Relating wing loading and ear size to bat diet types

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Relating wing loading and ear size to bat diet types

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Relating wing loading and ear size to bat diet types
Translated Title:
Relacionando carga alar y tamaño de oreja con tipo de alimentación en murciélagos
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McGuinness, Shilah
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Bats ( lcsh )
Murciélagos ( lcsh )
EAP Fall 2017
EAP Otoño 2017
Costa Rica--Puntarenas--Monteverde Zone
Costa Rica--Puntarenas--Zona de Monteverde
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Reports

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Abstract:
Bats have one of the widest diet varieties in the animal kingdom. With these varying diet niches, each bat species experiences a different set of evolutionary pressures from its ecological interactions. This study assessed the variation in wing and ear morphology in bats and how these values compare with their varying diet types, in order to assess the ecological specificity that these species have evolved. I set up mist nets over a series of two weeks and captured a total of 17 bats from 9 species, conducting a series of measurements to calculate the total wing area and ear/weight ratio of each bat. The results showed statistical significance in the larger ear sizes found in insectivores when compared to other diet types captured. Additionally, the wingloading of the insectivores was significantly smaller than those of nectarivorous and small fruit eaters, and the high wingloading of the large fruit eater was also shown to be significant. Overall, these results correlated with the known ecology of these bat species, as insectivores need less agility to forage for prey in the open than frugivorous and nectarivorous bats searching in the vegetation. Furthermore, because insectivore prey is in motion, it makes sense that their echolocation abilities are heightened in comparison to those species with diets involving sessile food sources. ( , )
Abstract:
Los murciélagos presentan dietas muy variadas. Relacionado a esto, cada especie de murciélago experimenta presiones evolutivas e interacciones ecológicas que moldean su anatomía. Este trabajo mira la variación en el tamaño y morfología de las alas y las orejas, y su relación con sus dietas específicas. Yo usé redes de niebla en el bosque durante dos semanas, y capturé diecisiete murciélagos de nueve especies. Hice cálculos del área alar total y estimé la relación del largo de la oreja/peso corporal de cada murciélago. Los resultados muestran que los murciélagos insectívoros tienen orejas significativamente más largas que las especies con otras dietas diferentes. La carga alar las especies insectívoras fue menor que la carga alar de las especies nectarívoras y frugívoras, en particular la carga alar de la especie frugívora más grande (Artibeus lituratus) fue mucho mayor. En total, estos resultados son consistentes con la ecológica de los murciélagos en este estudié. Las especies insectívoras necesitan menos agilidad al forrajear para capturar insectos, que las especies frugívoras y nectarívoras que requieren buscar frutos y flores entre la vegetación. Además, debido a que los insectos son presas en movimiento, los murciélagos insectívoros deben ecolocalizar más intensamente.
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Student affiliation: Department of Ecology and Evolutionary Biology, University of California, Los Angeles.

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Monteverde Institute
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Monteverde Institute
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M39-00651 ( USFLDC DOI )
m39.651 ( USFLDC Handle )

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Wing and Ear Morphology of Bats McGuinness 1 Relating wing loading and e ar s ize to b at d iet t ypes Shilah McGuinness Department of Ecology and Evolutionary Biology University of California, Los Angeles EAP Tropical Biology Program, Fall 2017 15 December 2017 _____________________________________________________________________________ ABSTRACT Bats have one of the widest diet varieties in the animal kingdom. W ith these varying diet niches, each bat species experiences a different set of evolutionary pressures from its ecological interactions. This study assessed the variation in wing and ear morphology in bats and how these values compare with their varying die t types, in order to assess the ecological specificity that these species have evolved I set up mist nets over a series of two weeks and captured a total of 17 bats from 9 species, conducting a series of measurements to calculate the total wing area and ear/weight ratio of each bat. The results showed statistical significance in the larger ear sizes found in insectivores when compared to other diet types captured. Additionally, the wingloading of the insectivores was significantly smaller than those of ne ct ar ivorous and small fruit eaters, and the high wingloading of the large fruit eater was also shown to be significant. Overall, these results correlated with the known ecology of these bat species, as insectivores need less agility to forage for prey in t he open than frugivorous and nec tarivorou s bats searching in the vegetation Furthermore, because insectivore prey is in motion, it makes sense that their echolocation abilities are heightened in comparison to those species with diets involving sessile foo d sources. __________________________________________________________________ Relacionando carga alar y tamao de oreja con tipo de alimentacin en murcilagos RESUMEN Los murcilagos presentan dietas muy variadas. Relacionado a esto, cada especie de murcilago experimenta presiones evolutivas e interacciones ecolgicas que moldean su anatoma. Este trabajo mira la variacin en el tamao y morfologa de las alas y las orejas, y su relacin con sus dietas especficas. Yo us redes de niebla en el bosque durante dos semanas, y captur diecisiete murcilagos de nueve especies. Hice clculos del rea alar total y estim la relacin del largo de la oreja/peso corporal de cada murcilago. Los resultados muestran que los murcilagos insectvoros tienen orejas significativamente ms largas que las especies con otras dietas diferentes. La carga alar las especies insectvoras fue menor que la carga alar de las especies nectarvoras y frugvoras, en particular la carga alar de la especie frugvora ms grande ( Artib eus lituratus ) fue mucho mayor. En total, estos resultados son consistentes con la ecolgica de los murcilagos en este estudi. Las especies insectvoras necesitan menos agilidad al forrajear para capturar insectos, que las especies frugvoras y nectarvo ras que requieren buscar frutos y flores entre la vegetacin. Adems, debido a que los insectos son presas en movimiento, los murcilagos insectvoros deben ecolocalizar ms intensamente. __________________________________________________________________

