! ISSN 2317-6105 Chiroptera Neotropical vol. 19 (3) Special Volume, December – 2013
Chief Editor: Ludmilla M.S. Aguiar Guest Editors: Marco A. R. Mello and Valéria C. Tavares !
Special Volume in honor to Elisabeth Klara Victoria Kalko (1962-2011) !
Elisabeth Kalko at Reserva Michelin (Bahia state, Brazil) in 2009. Photo by Marco Aurélio Mello. Chiroptera Neotropical ISSN 2317-6105
Chief Editor Ludmilla Moura de Souza Aguiar – University of Brasília - Brazil
Executive Editors Ricardo B. Machado – University of Brasília - Brazil Maria João Ramos Pereira – Federal University of Rio Grande do Sul - Brazil
Academic Editors Enrico Bernard – Federal University of Pernambuco – Brazil Carlos Eduardo Lustosa Esberárd – Federal University of Rio de Janeiro - Brazil Marco A. R. Mello – Federal University of Minas Gerais – Brazil Monik Oprea – Federal Univesity of Goiás – Brazil Valéria C. Tavares – Federal University of Minas Gerais - Brazil
Editorial Board Don E. Wilson Wilson Uieda Alfred Gardner Rodrigo Medellin Celia López-Gonzalez Adriano L. Peracchi Luis F. Aguirre Burton K. Lim
Chiroptera Neotropical is a peer-reviewed journal dedicated to publishing articles resulting from original research with bats (Order Chiroptera). Articles may be related to ecology, biology, biogeography and conservation of bat species in the Neotropics. Articles and short communication are published twiece in a year and all text are available for free at www.chiroptera.unb.br. Authors should access Chiroptera’s web site to registers then selfs and to get intructions for publication.
Chiroptera Neotropical 19(3) Special Volume, December 2013
A tribute to our Grand Master
Marco A. R. Mello1 & Valéria C. Tavares2,3
1 Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais. Avenida Antônio Carlos, 6.627. 31270-901 Belo Horizonte, MG, Brazil. E-mail: [email protected]. 2 Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais. Avenida Antônio Carlos, 6.627, 31270-901 Belo Horizonte, MG, Brazil. E-mail: [email protected]. 3 Programa de Pós-Graduação em Genética, Conservação e Biologia Evolutiva, Instituto Nacional de Pesquisas da Amazônia. Av. André Araújo, 2.936, 69067-375 Manaus, AM, Brazil.
Science is one of the most beautiful human Janeiro, Brazil. He sent Eli an e-mail, following cultures. For millennia it has been helping people the advice from Valéria, and asked several understand their place and improve their lives on questions about bat ecology. That was the Earth. Nevertheless, the “Path of the Young beginning of a great mentorship and friendship. In Scientist”, from kindergarten to the PhD, is the first years, Eli was like a fairy godmother: they challenging. A person who wants to be a scientist never met in person, but she was always there, must endure a series of sacrifices, deal positively helping him do his bat research and teaching him with frustration, and work incredibly hard. the “dos” and “don’ts” of science. Only in the Therefore, the challenge to strive in Academia final year of his PhD, in 2005, did Marco get the requires not only developing one’s intellect, but chance to go to Ulm University, Germany, and also taming one’s emotions. work for one year in Eli’s bat group (also known as “Bio 3”). After coming back to Brazil and As in other cutting-edge human cultures, the working at his first postdoc position, Marco went key to walking this path and succeeding in the end back to Ulm in 2009 and worked there until Eli’s is a well-balanced mixture of talent, perseverance, passing. She taught Marco how to overcome the and dedication. But those qualities are not enough: challenges that a young scientist from an one needs also to find good masters on the way, underdeveloped country has to face on a daily who help anticipate the crossroads ahead, in order basis. to choose one’s path wisely, and who help us focus our passion. In that matter, we, the editors of It is impossible to describe with words how this special issue, hit the jackpot: Elisabeth Kalko. fortunate we feel about having been mentored by the Grand Master of bat research. Eli taught us not When Valéria was a Master’s student at the only how to study bats in the field, the lab, and the Federal University of Minas Gerais, Brazil, back computer, but also how to be scientists. Above all, in 1998 she met Eli visiting Bahia for the first she taught us that a professional scientist does not workshop on bat bioacoustics in our country. have to be a taciturn, anti-social, long-faced Valéria was studying the wing morphology and person. Science goes together well with diet of phyllostomid bats in the Atlantic Forest of excitement, joy, and passion. Science “a la Eli” Rio Doce State Park (results of that study are was all about the pleasure of sharing discoveries partially published in this issue). Eli was excited with friends and colleagues who you respect. She about her ideas and prospects. She basically always tried to protect us from the “Dark Side of “shook” Valéria and said: “yes, you can!”. That Academia” and helped us focus on our research. was the starting point for a very shy student to take her first steps in the world of international We learned how to be bat scientists from her science. At that time, Eli stimulated Valéria to go example. By seeing her smile like a child with the to the National Museum of Natural History at the simplest things, such as capturing a Lonchorhina Smithsonian Institute in Washington, U.S.A. bat. By witnessing how she treated everyone Within two months Valéria was introduced to equally, from an undergrad student to the Charles Handley and could visit the mammal university’s president. By hearing her say “wir collection. Her life was never the same after being kriegen es hin!” when we were hopeless, thinking touched by Eli’s magic wand. that our projects were going south. By noticing the value she put in careful observation, thorough The first contact between Marco and Eli was in analysis, and rigorous inference. And, finally, by 1997, when he was an undergrad student in his watching her write a paper with the same mastery fourth term at the Federal University of Rio de ! i Chiroptera Neotropical 19(3) Special Volume, December 2013 as a chef would prepare the most exquisite meal (those who knew her surely remember her passion for food). Three years have passed since the world lost its greatest bat scientist, and it is still incredibly hard to assimilate that she will not be seen walking around with her bat recorders anymore. However, her legacy will endure forever in the literature and in the hearts and minds of the scientists she educated or inspired. In this special issue of Chiroptera Neotropical, we write in her honor. Several bat scientists from Latin America and Europe were invited, and all of them are grateful to Eli for different reasons. She helped so many people in so many ways, that we were surely unable to invite all of her former students and colleagues. We apologize for that and hope everyone can feel a bit represented. We are very grateful to all people who contributed with manuscripts, and especially to Ludmilla Aguiar and Ricardo Machado, who gave us the opportunity of publishing this special issue. We hope you enjoy the papers. Let us keep Eli’s memory alive. Let us stand on the shoulders of the greatest giant of all.
! ii Chiroptera Neotropical 19(3) Special Volume, December 2013 List of papers
Sergio Estrada-Villegas, Beatriz H. Ramírez. Bats of Casanare, Colombia...... 1-13
Sónia M.S. Pina, Christoph Meyer, Marlon Zortéa. A comparison of habitat use by phyllostomid bats (Chiroptera: Phyllostomidae) in natural forest fragments and Eucalyptus plantations in the Brazilian Cerrado...... 14-30
Marco A. R. Mello. The false dilemma of natural history vs. modern biology in Neotropical bat research...... 31-35
Phoebe Parker-Shames, Bernal Rodríguez-Herrera. Maximum weight capacity of leaves used by tent- roosting bats: implications for social structure ...... 36-43
Kathrin Barboza-Marquez, Luis F. Aguirre, José C. Pérez-Zubieta, Elisabeth K.V. Kalko. Habitat use by aerial insectivorous bat in shoreline areas of Barro Colorado Nature Monument, Panama ...... 44-56
Valéria da C. Tavares. Phyllostomid bat wings from Atlantic Forest bat ensembles: an ecomorphological study ...... 57-70
Benjamin Feit, Kirstin Übernickel, Marco Tschapka, Elisabeth K. V. Kalko. The potential function of individual signal frequency for masking avoidance in the greater bulldog bat Noctilio leporinus .. 71-79
! iii Chiroptera Neotropical 19(3) Special Volume, December 2013
List of authors (in alphabetical order)
Author Address Beatriz H. Ramírez Centro de Estudios Ambientales de la Orinoquia CEAO - Asociación de Becarios de Casanare Benjamin Feit University of Ulm, Institute of Experimental Ecology, Albert-Einstein- Allee 11, 89069 Ulm, Germany 2University of Western Sydney, Hawkesbury Institute for the Environment, Locked Bag 1791, Penrith, NSW, 2751 Australia Bernal Rodríguez-Herrera Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica.
Christoph Meyer Centro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal José C. Pérez-Zubieta Fundación Programa para la Conservación de los Murciélagos y la Biodiversidad. P.O.Box 994. La Paz, Bolivia.
Kathrin Barboza-Marquez Fundación Programa para la Conservación de los Murciélagos y la Biodiversidad. P.O.Box 994. La Paz, Bolivia. Asociación Bolivia para la Investigación y Conservación de Ecosistemas Andino Amazónicos. La Paz, Bolivia.
Kirstin Übernickel University of Ulm, Institute of Experimental Ecology, Albert-Einstein- Allee 11, 89069 Ulm, Germany
Luis F. Aguirre Fundación Programa para la Conservación de los Murciélagos y la Biodiversidad. P.O.Box 994. La Paz, Bolivia. Centro de Biodiversidad y Genética, Universidad Mayor de San Simón. P.O.Box 538. Cochabamba, Bolivia. Marco A. R. Mello Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais. Avenida Antônio Carlos, 6.627. 31270-901 Belo Horizonte, MG, Brazil. Marco Tschapka University of Ulm, Institute of Experimental Ecology, Albert-Einstein- Allee 11, 89069 Ulm, Germany Smithsonian Tropical Research Institute, P.O. Box 0843-03092 Balboa, Ancón, Republic of Panamá Marlon Zortéa Coordenação de Ciências Biológicas, Campus Jataí, Universidade Federal de Goiás – Br 364 Km 195 Jataí, Goiás, Brasil Phoebe Parker-Shames Colorado College Biology Department, 14 East Cache La Poudre St. Colorado Springs, Colorado, USA 80903. Present address 344 Bridge St. Ashland, Oregon, USA 97520. Sergio Estrada-Villegas Asociación de Becarios de Casanare-ABC. Calle 17#15-55, Yopal, Casanare, Colombia. Tel. +57 (8) 6358938. Programa para la Conservación de los Murciélagos de Colombia PCMCo. Calle 95 No. 17-37 Of. 104 Bogotá, Colombia. Tel. +57 (1) 6106051 Sónia M.S. Pina Centro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal Valéria da C. Tavares Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Universidade Federal de Minas Gerais (UFMG). Avenida Antônio Carlos, 6.627, 31270-901, Belo Horizonte, MG, Brazil. Programa de Pós-Graduação em Genética, Conservação e Biologia Evolutiva (PPGCBev); Instituto Nacional de Pesquisas da Amazônia (INPA), Av. André Araújo, 2.936, 69067-375, Manaus, AM, Brazil.
! iv Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
Bats of Casanare, Colombia
Sergio Estrada-Villegas1,2,* and Beatriz H. Ramírez3
1 Asociación de Becarios de Casanare-ABC. Calle 17#15-55, Yopal, Casanare, Colombia. Tel. +57 (8) 6358938. 2 Programa para la Conservación de los Murciélagos de Colombia PCMCo. Calle 95 No. 17-37 Of. 104 Bogotá, Colombia. Tel. +57 (1) 6106051. 3 Centro de Estudios Ambientales de la Orinoquia CEAO - Asociación de Becarios de Casanare
* Corresponding author: [email protected]
ARTICLE Abstract Manuscript history: Colombia is known for its high bat richness, but regions like Submitted in 31/May/2012 Orinoquía remain poorly known for this group. Here we present Accepted in 26/Jun/2013 results from seven biodiversity assessments in Casanare, Colombia, a Available on line in 26JSep/2014 department circumscribed within Orinoquía. We captured 1,116 Editors: Marco A.R. Mello and Valéria C. Tavares individual bats of 51 species and five families. Desmodus rotundus, Carollia spp., and Artibeus spp. were the most abundant taxa sampled. We also captured elusive species such as Lampronycteris brachyotis and Sphaeronycteris toxophyllum. In general, sites with some sort of protection, lower in elevation, and towards the southwest tended to have richer assemblages with different composition than sites without protection, higher in elevation, and towards the northeast of our study area. This southwest-northeast site distribution follows a rainfall gradient, which might explain differences in bat composition among sites. Finally, we discuss our species list in light of others that have been published and present the first analysis of assemblage structure for the bats of Casanare using true diversities.
Keywords: Rényi diversity plot, true diversities, Orinoco basin, elevational gradient, diversity, Desmodus rotundus, Phyllostomidae, local communities.
! number of bat species lists and other peer- Introduction reviewed publications came from departments Colombia is known to harbor one of the richest within the Andes (e.g., Castaño et al. 2003; bat faunas in the world (Alberico et al. 2000) and Estrada-Villegas et al. 2010) than from other the richest phyllostomid assemblage in the biogeographic regions (Marín-Vásquez and Americas (Mantilla-Meluk et al. 2009). However, Aguilar-González 2005). One of these the bat richness of Colombia is not evenly undersampled biogeographic regions is Orinoquía distributed across its biogeographic regions. (Stevenson et al. 2004). Differences in energy availability across regions Orinoquía, defined by the Orinoco River might be an underlying ecological constraint Basin, is located on the eastern versant of the (Ruggiero and Kitzberger 2004), but this uneven Andes and is composed of lowland savannas and distribution of bat richness also reflects that some Andean ecosystems. It comprises approximately areas have been better sampled than others, thus 20.2% (17.4 million ha) of Colombia’s total area, producing patterns that are biased due to and four of the 11 largest rivers in the country differences in sampling effort. For example, flow through this region (Arango et al. 2003; Stevenson et al. (2004) and Mantilla-Meluk et al. Romero et al. 2004). Orinoquía includes 11 (2009) have shown that the number of departments, either partially or totally. Casanare is publications and sampling sites for bats are one of the four departments totally circumscribed clumped in the Andes and strongly biased towards in this region and provides great revenues in terms areas adjacent to the three largest cities in of oil and gas production, cattle farming, and palm Colombia: Bogotá, Cali, and Medellín. A larger
! 1 ! ! Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013 oil production. It is also one of the most degraded departments in the country, despite its size; 33.9% of its area has been transformed (Romero et al. 2004), and only three of its 14 natural ecosystems have more than 10% of their area protected by the national park system (Arango et al. 2003). In terms of biodiversity, bats have not been well studied in Casanare. Apart from a recent species list (Trujillo et al. 2011) and a detailed study from one location (Rodríguez 2009), the available information is scarce, has not been formally published in the peer-reviewed literature, and usually relies on data collected in departments around Casanare. No study has been published yet performing assemblage analysis or comparing Figure 1. Map of the department of Casanare. 1. different sites in Casanare. Municipality of Yopal; 2. Municipality of Aguazul; 3. Municipality of Tauramena; 4. Municipality of Maní; 5. The Asociación de Becarios de Casanare Municipality of Chámeza. Inset: political map of (ABC), a non-profit organization, is carrying out Colombia, Orinoco basin (departments of Meta, the largest environmental educational program in Vichada, and Arauca) in gray, department of Casanare the department up to date and has done detailed in dark gray. biodiversity assessments in several sites across the Andean foothills of Casanare and its savannas. common. Annual rainfall varies from 1,500 to Here we present the results of these assessments, 4,500 mm from northeast to southwest, January is which represent the first assemblage analysis of the driest month, and June the rainiest (Aguirre- the bats of Casanare. With the information at hand Gutiérrez 1999). Altitude varies from 100 to 3,800 we asked: (1) how complete were our surveys in m a.s.l., with an average of 350 m a.s.l. (Aguirre- terms of species richness and true diversity? And Gutiérrez 1999). (2) what are the diversity patters that emerge from We carried out seven biodiversity assessments our surveys and what are the most plausible in different sites, plus occasional non-standardized explanations for them? samplings in semirural areas in three Materials and Methods municipalities. Sampling was performed in three The department of Casanare comprises 3.9% out of eight biomes: zonobiome of the humid of Colombia’s total area. It is located on the tropical foothills Arauca-Casanare, amphibiome eastern versant of Cordillera Oriental and bordered Arauca-Casanare, and helobiome Orinoquian- by the departments of Arauca on the north, Meta Amazonian. The assessments encompass an on the south, Vichada and Meta on the east, and altitudinal range of about 1,000 m, sampling a Boyacá on the west (Figure 1). According to drastic change in forest structure, landscape Romero et al. (2004), Casanare has eight biomes, orography, and levels of anthropogenic and the amphibiome Arauca-Casanare is the most transformation (Table 1).
Table. 1. Sampling sites of biodiversity assessments carried out in Casanare, Colombia. Geographic coordinates and sampling effort for each site are provided. Average Net No. of No. of Sites Id elevation Season Coordinates meters nights hours (m) (m2) Tinije TIN 191 Both 4º53’42” N 72º24’12” W 270 21 138 Buenos Aires BUA 369 Dry 4°59'21" N 72°43'2" W 300 7 28 EPF Floreña EPF 570 Wet 5°26'33" N 72°27'21" W 270 3 12 Volcán blanco VOB 657 Wet 5°19'47" N 72°33'6" W 105 3 22 Floreña I FLI 672 Dry 5°29'46" N 72°23'45" W 270 3 12 Pauto J PAJ 924 Dry 5°23'12" N 72°28'51" W 270 3 16 Pauto M PAM 1036 Wet 5°24'23" N 72°28'22" W 240 3 12.5
! 2 ! ! Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
Site description M (PAM), despite being very close to Pauto J, has Tinije (TIN) is a wetland with a lake of 179 ha, large fragments of secondary and gallery forests surrounded by a matrix of primary and secondary with small grasslands. Forests were preserved in forests and savannas that become seasonally this area for unknown reasons until Equión Energy flooded. It is shared by the municipalities of bought those areas and protected them by banning Aguazul and Maní, and a detailed study, focused logging and hunting since 2009. In general, sites not only on bats, but also on other taxonomic are distributed along the rainfall gradient present groups, was carried out by Ramírez (2009) and is in Casanare and the aforementioned sites vary in available upon request. Sampling effort was annual rainfall from 4,500 to 3,000 mm, a highest at this site (Table 1) and was performed on considerable decrease of 1,500 mm of annual savannas adjacent to transitional forests and within rainfall. the primary forest that surrounds the lake. The Sampling methods most abundant plant species found were Protium At each site we conducted mist netting from sp. Burm.f., Mauritia flexuosa L.f., Licania 18:00 till midnight and from 3:00 till 6:00, subarachnophylla Cuatrec., Mabea occidentalis because previous studies in the area demonstrated Benth., Siparuna quianenesis Aubl., Henriettella that bat activity is extremely low between 0:00 silvestris Gleason., and Davilla nitida (Vahl) and 3:00. Rainy nights were avoided. Buenos Kubitzki. Aires and Pauto J were sampled in the dry season, Buenos Aires (BUA) is a tract of secondary whereas EPF Floreña, Volcán Blanco, Floreña I forest (55 ha) that surrounds an oil facility and and Pauto M were sampled in the rainy season. belongs to Equión Energy, an oil company that Tinije was sampled in both seasons. A preliminary operates in this region of the country. It has been analysis showed that seasonality did not affect the in an undisturbed forest recovery since 2000. differences in relative abundances between sites There are remnants of old gallery forests and (T-TEST, t 5.746= 0.0304 P = 0.9768). abandoned pastures that have turned into We captured bats with mist nets of different secondary forests. The most abundant plant lengths (6 and 12 m long x 2.5 m high) set up species found there were Genipa americana L., opportunistically on forest edges, over creeks, Banara guianensis Aubl., Miconia minutiflora across trails, and inside dense vegetation, in order (Bonpl.) DC., and Siparuna guianensis Aubl. to maximize the number of captures and increase Since 2000 Equión Energy has been actively the probability of capturing species that prefer protecting this area by banning logging and different habitats. The sampling effort per site was hunting. calculated using a modification of the index EPF Floreña (EPF) is an oil processing facility proposed by Straube and Bianconi (2002); square imbedded in a pasture-secondary-gallery-forest meters (transforming all nets into 12 m nets) matrix. We know no actions promoting forest multiplied by sampling hours. This approach helps conservation in the area. compare sites that were more intensively sampled Volcán Blanco (VOB) is a small watershed than others. Although we tried to avoid nights of with a gallery forest surrounded by pastures. full moon, some sites were sampled close to full Forests are secondary in nature but interconnected moon due to logistical constraints. Although lunar with other forest tracts at lower and higher phobia is known for some bat species (Morrison elevations. The most common tree species found 1978), sampling nights near full moon carried out were Miconia dolichorrhyncha Naudin., Inga in places with dense vegetation were as successful edulis Mart., Ficus insipida Willd., Aniba sp. as sampling nights in waning or waxing moon Aubl., and Oyedaea verbesinoides DC. This site (Estrada-Villegas and Ramírez personal had the smallest sampling effort (Table 1) and observations), so we are confident that capture there haven’t been any actions promoting forest success was not strongly affected by moon phase. conservation in the area that we know of. All bats that were captured were aged, sexed, Floreña I (FLI) is an area characterized by weighed, and measured following standardized well-preserved gallery forests and grasslands for protocols and observing the guidelines of the cattle farming. A particularity of this site is the American Society of Mammalogists (Sikes and abundance of the palm Scheelea sp. in the Gannon 2011). Field identifications and posterior grasslands due to the fact that cattle feed on its photographic confirmations were based on Timm fruits. We are not aware of any actions promoting and LaVal (1998), Gardner (2008), Aguirre et al. forest conservation in this area. (2009) and Díaz et al. (2011). Taxonomy followed Pauto J (PAJ) is an area with very small Simmons (2005) but we opted to use Dermanura remnants of gallery forests imbedded in open for lesser Artibeus according to Hoofer et al. grasslands with very few standing trees. There are (2008). We collected voucher specimens from no current conservation efforts in this area. Pauto some species to confirm our field identifications (Colección Teriológica Universidad de Antioquia ! 3 ! ! Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
817-822) and followed specific criteria for some upper boundary for the expected number of species that are difficult to identify in the field. species according to their distributions and offered We differentiated Anoura geoffroyi from Anoura a way to compare the result obtained with the luismanueli by size, as A. luismanueli is smaller in Jackknife 1 estimator. The Jackknife 1 richness forearm length and body size, and we followed the estimator was calculated in the package vegan 2.0- geographic distribution proposed by Mantilla- 2 for R (Oksanen et al. 2011). Meluk and Baker (2005) for A. luismanueli. Last, we used a qualitative measure of Carollia perspicillata was differentiated from abundance developed by Gaston (1994), in which Carollia brevicauda by its larger forearm length, we consider in how many sites a species occurred. lighter banding on the back fur, longer tibia, and If a species occurred in more than 75% of the forearm, tibia and feet sparsely haired. When sites, we considered it super-abundant, abundant if possible, we checked for size differences between it occurred in more than 50% of the sites, common inner and outer lower incisors as suggested by between 50% and 25%, and rare if it occurred in Timm and LaVal (1998). Dermanura anderseni less than 25% of the sites. was differentiated from Dermanura glauca by its We also chose to describe our survey in terms sparsely haired uropatagium, duller dorsal pelage of true diversities or effective numbers, which are and its rostrum tilted up when seen from the side. derived from parametric families of diversity When comparing these species in the field, D. functions (Tóthmérész 1995). In our work we used glauca has well-defined and brighter facial stripes two families, Rényi’s and Hill’s (Hill 1973; Rényi than D. anderseni (Gardner 2008). We grouped 1961), which are mathematically related to each Platyrrhinus helleri with Platyrrhinus other (Tóthmérész 1995), and change according to brachycephalus, because they are indistinguishable and the two accessory cusps on the scale parameter α for Rényi’s, and the order q the anterior margin of the second premolar are for Hill’s, respectively (following the terminology very difficult to see in the field. of Tóthmérész 1995 and Jost 2006). This approach changes the paradigm of how assemblages are Data analysis analyzed. Instead of using different diversity We analyzed our data in two ways; first, we indices (e.g., Shannon or Simpson), it uses species pooled data from all sites in order to have an frequencies and the order, or scale parameter, of assessment of the whole assemblage, and, second, the functions. Assemblages are described not in abundances were standardized by sampling effort terms of entropy but in terms of individual units or per site allowing us to unravel patterns at the effective number of species that are biologically landscape level (i.e., among sites). To calculate the meaningful and comparable. estimated richness (Sest) of the whole assemblage Effective numbers can be determined as and the inventory completeness of our surveys, we diversity of order zero, one, two, and infinity (0D, 1 2 ∞ took two approaches. D, D, and D for Hill numbers or H0, H1, H2 and First, we calculated the Jackknife 1 richness H∞ for Rényi diversities). When q or α=0, or estimator, which performs well compared to other diversity of order zero, the functions are estimators. It is reliable when habitats within the insensitive to species frequencies and the value landscape are heterogeneous, as in our case, and corresponds to the species richness. When q or suits the type of surveys we performed (Burnham α<1, true diversities favors rare species but when and Overton 1979; Meyer et al. 2011). For this q or α = 1 all species are weighted equally and analysis we used each sampling night per site and only by their frequencies. When q or α > 1 true included an additional row for species that have diversities favors common species (Jost 2006). been caught occasionally (two bat species in the The common diversity indices used in community municipality of Yopal and two in the municipality ecology are in fact special cases of Hill numbers of Chámeza). Then we calculated sampling or Rényi diversities. For Hill numbers 0D = S, 1D 2 ∞ completeness as a percentage of estimated = exp(H′), D = D2, and D = 1/(max pi); for richness. Rényi diversities H0 = log(S), H1 = H′, H2 = − 2 Second, we compared the observed richness log(Σpi ), and H∞ = − log(max pi) for Rényi (Sobs) with the number of bats species that have diversities (Oksanen et al. 2011). S = species been recorded for the department of Casanare and richness, H’ = Shannon–Weaver index, D2 = three departments around it, Arauca, Meta and inverse Simpson index and pi = frequency of the Vichada, according to the most up-to-date ith species. Both 1/(max pi) and − log(max pi) are mammal species list for Colombia (Solari et al. directly related to the Berger-Parker diversity -1 2013). Given that the number of studies on bats in index d (Kindt et al. 2006). Casanare is low, and these three departments share To analyze the diversity completeness for the the same biomes found in Casanare, probably the whole assemblage, we calculated 0D, 1D and 2D as bats present in these three departments are also proposed by Moreno et al. (2011) using the present in Casanare. This approach gave us an software SPADE (Chao and Shen 2010), and ! 4 ! ! Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
profile, the dissimilarity matrix, and the NMDS, we used the package vegan 2.0-2 for R (Oksanen et al. 2011). Rényi diversity plots were calculated 25 Tinije using the renyiplot function for R with the Buenos Aires EPF Floreña package BiodiversityR version 1.6 (Kindt and Coe 20 Volcán blanco 2005). All analyses were performed using R Floreña I Pauto J version 2.14.2 (R Foundation for Statistical 15 Pauto M Computing (2012)) except where stated otherwise. alpha − H
10 Results 5 We captured 1,116 individual bats of 51
0 species and five families in Casanare (Table 2 and
0 0.25 0.5 1 16 2 32 4 64 8 Inf 3), including occasional observations. alpha Phyllostomidae was the richest family, with 39
Figure 2. Rényi diversity profiles for seven sampling species, and Stenodermatinae, followed by sites in Casanare, Colombia. Occasional observations Phyllostominae, were the richest subfamilies. We were not included in this analysis. recorded elusive species in our assessments and occasional captures, such as Peropteryx macrotis, calculated the Abundance-based Coverage Lampronycteris brachyotis, Tonatia bidens, Estimator ACE, the Jackknife richness estimator Sphaeronycteris toxophyllum, Histiotus montanus, and the Minimum Variance Unbiased Estimator and Lasiurus blossevillii. Six species, including MVUE as expected diversities for 0D, 1D and 2D, Desmodus rotundus and Carollia perspicillata, respectively. Observed true diversities were were super-abundant, four were abundant, 16 were calculated using the Rényi function with the common, and 23 were rare (Table 2). The package vegan 2.0-2 for R and setting the output completeness of our surveys was intermediate for Hill numbers instead of Rényi diversities (Table 4); the lower boundary, determined by the (Oksanen et al. 2011). richness estimator, showed high completeness To compare our sampling sites in order to (80.04%). However if we use the expected number detect patterns across the landscape, we ordered of species according to the species that could be their true diversities calculating a Rényi plot, present in Casanare, Arauca, Meta, and Vichada which is a reliable method to compare (Solari et al. 2013), the completeness of our simultaneously the diversity functions of different surveys was low (51.52%). In terms of true assemblages and determine which one is truly diversity, the estimated 1D and 2D determined that more diverse (Kindt et al. 2006; Tóthmérész the assemblage should have had 1.03 and 0.99 1995). For this analysis, we corrected species times more effective species, respectively, than abundances by dividing abundance per species per what we were able to record (Table 4). site by the sampling effort employed in that site.
This correction allowed us to account for differences in sampling effort between assessments.
Then we calculated the dissimilarity in species 0.3 composition between all sampling sites with the
● binary version of Horn’s similarity index and used 0.2 BUA ● PAM ● two-dimensional non-metric multidimensional TIN scaling (NMDS) to compare assemblage 0.1 composition among sites. Horn’s index is a VOB suitable metric for our study because we are 0.0 interested in finding patterns in terms of the NMDS2 0.1 presence/absence data and it is unaffected by small − sample sizes (Krebs 1999). The Rényi plot FLI EPF 0.2 complements this pattern elucidation by using − PAJ corrected abundance data. Finally, to determine if 0.3 there has been an effect of conservation status, we − employed an analysis of similarity (ANOSIM) −0.4 −0.3 −0.2 −0.1 0.0 0.1 0.2 0.3 based on the dissimilarity matrix used in the NMDS1 NMDS, and grouped sites by management regime. Figure 3. Non-metric multidimensional scaling (NMDS) For analyzing the effect of elevation on based on the Horn dissimilarity index for seven community composition, we regressed the NMDS sampling sites in Casanare, Colombia. For site axis 1 against elevation. To calculate the Rényi abbreviation please see Table 1. ! 5 ! ! Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
Table 2. Bat species list of Casanare, Colombia. Information based on captures made in seven sampling sites. Family Subfamily Species Qualitative abundance Emballonuridae Peropteryx macrotis 1 Saccopteryx leptura R Rhynchonycteris naso R Noctilionidae Noctilio leporinus R Phyllostomidae Desmodontinae Desmodus rotundus SA Glossophaginae Anoura geoffroyi C Anoura luismanueli R Glossophaga soricina SA Lonchophylla sp. R Phyllostominae Lampronycteris brachyotis R Lophostoma brasiliense C Lophostoma silvicolum R Macrophyllum macrophyllum R Micronycteris microtis R Micronycteris schmidtorum R Mimon crenulatum R Phyllostomus discolor C Phyllostomus elongatus C Phyllostomus hastatus C Tonatia bidens R Tonatia saurophila R Trachops cirrhosus C Carollinae Carollia brevicauda SA Carollia castanea C Carollia perspicillata SA Stenodermatinae Artibeus lituratus SA Artibeus obscurus C Artibeus planirostris A Chiroderma trinitatum C Chiroderma villosum C Dermanura anderseni A Dermanura glauca C Mesophylla macconnelli C Platyrrhinus SA helleri/brachycephalus Platyrrhinus nigellus 2 Sphaeronycteris toxophyllum R Sturnira erythromos R Sturnira lillium C Sturnira oporaphilum R Uroderma bilobatum A Uroderma magnirostrum R Vampyriscus bidens R Vampyressa thyone A Vespertilionidae Myotinae Myotis albescens C Myotis keaysi R Myotis nigricans R Vespertilioninae Eptesicus brasiliensis C Eptesicus furinalis C Histiotus montanus 2 Lasiurus blossevillii R Molossidae Molossus molossus 1 1 Occasional observations made on mist netting nights in the municipality of Yopal. 2 Occasional observations made on netting nights in the municipality of Chámeza. These observations were not included in our biodiversity assessments; however, these species were included in a separate row to calculate the estimated richness for all our surveys. !
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Table 3. Bat species abundance at each sampling site in Casanare, Colombia. For site abbreviations see Table 1. Species TIN BUA EPF VOB FLI PAJ PAM Total Anoura geoffroyi 0 0 0 1 4 0 0 5 Anoura luismanueli 0 0 0 0 0 0 3 3 Artibeus lituratus 12 1 5 3 3 1 0 25 Artibeus obscurus 7 0 5 0 9 0 0 21 Artibeus planirostris 21 6 0 8 2 9 0 46 Carollia brevicauda 28 5 18 47 18 8 26 150 Carollia castanea 0 12 20 0 0 1 0 33 Carollia perspicillata 143 59 0 4 4 4 6 220 Chiroderma trinitatum 4 0 0 0 0 0 2 6 Chiroderma villosum 0 0 0 0 1 1 0 2 Dermanura anderseni 0 3 1 2 1 0 1 8 Dermanura glauca 6 0 0 0 1 2 0 9 Desmodus rotundus 248 13 2 6 2 4 6 281 Eptesicus brasiliensis 5 1 0 0 0 0 0 6 Eptesicus furinalis 0 0 0 1 0 0 1 2 Glossophaga soricina 3 16 7 6 3 1 0 36 Lampronycteris brachyotis 0 0 0 1 0 0 0 1 Lasiurus blossevillii 2 0 0 0 0 0 0 2 Lophostoma brasiliense 6 1 0 1 0 0 0 8 Lophostoma silvicolum 6 0 0 0 0 0 0 6 Lonchophylla sp. 0 1 0 0 0 0 0 1 Macrophyllum macrophyllum 1 0 0 0 0 0 0 1 Mesophylla macconnelli 2 7 0 0 0 0 1 10 Micronycteris microtis 2 0 0 0 0 0 0 2 Micronycteris schmidtorum 0 4 0 0 0 0 0 4 Mimon crenulatum 25 0 0 0 0 0 0 25 Myotis keaysi 0 0 1 0 0 0 0 1 Myotis nigricans 0 0 0 0 0 1 0 1 Noctilio leporinus 1 0 0 0 0 0 0 1 Phyllostomus discolor 2 3 0 0 0 0 0 5 Phyllostomus elongatus 18 11 0 0 0 0 0 29 Phyllostomus hastatus 2 5 0 0 0 0 0 7 Platyrrhinus helleri/brachycephalus 16 2 10 6 10 2 4 50 Rhynchonycteris naso 12 0 0 0 0 0 0 12 Saccopteryx leptura 2 0 0 0 0 0 0 2 Sphaeronycteris toxophyllum 0 0 1 0 0 0 0 1 Sturnira erythromos 0 0 0 0 1 0 0 1 Sturnira lillium 0 0 0 0 6 0 1 7 Sturnira oporaphilum 0 0 0 0 2 0 0 2 Tonatia bidens 2 0 0 0 0 0 0 2 Tonatia saurophila 0 2 0 0 0 0 0 2 Trachops cirrhosus 17 2 1 0 0 0 0 20 Uroderma bilobatum 0 3 2 2 12 0 1 20 Uroderma magnirostrum 0 21 0 0 0 0 0 21 Vampyriscus bidens 0 3 0 0 0 0 0 3 Vampyressa thyone 0 2 6 1 1 0 2 12 Total abundance 593 184 79 89 80 34 55 1114 Species richness 26 24 13 14 17 11 13 511
1 This tallying includes four occasional observations made in the municipality of Yopal and Chámeza; Peropteryx macrotis, Platyrrhinus nigellus, Histiotus montanus, and Molossus molossus. Occasional observations are not included in the tallying of total abundance.
