Biological Conservation 144 (2011) 937–941

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Biological Conservation

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Short communication Conservation education needs more parasites ⇑ Elizabeth Nichols a,b, , Andrés Gómez a a Center for and Conservation, American Museum of Natural History, New York, NY 10024, USA b Department of , and Environmental , Columbia University, New York, NY 10027, USA article info abstract

Article history: Formal training in education is an important component of the suite of solutions to Received 13 August 2010 current environmental problems. As conservation biology textbooks underpin many conservation educa- Received in revised form 27 October 2010 tion programs at both undergraduate and graduate levels, the portrayal of conservation issues and cov- Accepted 31 October 2010 erage of specific biotic groups plays a potentially important role in guiding the training of the next Available online 10 December 2010 generation of conservation professionals. Parasites represent the majority of species diversity on earth, play critical roles in ecology and evolution, and are often at higher risk of decline and extinction than Keywords: their free-living counterparts. Yet parasites continue to receive scant attention from conservation scien- tists and educators. We searched the index of 77 English language conservation biology textbooks for par- Biodiversity asite or related content, published between 1970 and 2009. When present, we categorized a Disease textbook’s parasite content as positive, neutral or negative with respect to the author’s portrayal of par- Teaching content asite biodiversity. The vast majority (72%) of conservation textbooks either portray parasites uniquely as Conservation threats to conservation goals established for free-living species or do not mention parasites at all. While no single textbook can be expected to provide extensive treatment of conservation-related topics across all biological groups, we outline three reasons why parasites should feature more prominently in formal conservation education, and suggest several ways in which greater incorporation of these parasite topics could strengthen the teaching and practice of conservation biology. Ó 2010 Published by Elsevier Ltd.

1. Introduction To the many voices suggesting improvements to conservation education, from basic pedagogical approaches (Brewer, 2006), pro- Conservation must work towards communicating gram availability and distribution (Mendez et al., 2007), and inte- arguments in favor of maintaining biodiversity to local, national, gration with other disciplines (Niesenbaum and Lewis, 2003), we and global audiences. This task is both vast and complex, and re- add a suggestion on content. Conservation textbooks generally quires a cadre of and practitioners well versed in a broad cover the main principles and goals of conservation biology, and spectrum of topics and skills. The last few decades have borne wit- no single textbook can be expected to thoroughly cover the intrica- ness to a shift in conservation biology from a field composed lar- cies of conservation strategies in every ecological or human con- gely of practitioners, to one that incorporates formal education at text, nor provide extensive treatment of conservation-related all levels. Conservation education is a necessary component of topics in all biological groups. However one element seems persis- the solution to current environmental problems, through its role tently absent from the textbooks that underpin basic conservation in increasing awareness and shifting attitudes in non-scientists, education: the importance of parasite biodiversity as fundamental and fostering the acquisition of knowledge and skills in conserva- components of , and in some cases, as conservation tar- tion scientists and practitioners (Brewer, 2006, Hudson, 2009). Ba- gets in their own right. sic textbooks are an especially important tool because they tend to Taken as a non-monophyletic whole, parasites represent the shape to a significant degree the scope and content of introductory most common life strategy on the planet, yet they receive scant classes, and thus the foundations of new students’ understanding positive attention from conservation scientists and educators. All of the field and their place in it. parasites use resources to feed and/or to reproduce, and conse- quently have a detrimental effect on host fitness, albeit to widely varying degrees. In humans, parasites can cause severe morbidity, ⇑ a wide range of physiological and developmental impairments, Corresponding author at: Center for Biodiversity and Conservation, American and continue to cause death in millions of people around the globe. Museum of Natural History, New York, NY 10024, USA. Tel.: +1 212 496 3684; fax: +1 212 796 5292. As a consequence, and for good reason, the stance of the medical E-mail address: [email protected] (E. Nichols). sciences towards parasites is best characterized by direct

0006-3207/$ - see front matter Ó 2010 Published by Elsevier Ltd. doi:10.1016/j.biocon.2010.10.025 938 E. Nichols, A. Gómez / Biological Conservation 144 (2011) 937–941 antagonism. Likewise, within conservation biology, practitioners parasites are major selective agents that play significant roles as and academics are more prone to evaluate the role of parasites as drivers of biodiversity in evolutionary time. The cumulative effects threats to host than discuss the need for conserving of host–parasite interactions through time include the evolution of host–parasite relationships (Gompper and Williams, 1998). Yet complex structures, mechanisms and behaviors, as well as macro- the effects of parasites on the overall functioning of ecosystems evolutionary change (Summers et al., 2003). are vast, complex, and often positive. Finally, beyond generally supporting ecosystem function, many Here we outline three central reasons why parasites