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Wing and Ear Morphology of Bats McGuinness 2 Bats in Costa Rica are known to have a wide range of diets, whether they are insectivores, frugivores, nectarivores, blood feeders, carnivores, fish eaters or a combination of these diet types (Janzen 1983). Due to these varying food sources bats occupy different ecological niches and thus forage through differen t parts of their environment. It is likely that these diet specific environmental pressures lead to the morphological differences between bat species. This study will be looking at the vari ation in flying area and ear morphology in bats and how these values compare with their varying diet types, in order to assess the ecological specificity that the species have evolved as a result of their ecology ly related to their ability to maneuver through their environment (Marinello 2014). And since their purpose for much of their movement is foraging behavior their w ing morphology highly relates to foraging strategy ( Altringham1996 ). One way to assess the ability of the bat to navigate thr ough its environment is by calculating its wingload (Altringham 1996) Wing load is a numerical value that relates the size a bat with its total wing area. This value demonstrates the navigation and carrying ability of the bat : bats with higher wingload values have a greater ability to maneuver through the forest and carry food while flying, but less of an ability to maintain a fast flight The reverse is true for a smaller wingload Wing loading for bats is represented by the weight of the bat divided by the total area of the flight membrane ( Altringham 1996 ). Since evolution ary pressures are constantly working how it feeds An a dditional morphological characteristic with potential diet specificity assessed in this study is ear size Ear size highly correlates with the echolocation abilities of a bat (Wainright 2007) Larger ears mean heightened echolocation skills, and therefore a better ability for the bat to sense its surroundings. Some bats need to find motile prey while others seek food that remains still, such as flowers or fruits. Will these varying food traits be reflected in the ear morphology of bats eating them? Overall, t he obj ective of this study is to see if there is a distinct correlation between a both ear size and wingload related to their diet Bats are important for the ecosystem; they function as predators, pollinators seed dis persers and more If a distinct pattern can be found among diet type and morphology, it will be indicative of the ecological role of each bat in its community. MATERIALS AND METHODS From November 20 th to December 2 nd 2017 I set up four mist nets nightly at six different study sites throughout Monteverde, Costa Rica. These locations include d San Gerardo, Bajo d el Tigre, Monteverde Institute g ardens, Rachel and Dwight Crandell Memorial Reserve, Macho Leiton Estacin Biol gica Monteverde Each night we opened two and later four nets for two and a half hours, t otaling 1080 meters mist net hours We lowered the nets at 5:30pm and close them at 8:00pm each night and checked for bats every 20 minutes. If a bat was captured, I untangled it while wearing gloves to protect myself from getting bitten After untangling the bat, I placed it in a canvas bag. For each bat, there were four steps towards acquiring the appropriate data needed for later analysis. The first step was to acquire the weight of the bat in grams. To accomplish this, I made two weight measurements with the spring scale after every capture. The primary measurement was the weight of t he bag while the bat was inside, and the second ary measurement was the weight o f the bag after the bat had been released. By subtracting the weight of the bag from the weight of the bag with the bat inside, I was able to

