Opposing Lethal Wildlife Research When Nonlethal Methods Exist: Scientific Whaling as a Case Study

Use of animals in research remains controversial because of clear differences in how people perceive the relative worth of certain species in any calculation of known costs (in suffering) and future benefits (usually in terms of advances in human or animal health). When public attitudes toward the use of animals for experimental and teaching purposes are surveyed, the majority of people favor such practices so long as the procedures are important and suffering is minimized (e.g., Pifer et al. 1994; Franklin 2007; Crettaz von Roten 2012). Specific attitudes can differ from country to country, by gender, and how well informed survey respondents are (Swami et al. 2008; Ormandy and Schuppli 2014). The species of animal used can also influence public attitudes (Ormandy et al. 2012).

Most discussion of the moral status of research animals has centered on laboratory-based experimentation in biomedicine. It is only relatively recently that the increasing role of interventionist conservation research involving free-living wildlife has been the focus of ethical debate (e.g., Monamy 2007). Discussion of individual laboratory animal welfare and experimentation has expanded to include debate over the relative worth of free-living individuals and their interest in not suffering, together with the moral value of studying populations of wildlife species (e.g., Bekoff 2007).

Ethical discussions often refer to appropriate interactions between humans, but the terminology is no less valid when exploring interactions between humans and other animals. Ethos refers to a predominant community spirit from which a society's ethical bases are derived; morality refers to the distinction between right and wrong within that community spirit. In any ethical discussion, consequentialist objections to an action relate to the harmful or beneficial consequences of that action in a utilitarian context. An example; in March 2000, after public outcry, the Australian Government banned the use of hot-iron identification branding of seals and sea lions on the basis that an individual animal's interests (in avoiding acute pain) outweighed long-term conservation benefits in understanding certain population parameters of pinniped species once hunted to near extinction. The ban triggered numerous arguments for and against research involving iconic wildlife (Monamy 2007). Despite all ethical and legislative permissions being granted for the research, and all researchers working within the prescribed permissions' boundaries, all research was stopped when video footage of the branding was shown in the media (Monamy 2007). This illustrated that wildlife research, at least within an Australian ethos, was viewed by many in society as a privilege granted to scientists by the public via their bureaucracies, rather than a right. Of relevance to the present discussion, the ban on hot-iron branding may have hastened the development of effective noninvasive methodologies, such as photo identification based on whisker spot patterns, to gain the same data for ecological studies of free-living otariid species (Osterrieder et al. 2015).

The “three Rs” principles of humane experimental design (replacement, reduction, and refinement; Russell and Burch 1959) were developed to promote acceptable methodologies when using sentient animals in laboratory research. They have been adopted as the ethical foundation of modern animal experimentation in many parts of the world (Monamy 2009). Replacement proposes the use of nonsentient organisms rather than higher animals for experiments. Reduction refers to obtaining the best quality and most precise information with the smallest possible number of animals. Refinement, as an active principle, emphasizes keeping any pain, suffering, or other harm that may be caused to a research animal to a minimum. The principle emphasizes the need to balance costs and benefits of any proposed research to make sure that harm is absent or minimal and that benefits are maximal. The three Rs were originally written for laboratory animal experimentation; there were no formalized ethical parallels for research involving free-living wildlife. We argue, however, that refinement has particular relevance and applicability.

Debate about permissible scientific research involving wildlife generally focusses on the welfare of sentient beings and intensifies when invasive or environmentally disruptive research is conducted, or proposed, on an iconic, or highly valued, free-living species (Monamy 2007). Charismatic megafauna populations are especially valued by many nations for many reasons, including high aesthetic appeal, conservation status, certain economic values, or as symbols of cultural significance (Lavigne 2005). How, then, should we proceed when such iconic wildlife is subjected to invasive procedures, or when highly valued sentient species are killed for scientific data collection?

Here we consider lethal scientific whaling in the Antarctic Ocean to illustrate the conflicting opinions of two nations' governments with strong views on the issue, Australia and Japan. Differing attitudes to animals among cultures have often led to intense debate about balancing intrinsic value and the instrumental worth of wildlife. Intrinsic value, in this sense, we define as the value an individual animal has “for its own sake” regardless of any value to humans. Here, instrumental worth refers to a value of wildlife to humans, as, for example, food, tourist opportunity, or research subject. Internationally, opinions on the relative value of whales have shifted increasingly toward prioritizing intrinsic value, with countries progressively abandoning whale hunting in favor of ecotourism opportunities that rely on ongoing conservation and management, particularly of vulnerable and threatened whale species (Bekoff 2007).

The management of whaling is governed by the International Convention for the Regulation of Whaling (ICRW), 1946, supported by the governments of 88 nations. Under this convention, a zero catch limit on commercial whaling (International Whaling Commission [IWC] 1946) came into effect in 1985, with three exceptions that allowed some whaling nations to continue harvesting. The exception provisions were utilized by: 1) Norway and Iceland, who continue to conduct commercial whaling under the provision that any member state could object to the ICRW within 90 d of its declaration and not be bound by it; 2) Alaska, Chukotka (Russian Far East), Greenland, and Bequia (West Indies), where Aboriginal subsistence whaling, which is categorized differently by the IWC and not subject to the moratorium, continues to take place; and 3) Japan, utilizing Article VIII of the ICRW to pursue special-permit whaling, or “scientific whaling” (see Table 1 for a summary of programs and objectives).

