Chelsea Wood | University of Washington (original) (raw)
Papers by Chelsea Wood
Cite this article: Sokolow SH et al. 2017
Despite a century of research into the factors that generate and maintain biodiversity, we know r... more Despite a century of research into the factors that generate and maintain biodiversity, we know remarkably little about the drivers of parasite diversity. To identify the mechanisms governing parasite diversity, we combined surveys of 8100 amphibian hosts with an outdoor experiment that tested theory developed for free-living species. Our analyses revealed that parasite diversity increased consistently with host diversity due to habitat (i.e. host) heterogeneity, with secondary contributions from parasite colonisation and host abundance. Results of the experiment, in which host diversity was manipulated while parasite colonisation and host abundance were fixed, further reinforced this conclusion. Finally, the coefficient of host diversity on parasite diversity increased with spatial grain, which was driven by differences in their species–area curves: while host richness quickly saturated, parasite richness continued to increase with neighbourhood size. These results offer mechanistic insights into drivers of parasite diversity and provide a hierarchical framework for multi-scale disease research.
Schistosomiasis – a parasitic disease that affects over 200 million people across the globe – is ... more Schistosomiasis – a parasitic disease that affects over 200 million people across the globe – is primarily transmitted between human definitive hosts and snail intermediate hosts. To reduce schistosomiasis transmission, some have advocated disrupting the schistosome life cycle through biological control of snails, achieved by boosting the abundance of snails' natural predators. But little is known about the effect of parasitic infection on predator–prey interactions, especially in the case of schistosomiasis. Here, we present the results of laboratory experiments performed on Bulinus truncatus and Biomphalaria glabrata snails to investigate: (i) rates of predation on schistosome-infected versus uninfected snails by a sympatric native river prawn, Macrobrachium vollenhovenii, and (ii) differences in snail behavior (including movement, refuge-seeking and anti-predator behavior) between infected and uninfected snails. In predation trials, prawns showed a preference for consuming snails infected with schistosome larvae. In behavioral trials, infected snails moved less quickly and less often than uninfected snails, and were less likely to avoid predation by exiting the water or hiding under substrate. Although the mechanism by which the parasite alters snail behavior remains unknown, these results provide insight into the effects of parasitic infection on predator–prey dynamics and suggest that boosting natural rates of predation on snails may be a useful strategy for reducing transmission in schistosomiasis hotspots.
Parasites have historically been considered a scourge, deserving of annihilation. Although parasi... more Parasites have historically been considered a scourge, deserving of annihilation. Although parasite eradications rank
among humanity’s greatest achievements, new research is shedding light on the collateral effects of parasite loss.
Here, we explore a “world without parasites”: a thought experiment for illuminating the ecological roles that parasites
play in ecosystems. While there is robust evidence for the effects of parasites on host individuals (eg affecting
host vital rates), this exercise highlights how little we know about the influence of parasites on communities and
ecosystems (eg altering energy flow through food webs). We present hypotheses for novel, interesting, and general
effects of parasites. These hypotheses are largely untested, and should be considered a springboard for future
research. While many uncertainties exist, the available evidence suggests that a world without parasites would be
very different from the world we know, with effects extending from host individuals to populations, communities,
and even ecosystems.
Variability in primary productivity and fishing pressure can shape the abundance, species composi... more Variability in primary productivity and fishing pressure can shape the abundance, species composition, and diversity of marine life. Though parasites comprise nearly half of marine species, their responses to these important forces remain little explored. We quantified parasite assemblages at two spatial scales, across a gradient in productivity and fishing pressure that spans six coral islands of the Line Islands archipelago and within the largest Line Island, Kiritimati, which experiences a west-to-east gradient in fishing pressure and upwelling-driven productivity. In the across-islands data set, we found that increasing productivity was correlated with increased parasite abundance overall, but that the effects of productivity differed among parasite groups. Trophically transmitted parasites increased in abundance with increasing productivity, but directly transmitted parasites did not exhibit significant changes. This probably arises because productivity has stronger effects on the abundance of the planktonic crustaceans and herbivorous snails that serve as the intermediate hosts of trophically transmitted parasites than on the higher-trophic level fishes that are the sole hosts of directly transmitted parasites. We also found that specialist parasites increased in response to increasing productivity, while generalists did not, possibly because specialist parasites tend to be more strongly limited by host availability than are generalist parasites. After the effect of productivity was controlled for, fishing was correlated with decreases in the abundance of trophically transmitted parasites, while directly transmitted parasites appeared to track host density; we observed increases in the abundance of parasites using hosts that experienced fishing-driven compensatory increases in abundance. The within-island data set confirmed these patterns for the combined effects of productivity and fishing on parasite abundance, suggesting that our conclusions are robust across a span of spatial scales. Overall, these results indicate that there are strong and variable effects of anthropogenic and natural drivers on parasite abundance and taxonomic richness. These effects are likely to be mediated by parasite traits, particularly by parasite transmission strategies.
