| |

Received: 9 January 2018    Revised: 8 May 2018    Accepted: 27 May 2018

DOI: 10.1111/zph.12489

REVIEW

Ecosystem change and zoonoses in the Anthropocene

Barry J. McMahon1  | Serge Morand2 | Jeremy S. Gray3

1
UCD School of Agriculture & Food
Science, University College Dublin, Dublin Abstract
4, Ireland Changes in land use, animal populations and climate, primarily due to increasing
2
CNRS – CIRAD ASTRE, Faculty of
human populations, drive the emergence of zoonoses. Force of infection (FOI), which
Veterinary Technology, Kasetsart University,
Bangkok, Thailand for these diseases is a measure of the ease with which a pathogen reaches the human
3
UCD School of Biology & Environmental population, can change with specific zoonoses and context. Here, we outline three
Science, University College Dublin, Dublin
ecosystem categories—domestic, peridomestic and sylvatic, where disease ecology
4, Ireland
alters the FOI of specific zoonoses. Human intervention is an overriding effect in the
Correspondence
emergence of zoonoses; therefore, we need to understand the disease ecology and
Barry J. McMahon, UCD School of
Agriculture & Food Science, University other influencing factors of pathogens and parasites that are likely to interact differ‐
College Dublin, Belfield, Dublin 4, Ireland.
ently within ecological and cultural contexts. Planning for One Health and commu‐
Email: barry.mcmahon@ucd.ie
nity ecology, such as an ecological impact assessment, is required to prepare and
Funding information
manage the emergence and impact of zoonoses in the Anthropocene.
European Cooperation in Science and
Technology, Grant/Award Number: TD1404;
ANR FutureHealthSEA, Grant/Award KEYWORDS
Number: ANR-17-CE35-0003-01 biodiversity, infectious disease, landscape, one Health

1 |  I NTRO D U C TI O N
Zoonotic diseases, those transmitted from nonhuman animals to
humans, are increasingly important in global public health (Jones
et al., 2008). Almost 60% of human pathogens and approximately
60% emerging infectious diseases are classified as zoonotic (Jones et
al., 2008; Woolhouse & Gowtage‐Sequeria, 2005). Although many
human diseases have zoonotic origins (e.g., avian influenza, HIV
AIDS, SARS and Ebola), we focus our attention here on those that
are not normally transmissible between humans or for only a short
period following the index case. The majority of recently emerged
zoonotic diseases originated in wildlife species (Jones et al., 2008).
With an ever‐increasing global human population (Gerland et al.,
2014) comes an associated spatial expansion of human activity (e.g.,
agriculture, urbanization and land‐use change). The result is that
the interface between humans, domesticated animals and wildlife
is likely to intensify during the Anthropocene (Jones et al., 2013),
while wildlife is undergoing a massive defaunation (Ceballos, Ehrlich,
& Dirzo, 2017). The terrestrial planet is increasingly a cultural rather
than a natural landscape because of the anthropogenic environ‐
mental footprint, thus requiring management of limited resources
(Hoekstra & Wiedmann, 2014). There are clear trade‐offs with the
management of land‐use changes including the regulation of infec‐
tious diseases (Foley et al., 2005; Karesh et al., 2012).
1.1 | Force of infection
Force of infection (FOI) is defined as the rate at which susceptible
individuals become infected per unit time and is used to compare
different diseases or transmission in different risk groups. It may
be expressed in its simplest form as follows (modified from Davis,
Calvet, & Leirs, 2005)
λ = cpv
where λ, force of infection; c, the number of transmission contacts
over a particular time period; p, the level of environmental contamina‐
tion or prevalence of infection in the reservoir host or vector popula‐
tion; and v, the probability that transmission occurs on contact.
For zoonoses, we propose the FOI is a measure of the ease
with which an infection reaches the human population from an an‐
imal origin, and can be changed by variation in several factors, the

Zoonoses Public Health. 2018;65:755–765. © 2018 Blackwell Verlag GmbH |  755

wileyonlinelibrary.com/journal/zph  
 |
756       McMAHON et al.

interrelationships of which are illustrated in Figure 1. The effective‐

ness of intervention strategies (prevention and control) influences
Impacts
FOI. Thus, preintervention, the FOI for a given disease, can be re‐
ferred to as “intrinsic FOI” and postintervention as “actual FOI,” • Zoonosis emergence can be a consequence of land‐use
the difference between the two being a measure of intervention change and other forms of human intervention.
effectiveness. In practice, accurate estimation of FOI for a disease • The nature of force of infection must be appreciated to
is very difficult because of the large number of variables. For exam‐ understand zoonosis emergence within different
ple, to determine the dynamics of force of infection in Echinococcus ecosystems.
multilocularis in red foxes, a mathematical modelling approach was • We focus on ecosystem classification to categorize
required, which showed that FOI was periodic with variable ampli‐ emergence of zoonoses in order to aid the understand‐
tude, differing markedly with season and between urban and peri‐ ing and role of force of infection with reference to fu‐
urban habitats, suggesting that optimal control strategies must be ture research, public health policy and landscape
tailored to local situations (Lewis, Otero‐Abad, Hegglin, Deplazes, & planning.
Torgerson, 2014).

F I G U R E 1   Interrelationships of factors that contribute to “Force of Infection” leading to zoonotic disease (P&C = prevention and control).
In this simplified scheme, the arrows indicate effects of one factor on another—in relation to the probability of a zoonotic organism causing
disease in the human population. For example, land development and/or ecological perturbation can influence the environmental availability
of zoonotic agents, directly or via other organisms (i.e., intermediate hosts, reservoir hosts and vectors), thus contributing to the likelihood
of infection occurring (force of infection) and so to the occurrence of disease, subject to the susceptibility of the human population. The
broken lines indicate that in a limited number of cases, the zoonotic agent is affected by a predator–prey relationship between reservoir and
intermediate host, for example, foxes and rodents in the case of Echinococcus multilocularis
McMAHON et al.
1.2 | Drivers of zoonotic disease emergence and
transmission
The emergence of zoonoses has been linked to a range of factors
including environmental, ecological and geographical variables
(Jones et al., 2008; Plowright et al., 2017). The transmission dynam‐
ics of many zoonotic pathogens are complicated due to the ecology
of animal reservoirs and their vectors, depending on the zoonosis
involved. The factors affecting the emergence and transmission of
zoonoses can be broadly categorized as follows.
1.2.1 | Human intervention
Humans influence, at some level, the emergence and/or trans‐
mission of practically all zoonoses, but in this section, we present
some specific examples of human activity as the primary driver.
Deforestation is a common source of zoonotic disease emergence,
resulting mainly from increased proximity of wild animals to the
human population. Important pathogens to have emerged in this
way over the last few decades include the highly pathogenic Ebola
virus and human immunodeficiency virus (HIV). In both cases, the
genetic relatedness of wild primates (great apes) to humans is prob‐
ably relevant. For Ebola, the primates are not the original source of
the virus, but may function as secondary or bridging hosts to humans
(Del Rio & Guarner, 2015). HIV on the other hand is derived from
a simian form of the virus which adapted to its human host (Sharp
& Hahn, 2011). In both cases, once the virus reached the human
population, transmission could occur from human to human and in
the case of HIV eventually caused the current AIDS pandemic. More
recent examples of deforestation resulting in new zoonotic diseases,
again involving nonhuman primates, include the monkey malarias,
caused by Plasmodium knowlesi and P. cynomolgi in South‐East Asia,
and P. simium in South America (Fornace et al., 2016). It is very likely
that other simian Plasmodium species can cause disease in humans,
that human Plasmodium species can infect monkeys and that such
reciprocal infections will increase in frequency with increasing de‐
forestation (Ramasamy, 2014).
