Redalyc.Reproductive Phenology of the American Bullfrog in Subtropical

Anais da Academia Brasileira de Ciências ISSN: 0001-3765 [email protected] Academia Brasileira de Ciências Brasil Medeiros, Camila I.; Both, Camila; Kaefer, Igor L.; Cechin, Sonia Z. Reproductive phenology of the American Bullfrog in subtropical Brazil: photoperiod as a main determinant of seasonal activity Anais da Academia Brasileira de Ciências, vol. 88, núm. 3, 2016, pp. 1909-1921 Academia Brasileira de Ciências Rio de Janeiro, Brasil Available in: http://www.redalyc.org/articulo.oa?id=32748476028 How to cite Complete issue Scientific Information System More information about this article Network of Scientific Journals from Latin America, the Caribbean, Spain and Portugal Journal's homepage in redalyc.org Non-profit academic project, developed under the open access initiative Anais da Academia Brasileira de Ciências (2016) 88(3 Suppl.): 1909-1921 (Annals of the Brazilian Academy of Sciences) Printed version ISSN 0001-3765 / Online version ISSN 1678-2690 http://dx.doi.org/10.1590/0001-3765201620150694 www.scielo.br/aabc Reproductive phenology of the American Bullfrog in subtropical Brazil: photoperiod as a main determinant of seasonal activity CAMILA I. MEDEIROS1, CAMILA BOTH1, IGOR L. KAEFER2 and SONIA Z. CECHIN1 1Departamento de Biologia, Universidade Federal de Santa Maria, Avenida Roraima, 1000, Camobi, 97105-900 Santa Maria, RS, Brasil 2Departamento de Biologia, Universidade Federal do Amazonas, Avenida General Rodrigo Octávio, 6200, Bairro Coroado, 69077-000 Manaus, AM, Brasil Manuscript received on October 5, 2015; accepted for publication on March 1, 2016 ABSTRACT The North American bullfrog Lithobates catesbeianus continues to invade ecosystems worldwide, potentially causing population declines and even extinctions. Within its native distribution, bullfrogs show prolonged reproductive seasons and high fertility. However, data on breeding biology of bullfrogs ex-situ in invaded localities mainly comes from anecdotal reports. Understanding how invasive species are adjusting their life histories to new colonized environments is important for conservation purposes. Here we describe temporal and spatial abundance, calling activity, spawning and tadpole distribution of bullfrogs in southern Brazil. Eighteen samplings occurred during one year. The abundance of individuals was positively related to longer photoperiods and higher temperatures. Reproductive activity was also positively associated with longer photoperiods. Calling sites, spawning and tadpoles were associated with microhabitats presenting hydrophytes, which may provide shelter and thermal stability to bullfrogs. The reproductive seasonal activity of bullfrogs can be highly variable across its growing geographical range, but in subtropical Brazil it is associated with photoperiod, a highly predictable abiotic determinant. In our study area, bullfrogs presented a breeding season twice as long as that observed in some native localities. We suggest that management strategies directed to bullfrog populations must consider the habitat structures and seasonal regimes determined by each invaded environment. Key words: breeding, invasive species, Lithobates catesbeianus, microhabitat, recruitment, spatial distribution. INTRODUCTION Lodge 2001, Facon et al. 2006), presence of natural enemies (Settle and Wilson 1990, Keane and When a species is introduced into new environments Crawley 2002) and availability of resources (Petren it may be able to survive, establish populations and Case 1996), among others. Once a species and become invasive. Invasion success depends becomes invasive, its presence can have significant on biological attributes of the species (Kolar and ecological impact and lead to the homogenization Correspondence to: Camila Ineu Medeiros of entire ecosystems (Mack et al. 2000). The E-mail: [email protected] bullfrog Lithobates catesbeianus (Shaw 1802), one An Acad Bras Cienc (2016) 88 (3 Suppl.) 1910 CAMILA I. MEDEIROS, CAMILA BOTH, IGOR L. KAEFER and SONIA Z. CECHIN of the most successful invasive species of the world exist on the reproductive biology of bullfrogs in (IUCN 2003), has been introduced in more than 40 ex-situ populations in Brazil. In the state of Minas countries and four continents over the last century Gerais (southeastern Brazil), abundances of tad- (Lever 2003). Its native region comprises southern poles are greater in the warmer months, coinciding Canada, the south-central and eastern United States with the period of male calling activity (Afonso et and northern Mexico (Frost 1985, Frost 2015). At al. 2010). A similar pattern has been found for pop- North American introduction sites of bullfrogs, ulations from Paraná (southern Brazil), where the the decline of various amphibian species was species’ reproductive activity is interrupted by low recorded (Bury and Luckenbach 1976, Hayes and temperatures in autumn/winter (Conte and Rossa- Jennings 1986, Hecnar and M’Closkey 1997, Pearl Feres 2006, Leivas et al. 2012). et al. 2005). Experimental studies have shown that Breeding activity in anuran amphibians is bullfrog tadpoles can reduce food resources for more strongly influenced by abiotic than by biotic tadpoles of others species like Ranidae, Bufonidae, factors: environmental variables such as light, rain- Hylidae and tiger salamander (Kupferberg 1997, fall and temperature (Duellmann and Trueb 1994, Adams 2000, Boone et al. 2004). Bullfrogs also Wells 2007). Additionally, photoperiod is increas- have the potential to affect native species in the ingly known to influence the timing of reproduc- acoustic niche (Both and Grant 2012). In addition, tion in subtropical anuran assemblages. (Both et al. they can be a threat to native frogs through the 2008, Canavero and Arim 2009), controlling events dissemination of pathogens and diseases, such as such as gametogenesis and anuran calling (Hatano chytridiomycosis (Berger et al. 1998, Daszak et al. et al. 2002, Kaefer et al. 2009). Thus, assessing the 2004, Schoegel et al. 2010). relation between reproductive activity and photoperiod presents an excellent opportunity to better A series of studies on bullfrog biology conduct- understand the reproductive phenology of bullfrogs ed in Brazil indicate that this species has adapted to in the subtropics and evaluate its invasion success. climatic conditions and can survive and reproduce Gonadal analyses of L. catesbeianus in sub- in invaded areas (Boelter and Cechin 2007, Kae- tropical Brazil indicated that although mature males fer et al. 2007, Alves et al. 2008, Silva et al. 2009, are found throughout the year, females produce Afonso et al. 2010, Leivas et al. 2012, Boelter et al. gametes in advanced developmental stages only in 2012). It has been suggested that bullfrogs might spring and summer (Kaefer et al. 2007). However, negatively affect various native species in Brazil, in despite the fact that research on bullfrog invasion however there is a lack of evidence supporting such has been growing in the last 10 years (see Cam- impacts (see Both et al. 2014). pos et al. 2014), little is known about the breeding Throughout its native distribution, L. catesbe- phenology of this species for most of the invaded ianus is known to occupy mainly permanent water localities. The geographical location directly influ- bodies, where it reproduces at high rates (Bury and ences life history traits of invasive species, affect- Whelan 1984). The prolonged reproductive season ing its timing of reproduction, and other traits such is characterized by male calling activity periods as body size, sexual maturity and fecundity (Bury (Emlen 1976, Ryan 1980, Bury and Whelan 1984) and Whelan 1984). Therefore, understanding how and by intense movement of females for partner invasive species respond to environmental changes selection (Wiewandt 1969, Howard 1978, Ryan in invaded areas is one of the first steps to plan fu- 1980). Spawning may occur once or twice in a ture studies and management strategies. given reproductive cycle (Emlen 1977, Ryan 1980, In this study, we characterized the reproductive Govindarajulu et al. 2006). However, few studies phenology of bullfrogs in an invaded region in An Acad Bras Cienc (2016) 88 (3 Suppl.) REPRODUCTIVE PHENOLOGY OF THE AMERICAN BULLFROG 1911 southern Brazil based on field observation records. once a month in autumn and winter (August and We investigated which environmental descriptors September 2010; April to July 2011). We sampled could explain the abundance of males, females and fortnightly in the spring and summer (October to juveniles of bullfrogs along the year. We described March 2010) because this is the period when both vocalization and spawning periods, as well as the sexes display mature gonads in southern Brazil temporal distribution of tadpoles, and characterized (Kaefer et al. 2007). This increased effort was em- microhabitats where calling males, egg masses and ployed with the intent to better characterize behav- tadpoles were found. Finally, we compared our data ior and microhabitat use for the species. with phenological data reported from other invaded We searched for spawning by visual inspection, and native localities. while walking around the pond banks during the day. For each microhabitat with spawns present, MATERIALS AND METHODS we recorded depth, distance from the margin, STUDY SITE and presence and type of structural vegetation. Vegetation types were categorized as ‘emergent’, We conducted the fieldwork in two permanent wa- ‘submerse’ and/or ‘floating’ hydrophytes. The ter bodies in the

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