Download Food for Thought Parasitic infection: a missing piece of the ocean

ICES Journal of Marine Science (2017), 74(4), 929–933. doi:10.1093/icesjms/fsw156
Contribution to Special Issue: ‘Towards a Broader Perspective on Ocean Acidification Research Part 2’
Food for Thought
Parasitic infection: a missing piece of the ocean
acidification puzzle
Colin D. MacLeod
Department of Zoology, University of Otago, PO Box 56, Dunedin 9054, New Zealand
Corresponding author: tel: þ64 3 471 6146; e-mail: [email protected]
MacLeod, C. D. Parasitic infection: a missing piece of the ocean acidification puzzle. – ICES Journal of Marine Science, 74: 929–933.
Received 30 May 2016; revised 19 August 2016; accepted 20 August 2016; advance access publication 8 September 2016.
Ocean acidification (OA) research has matured into a sophisticated experimental and theoretical scientific discipline, which now utilizes multiple stressor, mesocosm experiments, and mathematical simulation models to predict the near-future effects of continued acidification on
marine ecosystems. These advanced methodological approaches to OA research also include the study of inter-specific interactions that could
be disrupted if participant species exhibit differential tolerances to stressors associated with OA. The host-parasite relationship is one of the
most fundamental ecological interactions, alongside competition and predation, which can regulate individuals, populations, and communities. The recent integration of competition and predation into OA research has provided great insight into the potential effects of differential
tolerances to acidified seawater, and there is no reason to believe that expanding OA research to include parasitology will be less fruitful. This
essay outlines our current, limited understanding of how OA will affect parasitism as an ecological process, describes potential pitfalls for researchers who ignore parasites and the effects of infection, and suggests ways of developing parasitology as a sub-field of OA research.
Keywords: confounding factor, gastropod, marine ecology, ocean acidification, parasitic infection, trematode.
Introduction
The trajectory of ocean acidification (OA) research shares many
similarities with other marine ecology disciplines that emerged in
response to large-scale disturbances to the ocean’s abiotic environment caused by human activity, e.g. ocean warming, hypoxic
dead zones, and elevated nutrient input (Keeling et al., 2010;
Doney et al., 2012). First, the global decrease in seawater pH was
identified and quantified (Caldeira and Wickett, 2003), then
acknowledged by the marine research community (Doney et al.,
2009). This was followed by an increase in the number of singlefactor, single-species experiments designed to test the biological
effects of stressors associated with OA, i.e. reduced pH, increased
bicarbonate ion concentration, and decreased carbonate ion concentration (see review in Kroeker et al., 2013), before additional
abiotic and biotic variables were added to experimental design
(e.g. Ferrari et al., 2015). Eventually, empirical data was incorporated into ecological simulation models to predict the effects of
continued change to the abiotic environment (Queir
os et al.,
2015). Throughout the research trajectory of OA and other
marine ecology disciplines, metazoan and protozoan parasites
have been largely overlooked (MacLeod and Poulin, 2012;
Kroeker et al., 2014; Gaylord et al., 2015; Reusch, 2016), possibly
due to their small size, which leads to the erroneous assumption
that their influence must also be small (Marcogliese and Cone,
1997; Kuris et al., 2008), or due to the paucity of marine ecologists who integrate parasitology into their research (Poulin et al.,
2016). In either case, this is a remarkable oversight, as 30–50% of
known species are categorized as parasitic (De Mee^
us and
Renaud, 2002), parasites make up a large component of the total
biomass in many coastal ecosystems (Kuris et al., 2008), and
parasite species are simultaneously apex predators, prey, and
competitors (Thieltges et al., 2013). Parasitic infection can dramatically modify the fitness, behaviour, physiology, survival, and
fecundity of infected individuals, and regulate population-, community-, and ecosystem-level processes (Mouritsen and Poulin,
2002; Lefèvre et al., 2009; Hatcher et al., 2012). Parasitic infection
can also affect the aquaculture and fishing industries by reducing
the market value of commercial species (Perdiguero-Alonso et al.,
C International Council for the Exploration of the Sea 2016. All rights reserved.
