A method for considering the acceptability of novel biotechnologies for the control of brushtail possums

Abstract

Public acceptance and regulatory approval of biotechnologies is increasingly dependent on consideration of cultural, ethical and spiritual effects, and the opportunity for community involvement. The objective of this study was to articulate a means for researchers to identify relevant issues during the development of the technologies. It encompassed the substantive issues, such as safety, the provision of credible and adequate public information, and the opportunity for citizens, as well as stakeholders, to give society's informed consent. In this initial analysis of novel toxins and infertility or sterility-inducing agents being developed to manage pest populations of brushtail possums, several issues were identified. They included the risk associated with fertility controls entering the food chain, the severity of animal welfare compromise with toxins, and the adequacy of terminology used to describe pest control agents. This approach provides a means for researchers to acknowledge the issues contributing to public acceptance of biotechnologies during their development and with the involvement of those with interests in biotechnology.

Keywords:

• pest
• brushtail possum
• biotechnology
• ethics
• fertility
• toxin
• public involvement, information and concerns

Introduction

The threat to flora and fauna, and to the economic wealth of farming industries, from the introduced brushtail possum (Trichosurus vulpecula) has long been recognized in New Zealand (Montague 2000; Ritchie 2000; Clout 2006). A lack of competitors and predators, and an abundance of vegetation, has contributed to it becoming a pest. Possums damage forests and crops, reduce biodiversity and carry bovine tuberculosis. Consequently, possum numbers are routinely managed by trapping, shooting and poisoning. In addition, there are a number of innovative technologies being developed principally to overcome concerns with the acceptability of current technologies, specifically their humaneness, safety and specificity, and cost-effectiveness.

Technologies can make many things possible but their acceptability or place in the world is also determined by their social, economic, ethical, political, cultural, spiritual and global effects (DeWalt 1991; Carolan 2008; Perkins & Jamison 2008). Familiarity with once questionable technologies, e.g. margarine (Ball & Lilly 1982) or the dining fork (Frank 2006), and lessons from history, e.g. asbestos or thalidomide (Green 2001), highlight the difficulties in reconciling societal values with the development of technologies. Not surprisingly, individuals and communities can hold disparate views and attitudes towards pests and methods of managing them (e.g. Parliamentary Commissioner for the Environment 2000; Fraser 2006; Fitzgerald 2009). These views can result in disagreements (Kirkpatrick 1999; Morris & Weaver 2003; Potts 2009). Furthermore, while the scientific development of a technology generally reflects the mores of the dominant culture (Meghani 2008), there are differences within cultures (e.g. Shibata 1996; Slovic 1997; Ogilvie et al. 2006; Gamble & Kassardjian 2008) which need to be taken into account.

Ethics, taken to be the systematic reflection of moral issues raised in the public sphere (Lassen et al. 2006), provides an array of critiques and guidelines on pest control. For example, they include the views that there are no absolute rules but that the best results should be produced in particular circumstances (Singer 1997); consideration should incorporate ecological, animal and human interests (Eggleston et al. 2003); or that there is a need to learn and reduce uncertainty (Warburton & Norton 2009). There is a similar array of expectations associated with biotechnology necessitating additional consideration. For example, New Zealand's Environmental Risk Management Authority (ERMA 2005) ethics framework has general (respect for persons and for the environment) and applied (concern for animal welfare, autonomy, co-operation, cultural identity/pluralism, human rights and dignity, justice and equality, sustainability and well-being/non-harm) principles to be considered.

How should those responsible for the development of innovative pest control technologies respond to these seemingly complex expectations? The objective of this study was to articulate a method or framework whereby scientists and technologists responsible for developing technologies could identify, evaluate and if possible mitigate the issues and concerns of a particular technology during its development. To give focus to this complexity, the three types of concerns described by Korthals (2008) are addressed – the substantive issues such as safety and humaneness; the provision of credible information; and the opportunity for citizens to be involved, giving society's informed consent. To provide a suitable context for the study, two technologies currently being developed to manage possums, novel toxins and agents to interfere with reproduction are outlined.

