Despite their commercial importance in many parts of the world, the basic biology of many tropical snakes remains poorly understood. We gathered data on two species of semifossorial snakes – Cylindophis ruffus (N = 20) and Xenopeltis unicolor (N = 92) collected for the commercial trade in meat near Cirebon, West Java. The sample of harvested specimens was strongly male biased in both taxa but differed depending upon the month of collection. Male X. unicolor were larger than females, but there was no apparent sexual dimorphism in C. ruffus. Enlarged ovarian follicles and testes in certain months and not others (e.g. June and July) suggests strong seasonality in reproductive timing. Despite the small sample sizes, our data provide more detail on these topics than has been available in earlier literature.

Homalopsid snakes are diverse and abundant along the muddy edges of waterbodies in tropical Asia, but are understudied. We examined carcasses of 287 snakes (58 Fordonia leucobalia, 229 Hypsiscopus plumbeus) collected for the commercial leather industry in Cirebon, West Java. In both species females attained larger sizes than males, were heavier-bodied and had relatively shorter tails. Females outnumbered males in our samples. Both species are viviparous, with litter sizes increasing with maternal body size. Reproduction occurs over much of the year, but with seasonal variation in follicle sizes, testis volumes and the proportions of gravid individuals. In combination with studies on three other homalopsid species in the Cirebon area, our data reveal interspecific similarities in some traits (such as viviparity and female-larger sexual dimorphism) but divergence in others (e.g. reproduction was more seasonal in H. plumbeus than in F. leucobalia). High rates of reproduction buffer these species against commercial offtake.

We collated and analyzed information from multiple sources to assess conservation implications of the commercial trade in reptile skins from 2000 to 2020. Of > 71 million skins reported over that period, the most heavily-traded taxa were three crocodilians (Caiman crocodilus, Alligator mississippiensis, Crocodylus niloticus), three snakes (Homalopsis buccata, Cerberus rhynchops, Malayopython reticulatus) and one lizard (Varanus salvator). In total, 70% of exports were from Indonesia, Colombia, United States, Malaysia, and Argentina, and 78% of imports were from Singapore, Italy, Mexico, France, and Germany. Approximately 45% of traded animals were reported to be collected from the wild, with most others being captive-bred (37%). Traded species exhibited highly specific traits including large body size, broad distributions, and high reproductive output. The squamates in trade generally have relatively early age at maturity and large clutch sizes. Together, these life history and ecological traits make traded species amenable to sustainable use. Most reptiles in the skin trade are ranked as Least Concern by the IUCN, and reptile species traded for skins are less threatened overall than non-traded species. Despite the large volume of commercial trade in reptile skins globally, this harvesting appears to be biologically sustainable in the vast majority of cases.

This article belongs to the collection: Sexual Dimorphism and Reproduction in Snakes.

Dissections of 427 Javan Keelbacks, Fowlea melanzosta (Gravenhorst, 1807) - 263 females, 164 males, collected by commercial hunters in the Cirebon area of West Java, Indonesia, provided information on sexual dimorphism and reproduction. The harvest consisted mostly of adult snakes, especially females, perhaps reflecting greater commercial value of larger animals. Females grew much larger than males but had shorter tails relative to body length. Clutch sizes ranged from 5 to 46 (mean = 21.0) and increased with maternal body size. Adult females produce a single clutch of eggs annually, prior to the onset of the rainy season, and likely remain with those eggs until hatching (based on behaviour of the closely related F. piscator in India). Testis volumes in adult males showed strong seasonal variation. The high fecundity and ecological flexibility (diverse diets, use of disturbed habitats) of this species is likely to buffer it against any population-level impact of commercial harvesting.

