key: cord-0036686-thrnwrwj
authors: Deem, Sharon L.
title: Conservation Medicine: A Solution-Based Approach for Saving Nonhuman Primates
date: 2016-07-29
journal: Ethnoprimatology
DOI: 10.1007/978-3-319-30469-4_4
sha: 30cb8d2dcb923744c2154ebce6042477f7df07a8
doc_id: 36686
cord_uid: thrnwrwj

Challenges that threaten the long-term survival of nonhuman primates (NHP) include habitat fragmentation, hunting, and increasingly, infectious diseases. In addition to direct mortality from noninfectious diseases (e.g., hunting) and infectious diseases (e.g., Ebola), human-driven alterations of environments that support NHP often contribute to a decline in population viability. This decline is frequently the result of physiological stress, poor reproduction, decreased immunity, and exposure to novel pathogens. To better understand the diseases that threaten NHP populations, a conservation medicine approach—the application of medicine to augment the conservation of wildlife and ecosystems—is imperative so that we may provide management solutions to help ensure the long-term survival of NHP. Additionally, it is crucial that we gain a better understanding of pathogens at the interface of nonhuman and human primates since the zoonotic potential may create conservation challenges, or alternatively may provide the impetus for conservation actions to be practiced (e.g., minimize bushmeat trade).

The pressures limiting the long-term survival of many wildlife species, including nonhuman primates (NHP), are largely human-driven (anthropogenic). These pressures include climate change, habitat degradation and fragmentation, invasive species, trade in wildlife, and exposure to emerging pathogens, all of which are associated with the human population growth which surpassed seven billion individuals in 2012. In fact, these anthropogenic changes have led many to contend that the Earth is presently in a new "Anthropocene" epoch (Crutzen 2002 ) . Simply stated, humans are the drivers of planetary health.

Humans have transformed between one-third and one-half of the land surface, and now appropriate over 40 % of the net primary terrestrial productivity , consume 35 % of the productivity of the oceanic shelf, and use 60 % of the freshwater run-off each year (Vitousek et al. 1986 ; Pauly and Christensen 1995 ; Postel et al. 1996 ; Rojstaczer et al. 2001 ) . Additionally, with an estimated 50 % increase in animalbased protein for human consumption by the year 2020, it is inevitable that human use of resources will continue to rise (Delgado et al. 2001 ) . Lastly, the estimated billions of live wildlife animals and animal products, including NHP, that are traded annually also place heavy burdens that threaten the long-term survival of species (Rosen and Smith 2010 ) . In addition to the direct impacts of the wildlife trade on conservation are the potentially devastating impacts from cross-species microbial mixing and exposure to novel pathogens.

There are many examples of disease-related population declines and extirpations, as well as an increasing number of species' extinctions related to pathogen exposure (Cunningham and Daszak 1998 ; Skerratt et al. 2007 ). (In this chapter, the word pathogen will be used for all infectious and parasitic agents including viruses, bacteria, fungi, and parasites.) Diseases have ecological impacts on multiple scales, affecting individuals (survival, reproduction), populations (population size, gene fl ow), communities (shifts in dominant or abundant species, changes in species composition), and ecosystems (changes in ecosystem structure, function, and resilience) (Deem et al. 2008 ) . All these potential disease-related impacts should be considered in NHP conservation initiatives, since an increasing number of disease events have been demonstrated to infl uence NHP populations (Wallis 2000 ) . During the recent decades of increasing anthropogenic conservation challenges, including the threat of diseases, the need for a holistic approach for conservation and health care-conservation medicine-was realized.

Conservation medicine is an ecologically driven and conservation-minded approach which fi rst appeared in the literature in the 1990s (Koch 1996 ) . Although there are a number of defi nitions for conservation medicine, at the core is the realization that the health of environments, and the animals and people within, are intimately related. Conservation medicine may best be defi ned as a transdisciplinary approach to study the relationship between human, animal, and ecosystem health to ensure the conservation of all biodiversity, including Homo sapiens (Koch 1996 ; Deem et al. 2000 ; Aguirre et al. 2002 ; Jakob-Hoff and Warren 2012 ; Deem 2015 ) . In its simplest form, it is the application of medicine to augment the conservation of wildlife and ecosystems, while ensuring human public health. A conservation medicine approach may involve the documentation, evaluation, monitoring, modifying, and/or prevention of diseases in wildlife (Deem et al. 2001 ) . Following on the heels of this holistic conservation medicine approach, for planetary health care was a "new" initiative termed One Health .

