Disease invasion: Impacts on biodiversity and human health

Article (PDF Available)inPhilosophical Transactions of The Royal Society B Biological Sciences 367(1604):2804-6 · October 2012with55 Reads
DOI: 10.1098/rstb.2012.0331 · Source: PubMed
Abstract
An introduction to the theme issue that includes papers that identify how, where and why infectious diseases in wildlife emerge, while also addressing their possible conservation impacts.
Introduction
Disease invasion: impacts on biodiversity
and human health
Andrew A. Cunningham
1,
*
, Andrew P. Dobson
2
and Peter J. Hudson
3
1
Institute of Zoology, Zoological Society of London, Regent’s Park, London NW1 4RY, UK
2
Department of Ecology and Evolutionary Biology, Princeton University, 117 Eno Hall,
Princeton, NJ 08544, USA
3
Department of Biology, Huck Institutes of the Life Sciences, The Pennsylvania State University,
201 Life Sciences Building, University Park, PA 16802, USA
An introduction to the theme issue that includes papers that identify how, where and why infectious
diseases in wildlife emerge, while also addressing their possible conservation impacts.
Keywords: disease invasion; disease emergence; emerging infectious disease; spillover;
hostpathogen dynamics
The emergence of previously unknown infectious dis-
eases has been high on the medical and political
agendas in recent years, as evidenced by the global
responses to severe acute respiratory syndrome, bird
flu and swine flu, and the revision of the International
Health Regulations [1,2]. A number of studies cover-
ing a wide range of taxa [35], including plants [6],
have shown that such disease emergence is primarily
due to host shifts of pre-existing disease agents, usually
driven by anthropogenic factors, such as globalized
trade and increased human wildlife contact rates.
Wild animals are the primary reservoir of new infec-
tions that spill over and infect human beings directly
or via domestic or peri-domestic species, threatening
the health of people or their livestock, but it should
not be forgotten that wildlife are also the recipients
of diseases from other species, including human
beings. While infectious disease emergence has
mainly been seen as a public health threat or as a
direct threat to human resources and economies as a
consequence of epidemics of crops and livestock, the
transmission of infectious diseases from one species
to another also threatens wildlife [7], including the
survival of large and apparently robust wildlife popu-
lations [8]. This theme issue of the Philosophical
Transactions of the Royal Society follows a conference
held at the Zoological Society of London that focused
on the extent to which wildlife pathogens threaten bio-
diversity and human health, the processes driving
these disease threats, where future threats will arise,
and how these might be mitigated.
Most emerging disease threats are caused by patho-
gens that capitalize upon the opportunities of exposure
to transmit between species [3,4,6]. In most cases, one
(or more) host species act as a reservoir for a pathogen
that jumps species, with or without adaptation to the
novel host [5], to infect a novel species that is at a
twin disadvantage in being both susceptible and
naive, and so there is an opportunity for spread
throughout the population. These conditions set the
stage for either a disease outbreak that dies out after
causing a significant epidemic, or for the pathogen
becoming endemic and establishing in the new host
population, usually reducing it to a lower abundance
[9]. Thus, even if the population of the new host
falls below the level required for maintenance of infec-
tion, repeated spillover from the original host ensures
continued pathogen exposure. Several papers in this
issue explore our current understanding of the
dynamics of such diseases, the processes of circulation
in wild reservoirs, and the rare, enigmatic and critical
process of spillover that leads to infection, and
sometimes establishment, in new host species. This
spillover process is both poorly understood and
under-studied, partly because spillover events are
rarely captured and partly because current analytical
tools are inadequate to encapsulate the high degree
of complexity involved in such systems [5].
There has been a recent increase in the studies of
hostpathogen dynamics within reservoir hosts. This,
along with the dynamics of pathogen spillover into
new host species, is a key area for future studies. Ironi-
cally, the dynamics of the within-host interaction
between the immune system and the apparently grow-
ing population of pathogens is more likely to readily
match the underlying assumptions of many simple
predator prey systems, than are the actual dynamics
of vertebrate predators and their prey, or even insect
parasitoids and their hosts. There have been some
recent highlights in this area [10], and it is an increas-
ingly vibrant area of research that we expect to see
* Author for correspondence (a.cunningham@ioz.ac.uk).
One contribution of 10 to a Theme Issue ‘Disease invasion: impacts
on biodiversity and human health’.
Phil. Trans. R. Soc. B (2012) 367, 2804–2806
doi:10.1098/rstb.2012.0331
2804 This journal is q 2012 The Royal Society
expand, almost to the level of a sub-discipline, in the
next decade. A key step here will be the development
of a better understanding of the way that the
immune system functions in different host classes. At
present, we study the nuances of human immunity
with fervour and detail, yet we have a very thin under-
standing of how, for example, bat immunity differs
from mouse immunity; worse we tend to assume that
migrating waterfowl that act as major reservoirs for
influenza have analogous immune systems to chickens.