Abstract Evaluating sustainable levels of offtake is central to regulating the commercial harvest of wildlife species, but methods developed for temperate-zone mammal and bird species may be inapplicable to tropical rainforest reptiles. For example, population viability models require information on abundance and on rates of growth, maturation, survival, and reproduction. For some intensively harvested reptiles - especially well-camouflaged ambush predators in densely vegetated habitats - such data are difficult to obtain. The feasibility of gathering this information is central to current debates about how best to evaluate the sustainability of commercial harvesting of reticulated pythons ( Malayopython reticulatus) in Asia. Over a five-year period, we conducted 527 riverside surveys (with mark-recapture) for this species in a protected area in Sabah, Malaysia. Detectability of pythons was dependent on moon phase but always low (mean = 20%); and the total number of pythons captured ( N = 159 total, N = 83 during standardized surveys) and recaptured ( N = 25) despite that intensive long-term effort was insufficient to enable robust mathematical modelling. Our results suggest that attempts to base sustainable-harvesting targets for M. reticulatus on mathematical models are futile, and that repeated surveys of the attributes of harvested specimens provide a more reliable basis from which to evaluate sustainability.

Indonesian Spitting Cobras (Naja sputatrix) are abundant in agroecosystems on Java and adjacent islands, are a significant cause of snakebite, and are harvested commercially for their skins and meat. We examined carcasses of 159 snakes at processing facilities in and around the city of Cirebon in West Java. Males outnumbered females, and most specimens were adult. Males were more heavy-bodied than females of the same body length, and had longer tails. Gonadal size and condition and energy (fatbody) storage was seasonal, with females in our sample containing oviductal eggs during September–October and in February; we infer wet-season oviposition, although no data were available for December–January. Clutch size averaged 14, ranging from 6 to 23 eggs. Comparison of this sample with one taken 25 years previously in Central Java, using the same methods, revealed a similarity in male-biased sex ratio and the numerical preponderance of adults. Snakes of both sexes averaged larger in the current sample from West Java than in the earlier study from Central Java, likely reflecting geographic variation rather than any impacts of commercial harvesting over the intervening period. Exploitation of agricultural habitats, broad diets, high fecundity and formidable venom render this species resilient to current levels of commercial offtake.

Context Reflecting their large body sizes, wide geographic distribution and abundance in anthropogenically disturbed southeast Asian habitats, Indo-Chinese ratsnakes (Ptyas korros) are heavily exploited for skins, meat, and traditional medicine.Aims We aimed to quantify sexual dimorphism and reproductive biology of Ptyas korros to broaden our knowledge of population abundance in West Java, Indonesia.Methods We measured and dissected 817 snakes at six processing facilities near Cirebon, West Java.Key results Males outnumbered females among the harvested sample except in January, and >80% of specimens were adults. Males matured at smaller sizes than females, but attained larger maximum sizes and were heavier-bodied than females of the same snout-vent length. Relative tail lengths did not differ between the sexes. Mean fat-body sizes and gonadal volumes varied among seasons, but egg-laying occurred in most months of the year. Clutch size range was 1-14 eggs (mean = 7.12), and increased with maternal body size.Conclusions Early maturation, frequent and relatively aseasonal reproduction, medium-to-large clutch sizes, and broad diets contribute to this species' abundance in disturbed agroecosystems of West Java, enabling these snakes to persist despite heavy harvesting pressure.Implications Our data strongly suggest that offtake of this species in Java is sustainable.

Antaresia is a genus of small (<1.4 m) python species inhabiting mainland Australia, with one species (A. papuensis) recently described from New Guinea and several islands in the Torres Strait. Currently, only Antaresia maculosa peninsularis is formally known to occur in Cape York Peninsula in northern Queensland on the Australian mainland. We used molecular and morphological data to examine whether populations of Antaresia in northern Cape York comprised several distinct taxa (namely: A. childreni, A. maculosa peninsularis, and A. papuensis). A phylogenetic analysis of the mitochondrial cytochrome b locus recovered samples of Antaresia from far northern Cape York as part of the same clade as A. papuensis from New Guinea and islands in the Torres Strait. Further to the south, we found that A. m. peninsularis and A. childreni occur in sympatry together. With the possible exception of colouration and pattern, we found no aspects of scalation that allow for easy and consistent visual distinction between the three taxa on Cape York. We discuss our finding in the context of biogeography of the region.

