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Uso de tiendas de hojas por Artibeus y Uroderma (Chiroptera, Phyllostomidae) en el norte de Colombia.

TENT USE BY Artibeus AND Uroderma (CHIROPTERA, PHYLLOSTOMIDAE) IN NORTHERN COLOMBIA

Four out of the nine Neotropical bat families have species that use foliage as day roosts (Kunz & Lumsden 2003). Among foliage-roosting species, phyllostomid bats of subfamilies Rhinophyllinae and Stenodermatinae are the only Neotropical bats known to use modified leaves as shelters, which are commonly known as "leaf tents" (Chapman 1932). The first reports of leaf tents used by bats came from Panama, and most subsequent studies on tent-roosting bats were made in Central America and Trinidad (Barbour 1932; Kunz et al. 1994; Rodriguez-Herrera et al. 2007). Additional records of tent-roosting bat species have been made in Brazil, Colombia, Ecuador, French Guiana, and Peru (Koepcke 1984; Timm 1987; Charles-Dominique 1993; Zortea 1995; Herrera-Victoria et al. 2018), and currently 20 species of stenodermatine and rhinophylline bats are known to use tents (Garbino & Tavares 2018). However, most of the studies on tent-using bats in South America are based on occasional encounters and provide but a few details on group size, tent architecture and plant species used by the bats.

Aiming to contribute with basic information on tent-roosting bats in northern South America, we describe leaf tents used by Uroderma convexum and Artibeus jamaicensis in an area of northern Colombia, and comment on group size and composition.

We searched for bats roosting under modified and unmodified leaves along 6.6 kilometers of pre-existing tourist trails in Parque Nacional Natural Tayrona, Magdalena, Colombia (11[degrees]18' N, 53[degrees]57' W) on 3 August 2017 (Fig. S1). In most cases, reliable identification of the bats and the plants used as shelter was possible. All visits to roosts were made during daytime, between 11:00 and 15:00 h. We observed and photographed the bats, which could be identified at least to subtribe level.

A total of 13 occupied diurnal roosts of stenodermatine bats were recorded along the transect (Table 1). Among them, 10 were tents, one consisted of unmodified foliage, and in two cases we could not determine whether the leaf was modified. Roosts were recorded in two species of palms, Sabal mauritiiformis (locally known as "palma amarga") and coconut palms (Cocos nucifera). Following the tent architecture classification of Kunz et al. (1994), the type observed on S. mauritiiformis leaves was most similar to the "umbrella" tent (Fig. S2), and the modified coconut palm leaves matched the "pinnate" tent type. The architecture of the umbrella tents made of S. mauritiiformis leaves matched what has been described in the literature, as the leaves were chewed on veins and plications were made in a semicircular or polygonal pattern, causing the distal parts of the leaf to hang down (Kunz et al. 1994; Timm 1987). The pinnate tents are constructed by biting the midrib of the palm leaf's leaflets, which fold downward (Timm & Lewis 1991). On the two pinnate tents we found, architecture matched that described in previous studies (Timm & Lewis 1991; Garcia-Garcia & Santos-Moreno 2014), with the leaflets closer to the coconut palm trunk cut at greatest distance from the rachis.

We identified the species U. convexum and A. jamaicensis using the tents. Characters used to determine the species U. convexum included the distinct white stripe crossing the dorsum medially, and not reaching the nape and crown, the bicolored nose leaf with the lateral portions of the horseshoe pale-colored, and the anterodorsal margins of the ear white colored (Figs. 1A, S3-6). Although the external characters used to recognize the species U. convexum largely overlap with those defining U. bilobatum, we followed Mantilla-Meluk (2014) considering that only U. convexum is found in northern Colombia. We based our identification of a single individual of A. jamaicensis that we found in a tent roost in its large size, in the presence of a self-colored nose leaf, its grayish pelage, and not well-marked white stripes, and in the lack of a dorsal stripe (Fig. 1B).

A third recorded species could not be recognized by observation and is treated here as "unindentified Vampyressina" (Fig. S7). This single animal had a bicolored noseleaf, yellowish lateral borders of the horseshoe, and had a white stripe along the dorsum that did not reach the nape and crown. Based on these characters, the bat could be a species of Chiroderma, Vampyriscus or Uroderma. On one tent with two bats and one with at least five, the bats left the tents before they could be photographed.