Secretory toxins and reproductive controls

The current status of two approaches to controlling possum populations is summarized in Table 1. The first aims to identify toxins which are highly specific to marsupials, ideally brushtail possums. The intestinal physiology of the possum, especially the mechanisms responsible for fluid section across the gut wall, differs markedly from eutherian mammals (Butt et al. 2002; McDowell & McLeod 2007). Consequently, disrupting the proteins responsible for fluid transport could lead to irreversible and uncontrolled fluid secretion resulting in diarrhoea, dehydration, hypovolemic shock and death.

Table 1  A summary of the secretory toxins and reproductive controls being developed to control brushtail possums

Target	Primary agent	Facilitating agent	Administered to possums via	Experimental outcome	Desired outcome
Intestinal fluid secretion	Toxin to disrupt fluid secretion in the intestine	Unknown	Feed bait	Altered intestinal secretion/function	Death
Outer covering (zona pellucida) of the egg	Vaccine against zona pellucida to prevent the egg being fertilized	Adjuvant	Injection*	Reduction in fecundity, lower egg fertilization rates and fewer embryos in superovulated and artificially inseminated possums (Duckworth et al. 2007)	Infertility
		Bacterial ghosts	Nostrils and eyes	No effect on fertility but fewer fertilized eggs in superovulated and artificially inseminated possums (Walcher et al. 2008)	Infertility
Pituitary hormone secretion	Vaccine to disrupt reproductive hormone secretion	Adjuvant	Injection*	Infertility in 19/20 possums (Eckery et al. 2007)	Infertility
		Bacterial ghosts	Feed bait	Altered hormone secretion in possums	Infertility or sterility
Italicized text indicates proposed features, or experimental outcomes, which have yet to be developed or experimentally demonstrated. Note that a practicable control agent will not involve a treatment delivered by injection*.

The second approach aims to deliver an agent capable of rendering the animal infertile or sterile, principally by vaccinating the animal against a component of its normal reproductive system and interfering with the fertilization of the egg, or hormone secretion from the pituitary gland. To ensure the animal has an effective immune response, and in common with many vaccination protocols, the control or fertility-disrupting agent is administered with an additional agent designed to help produce a response. Several response-facilitating and/or enhancing agents are therefore also being researched. Bacterial ghosts are the non-living (killed) empty bacterial cells into which the infertility agent can be incorporated, either by physical loading after death or, more commonly, by genetic modification of the bacteria prior to its death (Lubitz et al. 1999; Mayr et al. 2005).

Both toxin and fertility approaches require their administration to the animal, probably orally, and most probably via a feed bait. This requires that the control agent is formulated and delivered to ensure protection from the denaturing environment of the stomach, remains active, and targets the appropriate part of the intestine or reproductive tract.

Substantive concerns with possum controls

The ideal pest control

Biotechnologies not only have to be technically feasible, but they also have to be publicly acceptable. In other words the views and concerns expressed by citizens and stakeholders have to be taken into account. Taking some of these concerns into account means an ideal pest control would be affordable, effective, safe and specific, environmentally benign and humane (e.g. see Tuyttens & Macdonald 1998; Littin et al. 2004). Examples of other ideal attributes of a pest control are that it must not spread outside New Zealand (Gilna et al. 2005); that its use must incorporate consideration of the responses of ecosystems (Moller 1989); and that there should be some form of preparation for the unknown, that they must be in keeping with our obligations to Maori, and involve the public in its development and application (Parliamentary Commissioner for the Environment 2000).

To do justice to the above and other concerns, it is proposed that a hypothetically acceptable pest control is one which meets the concerns of all stakeholders and citizens. Given the range of concerns and the disparate views of pests, pest controls and biotechnology within a community, a pest control that meets all ideals is realistically likely to be difficult if not impossible. Therefore it is proposed that any differences between an attribute of the ideal control and the proposed control, e.g. those currently being developed, have to be justified, or the control modified.

Typical of the questions asked of a technology in seeking to justify it are: do the benefits outweigh the costs or harms, are there any actions which should not be undertaken regardless of the benefits which might accrue, and how would persons of good character evaluate risks? (These questions reflect three main ethical theories relating to consequences, rights and virtues. There are other ethical theories giving additional insights into moral issues – see Hinman 1998.) To help society answer such questions, researchers gather and collate relevant evidence. Judgements about technology, then, are made on the basis of appropriate knowledge and moral standards. In this study, the likely justification for the ideals of safety and specificity, humaneness, and consideration of unknown consequences and whether it is inherently right to treat animals as pests in the proposed ways, are considered for the two technologies being developed.