Other examples include conversion of land to agriculture or
intensification of agricultural practices resulting in an increase in
the transmission of zoonotic diseases, exemplified by the diseases
caused by West Nile virus and Nipah virus among others (Epstein,
Field, Luby, Pulliam, & Daszak, 2006; Kilpatrick, 2011). On the con‐
trary, the reversion of agricultural land to tick‐permissive woodland
appears to be behind the emergence of the tick‐borne disease Lyme
borreliosis on the eastern seaboard of the United States (Matuschka
& Spielman, 1986). In the same way, an increase in tick‐borne en‐
cephalitis in eastern Europe can be partially attributed to firstly the
creation of suitable tick habitat by the abandonment of farmland in
the economic upheavals following the collapse of the Soviet Union
(Šumilo et al., 2008) and secondly increased use of forest by the
human population for the harvesting of mushrooms and wild fruit
(Randolph et al., 2008). Other more dramatic alterations to the land‐
scape that may influence the emergence of zoonoses are man‐made
|
      757
dams and irrigation projects. For example in certain parts of Africa,
the risk of schistosomiasis is increased where such structures im‐
prove the habitat for the snail intermediate host of the parasite
(Steinmann, Keiser, Bos, Tanner, & Utzinger, 2006).
On a larger scale, economic globalization was implicated as
a driver in the risk of scrub typhus in Taiwan (Kuo et al., 2012).
The rickettsial organism that causes scrub typhus, Orientia tsut-
sugamushi, utilizes trombiculid mites as vectors and certain rodent
species as reservoir hosts. Both mites and rodents are strongly asso‐
ciated with heterogenous forest and overgrown fallow land (Chaisiri,
Cosson, & Morand, 2017; Xu, Walker, Jupiter, Melby, & Arcari, 2017).
When Taiwan joined the World Trade Organization in 2001, local
rice production became economically uncompetitive because of the
removal of trade barriers and agricultural subsidies, and this had
profound effects on the agricultural landscape. The percentage of
uncultivated paddy fields increased from 20% before 2001 to nearly
45% by the end of 2004 (to finally stabilize at 40% in 2012), creating
ideal conditions for both the reservoir hosts and vectors of the scrub
typhus zoonotic agent. Not only did the rodent population expand,
particularly that of the striped field mouse, Apodemus agraruis, but
the intensity of mite infestation of mice from uncultivated fields in‐
creased threefold (Kuo et al., 2012). The incidence of scrub typhus
increased nearly 40%, comparing the two periods 1998–2001 and
2003–2007, and it is tempting to ascribe this to the changed envi‐
ronmental conditions stemming from globalization.
More subtle effects resulting from human intervention include
the rise in rabies incidence in India attributed to the widespread use
of the anti‐inflammatory pharmaceutical diclofenac in cattle. This
proved toxic to vultures causing a rapid decline in the vulture pop‐
ulation, resulting in an accumulation of cattle carcases in the land‐
scape. This in turn boosted the populations of stray dogs, the main
source of the rabies virus (Markandya et al., 2008). A more targeted
intervention, also with unintended consequences, was the dissem‐
ination of an antirabies vaccine for foxes in Europe, resulting in an
expansion of the red fox (Vulpes vulpes) population and a consequent
increase in the transmission of Echinococcus multilocularis, the cause
of alveolar hydatid disease. This topic is addressed in more detail as
a case study below.
1.2.2 | Changes in animal populations
As described above for schistosomiasis, scrub typhus, rabies and al‐
veolar hydatid disease, human influence can change animal numbers
(snails, mites, stray dogs and red foxes, respectively) and thus affect
the extent and timing of zoonotic disease emergence. Nonhuman
factors can also bring about changes in animal numbers and thus
have significant effects on the dynamics of zoonotic infections. This
is known to be the case for perhaps the most notorious zoonotic
disease in human history, bubonic plague, caused by the bacterium
Yersina pestis, which is acknowledged as the causal agent of the
“Black Death,” which killed as much as a third of the population of
Europe in the Middle Ages. The infection probably originated in cen‐
tral Asia where it is still maintained by burrowing rodents, mainly
 |
758       McMAHON et al.
species of gerbils, and is transmitted by fleas (Gage & Kosoy, 2005).
Periodically, these rodents become hyperabundant, resulting even‐
tually in a Y. pestis epizootic and die‐off. The high mortality of the
rodents deprives infected fleas of their natural hosts, so that they
then seek other hosts, including humans, thus giving rise to plague
epidemics (Samia et al., 2011). It is probable that climate factors are
involved in the generation of such epizootics, by driving up both ro‐
dent and flea numbers (Stenseth et al, 2006), but once the infection
spills over into other ecosystems, the epidemiology becomes more
complex. The three pandemics that have been recorded (the Black
Death occurring at the start of the second), probably all had their
origin in climate‐driven rodent population dynamics in central Asia,
and the apparent persistence of cases in areas where such rodents
are absent, may in fact be due to repeated waves of infection from
the central Asian source spilling over into other rodent populations,
such as that of the Black rat, Rattus rattus (Schmid et al., 2015).
Hantavirus and related pathogens also utilize rodents as reser‐
voir hosts, and there is strong evidence that major drivers of out‐
breaks caused by these viruses can be climatic factors causing peaks
in rodent numbers, particularly in rural areas (Jonsson, Figueiredo, &
Vapalahti, 2010). For example, Schwarz, Ranft, Piechotowski, Childs,
and Brockmann (2009) found that case rates of Puumala virus infec‐
tion in Germany were significantly associated with mast years which
boost rodent numbers in China, an abundance of field mice resulting
from low rainfall and lack of flooding preceded a higher incidence
of HFRS (haemorrhagic fever with renal syndrome) in China (Guan
et al., 2009), and in America, the emergence of hantavirus has been
linked to precipitation that indirectly stimulates rodent population
growth (Engelthaler et al., 1999; Yates et al., 2002).
In contrast to disease emergence caused by animal numbers that
have increased, there is at least one case where a decrease may have
contributed to higher disease rates. The incidence of tick‐borne en‐
cephalitis (TBE) in Sweden has risen over recent decades apparently
linked to a decrease in roe deer (Capreolus capreolus) populations, an
important host for all stages of the vector tick, Ixodes ricinus. This is
thought to have diverted host‐seeking ticks to bank voles (Myodes
glareolus), animal reservoirs of TBE, which coincidentally peaked in
numbers at the same time, resulting in increased transmission to hu‐
mans (Jaenson, Hjertqvist, Bergström, & Lundkvist, 2012).
1.2.3 | Changes in climate and weather
Empirical observations confirm that ongoing climate change is driv‐
ing certain diseases to higher latitudes or altitudes (Altizer, Ostfeld,
Johnson, Kutz, & Harvell, 2013). However, most of the knowledge
on the effects of climate change regarding the distribution and epi‐
demiology of infectious diseases comes from modelling approaches,
such as ecological niche modelling or climate simulation‐based risk
modelling (Guis et al., 2012). McIntyre et al. (2017) recently investi‐
gated the climate sensitivity of infectious pathogens and found that
two‐thirds of them were climate‐sensitive (rainfall and tempera‐
ture). Enterovirus infection and shigellosis were associated with wet
summer climate and abnormally heavy rainfalls, whereas typhoid
fever was associated with periods of high temperature in Europe
(McIntyre et al., 2017; Morand, Owers, Waret‐Szkuta, McIntyre, &
Baylis, 2013). Similar patterns have been observed for these diseases
in tropical regions (Wilson, Lush, & Baker, 2010); importantly, their
study also revealed that zoonotic pathogens are more climate‐sen‐
sitive than human‐ or animal‐only pathogens. Climate and weather
changes have consequences in relation to habitat management, es‐
pecially concerning food and water resources and movement and/
or migration of animals, including those belonging to climate refu‐
gees (Gortazar et al., 2014; Pongsiri et al., 2009). All of these may
facilitate increased contact between infected animals and suscepti‐
ble humans through increased range expansion or range overlap and
population growth (as described in the previous section) or aggrega‐
tion (Gortazar et al., 2014). These processes originate at a local level
but can have global consequences (e.g., outbreaks of avian influenza
in humans, which usually have zoonotic origins).
