Response to: Robinson et al. (2015) Captive Reptile Mortality Rates in the Home and Implications for the Wildlife Trade. PLoS ONE 10(11): e0141460. doi:10.1371/journal.pone.0141460

Arena et al response (2nd) to Robinson et al.


Robinson et al titled their paper ‘Captive reptile mortality rates in the home (our emphasis) and implications for the wildlife trade’. The authors convey as part of their defence that their conclusions refer to ‘private keepers and breeders of reptiles who attend reptile shows’. ‘Private keepers’ is a term usually ascribed to people who comprise the keepers of the 1.1+ million reptiles in homes generally. Furthermore, the paper, in particular the title, Abstract and Conclusion (three of the primary sections gleaned by readers for an overview of paper content), is very general in its application, again, referring to ‘the home’. A title that does not properly represent the contents is not a good foundation or messenger for a scientific article. Robinson et al redirect readers to their original paper for clarifications, which of course, is completely proper, to attain their own conclusions. However, in our view, this does not, as we will outline, aid in their defence. A good paper will have emphasised its limitations and applicability – spurring further research to address such deficits.

In their main paper, Robinson et al make numerous statements that imply their work has a broader implication beyond mere traders and keepers that attend shows (pet markets). For example, the authors state: “Given the lack of published studies and widely conflicting available reports, it is evident that current primary data on mortality rates of reptiles in the home would be welcomed by all interested stakeholders. Obtaining data on mortality of reptiles in the home relies on gathering information from consumers.” and “We investigated mortality rates of pet reptiles amongst domestic reptile keepers at two major herpetological events in the UK…”. The authors do not qualify these statements to infer they apply to anything other than ordinary homes of reptile keepers, and from the Introduction onwards the generality of their paper’s messaging is that the authors’ study (again) relates to the general ‘home’ environment and thus is relevant to the general population.

In addition, in the Discussion, the authors state: “We estimated the overall mortality rate of pet reptiles… amongst private breeders and keepers of reptiles, to be 3.6% within the first year of acquisition, which is considerably lower than some previous estimates.” However, here the only relevant estimates to which the authors are referring, and which they cite in their main paper, are Lawrence (1987), Clark (unpublished), and Toland et al (2012). We will not include the findings of Clark further here on the basis of that being an undergraduate essay. Therefore, because Lawrence (1987) and Toland et al (2012) relate to mortality in the home in general (rather than in trade and transport or other specific sectors), and because Robinson et al (2015) seek to compare their paper with these publications, it follows that the authors do effectively present their data as addressing mortality issues in the same context as these earlier works, that is, pertaining to the general population of reptiles in the home. At the very least, and regardless of methodology problems, we find the authors descriptions of mortality relevance ambiguous, and in this regard alone their paper has been unhelpful to animal welfare science because it is manifestly very open to convenient use by exploitative vested interests.

Regardless, Robinson et al are now unambiguously stating that their data do not apply to animals in the general private population. However, even if Robinson et al meant to comprehensively convey that their study does not relate to reptiles in general households throughout the country then it remains that the title of their paper implies greater relevance that it covers. Even if we were to accept (which we do not) that the authors aRRT methods were appropriate for the special dynamics and legal conundrums associated with the interview process, the authors ought to have titled their paper something like: ‘Declared unverified mortality rates among reptiles possessed by a limited sector of private keepers, covert and overt animal traders, and hobbyists’.

Although we have already cited the following example in our previous response we again draw attention to Robinson et al’s assertion that: “trends that are not statistically significant are interpreted cautiously”. However, in their Abstract they state that “results suggest that mortality rates may be lowest for captive bred animals”. Whereas in the body of the text the authors acknowledge that the difference in mortality rates between captive-bred, wild-caught or captive-farmed is not significant. Therefore, Robinson et al assign an insignificant message to a prominent position as a finding in their Abstract.

