Activity Patterns of Costa Rican Bat Species Orsi 1 Activity Patterns of Costa Rican Bat Species Nicole Orsi Department of Biological Sciences University of California, San Diego EAP Tropical Biology and Conservation Program, Fall 2017 14 December 2017 ABSTRACT In Costa Rica, bats are important nocturnal pollinators and seed dispersers. In this study, I investigated how diet type, species, levels of moonlight and moon phases, and nightly weather influenced the activity of bats. To do this, I used mist nets and an ultrasound detector for 11 nights to capture bats and record their species, sex, diet, and forearm length. Each night two to four mist nets were open from 17:30 to 20:00 and checked at 20 minute intervals. Nets were placed in Bajo del Tigre, the Monteverd e Institute, San Luis, the Crandell Memorial Reserve, and La EstaciÃ³n BiolÃ³gica Monteverde . I compared the time of each bat captured in terms of species and diet, and the number of individual bats captured per night to the corresponding moon phase, moon al titude, and weather. Of 23 total bats caught, 9 were different species. I found no clear species specific activity patterns. When comparing data across different diet types (insectivore, frugivore, nectarivore), there was a clear pattern of insectivore act ivity peaking around 18:00, nectarivore activity around 19:00, and frugivore activity occurring throughout the mist netting period. This finding is corroborated by the fact that peak insect activity occurs immediately after sunset and is therefore the opti mal feeding time for insectivores. The activity of nectar bats could be correlated with what time the desired flower opens. As for frugivorous bat, fruits are a widely available and stable food source which could explain their generalized activity. With re gard to moonlight, more bats were captured during periods with less moonlight. This finding is described by which is exhibited in some animals due to decreased prey availability and higher susceptibility to predation. Finally, there was some indication that the previous weather had an effect on bat activity the following night. Patrones de Actividad de las Especies de MurciÃ©lagos Costarricenses RESUMEN En Costa Rica, los murciÃ©lagos son importantes polinizadores nocturnos y dispersores de semillas. En este estudio, investiguÃ© cÃ³mo el tipo de dieta, las especies, los niveles de luz de la luna y las fases de la luna, asÃ como el clima nocturno influyeron e n la actividad de los murciÃ©lagos. Para hacer esto, utilicÃ© redes de neblina y un detector de ultrasonido durante 11 noches para capturar murciÃ©lagos y registrar su especie, sexo, dieta y longitud del antebrazo. Cada noche, dispuse dos o cuatro redes de ni ebla entre 17:30 a 20:00 de la noche y las revisÃ© en intervalos de 20 minutos. ColoquÃ© las redes en Bajo del Tigre, el Instituto Monteverde, San Luis Arriba y San Luis Abajo, la Reserva Crandell Memorial y La EstaciÃ³n BiolÃ³gica Monteverde. ComparÃ© la hora en la que cada murciÃ©lago fue capturado en tÃ©rminos de especies y dieta, y el nÃºmero de individuos capturados por noche a la fase lunar correspondiente, la altitud de la luna y el clima.
