Growth patterns of the Golden Lancehead and their determinants: Conservation strategies for critically endangered species

Growth patterns of the Golden Lancehead and their determinants: Conservation strategies for critically endangered species | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Research Article Growth patterns of the Golden Lancehead and their determinants: Conservation strategies for critically endangered species Karina Rodrigues Silva Banci, Lucas Henrique Carvalho Siqueira, and 1 more This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-4607766/v1 This work is licensed under a CC BY 4.0 License Status: Posted Version 1 posted You are reading this latest preprint version Abstract The Golden Lancehead, Bothrops insularis , is a critically endangered viperid species, endemic to Queimada Grande Island. The diet of adults relies mainly on migratory birds, which peaks in March and July on the island. Herein, we describe the growth rate of the Golden Lancehead for the very first time, testing the hypothesis that growth and adult body size may decrease as a result of resource scarcity and environmental variability in the island, in comparison to a captive population. Our findings suggest that both food intake, temperature, and reproductive requirements might influence body size, growth rate, and sexual maturity of B. insularis . More specifically, wild animals attain smaller body size and mass, show lower growth rate, and attain sexual maturity later, in comparison to the captive individuals of the same sex, possibly as a result of lower food availability. This situation is more evident among males, and, apparently, morphological constraints make it difficult for them to explore large prey at the island. Females are the largest sex, possibly as a result of fecundity optimization. Fecundity also depends on energy reserve for vitellogenesis, and, due to the metabolic costs involved, females take a longer time to mature, showing, therefore, delayed maturity when compared to males. These aspects are especially important for conservation. Concerning species conservation, the impact of the larger body size in captive animals on other traits, such as habitat use, must be considered, especially if reintroduction of these animals become necessary. As for the Golden Lanceheads in the island, it is mandatory that the conservation strategies encompass the maintenance of the population of the migratory birds, in order to ensure the energetic income to the snakes. Bothrops insularis food intake sexual maturity in situ conservation ex situ conservation snake Figures Figure 1 Figure 2 Figure 3 Figure 4 Introduction As with most ectothermic vertebrates, snakes show continuous and indeterminate growth throughout life (Shine and Charnov 1992 ; Saint-Girons 1994 , Hariharan et al 2015 ). Growth rate relies on several factors, such as genetic traits, availability of resources (such as food and water), climatic conditions, and success of capturing and digesting prey (Macartney et al 1990 ; Saint-Girons 1994 ; Lillywhite 2014 ; Hariharan et al 2015 ). It also varies according to age, so that snakes usually grow faster early in life, with growth rate decreasing after sexual maturation, closely following an asymptotic pattern (Shine and Charnov 1992 ; Lillywhite 2014 ). The reason why growth rate decreases after attaining sexual maturity is that the energy which was previously mobilized for growing starts being directed to the development of the structures and behaviours associated with reproduction (Lillywhite 2014 ). For males, it involves the development of the testicles and hypertrophy of the annex glands such as the epididymis and the sexual segment of the kidneys (Saint-Girons 1994 ). As for the females, a great energy intake is necessary for the vitellogenesis to occur previously to ovulation, and this process is so bioenergetically expensive that the costs may outweigh those of pregnancy itself (Saint-Girons 1994 ; Van Dyke and Beaupre 2011 ). For these processes, snakes may allocate either stored reserves (the so-called capital breeders), or energy obtained from recently-ingested food (the income breeders; Van Dyke et al 2012 ). Among ectotherms, there is also the so-called temperature-size rule, being that lower temperatures cause these animals to grow slower but mature at a larger body size (Angilletta et al 2004 ). This rule is verified in individuals of Thamnophis sirtalis and T. elegans which grow faster in warmer temperatures (Arnold and Peterson 1989 ; Bronikowski 2000; Gangloff et al 2015 ). On the other hand, this pattern was not observed in another species from temperate locality, Vipera aspis (Michel and Bonnet 2010). Nevertheless, knowledge on growth rate and pattern of snakes in warm climates is still scarce, especially for neotropical species. The Golden Lancehead Bothrops insularis is a viviparous species of the Bothrops jararaca complex (Alencar et al 2016 ). It is one of the most arboreal species of the genus, and shows morphological differences when compared to congeneric species (Amaral 1921 ; Martins et al 2002 ; Wüster et al 2005 ; Marques 2021). Similarly to other Bothrops species, females are larger than males (Marques et al 2013 ). The Golden Lancehead is endemic to Queimada Grande Island (QGI, São Paulo, Brazil), and is classified as a critically endangered species due to its endemism and restrict distribution, with habitat damaged by past fires, and populational decrease mainly attributed to biopiracy (Martins et al 2008; Guimarães et al 2014; Silveira et al 2023). For this reason, the International Union for Conservation of Nature (IUCN) recommends the establishment of captive populations in order to ensure the species’ ex-situ conservation. Therefore, the Laboratório de Ecologia e Evolução (LEEV) of Instituto Butantan has housed a captive population of Bothrops insularis since 2009. As mentioned above, food availability affects growth rate, and prey can be a limited and ephemeral resource for island snakes (Lillywhite 2014 ), such as B. insularis . Wild specimens of Golden Lancehead feeds mainly on migratory birds, namely the Tyrant Elaenia chilensis , that visits the island in mid-March, and the Yellow-legged Thrush ( Turdus flavipes ), which visits the island in mid-July, a resource that varies seasonally and from year to year (Marques et al 2012 , 2013 ). The captive individuals, however, receive water and food (mice) regularly throughout the year. Food intake influences snakes’ growth, so that scarcity of prey lead to decreased growth rate (Lindell and Forsman 2011 ), and supplementation of prey may cause snakes to be larger (Ford and Seigel 1994 ). Likewise, food intake may influence reproductive traits, causing females to show early maturation or even causing the number of reproductive females in “good” years of food availability to outnumber that of when prey was scarce ( e.g. Ford and Seigel 1994 ; Shine and Madsen 1997 ). Such influences are even more pronounced when this higher food supply happens in the first years of life, causing a “silver spoon effect” (Ford and Seigel 1994 ; Madsen and Shine 2000 ). Also, growth patterns differ between sexes in sexually dimorphic species (Madsen 1983 ; Plummer 1985 ). Considering the differences in resources availability to which the wild and the captive populations of B. insularis are submitted, the aim of the present work is to test the following hypotheses: (1) wild animals attain smaller size and mass than the captive ones; (2) sexual maturity (inferred by the animals’ SVL, based on Marques et al 2013 , and Passos 2018 ) of wild animals is reached later in comparison to that of captive ones; and (3) growth rate is lower in wild individuals. Because growth rate may be also related with climate regimen, we also tested for differences in temperature and humidity between both localities. Methods Data Collection Captive individuals are housed at Laboratório de Ecologia e Evolução, Instituto Butantan. They are kept in boxes individually, in a room with an average temperature with an average around 24ºC all year-round, average humidity around 23%, and photoperiod of 12:12h, with light phase from 6 a.m. to 6 p.m. The animals are monthly fed on mice, representing 20% of their body mass, and they are annually measured and weighed. The captive population is now made up of three generations. We only used morphometric data from the two generations which were born in the laboratory, in order to avoid bias arising from the animals having lived a part of their lives in the island. In this sense, we used data from 15 females, and 20 males, that were from one to ten years old. For the wild population, growth data were gathered from mark and recapture events of animals in the field. The identification of Golden Lanceheads from Queimada Grande Island (QGI) with 12mm passive integrated transponder (PIT) tags is a routine procedure during our expeditions, and made it possible for us to recapture some of the animals (general recapture rate is around 13%; present study). These data were obtained during sampling trips from 2004 to 2023, comprising 35 females and 37 males (which corresponds to a recapture rate of 8%, after filtering for complete records), and included recaptures ranging from 3 months up to almost 8 years after capture. Diet of wild snakes was inferred from data collected in the study by Marques et al ( 2012 ) added to information obtained on expeditions before or after this study mainly from palpation of fed animals found on QGI. Prey types were identified at the most specific taxonomic level as possible, and ranked according to their body mass ( cf. Sick 1984 ; Santos 2018 ; Marinho 2022 ; McGehee et al 2023, WikiAves 2024 , pers. obs.). Identified prey were then associated with the snout-vent length (SVL) and gender of the individuals of B. insularis which had fed on them, in order to evaluate dietary patterns in different sexes and size classes. For growth and body size analyses, we used data of 35 captive and of 710 wild individuals (395 females and 315 males) encountered at QGI from 2004 to 2023. The morphometric data utilized were: (1) snout-vent length (SVL), measured from the tip of the nose to the cloaca; (2) tail length (TL), measured from the cloaca to the end of the tail, using a measuring tape with accuracy of 1 mm; (3) total body length (TBL; calculated by SVL + TL); and (4) body mass, weighted using precision dynamometers (in the island; precision of 1 g) or precision scale (in the laboratory, precision of 0.1 g). In case of an individual being recaptured more than once in each field expedition, only the first biometric data were considered. Daily air temperature and humidity were collected in captivity using a thermohygrometer. Unfortunately, we lacked a meteorological station at QGI. Therefore, we considered data measured in the closest meteorological stations available: Itanhaém Municipality (from 2010 to 2016), and Bertioga Municipality (about 110 km away; from 2017 to 2020). Such data were provided by Instituto Nacional de Meteorologia (INMET, 2022). Previous analyses showed that these data were not normally-distributed, even after being log-transformed. Therefore, they were analysed using Paired Wilcoxon Test, using RStudio 2022.12.0 and The R Stats Package (R Core Team, 2022 ). Growth models and rates Two different methods were used, one for investigating growth of wild individuals, and another, for captive individuals, due to kind of data gathered for each population. In this sense, once we knew the birth date of all 35 individuals, we used the von Bertalanffy Typical model (1; von Bertalanffy 1938). Data for each sex was also analysed separately. Growth rate (GR) for each individual was calculated by the size it attained (SVL) at a certain age (given by time passed between birth and the last measuring event). For analysing mark-recapture data of the wild population, the von Bertalanffy logistic-by-length model (2) was used (Fabens 1965 ). We included literature data from the published literature as a parameter for size at birth (Marques et al 2013 ). Should an individual have more than one recapture event, all of them were considered, taking into account the time interval between them. (1) $${L}_{t}={L}_{\infty } (1-{e}^{-K*\left(t-t0\right)})$$ (2) $${L}_{r}={L}_{m}+\left({L}_{\infty }- {L}_{m}\right)(1-{e}^{-K*\varDelta t})$$ L t is the average length in age t , \({L}_{\infty }\) is the asymptotic average length, K is the growth rate coefficient, t 0 is the age when the average length is zero. \({L}_{r}\) is the length at recapture event, \({L}_{m}\) is the length at mark event and \(\varDelta t\) is the time interval between mark and recapture events. Growth rate for the wild population was calculated as the difference in SVL in mark-recapture events divided by the number of days between these events, and each individual was used only once, so that we had 19 observations for females, and 27 for males. For captive animals, instead of mark-recapture, each measurement event was considered as one observation, resulting in 65 observations for females, and 82 for males. Statistical Analyses Differences in SVL and growth rate between sexes and populations were assessed by performing two-way ANOVA, with sex, populations and interactions as fixed factors. ANCOVA was performed for analysing the relative body mass and relative growth rate between groups (captive males and females, and wild males and females), using SVL as a covariate. In case of the interaction being significant, the residuals from the regressions were then extracted and used in an ANOVA, with sex and population as fixed factors. Only data of adult Golden Lancehead were used in the morphological analyses (SVL and body mass), for avoiding biases due to ontogeny. Adulthood in the Golden Lancehead was inferred from SVL, based on data reported in the literature (Marques et al 2013 ; Passos 2018 ). Tukey analysis was used as a post-hoc test to determine the significance of pairwise comparisons between sexes and populations. For the morphometric analyses of SVL and body mass, we used samples of all the adult animals that were captured at QGI for which we had such data (n = 435), and samples of all captive-born adult individuals of LEEV (n = 31). Each animal was only used once, and whenever possible, the most recently measurements were considered. All analyses were performed in RStudio 4.0.2 (RStudio Team 2020), using the packages FSA (Ogle et al 2020 ), FSAdata (Ogle 2019 ), nlstools (Baty et al 2015 ), and plyr (Wickham 2011 ). Results Environmental data Mean temperature in captivity (x̅ = 23.7; range: 19 ‒ 29.8ºC) was higher than in natural habitat (x̅ = 22.6; range: 12.8 ‒ 38.3ºC; V = 206233; p < 0.05). The opposite happened to humidity, that was higher at QGI (x̅ = 86.1; range: 32.8 ‒ 100%) than in captivity (x̅ = 22.6; range: 28 ‒ 95.5%; V = 6579967; p < 0.05). Diet of wild animals Altogether, 106 fed animals were found. Birds represent around 90% of the diet, whereas ectotherms stand for the remaining 10%. It was possible to identify the prey at a specific level of 32 individuals of B. insularis (19 females and 13 males). Of this sample, ectotherms represent around 40% of the diet, whereas birds stand for the remaining 60% (Fig. 1 ). Considering the latter, prey ingested by B. insularis were mainly migratory birds of the species Elaenia chilensis (55%) and Turdus flavipes (25%). Considering the sexes separately, the only ectotherms found as prey of the females were anurans, and they represent around 30% of their diet, with the remaining 70% being make up of birds. Turdus flavipes , the larger bird species, were eaten exclusively by females. As for the males, ectotherms represent more than 45% of their diet, whereas usually small birds stand for the remaining 55%. Body Size Some of the animals of the present study attained larger size than the maximum previously reported for the species (females: SVL = 950, TL = 143, TBL = 1093 mm; males: SVL = 775, TL = 137, TBL = 912 mm; cf . Guimarães et al 2010 ; Table 1 ). The largest captive female showed 1250mm in TBL (SVL = 1050; TL = 155 mm; body mass = 556g), and the largest captive male was 945mm in TBL (SVL = 810mm; TL = 135mm; body mass = 227g). The largest female found during our expeditions at QGI was 1130mm in total length (SVL = 1005mm; TL = 125 mm; body mass = 240 g). Five captive-born females ranged from 1105 mm (SVL = 965, TL = 140 mm) to 1205 mm (SVL = 1050, TL = 155 mm) in TBL, and four captive-born males ranged between 920 mm (SVL = 780, TL = 140 mm) and 945 mm (SVL = 810, TL = 135 mm) in TBL. The captive females took a minimum of seven years, and the males, a minimum of six years to exceed the previous maximum size reported in literature. Table 1 Mean ± SD of snout-vent length (SVL), body mass (M) and growth rate (GR) of females and males of the wild and the captive population. SVL (mm) M (g) GR (mm.day − 1 ) WILD FEMALE 736.8 ± 74.4 196.2 ± 68.1 0.20 ± 0.16 MALE 591.8 ± 64.7 85.2 ± 32.2 0.07 ± 0.09 CAPTIVE FEMALE 921.25 ± 94.1 390.2 ± 157.2 0.21 ± 0.12 MALE 732.9 ± 60.0 146.0 ± 38.0 0.17 ± 0.16 Snout-vent length differed between sexes (F (1,796) = 140.986; P = 0.000; Fig. 2 ) and population (F (1,796) = 59.045; P = 0.000). The Tukey test revealed that captive females attain the largest SVL ( P < 0.001), while wild males were the smallest amongst all ( P = 0.000). Captive males were as large as wild females ( P = 0.470). Linear regression revealed a positive correlation between body mass and SVL (R² = 0.549; df = 724; P = 0.000). Therefore, the residuals of this regression were extracted and used in an ANOVA with sex and population as factors. A significant effect of the interaction sex*population on body mass was observed (F (1,722) = 27.990; P = 0.000). The post-hoc Tukey test revealed that captive females showed the highest relative body mass amongst all ( P = 0.000; Fig. 3 ). Wild females were relatively heavier than both wild ( P = 0.000) and captive males ( P = 0.002), and wild and captive males show similar relative body mass ( P = 0.382). Growth rates and curves Data reported herein comprises 78 growth intervals, 41 of them (ranging from 22 to 4639 days) obtained from the recapture of 35 wild females, and 37 growth intervals (ranging from 32 to 2714 days) from the recapture of 21 wild males of B. insularis . Concerning captive Golden Lanceheads, we used SVL of 15 females (ranging from 376 to 3612 days of life) and of 20 males (ranging from 8 to 3612 days). We found no significant association between growth rate and SVL increase (ANCOVA: F (1,223) = 0.377; P = 0.54). Therefore, we performed an ANOVA using sex and population as factors, which evinced that both factors affect GR (sex: F (1,221) = 7.577; P = 0.006; population: F (1,221) = 9.415; P = 0.002). Post-hoc tests reveal that wild males show the lowest growth rate amongst all (compared to captive females: P = 0.000; captive males: P = 0.009; and wild females: P = 0.020; Fig. 4 ). Asymptotic values show that females from QGI attain SVL up to about 850 mm, and the males, 600 mm (Fig. 5A). Growth curves of the captive animals suggest that females grow up to 1000 mm of SVL, and males, up to about 750 mm (Fig. 5B). Data from the literature show that minimum size at sexual maturity is 432 mm for males (Marques et al 2013 ) and 555 mm for females from QGI (Kasperoviczus 2009 ; Marques et al 2013 ), and 403 mm for males and 619 mm for females from captivity (Passos 2018 ). Based on such data, the growth curves suggest that captive females reach sexual maturity with about 3 years old, while captive males do so within less than one year. Wild females reach sexual maturity within 3.8 years, and the males, with 3.6 years old. Discussion In the present study, we provide the first estimate of GR for B. insularis . Additionally, we compare the GR of the wild population with that of the captive. Our first hypothesis was partially confirmed: wild animals indeed attain smaller body size and mass than captive individuals of the same sex. Our second hypothesis was also confirmed, as wild Golden Lancehead reach sexual maturation later, in comparison to captive individuals, possibly due to the fluctuations in food availability at QGI, following the premise that food input may influence maturation age (Ford and Seigel 1994 ). Also, following the pattern of animals which grow continuously and indefinitely throughout life (Shine and Charnov 1992 ), B. insularis showed a marked decrease in GR after maturation. Lastly, in our third hypothesis, we predicted that captive Golden Lancehead would show a higher GR in comparison to those from QGI. Nevertheless, only wild males showed lower GR. Snakes in QGI ‒ subject to lower temperatures than that of captivity ‒ were smaller and slighter, which was expected since warmer temperatures may be related to higher growth rate in snakes (Arnold and Peterson 1989 ; Gangloff et al 2015 ). Humidity was higher at QGI, but this variable does not seem to have direct effects on growth rate. It must be considered, however, that low humidity may be associated with dysecdysis whereas high humidity may cause dermatitis and lesions, especially in captive reptiles (Lillywhite and Gatten Jr. 1995; Oonincx and van Leeuwen 2017 ), what may ultimately compromise health conditions and growth in these animals. However, even though this scenario looks reasonable, we recognize that the lack of a meteorological station at the island may be an issue. A decrease of the GR is expected after sexual maturity, because both males and females need to mobilize energetic reserves for the development of structures and behaviours associated to reproduction, and such energy comes from food (Saint-Girons 1994 ). For viviparous female snakes, the reproduction involves high metabolic costs, especially during vitellogenesis, when mean metabolic costs represent about 30% of the total metabolic demand (Saint-Girons 1994 ; Van Dyke and Beaupre, 2011 ). Delayed maturation is often observed in the sex which experience higher reproductive costs (Shine 1994 ), which is evident when we analyse the growth curve of captive animals. Even though both males and females receive proportionally the same amount of food, in the same frequency, females take three times that which males take to reach maturity. By comparing the growth curves of both populations, it seems plausible that the delayed sexual maturity in B. insularis from QGI arises due a scarcity of resources. Apparently, the greater food input in captivity allows males to double their size and become sexually mature as one year old. Both in the wild and in captivity, females were the largest sex, confirming the marked sexual size dimorphism (SSD) reported for by B. insularis (Marques et al 2013 ), with females being larger than the males, like several other congeneric species (Valdujo et al 2002 ; Nogueira et al 2003 ; Hartmann et al 2004 ; Sasa et al 2009 ; Nunes et al 2010 ; Barros et al 2014 ; Leão et al 2014 ; Almeida-Santos et al 2017 ; Stuginski et al 2017 ; Silva et al 2017 ; Silva et al 2019 ; Silva et al 2020 ; Siqueira et al 2022 ). Body size may not represent an important reproductive constraint for the males, since their metabolic costs are lower than that of the females’. This is especially true for species in which males do not fight to access a female. In these species, SSD tend to be male-biased, with larger size of males being attained by prolonged growth after maturation (Shine 1994 ). Therefore, when there are no advantages arising from size, or even when the larger size may represent a disadvantage in resource partitioning, natural selection may favour smaller males (Madsen 1983 ). Because there is no apparent selective pressure for males to be larger, most of the energy obtained from food may be mobilized for reproductive purposes, instead of for growth. In reptiles, SSD may be the result of three main selective pressures: (1) sexual selection, (2) fecundity, and (3) reduction of intraspecific competition for prey (Cox et al 2007 ). Female-biased SSD in the Golden Lancehead seems to be influenced by the two latter. Because body size is an important constraint for females’ fecundity, it is expected that at QGI, GR in females is higher than that of males. Growth rate is influenced by variation in prey abundance, whether temporal or seasonally (Macartney et al 1990 ; Lindell and Forsman 2011 ). Avian prey, the main food item of adults’ diet, is limited and ephemeral at the island, so that this relative scarcity of resources could compromise GR of both males and females. It is possible that females, for having larger heads than males (Wüster et al 2005 ; Marques et al 2013 ), are able to feed on larger prey, balancing their great energetic expenditures on reproduction (Shine 1991 ), and attaining larger body size and mass, and higher GR. This morphological difference may also result in a reduction of intraspecific competition for prey. Bothrops insularis has an ontogenetic dietary shift, with juveniles feeding on ectothermic prey as anurans, lizards and centipedes, while the adults feed on birds (Marques et al 2002 ). Males have smaller heads and therefore perhaps depend on ectothermic prey for longer than females, as the size of their heads would be a restriction for hunting large birds that are prey with higher caloric value and that provide a higher growth rate. Accordingly, diet data sampled from fed snakes reveal that the larger birds ( T. flavipes ) are eaten exclusively by the females, whereas the males seem to rely on the smaller birds, such as Elaenia chilensis , or ectotherm prey, such as anurans, lizards and centipedes. Additionally, it is also interesting to notice that the relation prey mass x snake mass was usually higher for males than for females, showing that feeding on birds, may, indeed, impose a restriction, especially for the smaller males. It can be hypothesized that lower GR in males after sexual maturation is a consequence of constraints imposed by reproduction. Mate-searching may incur high energetic costs, with increased movement and activity of the males, as observed in many snake species ( e.g. Shine 2003 ; Jellen et al 2007 ; Glaudas and Rodríguez-Robles 2011 ; Bauder et al 2016 ). In snakes, fecundity is directly correlated to females’ size, and both the evolution of viviparity, and fecundity are associated with the selection for larger females (Fitch 1981 ; Shine 1994 ; Aubret et al 2002 ), as already evinced in B. insularis (Marques et al 2013 ). Therefore, larger body size in females may be favoured, resulting in greater litter size, increase in offspring, and females with better body condition after parturition (Hailey and Davies 1987 ; Ford and Seigel 1994 ; Madsen and Shine 1994 ; Shine and Madsen 1997 ). For having higher food intake, captive females are possibly able to store the energy as fat for future reproductive events (Shine 2003 ). It must also be considered that wild and captive animals feed on different kind of prey. While in the island the Golden Lancehead feed on birds, captive individuals feed on mice. Nutritional properties of these prey items are different, and may influence the energetic storage (Kremen et al 2013 ). Mean fecundity of B. insularis from QGI was estimated in 8.2 offspring per litter (range: 3–20; Marques et al 2013 ). Up to this moment, only five litters of the Golden Lancehead were born from the breeding among captive-born individuals. Fecundity (7.4 ± 3.65; range: 3–11; this study) was lower than that estimated for wild animals, which is intriguing, given that captive females are larger. It can be hypothesized that the larger body size of captive females is associated with increase in relative clutch mass ( e.g. Shine 2003 ). Unfortunately, we do not have data on body size and litter mass of B. insularis in the wild, so this could not be tested in the present study. In conclusion, our study provides evidence that body size, growth rate, and age of maturity in B. insularis is greatly influenced by food intake and costs of reproduction. Accordingly, the wild population show smaller body size and delayed maturity in comparison to the captive one. Likewise, females show delayed maturity when compared to males of the same population. Wild males show the lowest GR amongst all which may be a consequence of their smaller head that limits the ingestion of large prey. It is important to consider the effects of these differences. For the animals at QGI, slower growth and later maturation mainly in males may impact B. insularis of recovering from population declines (Blouin-Demers et al 2006 ). As for the captive ones, caution should be taken, considering that a negative correlation between fast growth and survival has already been evinced for snakes (Bronikowski and Arnold 1999 ; Rose et al 2021 ). Additionally, reptiles which are overfed (such as the captive ones, whose feeding frequency is higher than in the wild), may show rapid growth, obesity and secondary