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Wing and Ear Morphology of Bats McGuinness 3 calculate the weight of each bat in grams The second step necessary after bat capture was to acquire the measurem ents for total membranous wing area. These measurements included length of forearm, the fifth finger, and first finger Some species have more membranous flight material than just the wings; certain species have a membrane between the legs called the uropa tagium. Thus, if a species had an uropatagium I also measured the length of the tibia and calcar to ensure I had enough measurements to calculate the full membranous flight area This area was calculated at a later time. The third step was t he measurement of the ears in order to later look at varying echolocation abilities. And lastly, the fourth step was to identify the species of bat Using the field identification guide by Timm and LaVal (1998 ) I identified the species of bat captured. Prior to releasing the bat, I cut a small portion of their fur on their shoulder in order to identify the bat if it was caught again. With the data obtained membranous flight area of the wings an d uropatagium These area summations included the rectangle made by forearm and fifth finger, the right triangle with sides of fifth finger and first finger, and the rectangle made by the tibia and calcar. After totaling these areas I multiplied the value by two to account for both wings of the bat. Then, using both the total flight area and weight of the bat, I calculated the wing loading of each bat. The formula for wing loading is as follows: Wing loa ding= body mass (g)/wing area (c m 2 ). To analyze the echolocation morphology, I divided the ear length (cm) by weight of the bat (g) to create the Ear/Weight R atio. I created this ratio in order to en sure that the variation in ear size in the data was not solely due to a difference in body size. Statistical analysis of the data was done with the Kruskal Wallis test ( Ambrose & Ambrose 1995 ). This te st was used because it is a non parametric test for differences between means and can analyze groupings with differing quantities of data. This aligns well with th e data sample from this study because a varying number of bats from each diet were captured. RESULTS After 1080 meters mist netting hours, we collected a total of 17 different bats from 9 species. An i n depth listing of each bat speci es caught along with the quantity captured and its diet type can be found i n T able 1. While an overall significance was not found between diet types, t he difference in wingloading between M. pilosatibialis A. literatus and the remainder of the bats was shown to be statistically significant ( KW= 32.22, df=6, p=0.0006, see Figure 1). In addition, it should also be noted that the wingloading value of M. pilosatibialis is half that of M. schmidtorum in Figure 1 ( M. pilosatibialis = 0.0552, M. schmidtorum = 0.1044). The f ull extent of these data values can be found in the Appendix. The Ear/Weight Ratio study showed that the insectivorous bats, M. pilosatibialis and M. schmidtorum had ratio values that were both higher and statistically different than those of the fruit ea ters and nectarivorous bats (KW=53.62, df=2, p<0.05, see Figure 2).

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Wing and Ear Morphology of Bats McGuinness 4 Table 1. A Comprehensive List of Captured Bat Species and Diets Figure 1. Wing load values of highland bat species. Species with multiple bats captured are represented means. A. literatus A. tortecus C. sowelli C. perscipillata S. ludovici G. soricina H. underwoodi M. srimidtorum M. pilosatibialis 0 0,05 0,1 0,15 0,2 0,25 0,3 Wing Loading (g/ cm 2 ) Bat Species insectivore nectivorous frugivore Bat Species Number of Individuals Captured Diet Artibeus literatus 1 fruit Artibeus tortecus 2 fruit Carollia perscipillata 2 fruit Carollia sowelli 3 fruit Glossophaga soricina 1 nectar Hylonycteri s underwoodi 1 nectar Mi c r onycteris schmidtorum 1 gleaning insect Myotis pilosatibialis 1 aerial insect Sturina l udovici 5 fruit