Elucidating factors that drive microhabitat selection in a species is important for informing the conservation management of the species. For species that use microhabitats as long-term refuge sites, selection pressures are likely to be strong because the microhabitat must fulfil their eco-physiological and life history requirements. Smaug giganteus (Sungazer) is a threatened (Vulnerable) cordylid lizard species in the highveld grasslands of South Africa - a key agricultural area in the country. Individuals dig burrows as refuges, which increases their sensitivity to habitat transformation. In addition, previous attempts to translocate populations have failed due to a lack of knowledge about their specific microhabitat requirements. We assessed microhabitat characteristics that may influence burrow site selection by measuring vegetation characteristics surrounding Sungazer burrows and comparing these to vegetation at randomly selected sites. We also recorded orientation, aspect, soil composition, and the presence of other animal dung. Sungazers selected sites with sparse vegetation cover, and where grass height was short, but had no preference for soil composition. There was no relationship between the presence of ungulate dung and the placement of Sungazer burrows. Most Sungazer burrows were orientated in a northerly direction on north-facing slopes, suggesting that burrow placement has thermoregulatory advantages. We recommend that to identify suitable sites for Sungazer translocations, landscapes are thoroughly surveyed with cognisance to the findings in this study, and that a soft-release translocation protocol follows to maximise translocation success.

Large (>3 m) slender-bodied rat snakes are abundant in agroecosystems of southern Asia and are heavily exploited for their skins and meat. We examined 216 specimens killed at commercial facilities in Cirebon, West Java, to quantify morphological and reproductive traits and evaluate harvest sustainability by comparing this sample to one taken 25 years previously. The snakes we examined were mostly adults, and mostly male. Females were less heavy-bodied than males of the same body length, matured at a larger size than males, but attained smaller maximum sizes. Reproduction and energy (fatbody) storage was seasonal in both sexes, with females containing oviductal eggs primarily during the annual wet season. Clutch size averaged 12.6 eggs and increased with maternal body size. Comparison of the two samples taken 25 years apart revealed strong similarity in sex ratio, the numerical preponderance of adults, body sizes at sexual maturation and mean adult body sizes, sexual dimorphism in body length and mass, reproductive seasonality in females, mean fecundity, and the relationship between fecundity and maternal body size. That consistency suggests that commercial harvesting over the intervening period has not affected the biological traits of rat snake populations, consistent with a sustainable level of offtake.

Diminishing natural resources and increasing climatic volatility are impacting agri-food systems, prompting the need for sustainable and resilient alternatives. Python farming is well established in Asia but has received little attention from mainstream agricultural scientists. We measured growth rates in two species of large pythons (Malayopython reticulatus and Python bivittatus) in farms in Thailand and Vietnam and conducted feeding experiments to examine production efficiencies. Pythons grew rapidly over a 12-month period, and females grew faster than males. Food intake and growth rates early in life were strong predictors of total lifetime growth, with daily mass increments ranging from 0.24 to 19.7 g/day for M. reticulatus and 0.24 to 42.6 g/day for P. bivittatus, depending on food intake. Pythons that fasted for up to 4.2 months lost an average of 0.004% of their body mass per day, and resumed rapid growth as soon as feeding recommenced. Mean food conversion rate for dressed carcasses was 4.1%, with useable products (dressed carcass, skin, fat, gall bladder) comprising 82% of the mass of live animals. In terms of food and protein conversion ratios, pythons outperform all mainstream agricultural species studied to date. The ability of fasting pythons to regulate metabolic processes and maintain body condition enhances food security in volatile environments, suggesting that python farming may offer a flexible and efficient response to global food insecurity.