Starting in the 2000s, the One Health initiative has become widely accepted in both human and veterinary medicine, although initially the human medical profession may have more fully embraced the term, due in large part to the increasing recognition of globally signifi cant zoonotic emerging infectious diseases (EIDs) that threat human public health (Taylor et al. 2001 ; Kahn et al. 2007 ). However, the veterinary community also now embraces One Health, and indeed historically, it was a veterinary epidemiologist who coined the term One Medicine in the midtwentieth Century (Schwabe 1984 ; Gibbs 2014 ) . Many view this term as the building block for both conservation medicine and One Health. And if one wishes to go further in history, it was as early as the 1800s that a physician, Rudolf Virchow stated "Between animal and human medicine, there is no dividing line-nor should there be" (Klauder 1958 ) .

A One Health approach may be based less on an ecological understanding than conservation medicine. In fact, an early defi nition of the One Health concept stated that One Health is an initiative that aims to merge animal and human health science to benefi t both (Enserink 2007 ) . This defi nition, with the lack of ecosystem as one component of the triad, may miss the underlying, "Anthropocene" drivers of the health concerns that increasingly threaten human and animal health and biodiversity conservation . However, similar to conservation medicine, there have been a number of newer defi nitions of One Health that factor ecosystem health alongside humans and animals. One unifying theme has been that One Health is a strategy that strives to expand transdisciplinary collaborations and communications to improve health care for humans, animals, and the environment (Kahn et al. 2012 ). This defi ning theme is rather analogous to conservation medicine and thus semantics aside, we may see One Health and conservation medicine as two names for across discipline strategies to improve health care for the planet. In this chapter, we will call this holistic health care approach, focusing across ecosystems, animals and humans, conservation medicine since our primary objective is the long-term conservation of NHP species globally.

The long-term survival of many NHP species demands a conservation medicine approach. In today's "Anthropocene epoch," threats to NHP conservation are similar to other taxa and as such are mostly anthropogenic. Habitat loss and degradation, encroachment of humans and their domestic animals into NHP habitat, hunting for the pet and bushmeat trades, and increasingly infectious disease events continue to intensify and threaten NHP survival (Walsh et al. 2003 ; Chapman et al. 2005 ; Wich et al. 2011 ; LeBreton et al. 2012 ; Schwitzer et al. 2014 ). Human population growth and the rapid destruction of forested habitat are bringing humans and NHP into ever-increasing contact (Fig. 1 ) .

Although the exact number of NHP species is unknown, as new species are still being discovered and taxonomic reshuffl ing occurs, the IUCN Red List of threatened species has 92 % of all NHP species classifi ed as critically endangered, Fig. 1 A confi scated orphaned chimpanzee interacting with people at a café on the beach in Gabon. © Sharon L. Deem endangered, vulnerable, near threatened or of least concern ( http://www.iucnredlist. org , accessed January 24, 2015). For example, all of the great apes are listed as endangered or critically endangered, and 94 % of the world's lemur species are listed as critically endangered, endangered, or vulnerable Schwitzer et al. 2014 ) .

One major component of NHP conservation, and human public health, is the current realization that infectious diseases increasingly threaten species across the globe. In fact, anthropogenic global modifi cations are the most important variables associated with disease events in wildlife, including NHP, today (Dobson and Foufopoulos 2001 ) . As the threat of EID has become a tangible risk for NHP and human public health, this area of study has become increasingly important within NHP conservation (Wolfe et al. 1998 ; Wallis and Lee 1999 ; Wallis 2000 ; Daszak et al. 2000 ; Chapman et al. 2005 ) . Zoonotic pathogensthose agents shared between animals and humans-comprise 60.3 % of EIDs in humans, and of these, 71.8 % have originated from wildlife hosts and include sudden acute respiratory syndrome (SARS) , avian infl uenza, Ebola, monkeypox, and West Nile virus (Jones et al. 2008 ) . Although all animals may serve as a reservoir of zoonotic pathogens, NHP are one of the most common taxa to share infectious agents with humans.

One reason that pathogen sharing between NHP and humans is so common is because as our closest relatives they are the weakest barrier to cross-species transmission. An expression of this lack of a barrier is that primates constitute only 0.5 % of all vertebrate species but have contributed about 20 % of our major human diseases (Wolfe et al. 2007 ). Conversely, it has been well documented that infection with human pathogens may have fatal consequences for immunologically naïve NHP in captivity (Ruch 1959 ; Brack 1987 ) . Now there is evidence of similar events, with potentially catastrophic effects, in free-living NHP populations (Wolfe et al. 1998 ; Wallis and Lee 1999 ; Leroy et al. 2004 ). Chimpanzees, bonobos, and gorillas, as the NHP most phylogenetically similar to humans, are also the most highly susceptible to human pathogens, especially viruses (Benirschke and Adams 1980 ; Brack 1987 ; Ott-Joslin 1993 ; Wallis and Lee 1999 ; Wolfe et al. 1998 ; Murphy 2012 ; Gilardi et al. 2014 ) .

