Reproduction in the pitviper Bothrops jararacussu: large females increase their reproductive output while small males increase their potential to mate
Introduction
Reproductive traits vary widely within and among species of squamate reptiles. Variation in reproductive traits is often attributed to the occupation of regions with different environmental factors (Mesquita and Colli, 2003; Ji and Wang, 2005). For instance, temperate-zone squamates usually reproduce seasonally, with females ovipositing/giving birth during the warmer months, whereas tropical squamates tend to exhibit more variable cycles, with females reproducing over longer periods (James and Shine, 1985; Seigel and Ford, 1987). In turn, similarity in reproductive traits often occurs even in populations or closely related species inhabiting environmentally distinct areas. For instance, low and invariant clutch sizes characterize entire lineages of lizards from drastically different environments (Shine and Greer, 1991). Such similarity in reproductive patterns is often attributed to phylogenetic conservatism, since closely related species tend to exhibit similar traits because of their common ancestry (Harvey and Pagel, 1991). Additionally, variation in several reproductive traits is also attributed to variation in body size and its correlates, such as abdominal volume. Body size influences reproductive output, i.e., clutch/litter size, offspring size, and reproductive frequency. In species with variable clutch/litter size, larger females tend to produce more and/or larger offspring (Dunham et al., 1988; Shine, 1994). Moreover, in many species, larger females tend to reproduce more often than smaller conspecifics (Seigel and Ford, 1987). These patterns are evident across species and are also influenced by the environment and phylogeny (Dunham et al., 1988; Shine, 1994; Bellini et al., 2017).
In snakes, previous studies have shown that female reproductive phenology tends to be phylogenetically conserved (Shine, 1989; Pizzatto et al., 2008a, 2008b; Marques et al., 2013b; Shine et al., 2014). However, given the remarkable diversity in snake reproductive strategies (Seigel and Ford, 1987; Shine, 2003), a complex array of conservative and variable reproductive traits is also evident. For instance, the timing of vitellogenesis varies geographically within some species (e.g., Pizzatto et al., 2008b) but not in others (see examples in Aldridge et al., 2009). In addition, the possibility that phylogeny also constrains male reproductive patterns needs confirmation, as many studies on male reproduction lack direct evidence supporting the timing of spermatogenesis (reviewed in Mathies, 2011). Although clutch/litter size increases with maternal body size in most species, this relationship is not evident in all species (Seigel and Ford, 1987). Similarly, reproductive frequency increases with increasing female body size in several species (Blem, 1982; Seigel and Ford, 1987), but in others, it decreases with body size (Shine et al., 1998) or is maximized at intermediate body sizes (Madsen and Shine, 1996; Bonnet et al., 2000). Thus, it remains difficult to generalize the patterns of reproductive variation in snakes and, consequently, we need additional studies on several snake species, especially on tropical snake faunas.
Lancehead snakes (genus Bothrops) are an excellent study system in which to investigate factors that influence reproduction. The genus contains 45 species widely distributed over a range of climatically distinct ecoregions in Central and South America (Carrasco et al., 2019; Uetz et al., 2019). Moreover, Bothrops species vary greatly in body sizes, body shapes, and macrohabitat use (Martins et al., 2001), and their phylogenetic relationships are reasonably known (Alencar et al., 2016), thus facilitating the interpretation of the evolution of reproductive patterns. Female reproductive biology has been investigated in a reasonable number of Bothrops (Solórzano and Cerdas, 1989; Sazima, 1992; Almeida-Santos and Orsi, 2002; Almeida-Santos and Salomão, 2002; Valdujo et al., 2002; Nogueira et al., 2003; Hartmann et al., 2004; Monteiro et al., 2006; Nunes et al., 2010; Marques et al., 2013a; Barros et al., 2014a, 2014b; Leão et al., 2014; Almeida-Santos et al., 2017; Silva et al., 2019b). Irrespective of the diversity of habitats in which they occur (ranging from seasonal to aseasonal environments), female Bothrops reproduce seasonally and share similarities in various reproductive characteristics likely inherited from their ancestor (Almeida-Santos and Salomão, 2002). For instance, in most Bothrops species studied, mating occurs primarily in autumn, with females at early vitellogenesis. Consequently, females must store sperm in their reproductive tract