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Wing and Ear Morphology of Bats McGuinness 5 Figure 2. Ear/Weight ratio for each bat species. Species with multiple bat s captured are represented mean values DISCUSSION The morphological features studied, wing area and ear size, both showed to have statistical significance when comparing the diet types within our sample of bat species captured. Beginning with the wing morphology portion of this study, there was a distinct difference between the wing loads of differing species. B oth Myotis pilosatibialis and Micronycteris schmidtorum are insectivores and had the lowest wing loads of all bats caught in this study (Figure 1) M. pilosatibialis is an aerial insect ivore using the legs and tail membrane to capture flying moths and other insects (Reid 1997). This type of predation requires fast and steady flight (Wainwright 2007) Meanwhile, M. schmidtorum is an insect gleaner capturing insects from the dense vegetation (Reid 1997) This foraging strategy requires greater agility than that of an aerial insect eater because it involves searching through the understory for insects rather than sensing them in flight. In addition, s ome bat species of this foraging strategy e ven maintain a hovered flight (Ried 1997). T his known information about bat species ecology mirrors the data from this study; the gleaner species M. schmidtorum had double the wing load value than that of the aerial insectivore M. pilosatibialis (Figure 1) M. schmidtorum potentially underwent selection for wings with greater wingloading and therefore heightened agility because gleaners need advanced maneuverability though the forest vegetation In regard to the nectar eating bats, which include Glossophaga soricina and Hylonycteris underwoodi these species had significantly higher wing loads than the insect eaters (Figure 1) Nectar bats search from flower to flower to find nectar, and hover by the flower while they eat ( Wainwright 1997) This type of foraging and hovering demands higher flight mane uverability than an insectivore, and therefore a higher wingload. The smaller frugivore species captured in this study include Sturnira ludovici Carollia perscipillata Carollia sowelli and Artibeus tortecu s These four species had a slightly higher wingloading than the necta rivoro us bats but not to the point of statistical significance Both necta rivor ous bats and frugivorous bats need to A. literatus A. tortecus C. sowelli C. perscipillata S. ludovici G. soricina H. underwoodi M. srimidtorum M. pilosatibialis 0 0,05 0,1 0,15 0,2 0,25 0,3 Ear/Weight Ratio (cm/g) Bat Species M. srimidtorum H. underwoodi S. ludovici insectivore nectivorous frugivore

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Wing and Ear Morphology of Bats McGuinness 6 fly through difficult vegetation to find their food source, so the l ack of statistical significance between these two diet types is not shocking (Ried 1997) T he Artibeus literatus is the largest bat trapped during our mist netting sessions and has a sta ti sti cally significant higher wingloading value than the rest of the bats we captured (Figure 1) A. literatus is also a frugivore, but of much larger size than the others caught in the mist nets It is known to pluck large fruits and take them back to its perch for feeding, such as whole figs (R ied 1977). This diet explains the larger wingload calculated, not only is the bat flying through difficult forestry to obtain the fruit, it is also carrying a heavy fruit back to its perch. This need for both maneuverability and carrying capacity demands a higher wingload for the morphology of this species The other morphological feature studied was the ear length as a proxy for echolocation efficiency. The Ear/Weight Ratio was calculated in order to negate the effect of body size on the length of ear It should be noted that primarily using forearm as a body size proxy did not result in a significant difference between the diet types. However, s tatistical significance was given to the difference between the Ear/Weight Ratio of the insectivores and those o f other diets captured in this study (Figure 2) Although insectivores have been proven to be able to capture insects solely based on eyesight, their enhanced ears give way to advanced echolocation abilities (Wainwright 2007) This diet requires the detect ion of small objects in motion, a much more difficult task than finding a stagnant fruit or flower as would frugivores and nectarivores Although this study aimed to capture bats from a large sample of the diets known to be represented in Costa Rica, the re is a large bias towards specific bats in the mist net procedure for capturing bat species (Kunz 1996 ). Mist nets can favor the capture of bats of particular diets, for example, Handley (1967) reported more fruit bats captured than those of any other die t. Overall, this study showed a significant morphological difference in both ear size and wingload for insectivorous bat species M. pilosatibialis and M. schmidtorum, and a significantly large wingload for A. literatus and small wingload for M. pilosatibialis and M. sch m idtorum This data correlates with the known ecology of these species, and thus shows that the ecological pressures have caused morphological specification in bats of differing diets. LITERATURE CITED Ambrose, H. W., & Ambrose, H. W. 1995. A handbook of biological investigation (5th ed.). Winston Salem, NC: Hunter Textbooks. Handley, C. O., Jr. 1967. Bats of the canopy of an Amazonian forest. Atlas do Simposio sobre Biota Amazonica: Zoologica, 5, 211 215. Janzen, D. H. (Ed.). 1983. Costa Rican Natural History. Chicago and London: The University of Chicago Press Kunz, T. H. 1996. Ecological and Behavioral Methods for the Study of Bats. Washington, D.C.: Smithsonian Institution. Altringham J. D. Bats: Biology and Behaviour. Oxf ord: Oxford University Press. Marinello, M. M., & Bernard, E. 2014. Wing morphology of Neotropical bats: a quantitative and qualitative analysis with implications for habitat use [Abstract]. Canadian Journal of Zoology, 92(2), 141 147. doi: https://doi.or g/10.1139/cjz 2013 0127 Reid, F. A. 1997. A Field Guide to the Mammals of Central America & Southeast Mexico. New York, NY: Oxford University Press, Inc.