Of most concern at the NHP-human interface is hunting. Primates can make up over 10 % of captured animals in some areas (Wilkie and Carpenter 1999 ; Fa et al. 2003 ; Willcox and Nambu 2007 ) . The handling and consumption of NHP bushmeat provides an effective means for the spread of pathogens from NHP to humans. The best-known example for NHP-human transmission is the emergence of HIV, which originated from the simian variant of the virus SIV (Gao et al. 1999 ; Hahn et al. 2000 ; Wolfe and Switzer 2009 ) . Other important examples involve HTLV-1, which originated from STLV-1, simian foamy viruses, and Ebola virus (Morell 1995 ; Makuwa et al. 2004 ; Engel et al. 2006 ; Wolfe and Switzer 2009 ) . Ebola is a grave public health concern, but is also capable of extreme great ape population impacts including a documented 80 % decline of gorilla and chimpanzee populations in the Gabon/Republic of Congo border region in the early 2000s (Huijbregts et al. 2003 ; Walsh et al. 2003 ; Leroy et al. 2004 ).

The opposite transmission event-human-to-NHP ( anthropozoonoses )-historically has been less frequently reported. Few cases of human to NHP pathogen transmission have been demonstrated conclusively, but examples include giardia, sarcoptes mange, metapneumonia and other respiratory viruses, and herpes virus into NHP through ecotourism and conservation activities (Nizeyi et al. 1999 ; Cranfi eld et al. 2002 ; Kalema-Zikusoka et al. 2002 ; Kaur et al. 2008 ; Köndgen et al. 2008 ; Gilardi et al. 2014 ) . Other examples of infectious agents of NHP conservation concern that have a human link include Cryptosporidium, Plasmodium knowlesi , and measles (Hirsch et al. 1995 ; Wolfe et al. 1998 ; Rouquet et al. 2005 ) . These human-to-NHP transmission events are signifi cant for NHP conservation, but also substantiate the fact that pathogen sharing is bidirectional (Chen et al. 2011 ; Palacios et al. 2011 ) .

Although possibly less direct than pathogen exposure, potentially devastating impacts for NHP survival from human presence are those stressors (e.g., habitat fragmentation and degradation) that may cause behavioral modifi cations, reproduction decline, and poor immunity, along with traumatic injuries (e.g., snares), all of which may contribute to poor population viability (Chapman and Peres 2001 ; Junge et al. 2011 ; Cranfi eld et al. 2002 , Oates 2013 . Additionally, a number of research projects and management efforts for NHP conservation involve handling of animals that may require anesthesia and other veterinary techniques (Deem et al. 2001 ) . Conservation medicine offers a transdisciplinary approach and in this chapter, we will present some of the more common applications that are imperative for the longterm survival of NHP populations (Fig. 2 ) . 

Pathogens as part of any living community are known to drive evolution (Deem et al. 2010 ) . In fact, the evolution of a wide variety of behaviors observed in primates, ranging from the consumption of medicinal plants to fl y-swatting and other behaviors aimed at reducing contact with insect vectors of disease are driven by these agents (Huffman 1997 ; Dudley and Milton 1990 ) . Therefore, a fi rst step in understanding the role of pathogens in primate ecology is by surveillance to improve our knowledge of primate pathogens and their occurrence in natural populations (Nunn and Altizer 2005 ) . Data gleaned from surveillance programs that may be crucial for conservation efforts include knowing which pathogens are present, what percentage of any given population is infected, and how these pathogens impact NHP population viability (e.g., morbidity and mortality). Yet these data are still sadly limited. For example, even in lemurs, a taxa with a number of critically endangered species, the fi rst exogenous viruses of any lemur species were just described (Lim et al. 2015 ) .