Activity Patterns of Costa Rican Bat Species Orsi 2 De 23 murciÃ©lagos capturados en total, 9 fueron especies diferentes. No encontrÃ© patrones de actividad claros especÃficos. Al comparar datos entre diferentes tipos de dieta (insectÃvoro, frugÃvoro, nectarÃvoro), hubo un patrÃ³n claro de actividad insectÃvora que alcanzÃ³ un mÃ¡ximo alrededor de las 18:00, actividad nectarÃvor a alrededor de las 19:00, y actividad de frugÃvoros durante todo el perÃodo de las redes de neblina. Este hallazgo se corrobora por el hecho de que la actividad pico de los insectos ocurre inmediatamente despuÃ©s de la puesta del sol y, por lo tanto, es el tiempo de alimentaciÃ³n Ã³ptimo para los insectÃvoros. La actividad de los murciÃ©lagos nectarÃvoros podrÃa correlacionarse con a quÃ© hora se abren las flores. En cuanto al murciÃ©lago frugÃvoro, las frutas son una fuente de alimento estable y ampliamente disp onible que podrÃa explicar su actividad generalizada. Con respecto a la luz de la luna, capturÃ© mÃ¡s murciÃ©lagos durante perÃodos con menos luz de la luna. Este hallazgo se describe por la "fobia lunar" que se presenta en algunos animales debido a la menor disponibilidad de presas y una mayor susceptibilidad a la depredaciÃ³n. Finalmente, hubo algunos indicios de que el clima de la noche anterior afectÃ³ la actividad de los murciÃ©lagos la noche siguiente. In Costa Rica, the most diverse group of mammals is the order Chiroptera, comprising of 109 bat species that represent more than half of the 216 other mammal species in the country (Wainwright , 200 7). It is commonly known that bats are nocturnal creatures and therefore most active at night, but at what poin ts during the night? Do all bats have similar periods of activity? Does activity differ between bats with specific diets? Is there a peak activity time for various species? Do bats change their activity as moon phases change? Is activity affected by moon i llumination or altitude throughout a single night? How does bad weather affect a activity? One factor that influences activity is a bat food source and how obtained. Chiropterans have very diverse diets, ranging from fruits, nectar and polle n, insects, other animals, or solely blood in the case of vampire bats. Some of these diets may be more accessible as compared to those available only during a specific time of day. Past studies found that in the case of insectivorous bats, most activity o ccurs in the first few hours after sunset when insect abundance is highest (Boonman et al., 2013). However, some species within the largest bat family in the new world, Phyllostomidae (Leaf Nosed Bats), c an be active all night (La Val , 1970 ). This may be d ue to having a food source that is more widely available and less time sensitive, such as fruit. Contrary to the common misconception that bats are blind, many bats not only use echolocation but also vision for targeting their food source or foraging are a (Gonzalez Terrazas et al, 2016). When employed simultaneously, bats can use vision for locating large objects such as landmarks or trees, and echolocation for honing in on small objects such as prey or flowers (Gonzalez Terrazas et al, 2016). Bats also u se echolocation to maneuver their surroundings by making a sound and interpreting distance by hearing how quickly the sound bounces back (Cancel, 1998). Echolocation is done using ultrasonic frequency which ranges from 20 to 200 kHz and is too high for hum ans to hear (Cancel, 1998). Using specific devices that can detect ultrasonic frequencies and translate them into audible forms, echolocation calls could be monitored to determine the activity level of bats that are not easily seen or caught.
Activity Patterns of Costa Rican Bat Species Orsi 3 Another factor affecting bat activity is moonlight. The amount of light in the night sky increases as the moon becomes fuller , which may influence prey availability and/or increase a risk of being preyed upon (Lang et al., 2006). According to Morrison (1978), this idea may explain the trend of among bats, which is characterized by decreased activity with full moons and higher activity with new moons. For example, the Jamaican fruit bat ( Artibeus jamaicensis ) in Panam Ã¡ reduces its time flying in bright moonlight by only taking long flights during the new moon period (Morrison, 1978). In addition, the Jamaican fruit bat was recorded foraging continuously during nights of the new moon period but remained in its roost when the moon peaked during the full moon period (Morrison, 1978). The exact reason for nar is unknown but is assumed to be species specific and correlated with prey availability and susceptibility to predation by snakes, birds, and some mammals (La ng et al., 2005). Variations in resource abundance (especially temporal variation in food availability), weather, temperature, wind, and moonlight all potentially impact bats. How do activity patterns differ with these variables? How do activity pattern s differ among bat species, bats with various diets, with levels of moonlight and across moon phases, and depending on nightly weather? Based on studies that found peak insect activity occurring immediately after sunset, I expected all insectivorous specie s to peak in activity earlier in the night and to be less active