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International Journal for Parasitology 35 (2005) 725–732 www.parasitology-online.com Invited review Parasites, ecosystems and sustainability: an ecological and complex systems perspective Pierre Horwitza,*, Bruce A. Wilcoxb b a Consortium for Health and Ecology, Edith Cowan University, 100 Joondalup Drive, Joondalup, WA 6027, Australia Asia-Pacific Institute for Tropical Medicine and Infectious Diseases, John A. Burns School of Medicine, University of Hawaii, Honolulu 96822, Hawaii Received 20 December 2004; received in revised form 16 March 2005; accepted 16 March 2005 Abstract Host–parasite relationships can be conceptualised either narrowly, where the parasite is metabolically dependent on the host, or more broadly, as suggested by an ecological–evolutionary and complex systems perspective. In this view Host–parasite relationships are part of a larger set of ecological and co-evolutionary interdependencies and a complex adaptive system. These interdependencies affect not just the hosts, vectors, parasites, the immediate agents, but also those indirectly or consequentially affected by the relationship. Host–parasite relationships also can be viewed as systems embedded within larger systems represented by ecological communities and ecosystems. So defined, it can be argued that Host–parasite relationships may often benefit their hosts and contribute significantly to the structuring of ecological communities. The broader, complex adaptive system view also contributes to understanding the phenomenon of disease emergence, the ecological and evolutionary mechanisms involved, and the role of parasitology in research and management of ecosystems in light of the apparently growing problem of emerging infectious diseases in wildlife and humans. An expanded set of principles for integrated parasite management is suggested by this perspective. q 2005 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. Keywords: Parasites; Ecosystems; Sustainability; Emerging infectious disease; Integrated parasite management; Complexity 1. Introduction Host–parasite relationships are the ‘unseen’ part of an ecological community affecting, as do predator–prey relationships and inter-specific competition, species distribution and abundance and thus community composition. Parasites and their hosts are part of ecological communities, and just as they cannot be considered in isolation from one another they cannot be separated from the communities of which they form a part. Nor can Host–parasite relationships or their ecological communities be fully understood outside the ecosystem context within which both exist. We can conceive of Host–parasite relationships as being embedded. Hosts have other parasites, competitors and predators and each parasite has other hosts or vectors, and so on. Hosts are linked to other species and non-living * Corresponding author. Tel.: C61 8 63045558; fax: C61 8 63045509. E-mail address: [email protected] (P. Horwitz). properties of their surroundings, and so are parasites, depending on their life cycle. All of them are influenced by their environment. It is a truism to say that all Host– parasite relationships exist within a system, whether urban or agricultural systems, or ones where humans play a less dominant (but still significant) role, like a marine ecosystem. These complexes are dynamic and constantly changing and co-evolving. Our aim in this paper is to examine Host– parasite relationships from this perspective drawing on the notion of complex systems. According to this theory, all complex systems share similarities such as the nesting of systems within systems, non-linearity, uncertainty, scale, emergence and selforganisation (Levin, 1999; Gunderson and Holling, 2002), none of which are properties of simple systems. Exploring Host–parasite relationships and their ecological communities as such may provide insights into Host– parasite phenomena and ecosystem change, particularly where human health or natural resources are concerned. 0020-7519/$30.00 q 2005 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ijpara.2005.03.002 726 P. Horwitz, B.A. Wilcox / International Journal for Parasitology 35 (2005) 725–732 Finally, considering Host–parasite relationships from a complex systems perspective may assist in formulating more effective methods of disease management. 2. On the relativity of Host–parasite relations Parasites by definition have a dependence on their host for their survival and growth. Behind this simple conception lies a complexity that reflects the degree of dependence, of virulence, or both, and how these vary in time and space. The notion of dependence is relative, not absolute. As pointed out by Smyth (1994), a particular parasite may lie somewhere along the scale of 0% metabolic dependence (or being absolutely free-living) to 100% metabolically dependent (or ‘totally’ parasitic). The standard depiction found in textbooks of one host– one parasite systems, with parasites benefiting but injurious to hosts (C/K), commensals benign to the host (C/Z) and mutualists beneficial to host (C/C), belies the ecological– evolutionary nature and co-evolutionary behaviour of inter-species relationships, and the ecological complexes they constitute (see Smyth, 1994). An ecologic rule according to Hubalek (2003) specifies that an obligatory parasite should not kill (cause the ultimate harm to) its host to benefit from the adapted long-term symbiosis. Highly virulent parasites may lose their virulence, eventually resulting in a mutualistic relationship with the host. Host– parasite relations may switch from being apparently benign to injurious, that is, disease causing (Ewald, 1983). This may occur through context-dependent virulence in response to host condition, or through a ‘strategic’ expression of virulence aimed at enhancing transmission (Brown et al., 2003). These shifts occur at different temporal scales, either within the generation time of the host, or over perhaps extraordinarily long periods in an evolutionary sense. Thus any Host–parasite relationship is a dynamic one, shifting along a continuum precisely definable only at an instant in time and space. Much like a waltz, the ‘partners’ are constantly adapting to each other’s ‘moves’ in responses to the presence, or potential presence, of each other. This adaptive response can be behavioural, genotypic or phenotypic, implicating each of the partners, and the interaction between them, environmental noise and spatial population structures. An added dimension to this waltz is at what stage the injurious action occurs, and to whom. The standard definitions of host and parasite can obscure these ecological and evolutionary shifts and shuffles. The tendency has been to refer to disease-causing metazoan agents as ‘parasites’ and all other (invariably microbial or microscopic) organisms injurious to their hosts as ‘pathogens’. Size, coupled with the complexity of the life cycle, and the degree to which sexual reproduction occurs in or on a host, has lead to an epidemiological categorisation of ‘microparasites’ and ‘macroparasites’ (Anderson and May, 1979), though it is usually acknowledged as being somewhat arbitrary. The complex vector biology and food webs of some arboviruses (i.e. mosquito borne alphaviruses like Ross River virus in Australia; Mackenzie et al., 1994), or flatworms that reproduce on their host (ie. Temnocephalan flatworms on freshwater crayfish; Damborenea and Cannon, 2001) are examples. Arbitrariness also is evident in the grouping of diseases or parasites according to the source of the infection, of paramount importance to epidemiology (Hubalek, 2003). For parasites of humans, infections are categorised as anthroponotic (transmissible from humans to humans), zoonotic (from living animals to humans) or sapronotic (from abiotic environment like soils, water, decaying organic material etc. to humans). Further categorisation posits synanthropic zoonoses for sources of infection that are domestic and other animals associated with humans, and exoanthropic zoonoses for sources that are feral and wild, in ‘natural’ (non-human) settings (Hubalek, 2003). These categorisations breakdown for parasites that have more than one source, or where sources of infection appear to change, as they inevitably do. Arguably both these ‘exceptions’ might be the ecological rule in evolutionary time, and both are exemplified by ecosystem changes caused by human activities as described below. 3. The context and systems nature of parasite–host relationships The necessary arbitrariness of Host–parasite classification used in epidemiology and parasitology, which of course is not uncommon in classification systems of other health or biological disciplines, reflects the reality of ecosystems as complex adaptive systems (Levin, 1999; Gunderson and Holling, 2002). In light of this, it should be worthwhile asking whether there are principles from this body of theory that explain the conditions, dynamics and mechanisms involved in the movement along the continua from beneficial or not, injurious or not, dependent or not, and the jumping of parasites to new hosts? Since Host– parasite relationships are ecological, invariably involving communities and ecosystems, what does ecological theory, including that incorporating complexity theory, tell us? Here we examine three aspects of Host–parasite relationships in this regard: (i) the scaled nature of Host– parasite relationships in ecosystems (ii) the benefits of being parasitised and (iii) the role of Host–parasite relationships in ecosystem functioning. 3.1. Scales of parasitism Models that have been developed to describe the dynamics of parasitism (in particular parasitic worms and their hosts) require only minor modifications to describe the dynamics of an organism (as a guest) in its habitat patch (host) (Dobson, 2003). Described as such, an individual P. Horwitz, B.A. Wilcox / International Journal for Parasitology 35 (2005) 725–732 organism (i.e. a parasite) behaves as a system within its host, itself a system, nested within an ecological community, another system. An ecological community can be described as existing within a larger ecosystem, and so on. Thus parasitism can be viewed as a series of smaller systems, nested within larger systems, existing on increasingly larger space and time scales. This long accepted view of hierarchy in ecological communities has been explicitly defined by Allen and Starr (1982), more recently modified and elaborated to account