V
For Permissions, please email: [email protected]
930
2008) and altering recruitment rates of juveniles into commercially valuable populations (Shinn et al., 2015). Needless to say,
when parasitology is finally incorporated into novel research
areas, such as global warming, it offers valuable insight into the
effects of abiotic change in marine systems, e.g. increased prevalence and virulence of pre-existing diseases (Harvell, 1999). I
hope that this essay will encourage the rapid integration of parasitology in OA research, and initiate a productive dialogue between parasitologists and marine ecologists, as reduced seawater
pH is one of the most significant changes to the abiotic marine
environment that has occurred in the past two million years
(Honisch et al., 2012).
As with competitive and predator–prey interactions, the relationship between parasite and host is an arms race, in which the
end result is decided by the relative fitness of participant species
(Haraguchi and Sasaki, 1996). Even small changes in abiotic conditions can gradually affect the fitness of an individual and disrupt the expected outcome of these encounters, e.g.
compromised host defences against infection (Studer et al.,
2012), impaired predator evasion (Chivers et al., 2014), and a
decreased ability to absorb nutrients (Dutkiewicz et al., 2015).
Given the rapid changes to seawater chemistry caused by human
activity, it is highly likely that sympatric marine species will exhibit differential tolerances which could disturb stable community dynamics through altered inter-specific interaction, such as
those that exist between host and parasite (Mouritsen and Poulin,
2002).
To date, OA-parasite research has focussed on trematode parasites (MacLeod and Poulin, 2015b; Guilloteau et al., 2016) and
their interaction with gastropod hosts (Harland et al., 2015, 2016;
MacLeod and Poulin, 2015a, 2016a,b), although some research
has examined the immune response of gastropod and bivalve species exposed to simulated OA (Mackenzie, 1999; Bibby et al.,
2008; Ellis et al., 2015; Keppel et al., 2015). A search of the Web
of Science database using the keywords “OA AND parasit*” to
the end of 2013 returned only seven publications, the first of
which appeared in 2011 (Poulin et al., 2016); extending this
search to the end of 2015 finds another seven publications. Of
these, less than half are research articles, with the majority coming
from the Evolutionary and Ecological Parasitology Research
Group at the University of Otago, New Zealand, which often uses
gastropod hosts and trematode parasites in ecological studies.
Consequently, most of the examples used in this essay are from
trematode-gastropod systems, but it is critically important to
understand that there are other major parasitic taxa, e.g. nematodes, cestodes, acanthocephalans, crustaceans, and myxozoans,
that must ultimately be incorporated into OA research.
The direct effects of OA on parasites
Here, I define the direct effects of OA as those that occur when an
organism comes into immediate contact with high CO2 seawater.
In the context of parasites, this includes free-swimming transmission stages, cysts or eggs, and ectoparasites. From this perspective,
parasites that are directly affected by exposure to high CO2 seawater are not substantively different from non-parasitic marine
meiofauna, or the early developmental stages of larger marine organisms, which have been studied extensively over the past 10–15
years (see review in Kroeker et al., 2013). As such, parasites
exposed to acidified seawater are challenged by the same predominant physiological stressors as non-parasitic organisms, i.e.
C. D. MacLeod
increased metabolic costs of ionoregulation and calcification. As
the effects of simulated OA on non-parasitic organisms is generally negative, it is no surprise that exposure to high CO2 seawater
reduces the survival of free-swimming trematode larvae (cercariae) and external cysts (metacercariae) (MacLeod and Poulin,
2015b; Guilloteau et al., 2016). The reduced survival of transmission stages may decrease parasite prevalence, as the probability of
finding and successfully infecting an appropriate host will also be
decreased. Changes in parasite prevalence could alter the regulatory effect of parasites on host populations, and cause a shift
away from a previously stable state by altering host fecundity and
behaviour, and, subsequently, modifying the host’s ecological role
(Labaude et al., 2015). Some coastal habitats have a very high
prevalence of castrating parasites (Lafferty and Kuris, 2009) which
limit the fecundity of the host population (Gilardoni et al., 2012).