diseases (Pellett and Wissink-Argilaga 2015 ). Obesity may cause damage and even failure of the liver, ultimately leading a snake to death (Martins et al 2018 ). These aspects are especially important for conservation ex situ . Concerning species conservation, the impact of the larger body size in captive animals on other traits, such as habitat use, must be considered, especially if reintroduction of these animals become necessary. In this sense, a period in soft release methods would be crucial for better analysing such matters. As for the Golden Lanceheads in the island, it is mandatory that the conservation strategies encompass the maintenance of the population of the migratory birds, in order to ensure the energetic income to the snakes. Declarations Acknowledgements We would like to thank all the people who have greatly helped with data sampling in the field, especially Carlos Renato Azevedo, Cássia Domingos, Cássio Spercazechi, Diego Lorenzetto, Diego Muniz, Fausto Barbo, Fabiano Morezi, Juliana Medeiros, Kaline de Mello, Karina Kasperoviczus, Letícia Sueiro, Ligia Amorim, Luana Rosa, Maísa Matuoka, Marcio Martins, Mariana Guilardi, Natália Torello-Viera, Rafael Bovo, Ricardo Dias, Ricardo Sawaya, Rodrigo Castello, Silara Batista, Thiago Estimo, Valdir Germano, Vinicius Correia, and Wilian Borges. We would also like to thank Adriano Felone, Kelly Kishi, and Selma M. Almeida-Santos for providing access to the data from the captive population. Author’s Contribution KRSB and LHCS conceived the ideas and designed methodology; KRSB and LHCS collected and analysed the data; KRSB led the writing of the manuscript. OAV supervised the study. All authors contributed to the drafts and gave final approval for publication. Funding This work was supported by Fundação de Amparo à Pesquisa do Estado de São Paulo (Grants FAPESP #2012/07334-9, #2018/07507-7, and 2020/12658-4). Conflicts of interest The authors declare no conflicts of interest. Ethics approval This study was authorized by the Ethic Commission for Animal Usage of Instituto Butantan (certificates CEUAIB #983-12 and #1543170518), the Brazilian Ministry of the Environment (SISBIO #6295-7 and 16119), and the Brazilian Instituto of Environment and Renewable Natural Resources (IBAMA nº 25.650-1). References Alencar LRV, Quental TB, Grazziotin FG et al (2016) Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates. Mol Phylogenet Evol 105:50–62 Alencar LRV, Martins M, Burin G et al (2017) Arboreality constrains morphological evolution but not species diversification in vipers. Proc R Soc Lond B Biol Sci 284:20171775 Almeida-Santos SM, Barros VA, Rojas CA et al (2017) Reproductive biology of the Brazilian Lancehead, Bothrops moojeni (Serpentes, Viperidae), from the State of São Paulo, Southeastern Brazil. South Am J Herpetol 12:174–181 Amaral A (1921) Contribuição para o conhecimento dos Ofídios do Brasil. Mem Inst Butantan I:6–108 Angilletta MJ, Steury TD, Sears MW (2004) Temperature, Growth Rate, and Body Size in Ectotherms: Fitting Pieces of a Life-History Puzzle. Integr Comp Biol 44:498–509 Arnold SJ, Peterson CR (1989) A Test for Temperature Effects on the Ontogeny of Shape in the Garter Snake Thamnophis sirtalis . Physiol Zool 62:1316–1333 Aubret F, Bonnet X, Shine R et al (2002) Fat is sexy for females but not males: The influence of body reserves on reproduction in snakes ( Vipera aspis ). Horm Behav 42:135–147 Barros VA, Rojas CA, Almeida-Santos SM (2014) Reproductive Biology of Bothrops erythromelas from the Brazilian Caatinga. Adv Zool 2014:1–11 Baty F, Ritz C, Charles S et al (2015) A Toolbox for Nonlinear Regression in R: The Package nlstools. J Stat Softw 66:1–21 Bauder JM, Breininger DR, Bolt MR et al (2016) Seasonal variation in eastern Indigo Snake ( Drymarchon couperi ) movement patterns and space use in Peninsular Florida at multiple temporal scales. Herpetologica 72:214–226 Blouin-Demers G, Prior KA, Weatherhead PJ (2006) Comparative demography of black rat snakes ( Elaphe obsoleta ) in Ontario and Maryland. J Zool 256:1–10 Bonnet X, Naulleau G (1996) Are body reserves important for reproduction in male dark green snakes (Colubridae: Coluber viridiflavus )? Herpetologica 52:137–146 Bovo RP, Marques OAV, Andrade DV (2012) When Basking Is Not an Option: Thermoregulation of a Viperid Snake Endemic to a Small Island in the South Atlantic of Brazil. Copeia 2012:408–418 Bronikowski AM, Arnold SJ (1999) The evolutionary ecology of life history variation in the garter snake Thamnophis elegans . Ecology 80:2314–2325 Cox RM, Butler MA, John-Alder HB (2007) The evolution of sexual size dimorphism in reptiles. In: Fairbairn DJ, Blanckenhorn WU, Székely T (eds) Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press, Oxford, pp 38–49 Fabens AJ (1965) Properties and fitting of the von Bertalanffy growth curve. Growth 29:265–289 Fitch HS (1981) Sexual Size Differences in Reptiles. Sci Pap Univ Kans Nat Hist Mus 70:1–72 Ford NB, Seigel RA (1994) An Experimental Study of the Trade-Offs Between Age and Size at Maturity: Effects of Energy Availability. Funct Ecol 8:91–96 Gangloff EJ, Vleck D, Bronikowski AM (2015) Developmental and Immediate Thermal Environments Shape Energetic Trade-Offs, Growth Efficiency, and Metabolic Rate in Divergent Life-History Ecotypes of the Garter Snake Thamnophis elegans . Physiol Biochem Zool 88:550–563 Glaudas X, Rodríguez-Robles JA (2011) Vagabond males and sedentary females: spatial ecology and mating system of the Speckled Rattlesnake ( Crotalus mitchellii ). Biol J Linn Soc Lond 103:681–695 Guimarães MR, Bovo RP, Kasperoviczus KN et al (2010) Bothrops insularis (Golden Lancehead). Maximum length. Herpetol Rev 41:89 Hailey A, Davies PMC (1987) Maturity, mating and age-specific reproductive effort of the snake Natrix maura . J Zool 211:573–587 Hariharan IK, Wake DB, Wake MH (2015) Indeterminate Growth: Could It Represent the Ancestral Condition? Cold Spring Harb Perspect Biol 8:a019174 Hartmann MT, Marques OAV, Almeida-Santos SM (2004) Reproductive biology of the southern Brazilian pitviper Bothrops neuwiedi pubescens (Serpentes, Viperidae). Amphib Reptil 25:77–85 Jellen BC, Shepard DB, Dreslik MJ et al (2007) Male Movement and Body Size Affect Mate Acquisition in the Eastern Massasauga ( Sistrurus catenatus ). J Herpetol 41:451–457 Kasperoviczus KN (2009) Biologia reprodutiva da jararaca ilhoa, Bothrops insularis , (Serpentes: Viperidae) da Ilha da Queimada Grande, São Paulo. Thesis, Universidade de São Paulo Kremen NA, Calvert CC, Larsen JA et al (2013) Body composition and amino acid concentrations of select birds and mammals consumed by cats in northern and central California. J Anim Sci 91:1270–1276 Leão SM, Pelegrin N, Nogueira CC et al (2014) Natural history of Bothrops itapetiningae Boulenger, 1907 (Serpentes: Viperidae: Crotalinae), an endemic species of the Brazilian Cerrado. J Herpetol 48:324–331 Lillywhite HB (2014) How snakes work. Structure, function and behavior of the world’s snakes. Oxford University Press, Oxford Lillywhite HB, Gatten RE Jr (2023) Physiology and functional anatomy. In: Warwick C, Frye FL, Murphy JB (eds) Health and Welfare of Captive Reptiles. Chapman & Hall, London, pp 5–31 Lindell LE, Forsman A (2011) Density effects and snake predation: Prey limitation and reduced growth rate of adders at high density of conspecifics. Can J Zool 74:1000–1007 Macartney JM, Gregory PT, Charland MB (1990) Growth and Sexual Maturity of the Western Rattlesnake, Crotalus viridis , in British Columbia. Copeia 1990:528–542 Madsen T (1983) Growth Rates, Maturation and Sexual Size Dimorphism in a Population of Grass Snakes, Natrix natrix , in Southern Sweden. Oikos 40:277–282 Madsen T, Shine R (1994) Phenotypic Plasticity in Body Sizes and Sexual Size Dimorphism in European Grass Snakes. Evolution 48:1389–1397 Madsen T, Shine R (2000) Silver spoons and snake body sizes prey availability early in life influences long-term growth rates of free‐ranging pythons. J Anim Ecol 69:952–958 Marinho AF (2022) Aspectos ecológicos da lagartixa exótica Hemidactylus mabouia Moreau de Jonnès, 1818 (Gekkonidae) na Restinga de Itacoatiara, Niterói, RJ. Thesis, Universidade Federal Fluminense Marques OAV, Martins M, Sazima I (2002) A new insular species of pitviper from Brazil, with comments on evolutionary biology and conservation of the Bothrops jararaca group (Serpentes, Viperidae). Herpetologica 58:303–312 Marques OAV, Martins M, Develey PF et al (2012) The Golden Lancehead Bothrops insularis (Serpentes: Viperidae) relies on two seasonally plentiful bird species visiting its island habitat. J Nat Hist 46:885–895 Marques OAV, Kasperoviczus K, Almeida-Santos SM (2013) Reproductive ecology of the threatened Pitviper Bothrops insularis from Queimada Grande Island, Southeast Brazil. J Herpetol 47:393–399 Martins M, Marques OAV, Sazima I (2002) Ecological and Phylogenetic Correlates of Feeding Habits in Neotropical Pitvipers of the Genus Bothrops . In: Schuett GW, Hoggren M, Douglas ME et al (eds) Biology of the vipers. Eagle Mountain Publishing, Utah, pp 1–22 Martins NB, Ferreira LAR, Silva TSG et al (2018) Hepatic Lipidosis Due to Obesity in a Free-Living Snake ( Boa constrictor amarali ). Acta Sci Vet 46:265 McGehee SM, Hamilton P, Beatty B et al (2012) Seasonal Body Mass Changes in Six Forest Passerines of Southern Chile. Ornitol Neotrop 23:25–34 Nogueira C, Sawaya RJ, Martins M (2003) Ecology of the Pitviper, Bothrops moojeni , in the Brazilian Cerrado. J Herpetol 37:653–659 Nunes SF, Kaefer IL, Leite PT et al (2010) Reproductive and feeding biology of the pitviper Rhinocerophis alternatus from subtropical Brazil. Herpetol J 20:31–39 Ogle DH (2019) FSAdata: Fisheries Stock Analysis, Datasets. CRAN. R package version 0.3.8 Ogle DH, Wheeler P, Dinno A (2020) FSA: Fisheries Stock Analysis. CRAN. R package version 0.8.30 Oonincx D, van Leeuwen J (2017) Evidence-Based Reptile Housing and Nutrition. Vet Clin Exot Anim 20:885–898 Passos J (2018) Influência no crescimento de Bothrops insularis e Bothrops jararaca : a dieta pode interferir no tamanho da maturidade sexual em cativeiro? Thesis, Universidade de São Paulo Pellett S, Wissink-Argilaga N (2015) Nutrition — lizards and snakes. Companion Anim 20:362–366 Plummer MV (1985) Growth and maturity in green snake ( Opheodrys aestivus ). Herpetologica 41:28–33 R Core Team (2022) R: A Language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria Rose JP, Kim R, Schoenig EJ et al (2021) Integrating growth and survival models for flexible estimation of size-dependent survival in a cryptic, endangered snake. Ecol Evol 12:e8799 Saint-Girons H (1994) Growth & Reproduction. In: Bauchot R (ed) Snakes: A Natural History. Sterling Publishing Co. Inc, New York, pp 92–107 Salles-Oliveira I, Machado T, Banci KRS et al (2020) Genetic variability, management, and conservation implications of the critically endangered Brazilian pitviper Bothrops insularis . Ecol Evol 10:12870–12882 Santos MA (2018) Relações de tamanho, massa e dieta no nicho alimentar em uma comunidade de anuros na Mata Atlântica. Dissertation, Universidade do Estado do Rio de Janeiro Sasa M, Wasko DK, Lamar WW (2009) Natural history of the terciopelo Bothrops asper (Serpentes: Viperidae) in Costa Rica. Toxicon 54:904–922 Shine R (1991) Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. Am Nat 138:103–122 Shine R (1994) Sexual Size Dimorphism in Snakes Revisited. Copeia 1994:326–346 Shine R (2003) Reproductive strategies in snakes. Proc R Soc Lond B Biol Sci 270:995–1004 Shine R, Charnov EL (1992) Patterns of survival, growth, and maturation in snakes and lizards. Am Nat 139:1257–1269 Shine R, Madsen T (1997) Prey abundance and predator reproduction: Rats and pythons on a tropical Australian floodplain. Ecology 78:1078–1086 Sick H (1984) Ornitologia Brasileira, uma Introdução. Editora Universidade de Brasília, Brasília Silva FM, Oliveira LS, Nascimento LRS et al (2017) Sexual dimorphism and ontogenetic changes of Amazonian pit vipers ( Bothrops atrox ). Zool Anz 271:15–24 Silva KMP, Braz HB, Kasperoviczus KN et al (2020) Reproduction in the pitviper Bothrops jararacussu : large females increase their reproductive output while small males increase their potential to mate. Zoology 142:125816 Silva KMP, Silva KB, Sueiro LR et al (2019) Reproductive Biology of Bothrops atrox (Serpentes, Viperidae, Crotalinae) from the Brazilian Amazon. Herpetologica 75:198–207 Silveira AL, Prudente ALC, Argôlo AJS et al (2021) Bothrops insularis . The IUCN Red List of Threatened Species 2021:e.T2917A123180264 Siqueira LHC, Piantoni C, MARQUES OAV (2022) Morphological variation in the common lancehead populations: Sexual dimorphism and ontogenetic patterns. J Zool 318:283–296 Stuginski DR, Mendes GF, Sant’Anna SS et al (2017) Sexual Differences in Growth Rates of Juveniles from a Litter of Bothrops fonsecai : The Role of Feeding Conversion in a Female-Biased SSD Species. South Am J Herpetol 12:193–199 Valdujo PH, Nogueira C, Martins M (2002) Ecology of Bothrops neuwiedi pauloensis (Serpentes: Viperidae: Crotalinae) in the Brazilian Cerrado. J Herpetol 36:169–176 Van Dyke JU, Beaupre SJ (2011) Bioenergetic components of reproductive effort in viviparous snakes: Costs of vitellogenesis exceed costs of pregnancy. Comp Biochem Physiol Mol Integr Physiol 160:504–515 Van Dyke JU, Beaupre SJ, Kreider DL (2012) Snakes allocate amino acids acquired during vitellogenesis to offspring: Are capital and income breeding consequences of variable foraging success? Biol J Linn Soc Lond 106:390–404 Wickham H (2011) The Split-Apply-Combine Strategy for Data Analysis. J Stat Softw 40:1–29 WikiAves (2024) WikiAves, a Enciclopédia das Aves do Brasil. http://www.wikiaves.com.br/ , accessed in: 03/20/2024 Wüster W, Duarte MR, Salomão MG (2005) Morphological correlates of incipient arboreality and ornithophagy in island pitvipers, and the phylogenetic position of Bothrops insularis . J Zool 266:1–10 Additional Declarations No competing interests reported. Cite Share Download PDF Status: Posted Version 1 posted You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. As a division of Research Square Company, we’re committed to making research communication faster, fairer, and more useful. We do this by developing innovative software and high quality services for the global research community. Our growing team is made up of researchers and industry professionals working together to solve the most critical problems facing scientific publishing. Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-4607766","acceptedTermsAndConditions":true,"allowDirectSubmit":true,"archivedVersions":[],"articleType":"Research Article","associatedPublications":[],"authors":[{"id":323551725,"identity":"e2abe910-a272-473c-9d26-044570840307","order_by":0,"name":"Karina Rodrigues Silva Banci","email":"data:image/png;base64,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","orcid":"","institution":"Instituto Butantan","correspondingAuthor":true,"prefix":"","firstName":"Karina","middleName":"Rodrigues Silva","lastName":"Banci","suffix":""},{"id":323551726,"identity":"28a036f0-fcf1-43a1-a7d4-790e0fccc03f","order_by":1,"name":"Lucas Henrique Carvalho Siqueira","email":"","orcid":"","institution":"Instituto Butantan","correspondingAuthor":false,"prefix":"","firstName":"Lucas","middleName":"Henrique Carvalho","lastName":"Siqueira","suffix":""},{"id":323551727,"identity":"913afb93-5da9-4a06-abaa-3a9aa8efa061","order_by":2,"name":"Otavio Augusto Vuolo Marques","email":"","orcid":"","institution":"Instituto Butantan","correspondingAuthor":false,"prefix":"","firstName":"Otavio","middleName":"Augusto Vuolo","lastName":"Marques","suffix":""}],"badges":[],"createdAt":"2024-06-19 19:38:18","currentVersionCode":1,"declarations":"","doi":"10.21203/rs.3.rs-4607766/v1","doiUrl":"https://doi.org/10.21203/rs.3.rs-4607766/v1","draftVersion":[],"editorialEvents":[],"editorialNote":"","failedWorkflow":false,"files":[{"id":60615535,"identity":"3c531ff6-13df-42f3-80f2-97d1c8525964","added_by":"auto","created_at":"2024-07-18 20:13:15","extension":"jpeg","order_by":1,"title":"Figure 1","display":"","copyAsset":false,"role":"figure","size":170244,"visible":true,"origin":"","legend":"\u003cp\u003eBox-plot showing variation in snout-vent length in \u003cem\u003eBothrops insularis\u003c/em\u003efrom the island (females: IQG F; males: IQG M) and captivity (females: CAPTIVE F; males: CAPTIVE M)\u003cem\u003e.\u003c/em\u003e\u003c/p\u003e","description":"","filename":"floatimage1.jpeg","url":"https://assets-eu.researchsquare.com/files/rs-4607766/v1/b819c66a023128e9396f6fd4.jpeg"},{"id":60614774,"identity":"4981189f-e5cf-4109-8ec1-5239c1a1d4b3","added_by":"auto","created_at":"2024-07-18 20:05:14","extension":"jpeg","order_by":2,"title":"Figure 2","display":"","copyAsset":false,"role":"figure","size":171296,"visible":true,"origin":"","legend":"\u003cp\u003eBox-plot showing the relative body mass in \u003cem\u003eBothrops insularis\u003c/em\u003e from the island (females: IQG F; males: IQG M) and captivity (females: CAPTIVE F; males: CAPTIVE M)\u003cem\u003e.\u003c/em\u003e\u003c/p\u003e","description":"","filename":"floatimage2.jpeg","url":"https://assets-eu.researchsquare.com/files/rs-4607766/v1/cb98ac3f1da8b69a5569533f.jpeg"},{"id":60614775,"identity":"3dd97bca-68b2-47fc-ba2f-df33a3cbd615","added_by":"auto","created_at":"2024-07-18 20:05:15","extension":"jpeg","order_by":3,"title":"Figure 3","display":"","copyAsset":false,"role":"figure","size":167183,"visible":true,"origin":"","legend":"\u003cp\u003eGrowth rate of wild (A) and captive (B) females and males of \u003cem\u003eBothrops insularis\u003c/em\u003e, expressed in millimetres per day\u003cem\u003e.\u003c/em\u003e\u003c/p\u003e","description":"","filename":"floatimage3.jpeg","url":"https://assets-eu.researchsquare.com/files/rs-4607766/v1/704e992bbfe97e1b6b7c59ef.jpeg"},{"id":60614773,"identity":"41ae3a54-d0be-4512-b792-c39f492fa384","added_by":"auto","created_at":"2024-07-18 20:05:14","extension":"jpeg","order_by":4,"title":"Figure 4","display":"","copyAsset":false,"role":"figure","size":297270,"visible":true,"origin":"","legend":"\u003cp\u003eGrowth curves of captive (A) and wild (B) males and females of \u003cem\u003eBothrops insularis\u003c/em\u003e. The intersection of the segments with the x-axis correspond to age of sexual maturity, and that with the y-axis corresponds to size of sexual maturity reported in the literature (see text).\u003c/p\u003e","description":"","filename":"floatimage4.jpeg","url":"https://assets-eu.researchsquare.com/files/rs-4607766/v1/29f82453467a06e1367a1d03.jpeg"},{"id":70235353,"identity":"c7680b4d-cc34-4381-8ea3-f63474814024","added_by":"auto","created_at":"2024-11-30 04:31:37","extension":"pdf","order_by":0,"title":"","display":"","copyAsset":false,"role":"manuscript-pdf","size":1286202,"visible":true,"origin":"","legend":"","description":"","filename":"manuscript.pdf","url":"https://assets-eu.researchsquare.com/files/rs-4607766/v1/3d54c543-d46b-4c2f-b234-ede4781ac27d.pdf"}],"financialInterests":"No competing interests reported.","formattedTitle":"Growth patterns of the Golden Lancehead and their determinants: Conservation strategies for critically endangered species","fulltext":[{"header":"Introduction","content":"\u003cp\u003eAs with most ectothermic vertebrates, snakes show continuous and indeterminate growth throughout life (Shine and Charnov \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e1992\u003c/span\u003e; Saint-Girons \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e1994\u003c/span\u003e, Hariharan et al \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Growth rate relies on several factors, such as genetic traits, availability of resources (such as food and water), climatic conditions, and success of capturing and digesting prey (Macartney et al \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e1990\u003c/span\u003e; Saint-Girons \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Lillywhite \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Hariharan et al \u003cspan citationid=\"CR23\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). It also varies according to age, so that snakes usually grow faster early in life, with growth rate decreasing after sexual maturation, closely following an asymptotic pattern (Shine and Charnov \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e1992\u003c/span\u003e; Lillywhite \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2014\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe reason why growth rate decreases after attaining sexual maturity is that the energy which was previously mobilized for growing starts being directed to the development of the structures and behaviours associated with reproduction (Lillywhite \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2014\u003c/span\u003e). For males, it involves the development of the testicles and hypertrophy of the annex glands such as the epididymis and the sexual segment of the kidneys (Saint-Girons \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e1994\u003c/span\u003e). As for the females, a great energy intake is necessary for the vitellogenesis to occur previously to ovulation, and this process is so bioenergetically expensive that the costs may outweigh those of pregnancy itself (Saint-Girons \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Van Dyke and Beaupre \u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). For these processes, snakes may allocate either stored reserves (the so-called capital breeders), or energy obtained from recently-ingested food (the income breeders; Van Dyke et al \u003cspan citationid=\"CR71\" class=\"CitationRef\"\u003e2012\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eAmong ectotherms, there is also the so-called temperature-size rule, being that lower temperatures cause these animals to grow slower but mature at a larger body size (Angilletta et al \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e2004\u003c/span\u003e). This rule is verified in individuals of \u003cem\u003eThamnophis sirtalis\u003c/em\u003e and \u003cem\u003eT. elegans\u003c/em\u003e which grow faster in warmer temperatures (Arnold and Peterson \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e1989\u003c/span\u003e; Bronikowski 2000; Gangloff et al \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). On the other hand, this pattern was not observed in another species from temperate locality, \u003cem\u003eVipera aspis\u003c/em\u003e (Michel and Bonnet 2010). Nevertheless, knowledge on growth rate and pattern of snakes in warm climates is still scarce, especially for neotropical species.\u003c/p\u003e \u003cp\u003eThe Golden Lancehead \u003cem\u003eBothrops insularis\u003c/em\u003e is a viviparous species of the \u003cem\u003eBothrops jararaca\u003c/em\u003e complex (Alencar et al \u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). It is one of the most arboreal species of the genus, and shows morphological differences when compared to congeneric species (Amaral \u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e1921\u003c/span\u003e; Martins et al \u003cspan citationid=\"CR40\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; W\u0026uuml;ster et al \u003cspan citationid=\"CR74\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Marques 2021). Similarly to other \u003cem\u003eBothrops\u003c/em\u003e species, females are larger than males (Marques et al \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). The Golden Lancehead is endemic to Queimada Grande Island (QGI, S\u0026atilde;o Paulo, Brazil), and is classified as a critically endangered species due to its endemism and restrict distribution, with habitat damaged by past fires, and populational decrease mainly attributed to biopiracy (Martins et al 2008; Guimar\u0026atilde;es et al 2014; Silveira et al 2023).\u003c/p\u003e \u003cp\u003eFor this reason, the International Union for Conservation of Nature (IUCN) recommends the establishment of captive populations in order to ensure the species\u0026rsquo; \u003cem\u003eex-situ\u003c/em\u003e conservation. Therefore, the Laborat\u0026oacute;rio de Ecologia e Evolu\u0026ccedil;\u0026atilde;o (LEEV) of Instituto Butantan has housed a captive population of \u003cem\u003eBothrops insularis\u003c/em\u003e since 2009. As mentioned above, food availability affects growth rate, and prey can be a limited and ephemeral resource for island snakes (Lillywhite \u003cspan citationid=\"CR29\" class=\"CitationRef\"\u003e2014\u003c/span\u003e), such as \u003cem\u003eB. insularis\u003c/em\u003e. Wild specimens of Golden Lancehead feeds mainly on migratory birds, namely the Tyrant \u003cem\u003eElaenia chilensis\u003c/em\u003e, that visits the island in mid-March, and the Yellow-legged Thrush (\u003cem\u003eTurdus flavipes\u003c/em\u003e), which visits the island in mid-July, a resource that varies seasonally and from year to year (Marques et al \u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2012\u003c/span\u003e, \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). The captive individuals, however, receive water and food (mice) regularly throughout the year.\u003c/p\u003e \u003cp\u003eFood intake influences snakes\u0026rsquo; growth, so that scarcity of prey lead to decreased growth rate (Lindell and Forsman \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2011\u003c/span\u003e), and supplementation of prey may cause snakes to be larger (Ford and Seigel \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e1994\u003c/span\u003e). Likewise, food intake may influence reproductive traits, causing females to show early maturation or even causing the number of reproductive females in \u0026ldquo;good\u0026rdquo; years of food availability to outnumber that of when prey was scarce (\u003cem\u003ee.g.\u003c/em\u003e Ford and Seigel \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Shine and Madsen \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e1997\u003c/span\u003e). Such influences are even more pronounced when this higher food supply happens in the first years of life, causing a \u0026ldquo;silver spoon effect\u0026rdquo; (Ford and Seigel \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Madsen and Shine \u003cspan citationid=\"CR35\" class=\"CitationRef\"\u003e2000\u003c/span\u003e). Also, growth patterns differ between sexes in sexually dimorphic species (Madsen \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e1983\u003c/span\u003e; Plummer \u003cspan citationid=\"CR50\" class=\"CitationRef\"\u003e1985\u003c/span\u003e). Considering the differences in resources availability to which the wild and the captive populations of \u003cem\u003eB. insularis\u003c/em\u003e are submitted, the aim of the present work is to test the following hypotheses: (1) wild animals attain smaller size and mass than the captive ones; (2) sexual maturity (inferred by the animals\u0026rsquo; SVL, based on Marques et al \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e, and Passos \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2018\u003c/span\u003e) of wild animals is reached later in comparison to that of captive ones; and (3) growth rate is lower in wild individuals. Because growth rate may be also related with climate regimen, we also tested for differences in temperature and humidity between both localities.\u003c/p\u003e"},{"header":"Methods","content":"\u003cdiv id=\"Sec3\" class=\"Section2\"\u003e \u003ch2\u003eData Collection\u003c/h2\u003e \u003cp\u003eCaptive individuals are housed at Laborat\u0026oacute;rio de Ecologia e Evolu\u0026ccedil;\u0026atilde;o, Instituto Butantan. They are kept in boxes individually, in a room with an average temperature with an average around 24\u0026ordm;C all year-round, average humidity around 23%, and photoperiod of 12:12h, with light phase from 6 a.m. to 6 p.m. The animals are monthly fed on mice, representing 20% of their body mass, and they are annually measured and weighed. The captive population is now made up of three generations. We only used morphometric data from the two generations which were born in the laboratory, in order to avoid bias arising from the animals having lived a part of their lives in the island. In this sense, we used data from 15 females, and 20 males, that were from one to ten years old.\u003c/p\u003e \u003cp\u003eFor the wild population, growth data were gathered from mark and recapture events of animals in the field. The identification of Golden Lanceheads from Queimada Grande Island (QGI) with 12mm passive integrated transponder (PIT) tags is a routine procedure during our expeditions, and made it possible for us to recapture some of the animals (general recapture rate is around 13%; present study). These data were obtained during sampling trips from 2004 to 2023, comprising 35 females and 37 males (which corresponds to a recapture rate of 8%, after filtering for complete records), and included recaptures ranging from 3 months up to almost 8 years after capture. Diet of wild snakes was inferred from data collected in the study by Marques et al (\u003cspan citationid=\"CR38\" class=\"CitationRef\"\u003e2012\u003c/span\u003e) added to information obtained on expeditions before or after this study mainly from palpation of fed animals found on QGI. Prey types were identified at the most specific taxonomic level as possible, and ranked according to their body mass (\u003cem\u003ecf.