The Japanese Whale Research Program under Special Permit in the Antarctic (JARPA) commenced in 1987, continuing until 2005. Japan then initiated the JARPA-II program (2005–2014). Between 1987 and 2014, Japan killed 10,710 whales under special-permit whaling in the Antarctic (IWC 2015a). The scientific value of the JARPA and JARPA-II programs came under intense scrutiny when Australia initiated proceedings against Japan in the International Court of Justice (ICJ) in the Hague in 2010 (ICJ 2010). The ICJ delivered the decision on the case “Whaling in the Antarctic (Australia v. Japan: New Zealand intervening)” on 31 March 2014, ruling that Japan's whaling was not for purposes of scientific research and that the Antarctic whaling program (JARPA-II) should cease immediately (ICJ 2014). The legal arguments by Japan and Australia have been discussed in detail elsewhere (e.g., De La Mare et al. 2014; Clapham 2015). Briefly, the question was whether JARPA-II was a commercial whaling operation that included some science (illegal within the ICRW framework), or was it conducted exclusively for scientific research (legal under ICRW)? Japan claimed that their whaling program was within the ICRW framework (i.e., exclusively for scientific research) and was, as such, legal. Australia argued that it was a method to circumvent the zero catch limit imposed on commercial whaling by ICRW and was not primarily for scientific research purposes (Clapham 2015). Despite the ICJ's landmark decision in favor of Australia's case against Japan (Simmonds 2014), it was predicted that the ICJ decision would only represent a temporary setback for Japanese whaling (Clapham 2015). Indeed, in November 2014 the government of Japan submitted a new special-permit proposal to the IWC scientific committee (New Scientific Research Program in the Antarctic Ocean). This research program then commenced in the 2015/2016 Antarctic season (IWC 2015b). Japan's rationale for lethal scientific whaling in the New Scientific Research Program in the Antarctic Ocean application stated that the importance of scientific research in the Antarctic Ocean is its “…potential of abundant living resources that could be sustainably exploited for food” (IWC 2015b). Japan continues to argue that nonlethal methodologies are not adequate to answer their research questions.

Given that nonlethal methodologies in marine mammal research are highly advanced and readily utilized (see Hunt et al. 2013 for a comprehensive review), we argue that lethal methods are outdated and obsolete. Briefly, for example, in early dietary studies involving free-living marine wildlife, lethal sampling often was the simplest method available. However, recent studies involving stomach flushing of sharks (Barnett et al. 2010; Hammerschlag and Sulikowski 2011) and elephant seals (Daneri et al. 2015), fecal studies of fur seals (Gallo-Reynoso and Esperón-Rodríguez 2013) and penguins (Deagle et al. 2007), and stable isotope analysis of sea turtles (Shimada et al. 2014) all illustrate how nonlethal methodologies can be made best practice for marine species. In cetacean biology, whale abundance trends and biological parameters can be obtained via boat surveys, land-based observations, and mark–recapture studies. Recently, Peel et al. (2015) used passive acoustics to detect vocalizing whales (significantly increasing encounters when compared with visual detections alone), and, together with prioritizing biopsy data over photograph identification (when the choice arose), created a suitable method to estimate the abundance of circumpolar Antarctic blue whales (Balaenoptera musculus). Whale blow is increasingly being utilized for novel measures such as biogenic volatile organic compound profiling, which can be used to assess the health and physiological processes within an animal (Cumeras et al. 2014). Nonlethal whale blubber biopsies can be used for a large variety of studies and parameters including endocrinology (Vu et al. 2015), lipid and fatty acid and diet profiling (Waugh et al. 2012), as well as toxicological surveys (Waugh et al. 2014) and effects (Bengtson Nash et al. 2013). Whale skin samples can be used for studies such as enzyme activity and health biomarkers (Waugh et al. 2011; Bengtson Nash et al. 2014) and for epigenetic age estimation (Polanowski et al. 2014). These are just a few examples of the novel technologies that are continuing to expand the wide field of nonlethal marine mammal research.

