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Reproductive Biology of Bothrops Erythromelas from the Brazilian Caatinga

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Reproductive Biology of Bothrops Erythromelas from the Brazilian Caatinga Hindawi Publishing Corporation Advances in Zoology Volume 2014, Article ID 680861, 11 pages http://dx.doi.org/10.1155/2014/680861 Research Article Reproductive Biology of Bothrops erythromelas from the Brazilian Caatinga Verônica Alberto Barros,1,2,3 Claudio Augusto Rojas,2,4 and Selma Maria Almeida-Santos1,2 1 Animal Biology Postgraduate Programme, Sao˜ Paulo State University (UNESP), 2265 Cristovao˜ Colombo Street, 15054-000 Sao˜ JosedoRioPreto,SP,Brazil´ 2Laboratory of Ecology and Evolution, Butantan Institute, 1500 Vital Brasil Avenue, 05503-000 Sao˜ Paulo, SP, Brazil 3Department of Protected Areas, Ministry of the Environment in Brazil (MMA), Marie Prendi Cruz Building, SEPN 505 North, Room 401, 70.730-542 Bras´ılia, DF, Brazil 4Department of Experimental Neurology, Federal University of Sao˜ Paulo (UNIFESP), 669 Pedro de Toledo Street, Research Building II, 04039-032 Sao˜ Paulo, SP, Brazil Correspondence should be addressed to Veronicaˆ Alberto Barros; [email protected] Received 9 September 2014; Accepted 29 October 2014; Published 16 December 2014 Academic Editor: Ariovaldo A. Giaretta Copyright © 2014 Veronicaˆ Alberto Barros et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The reproductive biology of Bothrops erythromelas, a small pit viper from the Caatinga, a semiarid biome in Brazil, is described based on analysis of individuals deposited in zoological collections. Males are smaller and also attain sexual maturity at a smaller size than females. Female reproductive cycle is seasonal with an extended period of secondary vitellogenesis and births occurring in a restricted period from late spring to early summer. Sperm storage in females may probably occur in infundibular tubular glands and uterine muscular twisting (UMT), which is a polymorphic condition within B. erythromelas. Seasonal spermatogenesis in males is variable with some intraspecific variation regarding the male reproductive stage per season. Most males are reproductively active during spring/summer and reproductively quiescent during autumn/winter, although some individuals vary (e.g., show testicular spermatogenesis and active sexual segment of the kidneys (SSK) during winter). The SSK could be identified in every male. Most males showed highly hypertrophied SSK in spring/summer and moderately hypertrophied SSK in autumn/winter. The ampulla ductus deferentis was observed and histochemical reactions were conducted. We discuss the probable influence of the unique environmental conditions of the Caatinga region and phylogenetic inertia in the reproductive patterns of this snake species. 1. Introduction explore questions on the influence of environmental variables in the reproductive cycles because this region has unique The Caatinga domain, a mosaic of thorny bushes and seasonal characteristics regarding patterns of temperature and rainfall dry forest, is a semiarid biome exclusive to Brazil. It is [1],andsomedataonreproductionofpitviperspeciesfrom characterized by an extremely irregular rainfall pattern with the Neotropical region including species from the Caatinga severe dry seasons in some years [1]. Reptiles that live region are available for comparisons [4–9]. in arid environments may show physiological, behavioral, Bothrops erythromelas is a terrestrial and nocturnal ecological, and morphological adaptations related to water species, responsible for many snakebites in Northeastern scarcity in the environment [2]. Recently, a long-term study Brazil, occurring both in dry and wet habitats in the Caatinga in the field showed that timing of parturition is influenced vegetation [10–12]. This small pit viper (55 cm snout-vent by rainfall seasonality in Crotalus atrox,apitviperspecies length (SVL)—female average size) [13] is a dietary generalist from the Sonoran Desert [3]. To our knowledge, few studies that feeds on frogs, lizards, mammals, and centipedes [11] addressed questions related to the influence of rainfall in the and belongs to the Bothrops neuwiedi group [14]. Previous determination of reproductive strategies in snakes [3, 4]. Pit reports of B. erythromelas reproductionareanecdotal.Mating viper species from the Caatinga region are good models to wasobservedinautumn(AprilandMay)andbirthswere 2 Advances in Zoology Xique-Xique City, Bahia State, Brazil 1950–2000 40 140 35 120 C) 30 ∘ 100 Bothrops erythromelas ( PA T 25 80 ∘ CE 20 5 S MA 60 RN 15 40 PI PB 10 Rainfall (mm) PE Temperature 5 20 ∘ TO AL 10 S SE 0 0 Jul BA Jan Jun Sep Feb Oct Apr Dec Aug Mar Nov May N Summer Autumn Winter Spring ∘ GO (km) 15 S W E 0 250 500 T DF MG min S T max ∘ ∘ ∘ ∘ 45 W 40 W 35 W 30 W Rain (a) (b) Figure 1: (a) Geographical origin of Bothrops erythromelas specimens sampled for this study in Northeastern Brazil. Caatinga is marked in gray. (b) Climatic pattern of the Caatinga. observed in summer (January and February) in captivity using DIVA-GIS (version 7.1.7) and WorldClim Database [5, 15]. (current climate: 1950–2000, version 1.3, 10 min resolution). The aim of this study is to describe the reproductive High temperatures are maintained throughout the year. biology of B. erythromelas, considering male and female Rainfall is seasonal, characterizing two well-defined seasons: reproductive cycles, sperm storage, sexual maturity, and the dry and wet seasons (Figure 1(b)). The coldest months ∘ dimorphism. We discuss the existence of a strong phyloge- were July and/or August (temperature ranging from 13.3 C ∘ netic component in the determination of Bothrops reproduc- to 32 C) and the warmest months occurred between October tive patterns [5] versus the hypothesis of an environmentally and February, depending on the area (temperature ranging ∘ ∘ cued reproductive pattern for B. erythromelas.Ifphylogenetic from 16.6 Cto34.6C). Annual precipitation varies between inertia plays a major role in determining reproductive cycles, 424 and 978 mm amongst the sampled areas. Reproductive wewouldexpecttofindthesamereproductivetimingfor events are described according to austral seasons to allow species that live under different environmental conditions comparisons with snake species from various parts of the (i.e., species from different biomes showing similar reproduc- world. tive cycles). On the other hand, if patterns of temperature, We measured snout-vent length (SVL) to the nearest rainfall, prey availability, or other environmental variables 1 mm, and after dissection the following data were recorded: strongly affect reproductive cycles, we would expect to see a (1) diameter of the largest ovarian follicle or presence of different reproductive pattern for B. erythromelas in compar- embryos in females; (2) presence/absence of uterine muscular ison to Bothrops species from other biomes. Thus, we looked twisting (UMT), a sperm storage site in the posterior uterus for differences and similarities in the reproductive charac- [4–6]; (3) presence of corpora lutea in the ovaries; (4) teristics between pit vipers from the Caatinga and other testicular length; (5) width of the distal ductus deferens. These regions in Brazil with distinct climates and environmental measurements were taken to the nearest 0.1 mm. conditions. Ductus deferens was considered convoluted or noncon- voluted according to the macroscopic aspect. The presence 2. Materials and Methods of spermatozoa in the testes or ductus deferens in the histo- logical analysis was used as the main criterion to determine We examined a total of 246 preserved specimens of Bothrops sexual maturity in males. The convoluted aspect of the erythromelas (116 mature females, 97 mature males, and 33 ductus deferens was used as an additional criterion. Females immatures) held in the collections of the Instituto Butantan were considered mature if they had follicles in secondary (IB), Universidade Federal da Bahia (UFBA), and Museu vitellogenesis, based on the presence of oviductal embryos or Nacional (MNRJ). Individuals were originally collected from corpora lutea in the ovaries. Individuals that did not present 1927 to 2009 in the following states in the northeastern region these characteristics were considered immature. of Brazil: Bahia (BA), Pernambuco (PE), Para´ıba (PB), Rio The reproductive cycle of mature females was determined Grande do Norte (RN), and Ceara(CE).Amapshowingthe´ by comparing the length of the largest ovarian follicle or municipalities where snakes have been collected was made oviductal embryo at different times of the year. Records of using Arc Gis (version 9.3) (Figure 1(a)). mating and parturition in captivity were also incorporated To characterize the climatic patterns of the Caatinga re- to complete the cycle [5, 15]. Female oviduct (=8)was gion, climatograms were constructed for every municipality histologicallyexaminedtolookforthepresenceofsperm. Advances in Zoology 3 Se Sd L Sg L Sg Sp (a) (b) L Sd Sz Sg Sp (c) Figure 2: Spermatogenic stages in Bothrops erythromelas. (a) Regression. (b) Recrudescence. (c) Spermiogenesis. L = lumen; Sd = spermatid; Se = seminiferous epithelium; Sg = spermatogonia; Sp = primary spermatocyte; Sz = spermatozoa. We also provide a brief description of oviducal regions. A spermatozoa from the previous spermatogenic season in the preliminary analysis of the occurrence of UMT in Bothrops lumen, (2) recrudescence (mitotic and meiotic phase), char- snakes was made using Mesquite (version 2.75) [16]. The acterized
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