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After correcting for sampling effort, the Rényi plot showed that no site was truly more diverse than the others, because the profiles intersect each other (Figure 2). However, when making closer comparisons, some patterns emerged. Tinije and Buenos Aires were more diverse than Pauto M and 0.2 Volcán Blanco, and Floreña I was more diverse than Pauto M, Volcán Blanco, EPF Floreña, and Pauto J. However, Floreña I overlaps both with 0.0 Tinije and Buenos Aires, thus it is not more diverse than these two sites. At H0, Tinije showed NMDS axis 1 0.2 higher true diversity (i.e., richness) than Buenos − Aires, but Buenos Aires has a more even
assemblage than Tinije given that Tinije’s profile 0.4 − was steeper than Buenos Aires’s. At H1, Buenos 200 400 600 800 1000 Aires was 2.02 times more diverse than Volcán Blanco, the lowest diversity at this scale Elevation parameter, and 1.59 times more diverse than Figure 4. Non-metric multidimensional scaling (NMDS) Tinije, which was more diverse than Buenos Aires axis 1 regressed against elevation. For site-specific at H0. At H2 and H∞, Floreña I had higher true elevation, please see Table 1. diversities than the other sites, which is due to the fact that Rényi diversities at these scale parameter Colombia. We found 51 bat species of five favors common species. For example, the most families, which were sampled across abundant species in Floreña I had only 22.5% of representative biomes of the Orinoco Basin. We the total abundance, whereas the most abundant were able to survey both middle-sized and small- species Pauto M and Volcán Blanco had 47.3% sized forests, allowing us to detect rare species and 52.8% of the total abundance, respectively. that usually go unnoticed in inventories carried out In terms of species composition, the two- on other Neotropical areas. This work, as far as we dimensional NMDS had high goodness of fit (R2 = know, its the first study that employed Rényi plots 0.98) and low stress (stress = 0.05), indicating a and true diversities to describe a bat assemblage in high match between the dissimilarity matrix and Colombia and one of the few in the Neotropics the ordination. The NMDS axis 1 (Figure 3) (see Moreno et al. 2011 for another example). showed a week environmental gradient in species Other studies that made preliminary lists of the composition defined by altitude and a distribution bats of Casanare, such as those by Biocolombia of sites in the southwest-northeast direction. (1996), Vega-Orduz (2007), Garavito-Fonesca Assessments performed at lower altitudes and (2008), and Trujillo et al. (2011), have relied towards the southwest seemed to have low scores mostly on secondary sources and provided lists along axis 1, whereas assessments at higher that included species that are not or should not be altitudes and towards the northeast seemed to have present in Casanare according to well-established higher scores. Nevertheless, axis 2 reflected a distributions. For example, Trujillo et al. (2011) stronger gradient in species composition related to included Centurio senex and Rhinophylla fisherae, conservation status; sites surrounded by preserved as well as other species, in their bat list of forests (Tinije, Buenos Aires and Pauto M) had Casanare. The former is known to occur only in high scores along this axis, whereas assessments the Caribbean coast of Colombia and the latter is performed in unprotected areas (Volcán Blanco, restricted to the Amazon. Thus, their account for Floreña I, EPF Floreña and Pauto J) had low the number of species in the department (112) scores. The conservation status of the areas might be overestimated. Similarly, Vega-Orduz affected the assemblage structure; species (2007) included Rhogeessa minutilla and composition differed significantly between Molossus tropidorhynchus in her list: the former is protected and unprotected areas (ANOSIM, global restricted to dry areas of the northeastern tip of R = 0.528, P = 0.026). Although the relationship Colombia and the latter is a subspecies found only between the axis of species composition and in Cuba and the Cayman Islands. Thus, her list is elevation was not significant (T-TEST, F5 = 3.262, also questionable. On her account, Garavito- 2 P = 0.131, R = 0.274), there seems to be a trend Fonesca (2008) used secondary information and between elevation and composition (Figure 4). expert advice in order to classify each bat species Discussion as present or likely to be present in the department and was stated as such in her work. Surprisingly, Our study provided the first bat species list and Trujillo’s list only differs by two species analysis of assemblage structure and species compared to Garavito-Fonesca’s, and whereas composition for the department of Casanare, ! 8 ! ! Chiroptera Neotropical 19(3) Special Volume: 1-13, December 2013
Garavito-Fonesca clearly states which species are Sánchez-Palomino et al. 1993). Carollia was the likely to be present, Trujillo et al. (2011) does not most abundant genus, followed Artibeus. make such distinction. This casts more doubt on Desmodus rotundus is very abundant in sites the list published by Trujillo et al. (2011), which is where cattle has been intensively raised, such as the last list published to date. Finally, these Casanare, Meta (Sánchez-Palomino et al. 1993), studies, among others, have cited the list published and also Llanos de Moxos in Bolivia (Aguirre by Biocolombia (1996) as the most complete list 2002). Moreover, rare species found elsewhere, of the bats present in Casanare. However, this is a like Vampyriscus bidens, Trinycteris nycefori and hypothetical list, as the authors in its legend state Dermanura anderseni (Aguirre 2002; Rojas et al. it, and authors citing this list have created 2004; Sánchez-Palomino et al. 1993), were also confusion because they have used it for purposes rare in our study. Only a few studies have beyond its original intention. analyzed assemblages with the true diversity According to our results and the estimated approach. Moreno et al. (2011) seems to be the richness based on possible occurrences (Solari et first to encourage its use in analysis of bat al. 2013), the number of bat species present in assemblages. Our results suggest that the Casanare might be between 64 and 99, which is estimated true diversities for the whole highly likely because our sampling was biased assemblage (all sites pooled together) is high and towards phyllostomids, excluding emballonurids, indicates marked differences between sites that do vespertilionids, and molossids (Kalko et al. not overlap their diversity profiles. These 2008). In this regard, a recent study on the differences, however, should be interpreted with watershed of the Pauto River on the Municipalities caution because sampling effort varied among of Pore, Trinidad and San Luis de Palenque sites. This is due to the fact that different (Suárez-Castro et al. 2013), reports three biodiversity assessments aimed at different goals additional species that we missed in our surveys: (e.g., public vs. private contracts), some were Saccopteryx bilineata, Myotis riparius intended to be more intensive than others, and the and Rhogeessa io. All emballonurids that are time available to perform them also varied. One occasionally captured with mist nets. Moreover, pattern, however, is clear: Floreña I has higher veterinarians from Instituto Colombiano true diversity than EPF Floreña, Volcán Blanco, Agropecuario ICA have caught Diaemus yungi Pauto J and Pauto M, all sampled with very and Diphylla ecaudata (Tabares, personal similar efforts. communication), indicating that the number of bat Species composition seems to reflect the species in Casanare should be indeed higher than results in terms of structure. Tinije and Buenos 64, but probably not 112. Sánchez-Palomino et al. Aires showed high scores on the NMDS axis 2 (1993), Muñoz-Saba et al. (1997), and Rojas et al. and higher diversity profiles than other sites, both (2004) reported similar bat assemblages, although to the southwest of our study area and protected to less rich than the one we describe here. These some degree. Again, we cannot rule out the effect studies were carried out on Serranía de la of sampling effort but cannot rule out either a Macarena (department of Meta), which is strongly compounded effect of forest preservation and influenced by Amazonian ecosystems. Thus, it is altitude on species composition. Still, the effect of not surprising that they were able to find forest conservation was evident in terms of Rhinophylla fisherae. At a regional scale, the assemblage composition (see ANOSIM) and there assemblage in Casanare, and specially Tinije, is seems to be a changing trend with respect to similar to the one reported by Aguirre (2002). altitude. A monotonic decrease in bat richness Both sites are seasonally flooded savannas with with altitude has been found in Peru (Graham gallery forests, grasslands, and anthropogenic 1983; Patterson et al. 1996; Solari et al. 2006) and areas. Bolivia (Vargas and Patterson 2007), but other In terms of assemblage structure, our results examples from Colombia (Fawcett 1994; Munoz concur with other studies (Rojas et al. 2004; 1990) suggest a mid-elevation peak. However,
Table 4. Observed and estimated true diversities, estimated species richness, and percentage of completeness for the bat assemblage of Casanare, Colombia. All occasional observations were included in the analysis. Sobs = 51. 0 1 2 Estimator D D D Sest Completeness Observed by SPADE 51 14.204 7.773 Expected by SPADE 62 14.625 7.783 Expected by Jackknife 1 63.72 80.04% Expected by Solari et al. (2013) 99 51.52%
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Mantilla-Meluk (2009), using museum records for in a mountain range on the eastern versant of Phyllostomids at the scale of the whole country, Cordillera Oriental, have shown a decreasing and Marín-Vásquez and Aguilar-Gonzáles (2004), linear trend. Our results, in part, concur with their findings, Acknowledgments although our range only spans about 1,000 m and Studies in Buenos Aires, Floreña I, Pauto M, sampling efforts have not been the same across Pauto J, EPF Floreña, and Volcán Blanco were elevations. Although we did not find a decrease in funded by Equion Energía Limited. We thank all richness with elevation, the change in assemblage its external affairs and environmental teams for composition is somehow evident. The species the financial and logistic support. The study in richness elevation trend seems to be explained by Tinije was co-funded by Gobernación de poor thermoregulatory capabilities of Neotropical Casanare; we thank Manuel Rodríguez for his bats due to their small size and high surface to hard work and support for this study. Occasional volume ratio (Soriano 2000), and not by available captures in Chámeza were funded by the area or the mid-domain effect as it was claimed Municipality of Chámeza. We thank our field before McCain’s work (2007). assistants and the local communities, as well as Forest conservation is also known to have our work team at ABC. We thank S. Solari and M. paramount consequences on bat assemblage Rodríguez-Posada for species identification. structure and composition because anthropogenic Julieta Garavito deserves special thanks for transformation reduces the number of rare species sharing her Master’s thesis and data with us. and enhances the abundance of common species Finally, we thank Ricardo Tabares from Instituto (Ewers and Didham 2006; Meyer and Kalko Colombiano Agropecuario ICA for information 2008). In our case, phyllostomines such as about other vampire species he has captured. Phyllostomus elongatus, Tonatia saurophila, and Research permits were issued by Corporinoquia Lophostoma silvicolum, known as indicators of (numbers 500.57.12-0451, 200.41-10.1409, and preserved forests (Meyer and Kalko 2008), were 200.41.09.0681). only found in protected areas. However, how should we interpret the fact that Floreña I, which References is not protected, showed higher true diversity than Aguirre L.F. 2002. Structure of a Neotropical the other sites? We think this is related to habitat savanna bat community. Journal of Mammalogy quality at the sampling sites: the size of the stream 83(3): 775-784. and its gallery forest was larger than in other sites Aguirre L.F.; Vargas A. and Solari S. 2009. Clave and bats seem to be attracted to this type of area in de campo para la identificación de los the dry season. Finally, species composition in murciélagos de Bolivia. Centro de Estudios en Casanare also showed a climatic gradient, where Biología Teórica y Aplicada, Cochabamba, assemblages seemed to change in the southwest- Bolivia. northeast direction, as suggested by the ordination. This seems plausible given that rainfall decreases Aguirre-Gutiérrez N. 1999. Casanare: caracteríticas geográficas. Instituto Geogáfico from southwest to northeast (Aguirre-Gutiérrez "Agustín Codazzi", Bogotá. 1999), and rainfall is an important structuring factor of bat assemblages (Estrada-Villegas et al. Alberico M. C.A., Hernández-Camacho J., Y. 2012). Nonetheless, this hypothesis should be Muñoz-Saba. 2000. Mamíferos (Synapsida: further investigated given that we were unable to Theria) de Colombia. Biota Colombiana 1(1): study each site during both climatic seasons and/or 43-75. with similar sampling efforts. Arango N.; Armenteras D.; Castro M.; Gottsmann In conclusion, we present a species list of the T.; Hernández O.L.; Matallana C.L.; Morales department of Casanare based on field data and M.; Naranjo L.G.; Renjifo L.M.; F. T.A. and compare our results with those of previews Villareal H.F. 2003. Vacíos de conservación del studies, most of them based on hypothetical sistema de Parques Nacionales Naturales de presences. We show for the first time an Colombia desde una perspectiva ecorregional. assemblage-level analysis for the bats of Casanare, WWF Colombia and Instituto de Investigación and as far as we know, we are the first to use true de Recursos Biológicos Alexander von diversities and diversity profiles to compare bat Humboldt, Bogotá. assemblages in Colombia. With these analyses we Biocolombia. 1996. Faunula de vertebrados y su show that forest management has a positive effect entorno en la región de los campos de Cusiana y on assemblage composition, which also changes Cupiagua -Departamento de Casanare- Bases with elevation. para su uso, conservación y manejo. Informe final. Bogotá
Burnham K.P. and Overton W.S. 1979. Robust estimation of population size when capture
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probabilities vary among animals. Ecology 60: Papers, Museum of Texas Tech University 277: 927–936. 1–15. Castaño J.H.; Muñoz-Saba Y.; Botero J.E. and Jost L. 2006. Entropy and diversity. Oikos 113(2): Vélez J.H. 2003. Mamíferos del departamento 363-375. de Caldas-Colombia. Biota Colombiana 4(2): Kalko E.K.V.; Estrada-Villegas S.; Schmidt M.; 247-259. Wegmann M. and Meyer C.F.J. 2008. Flying Chao A. and Shen T.-J. 2010. Program SPADE high-assessing the use of the aerosphere by bats. (Species prediction and diversity estimation) Integrative and Comparative Biology 48(1): 60- http//:chaostatnthuedutw. 73. Díaz M.M.; Aguirre L.F. and Barquez R.M. 2011. Kindt R. and Coe R. 2005. Tree diversity analysis: Clave de identificación de los murciélagos del A manual and software for common statistical cono sur de Sudamérica. Centro de Estudios en methods for ecological and biodiversity studies. Biología Teórica y Aplicada., Cochabamba, World Agroforestry Centre (ICRAF), Nairobi. Bolivia. Kindt R.; Damme P. and Simons A. 2006. Tree Estrada-Villegas S.; McGill B.J. and Kalko E.K.V. diversity in western Kenya: using profiles to 2012. Climate, habitat, and species interactions characterise richness and evenness. Biodiversity at different scales determine the structure of a and Conservation 2(15):1253–1270. Neotropical bat community. Ecology. Doi. Krebs C.J. 1999. Ecological Methodology. http://dx.doi.org/10.1890/11-0275.1 Addison Wesley Longman, Menlo Park, Estrada-Villegas S.; Pérez-Torres J. and Stevenson California. P.R. 2010. Ensamblaje de murciélagos en un Mantilla-Meluk H. and Baker R.J. 2005. bosque subandino colombiano y análisis sobre Systematics of Small Anoura (Chiroptera: la dieta de algunas especies. Mastozoología Phyllostomidae) from Colombia, with neotropical 17(1): 31-41. description of a new species. Occasional Papers, Ewers R.M. and Didham R.K. 2006. Confounding Museum of Texas Tech University (261), 1-18. factors in the detection of species responses to Mantilla-Meluk H.; Jiménez-Ortega A.M. and habitat fragmentation. Biological Reviews Baker R.J. 2009. Phyllostomid bats of 81(1): 117-142. Colombia: Annotated checklist, distribution, and Fawcett D. 1994. Bats. in Surveys and biogeography. Special Publications Museum of conservation of biodiversity in the Chocó, Texas Tech University, Lubbock, TX. south-west Colombia (edited by Salaman Marín-Vásquez A. and Aguilar-González A.V. P.G.W.), pp. 60-67. BirdLife International, 2004. Diversidad de murciélagos en un Cambridge. gradiente altitudinal en la vertiente oriental de la Garavito-Fonseca J. 2008. Priorización de áreas cordillera oriental de los andes Colombianos para la conservación de la mastofauna silvestre (Florencia-Caqueta). Undergraduate, Facultad en Casanare - Colombia. Masters, Vicerectorado de Ciencias Básicas Universidad de la de Producción Agrícola, Universidad Nacional Amazonía. Experimental de los Llanos Occidentales Marín-Vásquez A. and Aguilar-González A.V. "Ezequiel Zamora". 2005. Murciélagos (Chiroptera) del Gardner A.L. 2008 [2007]. Mammals of South departamento de Caquetá-Colombia. Biota America, Volumen 1 Marsupials, Xenarthrans, Colombiana 6(2): 211-218. Shrews, and Bats. The University of Chicago McCain C.M. 2007. Area and Mammalian Press, Chicago. Elevational Diversity. Ecology 88(1): 76-86. Gaston K.J. 1994. Rarity. Chapman & Hall, Meyer C.F.J.; Aguiar L.M.S.; Aguirre L.F.; London. Baumgarten J.; Clarke F.M.; Cosson J.-F.; Graham G.L. 1983. Changes in bat species Villegas S.E.; Fahr J.; Faria D.; Furey N.; Henry diversity along an elevational gradient up the M.; Hodgkison R.; Jenkins R.K.B.; Jung K.G.; Peruvian Andes. Journal of Mammalogy 64(4): Kingston T.; Kunz T.H.; Cristina MacSwiney 559-571. Gonzalez M.; Moya I.; Patterson B.D.; Pons J.- Hill M.O. 1973. Diversity and evenness: A M.; Racey P.A.; Rex K.; Sampaio E.M.; Solari unifying notation and its consequences. Ecology S.; Stoner K.E.; Voigt C.C.; von Staden D.; 54(2): 427-432. Weise C.D. and Kalko E.K.V. 2011. Accounting for detectability improves estimates of species Hoofer S.R.; Solari S.; Larsen P.A.; Bradley R.D. richness in tropical bat surveys. Journal of and Baker R.J. 2008. Phylogenetics of the fruit- Applied Ecology 48(3): 777-787. eating bats (Phyllostomidae: Artibeina) inferred from mitochondrial DNA sequences. Occasional Meyer C.F.J. and Kalko E.K.V. 2008. Assemblage-level responses of phyllostomid
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bats to tropical forest fragmentation: land-bridge estructura ecológica de la laguna que conforma islands as a model system. Journal of el humedal “Laguna El Tinije”, que permitan Biogeography 35(9): 1711-1726. conocer su dinámica, estructura y funcionalidad Moreno C.E.; Barragán F.; Pineda E. and Pavón tendiente a su postulación como área Ramsar N.P. 2011. Reanálisis de la diversidad alfa: Convenio de Cooperación No 0126 de 10 de alternativas para interpretar y comparar Diciembre de 2008 Dirección Técnica de Medio información sobre comuniades ecológocas. Ambiente, Secretaría de Agricultura, Ganadería Revista Mexicana de Biodiversidad 82(1249- y Medio Ambiente, Gobernación de Casanare 1261). (edited by Ramírez B.), pp. 215-237. Asociación de Becarios de Casanare, Yopal. Morrison D.W. 1978. Lunar phobia in a neotropical bat, Artibeus jamaicensis Rojas A.M.; Cadena A. and Stevenson P. 2004. (Chiroptera: Phyllostomidae). Animal Preliminary study of the bat community at the Behaviour 26: 852-855. CIEM, Tinigua National Park, Colombia. Field Studies of Fauna and Flora La Macarena, Muñoz A.J. 1990. Diversity and feeding behavior Colombia 14: 45-53. of bats in an altitudinal transect across the Cordillera Central of the Colombian Andes. Romero M.; Galindo G.; Otero J. and Armenteras Studies on Neotropical Fauna & Environment D. 2004. Ecosistemas de la cuenca del Orinoco 25(1): 1-18. colombiano. Bogotá, Colombia. Muñoz-Saba Y.; Cadena A. and Rangel-Ch, J. O. Ruggiero A. and Kitzberger T. 2004. 1997. Ecología de los murciélagos antófilos del Environmental correlates of mammal species sector La Curia, Serraína La Macarena richness in South America: effects of spatial (Colombia). Revista de la Academia structure, taxonomy and geographic range. Colombiana de Ciencias 21(81): 473-486. Ecography 27(4): 401-417. Oksanen J.F.; Blanchet G.; Kindt R.; Legendre P.; Sánchez-Palomino P.; Rivas-Pava P. and Cadena Minchin P.R.; O'Hara R.B.; Simpson G.L.; A. 1993. Composición, abundancia y riqueza de Solymos P.; Stevens M.H.M. and Wagner H. especies de la comunidad de murciélagos en 2011. vegan: Community Ecology Package bosques de galería en la serranía de La version 2.0-2. http://CRAN.R- Macarena (Meta-Colombia). Caldasia 17(2): project.org/package=vegan. 301-312. Patterson B.D.; Pacheco V. and Solari S. 1996. Sikes R.S. and Gannon W.L. 2011. Guidelines of Distribution of bats along an elevational the American Society of Mammalogists for the gradient in the Andes of Peru. Journal of use of wild mammals in research. Journal of Zoology 240(4): 637-658. Mammalogy 92(1): 235-253. R Development Core Team (2012). R: A language Simmons N.B. 2005. Order Chiroptera. in and environment for statistical computing. R Mammal species of the world: a taxonomic and Foundation for Statistical Computing, Vienna, geographic reference (edited by Wilson D.E. Austria. and Reeder D.M.), pp. 312-529. The Johns Hopkins Press, Baltimore. Ramírez B.H. 2009. Establecimiento de la composición biológica y estructura ecológica de Solari, S.; Muñoz-Saba, Y.; Rodríguez-Mahecha, la laguna que conforma el humedal “Laguna El J.V.; Defler, T.R.; Ramírez-Chaves, H.E. and Tinije”, que permitan conocer su dinámica, Trujillo F. 2013. Riqueza, endemismo y estructura y funcionalidad tendiente a su conservación de los mamíferos de Colombia. postulación como área Ramsar. Convenio de Mastozoología Neotropical 20(2): 301-365. Cooperación No. 0126 de 10 de Diciembre de Solari S.; Pacheco V.; Luna L.; Velazco P.M. and 2008. Dirección Técnica de Medio Ambiente, Patterson B.D. 2006. Mammals of the Manu Secretaría de Agricultura, Ganadería y Medio Biosphere Reserve. Fieldiana Zoology 110: 13. Ambiente, Gobernación de Casanare. Soriano P. 2000. Functional structure of bat Asociación de Becarios de Casanare. Informe communities in tropical rainforest and andean Técnico Final. . Yopal. cloud forest. Ecotropicos 13 (1): 1-20. Rényi A. 1961. On measures of entropy and Stevenson P.; Perez J. and Munoz Y. 2004. Estado information. in Proceedings of the 4th Berkeley del conocimiento sobre los mamíferos terrestres Symposium on Mathematical Statistics and y voladores de Colombia. in Informe nacional Probability (edited by Neyman J.), pp. 547-561. sobre el avance en el conocimiento y la University of California Press, Berkeley, United información de la biodiversidad 1998-2004 States of America. Tomo II (edited by Chaves M.E. and Rodríguez M. 2009. Mastofauna. in Santamaría M.), pp. 151-170. Instituto de Establecimiento de la composición biológica y
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Investigación de Recursos Biológicos Alexander von Humboldt, Bogotá D.C. Straube, F. C. and Bianconi, G. V. 2002. Sobre a grandeza e a unidade utilizada para estimar esforço de captura com utilização de redes-de- neblina. Chiroptera Neotropical, Brasília 8(1-2): 150-152. Suárez-Castro, A.F.; Bueno-Castellanos J.C. and Mora--Fernández C. 2013. Mamíferos, in Guía de campo. Flora y fauna de las sabanas inundables asociadas a la cuenca del río Pauto, Casanare--Colombia (edited by Mora- -Fernández C. and Peñuela--Recio L.), pp. 200- 234. Serie Biodiversidad para la Sociedad No. 3. Yoluka ONG, fundación de investigación en biodiversidad y conservación, Fundación Horizonte Verde and Ecopetrol S.A. Timm R.M. and LaVal R.K. 1998. A field key to the bats of Costa Rica. Occasional Publication Series, University of Kansas 22: 1-30. Tóthmérész B. 1995. Comparison of different methods for diversity ordering. Journal of Vegetation Science 6(2): 283-290. Trujillo F.; Garavito-Fonseca J.; K. G.; Rodríguez- Maldonado M.V.; Combariza R.; Solano-Pérez L.; Pantoja G. and Ávila-Guillen J.P. 2011. Mamíferos de Casanare. in Biodiversidad de Casanare: Ecosistémas Estratégicos del Departamento (edited by Usma J.S. and Trujillo F.), pp. 286. Gobernación de Casanare-WWF Colombia, Bogotá. Vargas A. and Patterson B.D. 2007. Comunidades de murciélagos montanos en Bolivia. in Historia natural, distribución y conservación de los murciélagos de Bolivia (edited by Aguirre L.F.), pp. 82-86. Editorial Centro de Ecología y Difusión Simón I. Patiño, Santa Cruz de la Sierra. Vega-Orduz L.F. 2007. Mamíferos de Casanare: Una Aproximación a la riqueza de especies y los ecosistemas donde habitan. Informe Final. Yopal.
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A comparison of habitat use by phyllostomid bats (Chiroptera: Phyllostomidae) in natural forest fragments and Eucalyptus plantations in the Brazilian Cerrado
Sónia M.S. Pina1, Christoph F.J. Meyer1, Marlon Zortéa2,*
1 Centro de Biologia Ambiental, Faculdade de Ciências da Universidade de Lisboa, Campo Grande, 1749-016 Lisboa, Portugal Email: [email protected] 2 Coordenação de Ciências Biológicas, Campus Jataí, Universidade Federal de Goiás – Br 364 Km 195 Jataí, Goiás, Brasil
* Corresponding author: [email protected]
ARTICLE Abstract. Plantation forests are becoming increasingly important Manuscript history: elements of tropical human-modified landscapes, yet their Submitted in 31/Jul/2012 conservation value for many animal taxa remains little explored. We Accepted in 24/Jun/2013 compared phyllostomid bat assemblages in semideciduous forest Available on line in 26/Sep/2014 fragments in Brazilian Cerrado with those of eucalypt plantations Editors: Marco A.R. Mello and Valéria C. Tavares (Eucalyptus spp.). Specifically, we assessed differences in species richness, diversity, abundance, and species composition between habitat types and evaluated phyllostomid bat responses with respect to a variety of landscape characteristics and local-scale variables. Bats were sampled with mist nets in four replicates each of Eucalyptus plantations and fragments of native Cerrado. Of the total of 209 individuals captured, 75 were caught in plantations and 134 in native forest areas. Cerrado assemblages were characterized by higher species richness, diversity, and evenness compared to those in Eucalyptus plantations. Gleaning animalivorous phyllostomids seem to be most sensitive to plantation forests, as they were not captured in this habitat. Non-metric multidimensional scaling indicated no strong separation between habitat types and there were no significant differences in species composition based on an analysis of similarities. The proportion of forest cover (both Cerrado and Eucalyptus) in the landscape was the only landscape-scale variable which had a significant influence on species composition. In contrast, species composition was unrelated to geographical distance between forest fragments. A generalized linear mixed effects model for the three most frequently captured species (Carollia perspicillata, Artibeus planirostris, Platyrrhinus lineatus) only showed significant differences in abundance for Artibeus planirostris, the species being more abundant in native Cerrado. Our results demonstrate the impoverishment of bat assemblages in Eucalyptus plantations and highlight the importance of examining the effects of habitat conversion at the individual species level as responses are often species-specific.
Keywords: Bat assemblages; Cerrado; Chiroptera; Eucalyptus; landscape structure; Savanna
! ecosystem highly attractive for large-scale Introduction agricultural development and livestock farming The tropical savanna ecoregion of Brazil, also (Felfili et al. 2004; Klink & Machado 2005; 2 known as Cerrado, occupies around 2 million km Ferreira et al. 2009). and is the second largest Neotropical ecosystem Habitat loss and forest fragmentation are the (Machado et al. 2004). It is characterized by a two main consequences of intense human pressure complex and stratified vegetation, seasonal experienced in the tropics in the last decades climate and smooth topography that make this
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(Ewers & Didham 2006). Fragmentation and forests have a fairly short history and are much isolation of natural habitats are the main threats to less extensive than research in radiata pine regional and global biodiversity (Bianconi et al. plantations (Danielsen & Heegaard 1995; 2006; Klingbeil & Willig 2009). Reforestation, for Bernhard-Reversat 2001; Borsboom et al. 2002; vegetal coal, paper and cellulose production, is Lindenmayer et al. 2003; Barlow et al. 2007). contributing to the increase of large Eucalyptus Vertebrate assemblages in eucalypt plantations monocultures, which are replacing the native have been shown to be less diverse than those in Cerrado vegetation (Pereira & Oliveira 2005). In native vegetation, largely because of their relative the state of Goiás for instance, in the last years structural simplicity (Lindenmayer et al. 2003). several agricultural and livestock farming areas On the other hand, Barlow et al. (2007) concluded have been replaced by Eucalyptus plantations. that Eucalyptus plantations can help preserving a ABRAF (2011) estimated the planting of almost limited number of forest species. Most of the 60 000 hectares of Eucalyptus in this state alone. studies conducted in tree plantations are on bird Bats have been considered excellent communities (Marsden et al. 2001; Zurita et al. bioindicators of human-induced changes in habitat 2006; Hsu et al. 2010), whereas only a few quality (Jones et al. 2009). In Neotropical forests, focused on bat assemblages (Harvey & Villalobos Chiroptera may represent a keystone taxon due to 2007; Borkin & Parsons 2010). Harvey & the pollination and seed dispersal services they Villalobos (2007) showed that cacao and banana provide (Willig et al. 2007; Kunz et al. 2011). agroforestry systems in Costa Rica maintained bat Moreover, bats are an ideal model taxon for and bird assemblages similar to those observed in evaluating responses to habitat fragmentation as native forest areas. By contrast, Reis et al. (2006) they are ecologically highly diverse and mobile, revealed a less species-rich and structurally with the potential to move over extensive areas of simplified bat assemblage in Araucaria plantations fragmented landscapes (Meyer & Kalko 2008). compared to native forest, in a study on bats in Habitat fragmentation is a dominant Brazil. However, comparable studies for bats in characteristic of modern landscapes (Ewers & Eucalyptus plantations are lacking. Didham 2006), and recent studies have Thus, the overall goal of this work was to emphasized the importance of investigating bat investigate differences in bat diversity and species responses within the greater landscape abundance between eucalypt plantations and context by examining how species respond to fragments of native Cerrado. Specifically, we landscape composition (e.g. the amount of forest aimed to (a) compare bat species richness, cover) and configuration (e.g. edge density, mean diversity, and abundance between Cerrado nearest-neighbor distance) (Klingbeil & Willig fragments and Eucalyptus plantations and assess 2009; Meyer & Kalko 2008). differences in bat assemblage structure and Studies investigating fragmentation effects on composition between the two types of habitat; (b) tropical bats to date have produced somewhat test for an effect of habitat amount (landscape equivocal results. It has been demonstrated that composition) and spatial arrangement of forest bat assemblages tend to be less diverse and patches (landscape configuration) on bat species dominated by fewer species in fragmented habitats composition. with reduced forest cover (Faria 2006). Materials and Methods Neotropical bats respond to habitat fragmentation in a species-specific manner (Klingbeil & Willig Study area 2009) and at least two general trends in response Field work was carried out in Jataí (7º52'33" S; to logging and habitat fragmentation are evident. 51º43'14"W) in the southwest of the state of Gleaning animalivorous phyllostomids often Goiás, central Brazil, with altitudes of ca. 700 m decrease in abundance and species richness (Fig. 1). The climate is typical of tropical savanna whereas, in contrast, frugivorous and Aw, according to the classification of Kӧppen nectarivorous phyllostomids, often exhibit greater (1948), and divided into two well-defined seasons: abundances in forests that have been subjected to the dry season (May-September) and the wet logging or habitat disruption (Clarke et al. 2005; season (October-April), with average annual Castro-Arellano et al. 2007; Willig et al. 2007; precipitation of 600-2000 mm (Felfili et al. 2005; Meyer & Kalko 2008; Bobrowiec & Gribel 2010). Lima & Silva 2005). Little information is available on the The study area is located in the Brazilian conservation value of commercial tree plantations savannas known as Cerrado (sensu lato). This (Zurita et al. 2006) and production landscapes are biome is characterized by high spatial rarely considered priority areas for biodiversity heterogeneity and encompasses several conservation in the tropics (Barlow et al. 2007). physiognomic units. Cerrado includes a set of Studies on the conservation value of eucalypt vegetation types, ranging from more open plantations (Eucalyptus spp.) and other plantation formations with sparse trees and shrubs to ones
! 15 ! ! Chiroptera Neotropical 19(3) Special Volume: 14-30, December 2013 with a more closed canopy (cerradão). All sclerophyllous leaves (Felfili et al. 2004; Salgado- vegetation formations have an understory Labouriau 2005). The dominant vegetation in this dominated by shrubs and low, tortuous trees with region is semideciduous forest (Fig. 2).
Figure 1. Localization of the study area (Jataí, Goiás State – Brazil) and aerial photos of each type of habitat a) Eucalyptus plantations; b) semideciduous forest fragment. (Source: Fabiano R. Melo).