Context Masked water snakes (Homalopsis buccata, Homalopsidae) thrive in the muddy edges of agricultural ponds and canals in densely populated areas of West Java, Indonesia, and are harvested by local farmers to protect fish stocks and to provide meat, skins, and medicines for commercial use. Aims Here, we aimed to quantify sexual dimorphism and reproductive biology of H. buccata, so as to deepen our knowledge of the species’ inherent ability to withstand commercial harvests. Methods We examined carcasses of 4286 snakes at six processing sites to quantify biological attributes (e.g. sexual dimorphism in body size and shape, seasonality of reproduction, fecundity, reproductive frequency), with emphasis on traits that affect the ability of snake populations to withstand this intensive harvesting. Key results The snakes we examined were primarily adults (<1% juvenile), with approximately equal numbers of males and females except in January (when females comprised >90% of specimens). Females grow larger than males, and they are more heavy-bodied but shorter-tailed than are males of the same snout–vent length. Reproduction is seasonal in both sexes, with testis volumes decreasing to a minimum over the period August to November (late dry season) when most adult-size females were gravid. Litter sizes ranged from 1 to 37 (mean 12), increasing with maternal body size, with ~75% of females reproducing each year. Conclusions On the basis of these results, we infer that the life history of H. buccata (viviparity, high fecundity, frequent reproduction, rapid maturation) renders it inherently resilient to harvesting, especially because that offtake is based on males as well as females. Because a lack of sustainability is evident only in hindsight, regular monitoring of the trade could assure that any problems are detected rapidly. Implications To further buffer these populations from the impact of harvest, hunting could be restricted during January (a time when gravid females are disproportionately vulnerable) and the largest snakes (females, with high fecundity and reproductive frequency) could be excluded from harvests.

Context Unsustainable harvesting can threaten wildlife populations and jeopardise the livelihoods of people relying on wildlife resources. Although millions of rainbow mudsnakes (Enhydris enhydris) are harvested from wetland agroecosystems in tropical Asia each year, few detailed studies have been conducted on the biology of this species. Aims We aimed to address this knowledge gap by examining the reproductive biology and resilience to harvesting of E. enhydris, collecting from agricultural landscapes in West Java, Indonesia. Methods We measured and examined 1731 specimens that had been collected and killed for skins and meat near the city of Cirebon in West Java. Key results Most snakes that we examined were adults (94% of females, 88% of males), with females outnumbering males overall (69% female). Sex ratios varied seasonally and among processing facilities. Females attained larger body sizes than males, were more heavy-bodied, and had shorter tails relative to snout–vent length. Reproductive traits varied among months, with two peaks in the incidence of gravid snakes occurring in March and September. Litter sizes averaged 11.2 (range 2–31) and increased with maternal body size. About half of the adult females were reproductive (vitellogenic or gravid) at the time of collection. This proportion increased with maternal body size, such that 60–70% of large females were reproductive at the time of collection, suggesting that some females may produce two litters per year. Conclusions Rainbow mudsnakes remain exceptionally abundant in West Java, despite significant habitat modification and intensive harvesting. Implications The ability of this species to exploit anthropogenic subsidies in disturbed agricultural landscapes gives it access to plentiful food, and the resultant early maturation, frequent reproduction, and high fecundity enable it to withstand high levels of commercial offtake.

Context Across much of its geographic range, the masked water snake, Homalopsis buccata, is harvested each year in large numbers, questioning the sustainability of that offtake. Aims To quantify abundance and demography of water snakes in anthropogenically disturbed habitats in an area of West Java, where these snakes are subject to intensive harvest. Methods We accompanied professional snake-collectors, and conducted our own surveys of ponds and irrigation canals, to record the numbers and attributes (species, sex, size, etc.) of snakes that were captured using a variety of methods. Key results Snakes of several species were abundant, with mean capture rates of 32 666 snakes km−1 of irrigation canals, and 57 501 snakes km−2 of fishponds (9500 and 43 788 for H. buccata alone). Sex ratios of H. buccata were female-biased in ponds but not irrigation channels. Ponds underlain by deeper mud contained more snakes. Collecting methods varied among habitat types, in a way that reduced collateral risk to commercially farmed fish in ponds. Conclusions These water snakes are extremely abundant in Java, despite high levels of historical and continuing harvest. The inference of low population sizes for H. buccata in Indonesia, as presented in the IUCN Red List, is erroneous. Implications An ability to utilise anthropogenic resource subsidies (in this case, fish farmed in village ponds) allows some native predator species to attain remarkably high abundances, and to withstand intense efforts at harvesting.