until ovulation in spring, and parturition occurs mostly in summer but may extend to autumn (Almeida-Santos and Salomão, 2002; for an exception, see Silva et al., 2019b). Moreover, in all Bothrops species studied so far, females typically grow larger and mature at larger body sizes than males (e.g., Solórzano and Cerdas, 1989; Valdujo et al., 2002; Nogueira et al., 2003; Silva et al., 2019b). In contrast, litter size seems highly variable interspecifically (Almeida-Santos and Salomão, 2002) but typically increases with maternal body size intraspecifically (e.g., Solórzano and Cerdas, 1989; Nogueira et al., 2003; Hartmann et al., 2004). Male reproductive patterns have been less studied, but Almeida-Santos and Salomão (2002) hypothesized that spermatogenesis is also seasonal (occurring in spring-summer) and phylogenetically conserved. Recent studies have generally corroborated this hypothesis (Barros et al., 2014b; Almeida-Santos et al., 2017; Silva et al., 2019b; but see Barros et al., 2014a). However, male reproductive cycles have been investigated histologically in few Bothrops and therefore this hypothesis has not yet been tested.
This study describes the reproductive biology of B. jararacussu, a species found in southeastern South America (Campbell and Lamar, 2004; Marques et al., 2004). In Brazil, B. jararacussu inhabits primarily lowland (from 0-700 m of elevation) Atlantic forest areas along southeastern and southern regions (Nogueira et al., 2019). This species is a dietary generalist, and individuals are found active on the ground by day and night (Martins et al., 2002; Marques and Sazima, 2004). Female B. jararacussu have rather stout bodies and attain one of the largest sizes in the genus (Martins et al., 2001). However, no study has addressed its reproductive biology. We combined macroscopic and microscopic examinations of the reproductive system of museum specimens with observations of free-ranging and recently captured snakes to characterize size at sexual maturity, sexual size dimorphism, reproductive output, and male and female reproductive cycles. We address the following questions: (1) Is there sexual size dimorphism, and if so, what is the magnitude and the potential causes of such dimorphism? (2) Does the large female size result in an increase in reproductive output, compared with congeners? (3) Does the male reproductive phenology resemble that of its congeners, reflecting a conserved pattern? We also discuss the factors that may play a role in shaping the reproductive patterns observed in the genus.
Section snippets
Specimens and area
We collected reproductive data from 609 specimens housed in Brazilian museums (Supplementary Table S1). Specimens were collected between 1914-2016 in the Atlantic forest areas of the states of Rio de Janeiro, São Paulo, Paraná, and Santa Catarina (between 21 and 27 °S, 4–1000 m above sea level; Supplementary Table S1). The climate in this portion of the Atlantic Forest is seasonal. Warmer temperatures occur from spring (October-December) to summer (January-March) and are associated with higher
Body sizes, sexual maturity, and sexual size dimorphism
The smallest adult male measured 460 mm SVL, and all males larger than 610 mm SVL were adults. Most individual males (28 of 39; 76%) between 460-610 mm SVL were adults. The smallest adult female was pregnant and measured 800 mm SVL, and all females larger than 1010 mm SVL were adults. Most individual females (26 of 36, 72%) between 800-1010 mm SVL were adults. Therefore, males attained sexual maturity at smaller body sizes than females. Adult females averaged 1150.6 ± 144.7 mm SVL (range =
Sexual maturity, sexual size dimorphism, and reproductive output
As expected, female B. jararacussu mature at larger body sizes than males, and litter size increases with maternal body size. These patterns are common in snakes (Seigel and Ford, 1987; Shine, 1994), including Bothrops (Solórzano and Cerdas, 1989; Sazima, 1992; Valdujo et al., 2002; Hartmann et al., 2004; Monteiro et al., 2006; Marques et al., 2013a; Barros et al., 2014a, 2014b; Leão et al., 2014; Almeida-Santos et al., 2017; Silva et al., 2019b). Therefore, maturity at larger body sizes allows
Conclusions
Bothrops jararacussu shares several characteristics with its congeners such as autumn mating season, obligatory sperm storage in the female reproductive tract, timing of parturition, female-biased SSD, maturity at larger body sizes in females, and increases in litter size with increasing body size. We suggest that these characteristics are phylogenetically conserved in Bothrops. On the other hand, this pitviper has evolved some unique characteristics such as a high degree of SSD (one of the
Declaration of Competing Interest
The authors declare no conflict of interest.