1.3 | Effects of ecosystems on zoonoses
Evidence indicates that the susceptibility of humans to a specific zo‐
onosis can be highly variable (Civitello et al., 2015; Jones et al., 2008;
Salkeld, Padgett, Jones, & Lafferty, 2013; Wood et al., 2016), and
exploration of epidemiological and ecological principles can provide
further insights. A primary ecological component of any zoonosis
is the habitat occupied by the reservoir host(s). Although there are
detailed ecological descriptions of various habitats using vegetation
or urban categories to obtain greater resolution within classifica‐
tion categories, for example, CORINE (Co‐ORdinated INformation
on the Environment), for this study, following Schwabe (Schwabe,
1984), we categorize three major host habitat types or ecosystems
for zoonoses: “domestic,” “domiciliated” (or “peridomestic”) and “syl‐
vatic.” The terms “domiciliated,” “synanthropic” and “peridomestic”
are interchangeable, and here, “peridomestic” is used. Different eco‐
systems vary in species community and composition.
Potential exposure of humans usually decreases through the
ecosystem series “domestic,” “peridomestic” and “sylvatic,” whereas
biodiversity can be expected to increase. In domestic ecosystems,
force of infection (FOI) generally increases as a result of an increase
in pathogen abundance, often caused for example by systems fail‐
ures in abattoirs and by the amount of movement of the reservoir
hosts and/or mechanical vectors. In addition, animal breeding for
certain desirable traits may compromise immunogenetics. In sylvatic
ecosystems, exposure of humans is less frequent, but FOI may in‐
crease or decrease as a result of changes in human intrusion and/
or habitat degradation. Seasonal and annual variations in reservoir
host populations, as well as changes in species composition, are
important FOI factors in sylvatic zoonoses. The dilution effect, as
a general concept, suggests that naturally occurring biodiversity,
specifically species diversity, could reduce disease risk, including
zoonoses (Keesing, Holt, & Ostfeld, 2006). For example, the infec‐
tion prevalence of hantaviruses in wild rodent reservoir populations
and reservoir population density increased where small‐mammal
species diversity was reduced in an experimental study carried out
McMAHON et al.
in Panama (Suzán et al., 2009). The common appeal of the dilution
effect to public health and conservation is clear as with one initia‐
tive (i.e., increased biodiversity), multiple benefits could potentially
result, such as reduced human health risk and reduced infectious dis‐
ease in wildlife (Keesing et al., 2010; Pongsiri et al., 2009).
The factors responsible for FOI in peridomestic ecosystems,
in which wild animals occur in close association with humans, for
example black rat (Rattus rattus) and Norwegian rat (R. norvegicus),
can be a mix of those in the other two ecosystems. When zoonoses
involve arthropod vectors or parasite intermediate hosts, there are
more factors that might influence FOI and the system becomes more
complex, so that effective intervention becomes more difficult.
We use specific examples of zoonoses to demonstrate how the
ecological requirements of zoonotic pathogens in particular ecosys‐
tems can alter the FOI of the relevant zoonoses. The public health
relevance of the dilution effect is discussed in relation to zoonoses
prevalence and management. The information discussed could be
used to inform monitoring, surveillance and planning for a balanced
One Health approach.
2 | C A S E S T U D I E S
2.1 | Domestic ecosystem
It is understood that food‐borne infections are among the most im‐
portant zoonoses worldwide (EFSA, 2017), and intensification of
food producing systems has increased the associated risk. As the
number of farm animals serving as reservoir hosts rises, so does the
FOI, thus increasing the possibility of human infection (Pennington,
2010). In parallel with this, the industrialization of food‐processing
systems has increased the contamination of food with such patho‐
gens as Salmonella spp., Campylobacter jejuni and certain strains of
Escherichia coli.
F I G U R E 2   Relationships between
the pathogens, Escherichia coli, Leptospira
spp. and Echinococcus multilocularis with
their respective reservoirs hosts (cattle,
rodents, fox/rodents) and habitats
(domestic, peridomestic and sylvatic)
indicating the potential for human disease
|
      759
Escherichia coli O157 (Figure 2) is a bacterial pathogen that causes
gastroenteritis, occasionally resulting in life‐threatening kidney dys‐
function (Newell et al., 2010). The level of intensification of beef
production is clearly a factor and outbreaks have been associated
with the linking of intensification and biodiversity loss, resulting in
increased prevalence of the pathogen in cattle, the most important
reservoir host (Donald, Green, & Heath, 2001; Jones et al., 2013).
While the main risk to the human population is failure of food‐
processing safety systems such as appropriate application of hazard
analysis and critical control points (HACCP), management at farm
level also has a role to play because of an association between in‐
fection prevalence in cattle entering abattoirs and subsequent con‐
tamination levels (Loneragan & Brashears, 2005). Several preharvest
intervention measures, such as feeding probiotics or sodium chlorate
in feed or water, have shown promise, but so far, experimental re‐
sults have been inconsistent. There is no evidence that targeted an‐
tibiotic use reduces shedding or that antimicrobial growth promoters
increase shedding (Sargeant, Amezcua, Rajic, & Waddell, 2007).
For non‐food‐borne domestic zoonoses, cultural factors in the
human population are important. For example, the prevalence of the
nematode Toxocara canis and the cestode Echinococcus granulosus,
both of which utilize domestic dogs and other canids as definitive
hosts, is associated with lack of worming of dogs and the environ‐
mental dissemination of dog faeces. Although sheep are interme‐
diate hosts of E. granulosus, this infection is not associated with
intensification of agriculture, but rather with certain extensive agri‐
cultural systems in which knowledge of the risk is low (Otero‐Abad
& Torgerson, 2013).
2.2 | Peridomestic ecosystem
Wild animals inhabiting the domestic environment are part of
the peridomestic ecosystem and may contribute to peridomestic
 |
760       McMAHON et al.
zoonoses. A well‐known example is leptospirosis (Figure 2), a wide‐
spread and neglected worldwide bacterial spirochaete zoonosis
(Bharti et al., 2003), for which rodents, particularly the brown rat,
Rattus norvegicus, are the principal reservoirs. The introduction of
an invasive mammalian species by humans can, unintentionally, alter
reservoir host community composition, and thus change the dynam‐
ics of this zoonosis (Hubálek, 2003; Nally et al., 2016). Alterations in
rodent communities (Rattus rattus, R. norvegicus and R. exculans) as a
result of the introduction of the black rat, R. rattus, to the island of
Futuna (Western Polynesia), increased leptospirosis risk in humans
(Theuerkauf et al., 2013), thus demonstrating how an alteration in
community structure and composition of wild rodent species can in‐
fluence the FOI of peridomestic zoonoses. In developing countries,
it is a socioeconomic disease exacerbated by urbanization, rodent
infestation and transmission via contaminated water sources asso‐
ciated with inadequate infrastructures and severe flooding events
(Bharti et al., 2003). Elevated contact with spirochaetes within ro‐
dent‐infested areas as a result of behaviour change in risk groups
(e.g., farmers, veterinarians and water sports enthusiasts) is another
determining factor in leptospirosis incidence (Garvey, Connell,
O’Flanagan, & McKeown, 2014).