Surveillance programs of NHP populations may also indicate the risk of EID for humans, serving as important "sentinel species" for predicting human disease outbreaks (Wolfe et al. 1998 ; Rouquet et al. 2005 ; Leendertz et al. 2006 ). Programs such as the USAID PREDICT project will help to determine pathogen presence and provide missing data necessary for zoonoses preparedness, while gathering data important for conservation (Morse et al. 2012 ) . Other programs such as the Great Ape Health Monitoring Unit (GAHMU) is a transdisciplinary approach for the diagnoses of pathogens in great apes, with an objective to create a long term, systematic sampling system (Leendertz et al. 2006 ) . This program provides detailed health monitoring on wild great ape populations to establish baseline infectious agent exposure data of healthy animals, as well as to determine pathogens potentially causing morbidity and mortality. Similar surveillance programs exist for NHP populations in Asia and South America (Engel et al. 2006 ; Vitazkova 2009 ; Arajújo et al. 2013 ) . In fact, it is in Asia, with temple monkeys, and South America, with urban green centers providing habitat that may harbor a growing number of NHP, that close proximity of NHP and humans is increasing and the surveillance of pathogens in these populations is imperative.

Disease Risk Analysis is another conservation medicine approach that has gained momentum in recent years to help with our understanding of the health challenges that threaten wildlife conservation (Deem 2012 ) . Disease risk analysis is a formal procedure for estimating the likelihood and consequences of adverse effects occurring in a specifi c population, taking into consideration exposure to potential hazards and the nature of their effects (Thrusfi eld 2007 ). Components of a disease risk analysis consist of four interconnected phases: (1) hazard identifi cation, (2) risk assessment, (3) risk management, and (4) risk communication (Thrusfi eld 2007 ; Deem 2012 ) . All the phases are interactive with the others, and therefore the process should be iterative and not simply fl ow from phase 1 to 4. Hazard identifi cation may be viewed as the identifi cation of what may go wrong. It is important to identify what diseases have potential effects harmful enough to warrant inclusion in the disease risk analysis. These hazards may be infectious (e.g., Ebola virus) or noninfectious (e.g., snare wounds), with the criteria for inclusion in the disease risk analysis dependent on the potential for negative impacts. Risk assessment is the range of calculations required to estimate release, exposure, and consequence parameters for infectious diseases, or for noninfectious diseases the likelihood and consequences of a disease occurring in a population. Risk management provides conservationists with a focus on those responses that may decrease the likelihood of an adverse outcome and/or reduce the consequences if such an outcome occurs. This element of risk analysis may best be viewed as the reason for performing the analysis so that science may move into action. The fourth component, risk communication is a continuous process, necessitating respectful communication among the multiple stakeholders throughout the risk analysis (Offi ce of International Epizootics 2004 ). For a more in-depth discussion of this important tool for non-human primate conservation, please see Thrusfi eld ( 2007 ) and Deem ( 2012 ) .

A number of disease risk analyses for free-living NHP populations have been conducted. One example is an analysis using retrospective health data from the long-running Gombe chimpanzee study (Lonsdorf et al. 2006 ). This study provides an excellent example of how retrospective data may be used within a disease risk analysis framework. The analysis enumerates various factors, including a better understanding of disease threats to an endangered species, a guide to improve health data collection, and proper risk communication to advance highquality health care standards. A second study was derived from a workshop on Southeast Asian Macaque Risk Analysis. Field and laboratory data and expert opinion were combined to develop a model to predict transmission of simian foamy virus between temple macaques and humans accurately (Engel et al. 2006 ) . This study provides an example of integrating real data with expert opinion for a better understanding of zoonotic pathogens at the interface of semiwild NHP and humans.

A disease risk analysis in African great apes was performed using GIS overlay of data (Sleeman 2005 ) . Human demographic data and core human health indicators for African great ape range countries were evaluated. The combined indicators of environmental stress/vulnerability (as a proxy measure of human-great ape contact), and infant mortality rate and healthy life expectancy were used as separate indicators of disease burden among the human populations living in great ape ranges. These indicators were analyzed to create maps of critical areas with both environmental stress and high burden of human diseases, both signifi cant for great ape conservation (Sleeman 2005 ) .

An ex situ-in situ NHP conservation medicine approach exists at a growing number of zoos and primate centers. Many of the veterinary techniques (e.g., anesthesia) and preventive, diagnostic, and therapeutic care available for primate conservation projects are fi rst perfected with collection animals (Ølberg 1997 ; Sleeman 1997 ; Williams and Junge 1997 ; Calle and Joslin 2012 ; Murphy 2012 ) . Much of what we have learned about NHP infectious diseases, and their zoonotic potential, were fi rst discovered with animals in captivity but have implications for free-living populations (Ruch 1959 ; Brack 1987 ) . One project that offers a fence to fi eld link is the great ape heart program which strives to better understand the cardiovascular health challenges in great ape species ( http://greatapeheartproject.org/ accessed on January 24, 2015).

Another important fence to fi eld connection is the outreach and education these facilities provide to inspire people to care about NHP. Many zoos and primate centers participate in recovery plans that focus on the health and reproduction of collection animals as insurance populations and species' ambassadors, while also providing money, time, and resources to free-living NHP conservation efforts.