Acknowledgements
We thank Giuseppe Puorto, Francisco Franco, Paulo Passos, and Júlio Moura-Leite for allowing us to examine specimens under their care. We also thank Nina Furnari for assistance in data collection, Valdir Germano for assistance in the laboratory, Luciana Sato for assistance with the histochemical tests, Marta Antoniazzi and Carlos Jared for kindly allowing access to microscopic equipment, Fernanda Stender-Oliveira and Rodrigo Scartozzoni for providing unpublished information on mating and
References (113)
- et al.
Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates
Mol. Phylogenet. Evol.
(2016) - et al.
The reproductive biology of male cottonmouths (Agkistrodon piscivorus): Do plasma steroid hormones predict the mating season?
Gen. Comp. Endocrinol.
(2008) - et al.
Development of the renal sexual segment in immature snakes: effect of sex steroid hormones
Comp. Biochem. Physiol. Part A Mol. Integr. Physiol.
(2004) - et al.
Annual cycle of plasma testosterone in male copperheads, Agkistrodon contortrix(Serpentes, Viperidae): Relationship to timing of spermatogenesis, mating, and agonistic behavior
Gen. Comp. Endocrinol.
(1997) - et al.
Image processing with ImageJ
Biophotonics Int.
(2004) - et al.
Reproduction of the water snake Helicops infrataeniatus (Colubridae) in southern Brazil
Amphibia-Reptilia
(2005) Environmental control of spermatogenesis in the rattlesnake Crotalus viridis
Copeia
(1975)Seasonal spermatogenesis in sympatric Crotalus viridis and Arizona elegans in New Mexico
J. Herpetol.
(1979)The link between mating season and male reproductive anatomy in the rattlesnakes Crotalus viridis oreganus and Crotalus viridis helleri
J. Herpetol.
(2002)- et al.
Male reproductive cycle, age at maturity, and cost of reproduction in the timber rattlesnake (Crotalus horridus)
J. Herpetol.
(1995)
Evolution of the mating season in the pitvipers of North America
Herpetol. Monogr.
The reproductive cycle and estrus in the colubrid snakes of temperate North America
Contemp. Herpetol.
Reproductive biology of the massasauga (Sistrurus catenatus) from South-Central Illinois
The sexual segment of the kidney
Seasonal timing of spermatogenesis and mating in squamates: A reinterpretation
Copeia
Modelos reprodutivos em serpentes: estocagem de esperma e placentação em Crotalus durissus e Bothrops jararaca (Serpentes: Viperidae)
Reproductive biology of the Brazilian lancehead, Bothrops moojeni (Serpentes, Viperidae), from the state of São Paulo, southeastern Brazil
South Am. J. Herpetol.
Biologia reprodutiva de serpentes: recomendações para a coleta e análise de dados
Herpetol. Bras.
Ciclo reprodutivo de Crotalus durissus e Bothrops jararaca (Serpentes, Viperidae): morfologia e função do oviduto
Rev. Bras. Reprodução Anim.
Reproduction in Neotropical pitvipers, with emphasis on species of the genus Bothrops
Is rainfall seasonality important for reproductive strategies in viviparous Neotropical pitvipers? A case study with Bothrops leucurus from the Brazilian Atlantic Forest
Herpetol. J.
Reproductive biology of Bothrops erythromelas from the Brazilian Caatinga
Adv. Zool.
Male reproductive cycle of Bothrops pubescens(Serpentes, Viperidae) from Southern Brazil
South Am. J. Herpetol.