when the moon was full. Regardless of species, I expected larger bats to be more active than smaller bats during nights with a full moon. In a single night, I believed bat activity would incr ease when the altitude was lower. I also predicted that fruit bats would have a continuous span of activity because fruits are present all night, whereas nectar bats may have a more distinct active period depending on when certain flowers open at ni ght. Lastly, I expected that nights with more wind and rain would have less activity overall than nights with mild weather because bats might struggle to fly in strong wind and the mist nets are more easily detectable when weighed down by rainwater. METH ODS AND MATERIALS To measure bat activity across a single night, I used mist nets to capture low flying bats and an ultrasound detector to listen for bats that fly higher and are less likely to be captured in the nets. I set up mist nets, untangle d bats from the nets, and handled, identified, measured, and released bats. I set up mist nets in Bajo del Tigre (20 November), the Monteverde Institute (22 November), San Luis (24 & 25 November), the Crandell Reserve (26, 27, & 28 November), and La EstaciÃ³n Biol Ã³gica Monteverde (29, 30 November, & December 2). I mist netted for a total of 11 days and 1080 meters mist net hours. Each night we set up mist nets by 5PM, opened them around 5:30PM, and closed them around 8:00PM. I selected this time because bat activ ity begins after sunset and continues throughout the night. Nets were checked every 20 minutes. Each time I untangled a bat from a net, I recorded the time, general weather, the species, sex, diet and forearm length (in millimeters), and categorized bats as small (30 40 mm), average (40 50 mm), or large (50+ mm) based on the forearm length measurement. Half way through the project I began checking for evening bat calls using an ultrasound detector at 60 70 kHz. I also checked for bat sounds (5 minutes at a time) in between checking the nets.
Activity Patterns of Costa Rican Bat Species Orsi 4 After 11 days of mist netting, I compared the time of each species caught, checked for peak activity times, and analyzed how species differed from one another. I also checked for a correlation between activity a nd moon data by comparing the number of individual bats captured per night to the corresponding moon phase, illumination, time of moonrise/moonset, and altitude of the moon every 20 minutes for a given night. Each phase lasts about one week so I considered the number of bats captured within that week to be related to the current moon phase. I did this with every data except November 5th because I did not gather data again until 15 days following that night which would leave out two complete weeks of potential bat captures and moon phases to find any correlation between. In addition to the moon phases, I standardized the various weather conditions of each nights into four categories: good, fairly good, fairly bad, and bad. Good night s were clear and not too cold, fairly good was slightly windy, fairy bad was chilly and misty, bad was very windy and raining. I made a table with the date, number of individual bats caught, and nightly weather category. In order to look for a correlation b etween specific species and activity patterns, I graphed what time each species was caught from 5:30PM to 8PM, totaled from every night. In order to compare how activity patterns, differ depending on diet type, I graphed what time a species from the three diet types in the area was caught during the mist netting period . RESULTS Figure 1. of Species Captured Over
Activity Patterns of Costa Rican Bat Species Orsi 5 Of the 11 nights I mist netted, 23 total bats were caught, there were 9 different species, and 1 unidentified bat was heard using the ultrasound detector. Figure 1 contains the combined data points for nightly patterns of activity of each captured species across all 11 nights of mist netting. There does not appear to be a clear pattern between species because many species appeared once or twice in the study period. Figure 2. Activity by Figure 2 represents the combined number of bats captured in terms of their diet across all 11 nights of mist netting. There are three distinct patterns that can be seen in this graph. More insect eaters were captured at 18:00 than the rest of the sampling period a nd more nectarivores were captured around 19:00 (Shapiro Wilk test p < 0.001). Fruit eating bats were captured the most often and consistently throughout the night.
Activity Patterns of Costa Rican Bat Species Orsi 6 Figure 3. of Bats Caught During Each Moon Figure 3 represents the number of individual bats captured during three consecutive moon phases: New Moon (17 24 November), First Quarter (25 November 1 December), and Full Moon (2 December). As the figure shows, all 14 bats that were caught a fter the preliminary observations occurred during periods with less moonlight while not a single bat was caught during the full moon phase. I classified each phase as starting the day before the official moon period (for example, Full Moon started 2 Decemb er but the full moon occurred on 3 December) because the amount of light before a specific moon phase is more similar to that of the actual phase.