2.3 | Sylvatic ecosystem
The sylvatic cestode, Echinococcus multilocularis (Figure 2), causes in‐
fections that can have a poor prognosis in humans, and it appears the
dynamics of infection with this parasite has altered in recent years in
parts of Europe. E. multilocularis utilizes wild and domestic canids (in
Europe, red fox Vulpes vulpes, as well as domestic dogs) as definitive
hosts and rodents as intermediate hosts. The abundance of foxes is
a major contributor to the FOI of this pathogen. The red fox popula‐
tion has increased in European regions over the last few decades and
this has been attributed in part to the success of a vaccine against
fox rabies, in conjunction with the adaptability of foxes to the urban
landscape (Otero‐Abad & Torgerson, 2013). The fox population was
evidently held in check to some extent by the rabies virus, and when
this pressure was removed by the antirabies vaccination programme,
fox abundance increased, leading to increased transmission of the
cestode zoonosis (Combes et al., 2012; Schneider, Aspöck, & Auer,
2013; Schweiger et al., 2007). In addition, generally increased risk
is associated with humans entering sylvatic ecosystems, whereas
specific risk factors include owning a dog that hunts game, living in
a farmhouse and being a farmer therefore increasing the likelihood
of contact with the definitive hosts (Kern et al., 2004). This is an ex‐
ample of an intentional measure directed at one particular zoonosis
(rabies) having an unintentional effect on another (E. multilocularis)
and demonstrates the complexity of the eco‐epidemiological inter‐
actions that can occur in zoonoses.
2.4 | Vector‐borne zoonoses
Vector‐borne zoonoses, similar to those involving parasite interme‐
diate hosts, add an additional layer of complexity to the transmission
dynamics of the diseases they cause, because both the vectors and
the zoonotic pathogens must be maintained within the ecosystem.
The most common vector‐borne disease in the temperate northern
F I G U R E 3   Relationship between
the vector, pathogens, reservoirs hosts,
habitats and the potential for Lyme
borreliosis in humans. Vector ticks
(a) transmit the pathogens, Borrelia
burgdorferi sensu lato (b), to small
mammals and/or birds (c). The ticks also
acquire the infection from these animals
and thus pose an infection risk to humans
(d) in both sylvatic (e) and peridomestic
(f) habitats. Ticks do not acquire the
infection from large animals such as
deer (g) (in sylvatic and peridomestic
habitats), or from sheep and cattle (h) in
the domestic habitat (i), but these hosts
are essential for maintenance of the tick
population. Ticks that have fed exclusively
on such hosts do not pose an infection
risk when they infest humans (j)
McMAHON et al.
hemisphere, Lyme borreliosis (LB) (Figure 3), has attracted much at‐
tention in relation to the hypothesis that biodiversity can, through
the dilution effect, reduce transmission rates and thus the risk of
disease (LoGiudice, Ostfeld, Schmidt, & Keesing, 2003; Ostfeld &
Keesing, 2012). However, robust arguments have been made against
universal application of this hypothesis (Lafferty & Wood, 2013;
Ogden & Tsao, 2009; Randolph & Dobson, 2012). LB is caused by
members of the Borrelia burgdorferi sensu lato (s.l.) genospecies com‐
plex and is transmitted by ticks of the Ixodes ricinus species complex.
The reservoir hosts of the pathogens are mainly small mammals and
ground‐feeding passerine birds, but large mammals, though reser‐
voir incompetent, are required for the ticks to complete their life cy‐
cles (Gray et al., 1998). Deer rather than livestock are most typically
associated with LB, because they usually occur in the same habitats
as the spirochaete reservoir hosts (Figure 3). Thus humans are at risk
of infection when they enter woodland (sylvatic ecosystem) or when
the reservoir hosts and deer occur in periurban (i.e., peridomestic)
ecosystems (Rizzoli et al., 2014). Domestic livestock such as cattle
and sheep are not generally associated with LB, mainly because they
are usually farmed in open habitats that do not permit prolonged
survival of the desiccation‐susceptible nonparasitic stages of the
tick life cycle. Nevertheless, large tick populations can be maintained
by sheep and cattle in marginal farmland (which can feed all stages)
in the virtual absence of other hosts (Milne, 1949). In such scenarios,
the ticks are likely to show a low to zero prevalence of infection with
B. burgdorferi s.l. because of the relatively small numbers of reservoir
hosts present (Figure 3) (Gray, Kahl, Janetzki, Stein, & Guy, 1995;
Matuschka et al., 1993). This situation is in marked contrast to the
generalization that there is a high risk of LB wherever there are ap‐
preciable numbers of ticks (Jaenson et al., 2009).
The survival of ticks in undergrazed agricultural habitats, which
is typical of Ireland, particularly west of the Shannon River, also oc‐
curs in continental Europe but to a much lesser extent. In such areas,
an increase in biodiversity resulting from reforestation might actu‐
ally increase tick infection rates, in contradiction to the situation de‐
scribed for parts for the United States, where it has been suggested
that increased biodiversity reduces the FOI by diverting part of the
tick population to hosts that are not reservoirs of the tick‐borne
pathogen B. burgdorferi s.l. (Ostfeld & Keesing, 2012). The current
low tick infection rates in farmland‐dominated landscapes, such as in
Ireland, and the common occurrence of bird‐associated genospecies
such as B. garinii (some strains of which are zoonotic), in north‐west‐
ern Europe (Kurtenbach et al., 2006; Pichon, Rogers, Egan, & Gray,
2005; Rauter & Hartung, 2005; Saint Girons et al., 1998), could make
important contributions to a rise in infection rates, considering that
afforestation and reforestation increase bird species richness and
diversity (Graham et al., 2015). The process of reforestation in many
parts of western Europe is already in progress, and it remains to be
seen whether this results in a rise in the incidence of LB in these
areas. This issue illustrates the complexity that can exist in the dy‐
namics of transmission of a pathogen that circulates among several
species of vertebrate host and has a vector, I. ricinus, which feeds on
both reservoirs and nonreservoirs of the pathogens.
|
      761
3 | M A N AG E M E NT O F ZO O N OS I S R I S K
Effective management of zoonoses depends on greater advance‐
ment in the following to understand zoonoses: delineation of key
drivers of the zoonotic outbreaks, gathering of more empirical
data from both the field and laboratory experiments and further
exploration of the conceptual frameworks that develop our think‐
ing around the complexity of these outbreaks (Johnson, Ostfeld,
& Keesing, 2015). Future research should explore and harness
knowledge of the disease ecology and other influencing factors
of pathogens and parasites that are likely to interact differently
within dynamic landscapes in the Anthropocene in the coming
years to inform risk assessment. Combined with this, greater un‐
derstanding is also required for the life history traits of the zo‐
onosis vertebrate reservoirs, parasite intermediate hosts and
arthropod vectors, (where relevant) to provide a comprehensive
understanding of the likely risk. Linking these ecological factors
with particular landscape changes will enable authorities to offset
the risk of particular zoonoses in a specific set of circumstances.
As outlined in this paper, given the risks surrounding zoonoses
emergence and land‐use change (Jones et al., 2013; Kilpatrick,
2011; McCauley et al., 2015), where large‐scale landscape change
is proposed (e.g., alteration or intensification of agricultural lands
and urbanization), we have now reached a point in resource man‐
agement where an ecological impact assessment, similar to an
environmental impact assessment (McMahon, Wall, Fanning, &
Fahey, 2015) and in which potential disease is taken into account
(CIEEM, 2016), should be a requirement for such alterations to
proceed. The specifications for an ecological impact assessment
require further consideration but landscape ecology could inform
this process (Hartemink, Vanwambeke, Purse, Gilbert, & Dyck,
2015) using computer programs such as FRAGSTATS (McGarigal,
Cushman, & Ene, 2012) to quantify landscape configuration and
composition. The juxtaposition of the domestic, peridomestic and
sylvatic ecosystems influences zoonoses dynamics for both host
and pathogen/parasite populations (Kilpatrick, 2011; McCauley
et al., 2015). As intimated above, the importance of integration
of epidemiology and community ecology for understanding zoon‐
oses is clear due to the multispecies and multiple scales involved
(Johnson, de Roode, & Fenton, 2015) and is further highlighted in
the examples outlined in this paper. Diseases, zoonoses or other‐
wise, are components of ecological systems; therefore, eradica‐
tion is unlikely to result in entirely satisfactory outcomes because
the disease is a natural ecological process and other pathogens or
parasites tend to occupy the vacated niches (Lloyd‐Smith, 2013).