Although they are among the most abundant snakes on Earth, and are heavily exploited for their skins and meat, Asian bockadams (or “dog-faced water snakes”, Cerberus schneiderii) have attracted relatively little study across their wide geographic range. Based on dissection of 3,382 snakes brought to processing facilities in and around the city of Cirebon in West Java, Indonesia, we document facets of the biology of these mangrove-dwelling aquatic homalopsids. Females attain larger body sizes than do males, and are heavier-bodied (due in part to greater fat reserves) but have shorter tails relative to snout-vent length. Males showed testicular enlargement late in the year (August-November) but both reproductive and non-reproductive females were found year-round. Litters were large (3 to 45 offspring), especially in larger females. The commercial harvest falls mainly on adult snakes of both sexes, with seasonal variation in sex ratios. Life-history traits such as early maturation and frequent production of large litters render this species resilient to commercial harvesting. Future research should explore reasons for strong variation among facilities in the sex ratios of snakes, potentially identifying ways to focus the harvest on the sex (males) whose numbers are less critical for population viability.

D'Cruze et al. (2022) and Frank and Wilcove (2022) suggest that Challender et al. (2021) misrepresent their research. We reiterate that our intention was not to denigrate any particular study; instead, we aimed to draw attention to contemporary issues in wildlife trade research and highlight ways for research to better inform policy processes. Here, we respond to the points raised in these articles. D'Cruze et al. suggest that we were incorrect to deduce from Harrington et al. (2019) that their position is that “use/trade [in Asian otters as exotic pets] constitutes a threat to the species or is detrimental to wild populations.” This is despite the title of that article being “Popularity of pet otters on YouTube: evidence of an emerging trade threat.” It is difficult to reconcile this title and statements within the article with the assertion that Harrington et al. did not conclude that the pet trade posed a threat to wild populations of Asian otters. However, our primary concern is that Harrington et al.’s analysis of trends in popularity of social media videos of pet otters makes the jump to strongly endorsing an international trade policy (specifically, including two otter species in CITES Appendix I) despite the authors acknowledging that there is no evidence of a link between social media trends and trade trends. Trade bans via CITES may be considered as a sensible precautionary measure by some, but in some instances, they may do more harm than good for species (Challender et al., 2021). To avoid this scenario, the risks and benefits of such proposals should be fully assessed (Cooney et al., 2021). Regarding CITES source code “I,” users of data with this source code should be aware that CITES Parties use this code in various ways and therefore be clear whether data refer to illegal trade or legal (re-)exports of previously seized specimens. Otherwise, trade is likely to be mischaracterized (Lopes et al., 2017). A better method of characterizing illegal trade in CITES-listed species would be to use other available databases (see Supporting Information in Challender et al., 2021) and CITES source code “I” data that can be categorically identified as referring to illegal trade. Regarding Can et al.’s (2019) conclusion that “risks posed by pathogens…associated with the wildlife trade should not be under-estimated,” we agree and add that neither should they be overestimated. Both carry the risk of misleading policy processes. D'Cruze et al. also argue that their errors relating to transaction frequency in CITES trade data were minor and do not fundamentally alter their conclusions. While we acknowledge this, our concern remains that if mistakes made in published articles on wildlife trade are not addressed, there is a risk that they will be perpetuated by other authors in the future. We agree with Frank and Wilcove (2022) that the IUCN Red List of Threatened Species (hereafter “Red List”) can be used to inform the potential adoption of trade measures in CITES. Indeed, the Red List has informed CITES processes since its inception, and the potential for closer alignment is currently being explored. However, Frank and Wilcove (2022) claim that Challender et al. (2021) believe that “…CITES protection (via Appendices I and II) should be reserved for vanishing species whose main threat is international trade …” and cite the Convention text as justification for including species in CITES when trade may only be a contributing threat. They misrepresent our main point, namely that, based on lessons learnt in preceding decades (Cooney et al., 2021), species should be listed based on evidence that doing so is likely to contribute to (and not potentially undermine) their conservation. The precautionary principle which underpins conservation policy is not unidirectional and it cannot be assumed that tighter regulation of international trade, including bans, is always the most precautionary policy option. One of our major criticisms of Frank and Wilcove (2019) was that their recommendations were poorly developed, overlooking critical factors that would impede real-world adoption (Challender et al., 2021). There is far more exposition and “nuance” in their response to our commentary than their original article. We encourage researchers suggesting wildlife trade policy reforms to recognize and address the potential challenges in realistic terms, not least to ensure credibility with those who make and implement policy. Finally, we do not claim in Challender et al. (2021) that specific studies have misled policy; however, where wildlife trade data are interpreted inaccurately in research articles, there is potential to mislead policy processes, and to undermine the role of academic research in informing these processes. We would welcome collaboration with researchers interested in working with us to develop best practice guidelines that ensure that wildlife trade policy is based on the best evidence, appropriately interpreted. D.C. and E.J.M.G. acknowledge funding from the Oxford Martin Programme on Wildlife Trade and the UK Research and Innovation's Global Challenges Research Fund (UKRI GCRF) through the Trade, Development, and the Environment Hub project (project number ES/S008160/1). A.H. is funded by a Kadas Fellowship at Worcester College, Oxford. The authors declare no conflict of interest. All authors contributed to the conception, writing, editing, and reviewing of the manuscript. No primary data were collected for this manuscript and an ethical review process was not undertaken. No primary data were collected for this manuscript. No primary data were collected for this manuscript.