Robinson et al’s elaborate claim: “Over 56% of respondents felt that their answers were protected by aRRT compared to 13% who did not….’ We clarify here that the ‘highly significant 31%’ mentioned in Arena et al.’s comment regarding ‘respondent honesty’ refers to those who stated that they felt their answers were 'neither protected nor unprotected' (therefore, indifferent).” However, in answer to a direct question, 33.3% of those surveyed said that they thought it was unlikely that people would tell the truth about the quantity of their reptiles that had died (see S1 Table in appendix). Given the unlawful nature of much of the animal selling at the surveyed pet markets and the promotion of the survey for propagandist reasons, the actual number of dishonest respondents could be far greater.

An associated problem that we previously highlighted was the aRRT model used, which, in the interests of face-saving and anonymity, gave a numerical buffer of no more than ten to disguise the actual number of reptile mortalities. Clearly this model could not fulfill its purpose where keepers and dealers may have lost many tens or hundreds of animals over the five-year period. The authors report that an undergraduate student essay by Clark (unpublished), which was produced in association with reptile traders and trade representatives, informed the choice of aRRT model used (see S2 appendix). Clark’s (unpublished) essay is also liberally cited throughout Robinson et al’s study.

A key problem with the methodology of Robinson et al’s article was the illicit nature of animal selling at the events at which reptile keepers/sellers were surveyed. This important context was substantively omitted but is essential when considering the honesty of respondents’ answers on which the study relies. We maintain that asking questions dependent on honesty of respondents at two events with inherent dishonesty issues is incapable of providing reliable data, and instead constitutes a fundamental flaw in the methodology. Incidental or orchestrated dishonesty is not resolvable with the stated methodology.

Relatedly, Robinson et al seek to defend their data and the ‘honesty of respondents’ by citing studies that they claim have worked successfully for sensitive questions in relation to conservation and illegality issues. However, research into ‘sensitive conservation’ issues (arguably as contentious as mortality questions) has been unable to provide reliable, or even very approximate, figures. For example, the percentages for illegally traded wildlife have been cited at 25 – 44% (Karesh et al, 2007; Natusch & Lyons, 2012), and the global value of illegal wildlife trade is estimated at between $10-20bn (Webb, 2000; Rosen & Smith, 2010) – ergo both ‘sensitive’ subject estimates offer gross variation. The authors themselves comment that it is difficult to verify whether reptiles are captive-bred or wild-caught animals because there “may be some degree of sensitivity surrounding the topic”. Accordingly, on these key ‘sensitive’ questions, no research has provided reliable data using any method, not least because of the paradigm that, illegal, potentially illegal, or embarrassing activities are by their nature extremely difficult to ascertain.

Robinson et al comment that “as the intention of our study was to gather data on a wide range of reptile species in the trade, carrying out the survey at events attended by keepers of a wide range of species was entirely appropriate, and avoided potential biases associated with a focus on a narrower range of species that may be widely traded but unrepresentative of all species in the trade.” We agree with Robinson et al that studying a narrow set of species would not be appropriately representative. However, contrary to Robinson et al’s claim, the range of reptile (and amphibian) species present at the two events they studied did not represent all species in the trade, in fact not even close. For example, Arena et al (2012) recorded 178 species between three events (one of which was a same event studied by Robinson et al 2015, and two of a similar nature), whereas approximately 500 reptile species alone may occur in trade (Auliya, 2003). Accordingly, if Robinson et al considered a wide range of species to be relevant to reliable data, then this is another element of their data that was not representative.

Robinson et al comment that: “Although Arena et al. quote a range of 1-1003 snakes kept by respondents when referring to ‘respondent biases’ and ‘respondent recall’, we actually reported that a median of nine snakes, two chelonians (range: 1-30) and/or five lizards (range: 1-60) were kept by respondents over five years. This illustrates that most people did not keep very high numbers of animals that may have made it difficult for them to recall how many had died within the 1st year of acquisition without detailed records.” Robinson et al’s study took place at events where attendees (thus potentially all interviewees) are known to grossly understate the numbers of animals they possess and sell, partly due to risk of perception as commercial traders and thus risk of exposing themselves to prosecution or targeting for relevant taxation. Therefore, declarations giving rise to a median number are largely irrelevant. Regardless, the remaining data are sufficient to dramatically skew the median number of animals claimed to be held.