Figure 2 – Sampling areas (Euca = Eucalyptus plantations; F – Forest fragments). (Source: Google Earth (December 2010)).
differed in size, ranging from 150 ha to 378.2 ha Site selection and were generally irregularly shaped. Most sites We selected four fragments of each habitat were located near a road (<1.5 km) and type, Eucalyptus plantations and semideciduous surrounded by soybean and sugar cane plantations forest fragments (Cerrado). These fragments and cattle pastures.
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Bat sampling Jackknife 1 and eH were also calculated using Bats were sampled monthly (eight capture EstimateS. nights per month) between December 2010 and To compare rarefied species richness, April 2011 using 10 ground-level mist-nets per dominance, and evenness (Hurlbert’s probability night (dimension: 12 x 2.5 m, 16 mm mesh) that of interspecific encounter - Hurlbert’s PIE) were set along linear transect lines within each between the different types of habitats we used fragment. All sites were sampled during the week EcoSim software (Gotelli & Entsminger 2001). of new moon to minimize potential bias in capture Statistical significance was assessed based on the success as a result of lunar-phobic behavior (e.g. simulated 95% confidence intervals, using 1000 Morrison 1978). Mist nets were opened at sunset iterations (Gotelli & Entsminger 2001). and checked every 20 to 30 minutes for four Comparisons between habitat categories were hours. After capture, bats were placed in made at the abundance level of the one with individual cotton bags. The following standard lowest abundance, which were 75 individuals in measurements and data were recorded: weight this case for Eucalyptus. (recorded to the nearest 0.1 g with a digital scale), To determine variation in compositional forearm length (measured with a caliper to 0.01 structure of bat assemblages among sites, we mm), sex, and reproductive status. Bats were employed non-metric multidimensional scaling always released at the same site of capture. Bats (NMDS) based on a matrix of Bray-Curtis were usually identified in the field, however, in dissimilarities (Magurran 2004). NMDS is a some cases voucher specimens were collected robust, nonlinear ordination technique regarded as (IBAMA License number 35128167) for later an effective method for analyzing ecological taxonomic identification in the laboratory. These community data (McCune & Grace 2002). were deposited in the Laboratório de Zoologia do Statistical differences in species composition Campus Jataí, Universidade Federal de Goiás. between the two types of habitats were assessed Bats were mostly identified using Vizotto & using an analysis of similarity (ANOSIM; Taddei (1973) and Gardner (2007). For some taxa, McArdle & Anderson 2001; Clarke 1993), again additional literature was consulted: Platyrrhinus using the Bray-Curtis index as distance measure. (Ferrell & Wilson 1991); small Artibeus (Handley Calculations of NMDS and ANOSIM were 1987); Sturnira (Davis 1980); Myotis (Laval performed using PAST software (Hammer et al. 1973). 2001). Data analysis Differences in species abundance between The analysis was restricted to bats of the habitat types were assessed using generalized family Phyllostomidae to avoid biases associated linear mixed-effects models (GLMMs) (Zuur et al. with the use of ground-level mist nets as this 2009). Models were fitted using maximum capture method generally undersamples bats from likelihood estimation as implemented in the ‘lmer’ other Neotropical bat families (e.g. Kalko 1998; function in the R package ‘lme4’ (Bates et al. Zortéa et al. 2010). 2011), assuming a Poisson error distribution and log-link function. Habitat type was included as a Species richness, diversity, abundance, and fixed effect and individual sites and capture nights composition (nested within sites) were specified as random, Capture effort was calculated following which allowed to appropriately control for Straube & Bianconi (2002) as m2net h and relative pseudoreplication within a site and to account for abundance was measured as individuals/m2net h. site-specific variance. Statistical significance of Species inventory completeness for each the fixed effect ‘habitat’ was determined based on fragment and habitat type was assessed using a likelihood ratio test (Zuur et al. 2009). Because sample-based species accumulation curves the number of captures was very low for most of (Gotelli & Colwell 2001). Computations were the species, this analysis was restricted to Carollia made with the Mao Tao function implemented in perspicillata, Artibeus planirostris, and EstimateS 8.2.0 (Colwell 2009). In addition, we Platyrrhinus lineatus, the ones with sufficient data assessed the number of species expected to occur (more than 20 captures in total). at each site using a nonparametric species-richness Bat species composition and landscape structure estimator. We chose the first-order Jackknife We calculated a range of local and landscape (Jack1), which takes movement heterogeneity of metrics for each of the eight fragments using the mobile animals such as bats into account, based on software ImageJ 1.45j and Google Earth. The the work developed by Brose & Martinez (2004). local-scale variables measured were: (1) fragment Comparisons of diversity between Eucalyptus area (ha), (2) total length of edge (=perimeter, m), plantations and Cerrado fragments were based on (3) nearest straight-line distance (m) between two the exponential form of the Shannon index (eH).
! 17 ! ! Chiroptera Neotropical 19(3) Special Volume: 14-30, December 2013 fragment edges and (4) nearest straight-line Artibeus lituratus with 15 captures (10%) and distance between the center of each fragment. Sturnira lilium with 14 captures (7%). Taken In addition, we calculated the following together, the other species only represented 14% landscape-level metrics for a focal scale of 3 km of captures. circles (1.5 km radii) centered on each fragment to We captured 75 individuals in the Eucalyptus describe landscape structure: (1) mean patch size, sites. Carollia perspicillata was the most abundant (2) number of patches of eucalyptus (n.frag.euca), species with 48 individuals, followed by P. Cerrado (n.frag.forest), and total forest lineatus, with 8 individuals. In native forest we (n.frag.total), (3) patch density of eucalyptus captured 134 individuals, and C. perspicillata (dens.euca), Cerrado (dens.forest) and total forest comprised again most captures (44 individuals), (dens.total), and (4) proportion of forest cover of followed by Artibeus planirostris (35) and P. eucalyptus (p.euca.cover), Cerrado (p.forest.cover) lineatus (13). Overall, frugivores accounted for the and total forest (p.total.cover). This focal scale majority of captures (Table 2), and insectivores was adapted from that of Klingbeil & Willig and carnivores were exclusively caught in native (2009) and Meyer & Kalko (2008) to our forest areas. particular study area. We chose a focal scale of 3 Of the total of 12 phyllostomid species km to minimize spatial overlap between recorded, all were found in Cerrado, and four neighboring fragments and spatial autocorrelation species were unique to this type of habitat: among sampling locations (Fig. 2). Chrotopterus auritus, Lophostoma brasiliense, To assess the effect of these environmental Sturnira tildae, and Platyrrhinus incarum. In variables on bat species composition we contrast, only eight species were captured in performed a permutational multivariate analysis of eucalypt plantations (Table 1, Fig. 3). Exponential variance (PERMANOVA) using the ‘adonis’ Shannon diversity was also substantially lower for function in the R package vegan (Oksanen et al. plantation forests (eH = 3.62) than Cerrado (eH = 2011). Of the original suite of predictor variables, 6.23). only six (fragment area, perimeter, proportion of Expected species accumulation curves suggest Cerrado cover, proportion of eucalyptus cover, that sampling effort was satisfactory, although number of forest patches, and number of more species would clearly be detected with eucalyptus patches) were retained after pairwise increasing sampling effort (Fig. 4a). Based on the comparisons in order to avoid multicollinearity Jackknife 1 estimator we achieved a level of problems among explanatory variables. Predictor species inventory completeness of 80.8% for variables were standardized to zero mean and unit Cerrado (Sexp 14.85 species) and 73.7% for variance prior to analysis to adjust for differences Eucalyptus assemblages (Sexp 10.85 species) (Fig. in magnitude. Permutations were specified to 4b). occur only within habitats and not among habitat Rarefied bat species richness was significantly types to take into account the nestedness of the higher for Cerrado than for Eucalyptus, as study design. indicated by the 95% confidence intervals (Fig. 5). We used a Mantel test with 5000 permutations Cerrado assemblages also were characterized by to test for an effect of geographic distance on significantly greater evenness and lower species composition. The test was based on a dominance compared to those in plantations (Fig. Bray-Curtis dissimilarity matrix for species 5). These differences were also apparent when abundances and a matrix of Euclidean distances looking at the respective rank-abundance for geographical distances (Appendix B). distributions (Fig. 3). All these analyses were performed using the R In the species-level GLMM analyses, only statistical package (R Development Core Team, Artibeus planirostris showed a significant effect of 2010). habitat, being significantly more abundant in Results native forest areas than in Eucalyptus plantations (Table 3). A total of 209 bats belonging to two families, nine genera, and 13 species were captured during In the NMDS ordination (stress = 0.192), three 40 sampling nights (Table 1). Phyllostomid bats sites in Eucalyptus and 3 Cerrado fragments were the most captured (97%) and represented the loosely grouped together along dimension 2, majority of species (92%). Vespertilionidae was however no clearly distinct clusters were the only other family registered, with seven identifiable as species composition was quite captures of Myotis nigricans. variable among sites (Figure 6). Species composition did not differ significantly between Carollia perspicillata was the most abundant habitat types as indicated by the ANOSIM (global species with 92 captures, equivalent to 44% of the R = 0.094, P = 0.286). total, followed by A. planirostris with 39 captures (19%), P. lineatus with 21 captures (10%),
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0.01$
net(h)( Eucalyptus$ 2
0.001$ Cerrado$
0.0001$ Relative(abundance((m
0.00001$
Species(
Figure 3. Rank-abundance plots for phyllostomid bats captured in Eucalyptus plantations and Cerrado fragments in Jataí – Goiás
! Table 1 – Number of bat species captured in native forest areas and Eucalyptus monoculture plantations in the southwest of Goiás, Brazil. Family Subfamily Species Eucalyptus Cerrado Ensemble Phyllostomidae Phyllostominae Chrotopterus auritus 0 1 Ca Phyllostomus hastatus 3 4 Om Lophostoma brasiliense 0 3 In Stenodermatinae Artibeus planirostris 4 35 Fr Artibeus lituratus 5 10 Fr Artibeus cinereus 1 4 Fr Sturnira lilium 5 9 Fr Sturnira tildae 0 1 Fr Platyrrhinus lineatus 8 13 Fr Platyrrhinus incarum 0 1 Fr Desmodontinae Desmodus rotundus 1 2 Sa Carolliinae Carollia perspicillata 48 44 Fr Vespertilionidae Myotinae Myotis nigricans 0 7 In Total 75 134 Observations: Ca = Carnivores, Om = Omnivores, In = Insectivores, Fr = Frugivores, Sa = Sanguinivores ! Of the local- and landscape-scale metrics percentage of forest cover in the landscape on bat considered, species composition was only assemblage structure. significantly related to the proportion of forest Species composition was not significantly cover of Cerrado (PERMANOVA, R2 = 0.26, P = correlated with geographic isolation, irrespective 0.054), respectively, Eucalyptus (R2 = 0.28, P = of how it was quantified (Mantel test; nearest 0.040; Table 4), suggesting an overall effect of straight-line distance (a) between fragment
! 19 ! ! Chiroptera Neotropical 19(3) Special Volume: 14-30, December 2013
Table 2 – Species richness (S), number of captures (N) and relative abundance (%) of bat ensembles for Eucalyptus plantations and for areas of Cerrado in the southwest of Goiás, Brazil. Eucalyptus Cerrado Total
Ensemble S N % S N % S N %
Frugivores 6 71 95 8 117 87 8 188 90.0
Insectivores 0 0 0 2 10 7 2 10 4.8
Omnivores 1 3 4 1 4 3 1 7 3.3
Sanguivores 1 1 1 1 2 2 1 3 1.4
Carnivores 0 0 0 1 1 1 1 1 0.5
! ! ! Table 3 – Results of generalized linear mixed-effects models examining the influence of habitat type on phyllostomid bat species abundances. Species GLMM Parameter estimate Likelihood ratio ± SE test Chi 0.0059 Carollia perspicillata Df 1 Pr (> Chisq) 0.9388 Intercept 0.0026 ± 1.218 Chi 5.0185 Artibeus planirostris Habitat_Cerrado 0.0603 ± 1.376 Df 1 Pr (> Chisq) 0.0251 Chi 0.6521 Platyrrhinus lineatus Df 1 Pr (> Chisq) 0.4192 ! ! !
15
16
10 12 (Mao Tau) s b
o 8
S 5
Habitat 4 Cerrado Habitat 0 Eucalyptus Cerrado Estimated species richness (Jackknife1) Eucalyptus 0 50 100 0 50 100 Number of individuals Number of individuals !
Figure 4. (a) Expected species accumulation (Mao Tau) curves (plus 95% confidence interval curves) and (b) accumulated number of species based on the Jackknife 1 estimator (mean ± SD) for Eucalyptus and Cerrado fragments.
! 20 ! ! Chiroptera Neotropical 19(3) Special Volume: 14-30, December 2013
Table 4 – Results of a permutational multivariate analysis of variance (PERMANOVA) relating bat species composition to various landscape-level predictor variables (area, perimeter, p.forest.cover, p.euca.cover, n.frag.forest, n.frag.euca). See Appendix A for the complete names of predictor variables. Df SumsOfSqs MeanSqs F.Model R2 Pr (>F) area 1 0.055 0.055 0.753 0.055 0.617 perimeter 1 0.129 0.129 1.765 0.130 0.221 p.cober.mata 1 0.287 0.287 3.907 0.286 0.054 p.cober.euca 1 0.266 0.266 3.620 0.266 0.040 n.frag.mata 1 0.088 0.088 1.193 0.088 0.393 n.frag.euca 1 0.099 0.099 1.352 0.099 0.316 Residuals 1 0.073 0.073 0.074 Total 7 0.997 1.000
Figure 5 – Comparison of phyllostomid species richness, evenness (Hurlbert’s PIE), and dominance, rarefied to equal abundances, in Cerrado fragments and eucalyptus plantations. Error bars represent 95% confidence intervals.
0.32 F1
Euc a 4 0.24 F2
0.16
0.08 !!
0
NMDS2 F3 Coordinate 2 Coordinate
-0.08 F4 Euc a 3
-0.16
-0.24 ! ! Euc a 1
-0.32
Euc a 2 -0.4 -0.5 -0.4 -0.3 -0.2 -0.1 0 0.1 0.2 0.3 0.4 Coordinate 1
NMDS 1
Figure 6 – Non-metric multidimensional scaling (NMDS) ordination of phyllostomid bat assemblages in fragments of native forest and eucalyptus plantations, Jataí, Brazil.
! 21 ! ! Chiroptera Neotropical 19(3) Special Volume: 14-30, December 2013
centers: R = 0.082, P = 0.661, (b) between The decline in bat species richness, lower fragment edges: R = 0.081, P = 0.328). diversity, and increase in the proportion of dominant species observed in our study may Discussion similarly be related to the dependence of certain According to previous studies conducted species on native forest habitats. Four in the Cerrado biome, local bat species richness phyllostomid bats were unique to Cerrado, may range from 15 to 25 species when mist nets including two gleaning animalivorous species (L. are employed or when inventories are based on brasiliense and C. auritus), which were not captures in caves (Zortéa & Alho 2008). Similar captured in Eucalyptus. Compared to native forest, levels of species richness have also been phyllostomid assemblages in Eucalyptus thus were documented for the Goiás region (Zortéa et al. not only taxonomically but also functionally 2010, Rodrigues et al. 2002). Thus, species impoverished, and dominated by a few generalist richness observed in this study was lower (N=13) species. Eucalypt forest may not offer the specific than expected, representing only 12.9 % of the habitat or resource requirements of specialist species known to occur in Cerrado according to species such as the gleaning insectivorous L. the list compiled by Paglia et al. (2012). Possible brasiliense (Smith, 2008). explanations for this discrepancy could be the Richness and abundance patterns of animals in influence of factors that may directly affect bat tree plantations may be influenced by several abundance and diversity such as the scarcity of factors such as plantation age, climate, type of adequate roosting sites, increasing lack of native biome, and the presence or absence of understory habitat, and a modified floristic composition due vegetation (Marsden et al. 2001, Bernhard- to human land use change. Moreover, additional Reversat 2001). Our four fragments of Eucalyptus sampling methods such as diurnal roost searches were characterized by the presence of a sparse and acoustic sampling with ultrasound detectors understory. According to Marsden et al. (2001), (Kunz & Parsons 2009), together with an increase species poverty of birds in Eucalyptus plantations in sampling effort, likely would have considerably may be the result of intensive management and augmented the number of species detected. removal of the understory vegetation. A well- Dominant species vary geographically, however, developed understory generally makes plantations species such as C. perspicillata and large Artibeus less hostile (e.g. Barlow et al. 2007), and may be have been cited as the most common ones in crucial for ensuring that species, in particular Neotropical bat assemblages (Zortéa & Alho shrub-frugivores such as Carollia, use plantations 2008). Carollia perspicillata was the most not only for commuting, but also as feeding and abundant species in this study with 44% of shelter areas. captures, followed by A. planirostris and P. lineatus. These three species are all frugivorous Comparing forests and agroforestry systems of and, as pointed out by Aguiar & Zortéa (2008), banana and cacao, Harvey & Villalobos (2007) generally are among the most frequently captured found that bat species richness was similar in both bats in the Cerrado. The occurrence of the habitats, however some subtle differences were vampire-bat Desmodus rotundus was expected detected such as a greater number of nectarivorous since potential food was available due to the bats in agroforestry systems compared to forests. extensive conversion of marginal habitat into The authors presented several reasons, which grassland for cattle ranching (Greenhall et al., combined, could explain the high level of 1983; Zortéa & Alho 2008). biodiversity in agro-forestry systems, including a canopy structurally similar to the forest, the As expected, the replacement of native forests abundance of food resources (fruit, nectar, and by Eucalyptus plantations influenced bat species insects) and close proximity between forest richness and diversity. In our study, the fragments and agroforestry systems. differences in species richness were significant and native forest areas had greater species richness Many studies have highlighted the importance than eucalypt monocultures. A reduction in of conserving native forest fragments within species richness has been found for a range of taxa plantations. In general, the larger the patches of and in different types of (sub)tropical tree retained native vegetation within plantations the plantations, for instance for birds in eucalypt more species of vertebrates they support plantations in Atlantic Forest (Marsden et al. (Lindenmayer et al. 1999). However, retained 2001) and “Cerradão” (Gabriel et al. 2009) in patches do not always have to be large to be Brazil, in Pinus plantations in Atlantic forest in effective in conserving biodiversity (Lindenmayer Argentina (Zurita et al., 2006), and for bats in et al. 2003). The presence of native forest patches rubber and oil palm plantations in Indonesia near plantations may lead to an increase in species (Danielsen & Heegaard, 1995). richness in tree plantations, as Zurita et al. (2006) found for birds. In our study landscape there were
! 22 ! ! Chiroptera Neotropical 19(3) Special Volume: 14-30, December 2013 various small and medium-sized Cerrado investigating bat responses to landscape fragments embedded in or immediately adjacent to characteristics have likewise found the amount of the plantations, which therefore could be forest cover to be the best predictor of assemblage contributing to the richness observed in composition (Meyer & Kalko 2008) or as Eucalyptus. predictors of individual species or ensemble- The species-level analyses suggest that only specific responses (Klingbeil & Willig 2009). Our A. planirostris responded negatively to habitat results suggest that the absence of a significant conversion while there was no statistically influence of the local-scale variables on species significant effect for C. perspicillata and P. composition may be due to the proximity of lineatus. This may reflect general morphological patches of native vegetation (Cerrado) to the and ecological differences among these species, plantations sampled and generally high structural for instance concerning food, shelter, and connectivity conferred by the landscape matrix. preferred habitat type, as well as patterns of The importance of area effects has been found resource availability and abundance. Since C. to vary considerably between studies and to be perspicillata is a species that is well-known for its greatly dependent on the surrounding matrix. As considerable ecological plasticity (Fleming 1988) in previous work (Faria, 2006), we also found that it is not surprising that no effect of habitat type on fragment size had no significant effect on species abundances was observed. In contrast, for A. composition. Many bat species seem to be able to planirostris our data suggest that Eucalyptus persist in fragmented landscapes due to their plantations probably do not meet the species’ ability to explore the mosaic of modified habitats habitat and resource requirements in terms of food in the matrix and perform long-distance and shelter. This may be due to the lack of a well- movements (Faria, 2006). However, Faria (2006) developed understory, simplified vegetation adds that species may react in different ways to structure, and lack of adequate food resources different matrix components. Fischer & compared with patches of native Cerrado. Lindenmayer (2002) found no significant Eucalyptus areas likely serve as ecological relationship between bird species richness and the corridors that many bat species use merely for area of Eucalyptus fragments in a matrix of pine commuting between shelters and feeding areas. plantations (Pinus radiata) in Australia, whereas a The results from our species-level analyses should significant relationship was observed in a pasture be interpreted with some caution as the low matrix. This may reflect differences in sample sizes reduced the statistical power to detect connectivity between habitats due to differences in differences and in general limited our ability to matrix quality and permeability, as Estrada & assess species-specific responses to just a few of Coates-Estrada (2002) documented in a study in the most common species. Species may react in Mexico, where they observed that bats avoid a different ways to structural and compositional matrix composed only of pasture. features of the landscape and especially for the Conclusions examination of individual species responses it would be desirable that future studies employ an This study, conducted in a Cerrado area in increased sampling effort and also extend southwestern Goiás, represents a first attempt to sampling towards the dry season (May to identify the responses of bat assemblages to September) to be able to uncover potential conversion of native Cerrado habitat to eucalypt seasonal effects. plantations and to resulting changes in landscape structure. Our results provide evidence for the We predicted that bat assemblages in impoverishment of bat assemblages in Eucalyptus plantations forests would be poorer in species and plantations, suggesting that conservation measures characterized by lower species abundance than should be preferentially directed towards the those in native forest fragments and consequently preservation of native forest habitat. A richer bat expected to also find significant differences in fauna in eucalypt plantations could likely be species composition. However, the differences maintained if certain management options were found were only tenuous and not statistically considered by plantation managers, such as the significant based on ANOSIM. Our finding of a preservation of species-rich and well-developed lack of a significant relationship between the native understory vegetation. In addition, ensuring geographic distances of the study fragments and the presence of fragments of native forest of species composition is in line with results from appropriate size in the vicinity of plantations may other studies (e.g. Klingbeil & Willig 2009). Of help to mitigate some of the negative impacts of the range of local and landscape-scale variables plantation forestry on disturbance-sensitive tested, we found that only the proportion of forest species like gleaning animalivorous bats. Further, cover (Eucalyptus and forest) was significantly more in-depth studies across a range of correlated with variation in compositional geographical localities are necessary to ascertain structure of bat assemblages. Previous studies
! 23 ! ! Chiroptera Neotropical 19(3) Special Volume: 14-30, December 2013 to what extent bats do make use of Eucalyptus reference to Eucalypts. Center for International plantation forests. Forestry Research, Indonesia. Acknowledgements Bianconi G.V.; Mikich S.B. & Pedro W.A. 2006. Movements of bats (Mammalia, Chiroptera) in We thank Fabiano Melo of Universidade Atlantic Forest remnants is southern Brazil. Federal de Goiás and the Center for Revista Brasileira de Zoologia 23: 1199-1206. Environmental Biology, University of Lisbon for logistic support. We gratefully acknowledge the Bobrowiec P.E.D. & Gribel R. 2010. Effects of farm owners for permission to work on their land. different secondary vegetation types on bat We further thank the people who helped with field community composition in Central Amazonia, work: Vinycio Carrijo, Diego Afonso, Daniel Brazil. Animal Conservation 13: 204-216. Santos, Paola Da Mata, Wagner Filho, Felipe Borkin K.M. & Parsons S. 2010. The importance Zenha, Laura Marcon and Tiago Dores. We thank of exotic plantation forest for the New Zealand Marco Mello and Valéria Tavares for inviting us long-tailed bat (Chalinolobus tuberculatus). to contribute to this special issue. Valéria Tavares New Zealand Journal of Zoology 37: 35–51. and two anonymous reviewers provided helpful Borsboom A.C.; Lees J.W.N.; Mathieson M. & comments on an earlier version of the manuscript. Hogan L. 2002. Measurement and integration of We dedicate this work to the memory of our fauna biodiversity values in Queensland mentor, friend, and colleague Elisabeth Kalko. agroforestry systems. A report for the RIRDC/ References Land and Water Australia/ FWPRDC Joint Venture Agroforestry Program Supported by the Aguiar L.M.S. & Zortéa M. 2008. A diversidade Natural Heritage Trust. Rural Industries de morcegos conhecida para o cerrado. IX Research and Development Corporation 02 Simpósio Nacional Cerrado. II Simpósio (044). Internacional Savanas Tropicais. Brasília. Brose U. & Martinez N. D. 2004. Estimating the ABRAF. 2011. Anuário estatístico da ABRAF ano richness of species with variable mobility. base 2010. ABRAF – Associação Brasileira de Oikos 105: 292-300. Produtores de Florestas Plantadas, Brasília. Castro-Arellano I.; Presley S.J.; Saldanha L.N.; Alho C.J.R. 2005. Desafios para a conservação do Willig M.R. & Wunderle Jr. J.M. 2007. Effects Cerrado face às atuais tendências de uso e of reduced impact logging on bat biodiversity in ocupação. In: Cerrado: Ecologia, Biodiversidade terra firme forest of lowland Amazonia. e Conservação (edited by Scariot A.; Silva Biological Conservation 138: 269-285. J.C.S. & Felfili J.M.), pp. 369-381. Ministério do Meio Ambiente, Brasília-DF. Clarke K. R. 1993. Non-parametric multivariate analyses of changes in community structure. Barlow J.; Gardner T.A.; Araujo I.S.; Ávila-Pires Australian Journal of Ecology 18: 117-143. T.C.; Bonaldo A.B.; Costa J.E.; Esposito M.C.; Ferreira L.V.; Hawes J.; Hernandez M.I.M.; Clarke F.M.; Rostant L.V. & Racey P.A. 2005. Hoogmoed M.S.; Leite R.N.; Lo-Man-Hung Life after logging: post-logging recovery of a N.F.; Malcolm J.R.; Martins M.B.; Mestre neotropical bat community. Journal of Applied L.A.M.; Miranda-Santos R.; Nunes-Gutjahr Ecology 42: 409-420. A.L.; Overal W.L.; Parry L.; Peters S.L.; Cloutier D. & Thomas D.W. 1992. Carollia Ribeiro-Junior M.A.; da Silva M.N.F.; da Silva perspicillata. Mammalian Species 417: 1-9. Motta C. & Peres C. A. 2007. Quantifying the Colwell R. K. 2009. EstimateS: Statistical biodiversity value of tropical primary, estimation of species richness and shared secondary, and plantation forests. PNAS 104: species from samples. Version 8.2. User's Guide 18555-18560. and application available at: http://purl.oclc.org Barlow J.; Araujo I.S.; Overal W.L.; Gardner /estimates T.A.; Mendes F.S.; Lake I.R. & Peres C.A. Danielsen F. & Heegaard M. 1995. Impact of 2008. Diversity and composition of fruit-feeding logging and plantation development on species butterflies in tropical Eucalyptus plantations. diversity: a case study from Sumatra. In: Biodiversity and Conservation 17: 1089-1104. Management of tropical forests: towards an Bates D.; Maechler M. & Bolker B. 2011. Lme4: integrated perspective (edited by Sandbukt), pp. Linear mixed-effects models using S4 classes. R 73-92. Oslo: Centre for Development and the package version 0.999375-39. Available at: Environment, University of Oslo. http://CRAN.R-project.org/package=lme4 Davis W.B. 1980. New Sturnira (Chiroptera: Bernhard-Reversat F. 2001. Effect of exotic tree Phyllostomidae) from Central and South plantations on plant diversity and biological soil America, with key to currently recognized fertility in the Congo Savanna: with special species. Occasional Papers, Museum of Texas, Tech University 70: 1 - 5.
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Salgado-Labouriau M.L. 2005. Alguns aspectos Willig M.R.; Presley S.J.; Bloch C.P.; Hice C.L.; sobre a Paleoecologia dos Cerrados. In: Yanoviak S.P.; Díaz M.M.; Chauca L.A.; Cerrado: Ecologia, Biodiversidade e Pacheco V. & Weaver S.C. 2007. Phyllostomid Conservação (edited by Scariot A.; Silva J.C.S. bats of Lowland Amazonia: effects of habitat & Felfili J.M.), pp. 109-118. Ministério do Meio alteration on abundance. Biotropica 39: 737- Ambiente, Brasília-DF. 746. Schipper J.; Chanson J.S.; Chiozza F.; Cox N.A.; Willig M.R. & Hollander R.R. 1987. Vampyrops Hoffmann M.; et al. 2008. The status of the lineatus. Mammalian Species 275: 1-4. World's land and marine mammals: diversity, Zortéa M. 1993. Folivory in Platyrrhinus threat, and knowledge. Science 322: 225-230. (Vampyrops) lineatus (Chiroptera: Simmons N.B. 2005. Order Chiroptera. Mammal Phyllostomidae). Bat Research News 39: 59-60. Species of the World: A Taxonomic and Zortéa M. 2007. Subfamília Stenodermatinae. In: Geographic Reference (edited by Wilson D.E. & Morcegos do Brasil (edited by Reis N.R.; Reeder D.M.), pp. 312-529. Johns Hopkins Peracchi A.L.; Pedro W.A. & Lima I.P.), pp. University Press. 107-127. Londrina. Smith P. 2008. Pygmy round-eared bat Zortéa M.; de Mel F.R.; Carvalho J.C. & Rocha Lophostoma brasiliense. Mammals of Z.D. 2010. Morcegos da Bacia do rio Corumbá, Paraguay. 28: 1-6. Goiás. Chiroptera Neotropical 16: 611-617. Straube F.C. & Bianconi G.V. 2002. Sobre a Zortéa M. & Alho, C.J.R. 2008. Bat diversity of a Grandeza e a unidade utilizada para estimar Cerrado habitat in central Brazil. Biodiversity esforço de captura som utilização de redes-de- and Conservation 17: 791-805. neblina. Chiroptera Neotropical 8: 150-152. Zurita G.A.; Rey N.; Varela D.M.; Villagra M. & Umetsu F. & Pardini R. 2007. Small mammals in Bellocq M.I. 2006. Conversion of the Atlantic a mosaic of forest remnants and anthropogenic Forest into native and exotic tree plantations: habitats – evaluating matrix quality in an Effects on bird communities from the local and Atlantic forest landscape. Landscape Ecology regional perspectives. Forest Ecology and 22: 517-530. Management 235: 164-173. Vizotto L. D. & Taddei V.A. 1973. Chave para Zuur A F.; Ieno E.N.; Walker N.J.; Saveliev A.A. determinação de quirópteros brasileiros. & Smith G.M. 2009. Mixed effects models and Publicação da Faculdade de Filosofia, Ciências extensions in ecology with R. Springer, New e Letras de São José do Rio Preto, São José do York. Rio Preto.
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Appendices
Appendix A - Summary table of patch-level characteristics and landscape metrics for each study site. Area (fragment area (ha)), edge length (total edge length (m)), p.forest.cover (proportion of forest cover of Cerrado), p.euca.cover (proportion of forest cover of eucalyptus), p.total.cover (total proportion of forest cover), dens.forest (density of Cerrado patches), dens.euca (density of eucalyptus patches), dens.total total (total patch density), n.frag.forest (number of patches of Cerrado), n.frag.euca (number of patches of eucalyptus), n.frag.total (total number of patches), NMDS1 (scores NMDS axis 1), NMDS2 (scores of NMDS axis 2), Sobs (observed species richness).
Patch area edge length p.forest.cover p.euca.cover p.total.cover dens.forest dens.euca dens.total n.frag.forest n.frag.euca n.frag.total NMDS1 NMDS2 Sobs F1 172.7 5776 0.2611 0 0.2611 0.0028 0 0.0028 2 0 2 0.03965 -0.262 8 F2 216.2 12078 0.3060 0 0.3060 0.0014 0 0.0014 1 0 1 0.10789 -0.366 8 F3 67.9 5285 0.1610 0 0.1610 0.0071 0 0.0071 5 0 5 -0.4397 -0.089 6 F4 52.2 3756 0.1672 0.2195 0.3867 0.0113 0.0028 0.0142 8 2 10 0.37829 0.2709 6 Euca1 370.1 15880 0.0620 0.5238 0.5858 0.0028 0.0014 0.0042 2 1 3 0.01579 0.3125 4 Euca2 150.1 8497 0.0465 0.2124 0.2589 0.0057 0.0014 0.0071 4 1 5 -0.316 0.2374 2 Euca3 378.2 12162 0.0770 0.5268 0.6038 0.0127 0.0014 0.0142 9 1 10 -0.0859 -0.025 6 Euca4 372.2 36537 0.0251 0.6683 0.6934 0.0014 0.0014 0.0028 1 1 2 0.30002 -0.079 4
!
! 28 ! ! Chiroptera Neotropical 19(3) Special Volume: 14-30, December 2013
Appendix B – Matrix of geographic distances between fragments. (a) Nearest straight-line distance (m) between the center of two fragments and (b) nearest straight-line distance (m) between fragment edges. (a) F1 F2 F3 F4 Euca1 Euca2 Euca3 Euca4 F1 0 4380 5330 30730 19970 22280 29690 43600 F2 4380 0 2590 2619 15350 17630 25020 39290
F3 5330 2590 0 2580 15150 17670 24750 38300 F4 30730 2619 2580 0 10750 9240 1700 16130 Euca1 19970 15350 15150 10750 0 2900 9830 25530 Euca2 22280 17630 17670 9240 2900 0 7660 24640
Euca3 29690 25020 24750 1700 9830 7660 0 17880 Euca4 43600 39290 38300 16130 25530 24640 17880 0
(b) F1 F2 F3 F4 Euca1 Euca2 Euca3 Euca4 ! F1 0 2400 4230 29310 17700 20610 27190 40070 F2 2400 0 640 2505 14040 16480 22790 35860 F3 4230 640 0 24790 13270 16370 22630 35170 F4 29310 2505 24790 0 8830 7680 0 13820 Euca1 17700 14040 13270 8830 0 840 6660 21700 Euca2 20610 16480 16370 7680 840 0 5370 21950 Euca3 27190 22790 22630 0 6660 5370 0 14630 Euca4 40070 35860 35170 13820 21700 21950 14630 0
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Appendix C – Species by site matrix of bat species abundances in Eucalyptus plantations and Cerrado fragments. See Appendix A for complete species names. A. L. P. C. perspicillata P. lineatus A. lituratus S. lilium P. hastatus A. cinereus D. rotundus S. tildae C. auritus planirostris brasiliensis incarum Euca1 10 0 1 2 0 0 0 1 0 0 0 0 Euca2 7 0 2 0 0 0 0 0 0 0 0 0 Euca3 5 3 0 3 1 3 1 0 0 0 0 0 Euca4 26 1 5 0 4 0 0 0 0 0 0 0 F1 20 12 5 2 1 4 1 0 0 1 0 0 F2 6 14 3 6 1 0 3 1 0 0 1 0 F3 9 9 1 1 0 0 0 1 2 0 0 0 F4 9 0 4 1 7 0 0 0 1 0 0 1
! 30 ! ! Chiroptera Neotropical 19(3) Special Volume: 31-35, December 2013
The false dilemma of natural history vs. modern biology in Neotropical bat research
Marco A. R. Mello !
