Ethical standards for research on marine mammals

Abstract

Conducting marine mammal research can raise several important ethical issues. For example, the continuation of whaling for commercial purposes despite the international moratorium provides opportunities for scientists to obtain data and tissue samples. In 2021 we analysed 35 peer-reviewed papers reporting research based on collaborations with Icelandic whalers. Results highlighted little consideration or understanding of the legal and ethical issues associated with the deliberate killing of whales amongst those researchers, funding bodies, universities and journals involved. Ethical statements were rarely provided. Those that were written were incomplete. Whilst research using whaling data may seem acceptable to some, it often becomes hard to justify when subject to scrutiny by the media and the public. Thus, there is a particular danger of reputational harm for early career researchers who may become unwittingly involved in such activities. Here we also consider the broader variety of ethical issues raised by non-lethal research (both historical and recent) on marine mammals including tagging and biopsy. We discuss instances where study animals were harmed or even killed and where the public mistook tags for harpoons. Without clear guidelines, reviewers and journal editors are put in an impossible position when considering whether to reject papers on ethical grounds. We propose that for such studies, universities, funders, journals, and permit issuers must require ethical assessments and that journals more effectively implement their existing policies on publishing ethical statements. The professional marine mammal societies need to work together to produce modern ethical guidance. Such guidance should require transparency in the provenance of data and samples while including advice on law, welfare issues, involvement of local scientists, and offshoring. Furthermore, it should require appraisal of and justification for the absolute necessity of invasive procedures. As is already the case in biomedical disciplines, ethical statements should be required in marine mammal science.

Introduction and background

The ethical and animal welfare issues concerning research conducted on marine mammals represents an interesting case study because most species of marine mammals have sophisticated social structures, strong social bonds and are highly sentient. Some populations are highly endangered which means that researchers need to take additional special care to minimise any disturbance or other negative impacts, particularly when attempting to save a species from extinction (Félix and Van Waerebeek, 2021). The movements and migrations of some species mean that they undergo transnational changes through different jurisdictions and legal regimes. Many species of marine mammals are difficult to locate as they live in remote ocean habitats which make them hard to study. Even those animals which live in coastal areas or haul-out on land are only easily visible for a part of their life history. Furthermore, on account of their large body sizes, handling marine mammals in order to take blood samples, attach tags or conduct other invasive sampling is also difficult.

Attempts to catch and restrain great whales (or study those already restrained) have occasionally been made (Beamish, 1978; Ray and Schevill, 1974; Sumich, 2001; Sumich et al., 2001; Wahrenbrock et al., 1974; Winn et al., 1979). But these have often not been successful and even smaller marine mammals present considerable difficulties in this regard, with a risk that the stress from being restrained will be fatal (see below for discussion of vaquita, a species of porpoise) or will compromise their welfare, including concerns such as hyperthermia amongst others. Specific physiological, anatomical and behavioural adaptations (e.g. breath-hold diving), pose challenges in safe and effective anaesthesia that are particular to cetaceans, requiring a high level of technical skill, infrastructure and experience (Dold and Ridgway, 2014).

A separate ethical issue, widespread in (although not unique to) the field of marine mammal science, is the lack of involvement of local scientists, that is, ‘parachute science’ (de Vos, 2020; Stefanoudis et al., 2021). Parachute science typically involves researchers from the Global North conducting their work in the Global South without adequately involving or acknowledging (as co-authors in publications) the local scientists who they often rely upon for the success of their work. It is problematic for multiple reasons, sometimes related to colonialist attitudes and because well-intentioned parachute science can ultimately hinder local conservation efforts (de Vos and Schwartz, 2022). Some scientists are keenly aware of this issue and have encouraged and involved local scientists for many decades. One such example is Koen Van Waerebeek, a prolific author who has worked in Africa, China, the Middle East and Latin America, offering training in marine mammalogy to biologists and encouraging them to publish (e.g. Bilal et al., 2023; Reyes et al., 1995; Sohou et al., 2013). ¹

Given the difficulties of studying marine mammals, a variety of innovative techniques have been developed to study them which are summarised in Ryan et al. (2021). A non-exhaustive list includes: passive acoustics, visual line-transect surveys, video-range tracking, theodolite tracking and scat sampling. Many of these techniques are minimally or completely non-invasive and while ethical assessments should still be conducted, they will likely be much more straightforward. Other techniques such as biopsy sampling, suction cup tagging, photo identification, and the use of drones (see section on drones) may present some ethical issues. We argue that ethical reviews should be conducted for all these techniques.