Our knowledge of the immune systems of reptiles and
amphibians is woefully vague, and this is particularly
worrying given the global extinction of amphibians
associated with the infectious fungal disease, chytridio-
mycosis [11]. Increases in the power of computers,
coupled with increased availability of data, will make
the development of within-host models a viable exer-
cise, although the area is also ripe for insights
derived from simple empirical studies and analytical
models of the dynamics of a pathogen and the different
major components of immunity. Some may complain
that the devil is in the fine detail of immunologi-
cal function, but, as with any complex emerging
system, the detail of the immune system is likely
to be organized in a way that is both hierarchical
and containing subtly nested redundancies that
interact to determine host susceptibility and infec-
tion outcomes, including pathogen transmission.
There will certainly be more similarities between the
network structure of food webs, nervous systems and
immune systems than is currently perceived by most
of those working in each of these fields, or by the
funding agencies.
This theme issue not only includes papers that
identify how, where and why infectious diseases in
wildlife emerge, but also addresses their possible con-
servation impacts. Several papers present new ways of
addressing disease emergence through modelling
insights gained from empirical studies. These include
new approaches to evaluating the biological and
anthropogenic mechanisms that facilitate the spillover
and spread of infection into new species (including
humans) and geographical regions, and the selection
pressures that can then lead to new endemic infections
evolving [12,13]. Understanding the mechanisms
involved in disease invasion is fundamental to under-
standing how emerging diseases can be best
prevented and controlled [7,8]. This includes a need
for natural scientists to work more closely with social
scientists in order to improve our understanding of
the drivers of disease emergence and spread [14].
Human activities are, after all, usually at the root of
the problem, and their underlying causes need to be
understood if behaviours are to be modified effectively
to produce a sustainable solution. Aspects of emerging
disease mitigation also are addressed in this issue,
including the control of infections within their reser-
voir hosts and within the target species [2,15], as is a
range of issues, from understanding molecular pro-
cesses to the management of ecosystems, in order to
identify and predict future threats [16,17]. Finally,
policies for mitigating disease threats to conservation
and human health are examined and science-based
recommendations made.
It is always instructive to consider what is missed
from a theme issue such as this, and to briefly scan
likely future areas of development. We each felt it
would have been deeply insightful to include more
papers about plants and plant pathogens. The current
epidemic of white pine blister rust in Canada and the
northwestern United States illustrates that plant
pathogens can have equally marked impacts on the
structure of relatively pristine ecological communities,
comparable to the rinderpest outbreak in nineteenth
century sub-Saharan Africa, or the myxomatosis epi-
demic in rabbits in Australia and Europe [18].
Similarly, it would have been insightful to have
included papers that examine the role of pathogen
and host genetic diversity, although these will be cov-
ered in a forthcoming symposium that will be
published as a theme issue of Philosophical Transactions
of the Royal Society, B: Biological Sciences.
Overall, the meeting held at the Zoological Society
of London and the papers that follow in this theme
issue illustrate the energy and vibrancy of the field, lab-
oratory and theoretical studies that are rapidly
expanding our understanding of the dynamics of dis-
ease invasion and of infectious disease dynamics in
their natural hosts. As McCallum remarked on the
opening day of the symposium, the pioneering studies
of Anderson & May [19] have themselves ignited an
epidemic of studies that is far removed from the stut-
tering chains of intellectual infection that often
characterize the emergence of new ideas and synthesis
in other domains of scientific endeavour.
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2806 A. A. Cunningham et al. Introduction. Disease invasion
Phil. Trans. R. Soc. B (2012)
    • "Th e application of the EMS framework and determination of variables associated with metacommunity structure is new to host – parasite systems and is particularly important for understanding relationships between hosts, which may be reservoirs for emerging diseases, and their parasites, which may be vectors that transmit disease to humans or agriculturally important domestic animals (Daszak et al. 2000, Cunningham et al. 2012). Only host traits associated with the environment were signifi cantly associated with variation in species composition, indicating that responses to the same type of environmental variation can be associated with multiple types of metacommunity structure. "
    [Show abstract] [Hide abstract] ABSTRACT: Identification of mechanisms that shape parasite community and metacommunity structures have important implications to host health, disease transmission, and the understanding of community assembly in general. Using a long-term dataset on parasites from desert rodents, we examined the relative contributions of host traits that represent important aspects of parasite environment, transmission probability between host species, and host phylogeny to the structure of a parasite metacommunity as well as for taxonomically restricted parasite metacommunities (coccidians, ectoparasites and helminths). This was done using a combination of metacommunity analysis and variance partitioning based on canonical correspondence analysis. Coccidian and ectoparasite metacommunities did not exhibit coherent structure. In contrast, helminths and the full parasite metacommunity had Clementsian and quasi-Clementsian structure, respectively, indicating that parasite species distributions for these metacommunities were compartmentalized along a dominant gradient. Variance decomposition indicated that characteristics associated with the host environment consistently explained more variation than did host traits associated with transmission opportunities or host phylogeny, indicating that the host environment is primary in shaping parasite species distributions among host species. Moreover, the importance of different types of host traits in structuring parasite metacommunities was consistent among taxonomic groups (i.e. full metacommunity, coccidians, and helminths) despite manifest differences in emergent structures (i.e. Clementsian, quasi-Clementsian, and random) that arose in response to variation in host environment.