should fea- parasites also provide humans with direct ecosystem services. ture more prominently in formal conservation education, discuss These range from being sources of novel therapeutic and diagnostic the extent to which parasite conservation issues are overlooked (Fallon and Alcami, 2006; McKay, 2006), acting as deliv- in many existing conservation textbooks, and suggest ways in ery agents for medically relevant compounds (Douglas and Young, which greater incorporation of these topics could strengthen the 2006), and providing sensitive sentinel species for environmental teaching and practice of conservation biology. pollutants (Sures, 2004). Finally, empirical evidence supports the overarching concept of the ‘hygiene hypothesis’, which suggests that contact with certain bacteria and parasitic helminths can re- 2. The argument for more parasites in conservation education duce the risk of immune-mediated disorders such as inflammatory bowel disease and asthma (Rook, 2009). While certain parasites are 2.1. Parasites are dominant and diverse still significant contributors to the global burden of disease in to- day’s world (Lopez et al., 2006), these ideas suggest that blanket Perhaps the simplest reason to consider parasites within con- parasite eradication strategies are not without unintended costs servation biology is their numerical dominance and taxonomic for human populations. diversity. is in fact the most common life strategy on the planet, with nine entirely parasitic phyla, 22 predominantly 2.3. Parasite conservation are alarming (>99%) parasitic phyla, and multiple parasitic clades within most of the remaining 11 phyla (DeMeeûs and Renaud, 2002; Dobson The modern day biodiversity crisis is most often portrayed in et al., 2008; Poulin and Morand, 2000). Recent estimates (based so- vertebrate terms, yet it is overwhelmingly a loss of invertebrate life lely on the diversity of described helminths) suggest that parasites (Dunn et al., 2009). This is more accurately portrayed as a mass outnumber free-living biodiversity by as much as 50%, and that at coextinction crisis (Dunn et al., 2009), in which parasites stand to least 76,000 parasitic species inhabit the nearly 45,000 species of be among the biggest losers (Lafferty et al., 2006). Parasites are described vertebrate hosts (Dobson et al., 2008; Poulin and one of the few groups for whom eradication remains a predomi- Morand, 2000). nant goal within public health strategies, and captive breeding and wildlife management programs (Wobeser, 2002). The long- 2.2. Parasites are of fundamental ecological and evolutionary term persistence of parasite diversity is intimately tied with host importance threats, from loss to overexploitation and (paradoxically) emerging disease. Finally, some parasite transmission cycles re- Beyond these striking figures of global diversity, parasites are quire the presence of multiple species (e.g. vectors and intermedi- critical to the conservation of fully functioning ecosystems. We ate hosts), and therefore require the conservation of multiple taxa, now understand parasites as major drivers of ecosystem organiza- often living in different . These factors and their interac- tion and and . Recent studies find tions can create unique and often synergistic threats to parasite that parasitic life strategies lie at the core of ecological processes persistence. that maintain species coexistence across space and time (Grewell, Compounding the issue, host conservation is a necessary but 2008). For example, host selectivity by the vine holoparasite insufficient step for parasite persistence. As parasites require host Cuscuta salina reduces the abundance of a dominant host species populations to remain above parasite species-specific thresholds of Plantago maritima in northern Californian salt marsh communities abundance to sustain transmission, it can often be expected that – promoting evenness among species, and contributing to species parasite species will disappear even when host populations persist co-existence (Grewell, 2008). At the level, the trema- at low levels (Dunne and Williams, 2009). Not surprisingly, the few tode Microphallus papillorobustus effectively causes population existing estimations of threat in parasite species paint a somber subdivision of their gammarid shrimp hosts within a single water picture. Estimates of the number of parasite species currently column by causing infected individuals to live closer to the surface threatened with extinction range vary according to the degree of than their uninfected counterparts (Ponton et al., 2005). At a con- host specificity assumed and estimates of host threat, ranging be- tinental scale, trypanosomiasis has long played a role in determin- tween 1959 (Gómez et al., 2011), 2115 (Dobson et al., 2008) to over ing the distribution of humans and animals across continental 5700 for helminths alone (Poulin and Morand, 2004). Hundreds of Africa (Knight, 1971; Rogers and Randolph, 1988). species are expected to already be extinct (Dunn et al., 2009). Parasites also strengthen trophic interactions (Kuris, 2005) and These numbers are especially telling when compared to current generally maintain a ‘‘cohesive matrix’’ of interactions within food figures for those vertebrates listed as critically endangered and webs (Lafferty et al., 2006). While our theoretical understanding of endangered (3300), and extinct and extinct in the wild (400), most food web relationships remain based on free-living - and with the numbers of parasitic actually listed by isms, empirical evidence demonstrates a positive influence of par- the IUCN Red List (1, the pygmy hog sucking ) (IUCN, asites on food web connectance: the percent of a food web’s 2009). realized use links (Lafferty et al., 2006). Connectance These conservation trends have not gone unnoticed by the con- has empirical and theoretical positive relationships with food servation community. Individual researchers have called for