To consider one of the above research techniques in more detail, passive acoustic monitoring is usually non-invasive where it involves the deployment of hydrophones (underwater microphones) which are either static and attached to the seabed or towed by a research vessel. Recent developments have resulted from improvements in computing power and software that allow sounds to be recognised automatically, and ranges and bearings to tracked animals determined. Passive acoustics can be used to locate and follow individual animals and thus permit some of the other research techniques (such as photo-identification of individual animals) to be used. Despite the above approaches, more invasive techniques, or the use of materials from questionable sources, continue to be used.

Law

The law regarding marine mammals is so complex that some scientists have an incomplete grasp of the legal ramifications in relation to their own research. In Ryan et al. (2021) we used the example of the University of Aberdeen (UK) becoming involved in Icelandic ‘scientific whaling’ in 2003. The head of Life Sciences at the university believed that this whaling was supported by the International Whaling Commission (IWC) when the reverse was the case. In reality the IWC had condemned the practice through a resolution which was adopted by a simple majority of 24 votes in favour and 21 against with 1 abstention. ²

International law is a particularly complex and evolving landscape when it concerns marine mammals. It involves a number of intergovernmental organisations and other bodies that have accrued decisions over their meetings, sometimes for half a century or more.

The IWC (mentioned briefly above) is a key intergovernmental body and thus merits particular focus. It was established under the 1946 International Convention for the Regulation of Whaling and has held meetings annually or biennially since 1948. The IWC takes advice from its Scientific Committee. Initially all of its members were whaling nations but the number of member countries engaged in commercial whaling has decreased with the decline in whaling. Non-whaling countries which were concerned about whale conservation have joined the IWC, together with non-whaling countries that support whaling. As of February 2023, it has 88 members with a range of views on whaling but only two (Norway and Iceland) that conducted commercial whaling during 2022, with varying assessments of compliance with international law. Japan (no longer an IWC member, rendering its whaling legally problematic) also caught whales for commercial purposes in 2022.

The best-known IWC decision is the 1982 moratorium on commercial whaling, but other decisions include earlier restrictions of whaling on various whale populations, the designation of whale sanctuaries and other aspects of the regulation of whaling including welfare issues such as the banning of the cold (i.e. non-exploding) harpoon. Binding decisions (such as those listed above) are recorded in the IWC Schedule which is not always easily understandable without knowledge of the history of how those decisions accrued. In addition to schedule amendments, the IWC also adopts resolutions, but these are considered non-binding. The IWC also regulates subsistence whaling by indigenous people which is not covered by the moratorium.

‘Scientific whaling’, which is the killing of whales for claimed scientific purposes, has long been controversial as it has been seen as a way of avoiding IWC decisions to limit catches or protect endangered species (see e.g. Clapham et al. (2003) for a review). Norway first raised the problem of ‘scientific whaling’ at the IWC in 1957 ³ and it has been a subject of controversy ever since with a dramatic expansion when the IWC moratorium came into effect. Since 2000, only Japan and Iceland have conducted ‘scientific whaling’. Japan’s ‘scientific whaling’ was subject to detailed scrutiny by the International Court of Justice (see below) whose judgement and court documents provide accessible, key analyses for scholars. It is our experience that researchers who are unfamiliar with the IWC are liable to make errors when reporting decisions made by the body (see above for the example from the University of Aberdeen).

A list of the other key intergovernmental conventions relevant to marine mammal research includes the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES) and the Convention on the Conservation of Migratory Species of Wild Animals (CMS). With the exception of porpoises, the Order Cetacea (which consists of whales, dolphins and porpoises) has a special legal status as highly migratory species under the UN Convention on the Law of the Sea (UNCLOS).) In addition, the Antarctic Treaty System consists of the Antarctic Treaty and related agreements which applies to all waters south of 60°S.

