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International Journal for Parasitology 35 (2005) 725–732
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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
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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.
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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
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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
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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. Infectious Diseases of Humans.
Dynamics and Control. Oxford University Press, Oxford.
Besier, R.D., 2002. New approaches to sheep parasite control. The potential
for individual sheep management. Anim. Prod. Aust. 25, 13–16.
Birkes, F., Colding, J., Folke, C. (Eds.), 2003. Navigating Social-Ecological
Systems: Building Resilience for Complexity and Change. Cambridge
University Press, Cambridge, UK.
Brown, M.J.F., Schmid-Hempel, R., Schmid-Hempel, P., 2003. Strong
context-dependent virulence in a Host–parasite system: reconciling
genetic evidence with theory. J. Anim. Ecol. 72, 994–1002.
Brownstein, J.S., Holford, T.R., Fish, D., 2005. Impact of climate change on
Lyme disease risk in North America. EcoHealth 2, 38–46.
Damborenea, M.C., Cannon, L.R.G., 2001. On neotropical Temnocephala
(Platyhelminthes). J. Nat. Hist. 35, 1103–1118.
Daszak, P., 2000. EID: bridging the gap between humans and wildlife. The
Scientist 14, 14.
Daughton, C.G., Ternes, T.A., 1999. Pharmaceuticals and personal care
products in the environment: agents of subtle change?. Env. Health
Persp. 107, 907–938.
Dobson, A., 2003. Metalife!. Science 301, 1488–1490.
Ewald, P.E., 1983. Host–parasite relations, vectors, and the evolution of
disease severity. Ann. Rev. Ecol. Syst. 14, 465–485.
Flatt, T., Scheuring, I., 2004. Stabilizing factors interact in promoting host–
parasite coexistence. J. Theor. Biol. 228, 241–249.
Galvani, A.P., 2003. Epidemiology meets evolutionary ecology. Tr. Ecol.
Evol. 18, 132–139.
Gunderson, L.H., 2003. Adaptive dancing: interactions between social
resilience and ecological crises. In: Birkes, F., Colding, J., Folke, C. (Eds.),
Navigating Social-Ecological Systems: Building Resilience for Complexity and Change. Cambridge University Press, Cambridge, UK, pp. 33–52.
Gunderson, L.H., Holling, C.S. (Eds.), 2002. Panarchy. Understanding
Transformations in Human and Natural Systems. Island Press,
Washington.
Gunther, F., Folke, C., 1992. Characteristics of nested living systems.
J. Biol. Syst. 1, 257–274.
Holling, C.S., 1986. The resilience of terrestrial ecosystems: local
surprise and global change. In: Clark, W.C., Munn, R.E. (Eds.),
Sustainable Development for the Biosphere. Cambridge University Press,
Cambridge, UK.
732
P. Horwitz, B.A. Wilcox / International Journal for Parasitology 35 (2005) 725–732
Holling, C.S., Gunderson, L.H., 2002. Resilience and adaptive cycles. In:
Gunderson, L.H., Holling, C.S. (Eds.), Panarchy. Understanding
Transformations in Human and Natural Systems. Island Press,
Washington, pp. 25–62.
Holt, R.D., Dobson, A.P., Begon, M., Bowers, R.G., Schauber, E.M., 2003.
Parasite establishment in host communities. Ecol. Lett. 6, 837–842.
Howe, H.F., Smallwood, J., 1982. Ecology of seed dispersal. Ann. Rev.
Ecol. Syst. 13, 201–228.
Hubalek, Z., 2003. Emerging human infectious diseases: anthroponoses,
zoonoses and sapronoses. Emerg. Infect. Dis. 9, 403–404.
Institute of Medicine, 2003. In: Smolinski, Mark S., Hamburg, Margaret A.,
Joshua Lederberg (Eds.), Microbial Threats to Health: Emergence,
Detection, and Response. National Academy Press, Washington.
Janssen, M.A., 2005. Adaptive capacity of social–ecological systems:
lessons from immune systems. EcoHealth 2 (2).