To understand how fisheries affect parasites, we conducted a meta-analysis of studies that contra... more To understand how fisheries affect parasites, we conducted a meta-analysis of studies that contrasted parasite assemblages
in fished and unfished areas. Parasite diversity was lower in hosts from fished areas. Larger hosts had a greater abundance of
parasites, suggesting that fishing might reduce the abundance of parasites by selectively removing the largest, most heavily
parasitized individuals. After controlling for size, the effect of fishing on parasite abundance varied according to whether the
host was fished and the parasite’s life cycle. Parasites of unfished hosts were more likely to increase in abundance in response
to fishing than were parasites of fished hosts, possibly due to compensatory increases in the abundance of unfished hosts.
While complex life cycle parasites tended to decline in abundance in response to fishing, directly transmitted parasites
tended to increase. Among complex life cycle parasites, those with fished hosts tended to decline in abundance in response to
fishing, while those with unfished hosts tended to increase. However, among directly transmitted parasites, responses did
not differ between parasites with and without fished hosts. This work suggests that parasite assemblages are likely to change
substantially in composition in increasingly fished ecosystems, and that parasite life history and fishing status of the host are
important in predicting the response of individual parasite species or groups to fishing.
The range of the sicklefin lemon shark (Negaprion acutidens) is expanded to include Palmyra Atoll... more The range of the sicklefin lemon shark (Negaprion acutidens) is expanded to include Palmyra Atoll, in the Northern Line Islands, central Pacific. Despite the fact that researchers have been studying reef and lagoon flat habitats of the Atoll since 2003, lemon sharks were first observed in 2010, suggesting a recent colonization event. To date, only juveniles and sub-adult sharks have been observed.
Despite the ubiquity and ecological importance of parasites, relatively few studies have assessed... more Despite the ubiquity and ecological importance of parasites, relatively few
studies have assessed their response to anthropogenic environmental change. Heuristic models
have predicted both increases and decreases in parasite abundance in response to human
disturbance, with empirical support for both. However, most studies focus on one or a few
selected parasite species. Here, we assess the abundance of parasites of seven species of coral
reef fishes collected from three fished and three unfished islands of the Line Islands archipelago
in the central equatorial Pacific. Because we chose fish hosts that spanned different trophic
levels, taxonomic groups, and body sizes, we were able to compare parasite responses across a
broad cross section of the total parasite community in the presence and absence of fishing, a
major human impact on marine ecosystems. We found that overall parasite species richness
was substantially depressed on fished islands, but that the response of parasite abundance
varied among parasite taxa: directly transmitted parasites were significantly more abundant on
fished than on unfished islands, while the reverse was true for trophically transmitted parasites.
This probably arises because trophically transmitted parasites require multiple host species,
some of which are the top predators most sensitive to fishing impacts. The increase in directly
transmitted parasites appeared to be due to fishing-driven compensatory increases in the
abundance of their hosts. Together, these results provide support for the predictions of both
heuristic models, and indicate that the direction of fishing’s impact on parasite abundance is
mediated by parasite traits, notably parasite transmission strategies.
