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.