Further to intergovernmental conventions there are court decisions that need to be considered. For example, in 2014 the International Court of Justice (ICJ) ruled in a case brought by Australia (with New Zealand intervening) against Japan regarding Japan’s whaling in the Antarctic. ⁴ Japan had long argued that its whaling there was exempt from the IWC moratorium and Southern Ocean Sanctuary decisions because it was ‘scientific whaling’. The court ruled in favour of Australia primarily because it decided that Japan’s whaling was ‘not for purposes of scientific research’. Whilst the ICJ case was limited to Japan’s whaling at that time in the Antarctic, the arguments in the detailed judgement may also apply to ‘scientific whaling’ elsewhere.

Researchers would do well to consider whether by using materials from ‘scientific whaling’ they are engaged in activities that may not be legal. We argue that ethical reviews should be conducted for all the above research techniques in order formally to determine whether ethical issues have been addressed including whether the research may encourage future whaling that is contrary to IWC decisions. Journals and their editors should also consider these issues. By publishing whaling research, they may be participating in an activity that is contrary to international law. In addition, they are providing a veneer of scientific credibility that encourages whaling nations to continue existing ‘scientific whaling’ programmes or to start new ones (Ryan et al., 2023).

Some examples of relevant regional agreements include the EU Habitats Directive ⁵ and those various agreements drawn up under the Convention on Migratory Species (such as the Agreement on the Conservation of Seals in the Wadden Sea). Regional agreements can also be difficult to interpret. For example, the UK government took the view that the EU Habitats Directive only applied to the 12 nautical mile territorial sea. But after a UK Judicial Review case brought by Greenpeace, it was ruled ⁶ that the legislation applied to the Exclusive Economic Zone, up to 200 nautical miles offshore (De Santo and Jones, 2007).

National Laws and regulations are many and varied. The 1972 US Marine Mammal Protection Act places legal obligations on US citizens conducting research not only in US waters, but also on the High Seas (outside the 200 nautical mile zone) and in the Southern Ocean. In another example, Van Bressem et al. (2006) summarise the various Ministerial Decrees and Laws that have been adopted over time in Peru to protect cetaceans and other marine mammals from capture, trade and consumption. We urge researchers to seek appropriate legal advice to ensure that their work does not fall foul of key legislation. Possible sources of advice would be the government agency responsible for permits, the CITES Management authority of the relevant country and appropriate specialists in international law. One of the potential pitfalls of parachute science (discussed above), is a poor working knowledge of these national laws and regulations, which demonstrates the practical benefits of local collaboration.

The case study of Icelandic Whaling Science

We examined the poor understanding of ethics and legislation among scientists conducting whaling research with a case study in which international scientists collaborate with an Icelandic whaling company for access to data or whale samples (Ryan et al., 2021). At the time, we found 35 papers involving 56 institutions in 12 countries and there have since been several more published. Ethical assessments were rarely reported in the published papers, so it is not possible to determine if indeed they were conducted. There were scientists from four countries whose governments had formally, diplomatically objected to this whaling: this raises questions as to whether the researchers undermined the diplomatic efforts of the governments (some of which had funded the science) towards ending this whaling. Studies were often inconsistent with the ethical standards of the home countries of the scientists and there were many ethical issues to consider. For example, Iceland’s ‘scientific whaling’ shared many attributes in common with Japan’s ‘scientific whaling’ which had been ruled against by the ICJ and therefore may not have been lawful. Iceland also conducted commercial whaling under a legally dubious ‘reservation’ to the whaling moratorium – the only IWC member ever to attempt this argument to justify continuing commercial whaling despite the moratorium decision.

Our aim in writing that paper was to stimulate debate and argue the case for modern legal and ethical guidelines to be adopted in the field of marine mammal science and by its professional societies. In a magazine article written about the paper, two scientists who were directly involved in the research that we analysed were quoted (Mulvaney, 2021). One stated that, ‘Not only would I not use such tissues again, but I would be happiest if no one did’. Whilst the other researcher cited in the same article said that whaling ‘should be utilized as a source of material for scientific studies of marine mammals’ and took the opposite position to us stating that commercial whaling ‘is a perfectly acceptable activity for many IWC member countries’ apparently without considering whether such whaling was even legal.