Control of human infectious disease has been promoted as a valuable ecosystem service arising fro... more Control of human infectious disease has been promoted as a valuable ecosystem service arising from the conservation of biodiversity. There are two commonly discussed mechanisms by which biodiversity loss could increase rates of infectious disease in a landscape. First, loss of competitors or predators could facilitate an increase in the abundance of competent reservoir hosts. Second, biodiversity loss could disproportionately affect non-competent, or less competent reservoir hosts, which would otherwise interfere with pathogen transmission to human populations by, for example, wasting the bites of infected vectors. A negative association between biodiversity and disease risk, sometimes called the ''dilution effect hypothesis,'' has been supported for a few disease agents, suggests an exciting win–win outcome for the environment and society, and has become a pervasive topic in the disease ecology literature. Case studies have been assembled to argue that the dilution effect is general across disease agents. Less touted are examples in which elevated biodiversity does not affect or increases infectious disease risk for pathogens of public health concern. In order to assess the likely generality of the dilution effect, we review the association between biodiversity and public health across a broad variety of human disease agents. Overall, we hypothesize that conditions for the dilution effect are unlikely to be met for most important diseases of humans. Biodiversity probably has little net effect on most human infectious diseases but, when it does have an effect, observation and basic logic suggest that biodiversity will be more likely to increase than to decrease infectious disease risk.
1. Parasites comprise a substantial proportion of global biodiversity and exert important ecologi... more 1. Parasites comprise a substantial proportion of global biodiversity and exert important ecological influences on hosts, communities and ecosystems, but our knowledge of how parasite populations respond to human impacts is in its infancy. 2. Here, we present the results of a natural experiment in which we used a system of highly successful marine protected areas and matched open-access areas in central Chile to assess the influence of fishing-driven biodiversity loss on parasites of exploited fish and invertebrate hosts. We measured the burden of gill parasites for two reef fishes (Cheilodactylus variegatus and Aplodactylus punctatus), trematode parasites for a keyhole limpet (Fissurella latimarginat-a), and pinnotherid pea crab parasites for a sea urchin (Loxechinus albus). We also measured host density for all four hosts. 3. We found that nearly all parasite species exhibited substantially greater density (# parasites m À2) in protected than in open-access areas, but only one parasite species (a gill monogenean of C. variegatus) was more abundant within hosts collected from protected relative to open-access areas. 4. These data indicate that fishing can drive declines in parasite abundance at the parasite population level by reducing the availability of habitat and resources for parasites, but less commonly affects the abundance of parasites at the infrapopulation level (within individual hosts). 5. Considering the substantial ecological role that many parasites play in marine communities , fishing and other human impacts could exert cryptic but important effects on marine community structure and ecosystem functioning via reductions in parasite abundance.
Many studies have suggested that ecosystem conservation protects human and wildlife populations a... more Many studies have suggested that ecosystem conservation protects human and wildlife populations against infectious disease. We tested this hypothesis using data on primates and their parasites. First, we tested for relationships between species' resilience to human disturbance and their parasite richness, prevalence and immune defences, but found no associations. We then conducted a meta-analysis of the effects of disturbance on parasite prevalence, which revealed no overall effect, but a positive effect for one of four types of parasites (indirectly transmitted parasites). Finally, we conducted intraspecific analyses of malaria prevalence as a function of mammalian species richness in chimpanzees and gorillas, and an interspecific analysis of geographic overlap and parasite species richness, finding that higher levels of host richness favoured greater parasite risk. These results suggest that anthropogenic effects on disease transmission are complex, and highlight the need to define the conditions under which environmental change will increase or decrease disease transmission.
Recent reviews have argued that disease control is among the ecosystem services yielded by biodiv... more Recent reviews have argued that disease control is
among the ecosystem services yielded by biodiversity.
Lyme disease (LD) is commonly cited as the best example
of the ‘diluting’ effect of biodiversity on disease
transmission, but many studies document the opposite
relationship, showing that human LD risk can increase
with forestation. Here, we unify these divergent perspectives
and find strong evidence for a positive link between
biodiversity and LD at broad spatial scales (urban to
suburban to rural) and equivocal evidence for a negative
link between biodiversity and LD at varying levels of
biodiversity within forests. This finding suggests that,
across zoonotic disease agents, the biodiversity–disease
relationship is scale dependent and complex.