Activity Patterns of Costa Rican Bat Species Orsi 7 Table 1. Weather Category Color Symbol Good Fairly Good Fairly Bad Bad Table 2. and number of bats caught each Date (DD/MM) Individuals Caught Weather 20/11 4 22/11 2 24/11 1 25/11 0 26/11 4 27/11 1 28/11 1 29/11 1 30/11 0 2/12 0 The following tables show the dates, number of individual bats captured, and weather for each day. According to Table 2, bat activity may be correlated with weather from the previous night. For example, bad weather nights precede nights of low catches, e ven if that day's weather is more mild . In another example, the one night with weather preceded the night with four bat captures which had weather.
Activity Patterns of Costa Rican Bat Species Orsi 8 DISCUSSION These results corroborate findings from the research mentioned previously, such as insectivorous activity peaking earlier in the night due to the increased presence of insects (Boonman et al., 2013 ). Results similarly showed that nectar bats appear to be active in a short, specific period during the night, perhaps correlating to the blooming of a particular nocturnal flower. Future studies should consider swabbing these bats for pollen to attempt to identify which flowers they visit and what times they bloom. Related future studies could t est if these flowers had any other visitors besides bats. In a continuation of this study, researchers could evaluate the specialization level of nectar bats and if they visit many flowers or just one/a few species. My results also reveal the lack of time specificity within fruit eating bats which is show n in Figure 2. This is likely due to the fact that fruits are a more stable and stationary food source compared to time sensitive flowers and insects. My results also reveal the phenomenon of phobi among bats. Across the three lunar phases, there was a clear correlation of increased bat activity with decreased moonlight. Whether prey activity or threat of predation causes this trend, bats are less active when the moon is full regardless of body si ze (Lang et al., 2006). I originally hypothesized that larger bats may be more active during nights with more moonlight compared to small bats because they can be fruit eaters and fruit is not affected by moonlight. However, data showed that for nights wit h more than one capture, bats had very similar forearm lengths and there was a general decrease in bats caught when the moon was becoming fuller. Also , there did not appear to be any correlation between moon altitude and hourly bat activity. For example, S turnira ludovici was the most frequently captured species and appeared continuously throughout the night, regardless of moon altitude. Future studies might continue mist netting for a month to compare the number of bats caught over an entire lunar month an d whether lunar phase or weather patterns influence bat activity more. The most surprising result was increased bat activity during nights with fairly bad weather, as compared to nights with good weather. Moonlight could have caused this pattern rather than weather because as the weather was getting w or se, the moon was be c oming more full . Despite this, the results suggest it is plausible that bats determine their nightly activity based on the previous weather. The overall number of bats captured could also decrease as the climate gets colder. For example, in climates that reach freezing temperatures, some bats migrate or enter a state of torpor which slow s down bodily functions and save s energy for periods of a few hours to a month ( or About the single bat observed at 70 kHz with the ultrasound detector, I could not identify the species. However, the call occurred at 6:03PM and minutes later at 6:12PM a Myotis pilosatibialis bat was captured in the net and could very possibly have been the same bat that was heard making the calls. Error in my results might stem from the bias of using mist nets and the non specificity of ultrasound detectors. Mist nets only targ et bats that fly low enough to get caught and do not work well in storms due to heightened detectability when wet. Identifying bats heard on the ultrasound