Regarding the Toland et al (2012) study, Robinson et al comment that: “Moreover, the taxa on which the figure of 75% mortality is based are not stated, nor are the data in the public domain. It is therefore currently impossible to assess the validity of Toland et al’s (2012) findings in relation to ours.” Unlike in Robinson et al’s main paper, Toland et al’s (2012) study represented all taxa.

In Toland et al, the approach taken involved total numbers (derived from government and declared trade data including some of the same material used in Robinson et al, 2015) of reptiles entering the trade and keeping pipeline annually compared with total numbers of surviving reptiles (based on entirely independent surveys by statistical data gatherers utilised by government for their data quality and relevance) in homes year on year. Toland et al’s methodology was reduced and summarised by the publisher, not the authors, for spatial reasons after extensive peer-review for data and analytical robustness. For the avoidance of doubt, Toland et al’s (2012) article appeared in a peer-reviewed publication after a long and robust peer-review process. Nevertheless, Toland et al’s (2012) data has been incorporated into an even more extensive, multi-animal class study, to appear in an open access, and less spatially restrictive, journal later in 2016/17.

We agree with Robinson et al that the international trade in exotic pets is a significant cause for conservation concern. In our view, concern extends as much to the welfare of these animals as to any other aspect of the pressures on wild animals (whether wild-caught or captive-bred) for the exotic pet trade. However, as we predicted in our first response, Robinson et al’s study is being utilised by reptile traders and keepers (including those who assisted Robinson et al with their study) as a device to lead (or mislead) others, particularly those responsible for regulating trade and keeping, into believing that reptile mortality ‘in the home’ is low. In part, this misuse of information is unsurprising, given the exploitative nature of wildlife traders and keepers and the misleading title and ambiguous results of Robinson et al’s paper. Accordingly, we do not consider that Robinson et al’s response should alter our primary comments.

Phillip C Arena BSc(Hons) PhD
Robert Laidlaw CBiol MRSB
Angelo J L Lambiris NHED MSc PhD CBiol FRSB
Thomas E S Langton BSc(Hons) CBiol FRSB
Anthony Pilny DVM DABVP
Catrina Steedman BSc(Hons) MRSB
Elaine Toland BSc(Hons) MRSB FRSPH
Clifford Warwick PGDipMedSci CBiol CSci EurProBiol FOCAE FRSB

References

Arena, P. C., Steedman, C., & Warwick, C. (2012). Amphibian and reptile pet markets in the EU: An investigation and assessment. Animal Protection Agency, Animal Public, International Animal Rescue, Eurogroup for Wildlife and Laboratory Animals, Fundación para la Adopción, el Apadrinamiento y la Defensa de los Animales, 52.

Auliya, M. (2003). Hot trade in cool creatures: A review of the live reptile trade in the European Union in the 1990s with a focus on Germany. TRAFFIC Europe, Brussels, Belgium.

Karesh, W. B., Cook, R. A., Gilbert, M., & Newcomb, J. (2007). Implications of wildlife trade on the movement of avian influenza and other infectious diseases. Journal of Wildlife Diseases, 43(3), S55.

Lawrence, K. (1987). The tortoise trade—Mortality in transport: An analysis of 21 years of importations into the United Kingdom. British Veterinary Journal, 143(5), 432-438.

Natusch, D. J., & Lyons, J. A. (2012). Exploited for pets: the harvest and trade of amphibians and reptiles from Indonesian New Guinea. Biodiversity and Conservation, 21(11), 2899-2911.

Rosen, G. E., & Smith, K. F. (2010). Summarizing the evidence on the international trade in illegal wildlife. EcoHealth, 7(1), 24-32.

Toland, E., Warwick, C., & Arena, P. C. (2012). The exotic pet trade: pet hate. Biologist, 59(3), 14-18.

Webb, J. T. (2000). Prosecuting Wildlife Traffickers: important cases, many tools, good results. Vt. J. Envtl. L., 2, 1.