Departamento de Biologia Geral, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais. Avenida Antônio Carlos, 6.627. 31270-901 Belo Horizonte, MG, Brazil.
E-mail: [email protected].
ARTICLE Abstract. Today’s biology is marked by a conflict of approaches due Manuscript history: to changes in the way scientific knowledge is produced. Bat research Submitted in 28/Nov/2012 is no exception, and colleagues from different schools struggle with Accepted in 26/Jun/2013 each other in conferences and journals because some stand for ‘old- Available on line in 26/Sep2014 fashioned’, organism-oriented research, while others wholeheartedly Editor: Valéria C. Tavares defend ‘modern’, theory-oriented approaches. From some grand masters, especially Elisabeth Kalko and Adriano Peracchi, I learned that this is a false dilemma: we do not need to choose between one view and the other, but rather can combine them. In this article, I make the case for this integration, aiming at a productive agreement in the chiropterological world.
Keywords: bat research, epistemology, knowledge, philosophy, scientific method, scientometrics.
! Introduction At this point, it is important to define some keystone concepts. Although there are several
definitions of natural history, here I will focus on “Experience without theory is blind, but theory the first definition provided by the New Oxford without experience is mere intellectual play” - American Dictionary: “the scientific study of Immanuel Kant. animals or plants, esp. as concerned with observation rather than experiment, and presented It is human nature to live in groups and to say in popular rather than academic form.” The second that other groups are wrong, while your own part of this definition is not entirely correct, as group is absolutely right. The same happens in there are still some scientific journals that publish science, unfortunately, and bat research is no natural history nowadays, and even some journals exception. This kind of group behavior has focused on it, such as the Journal of Natural multiple faces: one is a conflict of approaches. History (http://www.tandfonline.com/loi/tnah20) The ‘modern’ accuse the ‘old-fashioned’ of being and other more regional publications. There are outdated and conservative, while the ‘old- also some top journals, such as The American fashioned’ accuse the ‘modern’ of jumping on Naturalist (http://www.press.uchicago.edu/ every bandwagon and forgetting the true nature of ucp/journals/journal/an.html), which, despite not their scientific discipline (as already commented having natural history as their main focus, still in Mello 2010). We see this conflict in the give space to interesting, well-written, relevant chiropterological community especially in descriptive studies. However, the space devoted to discussions about what approach is best to unveil natural history in biological journals is indeed the mysteries of bats: natural history focused on shrinking, as well as the funding for naturalistic the organism or a modern approach focused on studies, and many naturalists see a crisis and theory and coupled with quantitative analysis. In worry about the future of their field (Greene the present essay I address the following question: 2005). The second definition given by the same do we really need to choose between one and the dictionary states that natural history is “the study other approach? To avoid unnecessary suspense, of the whole natural world, including mineralogy and paleontology.” This was true some centuries here is my answer: no, we do not. Now allow me th to explain my point of view. ago, but especially since the 18 century there has been an increasing specialization of scientific
! 31 ! ! Chiroptera Neotropical 19(3) Special Volume: 31-35, December 2013 disciplines, and natural history is now almost and their habits are seen. However, it would be entirely included within biology, especially impossible to see further, if the giants of bat ecology, zoology, and botany (McIntosh 1986). research did not build a solid basis on which Therefore, in the realm of biological modern bat research started to grow. disciplines, chiropterology is relatively old also in The fact is that it is now very difficult to the Neotropics. Early naturalists such as publish purely descriptive studies, even in venues Humboldt, Natterer, and Ihering were the first to that were traditionally oriented to natural history, investigate the bat fauna of Brazil and other such as Zoologia or Journal of Mammalogy. So, Neotropical countries (Pacheco et al. 2009). The should we just forget about describing the habits way the first generation of native Neotropical bat and diversity of bats in the Neotropics? Is researchers started their studies was strongly organism-oriented research out of fashion? In my influenced by these naturalists and their modus personal opinion, there are two reasons for this operandi. Consequently, in the 20th century, crisis in the publishing of natural history studies in scientific investigations about bats were done in Neotropical countries and also in the world as a depth, thoroughly, without pressure for rapid whole. I will comment on them separately, and production. Nevertheless, this so-called ‘slow will try to show their pros and cons. science’ was very productive, contrary to what is First, there is no denying that theory-oriented now believed. Thanks to these modern naturalists, research is appealing and extremely useful to we got a nice first picture of the impressive advancing the scientific knowledge. Furthermore, Neotropical bat fauna and its habits (e.g., Handley quantitative approaches help us elaborate and test 1967; Málaga 1954; Peracchi 1968). These much more precise and powerful predictions than pioneers paved the way for modern research and purely discursive approaches. Let us use, for produced seminal works, which will never be instance, diffuse coevolution as an example. The entirely outdated. A good example is the first concept of ‘key-and-lock’ coevolution was first identification key for Brazilian bats (Vizotto and advanced by Ehrlich (1964). Later, Janzen (1980) Taddei 1973); despite comprising only one half of adapted it to multispecies systems, coining the the bat fauna currently known for the country term diffuse coevolution. Janzen’s paper was (178, Nogueira et al. 2014), this key contains sharp and brilliant, but the concept of diffuse precise illustrations and a large bulk of coevolution was formulated without rigor, only in knowledge, which are still very useful for training a discursive way, so several biologists interpreted new bat scientists. There are many other it wrong and abused the term. Only after people masterpieces, especially monographs, which gave diffuse coevolution mathematical influenced generations of bat biologists (e.g., formulations was it possible to make sense of the Kalko 1998; Taddei 1980). evidence available and precisely identify when a Nevertheless, “nothing is constant but change”, given study system really fitted the concept as beautifully stated by Heraclitus. Since the (Thompson 2005). That is why modern bat 1990s, Neotropical bat researchers started biology, as well as other fields, became so integrating their knowledge of bats with current strongly biased towards general theories, ecological, behavioral, physiological, genetic, and mathematical modeling, and statistics. These evolutionary theories. Contemporary approaches work. Period. chiropterologists aim not only at describing the That is how modern science is done and it is diet of a given bat species, but also at good that the new generations of bat researchers understanding what its feeding preferences tell us have been updating the field. However, we cannot about its ecological role (Nogueira et al. 2005) or perfectly work oriented by general theories and evolutionary relationships (Dumont et al. 2012). help improve them, if we simply lack real-world Therefore, the new generations of bat data. How can we test fancy hypotheses on the biologists have a strong tendency towards theory- mechanisms that generate the astonishing patterns oriented research, in most cases coupled with of Neotropical bat diversity, if our biomes have heavy quantitative analysis. For instance, bat not yet been well sampled (see Bernard et al. inventories that present simple species lists 2011)? How can we precisely unveil the became rarer, giving place to studies on the relationships between the evolution and diet of community structure of bat assemblages (Estrada- phyllostomid bats based only on molecular Villegas et al. 2012). Studies on bat diversity now markers (as in Datzmann et al. 2010), without aim also at revealing some of the mechanisms that considering the functional morphology and generate the patterns observed (Meyer and Kalko physiology of these organisms? In a nutshell, what 2008) and where some relationships came from in use is a sexy, mathematical, highly general theory, evolutionary terms (Rojas et al. 2012). This new if we have no real-world data against which it can take on bat research brought out exciting be contrasted? What is the difference between an discoveries and changed the way some bat groups appealing but ethereal mathematical hypothesis
! 32 ! ! Chiroptera Neotropical 19(3) Special Volume: 31-35, December 2013 and numerology? Theories, postulates, rules, who go to the field and describe bat species, as hypotheses, theses, and real-world evidence feed well as the relationship between bats and other each other in good science. On the one hand, organisms and their environment. If we consider hypotheses must be contrasted with reality, in science a giant cooperative puzzle, it becomes order to prove themselves. On the other hand, self-evident that we need people who collect punctual field data must be bound together by pieces to solve the puzzle (empiricists). But we creative theories otherwise they remain quasi- also need people who look at the puzzle and point anecdotal. to others where those new-found pieces fit Here comes my second argument on the (theoreticians). reasons for the natural history publishing crisis in Therefore, I advocate that we, Neotropical bat Brazil and other Neotropical countries. One reason researchers, should foment not only studies that why purely descriptive natural history is now out are well connected to current general theories and of fashion is that the scientific literature is studies with strong quantitative approaches, but crowded and the flow of information is too strong also good, well-designed, descriptive natural for anyone to keep the pace. If one has to choose history studies, including those that are not based between reading one paper and the other, one on quantitative analysis. We still need to gather probably makes the decision based on the general much more baseline knowledge of bats in the relevance of the study. If you try to submit your Neotropics. Of course, we should not be paralyzed naturalistic manuscript to a top journal, and its by these impressive gaps, and can also carry out title goes something like “Bats of the X Reserve, innovative, theory-oriented research. The point is: state of Y, country Z: biology and ecology”, in the it would be suicidal to put all coins on a single first place nobody will have a precise clue about number in the scientific roulette. We do much the content of your article, which enormously better by hedging our bets between naturalistic reduces the chance of its advancing in the peer and modern bat research, and by carrying out review streamline. Second, if the abstract does not hypothesis-driven research, no matter if oriented help understand the context and relevance of your by the biology of a single organism or by theories study, most probably only people interested in bats that aim at explaining life on Earth. I am not that occur in the same region or people who study saying that natural history is a synonym for the fauna of the ‘X Reserve’ would like to read organism biology, but rather that it frequently your paper. In order to understand this, put aims at explaining phenomena related to a single yourself in the reader’s place: would you like to taxon and not phenomena that are observed in read a paper on the bat fauna of a district located several taxa. Elisabeth Kalko was an awesome on a very distant country, if its findings are not example of this scientific bet hedging. Her work placed in a broad, interesting scientific context? In combined highly interesting naturalistic order to draw the attention of a broader audience, descriptions with theory-oriented research and you need to clearly say which piece of a large really fancy experimental approaches in the field scientific puzzle your study helps to fit. Most and the lab (take a look at the website of her contemporary naturalistic studies fail to do that, former research group and see the variety of and so they are losing space in top journals that approaches: http://www.uni-ulm.de/nawi/bio3/ want to be read and cited by as much people as kalko/ research/ publications.html). Think possible. about echolocation, her favorite topic: in one Anyway, who said that natural history cannot paper she and her colleagues and students were be theory-oriented too? Who said that natural able to reveal to us the details of the sonar of a bat history focused on a particular organism in its species (Schnitzler et al. 1987), while in another environment (as defined by Greene 2005) cannot paper they unveiled experimentally how another draw the attention of people interested in other bat species identifies its targets, using state-of-the- organisms? Good natural history, even some art gadgets and models (Page et al. 2012). centuries ago, was also driven by nice theories that Still using the example of Elisabeth Kalko’s vary in scope. Think about Darwin’s work, for career, one may ask: what makes naturalistic instance. Or Wallace’s and Couvier’s. The studies, such as those mentioned above, stand out difference is that in some cases naturalists were and be published in top-ranked journals, while interested in theories designed for particular most other naturalistic studies fail even to get into organisms. In other cases, these theories proved to mid-ranked journals? The answer was already be more general than previously thought. To be a given some paragraphs ago, when I compared naturalist does not mean going blindly to the field science to a cooperative puzzle. Elisabeth Kalko’s and collecting bats like one collects stamps. studies were always very well-written and clearly Naturalists, especially the good ones, do also go to placed in a broad scientific context. She knew how the field with a searchlight (read more about this to inform the reader about the piece that was being nice allegory in Popper 2000). We need people fitted and to which puzzle did it belong. Therefore,
! 33 ! ! Chiroptera Neotropical 19(3) Special Volume: 31-35, December 2013 her studies were read not only by bat biologists, the Royal Society B: Biological Sciences but also by ecologists, taxonomists, and 279(1734): 1797-1805. conservationists all around the world. Elisabeth Ehrlich P. 1964. Butterflies and plants: a study in Kalko was also very good at investigating bats at coevolution Evolution 18(4): 586-608. different levels of organization, from the Estrada-Villegas S.; McGill B.J. and Kalko E.K.V. individual to the community (see, for instance, 2012. Determinants of species evenness in a Kalko 1998). This kind of natural history, which is neotropical bat ensemble. Oikos: no-no. not afraid of moving freely between scales and aims at explaining hierarchical phenomena, is Greene H.W. 2005. Organisms in nature as a highly attractive to several kinds of scientists and central focus for biology. Trends in Ecology & may draw attention even outside of biology. In her Evolution 20(1): 23-27. last years, Elisabeth Kalko was even collaborating Handley C.O. 1967. Bats of the canopy of an with engineers to build ‘robot bats’ for the study Amazonian Forest. Atlas do Simpósio sobre a of echolocation (see the website of Project Biota Amazônica 5: 211-215. ChiroPing: http://www.chiroping.org). Janzen D.H. 1980. When is it coevolution? My final message to the young Neotropical bat Evolution 34(3): 611-612. researcher: do not fight over non-questions. We Kalko E. 1998. Organization and diversity of can use our energy and time in much more tropical bat communities through space and productive ways, if we take advantage of the time. Zoology: Analysis of Complex Systems diversity of approaches that can be used in 101: 281-297. science. Bat research needs modern naturalists who get their feet wet and their hands bitten by Málaga A. 1954. El vampiro portador de la rabia. Bol Of Sanit Panam 37: 53-65. angry ‘Carollias’ in the field, theoretical biologists who do fieldwork in Excel and are able to McIntosh R.P. 1986. Background of ecology: integrate bat science with current general theories, concept and theory. Cambridge University and empiricists who think creatively and test Press, Cambridge. predictions of current theories against field reality. Mello M.A.R. 2010. On the shoulder of giants: how to go further in the study of bat-plant Acknowledgments interactions. Chiroptera Neotropical 16(1): 497- Above all, I thank Elisabeth Kalko, my dear 500. mentor and friend, to whom this special issue of Meyer C.F.J. and Kalko E.K.V. 2008. Bat Chiroptera Neotropical is dedicated. She taught assemblages on Neotropical land-bridge islands: me not only how to be a scientist, but also how to nested subsets and null model analyses of take calculated risks in my career and find my own species co-occurrence patterns. Diversity and way in Academia. Above all, she taught me that theory and fieldwork are not mutually exclusive. Distributions 14(4): 644-654. This work was funded by the Alexander von Nogueira M.R.; Monteiro L.R.; Peracchi A.L. and Humboldt Foundation (AvH, 1134644), Federal Araújo A.F.B. 2005. Ecomorphological analysis University of Minas Gerais (UFMG, of the masticatory apparatus in the seed-eating Edital 2013/1), Minas Gerais Research Foundation bats, genus Chiroderma (Chiroptera: (FAPEMIG, APQ – 01043 - 13), Brazilian Phyllostomidae). Journal of Zoology 266(4): Research Council (CNPq, 472372 /2013-0), 355-364. Research Program on Atlantic Forest Biodiversity Nogueira, M.R., I.P. de Lima, R. Moratelli, V. da (PPBio-MA/CNPq), and Ecotone Inc. (“Do C. Tavares, R. Gregorin, and A.L. Peracchi, Science and Get Support Program”) 2014. Checklist of Brazilian bats, with comments on original records. Check List 10: References p.808–821. Available at: http://biotaxa.org/cl/ Bernard E.; Aguiar L.M.S. and Machado R.B. article/view/10.4.808 [Accessed September 3, 2011. Discovering the Brazilian bat fauna: a 2014]. task for two centuries? Mammal Review 41(1): Pacheco S.M.; Sodré M.; Mello M.A.R.; Marques 23-39. R.V.; Uieda W.; Aguiar L.M.S.; Passos F.C.; Datzmann T.; von Helversen O. and Mayer F. Trajano E. and Bredt A. 2009. Chiroptera. in 2010. Evolution of nectarivory in phyllostomid Estado da arte e perspectivas para a Zoologia no bats (Phyllostomidae Gray, 1825, Chiroptera: Brasil (edited by Rocha R.M. and Boeger W.), Mammalia). BMC Evolutionary Biology 10(1): pp. 231-248. Editora da UFPR, Curitiba. 165. Page R.A.; Schnelle T.; Kalko E.K.V.; Bunge T. Dumont E.R.; Dávalos L.M.; Goldberg A.; and Bernal X.E. 2012. Sequential assessment of Santana S.E.; Rex K. and Voigt C.C. 2012. prey through the use of multiple sensory cues by Morphological innovation, diversification and invasion of a new adaptive zone. Proceedings of ! 34 ! ! Chiroptera Neotropical 19(3) Special Volume: 31-35, December 2013
an eavesdropping bat. Naturwissenschaften 99(6): 505-509. Peracchi A.L. 1968. Sobre os hábitos de Histiotus velatus (Geoffroy, 1824) (Mammalia, Chiroptera, Vespertiliionidae). Revista Brasileira de Biologia 28(4): 469-473. Popper K. 2000. The bucket and the searchlight: two theories of knowledge. in The philosophy of ecology: from science to synthesis (edited by Keller D.R. and Golley F.B.), pp. 141-146. The University of Georgia Press, London. Rojas D.; Vale n.; Ferrero V. and Navarro L. 2012. The role of frugivory in the diversification of bats in the Neotropics. Journal of Biogeography 39(11): 1948-1960. Schnitzler H.U.; Kalko E.K.V.; Miller L.A. and Surlykke A. 1987. The echolocation and hunting behavior of the bat, Pipistrellus kuhli. Journal of Comparative Physiology 161: 267-274. Taddei V. 1980. Biologia reprodutiva de Chiroptera: perspectivas e problemas. Inter- Facies 6: 1-19. Thompson J.N. 2005. The geographic mosaic of coevolution. The University of Chicago Press, London. Vizotto L.D. and Taddei V.A. 1973. Chave para determinação de quirópteros brasileiros. Editora da Universidade Estadual de São Paulo, São José do Rio Preto.
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Maximum weight capacity of leaves used by tent-roosting bats: implications for social structure
“... whish you were here (Pink Floyd)” Bernal.
Phoebe Parker-Shames1, 2 and Bernal Rodríguez-Herrera3,*
1Colorado College Biology Department, 14 East Cache La Poudre St. Colorado Springs, Colorado, USA 80903. 2Present address 344 Bridge St. Ashland, Oregon, USA 97520. 3Escuela de Biología, Universidad de Costa Rica, San José, Costa Rica.
* Corresponding author: [email protected]
ARTICLE Abstract. Fewer than 2% of the extant bat species can modify their Manuscript history: environment to build roosts. Tent-roosting bats cut and fold leaves to Submitted in 18/Jun/2013 form roosts known as tents. Unlike the caves or hollow trees used by Accepted in 8/Abr/2014 some bats, leaves possess an upper limit on their capacity to support Available on line in 26/Sep/2014 weight. We tested the hypothesis that the maximum weight capacity Editors: Marco A.R. Mello and Valéria C. Tavares that leaves can support limits the maximum social group size of bats that roost in them. We carried out fieldwork in the Tirimbina Biological Reserve (TBR), Sarapiquí, Costa Rica, between February and March 2012. We added weight incrementally to new leaves of three plant species until the angle of the leaves fell below that which bats naturally use. Philodendron fragrantissimum and Heliconia imbricata support one-third more weight than Asterogyne martiana. The present study demonstrates that the maximum weight that the leaves can support is similar to the mean social group weight of Dermanura watsoni and Ectophylla alba reported in the literature for these plant species and lower than the maximum reported social group weights. Therefore, it is possible that the maximum weight capacity of the leaves used to build roosts limits the maximum social group size.
Keywords: Asterogyne martiana, Dermanura watsoni, Ectophylla alba, Heliconia imbricata, Philodendron fragrantissimum, roost, tents, Tirimbina.
! very little research has focused on the interaction Introduction between costs and benefits of tent construction Roosts are critical for bat survival. Bats rely on (Chaverri & Kunz 2010; Rodríguez-Herrera et al. them to protect themselves against predators and 2007). weather, facilitate social interactions such as Many species of bats use caves, hollow trees, mating and rearing young, and promote energy or buildings as roosts, but approximately 50% of conservation and foraging (Chaverri & Kunz the species use foliage (Kunz & Lumsden 2003). 2010; Kunz 1982; Kunz & Lumsden 2003; Just twenty-two species (2%) of all bats have the McCracken et al. 2006). Roosts influence bat ability to modify plants to build structures called social interactions and ecology because the tents (Rodríguez-Herrera et al. 2007). These bats success of roost selection affects social group size bite leaves to create cuts along the midrib and and survival (Kunz 1982; Kunz & Lumsden 2003; veins so that part of the leaf folds down to create a McCracken et al. 2006). There is also an energy tent. They do this without cutting off water supply cost involved in tent location and construction that to the leaves (Cholewa et al. 2001). All tent- controls the balance of benefits received from roosting bats are confined to warmer climates roosts (Chaverri & Kunz 2010; Rodríguez-Herrera where leaf sizes are larger, and in the Neotropics et al. 2007; Rodríguez-Herrera et al. 2011). there are seventeen primarily frugivorous species However, despite the presumed impact of roost that build tents (Rodríguez-Herrera et al. 2007). limitations on bat social structure and ecology, These bats, members of the family
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Phyllostomidae, are important to tropical limit social group size: roost abundance, roost ecosystems as seed dispersers (LaVal & size, and roost weight support. Rodríguez-H 2002; Medellín & Gaona 1999). The first hypothesis states that large spaces Another characteristic of tent-roosting bats is such as caves support large social groups because that they all roost in groups (Rodríguez-Herrera et there are fewer of them. In this theory, abundance al. 2007; Chaverri & Kunz 2010). Additionally, of these large spaces limits social group size most Neotropical tent-roosting bats are small- (McCracken et al. 2006; Kerth 2008). Chaverri & bodied. For example, Ectophylla alba Allen, 1892 Kunz (2010) reviewed this theory with tent- and Vampyressa thyone Thomas, 1909 weigh from roosting bats and concluded that bats form large 5 to 8 g, and Dermanura watsoni Thomas, 1901 social groups when leaves are more abundant. (previously known as Artibeus watsoni) weighs However, bat researchers do not universally accept around 11 g. A few species are medium-sized, this hypothesis (Rodríguez-Herrera et al. 2007; such as Artibeus jamaicensis Leach, 1821, which Chaverri & Kunz 2010), and it does not explain weighs over 60 g. However, most species are what governs the social group dynamics of tent- small (Rodríguez-Herrera et al. 2007; Chaverri & roosting bats when leaves are abundant, as they Kunz 2010). usually are (Chaverri & Kunz 2010). Tent- It has been thought that bats build tents for a roosting bats can often use a range of plant variety of reasons: to protect themselves against species, which also increases roost availability. predators, to conserve heat, and to bring social They are known to use more than 77 different groups together, in order to facilitate foraging, species of plants, with D. watsoni using the largest mating, and nursing (Rodríguez-Herrera et al. number of species: 41 (Rodríguez-Herrera et al. 2007). There are also social and mechanical costs 2007; Chaverri & Kunz 2010). Many plant species to tent building. Social costs include increased used by bats have yet to be formally recorded competition, aggression, and facilitated (Bernal Rodríguez-Herrera, personal observation). transmission of parasites (Chaverri & Kunz 2010). The second hypothesis states that roost size is Bats incur mechanical costs when cutting leaves to what controls social group size. According to this create roosts, and these costs vary with the hypothesis, large spaces habor more bats because hardness and size of leaves (Rodríguez-Herrera et of their size. However, in some situations, a space al. 2007). To offset these costs, bats may try to may be large enough to hold more bats but maximize tent benefits by increasing social group incapable of supporting them. This has led size, but the costs also limit their ability to do so researchers to the third, most probable hypothesis (Chaverri & Kunz 2010; Rodríguez-Herrera et al. that the weight that a roost can support limits the 2011). Because mechanical costs vary depending social group size. In this hypothesis, large spaces on the leaf, the cost-benefit balance between social such as caves support large social groups not group size and the limits of the leaf itself will be because they are a finite resource or provide more different for each species of bat with each species space, but because they are unlikely to collapse of leaf. under the weight of large bat colonies (Chaverri & Bats must select appropriate leaves because an Kunz 2010). This hypothesis relates perhaps most old, weak, or otherwise unsuitable leaves do not relevantly to foliage-roosting bats. Because tent- provide benefits that outweigh the costs of roosting bats are relatively small compared to building a tent (Cholewa et al. 2001; Rodríguez- other bat species, many researchers have Herrera et al. 2007). However, there are also speculated that the size of either the bat or the leaf several factors that influence a bat’s ability to use might limit tent building or influence bat social different kinds of leaves: (1) some bats may not structure (Rodríguez-Herrera et al. 2007; Kerth recognize certain species of plants as roost sites 2008; Chaverri & Kunz 2010). However, due to phylogenetic constraints, (2) bats may researchers have not studied this concept and are select specific plants and habitats because of their unclear about in what situations weight might ecological requirements, and (3) the structure of limit social group size. This is the first study to the leaves may mechanically limit the construction examine maximum weight capacities of tent of tents and the amount of weight they can support leaves and their potential influences on bat social (Rodríguez-Herrera et al. 2007). group size. Mechanical limitations may impact bat social Our objectives were: (1) to estimate the weight structure. Chaverri & Kunz (2010) noted that bat that leaves of Asterogyne martiana Wendland, weight and social group size often correlate with 1857, Heliconia imbricata Baker, 1893, and roost size. For example, bats that roost in large Philodendron fragrantissimum Hook, 1834 can spaces like caves or tree trunks tend to form larger support, and (2) to examine whether and to what social groups than those that roost in small rock extent the maximum weight capacity (hereafter crevices or bamboo. This review included three MWC) of these three plant species limits the popular hypotheses on roost factors that might social group size of the bats.
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Methods what the bats have available to them as well. In this study area, there is little seasonal variation of Study Area leaf production (Reich 1995). We carried out fieldwork at Tirimbina For each leaf, we recorded length (from base Biological Reserve (TBR; 10°26’N, 83°59’W) in of petiole to the end of the furthest tip), leaf width central Heredia Province, Costa Rica. TBR covers at the widest point, its undisturbed height above an area of 345 ha of rainforest (85% primary). the ground at the leaf base and at the leaf tip (for Mean annual rainfall is 3,777 mm and mean P. fragrantissimum, this was measured from the annual temperature is 25.3 °C, ranging between point at which the stem attaches to the vine instead 20.2 °C and 30.0 °C (Tirimbina Biological of from the ground), and width of the stem at the Reserve 2010). The reserve has two Holdridge petiole. We used a paperclip and string to hang Life Zones (Holdridge 1969): very humid Pre- 10g bags of sand across the midrib of the leaf at Montane Forest with transition to Basal (bmh-P) the position at which the bats would hang. and very humid Tropical Forest (bmh-T). The Ectophylla alba and D. watsoni on average weigh largest numbers of plants in the reserve belong to 5-6 g and 11 g respectively, so 10 g reasonably the families Rubiaceae and Arecaceae (Delgado et approximates the weight of one or two bats al. 1997). Palms (Euterpe, Prestoea, Geonoma) (Chaverri & Kunz 2010). At each interval, we and small trees of the family Rubiaceae and added additional bags one at a time by tying them Melastomataceae characterize the understory in to the string. For A. martiana, we hung the weight areas of primary forest, while Heliconia 5 cm from the point at which the leaf splits, for H. pogonantha and pioneers of the families imbricata, we hung the weight 5 cm closer to the Melastomataceae, Piperaceae and Rubiaceae leaf base from the midpoint of the leaf length, and dominate more disturbed areas (Rincón et al. for P. fragrantissimum, we hung the weight 3 cm 1997). The reserve supports mammals from the base of the leaf. characteristic of the Caribbean Lowlands, including more than 60 species of bats (Tirimbina Before and immediately after adding each bag, Biological Reserve 2010). we recorded the height of the leaf at the base and tip, until the leaf reached MWC and was no longer usable by tent-roosting bats. We defined MWC as Maximum Weight Capacity when the two heights were equal or the tip was lower than the base (see Figure 1). For P. We studied the plant species Asterogyne fragrantissimum, we used the point of bag martiana (Fam. Arecaceae), Heliconia imbricata attachment instead of the leaf tip. We repeated this (Fam. Heliconiaceae), and Philodendron for each leaf of each species that was used. fragrantissimum (Fam. Araceae). They have different tent architectures: A. martiana tents are To compare the effects of time on sagging of bifid, P. fragrantissimum tents are apical, and H. leaves, we used two experimental groups for each imbricata tents are invert-boat. The present study leaf species: one in which we added bags one at a focused on two common tent-roosting bats in time each hour, and one in which we added bags TBR. The generalist D. watsoni uses all three one each day. We used between 30 and 36 leaves selected plant species while the specialist E. alba of each species for the hourly trials and between 9 uses only H. imbricata (Rodríguez-Herrera et al. and 10 leaves of each species for the daily trials 2007). Dermanura watsoni commonly uses P. (see Figure 3). We conducted trials between fragrantissimum in TBR, although this is the first February and March 2012. study to formally record it as a species used by tent-roosting bats. Social Group Size and To determine tent leaf MWC, we identified accessible leaves of each plant species that were Maximum Weight Capacity new and in good condition, since the newness of If the plant’s MWC limits bat social group the leaves is the most important factor for leaf use size, then the maximum social group size will be (Rodríguez-Herrera et al. 2008; Rodríguez-Herrera limited to the mean social group size in these et al. 2011). We measured all leaves available in plants, which will be correlated with MWC. To each given area where we encountered plants of test this hypothesis, we compared the data on the desired species along the main trail system of 2 MWC to maximum and mean social group TBR (usually an area of approximately 300m but weights of E. alba and D. watsoni in each plant the size depended on the individual group of species. To calculate maximum and mean social leaves). We assumed that if we used every new group weight, we used the following formula for leaf as it became available, it would be a each bat in each plant species: reasonably random and representative sample of
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Figure 1. Asterogyne martiana leaves at different stages of weight addition. Blue lines are the height at leaf tip (in this case, the end of the midrib), yellow lines are the height at leaf base, and red lines are the horizontal height at leaf base for comparison with height at leaf tip. A is a leaf without weight. B is a weighted leaf before it reaches MWC. C is a weighted leaf at MWC. Rohlf 1995) in Minitab 16 because data were not normally distributed. We used α significance of Social Group Weight = S x W p b 0.05 in all tests. Where S is maximum or mean bat social p We compared bat maximum social group group size specific for each plant species and W b weight to MWC and estimated their differences is the mean bat weight. We used maximum and with a Wilcoxon signed rank test using Minitab mean social group size and bat weights presented 16. We estimated the strength of the relationship in Chaverri & Kunz (2010). Because there are no between mean MWC (independent variable) of data for D. watsoni utilizing P. fragrantissimum, plant species to mean bat social group weight we used a similar species, Philodendron pterotum, (dependent variable) with a simple linear Koch & Augustin 1854. regression with Statgraphics Online. We used D. Data Analysis watsoni for all three species and E. alba with H. We used three different statistical packages for imbricata only, based on plant use we observed in our analyses: Minitab 16 (Minitab 16 Statistical our study site. Software 2010), Statgraphics Online (statgraphicsonline.com), and BrightStat Online (Stricker 2008). We tested for differences in Results median maximum weight capacities among plant Maximum Weight Capacity species and then between hourly and daily Philodendron fragrantissimum had the largest treatments with Kruskal-Wallis tests (Sokal & MWC (n = 30, x = 44.0 ± 2.52 SE g, median = 40 g), followed closely by H. imbricata (n = 36, x = 42.2 ± 2.73 SE g, median=40 g), and A. martiana had a significantly lower MWC compared€ to the other two species (n = 33, x = 33.3 ± 1.83 SE g, median = 30g; H = 9.57, df = 2, € 96, P = 0.0083) (Figure 2). There was no statistical difference between adding weight hourly or daily for €any of the three species (A. martiana: H = 1.36, df = 1, 40, P = 0.21, H. imbricata: H = 0.10, df = 1, 44, P = 0.68, P. fragrantissimum: H = 3.02, df = 1, 37, P = 0.09) (Figure 3). Figure 2. Box and whisker plot of A. martiana, H. imbricata, and P. fragrantissimum MWC. Red pluses Social Group Size and Maximum Weight Capacity represent means and values are divided into quartiles. Mean social group weight follows the same Notches in box represent 95% confidence intervals for pattern as MWC, while MWC limits the maximum medians (horizontal lines closest to red pluses). Points social group weight to the mean (Figure 4). Mean beyond external quartile maximums are outliers. Letters social group weights of D. watsoni and E. alba indicate significant differences. ! 39 ! ! Chiroptera Neotropical 19(3) Special Volume: 36-43, December 2013
!
! Figure 3. Box and whisker plot of A. martiana, H. imbricata, and P. fragrantissimum MWC for hourly versus daily weight addition. Red pluses represent means and values are divided into quartiles. Notches in box represent 95% confidence intervals for medians (horizontal lines closest to red pluses). Points beyond external quartile maximums are outliers. All hourly and daily comparisons were not significantly different.
!