However, community ecology in conjunction with epidemiology
can bring about a greater understanding of the processes involved
in zoonotic outbreaks and facilitate better public health manage‐
ment (Cunningham, Scoones, & Wood, 2017; Johnson, de Roode,
et al., 2015; Young et al., 2017). It is well accepted that there is
unprecedented pressure on the planet to sustain ever‐increasing
numbers of humans (Gerland et al., 2014). The interconnectedness
of humans, livestock and wildlife is core to many of our current
 |
762       McMAHON et al.
global challenges. It is important to understand the impacts that
changes in human populations have on pathogen exchange be‐
tween humans, wildlife and livestock in varying ecological and cul‐
tural contexts (Jones et al., 2013; Muehlenbein, 2016).
4 |  CO N C LU S I O N
Anthropogenic changes, including agricultural specialization and in‐
tensification accompanied by environmental effects, are occurring
constantly and so zoonotic diseases will continue to emerge (Jones
et al., 2013). In view of the growth of the human population, it is nec‐
essary to understand the domestic, peridomestic and sylvatic eco‐
systems in this context in order to predict emergence of zoonoses
and system resilience (Suter, 1993). Landscape planning for One
Health and community ecology is required to understand and man‐
age outbreaks of zoonoses (Hassell, Begon, Ward, & Fèvre, 2017)
incorporating a net health effect for conservation and public health
(Myers et al., 2013). Drivers of human diseases, including zoonoses,
are context‐ and species‐dependent demonstrating spatial and tem‐
poral variability (Civitello et al., 2015; Keesing et al., 2010; Salkeld et
al., 2013; Salkeld, Padgett, Jones, & Antolin, 2015). Interdisciplinary
collaboration, incorporating One Health land‐use planning, must
appreciate that conducting empirical studies with controls, using
standardization, randomization and replication of comparable ex‐
perimental units with the aim of producing results with powerful
inference are not possible without large‐scale investment in long‐
term landscape experiments. Until the experiments are conducted,
such local context that drives the emergence of zoonoses must be
respected.
AC K N OW L E D G E M E N T S
The authors would like to thank Bernard Kaye for his help prepar‐
ing the figures and Jarlath Nally, Laura Espinosa, John Fry and an
anonymous reviewer for comments on previous versions of the
manuscript. BMcM was supported by European Cooperation in
Science and Technology TD1404 Network for the Evaluation of
One Health, and SM was supported by ANR FutureHealthSEA
(ANR‐17‐CE35‐0003‐01).
C O N FL I C T O F I N T E R E S T
None declared.
ORCID
Barry J. McMahon  http://orcid.org/0000-0003-3143-8075
REFERENCES
Altizer, S., Ostfeld, R. S., Johnson, P. T. J., Kutz, S., & Harvell, C. D.
(2013). Climate change and infectious diseases: From evidence
to a predictive framework. Science, 341, 514–519. https://doi.
org/10.1126/science.1239401
Bharti, A. R., Nally, J. E., Ricaldi, J. N., Matthias, M. A., Diaz, M. M., &
Lovett, M. A., …Peru‐United States Leptospirosis Consortium
(2003). Leptospirosis: A zoonotic disease of global importance.
Lancet Infectious Diseases, 3, 757–771. https://doi.org/10.1016/
S1473-3099(03)00830-2
Ceballos, G., Ehrlich, P. R., & Dirzo, R. (2017). Biological annihilation
via the ongoing sixth mass extinction signaled by vertebrate pop‐
ulation losses and declines. Proceedings of the National Academy of
Sciences of the United States of America, 114, 6089–6096. https://doi.
org/10.1073/pnas.1704949114
Chaisiri, K., Cosson, J.‐F., & Morand, S. (2017). Infection of rodents
by Orientia tsutsugamushi, the agent of scrub typhus in relation to
land use in Thailand. Tropical Medicine and Infectious Disease, 2, 53.
https://doi.org/10.3390/tropicalmed2040053.
CIEEM (2016). Guidelines for ecological impact assessment in the UK
and Ireland: Terrestrial, freshwater and coastal, 2nd ed. Winchester,
UK: CIEEM. Retrieved from https://www.cieem.net/data/files/
Publications/EcIA_Guidelines_Terrestrial_Freshwater_and_Coastal_
Jan_2016.pdf
Civitello, D. J., Cohen, J., Fatima, H., Halstead, N. T., Liriano, J., McMahon,
T. A., … Rohr, J. R. (2015). Biodiversity inhibits parasites: Broad evi‐
dence for the dilution effect. Proceedings of the National Academy of
Sciences of the United States of America, 112, 8667–8671. https://doi.
org/10.1073/pnas.1506279112
Combes, B., Comte, S., Raton, V., Raoul, F., Boué, F., Umhang, G., …
Giraudoux, P. (2012). Westward spread of Echinococcus multilocu-
laris in foxes, France, 2005–2010. Emerging Infectious Diseases, 18,
2059–2062. https://doi.org/10.3201/eid1812.120219
Cunningham, A. A., Scoones, I., & Wood, J. L. N. (2017). One Health
for a changing world: New perspectives from Africa. Philosophical
Transactions of the Royal Society of London. Series B, Biological Sciences,
372, 20160162. https://doi.org/10.1098/rstb.2016.0162
Davis, S., Calvet, E., & Leirs, H. (2005). Fluctuating rodent popula‐
tions and risk to humans from rodent‐borne zoonoses. Vector
Borne Zoonotic Diseases, 5, 305–314. https://doi.org/10.1089/
vbz.2005.5.305
Del Rio, C., & Guarner, J. (2015). Ebola: Implications and perspectives.
Transactions of the American Clinical and Climatological Association,
126, 93–112.
Donald, P. F., Green, R. E., & Heath, M. F. (2001). Agricultural intensi‐
fication and the collapse of Europe's farmland bird populations.
Proceedings of the Royal Society B: Biological Sciences, 268, 25–29.
https://doi.org/10.1098/rspb.2000.1325
EFSA (European Food Safety Authority), & ECDC (European Centre for
Disease Prevention and Control) (2017). The European Union sum‐
mary report on trends and sources of zoonoses, zoonotic agents
and food‐borne outbreaks in 2016. EFSA Journal, 15, 5077, 228 pp.
https://doi.org/10.2903/j.efsa.2017.5077
Engelthaler, D. M., Mosley, D. G., Cheek, J. E., Levy, C. E., Komatsu, K. K.,
Ettestad, P., …Bryan, R. T. (1999). Climatic and environmental pat‐
terns associated with hantavirus pulmonary syndrome, Four Corners
region, United States. Emerging Infectious Diseases, 5, 87–94. https://
doi.org/10.3201/eid0501.990110
Epstein, J. H., Field, H. E., Luby, S., Pulliam, J. R. C., & Daszak, P. (2006).
Nipah virus: Impact, origins, and causes of emergence. Current
Infectious Disease Reports, 8, 59–65. https://doi.org/10.1007/
s11908-006-0036-2
Foley, J. A., DeFries, R., Asner, G. P., Barford, C., Bonan, G., Carpenter, S.
R., … Snyder, P. K. (2005). Global consequences of land use. Science,
309, 570–574. https://doi.org/10.1126/science.1111772
Fornace, K. M., Abidin, T. R., Alexander, N., Brock, P., Grigg, M. J., Murphy,
A., … Cox, J. (2016). Association between landscape factors and spa‐
tial patterns of Plasmodium knowlesi infections in Sabah, Malaysia.
McMAHON et al.
Emerging Infectious Diseases, 22, 201–208. https://doi.org/10.3201/
eid2202.150656
Gage, K. L., & Kosoy, M. Y. (2005). Natural history of plague: Perspectives
from more than a century of research. Annual Review of Entomology, 50,
505–528. https://doi.org/10.1146/annurev.ento.50.071803.130337
Garvey, P., Connell, J., O’Flanagan, D., & McKeown, P. (2014).