for their cross-scale dynamics and other emergent properties (Gunderson and Holling, 2002), and described for ecological systems generally as the fundamental property of self-organisation (Birkes et al., 2003). Internal order is maintained at each level (or of each system) only by importing available energy/matter from, and exporting wastes back into, their host environments (see Gunther and Folke, 1992; Rees, 1998). Fig. 1 illustrates how dynamics operating on vastly different scales interact, and the broad causal mechanisms by which change and events on one scale produce effects on another. This figure, adapted from Holling and colleagues (see Holling, 1986; Gunderson and Holling, 2002) describes how interaction of ‘fast variables’ at the micro-scale and ‘slow variables’ at the macroscale are mediated by ‘mesoscale’ dynamics. A key mm cm m 100m 10km 1000 km 10,000 climate change century vertebrates ENSO decades log time (years) fire floods invertebrates years/ months storm protozoans weeks squall/ windstorm bacteria days winds virus hours mutation minutes log space (meters) Fig. 1. Diagrammatic representation of the scaled nature of Host–parasite relationships. Major groups of organisms (yellow) represent a continuum in spatial-temporal scales in which their life cycles and Host–parasite relationships are carried out. Disturbance/variation is represented by some examples on the right hand side (in orange), showing the scales at which they operate. Cross-scale mediations lie between these two continuums, and are represented in this figure by an elongate shape that expands towards the larger space and longer time scales. Two hypothetical examples of cross-scale mediations are shown by arrowed curves: one where a large scale long-timed event influences the nature of a viral infection of a protozoan (where the Host–parasite relationship is shown as a bold curve), and the second where a mutation in a bacterium alters a Host– parasite relationship (shown as a bold dotted curve) which influences the timing and spatial coverage of a fire. 727 problem in understanding the behaviour of ecosystems is explaining the operation of cross-scale influences. Obviously, highly local and short-term events such as the infection of a single host organism, or base-pair substitution in a single genome resulting in increased infectivity or pathogenicity may ultimately transform a Host–parasite system on a regional or even global scale, with compounding ecosystem consequences. Similarly, relatively gradual events or changes such as climate shifts or human transformations of a river catchment, river basin, on a regional or even global scale may influence the dynamics of Host–parasite systems locally. Fig. 1 illustrates three kinds of variables along space–time continua: a hierarchy of hosts and parasites according to size and generation time; atmospheric processes and associated environmental events; and cross-scale influences that mediate between the former two sets of variables. The figure illustrates how discrete processes (the life cycles of bacteria and decadal storm events) occurring on vastly different space–time scales are linked through cross-scale influences consisting of a set of continuous, interdependent processes (landscape change, parasite–host dynamics, and infection). 3.2. The benefits of being parasitised It can be demonstrated that the host and the parasite can co-exist at the population level over time, even when the parasite is highly virulent at some stage of that time continuum. Modelling has demonstrated that host density dependence, genetic variation (of both the host and the parasite), and sexual reproduction can stabilise a Host– parasite system (Flatt and Scheuring, 2004). Summers et al. (2003) argue that theory and evidence both point to the pervasive contribution made by parasitism on polymorphism within populations and divergence between populations and species. They proposed various types of co-evolutionary interactions: for instance, a Host–parasite interaction can produce an escalating arms race in which phenotypic traits under polygenic control undergo reciprocal increases over evolutionary time. Co-evolution between parasites and hosts is mediated via host recognition of parasite molecular elicitors, where recognition ability of hosts is matched by evasion capabilities of parasites. This occurs relatively rapidly, depending on the selective pressures and costs associated with each response. Also, the much shorter generation time and faster growth rate of a parasite population in relation to that of its host (as represented in Fig. 1) demonstrates that ‘evolutioning time’ for a parasite is often only ‘ecological time’ for the host, though the host’s immune response is evolutionary in its behaviour as a complex adaptive system (Jannsen, 2005). The Host–parasite relationship can involve co-existence at the individual or population level, even though it involves the diversion of resources by the parasite from the host that could otherwise be used for the host’s growth, maintenance or reproduction. How this asymmetrical relationship could 728 P. Horwitz, B.A. Wilcox / International Journal for Parasitology 35 (2005) 725–732 possibly persist becomes apparent considering the ecosystem-level interactions. When