\u003c/em\u003e Sick \u003cspan citationid=\"CR62\" class=\"CitationRef\"\u003e1984\u003c/span\u003e; Santos \u003cspan citationid=\"CR55\" class=\"CitationRef\"\u003e2018\u003c/span\u003e; Marinho \u003cspan citationid=\"CR36\" class=\"CitationRef\"\u003e2022\u003c/span\u003e; McGehee et al 2023, WikiAves \u003cspan citationid=\"CR73\" class=\"CitationRef\"\u003e2024\u003c/span\u003e, pers. obs.). Identified prey were then associated with the snout-vent length (SVL) and gender of the individuals of \u003cem\u003eB. insularis\u003c/em\u003e which had fed on them, in order to evaluate dietary patterns in different sexes and size classes.\u003c/p\u003e \u003cp\u003eFor growth and body size analyses, we used data of 35 captive and of 710 wild individuals (395 females and 315 males) encountered at QGI from 2004 to 2023. The morphometric data utilized were: (1) snout-vent length (SVL), measured from the tip of the nose to the cloaca; (2) tail length (TL), measured from the cloaca to the end of the tail, using a measuring tape with accuracy of 1 mm; (3) total body length (TBL; calculated by SVL\u0026thinsp;+\u0026thinsp;TL); and (4) body mass, weighted using precision dynamometers (in the island; precision of 1 g) or precision scale (in the laboratory, precision of 0.1 g). In case of an individual being recaptured more than once in each field expedition, only the first biometric data were considered.\u003c/p\u003e \u003cp\u003eDaily air temperature and humidity were collected in captivity using a thermohygrometer. Unfortunately, we lacked a meteorological station at QGI. Therefore, we considered data measured in the closest meteorological stations available: Itanha\u0026eacute;m Municipality (from 2010 to 2016), and Bertioga Municipality (about 110 km away; from 2017 to 2020). Such data were provided by Instituto Nacional de Meteorologia (INMET, 2022). Previous analyses showed that these data were not normally-distributed, even after being log-transformed. Therefore, they were analysed using Paired Wilcoxon Test, using RStudio 2022.12.0 and The R Stats Package (R Core Team, \u003cspan citationid=\"CR51\" class=\"CitationRef\"\u003e2022\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec4\" class=\"Section2\"\u003e \u003ch2\u003eGrowth models and rates\u003c/h2\u003e \u003cp\u003eTwo different methods were used, one for investigating growth of wild individuals, and another, for captive individuals, due to kind of data gathered for each population. In this sense, once we knew the birth date of all 35 individuals, we used the von Bertalanffy Typical model (1; von Bertalanffy 1938). Data for each sex was also analysed separately. Growth rate (GR) for each individual was calculated by the size it attained (SVL) at a certain age (given by time passed between birth and the last measuring event).\u003c/p\u003e \u003cp\u003eFor analysing mark-recapture data of the wild population, the von Bertalanffy logistic-by-length model (2) was used (Fabens \u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e1965\u003c/span\u003e). We included literature data from the published literature as a parameter for size at birth (Marques et al \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). Should an individual have more than one recapture event, all of them were considered, taking into account the time interval between them.\u003c/p\u003e \u003c/div\u003e\n\u003ch3\u003e(1)\u003c/h3\u003e\n\u003cp\u003e \u003cdiv id=\"Equa\" class=\"Equation\"\u003e \u003cdiv format=\"TEX\" class=\"mathdisplay\" id=\"FileID_Equa\" name=\"EquationSource\"\u003e\n$${L}_{t}={L}_{\\infty } (1-{e}^{-K*\\left(t-t0\\right)})$$\u003c/div\u003e \u003c/div\u003e \u003c/p\u003e\n\u003ch3\u003e(2)\u003c/h3\u003e\n\u003cp\u003e \u003cdiv id=\"Equb\" class=\"Equation\"\u003e \u003cdiv format=\"TEX\" class=\"mathdisplay\" id=\"FileID_Equb\" name=\"EquationSource\"\u003e\n$${L}_{r}={L}_{m}+\\left({L}_{\\infty }- {L}_{m}\\right)(1-{e}^{-K*\\varDelta t})$$\u003c/div\u003e \u003c/div\u003e \u003c/p\u003e \u003cp\u003e \u003cem\u003eL\u003c/em\u003e \u003csub\u003e \u003cem\u003et\u003c/em\u003e \u003c/sub\u003e is the average length in age \u003cem\u003et\u003c/em\u003e, \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\({L}_{\\infty }\\)\u003c/span\u003e\u003c/span\u003e is the asymptotic average length, \u003cem\u003eK\u003c/em\u003e is the growth rate coefficient, \u003cem\u003et\u003c/em\u003e\u003csub\u003e\u003cem\u003e0\u003c/em\u003e\u003c/sub\u003e is the age when the average length is zero. \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\({L}_{r}\\)\u003c/span\u003e\u003c/span\u003e is the length at recapture event, \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\({L}_{m}\\)\u003c/span\u003e\u003c/span\u003e is the length at mark event and \u003cspan class=\"InlineEquation\"\u003e\u003cspan class=\"mathinline\"\u003e\\(\\varDelta t\\)\u003c/span\u003e\u003c/span\u003e is the time interval between mark and recapture events.\u003c/p\u003e \u003cp\u003eGrowth rate for the wild population was calculated as the difference in SVL in mark-recapture events divided by the number of days between these events, and each individual was used only once, so that we had 19 observations for females, and 27 for males. For captive animals, instead of mark-recapture, each measurement event was considered as one observation, resulting in 65 observations for females, and 82 for males.\u003c/p\u003e \u003cdiv id=\"Sec7\" class=\"Section2\"\u003e \u003ch2\u003eStatistical Analyses\u003c/h2\u003e \u003cp\u003eDifferences in SVL and growth rate between sexes and populations were assessed by performing two-way ANOVA, with sex, populations and interactions as fixed factors. ANCOVA was performed for analysing the relative body mass and relative growth rate between groups (captive males and females, and wild males and females), using SVL as a covariate. In case of the interaction being significant, the residuals from the regressions were then extracted and used in an ANOVA, with sex and population as fixed factors. Only data of adult Golden Lancehead were used in the morphological analyses (SVL and body mass), for avoiding biases due to ontogeny. Adulthood in the Golden Lancehead was inferred from SVL, based on data reported in the literature (Marques et al \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e; Passos \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Tukey analysis was used as a post-hoc test to determine the significance of pairwise comparisons between sexes and populations.\u003c/p\u003e \u003cp\u003eFor the morphometric analyses of SVL and body mass, we used samples of all the adult animals that were captured at QGI for which we had such data (n\u0026thinsp;=\u0026thinsp;435), and samples of all captive-born adult individuals of LEEV (n\u0026thinsp;=\u0026thinsp;31). Each animal was only used once, and whenever possible, the most recently measurements were considered.\u003c/p\u003e \u003cp\u003eAll analyses were performed in RStudio 4.0.2 (RStudio Team 2020), using the packages FSA (Ogle et al \u003cspan citationid=\"CR46\" class=\"CitationRef\"\u003e2020\u003c/span\u003e), FSAdata (Ogle \u003cspan citationid=\"CR45\" class=\"CitationRef\"\u003e2019\u003c/span\u003e), nlstools (Baty et al \u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e2015\u003c/span\u003e), and plyr (Wickham \u003cspan citationid=\"CR72\" class=\"CitationRef\"\u003e2011\u003c/span\u003e).\u003c/p\u003e \u003c/div\u003e"},{"header":"Results","content":"\u003cdiv id=\"Sec9\" class=\"Section2\"\u003e \u003ch2\u003eEnvironmental data\u003c/h2\u003e \u003cp\u003eMean temperature in captivity (x̅ = 23.7; range: 19 ‒ 29.8\u0026ordm;C) was higher than in natural habitat (x̅ = 22.6; range: 12.8 ‒ 38.3\u0026ordm;C; V\u0026thinsp;=\u0026thinsp;206233; p\u0026thinsp;\u0026lt;\u0026thinsp;0.05). The opposite happened to humidity, that was higher at QGI (x̅ = 86.1; range: 32.8 ‒ 100%) than in captivity (x̅ = 22.6; range: 28 ‒ 95.5%; V\u0026thinsp;=\u0026thinsp;6579967; p\u0026thinsp;\u0026lt;\u0026thinsp;0.05).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec10\" class=\"Section2\"\u003e \u003ch2\u003eDiet of wild animals\u003c/h2\u003e \u003cp\u003eAltogether, 106 fed animals were found. Birds represent around 90% of the diet, whereas ectotherms stand for the remaining 10%. It was possible to identify the prey at a specific level of 32 individuals of \u003cem\u003eB. insularis\u003c/em\u003e (19 females and 13 males). Of this sample, ectotherms represent around 40% of the diet, whereas birds stand for the remaining 60% (Fig.\u0026nbsp;\u003cspan refid=\"Fig2\" class=\"InternalRef\"\u003e1\u003c/span\u003e). Considering the latter, prey ingested by \u003cem\u003eB. insularis\u003c/em\u003e were mainly migratory birds of the species \u003cem\u003eElaenia chilensis\u003c/em\u003e (55%) and \u003cem\u003eTurdus flavipes\u003c/em\u003e (25%). Considering the sexes separately, the only ectotherms found as prey of the females were anurans, and they represent around 30% of their diet, with the remaining 70% being make up of birds. \u003cem\u003eTurdus flavipes\u003c/em\u003e, the larger bird species, were eaten exclusively by females. As for the males, ectotherms represent more than 45% of their diet, whereas usually small birds stand for the remaining 55%.\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec11\" class=\"Section2\"\u003e \u003ch2\u003eBody Size\u003c/h2\u003e \u003cp\u003eSome of the animals of the present study attained larger size than the maximum previously reported for the species (females: SVL\u0026thinsp;=\u0026thinsp;950, TL\u0026thinsp;=\u0026thinsp;143, TBL\u0026thinsp;=\u0026thinsp;1093 mm; males: SVL\u0026thinsp;=\u0026thinsp;775, TL\u0026thinsp;=\u0026thinsp;137, TBL\u0026thinsp;=\u0026thinsp;912 mm; \u003cem\u003ecf\u003c/em\u003e. Guimar\u0026atilde;es et al \u003cspan citationid=\"CR21\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Table\u0026nbsp;\u003cspan refid=\"Tab1\" class=\"InternalRef\"\u003e1\u003c/span\u003e). The largest captive female showed 1250mm in TBL (SVL\u0026thinsp;=\u0026thinsp;1050; TL\u0026thinsp;=\u0026thinsp;155 mm; body mass\u0026thinsp;=\u0026thinsp;556g), and the largest captive male was 945mm in TBL (SVL\u0026thinsp;=\u0026thinsp;810mm; TL\u0026thinsp;=\u0026thinsp;135mm; body mass\u0026thinsp;=\u0026thinsp;227g). The largest female found during our expeditions at QGI was 1130mm in total length (SVL\u0026thinsp;=\u0026thinsp;1005mm; TL\u0026thinsp;=\u0026thinsp;125 mm; body mass\u0026thinsp;=\u0026thinsp;240 g). Five captive-born females ranged from 1105 mm (SVL\u0026thinsp;=\u0026thinsp;965, TL\u0026thinsp;=\u0026thinsp;140 mm) to 1205 mm (SVL\u0026thinsp;=\u0026thinsp;1050, TL\u0026thinsp;=\u0026thinsp;155 mm) in TBL, and four captive-born males ranged between 920 mm (SVL\u0026thinsp;=\u0026thinsp;780, TL\u0026thinsp;=\u0026thinsp;140 mm) and 945 mm (SVL\u0026thinsp;=\u0026thinsp;810, TL\u0026thinsp;=\u0026thinsp;135 mm) in TBL. The captive females took a minimum of seven years, and the males, a minimum of six years to exceed the previous maximum size reported in literature.\u003c/p\u003e \u003cp\u003e \u003cdiv class=\"gridtable\"\u003e\u003ctable float=\"Yes\" id=\"Tab1\" border=\"1\"\u003e \u003ccaption language=\"En\"\u003e \u003cdiv class=\"CaptionNumber\"\u003eTable 1\u003c/div\u003e \u003cdiv class=\"CaptionContent\"\u003e \u003cp\u003eMean\u0026thinsp;\u0026plusmn;\u0026thinsp;SD of snout-vent length (SVL), body mass (M) and growth rate (GR) of females and males of the wild and the captive population.\u003c/p\u003e \u003c/div\u003e \u003c/caption\u003e \u003ccolgroup cols=\"5\"\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c1\" colnum=\"1\"\u003e\u003c/div\u003e \u003cdiv align=\"left\" class=\"colspec\" colname=\"c2\" colnum=\"2\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\"\u0026plusmn;\" class=\"colspec\" colname=\"c3\" colnum=\"3\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\"\u0026plusmn;\" class=\"colspec\" colname=\"c4\" colnum=\"4\"\u003e\u003c/div\u003e \u003cdiv align=\"char\" char=\"\u0026plusmn;\" class=\"colspec\" colname=\"c5\" colnum=\"5\"\u003e\u003c/div\u003e \u003cthead\u003e \u003ctr\u003e \u003cth align=\"left\" colname=\"c1\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c2\"\u003e\u0026nbsp;\u003c/th\u003e \u003cth align=\"left\" colname=\"c3\"\u003e \u003cp\u003eSVL (mm)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c4\"\u003e \u003cp\u003eM (g)\u003c/p\u003e \u003c/th\u003e \u003cth align=\"left\" colname=\"c5\"\u003e \u003cp\u003eGR (mm.day\u003csup\u003e\u0026minus;\u0026thinsp;1\u003c/sup\u003e)\u003c/p\u003e \u003c/th\u003e \u003c/tr\u003e \u003c/thead\u003e \u003ctbody\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eWILD\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cb\u003eFEMALE\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e736.8\u0026thinsp;\u0026plusmn;\u0026thinsp;74.4\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c4\"\u003e \u003cp\u003e196.2\u0026thinsp;\u0026plusmn;\u0026thinsp;68.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c5\"\u003e \u003cp\u003e0.20\u0026thinsp;\u0026plusmn;\u0026thinsp;0.16\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cb\u003eMALE\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e591.8\u0026thinsp;\u0026plusmn;\u0026thinsp;64.7\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c4\"\u003e \u003cp\u003e85.2\u0026thinsp;\u0026plusmn;\u0026thinsp;32.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c5\"\u003e \u003cp\u003e0.07\u0026thinsp;\u0026plusmn;\u0026thinsp;0.09\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c1\" morerows=\"1\" rowspan=\"2\"\u003e \u003cp\u003e\u003cb\u003eCAPTIVE\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cb\u003eFEMALE\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e921.25\u0026thinsp;\u0026plusmn;\u0026thinsp;94.1\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c4\"\u003e \u003cp\u003e390.2\u0026thinsp;\u0026plusmn;\u0026thinsp;157.2\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c5\"\u003e \u003cp\u003e0.21\u0026thinsp;\u0026plusmn;\u0026thinsp;0.12\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003ctr\u003e \u003ctd align=\"left\" colname=\"c2\"\u003e \u003cp\u003e\u003cb\u003eMALE\u003c/b\u003e\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c3\"\u003e \u003cp\u003e732.9\u0026thinsp;\u0026plusmn;\u0026thinsp;60.