Figure 4. Mean tent leaf MWC compared to mean and maximum social group weights for D. watsoni and E. alba from Chaverri & Kunz (2010). Social group sizes for P. fragrantissimum approximated using P. pterotum, a similar species. display a positive relation to the corresponding Statistic = 10.0, df = 3, P = 0.05, Estimated plant species MWC (F = 12.2, df = 1, 2, P = 0.073 Median Difference = 12.30) (Figure 7). 2 R = 85.9) (Figure 5). All maximum social group Discussion and Conclusions weights were greater than maximum weight capacity (Wilcoxon Statistic = 10.0, df = 3, P = Maximum Weight Capacity 0.05, Estimated Median Difference = 29.68) We found that P. fragrantissimum and H. (Figure 6) and mean social group weights were all imbricata leaves supported more weight than A. smaller than maximum weight capacity (Wilcoxon martiana. Philodendron fragrantissimum and H.
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Figure 5. Regression of mean social group weight of D. watsoni and E. alba with the corresponding plant MWC. The blue line is the regression line and the green lines are 95% confidence intervals of slope. MWC = 2.66 + 1.35 ^ Bat (F = 12.2, df = 1,2, P = 0.073, R2 = 85.9).
100
90
80 )
g 70 (
t h g i
e 60 W
50
40
30 Maximum weight capacity Maximum social group weights
Figure 6. Box plot of bat maximum social group weight and plant MWC. Wilcoxon statistic = 10.0, df = 3, P = 0.05, estimated median = 29.68 (one-tailed Wilcoxon Rank Test of differences). The shaded boxes represent the interquartile range, the line inside the box is the median, and the circle is the mean. Points beyond external quartile maximums are outliers. imbricata both have thicker stem widths, which Social Group Size and Maximum Weight Capacity could provide more support for the leaves This study supports the hypothesis that the compared to A. martiana. While no other studies MWC of plant species limits the number of bats have measured MWC of leaves, some authors roosting together. Social and physical benefits have hypothesized that roost size limits social increase with group size; however, the group size (Chaverri & Kunz 2010). Since P. construction of tents is energetically costly for the fragrantissimum leaves tend to be much smaller bats, and this study shows that leaves can support than the other two, these results do not support a limited number of bats (Rodríguez-Herrera et al. that theory. 2007; Chaverri & Kunz 2010; Rodríguez-Herrera et al. 2011; Sagot & Stevens 2012).
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45
40
) 35 g (
t h g i e
W 30
25
20 Maximum weight capacity Mean social group weights
Figure 7. Box plot of bat mean social group weight and plant MWC. Wilcoxon statistic = 10.0, df = 3, P = 0.05, estimated median = 12.30 (one-tailed Wilcoxon Rank Test of differences). The shaded boxes represent the interquartile range, the line inside the box is the median, and the circle is the mean. Points beyond external quartile maximums are outliers. Largest know group size occurs only rarely in on bat social groups, with ramifications for an exceptionally strong leaf, but most leaves reproduction, foraging, and cooperative behaviors cannot support that number of bats. This implies (Sagot & Stevens 2012). that were there no weight limit of leaves, bats Conclusions would create larger social groups. Because leaves Many authors have theorized that MWC of present this weight limit that other kinds of roosts plant species used for tents limits bat social group (such as caves or tree cavities) likely do not, the size (Timm 1987; Stoner 2000; Rodríguez-Herrera specific benefits conferred by roosting in leaves, et al. 2007), yet until now, this idea had not been such as parasite control, predator avoidance, or use tested. This study supports the MWC theory and as a mode of sexual selection, may outweigh the demonstrates the potential for a large limiting costs of MWC (Rodríguez-Herrera et al. 2007). effect in some cases. However, MWC varies The weight limitation of leaves also explains greatly on an individual basis for all plant species. why mean social group weight correlates with Because this study showed a strong correlation plant species’ MWC. The mean social group between mean social group weight and maximum weight was slightly lower than the actual MWC, weight capacity, it suggests that this trend may presumably so that the bat group does not risk hold true for other species of tent-roosting bats collapsing the tent leaf. All three plants showed a and the plants they utilize. This study has laid out limiting effect, but it was especially large for H. a procedure that can be repeated with other species imbricata leaves. This species supported of plants used by tent-roosting bats in future maximum social group sizes of 8 D. watsoni bats studies to help explain the social behavior of a and 17 E. alba bats and mean social group sizes of wider range of species. Additionally, it would be 2.75 bats and 5.42 bats respectively (Chaverri & useful to expand this study to a wider geographic Kunz 2010). The standard deviation for H. area to see if these trends hold true in a greater imbricata MWC was also the largest of the three variety of habitats and levels of anthropogenic species, which could account for the wider disturbance. One of the major limiting factors of differences between the maximum and observed this study is that it relied on pre-existing data on mean. The difference in MWC between different social group sizes of bats in specific plant species, species of plants as well as between individual which is not well known. An important next step, leaves of the same species presents differential in addition to collecting MWC for more species of weight bearing capacities that could be a factor plants and examining the role of MWC in roost involved in bats’ preference and selection of roost site selection and social behavior, is to expand sites. This uncertainty of the MWC of all three knowledge on the social dynamics of tent-roosting species would therefore have a strong impact on bats in general. the cost-benefit balance of tent construction and
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Reich P.B. 1995. Phenology of tropical forests: Acknowledgements patterns, causes, and consequences. Canadian We would like to thank Tirimbina Biological Journal of Botany 73: 164-174. Reserve and its staff for allowing us to conduct Rincón M.; Roubik D.W.; Finegan B.; Delgado D. our research there and supporting our efforts. We & Zamora N. 1999. Understory bees and floral would also like to thank Manuel (Emmanuel) and resources in logged and silviculturally treated Cristian (Gato) for their assistance in data Costa Rican rainforest plots. Journal of the collection. Thanks also to the Associated Colleges Kansas Entomological Society 72: 379-393. of the Midwest Costa Rica program through which we collected data, specifically Dr. Michael McCoy Rodríguez-Herrera B.; Medellín R. & Gamba-Rios and Dr. Christopher Vaughan for their edits and M. 2008. Roosting requirements of white tent- comments. Finally, thanks to Colorado College making bat Ectophylla alba (Chiroptera: professors Dr. Marc Snyder and Dr. Jim Ebersole Phyllostomidae). Acta Chiropterologica 10: 89- for their edits. 95. Rodríguez-Herrera B.; Medellín R. & Timm R. References 2007. Murciélagos neotropicales que acampan Chaverri G. & Kunz T. 2010. Ecological en hojas: neotropical tent-roosting bats. InBio, determinants of social systems: perspectives on Santo-Domingo de Heredia. the functional role of roosting ecology in the Rodríguez-Herrera B.; Ceballos G. and Medellín social behavior of tent-roosting bats. Advances R. 2011. Ecological aspects of the tent building in the Study of Behavior 42: 275-318. process by Ectophylla alba (Chiroptera: Cholewa E.; Vonhof M.; Bouchard S.; Peterson C. Phyllostomidae). Acta Chiropterologica 13: & Fenton B. 2001. The pathways of water 365-372. movement in leaves modified into tents by bats. Sagot M. & Stevens R. 2012. The evolution of Biological Journal of the Linnean Society 72: group stability and roost lifespan: perspectives 179-191. from tent-roosting bats. Biotropica 44: 90-97. Delgado D.; Finegan B.; Zamora N. & Meir P. Sokal R.R. & Rohlf F.J. 1981. Biometry. W.H. 1997. Efectos del aprovechamiento forestal y el Freeman and Company, Salt Lake City. tratamiento silvicultural en un bosque húmedo del noroeste de Costa Rica: cambios en la Stoner K. 2000. Leaf selection by the tent-making riqueza y composición de la vegetación. CATIE, bat Artibeus watsoni in Asterogyne martiana Turrialba. palms in southwestern Costa Rica. Journal of Tropical Ecology 16: 151-157. Holdridge L.R. 1967. Life zone ecology. Stricker D. 2008. BrightStat.com: free statistics Tropical Science Center, San José. online. Computer Methods and Programs in Kerth G. 2008. Causes and consequences of Biomedicine 92: 135-143. sociality in bats. BioScience. 58: 737-746. Timm R. 1987. Tent construction by bats of the Kunz T. 1982. Roosting ecology of bats. In: genera Artibes and Uroderma. Fieldiana Ecology of bats (edited by Kunz T.), pp. 1-55. Zoology 39: 187-212. Plenum Press, New York. Tirimbina Biological Reserve. 2010. Tirimbina Kunz T. & Lumsden L. 2003. Ecology of cavity website: Physical description. Accessed on and foliage roosting bats. In: Bat Ecology 13/2/2012.
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Habitat use by aerial insectivorous bat in shoreline areas of Barro Colorado Nature Monument, Panama
Kathrin Barboza-Marquez1,2,*, Luis F. Aguirre1,3, José C. Pérez-Zubieta1, Elisabeth K.V. Kalko4,†
1 Fundación Programa para la Conservación de los Murciélagos y la Biodiversidad. P.O.Box 994. La Paz, Bolivia. 2 Asociación Bolivia para la Investigación y Conservación de Ecosistemas Andino Amazónicos. La Paz, Bolivia. 3 Centro de Biodiversidad y Genética, Universidad Mayor de San Simón. P.O.Box 538. Cochabamba, Bolivia. 4 Institute of Experimental Ecology, University of Ulm, Albert-Einstein-Allee 11, 89069 Ulm, Germany. Title (in memoriam)
* Corresponding author: [email protected] † Deceased in 26 September 2011
ARTICLE Abstract. Aerial insectivorous bats represent almost half of the bat Manuscript history: diversity in the Neotropics. They use mainly echolocation (active or Submtited in 18/Jun/2013 passive) to find their prey and contribute to pest control and Accepted in 20/Aug/2014 herbivory reduction. We assessed the structure of the community of Available on line in 25/Sep/2014 aerial insectivorous bats in four microhabitats (upper and lower Editors: Marco A.R. Mello and Valéria C. Tavares forest edge, and upper and lower open space) through acoustic sampling in shoreline areas of Barro Colorado Nature Monument, Panama. Seven sites were chosen for sampling, each was visited four times, and bat recordings were taken during four consecutive hours per site each time. We found differences among species in foraging microhabitat, and a tendency of some species to be associated with particular microhabitats. During search calls, species that preferred forest edges (e.g., Saccopteryx bilineata) produced high frequency echolocation calls of short duration, short pulse intervals, and a combination of components of frequency modulation (FM) and quasi-constant frequency (QCF). On the other hand, species that preferred open spaces (e.g., Diclidurus albus) produced echolocation calls with low frequency, long duration, long pulse intervals, and QCF combined with FM components. Differences between guilds are explained by foraging strategy, and some bats prefer the upper stratum while others the lower stratum. This result provides important information on resource partitioning in aerial insectivorous bat communities, as well as on the importance of having a standard protocol to improve the use of acoustic monitoring.
Keywords: aerial insectivorous bats, habitat use, acoustic monitoring.
! 1979; Kalko et al. 2008). This resource Introduction distribution has resulted in an astonishing variety Neotropical bat communities are composed of of feeding guilds, including frugivorous, a wide variety of species that can only coexist by nectarivorous, insectivorous, carnivorous, and partitioning the resources (Aguirre et al. 2003). hematophagous bats (Kalko 1997; Kalko et al. The flight and echolocation capacity of bats give 1996; Findley 1993). them access to a wide range of habitats and foods. Aerial insectivorous bats are characterized by Those abilities also allow navigating through having echolocation as a primary tool for cluttered environments and a higher precision in capturing their prey on flight. They represent the detection, classification, and location of food between 30-50% of the species in Neotropical bat in both enclosed and open spaces (Simmons et al. communities (Kalko 2008). Due to those
! 44 ! ! Chiroptera Neotropical 19(3) Special Volume: 44-56, December 2013 characteristics, Schnitzler et al. (2003) and Kalko habitat use and distribution across the landscape & Handley (2001) separate bats into three (Estrada et al. 2010). functional groups according to the use of space: A good example of the high diversity of (1) bats that forage in highly cluttered space and insectivorous bats in the Neotropics is Barro have auditory adaptations (i.e., Doppler Colorado National Monument, in Panamá. compensation) to capture their prey close to or Seventy-four bat species have been recorded there, within the vegetation; (2) bats that forage in out of which 46% are aerial insectivores (Kalko et background cluttered space, and hunt insects on al. 2008). Unfortunately, the use of space and food forest edges or gaps, or trawl them from the water by those bats has not been studied well enough surface; and (3) bats that forage in open spaces, and there is scarce information on insectivorous where they fly fast above the forest canopy. species in tropical lowland forests (Jung et al. The large consumption of insects by bats, 2007) especially phytophagous insects, contributes Using acoustic monitoring, the questions to be greatly to the reduction of herbivory in tropical answered in the present study were: (1) How is forests (Kalka et al. 2008; Kalka & Kalko 2006), the structure of the aerial insectivorous bat and to the reduction of crop pests (Cleveland et al. community in the shoreline areas of forest islands 2006). Despite the importance of insectivorous in Barro Colorado Monument, Panama? And (2) bats and their occupation of several habitat types, how different are species assemblages (species Neotropical species are usually underrepresented composition) in four different microhabitats in the or not even mentioned in species in inventories study area (upper and lower forest edge and upper (Kalko 1998), and the knowledge of their ecology and lower open space)? Considering the highly and natural history is scarce. Moreover, most adapted echolocation of bats that forage in habitats standardized protocols, which rely on mist netting, with different structure, we hypothesized that are not well suited for assessing aerial some species would belong to a specific insectivorous bats, thus thorough assessments of microhabitat due to their foraging mode, and this this group depend on complementary techniques would be reflected in differences in species (Estrada et al. 2010; Kalko et al. 2008). Although composition. intensive sampling in the upper stratum of the forest with mist nets has started to be used lately, Materials and Methods it is recognized that the richness and abundance of Study area and sampling sites aerial insectivorous bats has been underestimated, because they can easily detect and avoid mist nets This study was conducted during the months of March to June 2008 on three islands of Barro (Meyer & Kalko 2008; Bernard 2001; Kalko & Colorado Nature Monument (hereafter BCNM, Handley 2001). To solve this problem, acoustic 9˚09’N, 79˚ 51’W): Barro Colorado Island (BCI), monitoring techniques have been developed in Bohio Island, and Juan Gallegos Island, all located recent years and they have proved to be an in Gatun Lake, in the center of Panama Canal important tool to record aerial insectivorous bats (Fig. 1). Holdridge (1967) classified the vegetation through their echolocation calls (Barboza et al. of the area as semi-deciduous forest and tropical 2009). With this technique, it is possible to lowland rainforest. The climate is seasonal with a identify some species and assess patterns of rainy season from April or ! May to December, and a dry season usually from
Juan%% January to March Gallegos% (Windsor 1990). The annual rainfall is 1,600 mm and the average temperature is 27 °C. For acoustic sampling we randomly chose seven bays within BCNM as sampling sites: four on BCI, two on Bohio Island, and one on Juan Gallegos Island (Fig. 1). Each site N" was visited four times during the sampling period. Because the availability of prey to Figure 1. Sampling sites (circles) on islands at Barro Colorado Nature Monument, insectivorous bats, and Panamá. (Modified from Meyer & Kalko, 2008). ! 45 ! ! Chiroptera Neotropical 19(3) Special Volume: 44-56, December 2013 consequently their activity, could be affected by m, following the same microphone direction as in the moon cycle (Lang et al. 2006), we did not the forest edge points to record species of the UOS sample two days before and two days after the full and LOS (Fig. 2). The average distance among the moon. We visited each sampling site on a boat to four recording points was 230 m. record bat echolocation calls. Recording and analysis of echolocation calls Four microhabitats were sampled in each site For recording bat calls we used a high (bay) (Fig 2b). Two of them were located in the sensitivity condenser microphone (Microphone forest edge: upper forest edge (UFE) and lower CM 16, Avisoft, Berlin, Germany; range 10-180 forest edge (LFE); the other two were located in kHz frequency response, with higher sensitivity the open space: upper open space (UOS) and between 20 and 100 kHz) and a detector lower open space (LOS). (UltraSoundGate 116, Avisoft-RECORDER, Four recording points were marked according Avisoft, Berlin, Germany) which, connected to a to the shape of each bay (Fig. 2a). Two points computer, allow visualizing the calls thanks to a were classified as forest edge, 200 m distant from high-speed, real-time recording unit. The each other: there the microphone was directed recording parameters were the same used by upward at 90˚ above water in order to record Estrada et al. (2010): sampling rate of 300 kHz, 16 insectivorous bat species from the UFE and at 0˚ bit resolution, recording time of 6 s with 5 s of above water in order to record species from the pre-trigger time and 1 s post-trigger time, 0.05 LFE (Fig. 2b). The other two recording points buffer time, and maximal amplification and were located in the open space and were placed visualization with a 512 fast Fourier one in front of the other, perpendicularly to the transformation (FFT). forest edge and separated from each other by 300
Figure 2. (A) Scheme of the recording points selected on Bohio Island’s bay, in which circles represent the points on the forest edge, and triangles represent the points at the open space. (a), (b), (c), and (d) indicate the distance between recording points. (B) Profile of the recording points showing the four microhabitats (upper forest edge, lower forest edge, upper open space, and lower open space) at each sampling site at Barro Colorado Nature Monument, Panama. ! 46 ! ! Chiroptera Neotropical 19(3) Special Volume: 44-56, December 2013
! mV 500 0 -500 A.# kHz 120 a.# c.# 100 b.# 80 60 40 d.# 20 e.#
1V mV 20 ms 250 0 -250 B.# kHz 120 100 80 60 b.# a.# c.# 40 20 d.# e.#
1V 50 ms
Figure 3. Measurements taken from (A) Rhynchonycteris naso and (B) Lasiurus ega. (a) QCF component, (b) FM componente, (c) principal peak frequency of QCF component, (d) duration of the call, (e) pulse interval between the beginning of a call and the start of the next call. Recording made at Barro Colorado Nature Monument, Panama.
Every night one bay was visited, and at each Recordings were analyzed in Avisoft SASLAB bay we sampled the four recording points (UFE, Pro 4.52 (Raimund Specht, Avisoft, Berlin, LFE, UOS, and LOS). At each point we recorded Germany), in which spectrograms were visualized bat calls for 10 min: 5 min with the microphone with the following settings: 1) Window: pointing upwards for UFE and UOS, and 5 min Hamming, 2) FFT: 256, 3) Frame: 100% and 4) with the microphone pointing to the side parallel Overlap: 50%. We counted the number of bat to the water for LFE and LOS (Fig. 2b). It took 4 h passes per species in each recording sequence per night, from 18:30 to 22:30, to sample the calls, using the definition of bat pass as two or more including moving from one sampling point to pulses or echolocation pulses emitted by a bat another. No recordings were made while moving flying perpendicularly to the microphone (Fenton from point to point. After the first 10 min in each 2004). If two calls were separated from each other points, we repeated the recordings in the same by a gap of three times pulse interval or more they order, as many times as necessary, to complete were regarded as two bat passes (Estrada et al. four hours of sampling per bay per night. At each 2010). To validate our data, we observed the visit, recording started at a different point, either number of times when there was an increase on the edge of the island or in the open space. followed by a decrease in the amplitude of the When it rained, we stopped recording and oscillogram. If we had more than one species in continued the next day from the time when the same file, we counted each of these as separate recordings were stopped the previous day in order bat passes. to complete the working hours. ! 47 ! ! Chiroptera Neotropical 19(3) Special Volume: 44-56, December 2013
Foraging activity was measured by counting Since bat passes represent an activity index, the number of feeding attempts for each species as multiple bat passes may be obtained from the it can be observed by the presence of a terminal same individual. However, this is a great tool for phase (feeding buzz) in the echolocation calls activity data and behavior that could not be (Barboza et al. 2009; Schnitzler & Kalko 2001; achieved using only traditional techniques (Kalko Kalko & Schnitzler 1998). There can be more than et al. 2008; Kalko & Handley 2001). Therefore, one terminal phase (single species or several) in a we used the term "relative activity", following the single recording file and each was counted methodology proposed by Estrada et al. (2010), independently. By doing so, we obtained the which generated a count of individuals by number of feeding attempts per species within recording the presence of a particular species in each microhabitat. every five minutes recording point per In order to identify species in each microhabitat, and then pooling across all spectrogram, we used four important criteria microhabitats. This measure of “relative activity” (Barboza et al. 2006; 2009). First, we noted the was used for all statistical analyzes. Following highest intensity of the harmonic of the call (Fig. Estrada et al. (2010), we recognize that this 3a). Second, we observed the shape of the call and measure of the relative activity is not equivalent to we identified the following main components: the abundances measured with mist nets. Frequency modulated (FM) is a broadband In order to test whether the aerial insectivorous component characterized by an element of large bat community was well sampled, we built species bandwidth ; constant frequency (CF) is a accumulation curves for each microhabitat narrowband component, where the energy of the (Moreno & Halffter 2000) using the software signal is maintained at a constant frequency with Estimates 8.2 (Colwell 2006), which were frequency changes of a few hundred Hz within the adjusted through 1,000 randomizations using the component; and the quasi-constant frequency number of sampling nights as the effort unit (same component (QCF) is a narrowband component for all microhabitats). The rank-relative activity when the energy is concentrated in a band clearly curves (RRA curves) were used to represent bat shorter than in the previous case and with activity patterns per microhabitat. They are similar frequency changes of a few kHz between the onset to rank abundance curves (Feisinger 2003). and the end of the component (shallow Furthermore, those curves allowed us to determine modulation) (Fig. 3a,b - Kalko & Aguirre 2007; which species were the most active, and to test Schnitzler & Kalko 2001; Kalko & Schnitzler whether the hierarchy of species abundance was 1998). Third, after having identified these similar among the sampled microhabitats. In the components, we measured the peak frequency of RRA curves, the ordinate axis shows the logarithm the highest energy, taken at the middle of the call of the number of bat passes per species (in our spectrum (Fig. 3c). Finally, as a fourth feature, we case the count of the presence of each species measured call duration (from the beginning to the every 5 min of recording), and the abscissas shows end of one call) (Fig. 3d), and pulse interval the species ranked from highest to lowest activity. between calls (from the beginning of a call to the A positive feature of RRA curves is that they take beginning of the next) (Fig. 3e). into account the identity of each species and its Additionally we consulted the echolocation sequence of appearance (Feinsinger 2003). We calls reference library of species identified in the used a two-sample Kolmogorov-Smirnov test for BCNM and its surroundings which was comparisons among RRA curves between sampled constructed with compilation of more than 15 microhabitats, bootstrapping 1000 samples to years of research by Elisabeth Kalko and obtain p values (Efron 1982). With this colleagues (E. Kalko, unpublished). Literature was randomization technique we created a continuous also consulted (Estrada et al. 2010; Jung et al. distribution to compare our RRA curves and 2007; Rydell et al. 2002; Siemers et al. 2001; calculate the statistical significance of the test Schnitzler et al. 1994) (Estrada et al. 2010). Our confidence level was 95% (α =0 .05). Calls were categorized according to their quality as 1) Excellent, when there was a faint To measure the degree of similarity between background noise and it was easy to distinguish microhabitats, we calculated the Morisita-Horn the components of the calls because the signals index (Moreno 2001) with the program EstimateS were strong and not overloaded; 2) Good, with 8.2. (Colwell 2006). some background noise or overload, but it still Finally, to check for microhabitat preferences easy to distinguish call´s components and measure of a particular species, we conducted a their frequency and duration; 3) Poor, with a high Correspondence Factor Analysis (CFA) to detect background noise when calls were too faint. Poor relationships between sampling sites and quality calls were discarded. community composition (Quinn & Keough 2002). We performed this analysis by considering: 1) the Data analysis ! 48 ! ! Chiroptera Neotropical 19(3) Special Volume: 44-56, December 2013
number of bat passes (excellent and good quality) number of species recorded was Molossidae (nine by species every ten minutes of recording in each species), followed by Emballonuridae (seven microhabitat, and 2) the number of feeding species), Vespertilionidae (five species), attempts by each species in each microhabitat. For Mormoopidae (three species), and Noctilionidae all the statistical analyses we used a confidence (two species) (Table 1). level of 95% (α=0 .05). The sonospecies identified to the genus were: Results (1) Saccopteryx sp., found at a frequency range between S. bilineata and S. leptura, which We made a total of 112 h of sampling in 28 probably suggests that is is a different species due nights of work. We recorded 3,095 bat passes and to previous similar acoustic records and captured 520 feeding attempts, of which only 1,728 bat individuals; (2) Eumops sp., which, due to its passes and 335 feeding attempts were either frequency range and call shape, could be either E. excellent or good according to our quality criteria glaucinus or E. auripendulus; and (3) Molossus (Table 1). We recorded a total of 26 sonospecies: sp., which, due to its frequency range and call 19 identified to the species, three to the genus, and shape, could be either M. coibensis or M. four to the family. The family with the larges sinaloae.
Table 1. List of aerial insectivorous bat species recorded in the studied microhabitats (upper forest edge, lower forest edge, upper open spaces, and lower open space), with the total number of bat passes (BP) and the number of feeding attempts (FA), which correspond to excellent and good calls recorded for each microhabitat at Barro Colorado Nature Monument, Panama.
Forest Edge Open Space TOTAL Species of aerial insectivorous bats Upper Lower Upper Lower BP FA BP FA BP FA BP FA BP FA Emballonuridae Diclidurus albus 34 12 31 19 63 11 20 7 148 49 Peropteryx kappleri 17 6 5 1 0 0 0 0 22 7 Peropteryx macrotis 8 0 1 0 0 0 0 0 9 0 Rhynchonycteris naso 10 2 57 11 0 0 4 0 71 13 Saccopteryx bilineata 95 32 80 23 4 1 3 0 182 56 Saccopteryx leptura 29 11 38 11 0 0 1 0 68 22 Saccopteryx sp. 13 9 21 8 1 0 2 2 37 19 Mormoopidae Pteronotus personatus 6 0 0 0 1 0 1 0 8 0 Pteronotus gymnonotus 1 0 0 0 0 0 0 0 1 0 Pteronotus parnellii 1 0 2 0 1 0 1 0 5 0 Noctilionidae Noctilio albiventris 31 3 111 26 5 1 28 7 175 37 Noctilio leporinus 10 0 53 17 16 2 35 14 114 33 Vespertilionidae Lasiurus ega 0 0 1 0 15 3 8 1 24 4 Myotis albescens 0 0 32 13 0 0 9 1 41 14 Myotis nigricans 30 4 46 3 3 0 0 0 79 7 Myotis cf. riparius 29 2 17 1 1 0 2 0 49 3 Vespertilionidae 1 3 0 14 2 0 0 0 0 17 2 Molossidae Cynomops greenhallii 0 0 1 0 0 0 0 0 1 0 Cynomops planirostris 4 1 4 0 1 0 1 0 10 1 Eumops sp. 68 1 42 2 67 7 38 4 215 14 Eumops underwoodi 0 0 0 0 5 0 3 0 8 0 Molossus sp. 27 0 63 18 7 0 4 0 101 18 Molossus molossus 65 8 56 1 12 2 3 0 136 11 Molossidae 1 1 0 5 2 18 4 4 0 28 6 Molossidae 2 24 5 60 7 39 3 22 0 145 15 Molossidae 3 4 1 11 1 15 2 4 0 34 4 TOTAL 510 97 751 166 274 36 193 36 1 728 335
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1.6 a. b. c. d.
Dal 1.4 Nal Nle Mol1 Esp Dal Sbi Mni Mmo Rna 1.2 Mmo Sbi Nal Nle Esp Nal Esp Esp Sle Mol2 Dal Msp Nle Dal 1.0 Mri Mal Mol2
Mni Mri Mol3
Rna Msp Nle Mol2
0.8 Sle Leg Msp
LOG (BP+1) Mal Mol1 Ssp Pka Ves1Mol2Mol3 Mmo
Pma Sbi Sbi Rna Leg Mmo Mol3 0.6 Ves1Mol3 Ssp Pka Nal
Ppe Cpl Cpl Mni Msp 0.4
Leg Sle Ssp Ppe Ppa Mri Cpl Eun Pgy Ppa Mol1 PmaPpa Cgr Mol1 Ssp Ppe Ppa Mri Cpl Eun
0.2 Rank of species Figure 5. Rank-relative activity curves for: (a) upper forest edge, (b) lower forest edge, (c) upper open space, and (d) lower open space. The Y-axis shows the logarithm of the number of bat passes (BP) per species of aerial insectivorous bat, and the X-axis shows the species ranked from highest to lowest activity at Barro Colorado Nature Monument, Panama. Dal: Diclidurus albus, Pka: Peropteryx kappleri, Pma: P. macrotis, Rna: Rhynchonycteris naso, Sbi: Saccopteryx bilineata, Sle: S. leptura, Ssp: Saccopteryx sp., Ppe: Pteronotus personatus, Pgy: P. gymnonotus, Ppa: P. parnellii, Nal: Noctilio albiventris, Nle: N. leporinus, Leg: Lasiurus ega, Mal: Myotis albescens, Mni: M. nigricans, Mri: M. cf. riparius, Ves1: Vespertilionidae 1, Cgr: Cynomops greenhallii, Cpl: C. planirostris, Esp: Eumops sp., Eun: E. underwoodi, Msp: Molossus sp., Mmo: M. molossus, Mol1: Molossidae 1, Mol2: Molossidae 2 y Mol3: Molossidae 3. in community structure. The LFE showed higher evenness (based on 25 the curve width) and a smaller a. number of rare species (indicated b. by a shorter curve tail) than the 20 c. others (Fig. 5a). Diclidurus albus d. showed the highest activity pattern
15 at UFE and UOS (with 34 and 63 passes respectively) (Fig. 5a,c). However, the hierarchy order of 10 the species’ relative activity differed between these two Numberspecies of microhabitats. At LEF Noctilio 5 albiventris showed the highest activity pattern, and at LOS N. albiventris, N. leporinus, and 0 Eumops sp. were equally active 0 5 10 15 20 25 30 (Fig 5b,d). It is important to Number of sampling nights emphasize the presence of some Figure 4. Species accumulation curves built for each microhabitat species that only were recorded in sampled at Barro Colorado Nature Monumen, Panama, where (a) lower one or two microhabitats, such as forest edge, (b) upper forest edge, (c) open lower space, and (d) upper open space. Pteronotus gymnonotus, which was recorded only once at UFE, or Cynomops greenhallii which also The species accumulation curves showed that was recorded only once at LFE. Species such as we recorded 23 species at LFE (Fig. 4a), 22 Peropteryx kappleri, P. macrotis and species at UFE, 18 at UOS, and 23 at LOS. The Vespertilionidae 1 were recorded only at the forest curves tending to stabilize the most were the ones edge (upper and lower) but never at open space associated to the forest edge. microhabitats. In contrast, Eumops underwoodi was recorded only at open spaces (upper and Overall, the RRA curves of different lower) (Fig. 5). microhabitats were little different from each other in activity pattern, but there seem to be differences
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C (i,j) UFE LFE UOS LOS analysis (CFA) showed 22 that there was a significant dependency between Upper Forest Edge (UFE) 1 recorded bat species and 2 Lower Forest Edge (LFE) 0.87 1 sampled microhabitats (χ Upper Open Space (UOS) 0.63 0.47 1 = 754.98, d.f. = 75, p < 0.0001), where the first Lower Open Space (LOS) 0.77 0.79 0.74 1 two axes (F1 and F2) explained most of the
1! ! variation (85.86% Table 2. Values of the Morisita-Horn index of similarity (C22 (i,j)) calculated for the studied microhabitats (upper forest edge, lower forest edge, upper open cumulative). The CFA spaces, and lower open space) at Barro Colorado Nature Monument, Panama. calculated with the number of bat passes showed an association between some The Kolmogorov-Smirnov test detected species and microhabitats (Fig. 6). Saccopteryx significant differences in the distribution of RRA bilineata, Myotis riparius, Molossus molossus, and curves in all sampled microhabitats (p < 0.0001). Cynomops planirostris, tending to prefer UFE, The Morisita-Horn index (Table 2) indicates while Rhynchonycteris naso, Saccopteryx leptura, that, in terms of species composition, the two most Saccopteryx sp, Vespertilionidae 1, M. nigricans, similar microhabitats were UFE and LFE (C22 (i, j) and Molossus sp. seem to bemore strongly = 0.87), whereas the least similar microhabitats associated to LFE. The species that showed where LFE and UOS (C22 (i, j) = 0.47). stronger association with UOS were Diclidurus In general, the correspondence factorial albus and Molossidae 1, while Noctilio leporinus,
1.5 Pgy
Pma 1.0 Ppe Pka
0.5 Mri UFE Sbi Mmo Nal Esp Cpl Dal UOS Sle Mol1 Leg Eun Mni Mol3 0.0 Ssp Ppa Mol2 Msp
F2(24.96%) LOS Nle Ves1 LFE -0.5 Rna
Mal Cgr -1.0
-1.5 -1.0 -0.5 0.0 0.5 1.0 1.5 2.0
F1(60.89%) Figure 6. Correspondence factorial analysis with the number of passes of aerial insectivorous bats recorded at Barro Colorado Nature Monument, Panama. There was a tendency of each bat species to forage the upper forest edge (UFE), lower forest edge (LFE), upper open space (UOS) or lower open space (LOS). Emballonuridae (circles): Dal: Diclidurus albus, Peka: Peropteryx kappleri, Pema: P. macrotis, Rna: Rhynchonycteris naso, Sbi: Saccopteryx bilineata, Sle: S. leptura, Ssp: Saccopteryx sp. Mormoopidae (downward triangles): Ppe: Pteronotus personatus, Pgy: P. gymnonotus, Ppa: P. parnellii. Noctilionidae (rhombus): Nal: Noctilio albiventris, Nle: N. leporinus. Vespertilionidae (upward triangles): Leg: Lasiurus ega, Mal: Myotis albescens, Mni: M. nigricans, Mri: M. cf. riparius, Ves1: Vespertilionidae 1. Molossidae (squares): Cgr: Cynomops greenhallii, Cpl: C. planirostris, Esp: Eumops sp., Eun: E. underwoodi, Msp: Molossus sp., Mmo: M. molossus, Mol1: Molossidae 1, Mol2: Molossidae 2 y Mol3: Molossidae 3. ! 51 ! ! Chiroptera Neotropical 19(3) Special Volume: 44-56, December 2013
1.5 Leg
Mol1 Mol3 UOS 1.0 Mmo Cpl Esp
Pka 0.5 UFE Mri Mol2 Dal Sbi Mni Sle Ssp
F2 37.19% F2 0.0
LOS LFE -0.5 Rna Nal Nle
Ves1 Mal Msp -1.0 -1.5 -1.0 -0.5 0.0 0.5 1.0 1.5 2.0
F1 48.39% Figure 7. Correspondence factorial analysis with the number of feeding attempts of aerial insectivorous bats recorded at Barro Colorado Nature Monument, Panama. There was a tendency of each bat species to forage on the upper forest edge (UFE), lower forest edge (LFE), upper open space (UOS) or lower open space (LOS). Emballonuridae (circles): Dal: Diclidurus albus, Peka: Peropteryx kappleri, Rna: Rhynchonycteris naso, Sbi: Saccopteryx bilineata, Sle: S. leptura, Ssp: Saccopteryx sp. Noctilionidae (rhombus): Nal: Noctilio albiventris, Nle: N. leporinus. Vespertilionidae (upward triangles): Leg: Lasiurus ega, Mal: Myotis albescens, Mni: M. nigricans, Mri: M. cf. riparius, Ves1: Vespertilionidae 1. Molossidae (squares): Cpl: C. planirostris, Esp: Eumops sp., Molossus sp., Mmo: M. molossus, Mol1: Molossidae 1, Mol2: Molossidae 2 y Mol3: Molossidae 3.