great- web stability (Dunne et al., 2002; Lafferty et al., 2006), and is pos- er attention to the plights of parasites and for their inclusion in itively associated with food web robustness in the face of second- conservation strategies, including early calls for ‘Equal rights for ary extinctions (Bascompte and Jordano, 2007; Dunne and parasites’ (Windsor, 1995), and demonstrations of their impor- Williams, 2009). Parasites in fact dominate food webs, which have tance in both in situ and ex situ conservation strategies (Gompper historically been viewed as principally driven by interactions and Williams, 1998; Perez et al., 2006). Some of these calls have among free-living species (Lafferty et al., 2006). Additionally, most come from the medical community (Pizzi, 2009), have been E. Nichols, A. Gómez / Biological Conservation 144 (2011) 937–941 939 included in recent scientific discussions (e.g. http:// The presentation of any topic in conservation education mate- symposia.cbc.amnh.org/archives/microbes/index.html), and even rial is obviously contingent upon existing basic scientific knowl- made it into the popular literature that critically bridges the gap edge. That our understanding of the diversity and ecological between academics and the general public (Zuk, 2007). Yet the importance of parasites is a relatively recent phenomenon could peer-reviewed conservation literature largely continues to present be one possible explanation for the pattern we observed. Yet, even parasite biodiversity mainly as a threat to free-living species from 1998 to 2009, when pro-parasite conservation messages were (Smith et al., 2009). well established, the ratio of conservation textbooks conveying ‘negative’ messages to ‘positive’ ones was 3:1.

3. Overlooking parasite conservation issues in education 5. Strengthening the teaching and practice of conservation How then are parasites treated within the formal textbooks that biology through parasites support conservation education at undergraduate and graduate levels? We conducted an informal assessment of 77 English lan- We believe that lack of inclusion of parasites in basic conserva- guage conservation textbooks we found readily available, spanning tion education hinders the advancement of conservation in a broad a publication range from 1970 to 2009 (Table 1 see Appendix for a sense, and specifically helps perpetuate the scarcity of knowledge complete list of references). We looked for the keywords ‘parasite’ about the practice of parasite conservation. If the next generation or ‘pathogen’ in the index of each book. When a textbook men- of conservation academics and practitioners are to move towards tioned either word, we categorized the parasite content and rele- greater practice of systems-level conservation and emphasize hu- vant context into three categories; positive, neutral and negative. man dependency on multifunctional landscapes, failing to provide Textbook content that was classified as ‘positive’ included any information on parasite functions and services in tandem with is- mention that parasite biodiversity faces conservation challenges, sues of epidemic and emerging disease in basic conservation cur- is worthy of inclusion within a conservation strategy, or has some ricula is both ecologically incomplete and incorrect. Additionally, utilitarian or intrinsic worth. Content deemed ‘neutral’ included a we find the prevalence of portraying of parasites as unilateral dis- basic ecological description of parasites or parasitism, some men- turbances or threats to biodiversity and to humans troubling. We tion of extant parasite diversity at any scale (within host, within believe that it is more important than ever that the next generation host populations, or global), or explained the ecological or evolu- of conservation biologists encounter parasites early in their aca- tionary roles of parasites in natural systems, without any explicit demic career, for the following reasons. reference to the ‘positive’ characteristics described above. Content classified as ‘negative’ were those that lacked of any mention of po- 5.1. Parasites embody conservation conflict tential conservation value (utilitarian or intrinsic) of the parasites themselves, and referred to parasites exclusively as causes of agri- Conservation of host–parasite interactions is plagued with chal- cultural decline, threats to captive species in ex situ conservation lenges and is a potential source of conflicts, representing a rich situations, or disease threats to humans, or wild plant and animal landscape of opportunities to teach about the conflicts that arise species. While these texts also often contained a neutral descrip- in the practice of conservation biology. First, as parasites are dele- tion of parasites or parasitism, they were unified in their system- terious for their host, to conserve parasites is to explicitly conserve atic treatment of parasites as a threat, with a clear lack of morbidity and mortality in host populations. This has potentially counter examples of their utility or intrinsic worth. negative implications for the hosts’ persistence (Macdonald and Laurenson, 2006), yet is a necessary step towards the conservation of overall ecosystem health (Hudson et al., 2006). This tension be- 4. Results tween individual and overall ecosystem health can be exacerbated by conservation practice, as many common conservation strategies The first reference to parasites in our sample of conservation designed for hosts have consequences for parasite biodiversity biology texts appeared in 1981, portraying them as a threat to agri- (Ezenwa, 2003; Lebarbenchon et al., 2006). culture (see Appendix). This was quickly followed by the first posi- Second, there may be conflicts when limited resources for con- tive mention of parasites in 1983. Of the 74 books published since servation efforts must be allocated. Conservation practitioners 1981, any mention of parasite biodiversity is entirely absent