The single individual of Artibeus jamaicensis was found roosting in a Sabal mauritiiformis umbrella tent (Fig. 1B). This species is opportunistic in its selection of roosts, and may shelter in rock crevices, tree hollows and foliage (Morrison & Handley 1991). Some authors even suggest that it uses tents made by other species (Brooke 1987; Rodriguez-Herrera et al. 2007). Tent-use by A. jamaicensis has been previously recorded in Costa Rica (Foster & Timm 1976), on the island of Trinidad (Kunz & McCracken 1996), and in western Colombia (Herrera-Victoria et al. 2018).

We observed nine groups of Uroderma convexum with group size ranging from 1 to at least 23 individuals, and more than half of the roosts (5 out of 9) containing pairs (Table 1). In the colonies containing more than 2 animals, it was possible to identify the presence of small juveniles. We found roosting groups of Uroderma convexum in coconut palm leaves in three occasions, and in three different trees (Fig. S8). In one palm tree, we found a large colony containing at least 15 U. convexum adults under a pinnate tent (Fig. 2A), and two other groups with two bats each in other leaves. Our observations in coconut palm leaves agree with the findings of Timm & Lewis (1991), as the smallest groups of U. convexum were found in unaltered leaves, and the large group was under an altered leaf (Table 1).

Uroderma convexum has been previously recorded using umbrella tents in Costa Rica (Timm 1987), Panama (Barbour 1932), and western Colombia (Herrera-Victoria et al. 2018). Previous records of U. convexum using pinnate tents were made in Costa Rica, in tents made of Cocos nucifera and Attalea butyracea leaves (Timm & Lewis 1991; Timm & McClearn 2007), and in Mexico, in A. butyracea leaves (Garcia-Garcia & Santos-Moreno 2014).

Published studies indicate that males of Uroderma convexum and Artibeus jamaicensis form harems (Timm & Lewis 1991; Kunz & McCracken 1996), which appears to be the case at least for U. convexum according to our data. We observed females with their young in two of the tents of S. mauritiiformis (Figs. 1, S3-6), and in both cases a single individual roosting separately from the rest, which could probably be the adult male from the harem. Similar to our observations made in August, Timm & Lewis (1991) observed juveniles with the females in July in Costa Rica, and Fleming (1973) also reported a birth peak between July and August in Panama.

A single tent in an individual of Sabal mauritiiformis was occupied simultaneously by one individual of U. convexum, and by one nocturnal gecko of the species Thecadactylus rapicauda that we found adhered to the leaf's petiole (Figs. 2B, S9). In the seasonal dry forests of Caribbean Colombia, T. rapicauda is more commonly found on the lower forest levels (< 2.5 m high), although it has been recorded in trees of more than 30 m in the Amazonia (Vitt & Zani 1997; Rojas Murcia et al. 2016). This species is also known to use a wide variety of shelters, including tree trunks, branches and limbs, leaves of trees and bromeliads, and even human buildings (Vitt & Zani 1997). Therefore, this single observation of the two species sharing the same roost precludes from making further statements about eventual associations between the bat and gecko species. However, the fact that the gecko shares the same tent with the bat is noteworthy because T. rapicauda is preyed by carnivorous bats, such as Chrotopterus auritus and Trachops cirrhosus (Goodwin & Greenhall 1961; Tuttle 1967), and raises questions to whether there are any sort of recognition clues signaling the harmlessness of that particular bat to the gecko.

Considering that the diurnal roosts were found with relative ease, and many tents were observed along the transect but not personally verified by us, we assume that this region has great potential for studies of the dynamics of tent-roosting by bats.

https://doi.org/10.31687/saremMN.18.25.2.0.08

Acknowledgements. We are grateful to Henrique C. Costa for identifying the Thecadactylus species and to Raone Beltrao-Mendes for the discussion on the subject of this paper. Associate Editor Maria Sandoval and an anonymous reviewer provided very valuable suggestions on the manuscript. All authors were supported by the Brazilian Federal Agency for Support and Evaluation of Graduate Education (CAPES).

LITERATURE CITED

Barbour, T. 1932. A peculiar roosting habit of bats. The Quaterly Review of Biology 7:307-312.

Brooke, A. P. 1987. Tent construction and social organization in Vampyressa nymphaea (Chiroptera: Phyllostomidae) in Costa Rica. Journal of Tropical Ecology 3:171-175.

Chapman, F. M. 1932. A home-making bat. Natural History 32:555-556.

Charles-Dominique, P. 1993. Tent-use by the bat Rhinophylla pumilio (Phyllostomidae: Carolliinae) in French Guiana. Biotropica 25:111-116.