Despite the publication of our paper, the two largest professional societies (the European Cetacean Society, and the Society for Marine Mammalogy and its journal Marine Mammal Science) have not at the time of writing revised their ethical guidelines. The journal Marine Mammal Science recently published research on Antarctic minke whales killed using penthrite grenade harpoons by the Government of Japan in the Southern Ocean Whale Sanctuary (Yasunaga et al., 2023). In a response (Ryan et al., 2023), we argued that this paper did not meet existing ethical guidelines and should not have been published. Similarly, the largest professional society for marine mammals in Latin America, Sociedad Latinoamericana de Especialistas en Mamiferos Acuáticos, has been called on to establish an ethics code by members of the society’s ethics committee (Félix and Van Waerebeek, 2021).

Public perception

It appears that some scientists can be so focused on the task at hand that they don’t see the wider implications of their work until it gets into the public domain. An example of this comes from the University of St Andrews (UK) which was contracted by the Government of Japan’s Institute of Cetacean Research which managed Japan’s ‘scientific whaling’. The project was to analyse minke whale survey data where some of the revenue to fund that research was generated through the sale of the whales killed. The Guardian (UK) article, ⁷ University taking cash from whaling criticised, quoted Greenpeace who stated that ‘it is disgraceful that St Andrews is accepting cash from the sale of whale meat’. In addition to providing funding, the Government of Japan then used the work of the University of St Andrews to justify further ‘scientific whaling’. The university announced that it ‘was carrying out a detailed review. . . to ensure no inconsistency with our commitment to conservation’ but was unable to point to any ethical review prior to taking on the contract. Learning institutions should bear some responsibility to ensure that their personnel are sufficiently trained in completing an ethical review of the work being asked of them prior to it commencing.

A second example concerns a dead tagged sei whale that stranded in Chile in March 2020, apparently harpooned (see below). This type of research although invasive, may be considered by those undertaking it to be routine and thus not thought to require clear justification (Félix and Van Waerebeek, 2021). In the case of the sei whale, members of the public and journalists were quite understandably concerned that someone had harpooned and intentionally killed this whale. It turned out that the ‘harpoon’ was in fact a commonly-used satellite tag.

There is a particular danger for early career researchers who may become unwittingly involved in research that is later deemed to be unethical. Any resulting reputational damage will be longer lasting and thus disproportionately harmful for early career researchers. The power dynamics in some academic institutions can be such that early career researchers might find it difficult to challenge unethical research practices of their superiors (the powerholders), relating to animal welfare for example. Their superiors are likely to have embarked on their careers in a world with very different ethical values where invasive, cruel, or otherwise unethical research went unnoticed by the public or was accepted and routinely published in reputable journals.

Extreme examples of such research include an examination of the diving behaviour of sperm whales from whaling vessels (Lockyer, 1977) and the examination of the physiology and times to death from drowning of restrained and then submerged mink, muskrat and beaver (Gilbert and Gofton, 1982). ⁸ Another relevant example is a paper entitled ‘The true body shape of rorqual whales’ (Williamson, 1972). Here, live sei and minke whales were harpooned in the tail region. Once ‘tethered’, a diver entered the water to observe their swimming before they died.

We argue that the use of terms such as ‘instrumented’ or ‘surgical dart’ to describe implanting tags into animals aims to sanitise or downplay the invasiveness of muscle-implanted tagging. In practice the appearance of implanted cetacean tags is similar to small non-exploding harpoons which have been banned by the IWC for welfare reasons. Concerns about the public perception of invasive marine mammal research mean that photographs of the research being undertaken are often hidden from view. A WWF review of whale satellite telemetry is a case in point (Johnson et al., 2022). Despite the review being a full-colour 69 page report, there are no photographs of tags and no discussion of the tag-attachment methodology used and the ethical implications of this work. A more extreme example is where a tag manufacturing company published artist impressions of their devices implanted in marine mammals on Twitter, before quickly deleting it after it was shared with comments critical of the welfare impacts of their devices (Ryan and Papastavrou, 2022). The company chose this course of action instead of using the opportunity to publicly defend the suitability of their product. Ironically, the original published post was regarding their involvement in a workshop on best practice in cetacean tagging.