Leptospirosis in Ireland: Annual incidence and exposures associated
with infection. Epidemiology and Infection, 142, 847–855. https://doi.
org/10.1017/S0950268813001775
Gerland, P., Raftery, A. E., Ševčíková, H., Li, N., Gu, D., Spoorenberg,
T., … Wilmoth, J. (2014). World population stabilization unlikely
this century. Science, 346, 234–237. https://doi.org/10.1126/
science.1257469
Gortazar, C., Reperant, L. A., Kuiken, T., de la Fuente, J., Boadella, M.,
Martínez‐Lopez, B., … Keck, F. (2014). Crossing the interspecies bar‐
rier: Opening the door to zoonotic pathogens. PLoS Path, 10, 1–5.
https://doi.org/10.1371/journal.ppat.1004129
Graham, C. T., Wilson, M. W., Gittings, T., Kelly, T. C., Irwin, S., Quinn, J.
L., & O’Halloran, J. (2015). Implications of afforestation for bird com‐
munities: The importance of preceding land‐use type. Biodiversity
and Conservation, 1–21, https://doi.org/10.1007/s10531-015-0987-4
Gray, J. S., Kahl, O., Janetzki, C., Stein, J., & Guy, E. (1995). The spa‐
tial distribution of Borrelia burgdorferi‐infected Ixodes ricinus in the
Connemara region of County Galway, Ireland. Experimental & Applied
Acarology, 19, 163–172. https://doi.org/10.1007/BF00046288
Gray, J. S., Kahl, O., Robertson, J. N., Daniel, M., Estrada‐Peña, A.,
Gettinby, G., … Zeman, P. (1998). Lyme borreliosis habitat assessment.
Zentralblatt Für Bakteriologie, 287, 211–228. https://doi.org/10.1016/
S0934-8840(98)80123-0
Guan, P., Huang, D., He, M., Shen, T., Guo, J., & Zhou, B. (2009). Investigating
the effects of climatic variables and reservoir on the incidence of
hemorrhagic fever with renal syndrome in Huludao City, China: A 17‐
year data analysis based on structure equation model. BMC Infectious.
Diseases, 8, 109. https://doi.org/10.1186/1471-2334-9-109
Guis, H., Caminade, C., Calvete, C., Morse, A. P., Tran, A., & Baylis, M.
(2012). Modelling the effects of past and future climate on the risk
of bluetongue emergence in Europe. Journal of the Royal Society,
Interface, 9, 339–350. https://doi.org/10.1098/rsif.2011.0255
Hartemink, N., Vanwambeke, S. O., Purse, B. V., Gilbert, M., & Van Dyck,
H. (2015). Towards a resource‐based habitat approach for spatial
modelling of vector‐borne disease risks: Resource‐based habitats for
vector‐borne diseases. Biological Reviews, 90, 1151–1162. https://doi.
org/10.1111/brv.12149
Hassell, J. M., Begon, M., Ward, M. J., & Fèvre, E. M. (2017). Urbanization
and disease emergence: Dynamics at the wildlife–livestock–human
interface. Trends in Ecology & Evolution, 32, 55–67. https://doi.
org/10.1016/j.tree.2016.09.012
Hoekstra, A. Y., & Wiedmann, T. O. (2014). Humanity's unsustainable
environmental footprint. Science, 344, 1114–1117. https://doi.
org/10.1126/science.1248365
Hubálek, Z. (2003). Emerging human infectious diseases: Anthroponoses,
zoonoses, and sapronoses. Emerging Infectious Diseases, 9, 403–404.
https://doi.org/10.3201/eid0903.020208
Jaenson, T. G. T., Eisen, L., Comstedt, P., Mejlon, H. A., Lindgren,
E., Bergström, S., & Olsen, B. (2009). Risk indicators for the
tick Ixodes ricinus and Borrelia burgdorferi sensu lato in Sweden.
Medical and Veterinary Entomology, 23, 226–237. https://doi.
org/10.1111/j.1365-2915.2009.00813.x
Jaenson, T. G. T., Hjertqvist, M., Bergström, T., & Lundkvist, A. (2012).
Why is tick‐borne encephalitis increasing? A review of the key factors
causing the increasing incidence of human TBE in Sweden. Parasites
& Vectors, 5, 184. https://doi.org/10.1186/1756-3305-5-184
Johnson, P. T. J., de Roode, J. C., & Fenton, A. (2015). Why infectious
disease research needs community ecology. Science, 349, 1259504.
https://doi.org/10.1126/science.1259504
|
      763
Johnson, P. T. J., Ostfeld, R. S., & Keesing, F. (2015). Frontiers in research
on biodiversity and disease. Ecology Letters, 18, 1119–1133. https://
doi.org/10.1111/ele.12479
Jones, B. A., Grace, D., Kock, R., Alonso, S., Rushton, J., Said, M. Y., …
Udo Pfeiffer, D. (2013). Zoonosis emergence linked to agricultural
intensification and environmental change. Proceedings of the National
Academy of Sciences of the United States of America, 110, 8399–8404.
https://doi.org/10.1073/pnas.1208059110
Jones, K. E., Patel, N. G., Levy, M. A., Storeygard, A., Balk, D., Gittleman,
J. L., & Daszak, P. (2008). Global trends in emerging infectious dis‐
eases. Nature, 451, 990–993. https://doi.org/10.1038/nature06536
Jonsson, C. B., Figueiredo, L. T., & Vapalahti, O. (2010). A global per‐
spective on hantavirus ecology, epidemiology, and disease. Clinical
Microbiology Reviews, 23, 412–441. https://doi.org/10.1128/
CMR.00062-09
Karesh, W. B., Dobson, A., Lloyd‐Smith, J. O., Lubroth, J., Dixon, M.
A., Bennett, M., … Heymann, D. L. (2012). Ecology of zoonoses:
Natural and unnatural histories. Lancet, 380, 1936–1945. https://doi.
org/10.1016/S0140-6736(12)61678-X
Keesing, F., Belden, L. K., Daszak, P., Dobson, A., Harvell, C. D., Holt,
R. D., … Ostfeld, R. S. (2010). Impacts of biodiversity on the emer‐
gence and transmission of infectious diseases. Nature, 468, 647–652.
https://doi.org/10.1038/nature09575
Keesing, F., Holt, R. D., & Ostfeld, R. S. (2006). Effects of species di‐
versity on disease risk. Ecology Letters, 9, 485–498. https://doi.
org/10.1111/j.1461-0248.2006.00885.x
Kern, P., Ammon, A., Kron, M., Sinn, G., Sander, S., Petersen, L. R., …
Kern, P. (2004). Risk factors for alveolar echinococcosis in hu‐
mans. Emerging Infectious Diseases, 10, 2088–2093. https://doi.
org/10.3201/eid1012.030773
Kilpatrick, A. M. (2011). Globalization, land use, and the invasion of
West Nile virus. Science, 334, 323–327. https://doi.org/10.1126/
science.1201010
Kuo, C.‐C., Huang, J.‐L., Shu, P.‐Y., Lee, P.‐L., Kelt, D. A., & Wang, H.‐C.
(2012). Cascading effect of economic globalization on human
risks of scrub typhus and tick‐borne rickettsial diseases. Ecological
Applications, 22, 1803–1816. https://doi.org/10.1890/12-0031.1
Kurtenbach, K., Hanincová, K., Tsao, J. I., Margos, G., Fish, D., & Ogden,
N. H. (2006). Fundamental processes in the evolutionary ecology of
Lyme borreliosis. Nature Reviews Microbiology, 4, 660–669. https://
doi.org/10.1038/nrmicro1475
Lafferty, K. D., & Wood, C. L. (2013). It's a myth that protection against
disease is a strong and general service of biodiversity conservation:
Response to Ostfeld and Keesing. Trends in Ecology & Evolution, 28,
503–504. https://doi.org/10.1016/j.tree.2013.06.012
Lewis, F. I., Otero‐Abad, B., Hegglin, D., Deplazes, P., & Torgerson, P. R.