Fleming, T. H. 1973. The reproductive cycles of three species of opossums and other mammals in the Panama Canal Zone. Journal of Mammalogy 54:439-455.

Foster, M. S., & R. M. Timm. 1976. Tent-making by Artibeus jamaicensis (Chiroptera: Phyllostomatidae) with comments on plants used by bats for tents. Biotropica 8:265-269.

Garbino, G. S. T., & V. C. Tavares. 2018. Roosting ecology of Stenodermatinae bats (Phyllostomidae): evolution of foliage roosting and correlated phenotypes. Mammal Review 48:75-89.

Garcia-Garcia, J. L., & A. Santos-Moreno. 2014. Uso de la palma Attalea butyracea como tienda de percha por el murcielago Uroderma bilobatum en Oaxaca, Mexico. Acta Zoologica Mexicana 30:434-438.

Goodwin, G. G., & A. M. Greenhall. 1961. A review of the bats of Trinidad and Tobago. Bulletin of the American Museum of Natural History 122:187-301.

Herrera-Victoria, A. M., M. Zuluaga-Egas, V. Rojas-Diaz, L. A. Valenzuela, & G. H. Kattan. 2018. The dynamics of tent-roosts in the palm Sabal mauritiiformis and their use by bats in a montane dry forest. Biotropica 50:282-289.

Koepcke, J. 1984. "Blattzelte" als schlafplatze der Fledermaus Ectophylla macconnelli (Thomas, 1901) (Phyllostomidae) im tropischen regenwald von Peru. Saugetierkundliche Mitteilungen 31:123-126.

Kunz, T. H., M. S. Fujita, A. P. Brooke, & G. F. McCracken. 1994. Convergence in tent architecture and tent-making behavior among neotropical and paleotropical bats. Journal of Mammalian Evolution 2:57-78.

Kunz, T. H., & L. F. Lumsden. 2003. Ecology of cavity and foliage roosting bats. Bat ecology (T. H. Kunz & M. B. Fenton, eds.). University of Chicago Press, Chicago, IL.

Kunz, T. H., & G. F. McCracken. 1996. Tents and harems: apparent defence of foliage roosts by tent-making bats. Journal of Tropical Ecology 12:121-137.

Mantilla-Meluk, H. 2014. Defining species and species boundaries in Uroderma (Chiroptera: Phyllostomidae) with a description of a new species. Occasional Papers, Museum of Texas Tech University 325:1-25.

Rodriguez-Herrera, B., R. A. Medellin, & R. M. Timm. 2007. Murcielagos neotropicales que acampan en hojas. Editorial INBio, Santo Domingo.

Rojas Murcia, L. E., J. E. Carvajal Cogollo, & J. A. Cabrejo Bello. 2016. Reptiles del bosque seco estacional en el Caribe colombiano: distribucion de los habitats y del recurso alimentario. Acta Biologica Colombiana 21:365-377.

Timm, R. M. 1987. Tent construction by bats of the genera Artibeus and Uroderma. Fieldiana Zoology, New Series 39:187-212.

Timm, R. M., & S. E. Lewis. 1991. Tent construction and use by Uroderma bilobatum in coconut palms (Cocos nucifera) in Costa Rica. Bulletin of the American Museum of Natural History 206:251-260.

Timm, R. M., & D. K. McClearn. 2007. The bat fauna of Costa Rica's Reserva Natural Absoluta Cabo Blanco and its implications for bat conservation. Quintessential Naturalist: Honoring Life and Legacy of Oliver P. Pearson 134:303-352.

Tuttle, M. D. 1967. Predation by Chrotopterus auritus on geckos. Journal of Mammalogy 48:319.

Vitt, L. J., & P. A. Zani. 2018. Ecology of the nocturnal lizard Thecadactylus rapicauda (Sauria: Gekkonidae) in the Amazon region. Herpetologica 53:165-179.

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SUPPLEMENTARY ONLINE MATERIAL

Supplement 1

https://www.sarem.org.ar/wp-content/uploads/2018/09/SAREM_MastNeotrop_25-2_Garbino-sup1.pdf

Fig. S1. Study site at Parque Nacional Natural Tayrona, Magdalena, Colombia. The red track represents the walked transect.

Fig. S2. A) Sabal mauritiiformis palm with a leaf modified into "umbrella" tent (white arrow), B) detail of tent shown in (A).