viewed as part of an ecosystem, the parasitised host is subject to numerous other interactions that convey benefits, no apparent benefits, or harm or disbenefits to it. Thomas et al. (2000) argued that the direct costs to the host that reduce its fitness can be either exacerbated by indirect consequences (i.e. where parasitism renders predation more likely), or alleviated by indirect consequences. The alleviation conveys a benefit of being parasitised: (i) when the risk of being eaten is high, the infection by a parasite that induces avoidance by predators or cannibals would be advantageous; (ii) when harmful parasites are abundant, being infected by a less harmful parasite that prevents the establishment of other parasites may be advantageous (i.e. less virulent strains colonising host may convey a protection against closely related but more virulent strains); (iii) when a host can reduce the effects of its competitors (i.e. some host species can invade new areas only because the parasites they carry are more pathogenic to endemic hosts than they are to their original hosts; but see below); (iv) when exposure to parasites, and subsequent resistance to them, might play a role in mate choice of hosts; (v) when the direct cost of parasitism could be compensated for by the benefits of parasites as accumulators of toxins, through a mediating effect under conditions of deficient trophic conditions, or conferring some sort of resistance to an external stress, like the advantage conveyed by plasmids in bacterial antiobiotic resistance. In evolutionary terms, therefore, there are good reasons why we should see parasites as conveying a selective advantage to their hosts under certain circumstances. Thomas et al. (2000) concluded that “.the role of parasites as selective agents in the evolution of the host species requires a precise knowledge of the net selective pressures they really exert”, and that an exploration was required of the kinds of intimate connections that could exist between the symbiotic systems and their ecosystems as a whole. The phrase ‘under certain circumstances’ conveys the complexity of the relationships found within mutualism/ symbiosis, commensalism and parasitism. Our understanding of these circumstances that deliver benefits rather than disbenefits has been furthered by the studies of animal and plant invasions, and biological conservation. From an invasion perspective it has been argued by Prenter et al. (2004) that parasitism is implicated in the invasion process in three ways: (i) parasites have been important in invasions when naı̈ve host populations are infected by a new parasite transported with introduced hosts, thereby conveying an advantage to the invader; (ii) invaders lose their (co-evolved) parasites in the process of invasion, leading to the higher demographic success of invaders (the so-called ‘enemy release hypothesis’) (iii) invaders are often protected from native parasites due to the absence of transmission routes that may be specific to native hosts. These principles might be applied to all biological activities that result in the establishment of populations in areas where they have never been, or are not now, found. Where introduced disease has been implicated in an invasion that has led to the endangerment of a native species, a relevant question for conservation biology arises: if captive breeding is used, might it be better to ensure that their parasite loads are kept rather than reduced prior to reintroduction? (see Holt et al., 2003). Lyles and Dobson (1993) noted that reduced exposure to infectious disease may lower immunocompetency of individuals, reducing herd immunity, rendering groups of individuals vulnerable to infectious disease outbreaks. 3.3. The role of parasitism in ecosystem function Prenter et al. (2004; see also literature cited in Marcogliese, 2005 this issue) showed that studies of two host–one parasite systems can be used to suggest that parasites structure biological communities. This can occur either through catastrophic loss of key species, or pathogen outbreaks that produce total loss of species and flow-on effects for larger communities. However, they argued that the predominant pressure exerted by parasites on communities might not be the result of catastrophic outbreaks, but rather of less virulent, persistent and sub-lethal effects, where the parasites moderate or enhance the competitive or predatory capabilities of their hosts. Summers et al. (2003) also examined the role played by parasitism in structuring communities and underpinning diversity. They reviewed the evidence for Howe and Smallwood’s (1982) tropical rainforest ‘Escape Hypothesis’, where parasitism of seeds and young trees would be greatest in proximity to the parent trees and conspecific adults. This would favour individuals that attempt to establish more distantly, a frequency-dependent spacing mechanism that would create spaces for other species, promoting the alpha diversity of the forest. They concluded that the weight of evidence supported a hypothesis of density and frequency dependent herbivory and parasitism playing a crucial role in promoting diversity. It is clear then that parasitism, under all its forms and guises, is a profoundly important ecological process. In the context of wildlife and human infections, parasitism is not simply a pathogenic relationship requiring treatment, but rather a process that through multiple agencies contributes to within and between species diversity, community P. Horwitz, B.A. Wilcox / International Journal for Parasitology 35 (2005) 725–732 structure and diversity, and therefore to the ability of organisms to respond to change. Its significance, and ecologists’ lack of recognition of the significance has prompted some foundational work in areas like mathematical epidemiology (Anderson and May, 1991). 