    Full-text · Article · Feb 2014
    • "Understanding host–pathogen dynamics has become an urgent priority as emerging infectious diseases increase in abundance and impact and contribute to losses of biodiversity (Harvell et al. 1999; Daszak, Cunningham & Hyatt 2000; Keesing et al. 2010; Cunningham, Dobson & Hudson 2012; Fisher et al. 2012; McCallum 2012 ). For example , global amphibian population declines have been linked to the emerging infectious fungus Batrachochytrium dendrobatidis (Bd) (Stuart et al. 2004; Skerratt et al. 2007; Fisher, Garner & Walker 2009; Olson et al. 2013). "
    [Show abstract] [Hide abstract] ABSTRACT: Many pathogens infect a wide range of host species. However, variation in the outcome of infection often exists amongst hosts and is shaped by intrinsic host traits. For example, contact with pathogens may trigger changes in hosts directed toward preventing, fighting, or tolerating infection. Host responses to infection are dynamic; they change over time and vary depending on health, condition and within the context of the environment.Immunological defences are an important class of responses that mediate host–pathogen dynamics. Here, we examined temporal patterns of immunity in two amphibian species, Pacific tree frogs (Pseudacris regilla) and Cascades frogs (Rana cascadae), exposed to control conditions or experimental inoculation with the emerging infectious fungal pathogen, Batrachochytrium dendrobatidis (Bd). For each species, we compared bacterial killing ability of blood and differential white blood cell counts at four different time-points after pathogen inoculation. We also quantified infection load over time and monitored survival.We detected qualitative and quantitative differences in species responses to Bd. Pseudacris regilla exhibited an increase in infection load over time and 16% of Bd-exposed animals died during the experiment. Tree frogs lacked robust treatment differences in immune responses, but Bd-exposed P. regilla tended to display weaker bacterial killing responses than unexposed control animals. Neutrophil counts did not vary consistently with treatment and lymphocytes tended to be less abundant in Bd-exposed animals at the later sampling time-points.In contrast, Bd-exposed R. cascadae exhibited a decrease in infection load over time and no mortality occurred in the Bd treatment. Bd-exposed Cascades frogs showed stronger bacterial killing responses and an elevated number of neutrophils in blood when compared with control animals, and both responses were upregulated within 48 h of pathogen exposure. Lymphocyte counts did not vary significantly with treatment.Although only statistically significant in Cascades frogs, neutrophil:lymphocyte ratios showed a trend of being elevated in Bd-exposed animals of both species and are indicative of pathogen-induced physiological stress.Our results suggest that variation in systemic immunological responses of two syntopic amphibian species is associated with and may contribute to differential patterns of survival and infection load during exposure to the chytrid fungus. Species variation in immunological responses as soon as 48 h after pathogen exposure suggests that initial host–pathogen interactions may set the stage for subsequent infection and disease progression. Variation in host responses can drive disease dynamics and comparative studies of host responses to pathogens are critical for making predictions about pathogen emergence, spread and persistence.
    Full-text · Article · Nov 2013
    • "For species life-history traits, we used body mass, incubation time (gestation time for mammals), and clutch size (litter size for mammals). Incubation time and clutch size have been linked to the species' immune response [9], while body mass can serve as a surrogate for size-scaled life-history traits such as fecundity, metabolic requirements [14] and age at first breeding [15]. In addition, a species' potential to serve as a reservoir or transmit pathogens may have a phylogenetic signal. "
    [Show abstract] [Hide abstract] ABSTRACT: Hosts species for multi-host pathogens show considerable variation in the species' reservoir competence, which is usually used to measure species' potential to maintain and transmit these pathogens. Although accumulating research has proposed a trade-off between life-history strategies and immune defences, only a few studies extended this to host species' reservoir competence. Using a phylogenetic comparative approach, we studied the relationships between some species' life-history traits and reservoir competence in three emerging infectious vector-borne disease systems, namely Lyme disease, West Nile Encephalitis (WNE) and Eastern Equine Encephalitis (EEE). The results showed that interspecific variation in reservoir competence could be partly explained by the species' life histories. Species with larger body mass (for hosts of Lyme disease and WNE) or smaller clutch size (for hosts of EEE) had a higher reservoir competence. Given that both larger body mass and smaller clutch size were linked to higher extinction risk of local populations, our study suggests that with decreasing biodiversity, species with a higher reservoir competence are more likely to remain in the community, and thereby increase the risk of transmitting these pathogens, which might be a possible mechanism underlying the dilution effect.
    Full-text · Article · Sep 2013
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