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c4\"\u003e \u003cp\u003e146.0\u0026thinsp;\u0026plusmn;\u0026thinsp;38.0\u003c/p\u003e \u003c/td\u003e \u003ctd align=\"char\" char=\"\u0026plusmn;\" colname=\"c5\"\u003e \u003cp\u003e0.17\u0026thinsp;\u0026plusmn;\u0026thinsp;0.16\u003c/p\u003e \u003c/td\u003e \u003c/tr\u003e \u003c/tbody\u003e \u003c/colgroup\u003e \u003c/table\u003e\u003c/div\u003e \u003c/p\u003e \u003cp\u003eSnout-vent length differed between sexes (F\u003csub\u003e(1,796)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;140.986; \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.000; Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e2\u003c/span\u003e) and population (F\u003csub\u003e(1,796)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;59.045; \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.000). The Tukey test revealed that captive females attain the largest SVL (\u003cem\u003eP\u003c/em\u003e\u0026thinsp;\u0026lt;\u0026thinsp;0.001), while wild males were the smallest amongst all (\u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.000). Captive males were as large as wild females (\u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.470). Linear regression revealed a positive correlation between body mass and SVL (R\u0026sup2; = 0.549; \u003cem\u003edf\u003c/em\u003e\u0026thinsp;=\u0026thinsp;724; \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.000). Therefore, the residuals of this regression were extracted and used in an ANOVA with sex and population as factors. A significant effect of the interaction sex*population on body mass was observed (F\u003csub\u003e(1,722)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;27.990; \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.000). The post-hoc Tukey test revealed that captive females showed the highest relative body mass amongst all (\u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.000; Fig.\u0026nbsp;\u003cspan refid=\"Fig3\" class=\"InternalRef\"\u003e3\u003c/span\u003e). Wild females were relatively heavier than both wild (\u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.000) and captive males (\u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.002), and wild and captive males show similar relative body mass (\u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.382).\u003c/p\u003e \u003c/div\u003e \u003cdiv id=\"Sec12\" class=\"Section2\"\u003e \u003ch2\u003eGrowth rates and curves\u003c/h2\u003e \u003cp\u003eData reported herein comprises 78 growth intervals, 41 of them (ranging from 22 to 4639 days) obtained from the recapture of 35 wild females, and 37 growth intervals (ranging from 32 to 2714 days) from the recapture of 21 wild males of \u003cem\u003eB. insularis\u003c/em\u003e. Concerning captive Golden Lanceheads, we used SVL of 15 females (ranging from 376 to 3612 days of life) and of 20 males (ranging from 8 to 3612 days).\u003c/p\u003e \u003cp\u003eWe found no significant association between growth rate and SVL increase (ANCOVA: F\u003csub\u003e(1,223)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;0.377; \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.54). Therefore, we performed an ANOVA using sex and population as factors, which evinced that both factors affect GR (sex: F\u003csub\u003e(1,221)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;7.577; \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.006; population: F\u003csub\u003e(1,221)\u003c/sub\u003e\u0026thinsp;=\u0026thinsp;9.415; \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.002). Post-hoc tests reveal that wild males show the lowest growth rate amongst all (compared to captive females: \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.000; captive males: \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.009; and wild females: \u003cem\u003eP\u003c/em\u003e\u0026thinsp;=\u0026thinsp;0.020; Fig.\u0026nbsp;\u003cspan refid=\"Fig4\" class=\"InternalRef\"\u003e4\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eAsymptotic values show that females from QGI attain SVL up to about 850 mm, and the males, 600 mm (Fig.\u0026nbsp;5A). Growth curves of the captive animals suggest that females grow up to 1000 mm of SVL, and males, up to about 750 mm (Fig.\u0026nbsp;5B). Data from the literature show that minimum size at sexual maturity is 432 mm for males (Marques et al \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e) and 555 mm for females from QGI (Kasperoviczus \u003cspan citationid=\"CR26\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Marques et al \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e), and 403 mm for males and 619 mm for females from captivity (Passos \u003cspan citationid=\"CR48\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). Based on such data, the growth curves suggest that captive females reach sexual maturity with about 3 years old, while captive males do so within less than one year. Wild females reach sexual maturity within 3.8 years, and the males, with 3.6 years old.\u003c/p\u003e \u003c/div\u003e"},{"header":"Discussion","content":"\u003cp\u003eIn the present study, we provide the first estimate of GR for \u003cem\u003eB. insularis\u003c/em\u003e. Additionally, we compare the GR of the wild population with that of the captive. Our first hypothesis was partially confirmed: wild animals indeed attain smaller body size and mass than captive individuals of the same sex. Our second hypothesis was also confirmed, as wild Golden Lancehead reach sexual maturation later, in comparison to captive individuals, possibly due to the fluctuations in food availability at QGI, following the premise that food input may influence maturation age (Ford and Seigel \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e1994\u003c/span\u003e). Also, following the pattern of animals which grow continuously and indefinitely throughout life (Shine and Charnov \u003cspan citationid=\"CR60\" class=\"CitationRef\"\u003e1992\u003c/span\u003e), \u003cem\u003eB. insularis\u003c/em\u003e showed a marked decrease in GR after maturation. Lastly, in our third hypothesis, we predicted that captive Golden Lancehead would show a higher GR in comparison to those from QGI. Nevertheless, only wild males showed lower GR.\u003c/p\u003e \u003cp\u003eSnakes in QGI ‒ subject to lower temperatures than that of captivity ‒ were smaller and slighter, which was expected since warmer temperatures may be related to higher growth rate in snakes (Arnold and Peterson \u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e1989\u003c/span\u003e; Gangloff et al \u003cspan citationid=\"CR19\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Humidity was higher at QGI, but this variable does not seem to have direct effects on growth rate. It must be considered, however, that low humidity may be associated with dysecdysis whereas high humidity may cause dermatitis and lesions, especially in captive reptiles (Lillywhite and Gatten Jr. 1995; Oonincx and van Leeuwen \u003cspan citationid=\"CR47\" class=\"CitationRef\"\u003e2017\u003c/span\u003e), what may ultimately compromise health conditions and growth in these animals. However, even though this scenario looks reasonable, we recognize that the lack of a meteorological station at the island may be an issue.\u003c/p\u003e \u003cp\u003eA decrease of the GR is expected after sexual maturity, because both males and females need to mobilize energetic reserves for the development of structures and behaviours associated to reproduction, and such energy comes from food (Saint-Girons \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e1994\u003c/span\u003e). For viviparous female snakes, the reproduction involves high metabolic costs, especially during vitellogenesis, when mean metabolic costs represent about 30% of the total metabolic demand (Saint-Girons \u003cspan citationid=\"CR53\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Van Dyke and Beaupre, \u003cspan citationid=\"CR70\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). Delayed maturation is often observed in the sex which experience higher reproductive costs (Shine \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e1994\u003c/span\u003e), which is evident when we analyse the growth curve of captive animals. Even though both males and females receive proportionally the same amount of food, in the same frequency, females take three times that which males take to reach maturity. By comparing the growth curves of both populations, it seems plausible that the delayed sexual maturity in \u003cem\u003eB. insularis\u003c/em\u003e from QGI arises due a scarcity of resources. Apparently, the greater food input in captivity allows males to double their size and become sexually mature as one year old.\u003c/p\u003e \u003cp\u003eBoth in the wild and in captivity, females were the largest sex, confirming the marked sexual size dimorphism (SSD) reported for by \u003cem\u003eB. insularis\u003c/em\u003e (Marques et al \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e), with females being larger than the males, like several other congeneric species (Valdujo et al \u003cspan citationid=\"CR69\" class=\"CitationRef\"\u003e2002\u003c/span\u003e; Nogueira et al \u003cspan citationid=\"CR43\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Hartmann et al \u003cspan citationid=\"CR24\" class=\"CitationRef\"\u003e2004\u003c/span\u003e; Sasa et al \u003cspan citationid=\"CR56\" class=\"CitationRef\"\u003e2009\u003c/span\u003e; Nunes et al \u003cspan citationid=\"CR44\" class=\"CitationRef\"\u003e2010\u003c/span\u003e; Barros et al \u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Le\u0026atilde;o et al \u003cspan citationid=\"CR28\" class=\"CitationRef\"\u003e2014\u003c/span\u003e; Almeida-Santos et al \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Stuginski et al \u003cspan citationid=\"CR68\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Silva et al \u003cspan citationid=\"CR63\" class=\"CitationRef\"\u003e2017\u003c/span\u003e; Silva et al \u003cspan citationid=\"CR65\" class=\"CitationRef\"\u003e2019\u003c/span\u003e; Silva et al \u003cspan citationid=\"CR64\" class=\"CitationRef\"\u003e2020\u003c/span\u003e; Siqueira et al \u003cspan citationid=\"CR67\" class=\"CitationRef\"\u003e2022\u003c/span\u003e). Body size may not represent an important reproductive constraint for the males, since their metabolic costs are lower than that of the females\u0026rsquo;. This is especially true for species in which males do not fight to access a female. In these species, SSD tend to be male-biased, with larger size of males being attained by prolonged growth after maturation (Shine \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e1994\u003c/span\u003e). Therefore, when there are no advantages arising from size, or even when the larger size may represent a disadvantage in resource partitioning, natural selection may favour smaller males (Madsen \u003cspan citationid=\"CR33\" class=\"CitationRef\"\u003e1983\u003c/span\u003e). Because there is no apparent selective pressure for males to be larger, most of the energy obtained from food may be mobilized for reproductive purposes, instead of for growth. In reptiles, SSD may be the result of three main selective pressures: (1) sexual selection, (2) fecundity, and (3) reduction of intraspecific competition for prey (Cox et al \u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e2007\u003c/span\u003e). Female-biased SSD in the Golden Lancehead seems to be influenced by the two latter.\u003c/p\u003e \u003cp\u003eBecause body size is an important constraint for females\u0026rsquo; fecundity, it is expected that at QGI, GR in females is higher than that of males. Growth rate is influenced by variation in prey abundance, whether temporal or seasonally (Macartney et al \u003cspan citationid=\"CR32\" class=\"CitationRef\"\u003e1990\u003c/span\u003e; Lindell and Forsman \u003cspan citationid=\"CR31\" class=\"CitationRef\"\u003e2011\u003c/span\u003e). Avian prey, the main food item of adults\u0026rsquo; diet, is limited and ephemeral at the island, so that this relative scarcity of resources could compromise GR of both males and females. It is possible that females, for having larger heads than males (W\u0026uuml;ster et al \u003cspan citationid=\"CR74\" class=\"CitationRef\"\u003e2005\u003c/span\u003e; Marques et al \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e), are able to feed on larger prey, balancing their great energetic expenditures on reproduction (Shine \u003cspan citationid=\"CR57\" class=\"CitationRef\"\u003e1991\u003c/span\u003e), and attaining larger body size and mass, and higher GR. This morphological difference may also result in a reduction of intraspecific competition for prey. \u003cem\u003eBothrops insularis\u003c/em\u003e has an ontogenetic dietary shift, with juveniles feeding on ectothermic prey as anurans, lizards and centipedes, while the adults feed on birds (Marques et al \u003cspan citationid=\"CR37\" class=\"CitationRef\"\u003e2002\u003c/span\u003e). Males have smaller heads and therefore perhaps depend on ectothermic prey for longer than females, as the size of their heads would be a restriction for hunting large birds that are prey with higher caloric value and that provide a higher growth rate. Accordingly, diet data sampled from fed snakes reveal that the larger birds (\u003cem\u003eT. flavipes\u003c/em\u003e) are eaten exclusively by the females, whereas the males seem to rely on the smaller birds, such as \u003cem\u003eElaenia chilensis\u003c/em\u003e, or ectotherm prey, such as anurans, lizards and centipedes. Additionally, it is also interesting to notice that the relation prey mass x snake mass was usually higher for males than for females, showing that feeding on birds, may, indeed, impose a restriction, especially for the smaller males. It can be hypothesized that lower GR in males after sexual maturation is a consequence of constraints imposed by reproduction. Mate-searching may incur high energetic costs, with increased movement and activity of the males, as observed in many snake species (\u003cem\u003ee.g.