Activity Patterns of Costa Rican Bat Species Orsi 9 detector poses difficulties (and was impossible in this study), but knowing whether a bat is nearby based on its call still provides useful information. ACKNOWLEDGEMENTS: I would like to give a huge thanks to Federico Chinchilla for all his help during this research project. Thank you for going out of your way to help me despite how challenging my ori ginal project was. Thank you for encouraging me to try my ideas despite that fact that what I wanted to do was difficult. Thank you for all the phone calls you made and for driving me around town to get supplies for my project. Thank you for all your hard work in trying to find vampire bats with me never forget herding cattle down that mountain and trying to keep them from leaving the pasture. Thank you for staying out in the cold rain with Shilah and I and for telling scary stories with us. Thank you for always being so positive and fun in what was an otherwise stressful time. The experiences I gained from working with you are something I will take with me and cherish for the rest of my life. Thank you for everything! I would also like to give thanks to Shilah and Yibing for being great company to work with every night, Frank Joyce for all his advice and wisdom, the veterinarian from Santa Elena for getting us in touch with a farm, the Dairy Farm in Monteverde for letting me use their blood, and most of all the two cows that donated blood for my failed vampire bat project. Shout out to Miguel for being a last minute phlebotomist, to Kara for helping me with my graphs, and to Sierra for reviewing my paper and waking me up every morning. Thank you to AndrÃ©s and FÃ©lix for all the memes. Thank you to Macho Leton and Wagner GonzÃ¡lez for letting us se t up mist nets on their farms. And lastly thank you to la fami lia Alvarado and la EstaciÃ³n BiolÃ³gica for housing and feeding me and to the Montev erde Institute for letting me use the Fox Maple building to set up my original project. LITERATURE CITED Adams, A. M. 2013. Assessing and analyzing bat activity with acoustic monitoring: challenges and interpretations . The School of Graduate and Postdoctoral Studies the University of Western Ontario London, Ontario, Canada, pp. 1 194. Boonman, A., Bar On, Y., Cvikel, N., Yovel, Y. 2013. It's not black or white on the range of and echolocation in echolocating bats. Fronti ers in Physiology . NCBI, doi:10.3389/fphys. 2013.00248. Cancel, J. 1998. Frequency of Bat Sonar . The Physics Factbook , hypertextbook.com/facts/ 1998/JuanCancel.shtml Gonzalez Terrazas, T. P., Martel, C., Milet Pinheiro, P., Ayasse, M ., Kalko, E. K. V., Tschapka, M. 2016. Finding flowers in the dark: nectar Feedi ng bats integrate olfaction and echolocation while foraging for nectar. Royal Society Open Science , 10 Aug. NCBI , doi:10.1098/rsos.160199. or Migrate National Parks Service, U. S. Departme nt of the Interior, www.nps.gov/subjects/bats/hibernate or migrate.htm. La Val, R. K. 1970. Banding Returns and Activity Periods of Some Costa Rican Bats. The Southwestern Naturalist , 15 (1): 1 10, 1 June, JSTOR , doi: 10.2307/3670196.
