bat behavior was recorded (Kruskal- size groups (2—4 individuals, 4—7 individuals, Wallis test, K-W = 13.507, df = 6, P = 0.036; >7 individuals) differed significantly from Fig. 1). one another (F = 536.5, df = 2, P < 0.001). From 1000-1600 h, we found that bat fly- The smallest grouping occurred more often ing (F = 4.031, df = 5, P = 0.002), feeding than the medium (4-7) and large (>7) groups (F = 4.965, df = 5, P < 0.001), and roosting (P < 0.001 for both Tukey post-hoc compar- (F = 5.597, df = 5, P < 0.001) proportionally isons), and individuals in medium groups oc- differed across time blocks (Fig. 2). Specifi- curred more often than those in large groups cally, a Tukey's post-hoc test determined that (P = 0.006). Crawling (F = 1.694, df = 5, P more bats were flying in the 1100 h (i.e., be- = 0.143) and vocalizing (F = 0.958, df = 5, = tween 1100-1200 h) than the 1200 h (P P = 0.447) did not differ significantly across = 0.021), 1300 h (P = 0.005) and 1400 h (P any time intervals. 0.017) time blocks. Bats fed less often during the 1300 h than at 1100 h (P = 0.052) and DISCUSSION 1200 h (P < 0.001) and showed a trend in As expected, the captive colony of Jamai- feeding less often at 1400 h than at 1300 h (P can fruit bats exhibited a reverse-patterned TUNG & FRANCL—CAPTIVE BAT ACTIVITY PATTERNS 69

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Figure 2. —Proportional bat activity (with 95% CI) for captive Jamaican fruit bat colony, exposed to reverse daylight conditions. Behavioral observations recorded from 1000-1100 h, e.g.. are listed as an average at 1000 h. Bats were in darkness during all behavioral observation periods. An asterisk indicates that activity differed significantly across time blocks (see text for details).

circadian cycle complementary to the reverse- ally smaller than what had been found in pre- daylight pattern utilized in the Jamaican fruit vious studies of wild populations (Morrison bat exhibit. The Jamaican fruit bats showed 1978; Gorog 1999). While previous research significantly more echolocation activity dur- (e.g., Ortega & Arita 1999) has shown that ing unlit hours. Their natural nocturnal Jamaican fruit bats tend to form large harem rhythms, consistent with the hypothesis that groups for roosting in caves, these bats may the captive colony would adjust their circa- display more opportunistic day-roosting be- dian rhythms to the reverse-daylight cycles of havior, depending on the natural surroundings the exhibit. and availability of resources (Morrison 1979). The Jamaican fruit bats exhibited corre- With few males present, a guaranteed food sponding behavioral changes with respect to supply nearby, and multiple perching and the changes in light. Analyses of behavioral roosting sites within the enclosure, several data showed there was statistically more feed- large roosts seem unlikely. ing and flight activity during the earlier dark Peaks in flight and foraging activity of the hours while roosting increased as the dark captive colony of Jamaican fruit bats were hours progressed. However, vocalizing and also consistent with previous studies of wild crawling were not prevalent activities and did Jamaican fruit bats. The captive colony pre- not differ significantly across time. The be- sented two peaks oi' activity during the dark havioral data also revealed these captive fruit hours: one major peak during the first hour of bats to have a tendency to feed away from the darkness (0930-1000 h) and a minor peak ca. feeding cups, supporting the hypothesis that 1900 h (Fig. 1). Jamaican fruit bats in then- this group would retain wild tendencies. De- natural habitats are more active during the first spite being in a relatively small enclosure, the few hours of darkness with a maximum peak

Jamaican fruit bats still carried their food generally around midnight (Fenton e>: Run/ away from the food source for feeding, con- 1977). This peak at midnight might corre- tinuing their natural role as seed dispersers spond to a peak activity in this captive colom (Fleming & Heithaus 1981). at ca. 0930-1 130 h. However, the roosting groups were gener- Because ioo hours did not allow for 24-h 70 PROCEEDINGS OF THE INDIANA ACADEMY OF SCIENCE