Cite this article: Sokolow SH et al. 2017
Despite a century of research into the factors that generate and maintain biodiversity, we know r... more Despite a century of research into the factors that generate and maintain biodiversity, we know remarkably little about the drivers of parasite diversity. To identify the mechanisms governing parasite diversity, we combined surveys of 8100 amphibian hosts with an outdoor experiment that tested theory developed for free-living species. Our analyses revealed that parasite diversity increased consistently with host diversity due to habitat (i.e. host) heterogeneity, with secondary contributions from parasite colonisation and host abundance. Results of the experiment, in which host diversity was manipulated while parasite colonisation and host abundance were fixed, further reinforced this conclusion. Finally, the coefficient of host diversity on parasite diversity increased with spatial grain, which was driven by differences in their species–area curves: while host richness quickly saturated, parasite richness continued to increase with neighbourhood size. These results offer mechanistic insights into drivers of parasite diversity and provide a hierarchical framework for multi-scale disease research.
Schistosomiasis – a parasitic disease that affects over 200 million people across the globe – is ... more Schistosomiasis – a parasitic disease that affects over 200 million people across the globe – is primarily transmitted between human definitive hosts and snail intermediate hosts. To reduce schistosomiasis transmission, some have advocated disrupting the schistosome life cycle through biological control of snails, achieved by boosting the abundance of snails' natural predators. But little is known about the effect of parasitic infection on predator–prey interactions, especially in the case of schistosomiasis. Here, we present the results of laboratory experiments performed on Bulinus truncatus and Biomphalaria glabrata snails to investigate: (i) rates of predation on schistosome-infected versus uninfected snails by a sympatric native river prawn, Macrobrachium vollenhovenii, and (ii) differences in snail behavior (including movement, refuge-seeking and anti-predator behavior) between infected and uninfected snails. In predation trials, prawns showed a preference for consuming snails infected with schistosome larvae. In behavioral trials, infected snails moved less quickly and less often than uninfected snails, and were less likely to avoid predation by exiting the water or hiding under substrate. Although the mechanism by which the parasite alters snail behavior remains unknown, these results provide insight into the effects of parasitic infection on predator–prey dynamics and suggest that boosting natural rates of predation on snails may be a useful strategy for reducing transmission in schistosomiasis hotspots.
Parasites have historically been considered a scourge, deserving of annihilation. Although parasi... more Parasites have historically been considered a scourge, deserving of annihilation. Although parasite eradications rank
among humanity’s greatest achievements, new research is shedding light on the collateral effects of parasite loss.
Here, we explore a “world without parasites”: a thought experiment for illuminating the ecological roles that parasites
play in ecosystems. While there is robust evidence for the effects of parasites on host individuals (eg affecting
host vital rates), this exercise highlights how little we know about the influence of parasites on communities and
ecosystems (eg altering energy flow through food webs). We present hypotheses for novel, interesting, and general
effects of parasites. These hypotheses are largely untested, and should be considered a springboard for future
research. While many uncertainties exist, the available evidence suggests that a world without parasites would be
very different from the world we know, with effects extending from host individuals to populations, communities,
and even ecosystems.
Variability in primary productivity and fishing pressure can shape the abundance, species composi... more Variability in primary productivity and fishing pressure can shape the abundance, species composition, and diversity of marine life. Though parasites comprise nearly half of marine species, their responses to these important forces remain little explored. We quantified parasite assemblages at two spatial scales, across a gradient in productivity and fishing pressure that spans six coral islands of the Line Islands archipelago and within the largest Line Island, Kiritimati, which experiences a west-to-east gradient in fishing pressure and upwelling-driven productivity. In the across-islands data set, we found that increasing productivity was correlated with increased parasite abundance overall, but that the effects of productivity differed among parasite groups. Trophically transmitted parasites increased in abundance with increasing productivity, but directly transmitted parasites did not exhibit significant changes. This probably arises because productivity has stronger effects on the abundance of the planktonic crustaceans and herbivorous snails that serve as the intermediate hosts of trophically transmitted parasites than on the higher-trophic level fishes that are the sole hosts of directly transmitted parasites. We also found that specialist parasites increased in response to increasing productivity, while generalists did not, possibly because specialist parasites tend to be more strongly limited by host availability than are generalist parasites. After the effect of productivity was controlled for, fishing was correlated with decreases in the abundance of trophically transmitted parasites, while directly transmitted parasites appeared to track host density; we observed increases in the abundance of parasites using hosts that experienced fishing-driven compensatory increases in abundance. The within-island data set confirmed these patterns for the combined effects of productivity and fishing on parasite abundance, suggesting that our conclusions are robust across a span of spatial scales. Overall, these results indicate that there are strong and variable effects of anthropogenic and natural drivers on parasite abundance and taxonomic richness. These effects are likely to be mediated by parasite traits, particularly by parasite transmission strategies.