Activity Patterns of Costa Rican Bat Species Orsi 10 Lang, A. B., Kalko, E. K., RÃ¶mer, H., Bockholdt, C., Dechmann, D. K. 2006. Activity levels of bats and katydids in relation to the lunar cycle. Oecologia , 146 (4): 659 666, Jan., pp. 659 666 . SpringerLink , doi:10.1007/ s00442 005 0131 3. Morrison, D. W. 1978. Lunar phobia in a neotropical fruit bat, Art ibeu s jamaicensis (Chiroptera: Phyllostomidae). Animal Behaviour, 26 (3): 852 855, Aug., pp. 852 855 . ScienceDirect , doi:10.1016/0003 3472(78)90151 3. Wainwright, M. 2007. The Mammals of Costa Rica . Zona Tropical. pp. 75 77. APPENDIX Bats captured: Family: Phyllostomidae, Subfam: Phyllostominae Micronycteris shmidtorum Large Eared Bat) Diet: Gleaning insectivore Caught (date, time, location): 11/26 CR @ 6:00 FA: 34 mm Sex: M Family: Phyllostomidae, Subfam: Glossophaginae Glossophaga soricina Long Tongued Bat) Diet: Nectarivore; sometimes pollen, fruit insects, flower parts Caught (date, time, location): 11/24 SL @ 7:05 F A: 37mm Sex: M Notes: active just after dusk and just before (LaVal, 149 MurciÃ©lagos de Costa Rica). Hylonycteris underwoodi Long Tongued Bat) Diet: Nectarivore; sometimes pollen, insects, and fruit Caught (date, time, location): 11/29 EB @ 6:50 FA: 35 mm Sex: M Family: Phyllostomidae, Subfam: Carollinae Carollia brevicauda (sowelli) (Silky Short Tailed Bat). caught twice Diet: Frugivore, occasionally insects Caught (date, time, location): 11/5 EB by 7:30, 11/26 CR @ 7:55 FA: 40 mm, 40 mm Sex: NA, M
Activity Patterns of Costa Rican Bat Species Orsi 11 Carollia perspicillata Short Tailed Bat). Caught twice Diet: Frugivore, occasionally nectar and insects Caught (date, time, location): 11/20 BT @ 6:15, 11/20 BT @ 7:00 FA: 40 mm, 39 mm Sex: F, M Family: Phyllostomidae, Subfam: Stenodermatinae Artibeus lituratus (Big Fruit Eating Bat) Diet: Frugivore; occasionally nectar, pollen, leaves, and insects Caught (date, time, location): 11/27 CR @ 6:05 FA: 67 mm Sex: M Artibeus toltecus (Toltec Fruit Eating Bat). Caught three times Diet: Frugivore Caught (date, time, location): 11/5 EB by 7:30, 2x 11/20 BT @ 6:15 FA: 40 mm, 40 mm, 41 mm Sex: NA, F, M Sturnira ludovici (hondurensis) ( Highland Yellow Shouldered Bat). caught five times Diet: Frugivore Caught (date, time, location): 11/5 EB by 7:30, 11/22 MVI @ 6:55, 11/22 @ MVI @ 7:25, 11/26 CR @ 6:35, 11/26 CR @ 7:15 FA: 43 mm, 45 mm, 45 mm (juvenile), 44 mm, 47 mm Sex: NA, F, M, F, M Family: Vespertilionidae Myotis pilosatibialis (formally M. keaysi) (Hairy Legged Myotis) Diet: Aerial insectivore Caught (date, time, location): 11/28 CR @ 6:12 FA: 38 mm Sex: M
Activity Patterns of Costa Rican Bat Species Orsi 12 Notes: 11/28 likely the bat heard at 6:03 @ 70 kHz (insect eater) Family Subfamily Species Common Name Diet Caught (date, time, location) Forearm Length (mm) Sex Notes Phyllostomidae Phyllostominae Micronycteris shmidtorum Large Eared Bat Gleaning insectivore 11/26 CR @ 6:00 34 M Glossophaginae Glossophaga soricina Long Tongued Bat Nectarivore; sometimes pollen, fruit insects, flower parts 11/24 SL @ 7:05 37 M Most active just after dusk and just before (LaVal, 149 MurciÃ©lagos de Costa Rica) Hylonycteris underwoodi Long Tongued Bat Nectarivore; sometimes pollen, insects, and fruit 11/29 EB @ 6:50 35 M Carollinae Carollia brevicauda (sowelli) Silky Short Tailed Bat Frugivore, occasionally insects 11/5 EB by 7:30, 11/26 CR @ 7:55 40, 40 NA, M Carollia perspicillata Short Tailed Bat Frugivore, occasionally nectar and insects 11/20 BT @ 6:15, 11/20 BT @ 7:00 40, 39 F, M Stenodermatinae Artibeus lituratus Big Fruit Eating Bat Frugivore; occasionally nectar, pollen, leaves, and insects 11/27 CR @ 6:05 67 M Artibeus toltecus Toltec Fruit Eating Bat Frugivore 11/5 EB by 7:30, 2x 11/20 BT @ 6:15 40, 40, 41 NA, F, M Sturnira ludovici Bat; Highland Yellow Shouldered Bat Frugivore 11/5 EB by 7:30, 11/22 MVI @ 6:55, 11/22 @ MVI @ 7:25, 11/26 CR @ 6:35, 11/26 CR @ 7:15 43, 45, 45 (juvenile), 44, 47 NA, F, M, F, M Vespertilionidae Myotis pilosatibialis (formally M. keaysi) Hairy Legged Myotis Aerial insectivore 11/28 CR @ 6:12 38 M 11/28 likely the bat heard at 6:03 @ 70 kHz (insect eater)