behavioral observations of the captive colony, logical adaptation of circadian systems. Oecolo- these data do not represent a full behavioral gia 32:71-78. Fenton, M.B. T.H. Kunz. 1977. Movements and depiction of a typical captive Jamaican fruit & behavior. In Biology of the Bats of the New bat. However, we emphasize that they may be World Family Phyllostomidae. Part II. (R.J. Bak- useful in determining patterns during hours in er, J.K. Jones, Jr. & D.C. Carter, eds.). Special which bats are most active. Future experi- Publications, The Museum, Texas Tech Univer- ments might expand to 24-h behavioral ob- sity Press 13:351-364. servations for a more complete understanding Fleming, T.H. & E.R. Heithaus. 1981. Frugivorous of captive Jamaican fruit bat time budgets. bats, seed shadows, and the structure of tropical Other experiments may include tagging and forest. Reproductive Botany 13:45-43. monitoring specific bats to better elucidate be- Gorog, A. 1999. Artibeus jamaicensis. Di- versity 3 2006 at http:// havioral trends, and visibly marking the males Web. Accessed May animaldiversity.ummz.umich.edu/site/accounts/ to determine if a social structure exists within information/Artibeus-jamaicensis. the colony. Heffner, R.S., G. Koay & H.E. Heffner. 2003. These data suggest that captive colonies of Hearing in American leaf-nosed bats. Ill: Arti- Jamaican fruit bats will maintain their natural beus jamaicensis. Hearing Research 184:113- habits despite unnatural surroundings (i.e., a 122. zoo enclosure and reverse-lighting). Addition- Holland, R.A., D.A. Waters & J.M.V. Rayner. 2004. ally, because all of these Jamaican fruit bats Echolocation signal structure in the megachirop- were born in captivity, our data suggest that teran bat Rousettus aegypticus Geoffroy 1810. 207:4361- they have retained innate behaviors even un- Journal of Experimental Biology 4369. der these unnatural conditions. We, therefore, Johnson, J.B., M.A. Menzel, J.W Edwards & W.M. suggest that captive Jamaican fruit bat behav- Ford. 2002. A comparison of two acoustical bat ioral studies emulate behaviors of natural may survey techniques. Wildlife Society Bulletin 30: bat populations. For wildlife biologists and 931-936. zoologists, further behavioral studies of cap- Kunz, T.H., P.V. August & CD. Burnett. 1983. tive populations, like those suggested, may as- Harem social organization in cave roosting Ar- sist in making management decisions for wild tibeus jamaicensis (Chiroptera: Phyllostomidae). populations of Jamaican fruit bats. Biotropica 15:133-138. Marimuthu, G. 1984. Seasonal changes in the pre- ACKNOWLEDGMENTS cision of the circadian clock of a tropical bat un- der natural photoperiod. Oecologia 61:352-357. We thank Greg Bockheim, former Director Morrison, D.W 1978. Foraging ecology and en- of the Potawatomi Zoo (South Bend, Indiana) ergetics of the frugivorous bat Artibeus jamai- for allowing this study to be conducted. We censis. Ecology 59:716-723. especially thank zookeeper Gretchen Pitzer Morrison, D.W. 1979. Apparent male defense of and the zoo staff for their gracious assistance tree hollows in the fruit bat, Artibeus jamaicen- sis. Journal of Mammalogy 60:11-15. throughout the project. Maria Mazzillo and Novick, A. 1963. Orientation in Neotropical bats Kirsten Jackson also assisted with data collec- II: Phyllostomidae and Desmodontidae. Journal tion. The University of Notre Dame Environ- of Mammalogy 44:44-57. mental Research Center (UNDERC) and the Ortega, J. & H.T. Arita. 1999. Structure and social University of Notre Dame Department of Bi- dynamics of harem groups in Artibeus jamaicen- ological Sciences provided recording equip- sis (Chiroptera: Phyllostomidae). Journal of ment and supplies for this research. Mammalogy 80:1 173-1 185.

Ortega, J. & I. Castro- Arellano. 2001. Artibeus ja- LITERATURE CITED maicensis. Mammalian Species 662:1-9. von Herbert, H. 1985. Echoortungsverhalten des Corben, C. 2003. Analook. Version 4.9g. Comput- flughundes Rousettus aegypticus (Megachirop- er software. tera). Zeitschrift fauur Sauaugetierkunde 50:141- Erkert, H.G. 1978. Sunset-related timing of flight 152. activity in Neotropical bats. Oecologia 37:59- 67. Manuscript received 16 September 2006, revised 6 Erkert, H.G. & S. Kracht. 1978. Evidence for eco- February 2007.