(2014). Dynamics of the force of infection: Insights from Echinococcus
multilocularis infection in foxes. PLoS Neglected Tropical Diseases., 8,
e2731. https://doi.org/10.1371/journal.pntd.0002731
Lloyd‐Smith, J. O. (2013). Vacated niches, competitive release and
the community ecology of pathogen eradication. Philosophical
Transactions of the Royal Society of London. Series B, Biological Sciences,
368, 20120150. https://doi.org/10.1098/rstb.2012.0150
LoGiudice, K., Ostfeld, R. S., Schmidt, K. A., & Keesing, F. (2003). The
ecology of infectious disease: Effects of host diversity and commu‐
nity composition on Lyme disease risk. Proceedings of the National
Academy of Sciences of the United States of America, 100, 567–571.
https://doi.org/10.1073/pnas.0233733100
Loneragan, G. H., & Brashears, M. M. (2005). Pre‐harvest interven‐
tions to reduce carriage of E. coli O157 by harvest‐ready feed‐
lot cattle. Meat Science, 71, 72–78. https://doi.org/10.1016/j.
meatsci.2005.04.005
Markandya, A., Taylor, T., Longo, A., Murty, M. N., Murty, S., &
Dhavala, K. (2008). Counting the cost of vulture decline – An ap‐
praisal of the human health and other benefits of vultures in India.
 |
764       McMAHON et al.
Ecological Economics, 67, 194–204. https://doi.org/10.1016/j.
ecolecon.2008.04.020
Matuschka, F. R., Heiler, M., Eiffert, H., Fischer, P., Lotter, H., & Spielman,
A. (1993). Diversionary role of hoofed game in the transmission
of Lyme disease spirochetes. The American Journal of Tropical
Medicine and Hygiene, 48, 693–699. https://doi.org/10.4269/
ajtmh.1993.48.693
Matuschka, F. R., & Spielman, A. (1986). The emergence of Lyme dis‐
ease in a changing environment in North America and central
Europe. Experimental & Applied Acarology, 2, 337–353. https://doi.
org/10.1007/BF01193900
McCauley, D. J., Salkeld, D. J., Young, H. S., Makundi, R., Dirzo, R.,
Eckerlin, R. P., … Helgen, K. M. (2015). Effects of land use on plague
(Yersinia pestis) activity in rodents in Tanzania. The American Journal of
Tropical Medicine and Hygiene, 92, 776–783. https://doi.org/10.4269/
ajtmh.14-0504
McGarigal, K., Cushman, S. A., & Ene, E. (2012). FRAGSTATS v4: Spatial
pattern analysis program for categorical and continuous maps.
Computer software program produced by the authors at the University
of Massachusetts, Amherst. Retrieved from https://www.umass.edu/
landeco/research/fragstats/fragstats.html
McIntyre, K. M., Setzkorn, C., Hepworth, P. J., Morand, S., Morse,
A. P., & Baylis, M. (2017). Systematic assessment of the climate
sensitivity of important human and domestic animals pathogens
in Europe. Scientific Reports, 7, 7134. https://doi.org/10.1038/
s41598-017-06948-9
McMahon, B. J., Wall, P. G., Fanning, S., & Fahey, A. G. (2015). Targets to
increase food production: One Health implications. Infection Ecology
& Epidemiology, 5, 27708. https://doi.org/10.3402/iee.v5.27708
Milne, A. (1949). The ecology of the sheep tick, Ixodes ricinus L. Host
relationships of the tick: Part 2. Observations on hill and moorland
grazings in northern England. Parasitology, 39, 173–197. https://doi.
org/10.1017/S0031182000083736
Morand, S., Owers, K. A., Waret‐Szkuta, A., McIntyre, K. M., & Baylis,
M. (2013). Climate variability and outbreaks of infectious diseases
in Europe. Scientific Reports, 3, 1774. https://doi.org/10.1038/
srep01774
Muehlenbein, M. P. (2016). Disease and human/animal Interactions.
Annual Review of Anthropology, 45, 395–416. https://doi.org/10.1146/
annurev-anthro-102215-10003
Myers, S. S., Gaffikin, L., Golden, C. D., Ostfeld, R. S., Redford, K. H.,
Ricketts, T. H., … Osofsky, S. A. (2013). Human health impacts of
ecosystem alteration. Proceedings of the National Academy of Sciences
of the United States of America, 110, 18753–18760. https://doi.
org/10.1073/pnas.1218656110
Nally, J. E., Arent, Z., Bayles, D. O., Hornsby, R. L., Gilmore, C., Regan, S.,
… McMahon, B. J. (2016). Emerging infectious disease implications
of invasive mammalian species: The Greater White‐Toothed Shrew
(Crocidura russula) is associated with a novel serovar of pathogenic
Leptospira in Ireland. PLoS Neglected Tropical Diseases, 10, https://doi.
org/10.1371/journal.pntd.0005174
Newell, D. G., Koopmans, M., Verhoef, L., Duizer, E., Aidara‐Kane, A.,
Sprong, H., … Kruse, H. (2010). Food‐borne diseases — The chal‐
lenges of 20 years ago still persist while new ones continue to
emerge. International Journal of Food Microbiology, 139, S3–S15.
https://doi.org/10.1016/j.ijfoodmicro.2010.01.021
Ogden, N. H., & Tsao, J. I. (2009). Biodiversity and Lyme disease: Dilution
or amplification? Epidemics, 1, 196–206. https://doi.org/10.1016/j.
epidem.2009.06.002
Ostfeld, R. S., & Keesing, F. (2012). Effects of host diversity on infec‐
tious disease. Annual Review of Ecology, Evolution, and Systematics, 43,
157–182. https://doi.org/10.1146/annurev-ecolsys-102710-145022
Otero‐Abad, B., & Torgerson, P. R. (2013). A systematic review of the
epidemiology of echinococcosis in domestic and wild animals. PLOS
Neglected Tropical Diseases, 7, e2249. https://doi.org/10.1371/jour‐
nal.pntd.0002249
Pennington, H. (2010). Escherichia coli O157. Lancet, 376, 1428–1435.
https://doi.org/10.1016/S0140-6736(10)60963-4
Pichon, B., Rogers, M., Egan, D., & Gray, J. (2005). Blood‐meal analysis
for the identification of reservoir hosts of tick‐borne pathogens in
Ireland. Vector Borne and Zoonotic Diseases, 5, 172–180. https://doi.
org/10.1089/vbz.2005.5.172
Plowright, R. K., Parrish, C. R., McCallum, H., Hudson, P. J., Ko, A. I.,
Graham, A. L., & Lloyd‐Smith, J. O. (2017). Pathways to zoonotic
spillover. Nature Reviews Microbiology, 5, 502–510. https://doi.
org/10.1038/nrmicro.2017.45
Pongsiri, M. J., Roman, J., Ezenwa, V. O., Goldberg, T. L., Koren, H. S.,
Newbold, S. C., … Salkeld, D. J. (2009). Biodiversity loss affects global
disease ecology. BioScience, 59, 945–954. https://doi.org/10.1525/
bio.2009.59.11.6
Ramasamy, R. (2014). Zoonotic malaria – Global overview and research
and policy needs. Frontiers of Public Health, 2, 123. https://doi.
org/10.3389/fpubh.2014.00123
Randolph, S. E., Asokliene, L., Avsic‐Zupanc, T., Bormane, A., Burri, C.,
Gern, L., … Zygutiene, M. (2008). Variable spikes in tick‐borne en‐
cephalitis incidence in 2006 independent of variable tick abundance
but related to weather. Parasites and Vectors, 1, 44. https://doi.
org/10.1186/1756-3305-1-44
Randolph, S. E., & Dobson, A. D. M. (2012). Pangloss revisited: A cri‐
tique of the dilution effect and the biodiversity‐buffers‐disease
paradigm. Parasitology, 139, 847–863. https://doi.org/10.1017/
S0031182012000200
Rauter, C., & Hartung, T. (2005). Prevalence of Borrelia burgdorferi sensu
lato genospecies in Ixodes ricinus ticks in Europe: A metaanalysis.