Reproductive biology of the neotropical rattlesnake Crotalus durissus from northeastern Brazil: a test of phylogenetic conservatism of reproductive patterns
Herpetol. J.
Reproductive cycle and sperm storage of female coral snakes, Micrurus corallinus and Micrurus frontalis
Amphibia-Reptilia
Annual variation in time-energy allocation by timber rattlesnakes (Crotalus horridus) in relation to food acquisition
Is xenodontine snake reproduction shaped by ancestry, more than by ecology?
Ecol. Evol.
Biennial reproduction in snakes: an alternative hypothesis
Copeia
Reproductive versus ecological advantages to larger body size in female snakes, Vipera aspis
Oikos
Uterine and eggshell modifications associated with the evolution of viviparity in South American water snakes (Helicops spp.)
J. Exp. Zool. Part B Mol. Dev. Evol.
Reproductive ecology and diet of the fossorial snake Phalotris lativittatus in the Brazilian Cerrado
Herpetol. J.
Reproductive biology of the fossorial snake Apostolepis gaboi (Elapomorphini): a threatened and poorly known species from the Caatinga region
South Am. J. Herpetol.
A new species of Bothrops (Serpentes: Viperidae: Crotalinae) from Pampas del Heath, southeastern Peru, with comments on the systematics of the Bothrops neuwiedi species group
Zootaxa
The evolution of sexual size dimorphism in reptiles
Life history patterns in squamate reptiles
The influence of female body size and shape on the trade-off between offspring number and offspring size in two viviparous snakes
J. Zool.
Reproduction in the tiger rattlesnake, Crotalus tigris (Serpentes: Viperidae)
Texas J. Sci.
Reproduction in the blacktail rattlesnake, Crotalus molossus (Serpentes: Viperidae)
Texas J. Sci.
Reproduction in the speckled rattlesnake, Crotalus mitchellii (Serpentes: Viperidae)
Bull. South. Calif. Acad. Sci.
Reproduction in the twin-spotted rattlesnake, Crotalus pricei (Serpentes: Viperidae)
West. North Am. Nat.
Reproduction in the Baja California rattlesnake, Crotalus enyo (Serpentes: Viperidae)
Bull. South. Calif. Acad. Sci.
Seasonal testicular histology of the colubrid snakes, Masticophis taeniatus and Pituophis melanoleucus
Herpetologica
Reproduction in the Mojave rattlesnake, Crotalus scutulatus (Serpentes: Viperidae)
Texas J. Sci.
Snake litter size = live young + dead young + yolks
Herpetol. J.
Reproductive biology of the southern Brazilian pitviper Bothrops neuwiedi pubescens (Serpentes, Viperidae)
Amphibia-Reptilia
The Comparative Method in Evolutionary Biology
Ecological divergence and sexual selection drive sexual size dimorphism in new world pitvipers (Serpentes: Viperidae)
J. Evol. Biol.
Reproduction in northern populations of the ridgenose rattlesnake, Crotalus willardi (Serpentes: Viperidae)
Copeia
Understanding reproductive allometry in turtles: A slippery “slope”
Ecol. Evol.
Cited by (15)
Clinical implications of ontogenetic differences in the coagulotoxic activity of Bothrops jararacussu venoms
2021, Toxicology LettersCitation Excerpt :Belonging to the Bothrops genus, which is responsible for the majority of snakebite accidents in Brazil (Chippaux, 2015), B. jararacussu is included as a Category 1 by WHO as a species that has medical relevance, due to the number of accidents and morbidity of the snake envenomation (WHO, 1999). B othrops jararacussu is characterized by its sexual dimorphism, in which females are larger than males, thus being able to produce a high volume of venom (Melgarejo, 2009; Milani et al., 1997; Silva et al., 2020). This species is distributed in tropical forests in Brazil, southern Bolivia, Paraguay, and Northeastern Argentina (Melgarejo, 2009; Milani et al., 1997).
Sexual dimorphism in Louisiana pine snakes (Pituophis ruthveni)
2023, Zoo BiologySexual maturity of Bothrops asper (Serpentes: Viperidae) from Costa Rica
2023, Phyllomedusa