Increasingly this ex situ-in situ link is also conducted at NHP sanctuaries and rehabilitation centers globally. These centers often provide humane care for injured and confi scated NHP. Unfortunately, the close human to NHP contact at these sanctuaries and centers may lead to zoonotic disease issues, and conservation challenges if repatriated NHP carry human pathogens back into the wild. For example, a confi scated juvenile eastern lowland gorilla that had signifi cant human contact during care was diagnosed with a clinical case of human herpes simplex virus type 1 (Gilardi et al. 2014 ) . As a potentially chronic infection, the release of this gorilla back to the wild could serve as a vehicle of introduction of a human pathogen into the free-living population. The need for these centers to provide health care using a conservation medicine approach that ensures healthy animals and healthy people is being increasingly supported ( http://www.pasaprimates.org/ accessed January 24, 2015).

As discussed above, the NHP bushmeat trade is one of the biggest conservation challenges faced by many NHP species, but also has dire public health implications as best exemplifi ed by Ebola and HIV. The use of NHP for food and within the pet trade places serious pressures on free-living populations while also providing a perfect vehicle for pathogen transmission between NHP and humans. The benefi t of understanding this risk of pathogen transmission may allow for these data to help establish regulations to limit the trade in NHP. Poverty and hunger complicate the strength of this information. However, using a conservation medicine approach by working for alternative food sources while emphasizing human health, NHP populations may be better protected due in part to knowledge of zoonotic disease concerns (Golden et al. 2014) .

A second growing use of NHP has been in ecotourism. A sustainable version of tourism, ecotourism is a signifi cant proportion of all tourism which is estimated to generate more than 9 % of the global domestic product and may account for almost half of the gross domestic product in developing countries with biodiversity-rich areas (Muehlenbein and Ancrenaz 2009 ) . The need to perform ecotourism in a manner that does not harm the very NHP that tourists are keen to visit, leads to the need for preventive measures to ensure that the health of both human and NHP participants is not jeopardized. In the case of great ape ecotourism, which necessitates habituation, the stress of human proximity as well as the potential for zoonoses and anthropozoonoses makes the need for a conservation medicine approach imperative (Nutter and Whittier 2001 ; Woodford et al. 2002 ; Macfi e and Williamson 2010 ).

Combining all these approaches into an integrated conservation medicine program for NHP conservation is best exemplifi ed by the mountain gorilla program in Central Africa. This program is structured with a clear understanding that the conservation of mountain gorillas is inextricably linked to the health of their ecosystem, the health of humans who frequently contact gorillas, and the health of the animals themselves (Cranfi eld et al. 2002 ) . Documenting that infectious diseases are only second to trauma as a cause of death in this species, a conservation medicine approach that includes habitat health, preventive and therapeutic medicine for human and NHP alike is crucial (Mudakikwa et al. 2001 ) . And with 70 % of all traumatic lesions from 1971 to 1995 snare related, veterinary intervention for these injured gorillas may be a necessity for the long-term survival of the species (Cranfi eld et al. 2002 ) .

The Kibale EcoHealth Project is another example of a conservation medicine approach in that the aim is to better understand the health links at the interface of humans-animals and the ecosystem in a region with high NHP biomass (Goldberg et al. 2012 ) . This project has demonstrated the transmission of infectious agents from humans and their domestic livestock to primates in the region (Goldberg et al. 2007 ; Rwego et al. 2008 ) . Therefore, one of the big goals of the project, to promote human livelihoods and health, helps to ensure NHP conservation.

The many conservation challenges that threaten the long-term survival of NHP species are complex. These mostly anthropogenic threats, from habitat degradation to hunting to zoonoses/anthropozoonoses may differ depending on the species of NHP and/or geographical region, but most present serious health concerns for free-living NHP populations. The continuum from infectious disease epidemics, that may extirpate entire populations, to the more chronic stressors of habitat degradation and human encroachment, decreasing immunity and reproductive success, demand a conservation medicine approach. Additionally, with the zoonotic link between NHP and humans, which is predicted to become more serious as stable ecosystems and large genetically diverse populations of NHP are increasingly stressed by humans, the need for a conservation medicine approach has never been more urgent. Transdisciplinary conservation medicine teams may include ecologists, primatologists, veterinary and medical professionals, sociologists, anthropologists, and politicians, along with local stakeholders and laypersons. These teams are necessary to achieve the primary goal of minimizing the human created stressors and diseases that threaten the survival of NHP. As they say, "it takes a village."

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