Molossidae 2, and Molossidae 3 seem to be more Discussion strongly associated to LOS. The species Peropteryx macrotis, P. kappleri, Pteronotus We found differences in species composition gymnonotus, P. personatus, Myotis albescens, and between the studied microhabitats, and those Cynomops greenhallii were more dispersed differences are related to the echolocation and between the upper and lower forest edge. Other foraging strategies of the bats recorded in each species, such as Pteronotus parnellii, Noctilio microhabitat. Out of all results, the albiventris, Lasiurus ega, Eumops sp., and E. correspondence factorial analysis supports this underwoodi showed a similar trend to prefer the hypothesis the most, both in terms of number of open space. bat passes and feeding attempts. As proposed by Schnitzler & Kalko (2001), there were species that Considering the number of feeding attempts, showed a clear preference for upper and lower the CFA showed which microhabitats were used forest edge. These species correspond to those that as feeding sites (Fig. 7). P. kappleri, S. bilineata, forage in background cluttered space and have the S. leptura, Saccopteryx sp., M. riparius, C. following characteristics: echolocation calls with planirostris, and M. molossus were usually found relatively high frequeny (between 35 and 55 at UFE, whereas D. albus and Molossidae 2 were kHz.), duration between 5 and 14 ms, and associated with the upper stratum (UFE and UOS). intermediate pulse interval (between 65 and 150 With respect to LFE, we recorded more feeding ms). Furthermore, almost all of the echolocation attempts by R. naso, and Vespertilionidae 1 calls that we recorded have a combination of FM seemed to share feeding sites with Molossus sp., and QCF components. One of the main differences M albescens, and N. albiventris. At UOS we found between these species is their foraging strategy: Lasiurus ega, Eumops sp., Molossidae 1, and some capture their prey in the vertical stratum of Molossidae 2. Finally, N. leporinus was recorded the forest edge or in the canopy (e.g., S. bilineata feeding more often at LOS. and M. molossus), whereas others usually capture their prey on the water substratum (e.g., R. naso). ! 52 ! ! Chiroptera Neotropical 19(3) Special Volume: 44-56, December 2013
With respect to the Saccopteryx species associated with water, while Estrada et al. (2010) recorded on the forest edge (LFE and UFE in our classified them as typical of open space but also study), Bernard (2001) has suggested that these associated with water. In both cases, these species species tend to be relatively common in gaps and are associated with areas lacking obstacles and forest edge, to which we agree. Additionally, our will correspond to what we have classified as LFE results are consistent with Adams et al. (2009) and as well as LOS. In the case of Eumops sp. both Jones (1999), who suggested that species that authors classified this species as representative of forage in areas with dense background vegetation open space, which is consistent with the results of tend to have short and high frequency calls with our study, where this species was mostly active in combinations of FM and QCF components. In LOS and third in rank at the UOS. contrast, species that have a tendency to prefer Out of the two species recorded once, C. LOS and UOS, are adapted to foraging in greenhallii and P. gymnonotus, the first was found uncluttered space, as classified by Schnitzler & at the UFE, coinciding with Kalko et al. (2008) Kalko (2001). They have different characteristics and Estrada et al., (2010) who associated this compared to those that prefer LFE and UFE: low species with the forest and not with the open frequency echolocation calls (between 9 and 30 space. The second one, P. gymnonotus, was kHz), except for N. albiventris and N. leporinus recorded at the LFE; however Kalko et al. (2008), (between 50 and 70 kHz), longer call duration classified it as a typical species of open space, but (between 15 and 22 ms), and long pulse intervals also mentioned that this species has a very low (between 91 and 430 ms). As on the forest edge, sampling rate, and in fact was not recorded by the difference between them is their foraging Estrada et al. (2010). Therefore, it could be strategy, because some are better adapted to fly at considered a rare species and their recording was a UOS (e.g. D. albus and Eumops sp.), whereas valuable finding in this study. others capture their prey on water associated with For the species recorded only at the LFE, such LOS (e.g. N. leporinus). Those results are as P. kappleri and P. macrotis, Kalko et al. (2008) consistent with previous studies (e.g. Adams et al. classified them as typical edge species, unlike 2009; Holderied et al. 2008), which indicates that Estrada et al. (2010) who reported them as open species adapted to foraging in wide open spaces space bats. With this study, similarly to Kalko et emit low frequency calls, long calls with long al. (2008), we confirmed that these species are pulse intervals, and most of their calls have QCF typical of edge. Finally, E. underwoodi, which components. Those are adaptations to prey was recorded in open spaces (upper and lower), detection in open space, with long pulses in their Kalko et al. (2008) classified them as open space search calls that allow them to listen to the echoes habitats, same as in our work. of distant objects (Holderied & von Helversen 2003). The RRA curves and the Morisita-Horn similarity index, reasonably showed that both, the Schaub & Schnitzler (2007) noted that UFE and LFE, are the most similar habitats, differences in echolocation behavior separate sharing a large number of species. According to species of "edge" and "open space", but obviously the classification of Kalko & Schnitzler (2001), some distinctions may be specific to each species. these species are adapted to foraging in space with The differences mentioned by these authors are background cluttered space at the forest edge and consistent with our results, where the species from at water level. The same applies to the open space the "edge" showed short echolocation calls with (upper and lower) micro-habitats. They were QCF and FM components, while the species from similar to each other and showed species adapted "open space" had longer calls and QCF to foraging in the open space (Schnitzler & Kalko component. Thus, these bats are adapted to exploit 2001). their resources in different types of habitats, both within the forest edge and open space (Schnitzler Some of our data was also consistent with & Kalko 2001; Siemers & Schnitzler 2000; Kalko those reported by Estrada et al. (2010), who & Schnitzler 1998). conducted a study to see the effect of habitat fragmentation on aerial insectivorous bats in the The Rank-Relative Activity (RRA) curves interior of several islands of the BCNM. They showed that D. albus was the most active species recorded 23 species in total, from which 16 were in the UFE and in the UOS (Fig. 5). These results the same as presented in this study, and seven are consistent with those of Estrada et al. (2010) were different. Furthermore, some species (e.g. and Kalko et al. (2008) who classified this species Centronycteris centralis and Cormura as a typical open space bat. At the LFE and at the brevirostris) can be associated with the forest LOS, N. albiventris appeared to be the most interior and not with the forest edge. However, abundant species, together with N. leporinus and some species we recorded (e.g. Rhynchonycteris Eumops sp. Kalko et al. (2008) classified N. naso and Diclidurus albus) are more adapted to albiventris and N. leporinus as edge species foraging in the external areas of the forest and not
! 53 ! ! Chiroptera Neotropical 19(3) Special Volume: 44-56, December 2013 in the inside, at least in what we have show for the Simposio Ecuatoriano sobre Investigación y BCNM. It remains to be seen if this applies to Conservación de Murciélagos (Edited by Tirira, other sites, where some bats within the same D.), pp. 30-31. In press in Ecuador. family and same functional group, forage Bernard E. 2001. Vertical stratification of bat exclusively in the forest interior (such as C. communities in primary forests of Central brevirostris) whereas others don’t. Amazon, Brazil. Journal of Tropical Ecology In conclusion, our study is one of the few that 17: 115-126. have assessed the ecology of aerial insectivorous Cleveland C.J.; Betke M.; Federico P.; Frank J.D.; bats, the least known group of bats in the Hallam T.G.; Horn J.; López J.D.Jr.; Neotropics (Jung et al. 2007; Jung & Kalko 2010). McCracken G.F.; Medellín R.A.; Moreno- We emphasize the importance of using acoustic Valdez A.; Sansone C.G.; Westbrook J.K. & monitoring as a tool to obtain valuable Kunz T.H. 2006. Economic value of the pest information on how these species partition their control service provided by Brazilian free-tailed flight space. Finally, it is clear that the use of bats in Southcentral Texas. Frontiers in Ecology standard protocols greatly improves the quality of and Environment 4: 238-243. the data that can be obtained. With the sampling Colwell R.K. 2006. EstimateS: statistical design implemented in this study, we were able to estimation of species richness and shared better understand how the habitat is being used species from samples. Version 8.2 and how resources might be partitioned among aerial insectivorous bats in the Neotropics. (http://viceroy.eeb.uconn.edu/estimates/, last access June 2013). Acknowledgements Estrada-Villegas S.; Meyer C.F.J. & Kalko E.K.V. We thank the Smithsonian Tropical Research 2010. Effects of tropical fragmentation on aerial Institute for the fellowship program “Adelante” insectivorous bats in a land-bridge island and the Bolivian Bat Conservation Program for system. Biological Conservation 143:597-608. the funding. Thanks to all staff of Barro Colorado Efron B. 1982. The jackknife, the bootstrap and Nature Monument, researchers of the "Bat Lab", other resampling methods. Society for Industrial in special to Larissa Albrecht and Katrin Heer. We and Applied Mathematics, CBMS-NSF thank all the people on Barro Colorado Island, Monograph 38, Philadelphia. who participated in the fieldwork. Thanks to Sergio Estrada for his invaluable collaboration Feisinger P. 2003. El diseño de estudios de campo throughout the development of this study. Thanks para la conservación de la biodiversidad. to Jesús Muñoz and the Master’s Program in Editorial FAN, Santa Cruz de la Sierra, Bolivia. Biodiversity and Conservation of Tropical Areas Fenton M.B. 2004. Reporting: essential from “Consejo Superior de Investigaciones information and analysis. In: Bat Echolocation Científicas de España”. Thanks to Karen Córdova Research: tools, techniques and analysis. for her collaboration in the translation and (Edited by Brigham M.; Kalko E.K.V.; Jones correction of the manuscript. G.; Parsons S. & Limpens H.J.G.A.), pp. 133- 140. Bat Conservation International, Austin. References Findley J.S. 1993. Bats: a community perspective. Adams M.D.; B.S. Law & K.O. French. 2009. Cambridge Studies in Ecology. Cambridge Vegetation structure influences the vertical University Press, Cambridge. stratification of open-and edge-space aerial- foraging bats in harvested forests. Forest Hayes J.P. 2000. Assumptions and practical Ecology and Management 258: 2090-2100. considerations in the design and interpretation of echolocation-monitoring studies. Acta Aguirre L.F.; Herrel A.; Van Damme E.& Chiropterologica 2: 225-236. Matthysen E. 2003. The implication of food hardness for diet in bats. Functional Ecology 17: Holderied M. W. & von Helversen O. 2003. 201-212. Echolocation range and wingbeat period match in aerial-hawking bats. Proceedings of the Royal Barboza K.; Aguirre L.F. & Kalko E.K.V. 2006. Society of London B 270: 2293-2299. Protocolo estandarizado para obtener el registro y el análisis de llamadas emitidas por Holderied M.W.; Baker C.J.; Vespe M. & Jones murciélagos. Revista de Ciencia y Tecnología 5: G. 2008. Understating signal design during the 9-13. pursuit of aerial insects by echolocation bats: tools and applications. Integrative and Barboza K; Pérez-Zubieta. J.C.; Kalko E.K.V.; Comparative Biology 48: 74-84. Aguirre L.F.; Estrada-Villegas S. & Ossa G. 2009. La importancia del monitoreo acústico en Holdridge L.R. 1967. Life zone ecology, Rev. ed. el estudio de las comunidades de murciélagos en Occasional Papers of the Tropical Science Latinoamérica. In: Memorias del Primer Center. San José, Costa Rica.
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Jones G. 1999. Scaling of echolocation call Lang A.B.; Kalko E.K.V.; Römer H.; Bockholdt parameters in bats. Journal of Experimental C. & Dechmann D.K. Activity levels of bats and Biology 202: 3359-3367. katykids in relation to the lunas cycle. Jung K.; Kalko E.K.V. & von Herlversen O. 2007. Oecologia 146: 659-666. Echolocation calls in Central American Meyer C.F.J. & Kalko E.K.V. 2008. Assemblage- emballonurid bats: signal design and call level responses of phyllostomid bats to tropical frequency alternation. Journal of Zoology, forest fragmentation: land-bridge islands as a London 272: 125-137. model system. Journal of Biogeography 35: Jung K. & Kalko E.K.V. 2010. Where forest 1711-1726. metes urbanization: foraging plasticity of aerial Moeschler P. & Blant J.-D. 1990. Recherches insectivorous bats in an anthropogenically appliquées á la protection des chiropteres. 3. altered environment. Journal of Mammalogy 91: Bioévaluation de structures paysageres á I'aide 144-153, de chauves-souris en activité de chasse. Kalka M.B. & Kalko E.K.V. 2006. Gleaning bats Rhinolophe 7: 19-28. as underestimated predators of herbivorous Moreno C.E. 2001. Métodos para medir la insects: diet of Micronycteris microtis biodiversidad. M&T - Manuales y Tesis SEA. (Phyllostomidae) in Panama. Journal of Tropical Vol 1. Zaragoza, España. Ecology 22: 1-10. Moreno C.E. & Halffter G. 2001. On the measure Kalka M.B.; Smith A.R. & Kalko E.K.V. 2008. of sampling effort used in species accumulation Bats limit arthropods and herbivory in a tropical curves. Journal of Applied Ecology 38: 487- forest. Science 320: 71. 490. Kalko E.K.V.; Handley C.O. & Handley D. 1996. Norberg U.M. & Rayner J.M. 1987. Ecological Organization, diversity, and long-term dynamics morphology and flight in bats (Mammalia: of a neotropical bat community. In: Long term Chiroptera): wing adaptations, flight studies in vertebrate communities (Edited by performance, foraging strategy and Cody M. & Smallwood J.), pp. 503-551. echolocation. Philosophical Transactions of the Academic Press, San Diego. Royal Society of London B, 316: 335-427. Kalko E.K.V. 1997. Diversity in tropical bats. In: Quinn G. & Keough M. 2002. Experimental Tropical biodiversity and systematics. (Edited design and data analysis for biologists. by Ulrich H.) pp. 13-43. Bonn: Zoologisches Cambridge University Press. UK, England. Forschungsinstitut und Museum Alexander Rydell, J.; Arita H.T.; Santos M. & Granados, J. König. 2002. Acoustic identification of insectivorous Kalko E.K.V. 1998. Organisation and diversity of bats (Order Chiroptera) of Yucatan, Mexico. tropical bat communities through space and Journal of Zoology(London) 257, 27-36. time. Zoology 101: 281-297. Schnitzler H.-U., Kalko E.K.V., Kaipf I. & Kalko E.K.V. & Schnitzler H.-U. 1998. How Grinnell A.D. 1994. Fishing and echolocation echolocating bats approach and acquire food. In: behavior of the greater bulldog bat, Noctilio Bat Biology and Conservation. (Edited by Kunz leporinus, in the field. Behavioral Ecology and T.H. & Racey P.A.), pp. 197-204. Smithsonian Sociobiology 35, 327-345. Institution Press, Washington. Schnitzler H.-U. & Kalko E.K.V. 2001. Kalko E.K.V. & Handley C.O.Jr. 2001. Echolocation by insect-eating bats. BioScience Neotropical bats in the canopy: diversity, 51: 557-569. community structure, and implications for Schnitzler H.-U.; Moss C.F. & Dezinger A. 2003. conservation. Plant Ecology 153: 319-333. From spatial orientation to food acquisition in Kalko E.K.V. & Aguirre L.F. 2007. echolocating bats. Trends in Ecology and Comportamiento de ecolocación para la Evolution 18: 386-94. identificación de especies y evaluación de la Schaub A. & Schnitzler H.-U. 2007. Echolocation estructura de las comunidades de murciélagos behavior of the bat Vespertilio murinus reveals insectívoros en Bolivia. In: Historia natural, the border beteen the habitat types “edge” and distribución y conservación de los murciélagos “open space”. Behavioral Ecology and de Bolivia. (Edited by Aguirre L.F.), pp. 41-53. Sociobiology 193: 1185-1194. Editorial: Centro de Ecología y Difusión Simón Siemers B.M. & Schnitzler H.-U. 2000. Natterer’s I. Patiño. Santa Cruz, Bolivia. bat (Myotis nattereri, Kuhl 1818) hawks for Kalko E.K.V.; Estrada Villegas S.; Schmidt M.; prey close to vegetation using echolocation Wegmann M. & Meyer C.F.J. 2008. Flying high signals of very broad bandwidth. Behavioral - assessing the use of the aerosphere by bats. Ecology and Sociobiology 47: 400-412. Integrative and Comparative Biology 48; 60-73.
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Siemers B.M.; Kalko E.K.V. & Schnitzler H.-U. Windsor D.M. 1990. Climate and moisture 2001. Echolocation behavior and signal variability in a tropical forest: long-term records plasticity in the Neotropical bat Myotis from Barro Colorado Island, Panama. nigricans (Schinz, 1821) (Vespertilionidae): a Smithsonian Contributions to the Earth Sciences convergent case with European species of 29: 1-145. Pipistrellus. Behavioral Ecology and Sociobiology 50, 317-328.
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! 56 ! ! Chiroptera Neotropical 19(3) Special Volume: 57-70, December 2013
Phyllostomid bat wings from Atlantic Forest bat ensembles: an ecomorphological study
Valéria da C. Tavares1,2 ! 1Departamento de Zoologia, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Universidade Federal de Minas Gerais (UFMG). Avenida Antônio Carlos, 6.627, 31270-901, Belo Horizonte, MG, Brazil. 2Programa de Pós-Graduação em Genética, Conservação e Biologia Evolutiva (PPGCBev); Instituto Nacional de Pesquisas da Amazônia (INPA), Av. André Araújo, 2.936, 69067-375, Manaus, AM, Brazil.
E-mail: [email protected]
ARTICLE Abstract. Under the assumption that wing shape predicts bat species Manuscript history: flight performance, I analyzed wing shape data of phylostomid bats Submitted in 14/Mar/2014 from Rio Doce State Park (PERD), located in the Brazilian Atlantic Accepted in 18/Jul/2014 Forest. Correlations between size-related variables in phyllostomid Available on line in 26/Sep/2014 species were positive as expected, with the exception of those Editor: Marco A.R. Mello between mass and aspect ratio. Wing loadings varied from low to very high, and increased with body mass less than expected. Aspect ratios were homogeneously low, and wingtips were more variable in length than in area. Most phyllostomids had tip shape indexes close to or larger than 1, with the exceptions of Chiroderma and Tonatia. The foraging guilds matrix incorporating three fruit bats ensembles amplified the number of potential, suitable niche categories for bats from PERD: (1) understorey frugivores that consume Piperaceae and have broad wing surfaces, developed interfemoral membranes, low wing loadings (WL) aspect ratios (AR), and high tip shape indexes (TSI); (2) canopy frugivores that consume Cecropiaceae and Moraceae, have high WL, variable AR tending to low, and pointed wingtips with large areas; and (3) frugivores that consume plants distributed both in open and forest habitats, with broad dietary spectrum, high WL, intermediate AR, and TSI close to 1. I hypothesize that the ecology of the bat species from PERD is constrained by flight modes correlated with species-specific flight- related characters, which consequently constraints habitat and microhabitat selection by those bats, and has implications for food choice.
Keywords: Functional morphology, niche matrix, foraging guilds, fruit bats, allometry, bat ensembles.
! wings alone (e.g. Aldridge & Rauntenbach 1986, Introduction Baggøe 1987, Norberg & Rayner 1987, Norberg An increasing body of evidence has placed 1994, Canals et al. 2001, Dietz et al. 2006, Adams bats among the most suitable models for et al. 2012), and noseleaves (e g. Bogdanowicz et ecomorphological studies (e.g., Dumont & Swartz al. 1997). 2009). The analysis of shape has been successfully Bats are the only mammals capable of active employed to the study of patterns of flight, an ability that therefore evolved only once morphological adaptation and its ecological in Mammalia. Although similar aerodynamic correlates in bats (Findley & Wilson 1982, Findley principles are involved in vertebrate flight, bat 1993, Arita & Fenton 1997, Norberg 2002). flight is highly variable according to the shape and Several studies have shown correlations between the size of wings (Norberg 1990). This variability bat morphology and performance, such as in wing shape is correlated with different foraging morphological variation in ears and wings (Fenton strategies (Norberg 1987, Norberg & Rayner 1972), wings and hindlimbs (Norberg 1981), 1987, Norberg 1994). ! 57 ! ! Chiroptera Neotropical 19(3) Special Volume: 57-70, December 2013
Since the 1970s studies focused on bat wing could contribute to niche segregation in bat morphology have reported measurements of ensembles (e.g. Fenton 1972, Humphrey & flight-related variables, such as wing loading Bonaccorso 1983). On the other hand, similarities (ratio between body mass and wing area) and in morphological functional predictors may be comparisons between bird and bat wings. Among useful for the delimitation of foraging guilds and those studies, there is the comprehensive bat ensembles. Some authors indeed have monograph by Vaughan (1959) with comparisons suggested that besides size and diet, other of morphological characters related to flight in variables such as a bat’s movement in space might species of three families, and the study by play a role in the structuring of bat ensembles Struhsaker (1961) who introduced and discussed (MacNab 1971, Humphrey & Bonaccorso 1983, the concept of aspect ratio (ratio between McKenzie & Rolfe 1986, Aldridge & wingspan and wing area). Findley et al. (1972) Rauntenbach 1986, Arita & Fenton 1997, Kalko published a first broad analysis of wing shape in 1997). McKenzie & Rolfe (1986) characterized bats at the family and tribe levels, including 136 potential niches of Australian insectivorous bats, species and data on wingtip shape. Norberg and considering foraging strategies, and using indexes her collaborators published an extensive series of to characterize the flight ability of each species. studies on physiology, bioenergetics, Aldrigde & Rauntenbach (1986) postulated that biomechanics, functional morphology, and the the wing morphology of African insectivorous bat evolution of bat flight (e.g., Norberg 1976a, b, c, ensembles play important roles in habitat and diet 1981, 1987, 1989,1990, 1994, Norberg & Rayner selection. A recent study presented data on wing 1987). Norberg and Rayner (1987) provided a morphology of Amazonian bat species (Marinello framework with a functional predictive basis for & Bernard 2014), but to date I am not aware of studies on flight ecomorphology in bats, with a any study on the wing morphology of bat multivariate analysis of wing morphology in 215 assemblages from the Atlantic forest of bat species. Flight morphology assessments have southeastern Brazil. also been used to set the ground for analyses on Neotropical phyllostomid bats have a diverse the origin and evolution of bat flight and array of dietary specializations, and all kinds of predictions on the flight biomechanics of fossil feeding habits found within chiropteran clades are bats (Norberg 1989, Simmons 1995, Simmons & represented within the family. Niche matrices have Geisler 1998, Norberg et al. 2012). proven to be informative in summarizing bat Norberg & Rayner (1987) demonstrated that ensemble structure (e.g., Fleming et al. 1972, body mass, wingspan, and wing area are the three Willig 1986, Lim & Engstrom 2001), but most important parameters of the induced flight parameters used to define them vary among power, which is related to a bat's propulsion and studies. Definition of guilds or ensembles within inertial overcoming (Thollesson & Norberg 1991). phyllostomid assemblages have traditionally been Limitations to the bat flight power may be determined by the type and size of food and by explained by several parameters, such as the feeding preferences, species diversity and parasite and the profile powers, related to the form abundance, and body size of bats (e.g., Tamsitt and the friction drag on the body and the wings of 1967, McNab 1971). Kalko et al. (1996) suggested bats (Norberg & Rayner 1987, Norberg 1990, the inclusion of observations on diet, habitat Thollesson & Norberg 1991). Relationships preference, and foraging behavior to define bat between body mass, wingspan, and wing area can ensembles in Barro Colorado Island, Panama. Lim provide information on the speed and & Engstrom (2001) characterized bat ensembles in maneuverability of flight, and are particularly Guyanan Iwokrama Reserve according to biomass, limiting in large and heavy bats (e.g., Norberg & vertical stratification, trophic-size niche, species Fenton 1988). On the other hand, the relative area diversity and abundance. and length of the wingtips are directly related to Under the assumption that wing shape can the agility and maneuverability of bats, and are predict aspects of bat flight performance (e.g., particularly limiting for small and light bats Aldridge & Rautenbach, 1986, McKenzie & (Norberg & Rayner 1987, Norberg 1994). Rolfe, 1986, Norberg & Rayner, 1987), I analyzed Ultimately, wing morphology may be a result of a wing shape data of phyllostomid bats from the combination of constraints and a compromise of Brazilian Atlantic Forest together with a set of adaptations, which themselves constraint the flight ecological data, and I suggest additional fruit bat performance of a bat. ensembles that may help understand the structure The final shape of a bat is correlated to several of these bat assemblages. requirements in terms of habitat use, and it is limited by phylogeny (Norberg 1994, Arita & Fenton, 1997). The morphology of bats has been used as a predictor of behavioral differences that
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Material and Methods AUTOCAD 14.0©. Wing characters estimated from wing images were (Fig. 1): area of the wing Study sites and ecological data (S) – twice the area of the right profile of the wing Rio Doce State Park (hereafter PERD) is a and the right portion of the tail membrane; tip area 36,000 ha lowland area of continuous Atlantic or handwing (HW) – the area encompassing the Forest located at approximately 250 km east of dactylopatagium between the digits II and V; Belo Horizonte, Minas Gerais, southeastern Brazil proximal area or arm wing (AW) – the area (19°29' S and 42°28' W). PERD is located in a between the proximal part of the bat wing large floodplain at 230 to 515 m a.s.l. (Stallings et including the propatagium, plagiopatagium, al. 1990). The vegetation is a mosaic of primary uropatagium, and half of the bat’s ventral surface; and second-growth Atlantic Forest. Fern tip length or length of hand wing (CHW) – the assemblages locally known as samambaial and length from the second and fifth digit joint and seasonally flooded grasslands dominated by thumb to the tip of the wing; and length of Cecropia are also typical. The climate is tropical proximal wing or length of the arm wing (CAW) – semi-humid, with well-defined dry winters and measured from the line that crosses the sagital rainy summers. The annual temperature averages plane of the bat body to the articulation of the 22 °C and the annual rainfall, 1,478 mm. During thumb with the digits II and V. Figure 2 illustrates the present study (January to October 1997), the wing characters measured. rainfall averaged 1,400 m and temperature, 23 °C. Additional details on the bat assemblages and bat Indexes diets in the study area are given in Tavares et al. The indexes calculated were: wing loading (2007). (WL) – weight (mass times gravitational acceleration, in g) divided by wing area (S), Morphological data calculated as WL = Mg/S, (Nm3), where M is the Individual live bats were placed on millimetric body mass, g is the acceleration of gravity (9.8 paper to be measured (Fig. 1) and photographed at m/s2), and S is wing area (S) (m2); aspect ratio standard distance and position. Photographs were (AR) – the ratio of the wingspan (WSP) and the scanned and digitalized in .bmp format using wing area (S) (Norberg 1981), calculated as AR = CORELDRAW© (Fig. 2) and processed in WSP2/S, where WSP is the wingspan (m), and S is the wing area (m2); tip area ratio index (TA) (Norberg and Rayner, 1987) – the ratio between wingtip area (HW) and the proximal wing area (CW) calculated as TA = HW/AW where HW is the hand wing area (m2), and AW is the arm wing area (m2); the linear tip length ratio (TL) (Norberg and Rayner, 1987) – the ratio
Figure 1. Platyrrhinus lineatus (Phyllostomidae) in the position for the between the wingtip and picture used for wing measurements. proximal wing length calculated as TL = CHW/CAW, where CHW is the length of the hand wing and CAW is the length of the proximal wing. Finally, the tip shape index (TSI) (Norberg and Rayner, 1987) was used to estimate the shape of the wing tip: TSI = TA/TL-TA, where TA is the tip area ratio, and TL is the tip length ratio. Statistical analysis I calculated linear regressions to test for relationships between pairs of! Figure 2: Wing profile of Artibeus obscurus showing the wing characters functional wing morphology used in the present study. The total area of the wing (S) is twice the total area variables related to active flight measured for one wing. Legend: S – wing area, HW - wingtip area, AW - (e.g. M), analyzed and proximal wing area, CHW - wingtip length, CAW – proximal wing area length, WSP – wingspan. ! 59 ! ! Chiroptera Neotropical 19(3) Special Volume: 57-70, December 2013
Figure 3: Scatterplots of log-transformed variables related to the functional flight morphology of phyllostomid bat species from Rio Doce State Park, southeastern Brazil. Legend: A = wing area (LOGS) X wingspan (LOGWSP): R2 = 0.96, F = 213, p < 0.001, β = 0.46; B = weigth (LOGM) X wingspan (LOGWSP): R2 = 0.97; F = 301 p < 0.001, β = 0.36; C = weight (LOGM) X wing area (LOGS): R2 = 0.94, F = 143 p < 0.001, β = 0.75, D = weight (LOGM) X wing loading (LOGWL): R2 = 0.57, F = 12 p < 0.05, β = 0.21; and E = weight (LOGM) X aspect ratio (LOGAR): R2 = 0.19, F = 2 p > 0.05, β = -0.067. Artibeus fimbriatus = Af, Artibeus obscurus = Ao, Artibeus lituratus = Al, Carollia perspicillata = Cp, Chiroderma doriae = Cd, Chiroderma villosum = Cv, Desmodus rotundus = Dr, Glossophaga soricina = Gs, Micronycteris schmidtorum = Ms, Platyrrhinus lineatus = Pl, Platyrrhinus recifinus = Pr, Sturnira lilium = Sl, Tonatia bidens =Tb, Uroderma magnirostrum = Um, Vampyressa pusilla = Vp. compared regression slopes and coefficients with information provided by wing and flight indexes, those expected for allometric relationships. I which allowed combinations of ratios of variables, analyzed two sets of taxa separately: one formed while supporting inference on shape (Hespenheide by phyllostomid bats from PERD and the other by 1973, Ricklefs & Miles 1994). I used the stenodermatine species, the latter by adding to my softwares SYSTAT and STATISTICA for the sample from PERD values of wing measurements statistical analyzes. from the literature (Lawlor 1973, and Norberg Niche matrices 1981). I log-transformed the average values of the selected indexes (M, WSP, and S) and built a I followed Root (1967) and Fauth et al. (1996) correlation matrix to conduct a PCA, following the in the delimitation of the concepts of community, protocol of Norberg & Rayner (1987), and assemblage, guild, and ensemble. A community is comparatively analyzed the wing morphology of a set of species that occur in the same place at the the phyllostomid bat species compiled. The PCA same time; an assemblage is a set of with log-transformed variables complemented the phyllogenetically related species within a
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Figure 4: Scatterplots of log-transformed variables related to the functional flight morphology of frugivorous stenodermatine bats from Rio Doce State Park, southeastern Brazil. Legend: A = wing area (LOGS) X wingspan (LOGWSP), R2 = 0.97; F = 450 p < 0.001, β = 0.47; B = weigth (LOGM) X wingspan (LOGWSP): R2 = 0.98; F = 646 p < 0.001, β = 0.36; C = weight (LOGM) X wing area (LOGS): R2 = 0.95 F = 279 p < 0.001, β = 0.74, D = weight (LOGM) X wing loading (LOGWL): R2 = 0.70 F = 29.9 p < 0.001, β = 0.24, and E = weight (LOGM) X aspect ratio (LOGAR): R2 = 0.11, F = 1.6, p > 0.05, β = -0.04. Artibeus fimbriatus = Af, Artibeus jamaicensis =Aj, Artibeus obscurus = Ao, Artibeus phaeotis = Ap, Artibeus lituratus = Al, Chiroderma doriae = Cd, Chiroderma villosum = Cv, Platyrrhinus helleri = Ph, Platyrrhinus lineatus = Pl, Platyrrhinus recifinus = Pr, Sturnira lilium = Sl, Uroderma magnirostrum = Um, Uroderma bilobatum = Ub, Vampyrodes caraccioli = Vc, Vampyressa pusilla = Vp. community; a guild is a set of species, without weight, I used the factor of 2.0 (1. 263) as regard for taxonomic position, which exploit the suggested by McNab (1971) based on the earlier same class of resource in a similar way; an work of Hutchison (1959). The results of ensemble is a set of phyllogenetically related vegetation and the dietary survey incorporated to species that use a similar set of resources within a the reconstruction of the second niche matrix are community. described in Tavares et al. (2007). I built a trophic-size niche matrix as developed Results by McNab (1971) and a foraging-guilds/fruit bats ensembles matrix including classes of weight, Analysis of wing morphology habitat preference, diet, foraging mode, and wing The regression slopes and β values resulting functional morphology, modified from Kalko et al. from the analyses of the functional morphology (1996) and Kalko (1997) for all bats recorded in parameters related to the flight of phyllostomids PERD up to Tavares et al. (2007). For classes of are listed in the table 1. Relationships between S
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Table 1. Component loadings from the analysis of principal components for flight functional morphology variables analyzed. Characters Factor1 Factor2 Factor3 Mass (m) 0.994 0.101 0.047 Wingspan (wsp) 0.997 0.040 -0.063 Area (s) 0.990 -1.0 0.016 Variance explained 98.7% 1.1% 0.2% 1
Table 2. Mean values for the wing parameters for the Phyllostomidae bats from the Parque Estadual do Rio Doce. Legend: M = Mass, WSP = Wingspan, S = Area, WL = Wing Loading, AR = Aspect Ratio, TA = Tip Area, TL = Tip Length, TSI = Tip Shape Index. Characters Indexes Taxon N M (Kg) WSP S (m2) WL AR TA TL TSI (m) (Nm-2) (mm) (mm) Artibeus fimbriatus 7 0.063 0.510 0.046 13.4 5.6 0.737 1.476 1.0 Artibeus lituratus 19 0.064 0.486 0.038 16.6 6.2 0.726 1.368 1.1 Artibeus obscurus 4 0.041 0.407 0.025 16.1 6.6 0.791 1.376 1.0 Carollia perspicillata 16 0.015 0.308 0.015 9.7 6.2 0.939 1.618 1.4 Chiroderma doriae 5 0.025 0.342 0.015 15.9 7.6 0.788 1.959 0.7 Chiroderma villosum 3 0.026 0.361 0.018 14.3 7.3 0.698 1.884 0.6 Glossophaga soricina 4 0.009 0.251 0.011 8.8 6.0 0.797 1.239 1.7 Micronycteris 3 0.009 0.235 0.009 9.9 6.9 0.717 1.397 1.0 schmidtorum Platyrrhinus lineatus 5 0.028 0.349 0.019 13.8 6.1 0.793 1.579 1.0 Platyrrhinus recifinus 4 0.019 0.313 0.015 12.1 6.6 0.778 1.452 1.2 Sturnira lilium 5 0.018 0.307 0.014 12.6 6.5 0.911 1.715 1.1 Tonatia bidens 4 0.025 0.340 0.022 10.9 5.1 0.655 1.449 0.8 Uroderma 3 0.021 0.323 0.017 12.2 6.1 0.893 1.743 1.1 magnirostrum Vampyressa pusilla 3 0.009 0.240 0.009 9.5 6.6 0.852 1.675 1.0
1 and WSP, M and WSP, and M and S (figs. 3 and 4) low and ranged from 5.1 to 7.6 (table 2). Overall were strongly proportional, as expected by wingtips of phyllostomids had more variation in allometry since these are size variables. On the linear measurements and more similar areas, other hand, there was no correlation between M although area variation occurs. Vampyressa and AR for the groups analysed (figs. 3 and 4). pusilla, Uroderma magnirostrum, Sturnira lilium, st The 1 principal component resulting from the and Carollia perspicillata have large tip areas PCA analysis accounted for most (98.7%) of the representing approximately 90% of the proximal variation, the remaining 1.3% explained by the 2nd rd wing area, while other species have lower values, and 3 component altogether. Weight (M), accounting for less than 80% of the proximal wing wingspan (WSP), and wing area (S) were all area. highly correlated (table 1). The plot of the 1st and Most phyllostomids had TSI close to, or larger the 2nd component scores showed mainly than 1, with the exception of Chiroderma doriae, variation in size of the wings of the different Chiroderma villosum, and Tonatia bidens, which species, and the second component represented had TSI values lower than 1 (Table 2, fig. 6). WL variation among the species (fig. 5). Artibeus fimbriatus, A. obscurus, P. lineatus, V. The values for wing loading varied among the pusilla and M. schmidtorum had TSI = 1 indicating phyllostomid species sampled (table 2): low WL that their wing tips are neither long or large and species (up to 9.4), moderate WL species (9.5 – have the approximate shape of an equilateral 11.9), high WL species (12 – 13.9), and very high triangle. In contrast, TSI values were large for WL species (≥14). In contrast, the aspect ratio of Carollia perspicillata (1.4) that had also the phyllostomids from PERD was homogeneously largest TA within the present sample and for Glossophaga soricina (1.7) that had a short ! 62 ! ! Chiroptera Neotropical 19(3) Special Volume: 57-70, December 2013
Figure 5. Scatterplot of the first and second principal components of a PCA based on wing morphology characters of phyllostomid bats from Rio Doce State Park, southeastern Brazil.