Safety and specificity

The need to overcome the suffering and death of non-target species associated with conventional methods of possum control (e.g. sodium monofluroacetate or 1080) has been a major impetus for the development of novel controls. Specificity (and safety) is a major issue in the acceptance of any control – potential harm to valued non-target animals, including humans (from occupational exposure to bioterroism), perhaps the most significant risk and fear. As possums are valued by some people as economic resources, pets, research animals, or native species in Australia and other countries (both brushtail and other species), and the ‘possum risk is high only in specific areas’ (Parliamentary Commissioner for the Environment 1994), the ideal control should be specific to pest-possums (those in areas where their impacts are considered significant).

The proposed control agents (and any immune enhancers and bait attractants) are not demonstrably specific to pest populations of brushtail possums (although, unlike in possums, there were no effects of possum-derived zona pellucida vaccines on the fertility of laboratory mice or domestic chickens; Duckworth et al. 2008). Indeed, some of the same approaches are being researched in a wide range of species, most notably vaccination against components of the zona pellucida in wildlife and humans (Mettens & Monteyne 2002; Kirkpatrick & Frank 2005) and reproductive hormones in wildlife, pets, and livestock (Jago et al. 1997; Purswell & Kolster 2006). The fate of the control, or the changes it induces, in the target and non-target organisms is also important. A significant public issue is likely to be the possibility of unintentional transfer through the food chain. This is especially since some feral animals (deer and pigs) sharing territory with possums are a valued food source. An important factor in the acceptance of fertility controls in the USA was that they ‘cannot pass through the digestive tract and remain biologically active’ (Kirkpatrick 2005). Since the current research includes attempting to produce oral formulations, it will be necessary to demonstrate their fate.

Might the benefits of the proposed pest controls outweigh the harms? The history of pesticide use in agriculture shows that pest populations adapt and recover, that pesticides ‘move’ through ecosystems, and that they may be toxic in unanticipated ways (Perkins & Jamison 2008). It is suggested that the safety and specificity of the control technologies may therefore require more detailed consideration before differences between proposed and ideal controls can be justified.

Humaneness

While concern for humaneness may not contraindicate the use of novel pest controls, it does indicate that, like other methods of controlling possums (Warburton & Choquenot 1999; O'Connor et al. 2003), any costs to the animals need to be considered. Potential welfare implications range from direct effects resulting in discomfort and illness to indirect effects such as repeated mating (Tuyttens & Macdonald 1998) and allowing unaffected animals to lead natural lives (Meerburg et al. 2008).

Humaneness depends on both the duration and severity of suffering. Although the duration of possible suffering with a secretory toxin is thought to be minimal, perhaps only 1–2 hours, severity is unknown. Until such a toxin is identified and tested, it is suggested that the clinical effects, based on studies in other species, could be characterized according to the suffering they are assumed to indicate (O'Connor et al. 2003). Diarrhoea-induced dehydration, as is expected with a novel toxin, may be associated with abdominal pain, the urge to defecate, perianal soreness or discomfort, incontinence, weakness and lethargy, and dehydration and thirst (Gregory 2004).

Techniques for modifying an animal's fertility can impact, both positively and negatively, on the target animal's physiology and behaviour, as well as have indirect impacts on the non-affected population at both an individual and evolutionary level (Gray & Cameron 2010). For example, treatments rendering female possums reproductively incompetent have been reported to extend the breeding season and result in males of poorer body condition in the winter post-mating period (Ji et al. 2000); result in higher annual survival rates in females (Ramsey 2005); or have no effect on female seasonal breeding range size (Ramsey 2007) or social hierarchies (Jolly et al. 1996). Finally, there are possible changes in the genetic makeup of possum populations if there are heritable differences in immune and contraceptive responses (Magiafoglou et al. 2003; Cooper & Larsen 2006).