The most effective way to ward against the problems discussed above is to routinely conduct ethical reviews of work prior to the work being carried out. The goals of a study that employs invasive research methods need to be weighed against the long-term welfare consequences to the study individuals and their populations (Hooker et al., 2007; Walker et al., 2012). We argue that this should be communicated proactively with the general public, rather than hidden from view, to avoid the kind of fallout described above. Poor (or no) ethical oversight can undermine public confidence in the scientific process. In other fields it has been shown to be highly damaging with long-term consequences. One example is the controversial and unethical Tuskegee syphilis study which ended in 1972 and resulted in reluctance for decades by African Americans to participate in clinical trials (Scharff et al., 2010).

Other case studies

Cetacean tagging is a particularly interesting case study in animal ethics. Findings from tagging studies have advanced our understanding of some whale populations, particularly those in remote regions (e.g. Johnson et al., 2022; Robbins et al., 2013 and citations therein). The Society of Marine Mammalogy guidelines on the treatment of marine mammals in field research state that ‘Instrument effects on some marine mammals have included acute and chronic changes in behaviour, increased energetic costs (particularly of swimming), burn injuries from exothermic glues, penetrative injuries from attachment components, and in extreme circumstances the death of instrumented animals. Researchers are encouraged to conduct and publish studies of the short- and long-term effects of these tags’ (Gales et al., 2009).

Because whales cannot be reliably relocated, the removal of implanted or pinned tags is not possible so the tag may remain embedded for up to 10 or even 21 years (Gendron et al., 2015; Ryan et al., 2022) and potentially for the rest of the whale’s life. Swelling and infections can occur around the tagging site (Gendron et al., 2015). The tags used for long-term tracking of large whales typically contain all of the components, apart from an antenna and saltwater switch, in a barbed cylindrical metal casing which is implanted through the blubber and into the muscle (Moore and Zerbini, 2017). Referred to as Type-C tags by Andrews et al. (2019), these tags are typically 27–29 cm deep and 1.9 cm wide and have been in widespread use since the 1970s (Watkins et al., 1981). Nevertheless, detailed peer-reviewed ethical guidelines on their usage have been absent until recently (Andrews et al., 2019).

A study of 16 southern right whales found that this type of tag is shed after 2.25 years on average, although in one case it was a minimum of 11 years (Best et al., 2015). Although tagging impact studies are recommended in best practice guidelines, they are difficult to implement because, in contrast with terrestrial animal tracking, locating an animal whose tag is no longer transmitting is unfeasibly difficult except for in very specific cases (Best et al., 2015; Robbins et al., 2013). As such, potential deaths from poor tag placement, organ damage or inward migration of the tag are exceptionally difficult to monitor (Andrews et al., 2019) with the potential for ‘substantial chronic pain at the tagging site’ (Moore and Zerbini, 2017).

In March 2020, as mentioned earlier, a dead sei whale stranded on the coast near Porvenir, Tierra Del Fuego, Chile. While the cause of death was not determined, a type of tag which is typical of those used to satellite-track baleen whales was protruding from the whale’s blubber. The tag was mistaken for a harpoon, presumably given its size and that of the associated wound. When interviewed by a local news agency Cooperativa Regiones, local conservationists cited Chilean law that protects whales from hunting and called for an investigation into the alleged illegal activity in the region (Coopertiva, 2020). The tag was a consolidated ‘Type C’ tag which is typically 27 cm long and 1.9 cm wide and deployed using an air-rocket system to implant it sub-dermally into the blubber-muscle (Andrews et al., 2019; Best et al., 2015; Watkins et al., 1996). That the discovery of this tag by members of the public invoked such a strong reaction indicates that this type of tag anchoring is out of line with modern sensibilities regarding the welfare of animals. In this case, it appears that compromising the whale’s welfare was deemed acceptable to researchers but not to onlooking members of the public. Despite the deployment of >1000 tags (Johnson et al., 2022), pathological assessment of tissue damage caused by tags has never been published (Moore and Zerbini, 2017) while the pain inflicted by them remains a key knowledge gap (Palacios et al., 2022).