If parasite prevalence was reduced in these systems by changing
abiotic conditions, the reproductive output of host populations
could increase and alter the host species’ role as competitor or
predator. Similarly, many species of parasite alter the behaviour
of infected individuals, such that the latter are more likely to be
predated upon by the next host in the parasite’s life-cycle
(Thomas et al., 1998). Consequently, reduced parasite prevalence
could cause a decrease in food availability for the predator species
and increase the survival rates of the host species (Sato et al.,
2011; Labaude et al., 2015). Of course, we cannot begin to predict
changes to parasite prevalence until more trials investigate how
host susceptibility to infection is altered by exposure to high CO2
seawater. To my knowledge, only five such articles have been
published to date, and they show no consistent pattern in host response: two tested the immune function parameters of mussels
(Mytilus edulis) as a proxy for susceptibility to bacterial infection
(Bibby et al., 2008; Mackenzie et al., 2014); Ellis et al. (2015)
tested the immune response of M. edulis exposed to bacteria
(Vibrio tubiashii); Harland et al. (2015) recorded the infection
rates of amphipods (Paracalliope novizealandiae) exposed to
trematode infection (Maritrema novaezealandensis); and Keppel
et al. (2015) recorded the acquisition and progression of protistan
infections (Perkinsus marinus) by the eastern oyster (Crassostrea
virginica).This lack of conclusive data to describe the effect of OA
on host susceptibility to infection should be urgently addressed,
as increased infection rates, particularly of parasitic species that
alter host fecundity, could have dramatic consequences for ecologically or commercially important species.
A second important effect of high CO2-mediated mortality of
the free-living stages of parasites is a reduction in the availability
of food to non-host organisms that prey on the parasite. Freeswimming parasite larvae, such as cercariae, make up a substantial proportion of the zooplankton component of many food
chains (Thieltges et al., 2013). If high CO2-mediated mortality removes a significant proportion of free-living parasite life stages
from marine food webs, there could be major consequences for
the dynamics, structure, and resilience of trophic networks
(Poulin et al., 2013). In addition, differential mortality of the
free-living stages of parasite species that compete for the same
host could alter the competitive interactions between sympatric
parasite populations, altering the prevalence of the less tolerant
species. Clearly, the direct effects described above all have the potential to significantly decrease the established ecological role of
parasites and alter community structure either through reduced
parasite prevalence or abundance.
931
A missing piece of the OA puzzle
The interactive effects of OA and infection stress
The confounding effects of parasitic infection
Despite their disparate origins, stressors associated with both OA
and parasitic infection affect host organisms in fundamentally
similar ways, increasing the likelihood that, in combination, they
will have synergistic or additive effects. Exposure to high CO2 seawater increases the energy required to fuel ionoregulatory mechanisms or biomineralisation (Kelly and Hofmann, 2013; Pan
et al., 2015), while infection increases the metabolic demands of
the host as it supplies energy to the parasite in addition to meeting its own energetic requirements. Parasitic infection and exposure to acidified seawater alter the biogenesis of calcium carbonate
structures by shell-forming species, e.g. shell growth rates (OA,
Coleman et al., 2014; infection, Probst and Kube, 1999) and
morphology (OA, Bibby et al., 2007; infection, Hay et al., 2005).
For instance, parasitic infection has already been shown to alter
the calcifying and physiological ability of infected gastropods
exposed to acidified seawater (MacLeod and Poulin, 2015a,
2016a). Furthermore, both exposure to high CO2 seawater and
parasitic infection can independently alter the behaviour of infected individuals, e.g. inhibited neurological function (OA,
Hamilton et al., 2013; infection, Shaw et al., 2009).