wingtip proportionally to its TA. Chiroderma developed uropatagium that contributed to its doriae and C. villosum had the longest and more funcional wing and to the lowering of its WL, pointed wingtips among the bats studies, and T. which was in turn moderate, and it had a relatively bidens had a shortened and acute wingtip (Table 2, large AR and intermediate wingtips (approximate fig. 6). The relative length of the wingtip was the proportions of an equilateral triangle). The nectar- most variable character analyzed ranging from a feeding bat Glossophaga soricina had a lower WL low relative length of the tip in Glossophaga compared to M. schmidtorum because of its large soricina to the longest wing tip of Chiroderma S. The wingtip of G. soricina was long and broad doriae (Table 2). having the largest TA and TL among the species Among small-bodied bats, the insectivourous studied. The small fruit bat Vampyressa pusilla foliage-gleaner Micronycteris schmidtorum had a had very broad wings proportionally to its size,
TA=0,5T L 1.1
1 Cp Sl 0.9 Vp TA Um Gs Pl Cd 0.8 Pr Al Af Cv 0.7 Tb
0.6
0.5 1.1 1.3 1.5 1.7 1.9 2.1 TL Figure 6. Scatter plot with values of wing tip shape (TSI) for bats from from Rio Doce State Park, southeastern Brazil. TA = tip area ratio, TL = tip lenght ratio (TA = 0,5TL). Empty squares are Stenodermatinae (Artibeus fimbriatus, A. lituratus, A. obscurus, Chiroderma doriae, C. villosum, Platyrrhinus recifinus, P. lineatus, Sturnira lilium, Uroderma magnirostrum, Vampyressa pusilla) the cross is Glossophaginae (Glossophaga soricina), full triangles are Phyllostominae (Micronycteris schmidtorum and Tonatia bidens), and full circles is Carolliinae (Carollia perspicillata). ! 63 ! ! Chiroptera Neotropical 19(3) Special Volume: 57-70, December 2013 contributing to the lowering of the WL, and acute Aerial insectivorous, carnivorous, and (long) wingtips. sanguivorous bats were distributed in the niche Medium-bodied bats were represented by five matrices based on the literature (tables 3 and 4). frugivorous bat species of the subfamily Glossophagines were distributed, without Stenodermatinae and by the frugivorous bat C. overlapping, in different weight classes in both perspicillata (Carolliinae). Carollia perspicillata matrices. In the foraging guilds/ensembles matrix had large S, as a result of the contribution of a suggested for the phyllostomid bat assemblages of large uropatagium, and its large and rounded PERD, I allocated the species to the guilds wingtips. In contrast, Chiroderma villosum, proposed by Kalko et al. (1996) and split Uroderma magnirostrum, Platyrrhinus lineatus, frugivorous bats in three ensembles based on the and P. recifinus had less rounded wingtips ranging present observations on the morphology of the from less to more acute. Sturnira lilium had higher wings and dietary diet from PERD (Tavares et al. WL than C. perspicillata, largely because it has a 2007) (table 4). reduced uropatagium, which lowers the wing Ensemble 1: Understorey frugivores that surface and increases the loading over the wings. consume Piperaceae, forage in forests, and have Tonatia bidens and C. perspicillata had developed broad wing surfaces and developed interfemoral interfemoral membranes, which contributed to the membrane, low WL and AR, and high TSI, with increment of the functional wing area just as in M. high maneuverability and swiftness to vertical schmidtorum, which may enable these species to movements. This ensemble had C. perspicillata as perform a slow, maneuverable flight and its only representative. elaborated vertical movements (Ulla M. Norberg, Ensemble 2: Frugivores that consume personal communication, Adams et al. 2012). The Cecropiaceae and Moraceae, forage in forest and uropatagium may also help to the performance of in the canopy, and have wings with high WL, quick changes of direction very useful in cluttered variable AR tending to low, and more pointed environments. Tonatia bidens had the shortest and wingtips with large areas. This group is formed by broadest wings of all phyllostomids analyzed, a eight species distributed in six weight classes pointed wingtip and a low WL. The flight of this (table 4): Artibeus fimbriatus, A. obscurus, A. species is highly maneuverable and very slow, and jamaicensis, Chiroderma doriae, C. villosum, the bat must be very agile owed to the Plathyrhinus recifinus, Uroderma magnirostrum, minimization of the inertia during the flight (lower and Vampyressa pusilla. TSI). The remaining medium-sized Ensemble 3: Frugivores that consume plants stenodermatines measured in this study had high distributed in open and forest habitats with WL and may flight slowly with maneuverability, flexible or broad diet (fruits), and have wings with and some limited abilities of hovering. Among high WL, intermediate AR, TSI close to 1 them P. recifinus seems to be the less capable to (approximately an equilateral triangle). This group hovering because of its shortened wingtip. is composed by Artibeus lituratus, Platyrrhinus The large frugivorous bats of the genus lineatus, and Sturnira lilium. Among Artibeus Artibeus had high WL and AR and broad wings. species, A. lituratus has a more rounded wing than The wingtip varied among Artibeus species: A. A. fimbriatus and A. obscurus, and higher WL and obscurus had the most rounded wingtip and A. AR, which can potentially increase its flight speed fimbriatus had the most pointed, and A. lituratus without losing maneuver abilities, characters that had an intermediate condition. may facilitate the use of a larger spectrum of Niche matrices microhabitats.
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Table 3: Niche matrix based on species average mass (g) and main diet, used to discriminate bat guilds from Rio Doce State Park, southeastern Brazil. Numbers are species/category. Classes of weight (g) Main diet 3 to 6 6 to 12 12 to 24 24 to 48 > 48 Insectivory 2 6 2 Nectarivory 1 1 1 Frugivory 1 4 4 3 Sanguivory 1 Carnivory* 2 Onivory 1 1 Table 4: Niche matrix based on foraging guilds, frugivorous bat ensembles, and body mass classes of bats from Rio Doce State Park, southeastern Brazil. Symbols for species are Ag: Anoura geoffroyi, Ac: Anoura caudifera, Af: Artibeus fimbriatus, Aj: Artibeus jamaicensis, Al: Artibeus lituratus, Ao: Artibeus obscurus, Ca: Chrotopterus auritus, Cp: Carollia perspicillata, Cd: Chiroderma doriae, Cv: Chiroderma villosum, Dr: Desmodus rotundus, Gs: Glossophaga soricina, Hv: Histiotus velatus, Mm: Macrophyllum macrophyllum, Mmo: Molossus molossus, Ms: Micronycteris schimdtorum, Ma: Myotis albescens, Mn: Myotis nigricans, Nl: Noctilio leporinus, Pl: Platyrrhinus lineatus, Pmcf: Peropteryx cf. macrotis Ph: Phyllostomus hastatus, Pr: Platyrrhinus recifinus, Sl: Sturnira lilium, Rn: Rhynchonycteris naso, Tb: Tonatia bidens, Tc: Trachops cirrhosus, Um: Uroderma magnirostrum, Vp: Vampyressa pusilla. Body mass classes (g) Foraging guilds < 6 6 to 12 12 to 24 24 to 48 > 48 1- Aerial insectivores/open areas Mmo Pm., Hv 2 - Aerial insectivores /edges, Mn, Rn Ma, Pm clearings, riparian areas 3 - Aerial insectivores /forested areas Hv 4 – Gleaning insectivores/ forested Mm, Ms Tc, Tb areas/understory 5 – Frugivorous Cp
Fruit bats ensemble 5.1: Forested areas/Understory frugivores/ Predominantly consumers of Piper
Fruit bats ensemble 5.2: Vp Pr, Um Ao, Cd, Af, Aj Forested areas/canopy/Predominantly Cv consumers of Moraceae and Cecropiaceae
Fruit bats ensemble 5.3: Sl Pl Al3 Flexible (vertical and interhabitat use)/ Oportunists in terms of diet
6- Piscivorous/forested areas Nl 7 - Sanguivorous/open and forested Dr areas 8 - Carnivorous/ forested areas Ca 9 - Nectarivorous/forested areas Ac Gs Ag 10 - Omnivorous/forested areas Ph 1 parameter such as mass is proportional to the cube Discussion of the linear dimension – 1:3 (Lawlor 1973, Analysis of wing morphology Norberg 1981). Correlations between wing area According to models of geometric similarity, and wingspan for phyllostomids and animals of different sizes have similar body stenodermatines closely fitted a geometric proportions, so that a bidimensional parameter similarity model with slopes of 0.46 and 0.47, such as area is proportional to the square of the respectively. Relationships between weight and linear dimension – 1:2 – and a volumetric wingspan for both groups analyzed also fitted well the geometric similarity expectations. Lawlor ! 65 ! ! Chiroptera Neotropical 19(3) Special Volume: 57-70, December 2013
(1973) drew similar conclusions on regressions of effects from opposite forces to lift. The flight of these parameters in his analysis of a set of 25 M. schmidtorum is probably slow and Neotropical bat species of four families, with maneuverable, including some hovering capacity diverse feeding habits. (sensu Rayner 1979), which is a similar flight I however found a deviation from the 2:3 pattern to the one described to the congeneric M. expected relationship between wing area (S) and megalotis (Norberg and Rayner 1987). body weight (M) for both group partitions Glossophaga soricina with its long and broad analyzed. According to my results, S increases wings is a bat with an excellent hovering ability, more than expected with body mass in and has the typical nectarivorous bat wings phyllostomids, and at a high rate (0.74 for all (Heithaus 1982, Lemke 1984, Norberg & Rayner phyllostomids, 0.75 for stenodermatines alone) 1987). Lengthier wing tips such as those of the contributing to the slow and maneuverable flight small fruit bat V. pusilla may contribute in the of these bats, even the large species. Interestingly, increment of agility, but this condition is generally Lawlor (1973) found a smaller than expected difficult to interpret isolately (Norberg & Rayner value for this relationship (slope of 0.59) and 1987). Among medium sized bats, the fruit bat C. concluded that small bats would have better ability perspicillata and the insect foliage-gleaning bat T. to deal with large wings in flight. However, he bidens have a set of characters suit to flying in analyzed a set of insectivorous bats of three cluttered spaces, including a large wing area (S), families (Molossidae, Phyllostomidae, and and a developed uropatagium. Carollia Emballonuridae) together with nectarivorous and perspicillata has also large wingtips, close to frugivorous bats (Phyllostomidae). Norberg values observed in G. soricina. High (1981) and Norberg and Rayner (1987) found a maneuverability and capacity of flying in dense less strong (β = 0.69) but positive deviation for the cluttered environments has been observed for C. relationship between wing area and body mass for perspicillata although flights tend to be short phyllostomid bats (including species of owed to low resistance (Heithaus & Fleming frugivorous, nectarivorous, partially and 1978). Having large wings may pose constraints to predominantly insectivorous, predominantly pursue insects inside the forest, and the foliage carnivorous, and sanguivores) and for a set of nine gleaning insect-feeding bat T. bidens has very stenodermatine bats. Large wings can increase the broad but short wings (low WSP and TL) with maneuverability of large bats, although acute tip (TSI<1) that may facilitate its flight in contributing for slowing their flight speed the clutter. Species of large fruit bats Artibeus (Norberg and Rayner 1987). The high increase in haver large, broad wings and a highly wing area in relation to body weight in strictly maneuverable, slow flight with some hovering frugivorous bats suggest that in large frugivorous abilities for A. lituratus and A. jamaicensis phyllostomids the burden of the load over the (Norberg & Rayner 1987, Morrison 1980 and wings is balanced by having larger wings than personal observations). expected for their size. Accordingly, WL increases Niche matrices less than expected with the increasing in mass Foraging behavior is a key point for units in the two groups of bats analyzed. The understanding the structure of tropical bat reduction in WL may play a role for the large ensembles and provides a more refined picture of frugivorous phyllostomids in allowing these them. Kalko (1997) proposed three parameters to species to carry extra load, such as fetuses and define bat guilds – diet, habitat, and foraging fruits from their sources to the feeding pools mode – and suggested the possibility of within- without compromising their ability to fly. guild splitting based on characters such as body AR is a constant in geometrically similar bats size, prey size, food choice, roosting sites, and (Norberg 1981), but there was a decrease in aspect temporal and spatial segregation. Whereas the ratio with the increase of weight of phylostomid trophic-size matrix (table 4) coarsely pooled in the frugivorous. Low values of aspect ratio represent same cells species with different diets and habitat shortened and broad wings, long and broad wings, preferences, the matrix including foraging or if narrow, very short wings. Broad wings are guilds/ensembles (table 5) amplified the number typical of frugivorous phyllostomid bats, which of potential niches available for bats. Foraging however present some variation in relative length guild categories for phyllostomid fruit bats due to wing tip size and shape. Increasing AR therefore summarize feeding preferences, wing decreases drag (Findley et al. 1972) and increases characters and flying mode. flight speed capacity as observed in molossid bats Small- and medium-bodied bats predominated (Norberg, 1994) with the cost of diminishing lift in the matrices, as expected for Neotropical and sustainability of flight. ensembles (Findley, 1993). In the foraging guilds Small bats have to cope with a smaller airfoil matrix incorporating additional ensembles (table surface but have the advantage of diminishing the 4), the absence of medium- and large-bodied
! 66 ! ! Chiroptera Neotropical 19(3) Special Volume: 57-70, December 2013 insectivores may be a sampling artifact (e.g., in able to fly in cluttered spaces (Norberg & Rayner the case of molossids not easily captured with 1987, this study) and has a strong preference for ground level mist-nets), but several cells, such as the Solanaceae (Marinho-Filho, 1991, Pedro & small- to medium-bodied piscivorous and Taddei 1997, Mello et al. 2008a, b). Within PERD carnivorous bats, and small- or large-bodied Solanaceae plants are frequently found in edges sanguivorous bats, will remain empty as there are and open habitats and in early succecional areas no such guilds represented within the bats of (Tavares et al. 2007), and so Solanaceae fruits are South America. All other categories will be filled relatively easy to find and catch. The architecture in with as more speciments are sampled in future of Cecropia plants does also not compromise their studies. In fact, I am aware that there are several accessibility to bats, and restrictions to consume new unpublished records of bat species from Cecropia by phyllostomids may be more strongly PERD (R. Gregorin, pers. comm.) including a related to foraging stratum selection (e.g. for recently described species (Velazco et al. 2014). understory bats, taller Cecropia are less likely to The wing morphology of bats of the genus be eaten), and to sensitivity of bat species (e.g., C. Carollia (frugivorous bat ensemble 1) have pachystachia is frequent everywhere so it may be similarities with that of phyllostomine consumed by a larger number of species, Tavares insectivorous bats that hunt in the understory, but 2007). Cecropia species are overall easy to be mixes conditions found in stenodermatine wings. accessed by consumers, having monopodial trunks Access of bats to forest Piper species is correlated of continuous growth, and ortogonal monopodial with their ability to flying in the understory, and branches (Bell 1991) and pendant or straight C. perspicillata has a set of flight abilities suited freely exposed fruits. for that. Like the phyllostomines, Carollia bats A next step to exploring niche matrices have broad wings and a developed interfemoral refinement is necessarily to expand the tests for membrane, forage mainly at ground level in the phyllostomid wing variation with a larger sample understory, may feed also on insects, but feed of data at hand (not only the bats captured in mainly on Piper in PERD and many other places PERD) in order to access the variances of wing (e.g., Fleming et al. 1977, Marinho-Filho 1991, parameters within species of phylostomids, and to Fleming 1991, Kalko et al. 1996, Pedro & Taddei include phylogeny as part of the equation. 1997, Mello et al. 2004, Tavares et al. 2007, Thies Phylogenetic correction may for instance reduce & Kalko 2004, Mello et al. 2011). the variance of the estimated regression Several species categorized in the frugivorous coefficients among traits (Rohlf 2006). bats ensemble category 2 have been considered Conclusions preferencial consumers of Moraceae fruits (e.g. Ecomorphology has ressurected in the 1990’s Kalko et al. 1996, Mello et al. 2011) or both as a tool to study the performance of organisms Moraceae and Cecropiaceae fruits (e.g. Fleming et and to understand the ecological and evolutionary al. 1977, Pedro & Taddei 1997, Tavares et al. consequences of design (Wainwright, 1994). 2007). Artibeus lituratus and A. jamaicensis have Flight is sensitive to microhabitat variation previously been considered canopy foragers (McKenzie & Rolfe, 1986) and plays a significant (Morrison 1980, Handley et al. 1991, Kalko et al. role in the ecofunctional segregation within bat 1996) and it is likely that A. fimbriatus may be guilds. Therefore, analyses of resource included in this category as suggested by the partitioning within Neotropical bat assemblages present data and data on feeding habits (Tavares et would benefit by encompassing both relationships al. 2007). The disposition of fig fruits can between feeding preferences, feeding apparatus sometimes compromise the efficiency of locating morphology, microhabitat selection, and them, but high frequency calls help locate locomotor apparatus morphology (see branches (Kalko & Condon 1998, Schnitzler & Hespenheide 1973). Kalko 1998) and olfaction seems to help locating figs inside clusters of plant parts and fruits (Kalko The fruit bat ensembles of PERD as here et al. 1996). Most fruit bats have also wing suggested would then be groups of species under morphologies that potentially enable them to make constrained ways of locomotion correlated with limited hovering movements that could help in similar wing morphology and other flight-related exploratory flights towards searching for fruits. characters (including weigth), similar feeding preferences, and similar constraints to habitat Artibeus lituratus, Platyrrhinus lineatus, and use/microhabitat selection. Sturnira lilium have either broad dietary spectra (fruits) or rely mostly on plants located in open Gianinni and Kalko (2004) found support for spaces, gaps or less cluttered areas in PERD and Fleming’s (1986) hypothesis of dietary elsewhere (e.g., Tavares et al. 2007, Mello et al. specialization among phytophagous phyllostomid 2008a, b). Sturnira lilium has no specialized wing bats as an evolved mechanism of coexistence. morphology to fly in the understory, although it is Studies of insect-eating bat ensembles have
! 67 ! ! Chiroptera Neotropical 19(3) Special Volume: 57-70, December 2013 pointed that flight behavior is correlated to species horseshoe bat species (Chiroptera: selection for microhabitat and diet (e.g. McKenzie Rhinolophidae). Journal of Mammalogy 87: & Rolfe, 1986, Aldrigde & Rauntenbach, 1986). I 1241-1251. suggest that constraints to bat flight and to the Dumont E.R. & Swartz S.M. 2009. Biomechanical local distribution of chiropterochoric plant species approaches and ecological research for the study in PERD play a role in shaping a bat’s food choice of bats. In: Ecological and behavioral methods in an ecological (proximate) context. Preferred for the study of bats (edited by Kunz T.H. and foraging stratum, diet, and microhabitat selection Parsons S.), pp. 257–300.The Johns Hopkins are related to energetic balance and optimal flight University Press, Baltimore, Md. performance of the bat and also to historical Fauth, J.E., Bernardo, J., Camara, M., Resetarits, (evolutionary) constraints to flight performance, W.J., Van Burskirk, J. & McColum, S.A. conferred by wing shape (e.g. Norberg and Rayner Simplifying the jargon of Community Ecology: 1987) and echolocation (Kalko et al. 1996). a conceptual approach. The American Acknowledgements Naturalist 147(2): 282-286. The present study was part of my Master’s Fenton M.B. 1972. The structure of aerial-feeding dissertation and was funded by the Brazilian bat faunas as indicated by ears and wing Research Council (CNPq). I was also funded by a elements. Canadian Journal of Zoology 50: 287- fellowship from the CAPES/PNPD program for 296. post-doctoral studies. I dedicate this work to Eli Findley J.S. 1993. Bats: a Community Perspective. Kalko with love and reverence. Cambridge University Press. References Findley J.S. & Wilson D.E. 1982. Ecological Adams R.A.; Snode E.R. & Shaw J.B. 2012. Significance of Chiropteran Morphology. In: Flapping tail membrane in bats produces Ecology of Bats (ed. Kunz, T.H.). Plenum Press, potentially important thrust during horizontal New York, USA. takeoffs and very slow flight. PLoS ONE 7: Findley J.S.; Studier E.H. & Wilson D.E. 1972. e32074. Morphologic properties of bat wings. Journal of Aldridge H.D.J.N. & Rautenbach I.L. 1986. Mammalogy 53:429-444. Morphology, echolocation and resource Fleming T.H. 1986. Opportunism versus partitioning in insectivorous bats. Journal of specialization: the evolution of feeding Animal Behavior 56: 763–778. strategies in frugivorous bats. In: Frugivores and Arita H.T. & Fenton M.B. 1997. Flight and seed dispersal (edited by Estrada, A. & Fleming, echolocation in the ecology and evolution of T.H.), pp. 105-118. Dr. Junk Publishers, bats. Trends in Ecology and Evolution 2: 53–58. Dordrecht, The Netherlands. Bagg∅e H.J. 1987. The Scandinavian bat fauna: Fleming T.H. 1991. The relationship between Adaptive wing morphology and free flight body size, diet, and habitat use in frugivorous behavior in the field. In: Recent Advances in the bats, genus Carollia (Phyllostomidae). Journal Study of Bats (edited by Fenton M.B.; Racey of Mammalogy 72: 493-501. P.A. & Rayner J.M.V.), pp. 57-74. Cambridge Fleming T.H.; Hooper E.T.& Wilson D.E. 1972. University Press, Cambridge. Three Central American bat communities: Bell A.D. 1991. Plant Form - An Illustrated Guide structure, reproductive cycles, and movement to Flowering Plant Morphology. Oxford patterns. Ecology 53: 555-569. University Press, Oxford, New York and Tokyo. Fleming T.H.; Heithaus E.R. & Sawyer W.B. 341 pp. 1977. An experimental analysis of food location Bogdanowicz W.; Csada R.D. & Fenton M.B. of frugivorous bats. Ecology 58: 619-627. 1997. Noseleaf structure, echolocation, and Giannini N.P. & Kalko E.K.V. 2004. Trophic foraging behavior in the Phyllostomidae Structure in a Large Assemblage of (Chiroptera). Journal of Mammalogy 78: 942- Phyllostomid Bats in Panama. Oikos 2: 209-220 953. Handley, C.O., Jr.; Gardner A.L. & Wilson D. E. Canals M.; Iriarte-Díaz J.; Olivares R. & Novoa 1991. Demography and Natural History of the F.F. 2001. Comparación de La morfología alar Common Fruit Bat, Artibeus jamaicensis, on de Tadarida brasiliensis (Chiroptera: Barro Colorado Island, Panamá. Smithsonian Molossidae) y Myotis chiloensis (Chiroptera: Contributions to Zoology 511. Smithsonian Vespertilionidae), representantes de dos Institution Press, Washington, D.C. diferentes patrones de vuelo. Revista Chilena de Heithaus E.R. 1982. Coevolution between bats Historia Natural 74: 699-704. and plants. In: Ecology of Bats (ed. Kunz, T.H.). Dietz C.; Dietz I. & Siemers B.M. 2006. Wing Plenum Press, New York, USA. measurement variations in the five European ! 68 ! ! Chiroptera Neotropical 19(3) Special Volume: 57-70, December 2013
Heithaus E.R. & Fleming T.H. 1978. Foraging reproductive patterns of the bat Carollia movements of a frugivorous bat, Carollia perspicillata (Phyllostomidae). Acta perspicillata (Phyllostomidae). Ecological Chiropterologica 6: 309-318. Monographs 48: 127-143. Mello M.A.R.; Silva W.R. & Kalko E.K.V. 2008a. Hespenheide, H.A. 1973. Ecological inferences Movements of the bat Sturnira lilium and its from morphological data. Annual Reviews in role as a seed disperser of Solanaceae in the Ecology and Systematics 4: 213-229. Brazilian Atlantic forest. Journal of Tropical Humphrey S.R.; Bonnacorso F.J. & Zinn T.L. Ecology 24: 225-228. 1983. Guild structure of surface-gleaning bats in Mello M.A.R.; Silva W.R. & Kalko E.K.V.2008b. Panama. Ecology 64: 284-294. Diet and abundance of the bat Sturnira lilium Hutchinson G.E. 1959. Homage to Santa Rosalia, (Chiroptera: Phyllostomidae) in a Brazilian or why are there so many kinds of animals? The Montane Atlantic Forest. Journal of American Naturalist 93: 145-161. Mammalogy 89: 485-492. Kalko E.K.V. 1997. Diversity in tropical bats. Mello M.A.R.; Marquitti F.M.D.; Guimarães Jr. Tropical diversity and systematics. Proceedings P.R.; Kalko E.K.V; Jordano P. & Aguiar of the International Symposium on Biodiversity M.A.M. 2011. The missing part of seed and Systematics in Tropical Ecossystems. Bonn, dispersal networks: structure and robustness of Germany. bat-fruit interactions. PLoS One 6: e17395. Kalko E.K.V. & Condon M.A. 1998. Morrison D.W. 1980. Foraging and day-roosting Echolocation, Olfaction and Fruit Display: How dynamics of canopy fruit bats in Panama. Bats Find Fruit of Flagellichorous Cucurbits. Journal of Mammalogy 61: 20-29. Functional Ecology 3: 364-372. Norberg U.M. 1976a. Kinematics, aerodynamics, Kalko E.K.V.; Handley Jr. C.O. & Handley D. and energetics of horizontal flapping flight in 1996. Organization, Diversity, and Long Term the log-eared bat Plecotus auritus. Journal of Dynamics of a Neotropical Bat Community. In: Experimental Biology 65: 179-212. Long-Term Studies of Vertebrate Communities Norberg U.M. 1976b. Aerodynamics of hovering (Cody M.L. & Smallwood J.A. eds.), pp. 503- flight in the long-eared bat Plecotus auritus. 552 Academic Press, Inc, San Diego and Journal of Experimental Biology 65: 459-470. London. Norberg U.M. 1976c. Some advanced flight Lawlor T. 1973. Aerodynamic characteristics of manoeuvres of bats. Journal of Experimental some neotropical bats. Journal of Mammalogy Biology 64: 489-495. 54: 71-78. Norberg U.M. 1981. Allometry of bat wings and Lemke T.O. 1984. Foraging ecology of the long- legs and comparison with bird wings. nosed bat, Glossophaga, with respect to Philosophical Transactionsof the Royal Society resource availability. Ecology 65: 538-548. of London B 292: 359-398. Lim B.K. & Engstrom M.D. 2001. Bat community Norberg U.M. 1987. Wing form and flight mode structure at Iwokrama Forest, Guyana. Journal in bats. In: Recent Advances in the Study of of Tropical Ecology 17: 647-665. Bats (edited by Fenton M.B.; Racey P.A. & Marinello, M.M. & Bernard, E. 2014. Wing Rayner J.M.V.), pp. 43-56. Cambridge morphology of Neotropical bats: a quantitative University Press, Cambridge. and qualitative analysis with implications for Norberg U.M. 1989. Ecological determinants of habitat use. Canadian Journal of Zoology 92(2): bat wing shape and echolocation-call structure 141-147. with implications for some fossil bats. In: Marinho-Filho J.S. 1991. The coexistence of two European Bat Research (Hanák V.; Horácèk I. frugivorous bat species and the phenology of & Gaisle J., eds.). pp. 197-211. Charles their food plants in Brazil. Journal of Tropical University Press, Prague. Ecology 7: 59-67. Norberg U.M. 1990. Vertebrate Flight. Springer, McKenzie N.L. & Rolfe J.K. 1986. Structure of Berlin. bat guilds in the Kimberly Mangroves, Norberg U.M. 1994. Wing design, Flight Australia. Journal of Animal Ecology 55: 401- Performance, and Habitat Use in Bats. In: 420. Ecological Morphology (Wainwright P.C. & McNab B.K. 1971. The structure of tropical bat Reilly S. M., eds.), pp. 205-239. The University faunas. Ecology 52: 352-358. of Chicago Press, Chicago and London. Mello M.A.R.; Schittini G.M.; Selig P. & Bergallo Norberg U.M. 2002. Structure, form, and function H.G. 2004. A test of the effects of climate and of flight in engineering and the living world. fruiting of Piper species (Piperaceae) on Journal of Morphology 252: 52–81.
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Norberg U.M. & Fenton M.B. 1988. Carnivorous Tavares V. da C.; Perini F.A. & Lombardi J.A. bats? Biological Journal of Linnean Society 33: 2007. The bat communities (Chiroptera) of the 383-394. Parque Estadual do Rio Doce, a continuous Norberg U.M. & Norberg R.Å. 2012. Scaling of remnant of Atlantic Forest in southeastern wingbeat frequency with body mass in bats and Brazil. Lundiana (UFMG) 8: 35 - 47. limits to maximum bat size. Journal of Thies, W. & Kalko E.K.V. 2004. Phenology of Experimental Biology 215: 711-722. Neotropical pepper plants (Piperaceae) and their Norberg U.M. & Rayner J.M.V. 1987. Ecological association with their main dispersers, two morphology and flight in bats (Mammalia: short-tailed fruit bats, Carollia perspicillata and Chiroptera): wing adaptations, flight C. castanea. Oikos 104: 362 - 376. performance, foraging strategy and Thollesson M. & Norberg U.M. 1991. Moments of echolocation. Philosophical Transactions of the inertia of bat wings and body. Journal of Royal Society of London B 316: 335-427. experimental Biology 158: 19-35. Pedro W.A. & Taddei V.A. 1997. Taxonomic Vaughan T.A. 1959. Functional morphology of assemblage of bats from Panga reserve, three bats: Eumops, Myotis, Macrotus. southeastern Brazil: abundance patterns and Publications of the University of Kansas trophic relations in the Phyllostomidae Museum of Natural History 12. 153 pp. (Chiroptera). Boletim do Museu de Biologia Velazco P.M.; Gregorin R.; Voss R.S. & Simmons Mello Leitão (Nova Série) 6: 3-21. N.B. 2014. Extraordinary local diversity of disk- Rayner J.M.V. 1979. A new approach to animal winged bats (Thyropteridae: Thyroptera) in flight mechanics. Journal of Experimental northeastern Peru, with the description of a new Biology 80: 17-54. species and comments on roosting behavior. Root, R.B. 1967. The niche exploitation pattern of American Museum Novitates 3795: 1-28. the blue-grey gnatcatcher. Ecol. Monogr. 37: Wainwright, P.C.; Reilly, S.M. 1994 (Eds). 317-350. Ecological morphology. Integrative organismal Ricklefs R.E. & Miles D.B. 1994. Ecological and biology: University of Chicago Press, Chicago, Evolutionary Inferences from Morphology: an Illinois, 368. Ecological Perspective. In: Ecological Willig M.R. 1986. Bat community structure in Morphology (Wainwright P.C. & Reilly S.M., South America: A tenacious chimera. Revista eds.), pp.13-41. The University of Chicago Chilena de Historia Natural 59:151-168. Press, Chicago and London. Schnitzler H-U. & Kalko E.K.V. 1998. How echolocating bats search and find food. In: Bat biology and conservation (Kunz T.H. & Racey P.A. eds.), pp. 183-196. Smithsonian Institution Press, Washington & London. Simmons N.B. 1995. Bat relationships and the origin of flight. Symposia of the Zoological Society of London 67: 27-43. Simmons N.B. & Geisler J.H. 1998. Phylogenetic relationships of Icaronycteris, Archaeonycteris, Hassianycteris, and Palaeochiropteryx, with comments on the evolution of the echolocation and foraging strategies in Microchiroptera. Bulletin of the American Museum of Natural History 235. 182 pp. Stallings J.R.; Fonseca G.A.B.; Pinto L.P.; Aguiar L.M.S. & Sábato E.L. 1990. Mamíferos do Parque Florestal do Rio Doce, Minas Gerais, Brasil. Revista Brasileira de Zoologia 7: 663- 677. Struhsaker T. 1961. Morphological factors regulating flight in bats. Journal of Mammalogy 42: 152-159. Tamsitt J.R. 1967. Niche and species diversity in Neotropical bats. Nature 213: 784-786.