Satellite-telemetry for small cetaceans is typically conducted using smaller tags in which all electronic components are housed externally. Referred to by Andrews et al. (2019) as Type-A tags, they are attached using barbs anchored to the skin and outer-blubber. Although the attachment method is more superficial than for Type-C tags, their use has contributed to the death of a killer whale (identified as L95) tagged in US waters and later found dead in British Colombia, Canada: ‘The proximate cause of death may be attributed to the relatively deep tissue perforation with the tag deployment and the ultimate cause of mortality is disseminated mucormycosis’ (Raverty, 2016). A subsequent report concluded that ‘infection at the tag site contributed to the illness, stranding, and death of this whale’ (National Oceanographic and Atmospheric Administration, 2016). Given the widely publicised death of L95 and the halting of the associated tagging programme, a subsequent study using two similar (i.e. with four 68 mm titanium barbs) tags per killer whale raises concerns and demonstrates how difficult it can be to prevent repeated exposure to invasive research methods (Mul et al., 2019).

In summary, cetacean satellite telemetry usually involves the use of a firearm to remotely implant a barbed metal anchor into the blubber-muscle interface without anaesthesia and without plans to remove it for the remainder of the animal’s life. Tagging guidelines recently developed by the International Whaling Commission (Andrews et al., 2019) have been criticised for putting technical considerations before ethical ones (Félix and Van Waerebeek, 2021). We agree with Félix and Van Waerebeek (2021) that the absolute necessity of invasive methods such as tagging should be clearly justified for each study, as part of a prior ethical assessment. Reporting that these techniques are routine or vital without critically evaluating their impacts on the welfare of individuals and the impacts on the conservation status of populations being studied should be viewed as insufficient.

As with tagging, biopsy sampling of cetaceans has permitted a more in-depth understanding of cetacean ecology and the various threats that they face including from persistent organic pollutants. Biopsy sampling involves using a crossbow to fire a device which penetrates the skin and blubber of the animal to retrieve a core of biological material. Decisions on the depth of the sampling core have implications for the welfare of the animals being sampled and the immediate pain and longer-term health implications for the individual concerned. Deeper sampling brings with it a greater risk of internal damage and infection due to longer wound-healing times. The use of deep-blubber biopsies is therefore a welfare concern. A study in Norway used 10 cm deep sampling cores for killer whales (Bories et al., 2021). However, it has been demonstrated that killer whale blubber is typically less than 10 cm deep (N = 53, Raverty et al., 2020). Thus, 10 cm blubber biopsies could potentially impact on muscle or even bone.

Restraining or handling cetaceans can have fatal consequences. Attempts to save the vaquita from extinction by establishing a captive breeding programme involved capturing some of the few remaining animals: 7–15 unique individuals remaining in 2019 (Rojas-Bracho et al., 2022). A panel of 90 world experts in cetacean handling were involved, and carefully considered the risks and benefits prior to the work being conducted. Thus, a careful and extensive ethical review was conducted prior to the intervention. Yet field efforts lead to the discovery that this species is prone to capture myopathy leading to the confirmed death of two adult females and the subsequent suspension of the project (Félix and Van Waerebeek, 2021; Rojas-Bracho et al., 2022). This demonstrates the poorly understood risks associated with captures of free-ranging cetaceans for research (Mooney et al., 2009) or conducting neurological experiments on restrained minke whales in Norway (National Marine Mammal Foundation, 2021) which we discuss below.

The use of drones has resulted in increased animal welfare standards in some areas of research, for example by replacing lethal methods such as estimating the mass of whales (Glarou et al., 2023) and often allowing research to be conducted in a less invasive way than if researchers had to approach the study animals closely from a boat (which may have more potential for disturbance and harm than a drone). Given that drones are a relatively new research tool, the ethical issues surrounding their use are still being evaluated (Kannan and Ranganathan, 2020). The potential for drone disturbance of marine mammals is a growing area of research and behavioural response studies are providing mixed results depending on the target species. This ranges from considerable disturbance, mostly hauled out pinnipeds (Palomino-Gonzalez et al., 2021), to short term disturbance for example, belugas (Aubin et al., 2023) to reports of a lack of observable response (Castro et al., 2021; Christiansen et al., 2016; Domínguez-Sánchez et al., 2018). It is concerning that most marine mammal drone papers do not include ethical statements. We suggest that ethical statements should be required for drone studies: if the effects are expected to be minimal, then the ethical statements will be straightforward.