Do the benefits of fertility controls outweigh the harms, especially when compared with those associated with lethal control methods (e.g. poisoning or trapping)? Some, including animal welfare proponents, have concluded that fertility controls are relatively benign (e.g. Oogjes 1997; Grandy & Rutberg, 2002; Porton 2005). Although the sorts of impacts noted above may seem trivial compared with death, two potential adverse impacts, the effects of births late in the season affecting the survival of mother or young, and the effects of female-targeted fertility controls on males or prepubertal females, remain unknown. Furthermore, as Gray and Cameron (2010) noted, while all studies investigating secondary impacts consistently found them, none was designed to specifically address the welfare of individuals, and few were not undertaken in captivity. These observations contributed to the authors suggesting a need for future research involving more detailed behavioural and ecological measures, larger sample sizes and longer study durations.

Unknown consequences

Safety and specificity, and humaneness, are examples of consequences of technologies that can be reasonably anticipated. However, since ‘the latent properties of natural systems defy the imaginations of even the scientific elite’ (Tenner 1996), the development of a control agent would, ideally, include some sort of consideration of the possibility of unknown consequences. To achieve this, it is suggested all creative human qualities – common sense, imagination, intuition, and memory, as well as reason (science) and ethics (Saul 2001) – are employed. Since science primarily deals with ‘known uncertainites’ (Zimdahl 2006) it is necessary to look elsewhere. Stories not only inform us but guide our behaviour (Armstrong 2005) because they provide us with (1) paradigms, examples or patterns which are generalizable and can illuminate and make sense of our own experience, and (2) can do so only because they are stories about particular individuals, and because that is what makes them convincing and brings them to life (Norman 2004). Moreover, fiction may have evolved to improve our capacity to interpret and understand social events through enhancing creativity and imagining different possibilities (Boyd 2009). Few would doubt the power of Mary Shelley's Frankenstein in helping science and society shape modern biotechnology. Human infertility is the background for several literary and cinematic works, among them Children of Men (adapted from James 1992), Galapágos (Vonnegut 1985) and The Handmaid's Tale (Atwood 1985). These works remind us of the potential of control agents to adversely affect humans. At one level, it would seem sensible to consider monitoring the effects of occupational exposure to control agents, or consider their potential for deliberate malevolent use. At another level, the development of fertility-based controls could include considerations of a ‘deadman's switch’ (Hill 2006) ensuring the technology only operates in certain circumstances, such as the presence of a chemical, or is short-lived, for example is denatured by sunlight. Greater reflection on these and other possibilities might represent one of society's virtues.

Inherent or intrinsic rights and wrongs

Although there are sophisticated philosophical challenges to the predominant human attitudes to animals (e.g. Regan 1983; Singer 1990), it is commonly accepted that it is permissible to use animals, including killing them, usually provided their populations are not endangered and that their death is humane. Controlling fertility is similarly accepted as evident in the long history of eunuchs, castrated livestock and spayed pets, and human contraception. However, we need to be aware of developing stances questioning whether manipulating organisms is disrespectful to their integrity or intrinsic value.

An ideal control agent may then be one which is in keeping with concerns about the integrity and intrinsic value of possums. It is difficult to interpret these concerns as providing guidelines and limits to human actions relating to possum controls but there may be value in understanding them and drawing on the insights they provide, as a form of moral intuition (Kirkham 2006). Perhaps researchers and stakeholders should use them as a reminder of human pretensions of infallibility (Fisher & Mellor 2008), or as a means of examining the impact of technologies on our world views and myths (Midgley 2003). Novel controls may fit with our current view of environmental management but what about an alternative view? Will possums come to be regarded as a natural part of our environment (see Fraser 2001)? The future of pest control, like any relationship between people and animals, will almost certainly involve greater reflection of animal rights as a social relationship between humans and animals, the emotional and spiritual dimensions of animal welfare, and increased engagement with a plurality of values, especially sympathy, respect, wonder and awe (Hodgson 2002; Anderson 2004).