4. Emerging Host–parasite relationships The cross-scale nature of the affects of Host–parasite relationships in ecosystems, the benefits of being parasitised, and the role of Host–parasite relationships in ecosystem functioning all suggest a broader interpretation of disease and of the role of ecosystem change in disease emergence than is normally considered. When ecosystems change some species are advantaged in the sense that they are presented with opportunities that previously did not exist to them. ‘New diseases’ are an example (Yuill, 1986). The so-called ‘emerging infectious diseases’ (EIDs) have been connected with land-use change and the changing nature of the land-water interface, where parasite and host switches can occur as either ‘spillover’, cross-species transmissions or introductions/extension of geographic range into new or changed habitats (Patz et al., 2004). Patz et al. (2000) summarise the types of environmental changes and conditions that contribute to the proliferation of emerging zoonotic parasitic diseases, arguing that most have three distinct life cycles: sylvanic, zoonotic, and anthroponotic. They outline a number of characteristic ways in which parasite-vector-host relationships can be distorted by changes to land and water conditions. Deforestation, replacement of forests with crop farming, ranching, small animals, bodies of water in disrupted areas, and human movement all contribute to changing breeding conditions of vectors, and changing non-human and human host populations, resulting in shifts between parasites, vectors and their hosts (see also Lafferty and Kuris, 1999; Wilcox and Gubler, 2005). Animal conservation programmes, nature reserves or wildlife refuges can contribute to the process by harbouring vectors and parasites during shifts from zoonotic to anthroponotic life cycles. These types of shifts are exacerbated by water ‘development’ projects, road construction and changed access to forested areas, the El Nino phenomenon, climate change caused by the accumulation of greenhouse gases in the atmosphere, changing temperature and rainfall patterns. Our interpretation of the point being made by Patz et al. (2000) is that these types of environmental changes will produce shuffles and shifts between species relationships, increasing the likelihood that humans nearby or in the same ecosystems will be affected either directly by becoming a new host for a parasite, or indirectly via domesticated organisms and associated agricultural production activities. An excellent example is that of domesticated plants or animals indirectly conveying a disease-causing organism (Daszak, 2000; Lafferty and 729 Gerber, 2002). Furthermore, these species relationships are compounded by intensification of animal or plant production, by antibiotic treatment, relative immunity, migration into and out of human populations, nutrition, poverty and other determinants (Institute of Medicine, 2003). However, while there are well documented cases of disease emergence associated with deforestation or ecosystem disruption in general, it does not follow that reforestation or habitat restoration generally will necessarily reduce disease emergence, as is amply demonstrated by the case of Lyme disease in the USA. In this disease the character of the secondary forest, particularly its spatial structure and the affect on the reservoir community, plus changes in human settlement patterns have contributed to this emerging zoonosis (LoGiudice et al., 2003). It is likely that the pathogen involved, Borellia burgdorferi was enzootic, if not endemic in the Native American population in the New England region at the time of European contact. This Host– parasite system simply was locally extirpated as a result of the deforestation that ensued (Brownstein et al., 2005). In this case, as with EIDs in general, ecological theory and empirical data suggest destabilisation of Host–parasite systems associated with ecosystem disruption is ephemeral. Assuming disturbance is attenuated, and the ecosystem returns to its original or a new configuration, the conditions effecting disease emergence will no longer exist. However, the time required for reconfiguration may be many human generations in the absence of rational intervention. In the above studies (LoGiudice et al., 2003; Patz et al., 2000), the association of emerging infectious diseases with ecosystem change was framed in terms of the departure of ecosystems from a natural or healthy state in which pathogen outbreaks are regulated as an ecosystem service. This destabilisation model represents a somewhat different perspective consistent with the model of Host–parasite relationships embedded in a