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The potential function of individual signal frequency for masking avoidance in the greater bulldog bat Noctilio leporinus
Benjamin Feit1,2 *, Kirstin Übernickel1, Marco Tschapka1,3, Elisabeth K. V. Kalko1,3,†
1University of Ulm, Institute of Experimental Ecology, Albert-Einstein-Allee 11, 89069 Ulm, Germany 2University of Western Sydney, Hawkesbury Institute for the Environment, Locked Bag 1791, Penrith, NSW, 2751 Australia 3Smithsonian Tropical Research Institute, P.O. Box 0843-03092 Balboa, Ancón, Republic of Panamá
* Corresponding author: [email protected] † Deceased in 26 September 2011
ARTICLE Abstract. Bats using echolocation for orientation in space and for Manuscript history: foraging rely on the information provided by the echoes of their Submmited in 2/Oct/2013 emitted signals. In the presence of conspecifics, signals of Accepted in 22/May/2014 individuals may overlap in time and frequency and may impede the Available on line in 25/Aug/2014 bats’ ability to process their own echo information. It has been Editors: Marco A.R. Mello and Valéria C. Tavares proposed that bats may adjust their echolocation signal parameters to minimize the effects of signal overlap. We carried out a field study in Panama, and confronted free-flying greater bulldog bats Noctilio leporinus (Noctilionidae) with playbacks of conspecific search signals that matched the quasi-constant frequency (QCF) signal component of the bats’ expected echo. Additionally, we recorded echolocation signals of bats flying in pairs to compare the results of our playback experiments with bats encountering conspecifics under natural conditions. Noctilio leporinus did not shift the main frequency of its QCF components, neither when confronted with our playbacks nor in the presence of conspecifics. We discuss modifications of signal parameters and foraging behavior as strategies to avoid masking situations in N. leporinus.
Keywords: behavior, echolocation, field study, jamming, playback experiments, signal modification
! interval, intensity, or bandwidth) (Pye 1980; Introduction Obrist 1995; Schnitzler & Kalko 2001; Brinkløv et Most bat species use echolocation as an active al. 2010). sensory system for orientation and capture of prey In addition to masking effects caused by the in the dark. They depend largely on the environment, bats encounter even more complex information contained in the echoes of their perceptual tasks in the presence of conspecifics or signals for an adequate evaluation of their heterospecifics with a similar call structure, as environment (Schnitzler & Kalko 2001). Masking, echolocation signals and associated echoes of bats defined as an overlap between an echo and any flying in close proximity to each other might noise that obstructs the processing of information overlap in time and frequency, thus leading to (Schnitzler & Kalko 2001), may severely diminish masking effects or “jamming” (e.g. Ulanovsky et the information bats can obtain from their own al. 2004). signals’ echoes. Bats may experience diminishment or failure of processing echo Previous studies suggest that the general information when target echoes are overlapped by structure of a bat species’ echolocation signals signal emission (forward-masking effects) or by determines whether a bat needs to adjust its signal background clutter echoes (backward-masking parameters in order to avoid potential jamming effects) (Schnitzler & Kalko 2001; Schnitzler et al. situations. For bats using short frequency- 2003). As a reaction to occurring masking modulated (FM) signals it has been proposed that conditions, bats developed strategies to minimize they overcome jamming situations through masking by adjusting the structure of their changes in peak frequency (Obrist 1995; Ratcliffe echolocation signals (e.g., sound duration, pulse et al. 2004; Ulanovsky et al. 2007; Gillam et al.
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2007; Necknig & Zahn 2011), signal duration field, using standardized playback experiments (Obrist 1995; Gillam et al. 2007), or signal (Hartley et al. 1989; Surlykke & Moss 2000). bandwidth (Obrist 1995; Gillam et al. 2007). The Greater bulldog bat Noctilio leporinus Nevertheless, when and how exactly bats (Noctilionidae) emits variable combinations of change signal parameters to avoid jamming is not quasi-constant frequency (QCF) and QCF-FM yet fully understood. Variability among peak signals during search flight (Schnitzler et al. frequencies of signals is larger when bats are 1994). The search signals in the field are with up flying in the presence of conspecifics in to 142.7 dB sound pressure level (SPL) among the comparison to bats flying alone (e.g., Tadarida loudest recorded for bats (Surlykke & Kalko brasiliensis: Ratcliffe et al. 2004; Pipistrellus 2008) and thus highly likely to be perceived by pipistrellus and Pipistrellus nathusii: Necknig & bats flying nearby. Furthermore, natural flight Zahn 2011). In addition, masking avoidance has behavior of N. leporinus encompasses situations been described between sister species, i.e., P. where jamming may occur, e.g., multiple bats pipistrellus uses higher peak frequencies in the hunting under a dock light that attracted fish to the presence of P. nathusii than when recorded alone surface (A. Grinnell, pers. com.), and roost sharing (Necknig & Zahn 2011). In contrast, P. female N. leporinus have been observed to hunt in pipistrellus has also been found not to shift small groups (Brooke 1997). frequencies away from their call repertoire in We confronted free-flying N. leporinus with single flight during frontal encounter of playbacks of conspecific search calls. We conspecifics but to use shorter signals with higher hypothesized that masking is most likely to occur frequencies for precise localization and therefore when playback signals overlap with the frequency collision avoidance, similar to signal of the QCF component echoes expected by the modifications as a reaction to obstacles (S. Götze, bats. Therefore, we confronted individually flying pers. com.). In a controlled playback experiment, bats with playbacks that highly overlapped the Gillam et al. (2007) successfully provoked free- peak frequency of the QCF component of their flying FM bats (T. brasiliensis) to adjust their own echoes, and compared the signal parameters signals in order to increase differences in peak peak frequency and duration of the QCF and QCF- frequency by confronting them with pre-recorded FM signals, as well as the bandwidth of the entire echolocation signals with peak frequencies QCF-FM signals emitted before and during the matched to the flying bats’ signals. playback phase. In addition, we recorded In contrast to these heterogeneous findings echolocation sequences of two N. leporinus flying regarding FM bats, bats using echolocation signals together and compared the same parameters as in with dominant constant frequency (CF) the playback experiments. components did not shift frequency significantly Materials and Methods in the presence of conspecifics during laboratory studies (Asellia tridens (CF-FM): Jones et al. Experimental setup 1993; Rhinolophus ferrumequinum nippon (CF): The study was conducted from August to Furusawa et al. 2010). These findings for CF and November 2009 on Barro Colorado Island (BCI), CF-FM bats indicate that they encounter the same a field station of the Smithsonian Tropical complex perceptual tasks in the presence of Research Institute, Panama. We selected five sites conspecifics as FM bats, but in contrast to these on Gatun Lake at the shore of BCI and they seem not to reduce masking by shifting surrounding peninsulas (Bat cove, Bohio, Lab frequency of CF components. Nevertheless, cove, Miller cove, Poacher’s Point, and Wheeler experimental evidence for this assumption was cove; Fig. 1) to conduct our signal recordings and generated only in space-restricted environments playback experiments from a small motorboat. and information remains missing for natural The experiments started around sunset at 6 pm. situations. As the spatial confinements of the We conducted experiments until activity of the laboratory could diminish both the detectability bats decreased considerably after 11 pm and and the inclination of bats to show masking stopped during rain. avoidance behavior especially within the CF components, we addressed this question in the
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The loudspeaker and microphone were mounted on tripods approximately 40 cm above the water level. The microphone for recording the approaching bats was positioned about 10 to 20 cm to the left and about 10 cm behind the speaker to minimize potential overloading effects from the speaker on our recordings. Speaker and microphone were aligned parallel to the water surface and away from the closest shoreline. Visual documentation of passing bats was made with a thermal camera (VarioCAM, InfraTec GmbH, Dresden, Germany) mounted on a tripod at 1 m height above the water surface. For synchronization of the video recordings with the simultaneously recorded ultrasound files, we recorded additional real-time audio information of the bat signals via the heterodyning function of a bat detector (D230, Pettersson Electronic AB, Uppsala, Sweden). Visual information and synchronized low-frequency audio data were Figure 1: Sites selected for playback experiments with Noctilio leporinus around the shoreline of Barro stored on digital video (DV) tapes (Premium Mini Colorado Island and surrounding peninsulas. Playback DV 60, Sony, Tokyo, Japan) using a portable DV experiments were conducted at the five experimental recorder (Video Walkman GV-D1000E, Sony, sites, playback sequences originated from the three Tokyo, Japan). playback recording sites. BC = Bat cove; BO = Bohio; LC = Lab cove; PP = Poacher’s Point; WC = Wheeler Playback files preparation cove; B.C.N.M. = Barro Colorado Nature Monument; Playbacks were generated from bats recorded PB = playback. during search flight at three selected sites along the BCI shoreline (Bat cove, Lab cove, and Miller For all sound recordings we used a condenser cove; Fig. 1). We selected one recording per site microphone (CM16/CMPA, flat frequency that consisted of signals with a good signal-to- response between 25 - 150 kHz ( ± 3 dB), 6 dB noise ratio (energy of the signal at least 40 dB linear drop off < 25 kHz, approximate sensitivity: above background noise). Each of the three 50 mV/Pa, Avisoft-Bioacoustics, Berlin, selected sequences consisted of one pass, Germany) connected to a real-time recording characterized by an increase in amplitude of the system (UltraSoundGate 116Hm, version 3.4, recorded signals while the bat approached the Avisoft-Bioacoustics, Berlin, Germany) with a microphone, followed by a decrease in amplitude laptop (Toughbook® CF-30 series, Panasonic) when the bat departed. Passes consisted of nine to where data were stored as *.wav-files. The twelve consecutive QCF and QCF-FM signals sampling rate of all recordings was 300 kHz. emitted by singly flying bats. In view of the For sound analyses and manual signal Noctilio specific frequency range of 30 to 60 kHz modifications in the playback files we used in the first harmonic, we band-pass filtered the Avisoft SASLab Pro software (versions 4.50 and sequences outside the range of 20 to 70 kHz and 4.53, Avisoft-Bioacoustics, Berlin, Germany). The subsequently cleaned off manually all noise and modified playbacks were broadcasted using echoes that were no direct part of the signals, Avisoft Recorder software (NI-DAQmx, hard disc using Avisoft SASLab software. recorder, version 3.4, Avisoft-Bioacoustics, Field recordings of bats always have the Berlin, Germany) via a digital-analog interface artifact of frequency shifts caused by the Doppler card (6062E, National Instruments, Austin, Texas, shift phenomenon generated by the bat moving to USA) connected to an Ultrasonic Power Amplifier or away from the recording microphone (UltraSoundGate Player 116, Avisoft- (Schnitzler 1973; Gillam et al. 2007). To ensure a Bioacoustics, Berlin, Germany, frequency range ± consistent QCF frequency within each playback 1 dB: 1 - 180 kHz, slew rate: 8 V/µsec) with an sequence we removed the frequency shifts in the ultrasound speaker (Ultrasonic Dynamic Speaker recordings due to the bat’s flight movement. By ScanSpeak, Avisoft-Bioacoustics, Berlin, entering the desired frequency alteration in the Germany, frequency range ± 9 dB between 1 and frequency shift function in SASLab Pro we shifted 100 kHz with ± 4 dB between 50 and 60 kHz, the signal frequency of approaching and departing sensitivity at 50 kHz: 93 dB / 2.83 V / 1 m). periods up- or downwards, respectively, until the QCF components of all signals in one playback
! 73 ! ! Chiroptera Neotropical 19(3) Special Volume: 71-79, July 2014 file matched the frequency that was recorded when conservatively estimated target strength of the the bat was closest to the microphone. boat of -30 dB (Stilz & Schnitzler 2012), Preliminary recordings at our study sites maximum SPL of the returning echoes range revealed that the most common frequencies of between 68 dB at 2 m and 59 dB at 4 m distance QCF components emitted by N. leporinus ranged from the boat, respectively, and thus are well between 53 and 55 kHz. Bats in flight hear the under the intensity of our playbacks. echoes of their signals with an upward shift in Assuming a maximum sensitivity of the frequency that is proportional to their respective auditory system in N. leporinus in the frequency flight speed, due to the Doppler shift. As we were region of their QCF components with thresholds aiming to jam the peak frequency of the returning less than 5 dB (Wenstrup 1984), and an average echoes we created three variations of playback hearing threshold of 0-20 dB for bats (Kick 1982), sequences with mean peak frequencies of 54, 55 we are confident that all of our playbacks were and 56 kHz through shifting of the signals in loud enough to be perceived by N. leporinus at on- frequency from each original recording by using axis distances of 4 m or less. the frequency shift function of SASLab Pro. We Data selection thus generated nine versions from the three original recordings from three sites. All nine Based on spectrograms made in SASLab Pro sequences were used at all five experimental sites (see below) we selected sequences consisting to minimize possible bias in bat reactions caused exclusively of search signals emitted by N. by a specific original recording such as possible leporinus. We discarded all sequences where other individual recognition bias (Pfalzer & Kusch bat species were present and sequences where bats 2003, Siemers et al. 2005). clearly changed from search to approach and terminal phase signals (Schnitzler et al. 1994), Assessment of playback volume obviously concentrating on food. We focused our For our playback experiments it was essential analysis only on the part of the sequences during to assure that the bats were able to perceive the the bats’ approach to the microphone, using the playback sequences. To assess the sound intensity visual information provided by the thermal camera of the playback signals we broadcasted the 55 kHz and the increase in signal intensity in our version of all three playback files using the same recordings for selection. Thus, as all signals settings as for the playback experiments and experienced the same upward frequency shift, the recorded it with a calibrated ultrasonic Doppler shift phenomenon did not obscure microphone (1/4” prepolarized free-field potential peak frequency adjustments by the bats. microphone type 40BF, frequency response For analysis of the playback experiments we between 4 Hz - 100 kHz = ± 2 dB, G.R.A.S., excluded all sequences with two or more bats Denmark). We recorded on-axis at distances of 2 present and analyzed only recordings where the and 4 m from the speaker. For analysis we playback signals matched the bats’ expected echo removed from the recordings all signals outside frequency of the QCF component within the the range of 20-70 kHz by using a band pass filter maximum resolution of the spectrograms used and measured background noise and the recorded (293 Hz, see below). peak volumes of all QCF signals and components For an additional analysis of a potential of the broadcasted sequences in a one-dimensional masking avoidance when bats were confronted transformation window, using the root mean with a conspecific, we selected sequences where square function as described in the Avisoft two bats approached the microphone at the same SASLab Pro manual (version 4.53). The peak SPL time with no playbacks present. of the playback signals in our recordings averaged 80 dB at 2 m and 71 dB at 4 m distance to the Data analysis speaker; the intensity of background noise in the To examine our dataset for possible masking frequency band most important for N. leporinus avoidance behavior of N. leporinus in reaction to (54 to 57 kHz) averaged 44 dB SPL. either our playbacks or the presence of We are confident that the playbacks were loud conspecifics we measured peak frequencies and enough to mask the echoes of the bats’ signal duration of the QCF and QCF-FM signals echolocation signals reflected by the boat. Noctilio and bandwidth of the QCF-FM signals manually leporinus emits signals with a source level of the in spectrograms (Hamming window, 1024 Fast QCF component of up to 142.7 dB SPL (Surlykke Fourier Transformation (FFT), frame size 100 %, & Kalko 2008). Assuming an approximate temporal overlap 93.75 %, resulting in a temperature of 24.5°C and an approximate relative maximum frequency resolution of 293 Hz and a humidity of 95 % during our experiments, a maximum temporal resolution of 0.21 ms). spherical spreading loss of -6 dB per doubled In the playback experiments we compared the distance, an atmospheric attenuation of -1.6 dB means of signal parameters from three consecutive per m at 55 kHz (Griffin 1971), and a ! 74 ! ! Chiroptera Neotropical 19(3) Special Volume: 71-79, July 2014
signals emitted directly before the beginning of a sequence to analyze for differences in signal playback sequence (signals 1, 2, 3; Fig. 2) with the parameters between the passing bat and our respective means of three consecutive signals playbacks (all statistical analyses: level of emitted in the same pass during the playback significance p = 0.05, R version 2.13.0). sequence (signals 6, 7, 8; Fig. 2) to analyze Due to the small sample size of only four potential signal modifications as a reaction to our occasions of two bats flying together we could not playbacks. By excluding the first two signals perform statistical analyses of the differences in emitted during a playback sequence we took into call parameters for this situation. account the bat’s estimated reaction time of 50 – 70 ms at the beginning of a potential masking Results event (Schnitzler et al. 1994; Übernickel et al., Playback experiments 2013a). With mean signal durations of 13 ± 1.3 ms (SD) and interpulse intervals of 76.3 ± 38.2 ms We conducted recordings during 30 nights, resulting in a total of 383 audio files where we (SD) in high search flight (Schnitzler et al. 1994) attempted to confront passing N. leporinus with we are confident that exclusion of the first two our playbacks (191.5 min total recording time). In signals emitted during playback and analysis of 74 out of the 383 files we recorded passes of N. signals three, four, and five is adequate to detect leporinus during the replay of our playbacks. Our the possible reactions of bats to playbacks. Indeed, strict selection rules (see methods section) allowed Gillam et al. (2007) observed T. brasiliensis to eleven trials (nine trials with 55 kHz playbacks, shift the frequency of the first call less than 200 ms after a playback stimulus was presented. two trials with 56 kHz playbacks, no trial with 54 kHz playbacks) to enter subsequent analysis of the To analyze potential signal modifications in bats´ echolocation behavior. These files originated reaction to the presence of conspecifics we from three localities on non-successive recording compared the means of the signal parameters of nights (ten recordings from Lab cove, one six consecutive signals emitted by two bats recording from Bat cove, and one recording from approaching the microphone at the same time. Bohio). Timing and amplitudes of the individual signals allowed us to attribute the recorded signals to each We found no significant differences between mean peak frequencies of the QCF signals and of the individual bats. components, bandwidth or duration of signals Statistical analysis emitted by bats before and during the 55 kHz For statistical analysis of signal adjustments in playback sequences (MANOVA, Pillai’s trace = reaction to our playbacks we performed a 0.115, F3,14 = 0.531, P = 0.620; Tab. 1). Due to the MANOVA, using the experimental phases before low sample size of two trials, we could not playback and during playback as independent statistically analyze signal parameter categorical variables, and entered as dependent modifications as a reaction to the 56 kHz variables the mean values of peak frequency, playbacks but found only minute differences in bandwidth of the QCF-FM signals, and duration of peak frequency (x̅ = 0.2 ± 0.2 kHz), bandwidth (x̅ the signals emitted during the two experimental = 3.5 ± 1.3 kHz), and duration (x̅ = 1.3 ± 0.9 ms) phases in each trial. As a control we performed a of signals emitted before and during the replay of MANOVA, using the signals emitted during our playbacks (Tab. 1). playback and the signals of the applied playback
Table 1: Mean signal parameters (± 1 SD) of peak frequency, bandwidth, and duration of echolocation signals emitted by bats before and during the replay of playbacks and the associated playback sequences used to evoke masking. PB = playback sequences. n Peak frequency Bandwidth [kHz] Duration [ms] (passes) [kHz] Before PB 9 54.9 ± 0.2 29.8 ± 5.8 13.3 ± 2.4 During PB 9 54.9 ± 0.2 28.3 ± 5.3 12.0 ± 2.2 PB sequence 55.0 ± 0.0 15.0 ± 1.4 11.9 ± 0.7 Before PB 2 55.6 ± 0.1 31.3 ± 4.2 11.9 ± 0.9 During PB 2 55.8 ± 0.2 34.1 ± 0.9 9.6 ± 1.0 PB sequence 56.0 ± 0.0 15.0 ± 1.4 11.9 ± 0.7 1
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Figure 2: Example of a passing N. leporinus during playback onset with signals selected for parameter analysis marked. The bat emitted search calls during approach to the microphone (red); the playback (grey) was initiated during the pass at 0.35 s. The parameters of mean peak frequency, bandwidth, and duration of signals before playback (1, 2, 3) were compared with signals during playback (6, 7, 8). Signals number 4 and 5 have been excluded from the analysis to account for the bats’ reaction time.
The comparison of signals emitted by bats Bats flying in pairs emitted signals with only during a playback sequence with signals of the minute differences in peak frequency (x̅ = 0.2 ± applied playback sequence revealed a significant 0.1 kHz), bandwidth (x̅ = 2.2 ± 3.1 kHz), and difference in bandwidth (signals emitted during duration (x̅ = 1.4 ± 0.7 ms) (Tab. 2). Due to the playbacks: 28.3 ± 5.3 kHz, playback sequence small sample size of only four sequences we did signals: 15.0 ± 1.4 kHz, average bandwidth not statistically test these results. difference: 12.1 ± 1.2 kHz, p < 0.001, Tab. 1) but no difference in either peak frequency or duration (both p > 0.05, Tab. 1). Discussion We attempted to find masking avoidance Pairs of bats behaviour in N. leporinus in two different Individuals foraged at our study sites most of situations: free flying N. leporinus were the time alone, with the exception of a few confronted with playback sequences consisting of observations of multiple individuals foraging search signals matching the peak frequency of the briefly in close proximity to each other in the cove bats’ expected echoes and pairs of free flying bats closest to their roost (Bat cove) immediately after were recorded while approaching the microphone the emergence from their roost at sunset. Aiming together. In both cases we expected the bats to for sequences where only two bats were present at shift the peak frequency of the QCF signals or a time we had to discard all recordings of three or components to avoid masking by either our more bats flying simultaneously, resulting in only playbacks or the conspecific flying nearby. four sequences recorded in four different nights.
Table 2. Mean signal parameters (± 1 SD) of peak frequency, bandwidth, and duration of echolocation signals emitted by bats flying together.
Peak frequency Bandwidth n (signals) Duration [ms] [kHz] [kHz]
Bat 1 6 Pair 1 55.7 ± 0.4 33.4 ± 1.4 13.2 ± 0.2 Bat 2 6 56.0 ± 0.5 34.6 ± 0.5 10.8 ± 1.2 Bat 1 6 56.8 ± 0.2 33.5 ± 1.8 12.4 ± 0.1 Pair 2 Bat 2 6 56.3 ± 0.3 33.4 ± 1.9 13.3 ± 1.9 Bat 1 6 57.5 ± 0.4 34.3 ± 1.2 11.3 ± 0.2 Pair 3 Bat 2 6 57.5 ± 0.4 34.2 ± 1.6 12.2 ± 0.2 Bat 1 6 58.0 ± 0.2 34.4 ± 1.0 12.7 ± 0.1 Pair 4 Bat 2 6 58.1 ± 0.3 26.8 ± 8.1 11.4 ± 0.1 1 ! 76 ! ! Chiroptera Neotropical 19(3) Special Volume: 71-79, July 2014
Contrary to our expectations, neither the We cannot exclude that the small sample size confrontation with our playbacks nor the presence may have reduced the probability of observing of a conspecific led to significant alterations in distinct reactions towards our playbacks or the peak frequency, duration or bandwidth. However, presence of conspecifics. Nevertheless, our strict the bandwidth of the signals in our playbacks did criteria for selecting sequences were necessary to not match the bandwidth of the signals emitted by exclude the possibility that influences other than bats approaching the microphone. This was the our playbacks could have triggered signal result of our playbacks originating from modifications. Other strategies to avoid masking echolocation signals emitted by bats flying parallel by conspecifics may still occur. to the boat with no obstacle being in the center of One strategy to minimize chances of masking attention of the bats’ echolocation while bats in the presence of conspecifics could be the during the experiments were approaching the boat. development of specific individual peak Thus, the broader bandwidth is likely to be an frequencies as found in A. tridens. Here, potential adjustment for the approach to the obstacle as the signal masking during group flights is minimized accuracy of range determination increases with with peak frequencies ranging from 115 to 119 bandwidth (Schnitzler & Kalko, 2001). These kHz that depend on sex, age and size (Jones et al. differences could have provided N. leporinus with 1993). We recorded N. leporinus emitting QCF sufficient information to discriminate between its frequencies ranging from 51.2 to 60.3 kHz, while own signals and our playbacks and thus may have Doppler shift within a single pass of an individual reduced the occurrence of masking. However, bat did not exceed differences of 2 kHz between since we found also no differences in signal minimum and maximum frequencies. bandwidth when two bats flew together, Furthermore, a study on N. leporinus in Costa bandwidth similarity seems not to be a factor Rica reported QCF frequencies covering 52 to 56 triggering any masking avoidance response under kHz (Schnitzler et al. 1994). Hence, both results natural conditions. may promote the individual frequency hypothesis. An especially interesting result was that the Contrary to this hypothesis we found pairs of average difference in peak frequency of the QCF bats flying together to emit QCF signals and signals and components between bats flying in components with a similar peak frequency in all actual pairs was only 0.2 kHz and thus matched four analyzed sequences (Tab. 2). However, the the non-significant difference in peak frequency small sample size and the wide range of peak for bats confronted with our playbacks. In frequencies we found in recordings of singly contrast, earlier studies on free-flying FM bat flying bats in combination with the strategy of species reported peak frequency shifts in the foraging either solitary or in only small groups magnitude of 0.5 kHz in T. brasiliensis (Ratcliffe (Brooke 1997) support the assumption that et al. 2004), 1.2 kHz in T. teniotis (Ulanovsky et individual peak frequencies could be an effective al. 2004) and 1.7 kHz in P. pipistrellus (Necknig strategy to reduce the probability of masking & Zahn 2011) when confronted with nearby through signals of conspecifics. conspecifics. This suggests that N. leporinus does A second explanation why the bats did not not employ peak frequency shifts to avoid alter their peak frequency even in the presence of masking when encountering conspecific conspecifics or when confronted with our echolocation signals. playbacks could lie within their hearing We are confident that the bats were able to capabilities. Experimental evidence of frequency perceive our playbacks as all experiments were modifications as a reaction towards the presence conducted with a loudspeaker highly efficient in of conspecifics came from bats using FM signals the frequency range of the echolocation calls of N. such T. brasiliensis, which have a rather broad leporinus (for details see methods section). As we area of best hearing covering ca. 6 kHz (Vater & can assume a hearing threshold of 0-20 dB for N. Siefer 1995). Consequently, these bats may be leporinus in the field (Kick 1982) and as the SPL able to shift their peak energy without diminishing of our playbacks were 59 dB or higher at distances their ability to process relevant information. of up to 4 m in front of the loudspeaker (see However, audiograms of N. leporinus revealed assessment of playback volume section), we are maximum sensitivity within the frequency region confident that the playbacks were loud enough to of the QCF component covering only 2-3 kHz and be perceived by passing N. leporinus. This a sharp decrease in sensitivity in frequencies assumption was corroborated by our observation above that region (Wenstrup 1984). Furthermore, that most of the N. leporinus reacted towards the it seems that N. leporinus modulates its QCF playbacks by approaching the boat with the frequency in order to compensate for motion- playback speaker, often circling one or several induced Doppler shift (Wenstrup & Suthers 1984). times near the loudspeaker as described in This is likely to provide the bat with maximum Übernickel et al. (2013b). information content of their surroundings which
! 77 ! ! Chiroptera Neotropical 19(3) Special Volume: 71-79, July 2014 may be diminished if the bat alters the peak Kick S.A. 1982. Target-detection by the frequency of the QCF component to a frequency echolocating bat, Eptesicus fuscus. Journal of outside the area of maximum sensitivity Comparative Physiology A 145(4):431-435. (Schnitzler & Kalko 2001). Hence, it seems that Necknig V. & Zahn A. 2011. Between-species N. leporinus primarily uses the available jamming avoidance in Pipistrelles? Journal of frequency range limited by its hearing capacities Comparative Physiology A 197:469-473. to focus on constant echo frequency, and that Obrist M. 1995. Flexible bat echolocation: the occasional masking avoidance may be performed influence of individual, habitat and conspecifics by another strategy. on sonar signal design. Behavioral Ecology Acknowledgements Sociobiology 36:207-219. We would like to thank the Smithsonian Pfalzer G. & Kusch J. 2003. Structure and Tropical Research Institute, in particular the staff variability of bat social calls: implications for of the research station on BCI and the whole BCI specificity and individual recognition. Journal of BatLab team for help and assistance, Sebastian Zoology 261:21–33. Zschunke for technical support and Raimund Pye D. 1980. Adaptiveness of echolocation signals Specht from Avisoft for helpful advice on soft- in bats: Flexibility in behaviour and in and hardware. We are also grateful to Cristina evolution. Trends in Neuroscience 1:232-235. Urrutia and Maria Eckenweber for field assistance Ratcliffe J.M., Hofstede H.M., Avila-Flores R., and to Hans-Ulrich Schnitzler and Alan Grinnell Fenton M.B., McCracken G.F., Biscardi S., and two anonymous reviewers for helpful Blasko J., Gillam E., Orprecio J. & Spanjer G. comments on earlier drafts. We further thank the 2004. Conspecifics influence call design in the Smithsonian Tropical Research Institute and the Brazilian free-tailed bat, Tadarida brasiliensis. EU-funded ChiRoPing-Project (IST contract Canadian Journal of Zoology 82(6):966-971. number 215370) for financial support of this study. Schnitzler H.U. 1973. Control of Doppler shift compensation in the greater horseshoe bat, References Rhinolophus ferrumequinum. Journal of Brinkløv S., Kalko E.K.V. & Surlykke A. 2010a. Comparative Physiology A 82(1):79-92. Intensity of biosonar calls is adjusted to habitat Schnitzler H.U., Kalko E.K.V., Kaipf I. & clutter in the trawling bat Macrophyllum Grinnell A.D. 1994. Fishing and echolocation macrophyllum (Phyllostomidae). Behavioral behavior of the greater bulldog bat, Noctilio Ecology and Sociobiology 64:1867-1874. leporinus, in the field. Behavioral Ecology and Brooke, A. P. 1997. Social organization and Sociobiology 35:327-345. foraging behaviour of the fishing bat, Noctilio Schnitzler, H.U. & Kalko E.K.V. 2001. leporinus (Chiroptera: Noctilionidae). Ethology Echolocation by insect-eating bats. BioScience 103(5):421-436. 51(7): 557-569. Furusawa Y., Hiryu S. & Riquimaroux H. 2010. Schnitzler H.U., Moss C.F. & Denzinger A. 2003. Paradoxical reference frequency shifts during From spatial orientation to food acquisition in paired flights in Japanese horseshoe bats echolocating bats. Trends in Ecology and evaluated with a Telemike. Abstract published Evolution 18(8):386-394. in Journal of the Acoustical Society of America Siemers B. M., Beedholm K., Dietz C., Dietz I., & 127(3):1971-1971. Ivanova T. 2005. Is species identity, sex, age or Gillam E.H., Ulanovsky N. & McCracken G.F. individual quality conveyed by echolocation call 2007. Rapid jamming avoidance in biosonar. frequency in European horseshoe bats? Acta Proceedings of the Royal Society B 274:651- Chiropterologica 7(2), 259-274. 660. Stilz W.P. & Schnitzler H.U. 2012. Estimation of Griffin D.R. 1971. The importance for the acoustic range of bat echolocation for atmospheric attenuation for the echolocation of extended targets. Journal of the Acoustical bats (Chiroptera). Animal Behavior 19:55-61. Society of America 132:1765-1775. Hartley D.J., Campbell K. & Suthers R. 1989. The Surlykke A. & Kalko E.K.V. 2008. Echolocating acoustic behavior of the fish catching bat, bats cry out loud to detect their prey. PLoS One Noctilio leporinus, during prey capture. Journal 3(4):e2036(1-10). of the Acoustical Society of America 86:8-27. Surlykke A. & Moss C.F. 2000. Echolocation Jones G., Morton M., Hughes P.M. & Budden behavior of big brown bats, Eptesicus fuscus, in R.M. 1993. Echolocation, flight morphology the field and the laboratory. Journal of the and foraging strategies of some West African Acoustical Society of America 108(5):2419- hipposiderid bats. Journal of Zoology 2429. 230(3):385-400.
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Übernickel K., Tschapka M. & Kalko E.K.V. 2013a. Selective Eavesdropping Behaviour in Three Neotropical Bat Species. Ethology 119:66–76. Übernickel K., Tschapka M. & Kalko E.K.V. 2013b. Flexible echolocation behavior of trawling bats during approach of continuous or transient prey cues. Frontiers in Physiology 4. Ulanovsky N., Fenton M.B., Tsoar A. & Korine C. 2004. Dynamics of jamming avoidance in echolocating bats. Proceedings of the Royal Society B 271:1467-1475. Vater M. & Siefer W. 1995. The cochlea of Tadarida brasiliensis: specialized functional organization in a generalized bat. Hearing Research 91:178-195. Wenstrup J.J. 1984. Auditory sensitivity in the fish-catching bat, Noctilio leporinus. Journal of Comparative Physiology A 155(1):91-101. Wenstrup J.J. & Suthers R.A. 1984. Echolocation of moving targets by the fish-catching bat, Noctilio leporinus. Journal of Comparative Physiology A 155(1):75-89.
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