Applied and Environmental Microbiology, 71, 7203–7216. https://doi.
org/10.1128/AEM.71.11.7203-7216.2005
Rizzoli, A., Silaghi, C., Obiegala, A., Rudolf, I., Hubálek, Z., Földvári, G.,
… Kazimírová, M. (2014). Ixodes ricinus and its transmitted patho‐
gens in urban and peri‐urban areas in Europe: New hazards and rel‐
evance for public health. Frontiers in Public Health, 2, 251. https://doi.
org/10.3389/fpubh.2014.00251
Saint Girons, I., Gern, L., Gray, J. S., Guy, E. C., Korenberg, E., Nuttall,
P. A., … Postic, D. (1998). Identification of Borrelia burgdorferi sensu
lato species in Europe. Zentralblatt Für Bakteriologie, 287, 190–195.
https://doi.org/10.1016/S0934-8840(98)80120-5
Salkeld, D. J., Padgett, K. A., Jones, J. H., & Antolin, M. F. (2015). Public
health perspective on patterns of biodiversity and zoonotic disease.
Proceedings of the National Academy of Sciences of the United States of
America, 112, E6261. https://doi.org/10.1073/pnas.1517640112
Salkeld, D. J., Padgett, K. A., Jones, J. H., & Lafferty, K. (2013). A meta‐
analysis suggesting that the relationship between biodiversity and
risk of zoonotic pathogen transmission is idiosyncratic. Ecology
Letters, 16, 679–686. https://doi.org/10.1111/ele.12101
Samia, N. I., Kausrud, K. L., Heesterbeek, H., Ageyev, V., Begon, M., Chan,
K. S., & Stenseth, N. C. (2011). Dynamics of the plague‐wildlife‐
human system in Central Asia are controlled by two epidemiologi‐
cal thresholds. Proceedings of the National Academy of Sciences of the
United States of America, 108, 14527–14532. https://doi.org/10.1073/
pnas.1015946108
Sargeant, J. M., Amezcua, M. R., Rajic, A., & Waddell, L. (2007).
Pre‐harvest interventions to reduce the shedding of E. coli
O157 in the faeces of weaned domestic ruminants: A system‐
atic review. Zoonoses and Public Health, 54, 260–277. https://doi.
org/10.1111/j.1863-2378.2007.01059.x
Schmid, B. V., Büntgen, U., Easterday, W. R., Ginzler, C., Walløe, L.,
Bramanti, B., & Stenseth, N. C. (2015). Climate‐driven introduc‐
tion of the Black Death and successive plague reintroductions
into Europe. Proceedings of the National Academy of Sciences of the
McMAHON et al.
United States of America, 112, 3020–3025. https://doi.org/10.1073/
pnas.1412887112
Schneider, R., Aspöck, H., & Auer, H. (2013). Unexpected Increase of al‐
veolar echinococcosis, Austria, 2011. Emerging Infectious Diseases, 19,
475–477. https://doi.org/10.3201/eid1903.120595
Schwabe, C. W. (1984). Veterinary medicine and human health, 3rd ed.
Baltimore, MD: Williams & Wilkins.
Schwarz, A. C., Ranft, U., Piechotowski, I., Childs, J. E., & Brockmann,
S. O. (2009). Risk factors for human infection with Puumala virus,
southwestern Germany. Emerging Infectious Diseases, 15, 1032–1039.
https://doi.org/10.3201/eid1507.081413
Schweiger, A., Ammann, R. W., Candinas, D., Clavien, P.‐A., Eckert, J.,
Gottstein, B., … Deplazes, P. (2007). Human alveolar echinococco‐
sis after fox population increase, Switzerland. Emerging Infectious
Diseases, 13, 878–882. https://doi.org/10.3201/eid1306.061074
Sharp, P. M., & Hahn, B. H. (2011). Origins of HIV and the AIDS pandemic.
Cold Spring Harbor Perspectives in Medicine, 1, a006841. https://doi.
org/10.1101/cshperspect.a006841
Steinmann, P., Keiser, J., Bos, R., Tanner, M., & Utzinger, J. (2006).
Schistosomiasis and water resources development: Systematic
review, meta‐analysis, and estimates of people at risk. The
Lancet Infectious Diseases, 6, 411–425. https://doi.org/10.1016/
S1473-3099(06)70521-7
Stenseth, N. C., Samia, N. I., Viljugrein, H., Kausrud, K. L., Begon, M.,
Davis, S., … Chan, K. S. (2006). Plague dynamics are driven by cli‐
mate variation. Proceedings of the National Academy of Sciences of the
United States of America, 103, 13110–13115. https://doi.org/10.1073/
pnas.0602447103
Šumilo, D., Bormane, A., Asokliene, L., Vasilenko, V., Golovljova, I.,
Avsic‐Zupanc, T., … Randolph, S. E. (2008). Socio‐economic factors
in the differential upsurge of tick‐borne encephalitis in Central and
Eastern Europe. Reviews in Medical Virology, 18, 81–95. https://doi.
org/10.1002/rmv.566
Suter, G. W. (1993). A critique of ecosystem health concepts and indexes.
Environmental Toxicology and Chemistry, 12, 1533–1539. https://doi.
org/10.1002/etc.5620120903
Suzán, G., Marcé, E., Giermakowski, J. T., Mills, J. N., Ceballos,
G., Ostfeld, R. S., …Yates, T. L. (2009). Experimental evidence
for reduced rodent diversity causing increased hantavirus
|
      765
prevalence. PLoS ONE, 4, e5461. https://doi.org/10.1371/journal.
pone.0005461
Theuerkauf, J., Perez, J., Taugamoa, A., Niutoua, I., Labrousse, D., Gula,
R., … Goarant, C. (2013). Leptospirosis risk increases with changes
in species composition of rat populations. Die Naturwissenschaften,
100, 385–388. https://doi.org/10.1007/s00114-013-1033-6
Wilson, N., Lush, D., & Baker, M. G. (2010) Meteorological and climate
change themes at the 2010 International Conference on Emerging
Infectious Diseases. Eurosurveillance, 15, pii: 19627.
Wood, C. L., Lafferty, K. D., DeLeo, G., Young, H. S., Hudson, P. J., &
Kuris, A. M. (2016). Does biodiversity protect humans against
infectious disease? Reply. Ecology, 97, 543–546. https://doi.
org/10.1890/15-1503.1
Woolhouse, M. E. J., & Gowtage‐Sequeria, S. (2005). Host range and
emerging and reemerging pathogens. Emerging Infectious Diseases,
11, 1842–1847. https://doi.org/10.3201/eid1112.050997
Xu, G., Walker, D. H., Jupiter, D., Melby, P. C., & Arcari, C. M. (2017). A
review of the global epidemiology of scrub typhus. PLoS Neglected
Tropical Diseases, 11, e0006062. https://doi.org/10.1371/journal.
pntd.0006062
Yates, T. L., Mills, J. N., Parmenter, C. A., Ksiazek, T. G., Parmenter, R. R.,
& Vandecastle, J. R. (2002). The ecology and evolutionary history of
an emergent disease: Hantavirus pulmonary syndrome. BioScience,
52, 989–998. https://doi.org/10.1641/0006-3568(2002)052[098
9:TEAEHO]2.0.CO;2
Young, H. S., Wood, C. L., Kilpatrick, A. M., Lafferty, K. D., Nunn, C. L.,
& Vincent, J. R. (2017). Conservation, biodiversity and infectious
disease: Scientific evidence and policy implications. Philosophical
Transactions of the Royal Society B: Biological Sciences, 372, 20160124.
https://doi.org/10.1098/rstb.2016.0124
How to cite this article: McMahon BJ, Morand S, Gray JS.
Ecosystem change and zoonoses in the Anthropocene.
Zoonoses Public Health. 2018;65:755–765. https://doi.
org/10.1111/zph.12489