system, and a consequence of complex system behaviour. Thus EIDs, as the name aptly suggests, are an emerging property of a complex system. They have been described as a category of emerging properties characteristic of social-ecological systems (a type of complex adaptive system) called ‘surprise’(Gunderson, 2003). The view of ecosystems as not only linked humannatural systems, but complex adaptive systems is a significant departure from the classical view of ecosystems. In this view, the dynamics of ecological systems investigated in terms of ecological succession, represents the single equilibrium view of communities, persisting in the form of the near-equilibrium concept of stability. This is one of several incorrect or partially correct models evidently inconsistent with the accumulating evidence (Holling and Gunderson, 2002). As such, ecosystems are considered far from equilibrium, multiequilibrial, episodically changing systems in which uncertainty, unpredictability, and novelty are not the exception but the rule. The phenomenon of 730 P. Horwitz, B.A. Wilcox / International Journal for Parasitology 35 (2005) 725–732 emerging infectious diseases as part of parasite-systems both helps explain and supports this view of “.[t]he biosphere is a complex adaptive system in which the never ending generation of local variation creates an environment of continual exploration, selection, and replacement.” (Levin, 1999). 5. Sustainability and disease (parasite) management This paper has taken the view that closer attention to ecological–evolutionary and complex systems perspectives can clarify our understanding of Host–parasite relationships, the affects of ecosystem disruptions on them, as well as the reciprocal affect of Host–parasite relationships on ecosystems, and the phenomenon of emerging Host–parasite relationships and infectious diseases. Thus, this has important implications to the management of infectious diseases as critical natural resource and public health issues. This contrasts with the traditional veterinary and medical focus on diagnosis and treatment. For example, the parasite control approach of medicine and public health, focused on chemical control, should produce responses at all scales of the relationship with undesirable consequences: (i) Parasites are placed under intense selection pressure to develop genotypic resistance to antiparasitics, with disease vectors and agricultural pests developing resistance to pesticides for the same reason (Palumbi, 2003). (ii) For the host individual, metabolic, physiological or behavioural side effects of antibiotics are common, evidenced by the regulatory requirements for laboratory and clinical tests to proceed before marketing occurs. There are many examples of prolonged antibiotic therapy being harmful to the host individual (see Steere et al., 2004 for Lyme disease treatment). (iii) For the host population over-exposure to an antibiotic reduces the pressure to develop immunological, genotypic responses over a longer timescale (it has been shown that the presence of a parasite can lead to the production of immunologically enhanced offspring; Moret and Schmid-Hempel, 2001). (iv) At the level of the ecological community habitat nontarget side-effects occur such as loss of components of the system that might otherwise moderate the effects of the parasite and/or its vector, or the development of resistance by non-target organisms which may then become problematic (see Daughton and Ternes, 1999). (v) At the ecosystem level, change to the habitat may expose other environmental hazards, leaving a potential for other ecosystem change by moderating the capacity of the ecosystem to withstand other forms of disturbance. These undesirable consequences need to be placed alongside the obvious desirable consequences of chemical control of parasites. Together they present dilemmas: “Public health officials face an ethical dilemma if the optimal treatment for an individual patient is not optimal for the community. The resurgence of TB, the emergence of drug resistance in malaria, and the heightened virulence of pathogen populations result from intervention that has short term epidemiological benefits but deleterious long term evolutionary repercussions” (Galvani, 2003). A commensurate dilemma exists for the ecologist. When does the ethicist rule in favour of the population/herd or the ecological community? When does the health of the infected individual outweigh the well-being of the population to which it belongs, or the health of the ecological community, or the health of the ecosystem for which humans may also bear significant health as well as economic costs? Should mass vaccinations be applied (when mass vaccinations reduce the risk to non-vaccinates for a period of time but also raise the spectre of applying a strong selective pressure for the parasites to evolve a dispersal mechanism capable of finding the non-vaccinates)? These difficult issues are of course outside the realm of parasitology or ecology. However, they depend on sound technical information from environmental impact assessments or other technical analyses of the social, ecological, and environmental health consequences of ongoing or planned human activities. Accumulated evidence from an examination of activities related to natural resource exploitation, regional development, and infectious disease prevention appear more frequently than not to lead to failed policies, degraded ecosystems, and re-emergence of the undesirable condition (Gunderson and Holling, 2002). Whether parasite or pest populations are targeted for elimination, or other species for commercial exploitation, Gunderson and Holling describe how the resulting human-natural system dynamic has itself become described ‘pathological.’ Following Gunderson and Holling’s general description of system failure, Wilcox and Gubler (2005) describe the ‘pathology of regional infectious disease management’ as a series of responses and counter responses by human and natural systems, resulting in unexpected undesirable outcomes. From the standpoint of a parasite–host relationship, as part of a disease system, the sequence characteristically unfolds as follows. Government public health or environmental health agencies identify natural ‘variables’ for control programmes. For example, programmes that target vector habitat, vector life cycles or life stages are carried out with the goal of reducing or eliminating a ‘pest’ population. Thus uncertainty in nature is presumed replaced by human control, resulting in improved conditions for development and human health. These positive results, along with the jobs and agency infrastructure created to carry out P. Horwitz, B.A. Wilcox / International Journal for Parasitology 35 (2005) 725–732 the control programmes, reinforce the rationale for continued investment in this infrastructure and the focus on ‘control’. Yet, as the target variables are controlled and the agency and its programmes become increasingly stable, efficient and focused—encouraged by their success—slow changes are taking place in other variables. Vector populations begin to adapt to the pesticides or control regime, and the vector’s natural predators, competitors, parasites, or other factors normally regulating their abundance, decline. These ecological changes, characterised by what Holling and colleagues refer to as a loss of resilience (increase in ecosystem vulnerability), occur while institutional inflexibility increases, reducing its capacity to respond adaptively. In managing the effects of each parasite, to avoid this pathology, it seems there is a need for a detailed understanding of the ecological nature of the parasite–host relationship, the establishment of suitable surveillance operations, and the implementation of an adaptive response that recognises the fact that the system will respond to ‘control’ attempts at every scale. This calls for a type of parasite behaviour management that seeks to minimise parasite damage, not over-control it, and a preventative approach that pays closer attention to ecosystem level changes caused by human activities. Examples exist of such sustainable approaches to parasite–host relationships that use an understanding of the system, often referred to as ‘integrated parasite or pest management’. Sheep helminth programmes use a combination of strategic deworming for only heavily infested individuals (as a curative treatment) and at key times, with ensuring adequate nutrition, pasture management, and allowing host immune systems to build up (Besier, 2002; Wells, 1999). The issues discussed in this paper can therefore contribute to a broadening of the principles of integrated pest or parasite management to include: (i) ensuring the strategic application of chemical controls and only in combination with other practices, (ii) reservoir management to minimise re-infection, (iii) habitat management to maximise the effects other biota might have on the parasite, (iv) attention to the ability of the host to resist infection through its own well-being, nutritional status and/or immune system, (v) close attention through monitoring of all cross-scale components of a system to know when and where to implement or modify the approach, and (vi) critical attentiveness to disturbances from human activities that result in ecosystem level changes that produce emergent properties like new parasite–host relationships and emerging infectious diseases. Many of these principles are recognised in the literature. Together, and probably only together, they adopt an 731 approach to managing Host–parasite relationships sustainably where complexity is taken into account, and the coevolution and self-organisation of systems is acknowledged. Acknowledgements This review was prepared as an invited presentation for an Ecosystem Health Symposium at the Australian Society for Parasitology’s Conference held at Fremantle in September 2004, convened by Dr Alan Lymbery. Drs Shannon Bennett, Robert Doupe, David Spratt, David Marcogliese and David Forshaw provided useful comments on an earlier version of the manuscript. Assistance in the preparation of the manuscript was gratefully received from Kristin Duin and Caroline Barton. References Allen, T.F.R., Starr, T.B., 1982. Hierarchy: Perspectives for Ecological Complexity. University of Chicago Press, Chicago. Anderson, R.M., May, R.M., 1979. Population biology of infectious diseases: part I. Nature 280, 361–367. Anderson, R.M., May, R.M., 1991. 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