Fig. S3. Three adult females of Uroderma convexum with juveniles, roosting in a Sabal mauritiiformis tent.

Fig. S4. Two individuals of Uroderma convexum roosting in a Sabal mauritiiformis tent.

Fig. S5. Two individuals of Uroderma convexum roosting under an unmodified coconut palm leaf.

Fig. S6. Two individuals of Uroderma convexum roosting under an unmodified coconut palm leaf.

Fig. S7. Unidentified individual of Vampyressina in a Sabal mauritiiformis tent.

Fig. S8. A) Coconut palms (Cocos nucifera) where groups of Uroderma convexum were observed --the tree palms on the front had bats. The white arrow signals the group in (B). B) Group of U. convexum roosting under a pinnate tent.

Fig. S9. Close up of A) Thecadactylus rapicauda and B) Uroderma convexum in the same Sabal mauritiiformis tent.

Guilherme S. T. Garbino (1), Gabriela C. Rezende (2,3) and Valeria da Cunha Tavares (4,5)

(1) Pos-graduacao em Zoologia, Dept. de Zoologia, Instituto de Ciencias Biologicas, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Brazil. [Correspondence: <gstgarbino@hotmail.com>]

(2) Pos-graduacao em Zoologia, Dept. de Zoologia, Instituto de Biociencias, Universidade Estadual Paulista (UNESP), Rio Claro, Brazil.

(3) IPE--Instituto de Pesquisas Ecologicas, Nazare Paulista, Brazil.

(4) Departamento de Zoologia, Instituto de Ciencias Biologicas, Universidade Federal de Minas Gerais (UFMG), Belo Horizonte, Brazil.

(5) Departamento de Ciencias Biologicas, Universidade Estadual de Minas Gerais (UEMG), Ibirite, Brazil.

Caption: Fig. 1. A) Group of Uroderma convexum roosting under the modified Sabal mauritiformis leaf depicted in Fig. S2; B) Artibeus jamaicensis roosting under S. mauritiiformis "umbrella" leaf tent.

Caption: Fig. 2. A) Group of Uroderma convexum roosting under a Cocos nucifera leaf modified into a pinnate tent, B) Sabal mauritiiformis umbrella tent shared by Uroderma convexum and Thecadactylus rapicauda.
Table 1
Bat species, group size, plant species, and type of tents recorded.

Bat species                                  Group size

Artibeus jamaicensis                           1 adult
Uroderma convexum                             2 adults
Uroderma convexum                at least 15 adults and 8 juveniles
Uroderma convexum                             2 adults
Uroderma convexum                             2 adults
Uroderma convexum                             2 adults
Uroderma convexum                       4 adults, 3 juveniles
Uroderma convexum                      15 adults, 8 juveniles
Uroderma convexum                             2 adults
Uroderma convexum                              1 adult
Unindentified Stenodermatinae                 2 adults
Unindentified Stenodermatinae             at least 5 adults
Unindentified Vampyressina                     1 adult

Bat species                         Plant species

Artibeus jamaicensis             Sabal mauritiiformis
Uroderma convexum                   Cocos nucifera
Uroderma convexum                   Cocos nucifera
Uroderma convexum                   Cocos nucifera
Uroderma convexum                   Cocos nucifera
Uroderma convexum                   Cocos nucifera
Uroderma convexum                Sabal mauritiiformis
Uroderma convexum                Sabal mauritiiformis
Uroderma convexum                Sabal mauritiiformis
Uroderma convexum                Sabal mauritiiformis
Unindentified Stenodermatinae    Sabal mauritiiformis
Unindentified Stenodermatinae    Sabal mauritiiformis
Unindentified Vampyressina       Sabal mauritiiformis

Bat species                      Tent architecture

Artibeus jamaicensis                 umbrella
Uroderma convexum                     pinnate
Uroderma convexum                     pinnate
Uroderma convexum                 unmodified leaf
Uroderma convexum                  undetermined
Uroderma convexum                  undetermined
Uroderma convexum                    umbrella
Uroderma convexum                    umbrella
Uroderma convexum                    umbrella
Uroderma convexum                    umbrella
Unindentified Stenodermatinae        umbrella
Unindentified Stenodermatinae        umbrella
Unindentified Vampyressina           umbrella
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Author:Garbino, Guilherme S.T.; Rezende, Gabriela C.; Tavares, Valeria da Cunha
Publication:Mastozoologia Neotropical
Date:Dec 1, 2018
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