To understand how fisheries affect parasites, we conducted a meta-analysis of studies that contra... more To understand how fisheries affect parasites, we conducted a meta-analysis of studies that contrasted parasite assemblages
in fished and unfished areas. Parasite diversity was lower in hosts from fished areas. Larger hosts had a greater abundance of
parasites, suggesting that fishing might reduce the abundance of parasites by selectively removing the largest, most heavily
parasitized individuals. After controlling for size, the effect of fishing on parasite abundance varied according to whether the
host was fished and the parasite’s life cycle. Parasites of unfished hosts were more likely to increase in abundance in response
to fishing than were parasites of fished hosts, possibly due to compensatory increases in the abundance of unfished hosts.
While complex life cycle parasites tended to decline in abundance in response to fishing, directly transmitted parasites
tended to increase. Among complex life cycle parasites, those with fished hosts tended to decline in abundance in response to
fishing, while those with unfished hosts tended to increase. However, among directly transmitted parasites, responses did
not differ between parasites with and without fished hosts. This work suggests that parasite assemblages are likely to change
substantially in composition in increasingly fished ecosystems, and that parasite life history and fishing status of the host are
important in predicting the response of individual parasite species or groups to fishing.
The range of the sicklefin lemon shark (Negaprion acutidens) is expanded to include Palmyra Atoll... more The range of the sicklefin lemon shark (Negaprion acutidens) is expanded to include Palmyra Atoll, in the Northern Line Islands, central Pacific. Despite the fact that researchers have been studying reef and lagoon flat habitats of the Atoll since 2003, lemon sharks were first observed in 2010, suggesting a recent colonization event. To date, only juveniles and sub-adult sharks have been observed.
Despite the ubiquity and ecological importance of parasites, relatively few studies have assessed... more Despite the ubiquity and ecological importance of parasites, relatively few
studies have assessed their response to anthropogenic environmental change. Heuristic models
have predicted both increases and decreases in parasite abundance in response to human
disturbance, with empirical support for both. However, most studies focus on one or a few
selected parasite species. Here, we assess the abundance of parasites of seven species of coral
reef fishes collected from three fished and three unfished islands of the Line Islands archipelago
in the central equatorial Pacific. Because we chose fish hosts that spanned different trophic
levels, taxonomic groups, and body sizes, we were able to compare parasite responses across a
broad cross section of the total parasite community in the presence and absence of fishing, a
major human impact on marine ecosystems. We found that overall parasite species richness
was substantially depressed on fished islands, but that the response of parasite abundance
varied among parasite taxa: directly transmitted parasites were significantly more abundant on
fished than on unfished islands, while the reverse was true for trophically transmitted parasites.
This probably arises because trophically transmitted parasites require multiple host species,
some of which are the top predators most sensitive to fishing impacts. The increase in directly
transmitted parasites appeared to be due to fishing-driven compensatory increases in the
abundance of their hosts. Together, these results provide support for the predictions of both
heuristic models, and indicate that the direction of fishing’s impact on parasite abundance is
mediated by parasite traits, notably parasite transmission strategies.