GENERAL COMMENTARY article Front. Ecol. Evol., 25 April 2022Sec. Conservation and Restoration Ecology https://doi.org/10.3389/fevo.2022.889234

Although giant snakes are abundant in some tropical forests, their ecology is far less well-known than for smaller species of snakes in cooler climates. Information on spatial ecology can clarify management issues such as the sizes and types of habitats needed for conservation. We radio-tracked 27 scrub pythons ( Simalia amethistina; snout-vent lengths 2.02 to 3.70 m) in Cape York, near the northeastern tip of Australia, for a mean period of 426 days (up to 1001 days) per snake. Home ranges were larger in males than females (means 0.60 vs. 0.28 km 2 ) and overlapped considerably among individuals. All snakes used rainforest habitat, but seasonal shifts into open woodland were common. Snakes were active primarily by night, with larger snakes hunting less of the time overall, and more often by day. Hunting behaviour was seen more often during the wet season than the dry season. Average daily displacement was < 10 m, typically involving a shift from diurnal refuge to nocturnal ambush-site. A reliance on sit-and-wait predation results in small home ranges and limited movements, despite the large body size of this species.

The CITES treaty is the major international instrument designed to safeguard wild plants and animals from overexploitation by international trade. CITES is now approaching 50 years old, and we contend that it is showing its age. In stark contrast to most environmental policy arenas, CITES does not require, encourage, or even allow for, consideration of the impacts of its key decisions—those around listing species in the CITES Appendices. Decisions to list species in CITES are based on a simplistic set of biological and trade criteria that do not relate to the impact of the decision, and have little systematic evidentiary support. We explain the conservation failures that flow from this weakness and propose three key changes to the CITES listing process: (1) development of a formal mechanism for consideration by Parties of the likely consequences of species listing decisions; (2) broadening of the range of criteria used to make listing decisions; and (3) amplification of the input of local communities living alongside wildlife in the listing process. Embracing these changes will help to ensure CITES decisions more effectively respond to the needs of wildlife in today’s highly complex and dynamic conservation context.