The provision of information about possum controls

While there are substantive concerns about biotechnology and pest control, there are also concerns about the accessibility, trustworthiness and responsiveness of information to public needs. The Caught in the Headlights study (Parliamentary Commissioner for the Environment 2000) revealed four key areas of information critical to public acceptance of possum control biotechnologies. They were: (1) the extent of the possum problem; (2) the technical aspects of the biotechnology itself; (3) ethics and values and the cultural, philosophical and religious dimensions of human intervention of other species; and (4) the regulatory approval processes. In this section, the third of those areas, the cultural and ethical dimension, is progressed through consideration of the language or terminology and the underlying assumptions used by those developing the control technologies. The provision of credible information is arguably one of the more important but underestimated requirements of the popular media (Priest & Talbert 1994).

Terminology

Pest control agents are sometimes termed ‘biocontrols’, reflecting an expanded understanding of the term. Common or traditional usage of the term biocontrol, it is suggested, is more aligned with, and perhaps should be limited to, the introduction of a natural predator, the classical biological control agent (Goldburg 1996) than with more biotechnological understandings (Jolly 1994; Kerr 2007). Labelling novel toxins as biocontrols (they are fundamentally no different to existing toxins) may prevent society from drawing on a wealth of relevant experience with pesticides in dealing with them. Similarly, the term ‘delivery system’ used to describe agents facilitating or enhancing an immune response (e.g. Walcher et al. 2008); covering a variety of specific agents including bacterial ghosts, the term is likely to vary from common understanding (e.g. feed baits and helicopters) and may well contribute to confusion and even rejection of a technology in the public sphere.

Beliefs about controls

Underlying any information presented to society are a number of beliefs, assumptions, paradigms or myths, which help to reinforce what we think is real and what we want to be real (Fisher 2002). For example, ‘possums are New Zealand's public enemy number one’ and ‘biotechnology may be the only answer to the possum problem’. They are further reinforced by regulatory authority recommendations for research into alternatives to the current main toxin used (ERMA 2007). Such beliefs may or may not be correct, but they help shape perceptions, and thus should at least be articulated.

In the course of this study, the following were encountered. First, it is accepted that possums have negative impacts on native biodiversity or the productive sector that are sufficient for society to mitigate those impacts. This does not necessarily advocate the use of any novel control, as with any risk their acceptance also depends on the availability of other technologies or activities with less risk. Second, while New Zealand owns both the problem and the solution, all ‘voices’ should be encouraged and heard, including those in Australia and other parts of the world, to ensure equitable and trusted processes and technologies are developed. Third, there are two domains to developing controls – knowledge and ethics – and both are important; knowledge, both science and common knowledge, in providing empirical information and ethics in assisting with judgements. Fourth, scientists and technologists acting in the public interest should provide information for public decision-making – in the spirit of Lord May's comment ‘Lay it all on the table, uncertainty and all, and let the individual choose’ (Anonymous 2002). Fifth, the importance of scepticism, reflection and understanding is acknowledged and encouraged (see Sim 2006). Finally, science should be seen as a relationship with society, whereby rather than having to accept the burden of proof, what risks society is prepared to accept are negotiated with science assisting with ethical dilemmas rather than being the source of them (Meyer et al. 2005; Somerville 2006). Beliefs or assumptions like these can be, and indeed should be, continually questioned.

Opportunity for public involvement

In democratic societies, oversight belongs to the polity at large not just experts, be they scientific or ethical (Kass 2009). Thus acceptability of innovative technologies depends on individuals as citizens having an opportunity to be involved or ‘own’ them through input during their development rather than upon their completion. This enables both genuine concerns to be addressed, and the opportunity for familiarity borne of having time to consider them. Discontent with expert accounts of risk has been well acknowledged – they do not take into account lay and local people's knowledge, which can be more sophisticated and sensitive to reality (Yearly 2000; Marris et al. 2001). The sorts of things which the ‘public’ value as important aspects contributing to the acceptability of biotechnologies include acknowledging (1) inherent and unavoidable uncertainties (the denial of uncertainty is disconcerting and untrustworthy), (2) using knowledge from all relevant sources, not just scientific experts, and (3) overall, demonstrating that views of the public are understood, valued, respected, and taken into account – even if they cannot be reconciled.