Control of human infectious disease has been promoted as a valuable ecosystem service arising fro... more Control of human infectious disease has been promoted as a valuable ecosystem service arising from the conservation of biodiversity. There are two commonly discussed mechanisms by which biodiversity loss could increase rates of infectious disease in a landscape. First, loss of competitors or predators could facilitate an increase in the abundance of competent reservoir hosts. Second, biodiversity loss could disproportionately affect non-competent, or less competent reservoir hosts, which would otherwise interfere with pathogen transmission to human populations by, for example, wasting the bites of infected vectors. A negative association between biodiversity and disease risk, sometimes called the ''dilution effect hypothesis,'' has been supported for a few disease agents, suggests an exciting win–win outcome for the environment and society, and has become a pervasive topic in the disease ecology literature. Case studies have been assembled to argue that the dilution effect is general across disease agents. Less touted are examples in which elevated biodiversity does not affect or increases infectious disease risk for pathogens of public health concern. In order to assess the likely generality of the dilution effect, we review the association between biodiversity and public health across a broad variety of human disease agents. Overall, we hypothesize that conditions for the dilution effect are unlikely to be met for most important diseases of humans. Biodiversity probably has little net effect on most human infectious diseases but, when it does have an effect, observation and basic logic suggest that biodiversity will be more likely to increase than to decrease infectious disease risk.
1. Parasites comprise a substantial proportion of global biodiversity and exert important ecologi... more 1. Parasites comprise a substantial proportion of global biodiversity and exert important ecological influences on hosts, communities and ecosystems, but our knowledge of how parasite populations respond to human impacts is in its infancy. 2. Here, we present the results of a natural experiment in which we used a system of highly successful marine protected areas and matched open-access areas in central Chile to assess the influence of fishing-driven biodiversity loss on parasites of exploited fish and invertebrate hosts. We measured the burden of gill parasites for two reef fishes (Cheilodactylus variegatus and Aplodactylus punctatus), trematode parasites for a keyhole limpet (Fissurella latimarginat-a), and pinnotherid pea crab parasites for a sea urchin (Loxechinus albus). We also measured host density for all four hosts. 3. We found that nearly all parasite species exhibited substantially greater density (# parasites m À2) in protected than in open-access areas, but only one parasite species (a gill monogenean of C. variegatus) was more abundant within hosts collected from protected relative to open-access areas. 4. These data indicate that fishing can drive declines in parasite abundance at the parasite population level by reducing the availability of habitat and resources for parasites, but less commonly affects the abundance of parasites at the infrapopulation level (within individual hosts). 5. Considering the substantial ecological role that many parasites play in marine communities , fishing and other human impacts could exert cryptic but important effects on marine community structure and ecosystem functioning via reductions in parasite abundance.
Many studies have suggested that ecosystem conservation protects human and wildlife populations a... more Many studies have suggested that ecosystem conservation protects human and wildlife populations against infectious disease. We tested this hypothesis using data on primates and their parasites. First, we tested for relationships between species' resilience to human disturbance and their parasite richness, prevalence and immune defences, but found no associations. We then conducted a meta-analysis of the effects of disturbance on parasite prevalence, which revealed no overall effect, but a positive effect for one of four types of parasites (indirectly transmitted parasites). Finally, we conducted intraspecific analyses of malaria prevalence as a function of mammalian species richness in chimpanzees and gorillas, and an interspecific analysis of geographic overlap and parasite species richness, finding that higher levels of host richness favoured greater parasite risk. These results suggest that anthropogenic effects on disease transmission are complex, and highlight the need to define the conditions under which environmental change will increase or decrease disease transmission.
Recent reviews have argued that disease control is among the ecosystem services yielded by biodiv... more Recent reviews have argued that disease control is
among the ecosystem services yielded by biodiversity.
Lyme disease (LD) is commonly cited as the best example
of the ‘diluting’ effect of biodiversity on disease
transmission, but many studies document the opposite
relationship, showing that human LD risk can increase
with forestation. Here, we unify these divergent perspectives
and find strong evidence for a positive link between
biodiversity and LD at broad spatial scales (urban to
suburban to rural) and equivocal evidence for a negative
link between biodiversity and LD at varying levels of
biodiversity within forests. This finding suggests that,
across zoonotic disease agents, the biodiversity–disease
relationship is scale dependent and complex.