We must acknowledge, however, that below a certain pH
value, the internal fluids of host organisms may become acidified, as the ionoregulatory ability of the host organism is overwhelmed (Reipschl€ager and Pörtner, 1996). Beyond that point,
the endoparasites are directly exposed to an acidified environment, albeit acidified extracellular fluid rather than acidified
seawater. Consequently, we must return to the criteria defined
above for direct exposure to acidified conditions to evaluate the
endoparasite’s response, but with the understanding that any
adverse effects on the parasite will also affect the host organism
from within. In this scenario, endoparasites, stressed by an
acidified micro-environment, would increase their metabolic
energy consumption and cause a corresponding increase in the
energy requirements of the host. The host organisms would
then have to adapt to a greater overall energy budget or, if this
were not possible, experience a gradual decline in energy stores
as demand outpaced supply, ultimately leading to mortality.
Beyond changes to energy transfer between host and parasite,
direct exposure to acidified conditions may elicit the same response in endoparasites as was found in the free-living infective
stages, i.e. reduced survival. Only one study has investigated the
effects of exposure to high CO2 seawater on endoparasites; it
found that exposure of the gastropod hosts (Austrolittorina
cincta and Zeacumantus subcarinatus) to acidified conditions
caused significant increases in the reproductive output of trematode parasites (Parorchis sp. and Philophthalmus sp.)
(Guilloteau et al., 2016). It remains to be determined whether
these changes are due to altered energy budgets of infected organisms exposed to acidified seawater or the exposure of endoparasites to acidified host fluids. Although more research is
required, it is clear that the interaction of OA and infection
stress has the potential to have wide-ranging consequences in
the marine environment by altering the effect of parasitic infection on host organisms. As described in the “Introduction” section, parasitic infection can modify the survival, fecundity,
physiology, and behaviour of the host, and any OA-mediated
changes to these effects would likely alter the ecological role of
host populations.
Thus far, I have focussed on the few studies that investigated the
effects of exposure to high CO2 seawater on host-parasite associations, and the importance of this research with regards to understanding how marine ecosystems will respond to continued
acidification. However, the results of these studies also have extremely important implications for broader OA research. If parasitic infection can significantly alter the response of host
organisms to a high CO2 environment, it has the potential to confound the results of OA experiments where infection was not considered. This is a crucial point, as one of the major goals of OA
research is to quantify the tolerance of ecologically and commercially important species, in order to predict future changes to
marine biodiversity and identify potentially negative effects on
the aquaculture and fishing industries (Kroeker et al., 2013).
To date, two publications have examined the effects of infection on the overall response of host organisms exposed to high
CO2 seawater. MacLeod and Poulin (2016a) reported significant
effects of both infection status and pH on the tissue glucose concentration of four groups of snails: uninfected, and infected with
one of three trematode species. However, the analysis of pooled
data, i.e. the response of all snails regardless of infection status,
failed to detect the significant effect of pH. Similarly, MacLeod
and Poulin (2016b) showed that only the survival of uninfected
snails was significantly affected by exposure to acidified seawater,
and again found that the significant effect of pH was no longer
detectable when data from infected and uninfected individuals
was pooled. Both studies collected snails from a site of naturally
high parasite prevalence (>85%, Fredensborg et al., 2005); had
the experimental organisms not been screened for infection, they
would have been mistakenly categorized as tolerant of high CO2
conditions, when, in fact, this response was an artefact of infection. These two studies clearly illustrate the dangers of ignoring
the presence of parasites when conducting OA research, as the effects of infection were central to demonstrating that the host species was negatively affected by exposure to acidified seawater. In
both cases, if infection had not been included in the analysis, the
true response of the host species, i.e. the response of uninfected
individuals, would have been masked by the confounding effects
of the parasites.