Lafferty, K.D., Gerber, L.R., 2002. Good medicine for conservation
biology: the intersection of epidemiology and conservation theory.
Cons. Biol. 16, 593–604.
Lafferty, K.D., Kuris, A.M., 1999. How environmental stress affects the
impacts of parasites. Limnol. Ocean. 44, 564–590.
Levin, S.A., 1999. Fragile Dominion: Complexity and the Commons.
Perseus Publishing, Cambridge, MA.
LoGiudice, K., Ostfeld, R.S., Schmidt, K.A., Keesing, F., 2003. From the
cover: the ecology of infectious disease: effects of host diversity and
community composition on lyme disease risk. Proc. Natl Acad. Sci.
100, 567–571.
Lyles, A.M., Dobson, A.P., 1993. Infectious disease and intensive
management: population dynamics, threatened hosts and their parasites.
J. Zoo Wildl. Med. 24, 315–326.
Mackenzie, J.S., Lindsay, M.D., Coelen, R.J., Hall, R.A., Broom, A.K.,
Smith, D.W., 1994. Arboviruses causing human disease in the
Australian zoogeographic region. Arch. Virol. 136, 447–467.
Marcogliese, D.J., 2005. Parasites of the superorganism: are they indicators
of ecosystem health?. Int. J. Parasitol. 2005; (This issue).
Moret, Y., Schmid-Hempel, P., 2001. Immune defence in bumble-bee
offspring. Nature 414, 506.
Palumbi, S.R., 2003. Arms races and antimicrobial resistance: using
evolutionary science to slow evolution. In: Knobler, S.I., Lemon, S.M.,
Marjan Najafi (Eds.), The Resistance Phenomenon in Microbes and
Infectious Disease Vectors: Implications for Human Health and
Strategies for Containment, Workshop Summary. Institute of Medicine
of the National Academy. National Academy Press, Washington, D.C,
pp. 21–32.
Patz, J., Graczyk, T.K., Geller, N., Yitter, A.Y., 2000. Effects of
environmental change on emerging parasitic diseases. Int. J. Parasitol.
30, 1395–1405.
Patz, J., Daszak, P., Tabor, G.M., Aguirre, A.A., Pearl, M., Epstein, J.,
Wolfe, N., Kilpatrick, A.M., Foufopoulos, J., Molyneux, D.,
Bradley, D., Members of the Working Group on Land Use Change
and Disease Emergence, 2004. Unhealthy landscapes: policy recommendations on land use change and infectious disease emergence.
Env. Health Persp. 112, 1092–1097.
Prenter, J., MacNeil, C., Dick, J.T.A., Dunn, A.M., 2004. Roles of parasites
in animal invasions. Tr. Ecol. Evol. 19, 385–390.
Rees, W., 1998. How should a parasite value its host?. Ecol. Econ. 25,
49–52.
Smyth, J.D., 1994. Introduction to Animal Parasitology, Third ed
Cambridge University Press, Cambridge, UK.
Steere, A.C., Coburn, J., Glickstein, L., 2004. The emergence of lyme
disease. J. Clin. Invest. 113, 1093–1101.
Summers, K., McKeon, S., Sellars, J., Keusenkothen, M., Morris, J.,
Gloeckner, D., Pressley, C., Price, B., Snow, H., 2003.
Parasitic exploitation as an engine of diversity. Biol. Rev. 78, 639–675.
Thomas, F., Poulin, R., Guegan, J.-F., Michalakis, Y., Renaud, F., 2000.
Are there pros as well as cons to being parasitised?. Parasitol. Today 16,
533–536.
Wells, A., 1999. Integrated Parasite Management for Livestock. Appropriate Technology Transfer for Rural Areas. University of Arkansas,
Fayetteville, USA p. 9.
Wilcox, B.A., Gubler, D.J., 2005. Disease ecology and the global
emergence of zoonotic pathogens Env. Health Prev. Med. 10.
Yuill, T.M., 1986. The ecology of tropical arthropod-borne viruses. Ann.
Rev. Ecol. Syst. 17, 189–219.