The management of possums and of biotechnology in New Zealand has previously been the subject of extensive public discussion. The Parliamentary Commissioner for the Environment (2000) study Caught in the Headlights, the Royal Commission on Genetic Modification (2001), Hands Across the Water (Cronin & Jackson 2004) and the recent ERMA Reassessment of 1080 (ERMA 2007) are among many comprehensive initiatives which can be utilized. Further engagement with citizens, as guardians of public good, on cultural, ethical and spiritual issues of technologies such as novel toxins and agents interfering with reproduction will need to introduce the technologies, present the challenges (to public acceptance) they represent and consider how and who might address them.

Discussion

Arguably researchers developing a technology should not be expected to shoulder responsibility for anticipating all the effects of that technology. Others, both citizens and governmental regulatory bodies, also have a leadership role. Scientists and technologists can, however, understand different perspectives and engage in the issues of concern, thereby contributing to, or facilitating, public understanding. Alternatively, the technology may be modified with the benefit of public perspectives. This task is not insignificant: various expectations of an ideal technology, ethics and values and effects of technologies provide a bewildering challenge for both society and researchers.

This study has described a method, drawn from ethics, the systematic reflection of moral issues raised in the public sphere, for researchers to engage in the issues during the development of a technology. In the context of developing novel toxins and agents interfering with reproduction to manage pest populations of brushtail possums, several needs have been identified. They include the substantive issues of the risk of fertility agents entering the food chain; an estimate of the severity (as opposed to the duration) of animal welfare compromise caused by toxins acting in the gut; and the possible effects of occupational exposure to fertility agents. Similarly, in contributing to public understanding, terminology must be in keeping with common usage. Further initiatives in the provision of information will need to reflect what public individuals need, as well as want, to know and the Parliamentary Commissioner for the Environment's study, Caught in the Headlights, provides an invaluable foundation for identifying those needs. Finally, it is important that citizens are able to be involved, giving, in effect, society's informed consent. It may be worth exploring changing the emphasis from science being essentially an advocate for these technologies through its role in developing them, to a role in brokering society's expectations of the benefits and risks associated with managing possums, and the future of the social relationship between New Zealanders, their environment and possums.

While those responsible for developments such as pest controls make ethical decisions, pest control ethics has not often been explicitly discussed within the context of research programmes (Delfosse 2005). The approach outlined here is founded on the importance of dealing with controversial or innovative technologies as part of their development utilizing the principles of common morality to highlight the aspects of public concern. In order to do this, the concept of an ideal (i.e. acceptable) or ‘public good’ control was envisaged, not one which might be necessarily preferred by stakeholders. At first sight, the idea of a control being specific for pest possums might seem unnecessary. What it means, however, is that individuals and institutions with concerns, e.g. those with valued possums, be they pets, natives or parts of valued ecosystems etc., have been acknowledged, rather than seemingly dismissed, which any reliance on the benefits outweighing the harms can do to minority interests. At a practical level, this might give owners the opportunity to protect their animals, and researchers a responsibility to explore, for example, antidotes. At a societal and political level it might help engender greater respect in the development and regulation of biotechnology. Similarly, drawing on resources such as fictional narratives to explore the unknown aspects of technologies may improve the quality of risk assessment and help give assurance that it is not limited to the narrow field of science.

Support for innovative means of managing possums may well depend on society's ability to acknowledge and accommodate, even solve, the wider and often far-reaching social, ethical and economic problems and opportunities those technologies present. The sooner that society faces up to them, the sooner the benefits can be realized and the problems minimized or alleviated (Priest 2001). It is especially important with the possibility of self-dispersing or transmissible biocontrols quickly becoming a reality (e.g. Angulo & Bárcena 2007). The solution in a civilized society is not necessarily to ban or restrict contentious technologies, but to allow progress to continue with the beneficial insights of all those with legitimate interests.

Acknowledgements

Bernie McLeod (AgResearch), Will Allen, Phil Cowan, Janine Duckworth, Chrys Horn (Landcare Research), Grant Butt (Otago University), Doug Eckery (Victoria University) and others researching the possum control technologies in New Zealand are thanked for their generous insights and assistance. Henrik Moller (Otago University) is also thanked for his especially thoughtful comments on the manuscript. The study is part of research funded by the New Zealand Foundation for Research, Science and Technology.