Ethical issues are not just confined to the manner in which research is conducted but also to the way that other scientists’ research is reported. Wade et al. (2010) document that funding sources bias the conclusions of review papers. They examined reviews of research on the effects of anthropogenic noise on marine mammals, including military sonar which has the potential to kill marine mammals. If the reviews were funded by the military, papers which concluded that there was no effect of noise were 2.3 times more likely to be cited than if not (Wade et al., 2010). The authors stated that the US military claims to provide 50% of all funding for marine mammal research worldwide, so military influence in biasing conclusions is considerable. This will be a difficult issue to address but we flag it nevertheless.

It could be argued that the need for prior ethical approval by all institutions involved in a particular study may be unfeasible or unnecessary. However, we cite cases where the use of whaling data or samples justify this course of action. In the examples of Icelandic (and Japanese) whaling science, defenders of such research may argue that the whales were ‘already dead’ and even argue that given that they are dead that there is an imperative to use the materials for maximum benefit. The weakness of the ‘already dead’ argument is simply that the publishing of the research is often used to justify continuing the unethical activity and we cite examples above.

In internationally collaborative research, ethical clearance in one country might not stand up to scrutiny in another. The situation could arise where ethical approval is sought only in the country with the weakest ethical oversight, for example, in relation to animal welfare. In the following section, we address this issue of offshoring in more detail, but clearly requiring ethical approval in all involved institutions may be necessary to prevent this ‘weakest link’ approach and the ensuing harm that this can cause to the welfare of the animals being studied and indeed the reputations of the institutions and researchers involved.

In the field of marine mammal science, there are many cases where published studies cite no ethical assessment whatsoever (Ryan et al., 2021). To exemplify this point, we considered the peer-reviewed papers published in the past 12 months ⁹ that involve data or samples derived from the intentional killing of cetaceans (see Supplemental Information). Of those that are clearly required to include ethical statements according to the journal author guidelines, 80% (N = 4) omitted such statements. This is a failure of the journals to implement their own existing policies, as well as a lack of ethical oversight by the authors. The field of marine mammal research could look to the biomedical sciences for examples of how to address poor reporting of ethical assessments and indeed research conducted across many countries and institutions involving the use of data which has been obtained without proper ethical approval. The Helsinki Declaration of the World Medical Association places responsibility on journals to check and requires that, ‘Reports of research not in accordance with the principles of this Declaration should not be accepted for publication’. ¹⁰

Offshoring

In our earlier review of science that relies on collaboration with Icelandic whalers, there was evidence of offshoring (Ryan et al., 2021). In other words, we listed scientists conducting research elsewhere that would not be acceptable or perhaps even legal in their home country or that which their institute is based. This may not be confined to Iceland. We also note a recent publication where a Portuguese research institution is listed as the corresponding author’s secondary affiliation for a study that reports results from commercial whaling in Norwegian waters. (Freitas et al., 2023). Biomedical research has confronted a similar issue, that of conducting clinical trials in the Global South under regimes which are less well-regulated. There is an extensive literature on the ethical issues that arise and how they should be addressed: see for example (Bairu, 2011).

In the Icelandic whaling example, where papers were co-authored by US researchers, the laboratory analyses of whale products were conducted by co-authors outside the USA, notably in Canada. This may be due to the difficulty and perhaps impossibility of US researchers obtaining permits under the US Marine Mammal Protection Act (MMPA).

Another example of offshoring is the trapping of wild minke whales for hearing experiments in Norway (Kvadsheim et al., 2021). The research involved plans to trap up to 12 minke whales in order to assess their hearing by measuring auditory evoked potentials in restrained animals. A 2 km net was set across a strait in order to herd whales into the testing zone where they would be restrained, despite a lack of information as to how minke whales would react to this procedure. In the first season (2021), the research was suspended after one whale became trapped in the nets for 8 hours before subsequently escaping. ¹¹ Some 54 whale scientists from around the world wrote to the Government of Norway to ask that this research be halted citing welfare and safety reasons. ¹²

Given the invasive and unusual nature of this research, an obvious question is whether the US researchers decided to conduct the work in Norway rather than the USA in order to avoid the requirement to obtain a permit (which they may not have obtained) under the US Marine Mammal Protection Act. This question is partially answered by a document revealed through a Freedom of Information request to the US Government (Kate O’Connell, 2022, personal communication). The document states that the US Government does not require the researcher to obtain a MMPA permit, providing that the research is conducted in the territorial seas of Norway (within 12 nautical miles). The communication continues by stating ‘If in International waters, an MMPA Permit would be needed. It would be a major amendment to add a new geographic location and to evaluate the capture methods’.