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Wing and Ear Morphology of Bats McGuinness 7 Timm, R. M. and R. K. LaVal. 1998. A field key to the bats of Costa Rica. Occasional Publication Seri es, University of Kansas Center of Latin American Studies 22:1 30. Wainwright, M. 2007. The Mammals of Costa Rica: A Natural History and Field Guide. Ithaca: Cornell University Press. ACKNOWLEDGEMENTS This project would not have been possible without the help of many people, so I would first like to thank my bat team for keeping morale high even when bat populations were low. Fede thank you for introducing me to world of bats! You have been such a wonderful teacher and friend throughout this whole process Thanks to Nicole for helping me both handle a nd measure the bats A special thank you to Harold for everything he did to help make this project what it is today Thanks, Yibing for being so excited when the bats pooped. I could not have captured bats wit hout the people who graciously allowed me to use their property to set up my nets. So, thank you t his So, Frank Estacin Biolgica Monteverde, Instituto Monteverde, and Macho Leiton., thank you! Lastly, I would like to thank Elliot, Andrs, and Federico for helping me edit this paper and make it the best it could be APPENDIX Appendix 1. Total data collected and calculated from bats caught mist netting over the timespan of November 22 to December 2, 2017. B a t Genus species d i e t weight with bag weight of bag weight (g) forearm (cm) 5th finge r (cm) 1st finge r (cm) tibia (cm) calcar (cm) nose leaf e a r s e x C R T W 1 Artibeus litauratus f 74 17 57 6.70 9.1 12 2.6 0.8 1.4 1 9 m B T 1 Artibeus tortecus f 40 24 16 4.00 6.2 8 1.5 0.4 1.1 1 1 f B T 2 Artibeus tortecus f 42 25 17 4.10 6.1 8.3 2 0.5 1.2 1 2 m B T 3 Carollia perspicillata f 42 25 17 4.00 6.4 8.6 1.9 0.7 1 1 5 f B T 4 Carollia perspicillata f 35 19 16 3.90 6.1 8.9 1.9 0.6 1 1 6 m S G 1 Carollia sowelli f 64 44 20 4.10 6.5 8.8 2 0.7 1.2 1 6 m S G 3 Carollia sowelli f 64 46 18 4.60 7.1 9.7 2 1.1 1 1 9 f C R O 4 Carollia sowelli f 44 24 20 4.00 6.9 9.3 1.8 0.6 1.1 1 7 m S L C 1 Glossoph aga soricina n 37 26 11 3.70 5 7.2 1.7 0.5 0.6 1 2 m S T Hylonyct eris underwoodi n 33 24 9 3.50 4.6 7.1 1.5 0.6 0.6 1 m

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Wing and Ear Morphology of Bats McGuinness 8 A 1 C R O 1 Mircrony cteris schmidtorum i 33 26 7 3.40 4.8 6.3 1.6 1.3 1.1 1 7 m C R T H 1 Myotis pilosatibialis i 28 24 4 3.80 4.7 5.9 1.6 2.8 0 1 1 m M V I 1 Sturnira ludovici f 37 16 21 4.50 6.9 9.2 0 1 1 4 f M V I 2 Sturnira ludovici f 32 19 13 4.50 6.1 8 0 0.8 1 4 m C R O 2 Sturnira ludovici f 43 24 19 4.45 6.4 9.7 0 0.9 1 4 f C R O 3 Sturnira ludovici f 37 16 21 4.70 6.6 9.1 0 0.8 1 6 m S G 2 Sturnira ludovici f 64 45 19 4.40 6.5 8.7 0 0.9 1 1 f t and c calculation fifth forearm calc 1st and fifth triangle (cm2) total flight area (cm2) wing load (g/cm2) 2.08 60.97 54.6 235.3 0.242243944 0.6 24.8 24.8 100.4 0.15936255 1 25.01 25.315 102.65 0.165611301 1.33 25.6 27.52 108.9 0.15610652 1.14 23.79 27.145 104.15 0.15362458 1.4 26.65 28.6 113.3 0.176522507 2.2 32.66 34.435 138.59 0.129879501 1.08 27.6 32.085 121.53 0.164568419 0.85 18.5 18 74.7 0.147255689 0.9 16.1 16.33 66.66 0.135013501 2.08 16.32 15.12 67.04 0.104415274 4.48 17.86 13.865 72.41 0.055240989 0 31.05 31.74 125.58 0.16722408 0 27.45 24.4 103.7 0.12536162 0 28.48 31.04 119.04 0.159610215 0 31.02 30.03 122.1 0.171990172 0 28.6 28.275 113.75 0.167032967


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