Yet, the question then is, will mandating protection from harm for individuals, by limiting the availability of lethal methods, necessarily mean that long-term conservation and management of vulnerable populations are jeopardized? We do not believe so. Already the momentum shift to nonlethal methodologies, which is already occurring, continues to stimulate the advancement of novel and ethical techniques. The banning of invasive identification techniques in some species of wildlife has already stimulated a search for an alternative. This can result in more accurate methods, such as face recognition software for gorilla conservation research (Loos et al. 2011). Specifically for whales, a key example is the historical difficulty in accurately ageing large free-swimming cetacean species; this is one of Japan's main arguments for their continuation of lethal sampling (IWC 2015b). A search for a nonlethal alternative led to the development of a novel technique utilizing whale skin to form an epigenetic age estimation method (Polanowski et al. 2014). This technology was based on assays for human age that had recently been developed using age-induced changes in DNA methylation of specific genes (e.g., Hannum et al. 2013). The subsequent humpback epigenetic age assay developed by Polanowski et al. (2014) predicted age (±3 yr) from skin samples (using the three most age-informative cytosine markers). Despite this, Japan continues to argue that “DNA-based methods are not practicable” (IWC 2015b), and that counting of growth-layer groups accumulated in the earplug of whales (only accessible via lethal methods) is the only reliable method. However, there is measurement error in this method (Chittleborough 1959), with a lack of consensus on how many growth-layer groups are produced each year (Chittleborough 1959; Lockyer 1984; Gabriele et al. 2010). The most reliable method for age estimation remains visual identification of individuals that were first seen as calves (Polanowski et al. 2014). Using this example, we urge that any argued benefit of counting growth-layer groups over humpback epigenetic age assays does not outweigh the individual suffering caused by harpooning, which by general and scientific standards is deemed inhumane.

Lethal sampling of free-swimming whales after harpooning comes at a high cost to individual animals in terms of suffering before death. With data on Japanese killing methods showing that time to death averaged 10 min, with some animals taking up to 25 min to die (Gales et al. 2008), we believe that the continued use of these methods is morally indefensible. Instantaneous death rates are extremely low and time to death are too high (Gales et al. 2008). Comparisons with best practice in the lethal scientific sampling of free-living terrestrial wildlife, in recreational hunting, and in the humane slaughter of food animals show unacceptably low instantaneous death rates and unacceptably high time to death in lethal scientific whaling.

The three Rs principles of humane experimental design (Russell and Burch 1959) provide a framework to minimize suffering, and have not only been adopted as the foundation of modern laboratory animal experimentation among Western nations (Monamy 2009), but are also part of the Japan's regulation of animal research (Japanese Association for Laboratory Animal Science, JALAS 2013). Refinement as a governing ethical principle emphasizes keeping any pain, suffering, or other harm that may be caused to a minimum for each animal used in research. We believe Japan's continued use of lethal whaling methods needs to cease, given that there are proven nonlethal methods available (e.g., epigenetic age estimation). The extent of pain, suffering, and distress to the individual (inhumane killing methods) and lasting harm that might be caused to Antarctic whale stocks (which are still at a small fraction of their prewhaling levels) must thus be assessed, and methods put in place to determine the best ways to minimize these effects (i.e., a ban on lethal scientific whaling).

Refinement emphasizes the need to balance costs and benefits of any proposed research to make sure that any harm to an animal is minimized. So, does that mean that all invasive research involving free-living wildlife should cease? We do not believe so. In the case of scientific whaling, if the welfare costs are weighed and compared with the benefits that long-term population studies provide to the conservation of a species, then nonlethal sampling is demonstrably the best practice and such studies ought to replace all lethal studies. We argue, then, for the continued advancement of wildlife research based on a simple ethical model that privileges individual welfare over conservation outcomes by replacing inhumane lethal methodologies with nonlethal sampling. In a situation where nonlethal methods are not available and humane killing is not achievable, then such research should not be permitted until nonlethal methods have been developed. Using such an ethical model, Japan's lethal sampling of whale populations in the Southern Ocean is unethical because nonlethal methodologies exist (e.g., Polanowski et al. 2014) and because the instantaneous death rates and time to death from harpooning are inhumane. The use of lethal methods by Japanese researchers in the Southern Ocean does not adhere to the refinement principle (Russell and Burch 1959), as adopted by JALAS (2013), and the majority of the Western scientific community (e.g., National Research Council [US] Institute for Laboratory Animal Research 2004).

We believe that current research approaches ought to continue the shift toward prioritizing nonlethal data collection methods in wildlife research. We urge that the ICRW (IWC 1946) be newly negotiated by members of the IWC to exclude Article VIII so that lethal scientific whaling is banned. With further advances in nonlethal wildlife research being reported, we support a shift of thinking toward a new ethically attuned paradigm of modern wildlife research. This has applicability for terrestrial wildlife research as well. For example, in dietary studies, nonlethal sampling of salamanders (Crovetto et al. 2012; Costa et al. 2015) and lizards (Crovetto and Salvidio 2013) by stomach flushing and fecal analyses has already replaced the lethal methods once used. Lethal methods may be traditional in some cultures and conservation disciplines but that doesn't make them a moral “right” within a global community, or a “necessary evil” through which information is gathered. Research must continue to move our understanding of wild animals and their effective conservation and management forward, but only in pace with the advancement of nonlethal methodologies. It must continually strive toward improved data collection methods incorporating a regime of best practice that acknowledges ethical as well as technical advancements. Where a nonlethal methodology is poorly developed and lethal techniques are not humane, research questions ought to go unanswered until an acceptable nonlethal method is developed. Adherence to the ethical principle of refinement ensures that nonlethal research techniques, once available, take precedence over lethal data collection in conservation biology.

We acknowledge the journal Associate Editor and two anonymous reviewers whose comments significantly improved the manuscript.

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