Conclusion and future directions

It should not be assumed that the wide-ranging examples cited above all constitute unethical research. However, very few of them show evidence of an ethical statement in the publication that explains the ethical review that was conducted and the rationale for the research in question. ¹³ In addition, the decision by some researchers not to provide photographs of invasive procedures and /or downplay descriptions of the techniques draws into question whether the research may be out of synch with societal values. We argue that the more invasive the research, the more extensive an ethical review should be. In conducting such a risk-benefit analyses, if the risks to the individual animals (or indeed their populations) are substantial, then any benefit should also be substantial. Furthermore, if such risks are substantial, it is important that the research should be rigorously planned and conducted with wide peer review at every stage by appropriate experts.

Without clear ethical guidelines, reviewers and journal editors are put in an impossible position when considering whether to reject papers on ethical grounds. One of us (CR) has been put under pressure by a journal editor to accept a paper despite insufficient evidence that the research was ethical. Ethical guidelines need to be sufficiently clear that different reviewers come to the same conclusion and that the decisions are defensible. This is a complex area for discussion and we stress that we do not have all the answers and are not the arbiters of whether particular research is ethical or not.

In conclusion we propose a number of components below that should be considered to ensure that marine mammal research and the papers that result from that research meet ethical standards.

• Universities, funders, journals, and permit issuers must require ethical assessments to be included in publications. This should require appraisal and justification of the absolute necessity of invasive and apparently less invasive procedures.

• The professional marine mammal societies must urgently work together to produce modern ethical guidance.

• Such guidance must require transparency in the provenance of samples and include advice on law, welfare issues and involvement of local scientists.

• Risk benefit analyses need to be clearly stated. The greater the risk or cost to the individual animals the more substantial and certain any potential benefit must be.

• At a minimum, research should be legal in the country where the researchers (and the funders and universities concerned) are based as well as in the country where the research is undertaken. This in effect would end the practice of offshoring.

• Ethical assessment should involve the animal ethics office/secretariat in one’s institution to ensure compliance.

Reflexivity Statement

Both of us have focused our careers on developing and using non-invasive or minimally invasive techniques to study whales and have worked for various NGOs including the International Fund for Animal Welfare. Our ethical lens is that some harms may be acceptable if the likely benefits outweigh them but we understand that others take the alternative view that no harms should occur.

I (VP) started my career studying marine mammals in the early 1980s when the prevailing opinion was that most whale research required the use of dead animals and was conducted through the whaling industry. As an example of the prevailing opinion, my external examiner for my MSc research on sperm whales (studied from a small ocean-going sailing boat) was a scientist who was the former whaling inspector on South Georgia. Following some time spent studying whales, I focused my career on efforts to stop all forms of commercial whaling and to address various other conservation and welfare problems that marine mammals face.

As an early career researcher in search of whale tissue samples for ecological and biogeochemical research, I (CR) found myself navigating complex ethical issues that were insufficiently dealt with in the literature. My PhD research was carried out without any ethical training or ethical assessment beyond that required for government and CITES permits. I now conduct non-invasive research for NGOs, universities and government agencies. My judgements regarding animal welfare and the pain experienced by whales have been shaped by: dealing with live-stranded whales, witnessing whaling activities in Iceland and involvement in research towards mitigating whale entanglements in fishing gear in Scotland.

Supplemental Material

sj-docx-1-rea-10.1177_17470161231182066 – Supplemental material for Ethical standards for research on marine mammals

Supplemental material, sj-docx-1-rea-10.1177_17470161231182066 for Ethical standards for research on marine mammals by Vassili Papastavrou and Conor Ryan in Research Ethics