\u003c/em\u003e Shine \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2003\u003c/span\u003e; Jellen et al \u003cspan citationid=\"CR25\" class=\"CitationRef\"\u003e2007\u003c/span\u003e; Glaudas and Rodr\u0026iacute;guez-Robles \u003cspan citationid=\"CR20\" class=\"CitationRef\"\u003e2011\u003c/span\u003e; Bauder et al \u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e2016\u003c/span\u003e). In snakes, fecundity is directly correlated to females\u0026rsquo; size, and both the evolution of viviparity, and fecundity are associated with the selection for larger females (Fitch \u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e1981\u003c/span\u003e; Shine \u003cspan citationid=\"CR58\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Aubret et al \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e2002\u003c/span\u003e), as already evinced in \u003cem\u003eB. insularis\u003c/em\u003e (Marques et al \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). Therefore, larger body size in females may be favoured, resulting in greater litter size, increase in offspring, and females with better body condition after parturition (Hailey and Davies \u003cspan citationid=\"CR22\" class=\"CitationRef\"\u003e1987\u003c/span\u003e; Ford and Seigel \u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Madsen and Shine \u003cspan citationid=\"CR34\" class=\"CitationRef\"\u003e1994\u003c/span\u003e; Shine and Madsen \u003cspan citationid=\"CR61\" class=\"CitationRef\"\u003e1997\u003c/span\u003e). For having higher food intake, captive females are possibly able to store the energy as fat for future reproductive events (Shine \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2003\u003c/span\u003e). It must also be considered that wild and captive animals feed on different kind of prey. While in the island the Golden Lancehead feed on birds, captive individuals feed on mice. Nutritional properties of these prey items are different, and may influence the energetic storage (Kremen et al \u003cspan citationid=\"CR27\" class=\"CitationRef\"\u003e2013\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eMean fecundity of \u003cem\u003eB. insularis\u003c/em\u003e from QGI was estimated in 8.2 offspring per litter (range: 3\u0026ndash;20; Marques et al \u003cspan citationid=\"CR39\" class=\"CitationRef\"\u003e2013\u003c/span\u003e). Up to this moment, only five litters of the Golden Lancehead were born from the breeding among captive-born individuals. Fecundity (7.4\u0026thinsp;\u0026plusmn;\u0026thinsp;3.65; range: 3\u0026ndash;11; this study) was lower than that estimated for wild animals, which is intriguing, given that captive females are larger. It can be hypothesized that the larger body size of captive females is associated with increase in relative clutch mass (\u003cem\u003ee.g.\u003c/em\u003e Shine \u003cspan citationid=\"CR59\" class=\"CitationRef\"\u003e2003\u003c/span\u003e). Unfortunately, we do not have data on body size and litter mass of \u003cem\u003eB. insularis\u003c/em\u003e in the wild, so this could not be tested in the present study.\u003c/p\u003e \u003cp\u003eIn conclusion, our study provides evidence that body size, growth rate, and age of maturity in \u003cem\u003eB. insularis\u003c/em\u003e is greatly influenced by food intake and costs of reproduction. Accordingly, the wild population show smaller body size and delayed maturity in comparison to the captive one. Likewise, females show delayed maturity when compared to males of the same population. Wild males show the lowest GR amongst all which may be a consequence of their smaller head that limits the ingestion of large prey. It is important to consider the effects of these differences. For the animals at QGI, slower growth and later maturation mainly in males may impact \u003cem\u003eB. insularis\u003c/em\u003e of recovering from population declines (Blouin-Demers et al \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e2006\u003c/span\u003e). As for the captive ones, caution should be taken, considering that a negative correlation between fast growth and survival has already been evinced for snakes (Bronikowski and Arnold \u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e1999\u003c/span\u003e; Rose et al \u003cspan citationid=\"CR52\" class=\"CitationRef\"\u003e2021\u003c/span\u003e). Additionally, reptiles which are overfed (such as the captive ones, whose feeding frequency is higher than in the wild), may show rapid growth, obesity and secondary diseases (Pellett and Wissink-Argilaga \u003cspan citationid=\"CR49\" class=\"CitationRef\"\u003e2015\u003c/span\u003e). Obesity may cause damage and even failure of the liver, ultimately leading a snake to death (Martins et al \u003cspan citationid=\"CR41\" class=\"CitationRef\"\u003e2018\u003c/span\u003e). These aspects are especially important for conservation \u003cem\u003eex situ\u003c/em\u003e. Concerning species conservation, the impact of the larger body size in captive animals on other traits, such as habitat use, must be considered, especially if reintroduction of these animals become necessary. In this sense, a period in soft release methods would be crucial for better analysing such matters. As for the Golden Lanceheads in the island, it is mandatory that the conservation strategies encompass the maintenance of the population of the migratory birds, in order to ensure the energetic income to the snakes.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e\u003cstrong\u003eAcknowledgements \u0026nbsp;\u0026nbsp;\u003c/strong\u003eWe would like to thank all the people who have greatly helped with data sampling in the field, especially Carlos Renato Azevedo, C\u0026aacute;ssia Domingos, C\u0026aacute;ssio Spercazechi, Diego Lorenzetto, Diego Muniz, Fausto Barbo, Fabiano Morezi, Juliana Medeiros, Kaline de Mello, Karina Kasperoviczus, Let\u0026iacute;cia Sueiro, Ligia Amorim, Luana Rosa, Ma\u0026iacute;sa Matuoka, Marcio Martins, Mariana Guilardi, Nat\u0026aacute;lia Torello-Viera, Rafael Bovo, Ricardo Dias, Ricardo Sawaya, Rodrigo Castello, Silara Batista, Thiago Estimo, Valdir Germano, Vinicius Correia, and Wilian Borges. We would also like to thank Adriano Felone, Kelly Kishi, and Selma M. Almeida-Santos for providing access to the data from the captive population.\u0026nbsp;\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eAuthor\u0026rsquo;s Contribution \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp;\u003c/strong\u003eKRSB and LHCS conceived the ideas and designed methodology; KRSB and LHCS collected and analysed the data; KRSB led the writing of the manuscript. OAV supervised the study. All authors contributed to the drafts and gave final approval for publication.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eFunding \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp;\u003c/strong\u003eThis work was supported by Funda\u0026ccedil;\u0026atilde;o de Amparo \u0026agrave; Pesquisa do Estado de S\u0026atilde;o Paulo (Grants FAPESP #2012/07334-9, #2018/07507-7, and 2020/12658-4).\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eConflicts of interest \u0026nbsp;\u0026nbsp;\u003c/strong\u003eThe authors declare no conflicts of interest.\u003c/p\u003e\n\u003cp\u003e\u003cstrong\u003eEthics approval \u0026nbsp; \u0026nbsp; \u0026nbsp; \u0026nbsp;\u0026nbsp;\u003c/strong\u003eThis study was authorized by the Ethic Commission for Animal Usage of Instituto Butantan (certificates CEUAIB #983-12 and #1543170518), the Brazilian Ministry of the Environment (SISBIO #6295-7 and 16119), and the Brazilian Instituto of Environment and Renewable Natural Resources (IBAMA n\u0026ordm; 25.650-1).\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eAlencar LRV, Quental TB, Grazziotin FG et al (2016) Diversification in vipers: Phylogenetic relationships, time of divergence and shifts in speciation rates. Mol Phylogenet Evol 105:50\u0026ndash;62\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAlencar LRV, Martins M, Burin G et al (2017) Arboreality constrains morphological evolution but not species diversification in vipers. Proc R Soc Lond B Biol Sci 284:20171775\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAlmeida-Santos SM, Barros VA, Rojas CA et al (2017) Reproductive biology of the Brazilian Lancehead, \u003cem\u003eBothrops moojeni\u003c/em\u003e (Serpentes, Viperidae), from the State of S\u0026atilde;o Paulo, Southeastern Brazil. South Am J Herpetol 12:174\u0026ndash;181\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAmaral A (1921) Contribui\u0026ccedil;\u0026atilde;o para o conhecimento dos Of\u0026iacute;dios do Brasil. Mem Inst Butantan I:6\u0026ndash;108\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAngilletta MJ, Steury TD, Sears MW (2004) Temperature, Growth Rate, and Body Size in Ectotherms: Fitting Pieces of a Life-History Puzzle. Integr Comp Biol 44:498\u0026ndash;509\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eArnold SJ, Peterson CR (1989) A Test for Temperature Effects on the Ontogeny of Shape in the Garter Snake \u003cem\u003eThamnophis sirtalis\u003c/em\u003e. Physiol Zool 62:1316\u0026ndash;1333\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eAubret F, Bonnet X, Shine R et al (2002) Fat is sexy for females but not males: The influence of body reserves on reproduction in snakes (\u003cem\u003eVipera aspis\u003c/em\u003e). Horm Behav 42:135\u0026ndash;147\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBarros VA, Rojas CA, Almeida-Santos SM (2014) Reproductive Biology of \u003cem\u003eBothrops erythromelas\u003c/em\u003e from the Brazilian Caatinga. Adv Zool 2014:1\u0026ndash;11\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBaty F, Ritz C, Charles S et al (2015) A Toolbox for Nonlinear Regression in R: The Package nlstools. J Stat Softw 66:1\u0026ndash;21\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBauder JM, Breininger DR, Bolt MR et al (2016) Seasonal variation in eastern Indigo Snake (\u003cem\u003eDrymarchon couperi\u003c/em\u003e) movement patterns and space use in Peninsular Florida at multiple temporal scales. Herpetologica 72:214\u0026ndash;226\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBlouin-Demers G, Prior KA, Weatherhead PJ (2006) Comparative demography of black rat snakes (\u003cem\u003eElaphe obsoleta\u003c/em\u003e) in Ontario and Maryland. J Zool 256:1\u0026ndash;10\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBonnet X, Naulleau G (1996) Are body reserves important for reproduction in male dark green snakes (Colubridae: \u003cem\u003eColuber viridiflavus\u003c/em\u003e)? Herpetologica 52:137\u0026ndash;146\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBovo RP, Marques OAV, Andrade DV (2012) When Basking Is Not an Option: Thermoregulation of a Viperid Snake Endemic to a Small Island in the South Atlantic of Brazil. Copeia 2012:408\u0026ndash;418\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBronikowski AM, Arnold SJ (1999) The evolutionary ecology of life history variation in the garter snake \u003cem\u003eThamnophis elegans\u003c/em\u003e. Ecology 80:2314\u0026ndash;2325\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eCox RM, Butler MA, John-Alder HB (2007) The evolution of sexual size dimorphism in reptiles. In: Fairbairn DJ, Blanckenhorn WU, Sz\u0026eacute;kely T (eds) Sex, Size and Gender Roles: Evolutionary Studies of Sexual Size Dimorphism. Oxford University Press, Oxford, pp 38\u0026ndash;49\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eFabens AJ (1965) Properties and fitting of the von Bertalanffy growth curve. Growth 29:265\u0026ndash;289\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eFitch HS (1981) Sexual Size Differences in Reptiles. Sci Pap Univ Kans Nat Hist Mus 70:1\u0026ndash;72\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eFord NB, Seigel RA (1994) An Experimental Study of the Trade-Offs Between Age and Size at Maturity: Effects of Energy Availability. Funct Ecol 8:91\u0026ndash;96\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eGangloff EJ, Vleck D, Bronikowski AM (2015) Developmental and Immediate Thermal Environments Shape Energetic Trade-Offs, Growth Efficiency, and Metabolic Rate in Divergent Life-History Ecotypes of the Garter Snake \u003cem\u003eThamnophis elegans\u003c/em\u003e. Physiol Biochem Zool 88:550\u0026ndash;563\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eGlaudas X, Rodr\u0026iacute;guez-Robles JA (2011) Vagabond males and sedentary females: spatial ecology and mating system of the Speckled Rattlesnake (\u003cem\u003eCrotalus mitchellii\u003c/em\u003e). Biol J Linn Soc Lond 103:681\u0026ndash;695\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eGuimar\u0026atilde;es MR, Bovo RP, Kasperoviczus KN et al (2010) \u003cem\u003eBothrops insularis\u003c/em\u003e (Golden Lancehead). Maximum length. Herpetol Rev 41:89\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHailey A, Davies PMC (1987) Maturity, mating and age-specific reproductive effort of the snake \u003cem\u003eNatrix maura\u003c/em\u003e. J Zool 211:573\u0026ndash;587\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHariharan IK, Wake DB, Wake MH (2015) Indeterminate Growth: Could It Represent the Ancestral Condition? Cold Spring Harb Perspect Biol 8:a019174\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eHartmann MT, Marques OAV, Almeida-Santos SM (2004) Reproductive biology of the southern Brazilian pitviper \u003cem\u003eBothrops neuwiedi pubescens\u003c/em\u003e (Serpentes, Viperidae). Amphib Reptil 25:77\u0026ndash;85\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eJellen BC, Shepard DB, Dreslik MJ et al (2007) Male Movement and Body Size Affect Mate Acquisition in the Eastern Massasauga (\u003cem\u003eSistrurus catenatus\u003c/em\u003e). J Herpetol 41:451\u0026ndash;457\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKasperoviczus KN (2009) Biologia reprodutiva da jararaca ilhoa, \u003cem\u003eBothrops insularis\u003c/em\u003e, (Serpentes: Viperidae) da Ilha da Queimada Grande, S\u0026atilde;o Paulo. Thesis, Universidade de S\u0026atilde;o Paulo\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eKremen NA, Calvert CC, Larsen JA et al (2013) Body composition and amino acid concentrations of select birds and mammals consumed by cats in northern and central California. J Anim Sci 91:1270\u0026ndash;1276\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLe\u0026atilde;o SM, Pelegrin N, Nogueira CC et al (2014) Natural history of \u003cem\u003eBothrops itapetiningae\u003c/em\u003e Boulenger, 1907 (Serpentes: Viperidae: Crotalinae), an endemic species of the Brazilian Cerrado. J Herpetol 48:324\u0026ndash;331\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLillywhite HB (2014) How snakes work. Structure, function and behavior of the world\u0026rsquo;s snakes. Oxford University Press, Oxford\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLillywhite HB, Gatten RE Jr (2023) Physiology and functional anatomy. In: Warwick C, Frye FL, Murphy JB (eds) Health and Welfare of Captive Reptiles. Chapman \u0026amp; Hall, London, pp 5\u0026ndash;31\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eLindell LE, Forsman A (2011) Density effects and snake predation: Prey limitation and reduced growth rate of adders at high density of conspecifics. Can J Zool 74:1000\u0026ndash;1007\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMacartney JM, Gregory PT, Charland MB (1990) Growth and Sexual Maturity of the Western Rattlesnake, \u003cem\u003eCrotalus viridis\u003c/em\u003e, in British Columbia. Copeia 1990:528\u0026ndash;542\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMadsen T (1983) Growth Rates, Maturation and Sexual Size Dimorphism in a Population of Grass Snakes, \u003cem\u003eNatrix natrix\u003c/em\u003e, in Southern Sweden. Oikos 40:277\u0026ndash;282\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMadsen T, Shine R (1994) Phenotypic Plasticity in Body Sizes and Sexual Size Dimorphism in European Grass Snakes. Evolution 48:1389\u0026ndash;1397\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMadsen T, Shine R (2000) Silver spoons and snake body sizes prey availability early in life influences long-term growth rates of free‐ranging pythons. J Anim Ecol 69:952\u0026ndash;958\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMarinho AF (2022) Aspectos ecol\u0026oacute;gicos da lagartixa ex\u0026oacute;tica \u003cem\u003eHemidactylus mabouia\u003c/em\u003e Moreau de Jonn\u0026egrave;s, 1818 (Gekkonidae) na Restinga de Itacoatiara, Niter\u0026oacute;i, RJ. Thesis, Universidade Federal Fluminense\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMarques OAV, Martins M, Sazima I (2002) A new insular species of pitviper from Brazil, with comments on evolutionary biology and conservation of the \u003cem\u003eBothrops jararaca\u003c/em\u003e group (Serpentes, Viperidae). Herpetologica 58:303\u0026ndash;312\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMarques OAV, Martins M, Develey PF et al (2012) The Golden Lancehead \u003cem\u003eBothrops insularis\u003c/em\u003e (Serpentes: Viperidae) relies on two seasonally plentiful bird species visiting its island habitat. J Nat Hist 46:885\u0026ndash;895\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMarques OAV, Kasperoviczus K, Almeida-Santos SM (2013) Reproductive ecology of the threatened Pitviper \u003cem\u003eBothrops insularis\u003c/em\u003e from Queimada Grande Island, Southeast Brazil. J Herpetol 47:393\u0026ndash;399\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMartins M, Marques OAV, Sazima I (2002) Ecological and Phylogenetic Correlates of Feeding Habits in Neotropical Pitvipers of the Genus \u003cem\u003eBothrops\u003c/em\u003e. In: Schuett GW, Hoggren M, Douglas ME et al (eds) Biology of the vipers. Eagle Mountain Publishing, Utah, pp 1\u0026ndash;22\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMartins NB, Ferreira LAR, Silva TSG et al (2018) Hepatic Lipidosis Due to Obesity in a Free-Living Snake (\u003cem\u003eBoa constrictor amarali\u003c/em\u003e). Acta Sci Vet 46:265\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eMcGehee SM, Hamilton P, Beatty B et al (2012) Seasonal Body Mass Changes in Six Forest Passerines of Southern Chile. Ornitol Neotrop 23:25\u0026ndash;34\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eNogueira C, Sawaya RJ, Martins M (2003) Ecology of the Pitviper, \u003cem\u003eBothrops moojeni\u003c/em\u003e, in the Brazilian Cerrado. J Herpetol 37:653\u0026ndash;659\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eNunes SF, Kaefer IL, Leite PT et al (2010) Reproductive and feeding biology of the pitviper \u003cem\u003eRhinocerophis alternatus\u003c/em\u003e from subtropical Brazil. Herpetol J 20:31\u0026ndash;39\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eOgle DH (2019) FSAdata: Fisheries Stock Analysis, Datasets. CRAN. R package version 0.3.8\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eOgle DH, Wheeler P, Dinno A (2020) FSA: Fisheries Stock Analysis. CRAN. R package version 0.8.30\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eOonincx D, van Leeuwen J (2017) Evidence-Based Reptile Housing and Nutrition. Vet Clin Exot Anim 20:885\u0026ndash;898\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePassos J (2018) Influ\u0026ecirc;ncia no crescimento de \u003cem\u003eBothrops insularis\u003c/em\u003e e \u003cem\u003eBothrops jararaca\u003c/em\u003e: a dieta pode interferir no tamanho da maturidade sexual em cativeiro? Thesis, Universidade de S\u0026atilde;o Paulo\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePellett S, Wissink-Argilaga N (2015) Nutrition \u0026mdash; lizards and snakes. Companion Anim 20:362\u0026ndash;366\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ePlummer MV (1985) Growth and maturity in green snake (\u003cem\u003eOpheodrys aestivus\u003c/em\u003e). Herpetologica 41:28\u0026ndash;33\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eR Core Team (2022) R: A Language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRose JP, Kim R, Schoenig EJ et al (2021) Integrating growth and survival models for flexible estimation of size-dependent survival in a cryptic, endangered snake. Ecol Evol 12:e8799\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSaint-Girons H (1994) Growth \u0026amp; Reproduction. In: Bauchot R (ed) Snakes: A Natural History. Sterling Publishing Co. Inc, New York, pp 92\u0026ndash;107\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSalles-Oliveira I, Machado T, Banci KRS et al (2020) Genetic variability, management, and conservation implications of the critically endangered Brazilian pitviper \u003cem\u003eBothrops insularis\u003c/em\u003e. Ecol Evol 10:12870\u0026ndash;12882\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSantos MA (2018) Rela\u0026ccedil;\u0026otilde;es de tamanho, massa e dieta no nicho alimentar em uma comunidade de anuros na Mata Atl\u0026acirc;ntica. Dissertation, Universidade do Estado do Rio de Janeiro\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSasa M, Wasko DK, Lamar WW (2009) Natural history of the terciopelo \u003cem\u003eBothrops asper\u003c/em\u003e (Serpentes: Viperidae) in Costa Rica. Toxicon 54:904\u0026ndash;922\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eShine R (1991) Intersexual dietary divergence and the evolution of sexual dimorphism in snakes. Am Nat 138:103\u0026ndash;122\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eShine R (1994) Sexual Size Dimorphism in Snakes Revisited. Copeia 1994:326\u0026ndash;346\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eShine R (2003) Reproductive strategies in snakes. Proc R Soc Lond B Biol Sci 270:995\u0026ndash;1004\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eShine R, Charnov EL (1992) Patterns of survival, growth, and maturation in snakes and lizards. Am Nat 139:1257\u0026ndash;1269\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eShine R, Madsen T (1997) Prey abundance and predator reproduction: Rats and pythons on a tropical Australian floodplain. Ecology 78:1078\u0026ndash;1086\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSick H (1984) Ornitologia Brasileira, uma Introdu\u0026ccedil;\u0026atilde;o. Editora Universidade de Bras\u0026iacute;lia, Bras\u0026iacute;lia\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSilva FM, Oliveira LS, Nascimento LRS et al (2017) Sexual dimorphism and ontogenetic changes of Amazonian pit vipers (\u003cem\u003eBothrops atrox\u003c/em\u003e). Zool Anz 271:15\u0026ndash;24\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSilva KMP, Braz HB, Kasperoviczus KN et al (2020) Reproduction in the pitviper \u003cem\u003eBothrops jararacussu\u003c/em\u003e: large females increase their reproductive output while small males increase their potential to mate. Zoology 142:125816\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSilva KMP, Silva KB, Sueiro LR et al (2019) Reproductive Biology of \u003cem\u003eBothrops atrox\u003c/em\u003e (Serpentes, Viperidae, Crotalinae) from the Brazilian Amazon. Herpetologica 75:198\u0026ndash;207\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSilveira AL, Prudente ALC, Arg\u0026ocirc;lo AJS et al (2021) \u003cem\u003eBothrops insularis\u003c/em\u003e. The IUCN Red List of Threatened Species 2021:e.T2917A123180264\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSiqueira LHC, Piantoni C, MARQUES OAV (2022) Morphological variation in the common lancehead populations: Sexual dimorphism and ontogenetic patterns. J Zool 318:283\u0026ndash;296\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eStuginski DR, Mendes GF, Sant\u0026rsquo;Anna SS et al (2017) Sexual Differences in Growth Rates of Juveniles from a Litter of \u003cem\u003eBothrops fonsecai\u003c/em\u003e: The Role of Feeding Conversion in a Female-Biased SSD Species. South Am J Herpetol 12:193\u0026ndash;199\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eValdujo PH, Nogueira C, Martins M (2002) Ecology of \u003cem\u003eBothrops neuwiedi pauloensis\u003c/em\u003e (Serpentes: Viperidae: Crotalinae) in the Brazilian Cerrado. J Herpetol 36:169\u0026ndash;176\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eVan Dyke JU, Beaupre SJ (2011) Bioenergetic components of reproductive effort in viviparous snakes: Costs of vitellogenesis exceed costs of pregnancy. Comp Biochem Physiol Mol Integr Physiol 160:504\u0026ndash;515\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eVan Dyke JU, Beaupre SJ, Kreider DL (2012) Snakes allocate amino acids acquired during vitellogenesis to offspring: Are capital and income breeding consequences of variable foraging success? Biol J Linn Soc Lond 106:390\u0026ndash;404\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eWickham H (2011) The Split-Apply-Combine Strategy for Data Analysis. J Stat Softw 40:1\u0026ndash;29\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eWikiAves (2024) WikiAves, a Enciclop\u0026eacute;dia das Aves do Brasil. \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttp://www.wikiaves.com.br/\u003c/span\u003e\u003cspan address=\"http://www.wikiaves.com.br/\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e, accessed in: 03/20/2024\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eW\u0026uuml;ster W, Duarte MR, Salom\u0026atilde;o MG (2005) Morphological correlates of incipient arboreality and ornithophagy in island pitvipers, and the phylogenetic position of \u003cem\u003eBothrops insularis\u003c/em\u003e. J Zool 266:1\u0026ndash;10\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":true,"highlight":"","institution":"","isAcceptedByJournal":false,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true},"keywords":"Bothrops insularis, food intake, sexual maturity, in situ conservation, ex situ conservation, snake","lastPublishedDoi":"10.21203/rs.3.rs-4607766/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-4607766/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eThe Golden Lancehead, \u003cem\u003eBothrops insularis\u003c/em\u003e, is a critically endangered viperid species, endemic to Queimada Grande Island. The diet of adults relies mainly on migratory birds, which peaks in March and July on the island. Herein, we describe the growth rate of the Golden Lancehead for the very first time, testing the hypothesis that growth and adult body size may decrease as a result of resource scarcity and environmental variability in the island, in comparison to a captive population. Our findings suggest that both food intake, temperature, and reproductive requirements might influence body size, growth rate, and sexual maturity of \u003cem\u003eB. insularis\u003c/em\u003e. More specifically, wild animals attain smaller body size and mass, show lower growth rate, and attain sexual maturity later, in comparison to the captive individuals of the same sex, possibly as a result of lower food availability. This situation is more evident among males, and, apparently, morphological constraints make it difficult for them to explore large prey at the island. Females are the largest sex, possibly as a result of fecundity optimization. Fecundity also depends on energy reserve for vitellogenesis, and, due to the metabolic costs involved, females take a longer time to mature, showing, therefore, delayed maturity when compared to males. These aspects are especially important for conservation. Concerning species conservation, the impact of the larger body size in captive animals on other traits, such as habitat use, must be considered, especially if reintroduction of these animals become necessary. As for the Golden Lanceheads in the island, it is mandatory that the conservation strategies encompass the maintenance of the population of the migratory birds, in order to ensure the energetic income to the snakes.\u003c/p\u003e","manuscriptTitle":"Growth patterns of the Golden Lancehead and their determinants: Conservation strategies for critically endangered species","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-07-18 20:05:10","doi":"10.21203/rs.3.rs-4607766/v1","editorialEvents":[{"type":"communityComments","content":0}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"researchsquare","isNatureJournal":false,"hasQc":true,"allowDirectSubmit":true,"externalIdentity":"","sideBox":"","snPcode":"","submissionUrl":"/submission","title":"Research Square","twitterHandle":"researchsquare","acdcEnabled":true,"dfaEnabled":false,"editorialSystem":"","reportingPortfolio":"","inReviewEnabled":false,"inReviewRevisionsEnabled":true}}],"origin":"","ownerIdentity":"d9fed43e-44df-44db-ae14-56c1b7f74d12","owner":[],"postedDate":"July 18th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"posted","subjectAreas":[],"tags":[],"updatedAt":"2024-11-30T04:23:30+00:00","versionOfRecord":[],"versionCreatedAt":"2024-07-18 20:05:10","video":"","vorDoi":"","vorDoiUrl":"","workflowStages":[]},"version":"v1","identity":"rs-4607766","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-4607766","identity":"rs-4607766","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}