from have to make hard choices of which species, and which areas we 29 (39%). Twenty-four books (32%) present views of parasites so- prioritize. Managers interested in parasite conservation must deal lely as agents of disturbance or threats to free-living biodiversity. with population density or abundance targets for parasites that Ten textbooks (14%) espouse purely ecological, neutral descrip- straddle an often-thin line between endemic and epidemic. Erring tions of parasite biodiversity, and eleven (15%) contain at least a in either direction can threaten either parasite or host, or both. single sentence regarding parasites as objects of potential conser- Understanding these conflicts and finding potential avenues to vation value. Together, over 72% of the conservation textbooks alleviate them should be an important concern for conservation written since 1981 remain agnostic on the message that parasites biologists everywhere. Many conservation biologists are tasked are worthy of conservation consideration (Table 1). with evaluating risks and potential benefits, and generating sound management and communication strategies. In many ways, the Table 1 concept and conflicts brought about by parasite conservation pro- of parasite or pathogen related content found in 77 English language vides an ideal model with which to educate students about their conservation biology textbooks published between 1970 and 2009. The first future roles balancing disparate societal needs, and embodies these conservation textbook with parasite content classified here as ‘positive’ was intricate sets of non-overlapping goals among different stakehold- published in 1983. Complete reference information and study classification can be found in Appendix. ers that conservation professionals are likely to encounter. Finally, the public is generally unaccustomed to and often intol- Absent Negative Neutral Positive Total erant of visible illness in wild species. Intentionally managing for Total number of textbooks 32 24 10 11 77 parasite transmission may therefore result in a public relations Percent of total 1970–2010 42 31 13 14 100 challenge. Most emerging infectious pathogens of humans have a Percent of total 1983–2010 39 32 14 15 100 wildlife reservoir (Jones et al., 2008) and parasite conservation 940 E. Nichols, A. Gómez / Biological Conservation 144 (2011) 937–941 implies conserving this potential for emerging infectious spillover In our opinion, introductory conservation textbooks should in- to humans or domestic plants or animals. This may understandably clude at least five main points regarding parasite biodiversity. create potential conflicts with the public and with decision makers These include that parasites: (1) are diverse, and represent the in public health, planning and economic development. majority of all life in the planet, (2) are crucial players in ecological and evolutionary processes, (3) present challenges to conservation 5.2. Parasites call for multidisciplinarity practice through their roles in population declines, (4) deserve the same consideration to intrinsic, aesthetic and utilitarian value as Conservation science is inherently multidisciplinary. Under- their free-living hosts, and finally (5) are seldom targets of conser- standing parasites and their conservation requires input from sev- vation action. In a field that is largely predicated on changing hu- eral disciplines, merging the theory and practice of ecology, man attitudes, knowledge, beliefs, and behaviors to create conservation and , climate science, and the med- conditions favorable for the co-existence of humans and biodiver- ical and social sciences. Understanding the mechanisms behind the sity, parasite conservation represents a series of both opportunities response of free-living species to landuse change for example, may and challenges. often be incomplete without also including a parallel assessment of Demanding or even suggesting that we accept various degrees changes in parasite occupancy and abundance patterns (McKenzie, of morbidity (and even mortality) for the sake of species conserva- 2007). Zoonotic disease, the interrelation between environmental tion is a bitter pill to swallow, and will be heard by some ears as a change and health and between the health of humans and non-hu- challenge to the credibility of conservationists. Yet unless we intri- man species make the study of parasite biodiversity a rich way to gue and prepare the next generation of conservation leaders with illustrate the interrelatedness of life in the planet. Increasingly the information they will require to tackle these challenges, the important to the field of conservation, an appropriately broad view fate of the majority of species on earth may swing further in the of health extends beyond considerations of the simple absence of balance. infectious disease in individuals or populations, and includes envi- ronmental factors and health-sustaining ecosystem services. For Acknowledgements students, ensuring that this concept is grounded in a practical understanding of how multiple disciplines interact to create con- We would like to thank Eleanor Sterling and two anonymous servation outcomes is an important aspect of active teaching and reviewers for thoughtful commentary on this manuscript. E.N. also learning (Hudson, 2009). acknowledges funding from a Columbia University Faculty Fellow- ship and a Yeh Family Foundation Fellowship. 5.3. Parasites as a teaching tool Appendix A. Supplementary material Health is a topic of immediate concern, and infectious disease is a topic that, in our experience, elicits strong interest in a variety of Supplementary data associated with this article can be found, in audiences. All students have directly experienced the kinds of the online version, at doi:10.1016/j.biocon.2010.10.025. physiological, morphological, and behavioral changes that come with infectious disease. 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