Integrating parasitology into OA research
Primarily, the effects of parasitic infection on organisms exposed
to simulated OA should be investigated in greater depth and with
a more phylogenetically diverse range of parasite species. Given
the potential for endoparasites to alter the behaviour and fitness
of host species if they become exposed to an acidified microenvironment, further study is also required to investigate the effects of
acidification on the extracellular fluids of vertebrate and invertebrate hosts, particularly those with limited ionoregulatory capacity. One of the main challenges in parasitological research is
maintaining a complete parasite life-cycle under controlled lab
conditions, and such a model system is urgently required to study
the effects of high CO2 seawater on every stage of the parasite’s
life-cycle. Screening for parasites should become a standard operating procedure in experimental OA research, as the confounding
effects of infection could dilute the strength of an OA signal even
in systems with low parasite prevalence. Parasites should also be
included in all long-term ecological monitoring programmes to
932
conclusively establish if prevalence does change with the gradual
acidification of seawater.
Conclusion
Although research that supports the importance of parasitism in
an acidifying ocean is still extremely sparse, it strongly suggests
that the hidden effects of infection could change our understanding of how OA will affect many marine species. This research also
further demonstrates that inter-specific interactions, in this case
host-parasite associations, can influence the ecological effects of
changing abiotic conditions. To date, the host and parasite species used in OA research have been of ecological importance only,
so the possible implications for the aquaculture and fishing
industries are completely unknown. Given that the parasite component of many important marine ecosystems remains systemically understudied (Poulin et al., 2016), it is extremely unwise to
ignore the presence of parasites if our objective as OA researchers
is to fully elucidate the future effects of continued acidification.
Acknowledgements
I would like to thank three anonymous reviewers, Howard
Browman, and Robert Poulin for constructive comments on an
earlier draft of this essay.
References
Bibby, R., Cleall-Harding, P., Rundle, S., Widdicombe, S., and Spicer,
J. 2007. Ocean acidification disrupts induced defences in the
intertidal gastropod Littorina littorea. Biology Letters, 3: 699–701.
Bibby, R., Widdicombe, S., Parry, H., Spicer, J., and Pipe, R. 2008.
Effects of ocean acidification on the immune response of the blue
mussel Mytilus edulis. Aquatic Biology, 2: 67–74.
Caldeira, K., and Wickett, M. E. 2003. Oceanography: Anthropogenic
carbon and ocean pH. Nature, 425: 365365.
Chivers, D. P., McCormick, M. I., Nilsson, G. E., Munday, P. L.,
Watson, S. A., Meekan, M. G., Mitchell, M. D. et al. 2014.
Impaired learning of predators and lower prey survival under elevated CO2: a consequence of neurotransmitter interference.
Global Change Biology, 20: 515–522.
Coleman, D., Byrne, M., and Davis, A. 2014. Molluscs on acid:
gastropod shell repair and strength in acidifying oceans. Marine
Ecology Progress Series, 509: 203–211.
De Mee^
us, T., and Renaud, F. 2002. Parasites within the new phylogeny of eukaryotes. Trends in Parasitology, 18: 247–251.
Doney, S. C., Fabry, V. J., Feely, R. A., and Kleypas, J. A. 2009. Ocean
acidification: the other CO2 problem. Annual Review of Marine
Science, 1: 169–192.
Doney, S. C., Ruckelshaus, M., Emmett Duffy, J., Barry, J. P., Chan,
F., English, C. A., Galindo, H. M. et al. 2012. Climate change impacts on marine ecosystems. Annual Review of Marine Science, 4:
11–37.
Dutkiewicz, S., Morris, J. J., Follows, M. J., Scott, J., Levitan, O.,
Dyhrman, S. T., and Berman-Frank, I. 2015. Impact of ocean
acidification on the structure of future phytoplankton communities. Nature Climate Change, 5: 1002–1006.
Ellis, R. P., Widdicombe, S., Parry, H., Hutchinson, T. H., and
Spicer, J. I. 2015. Pathogenic challenge reveals immune trade-off
in mussels exposed to reduced seawater pH and increased temperature. Journal of Experimental Marine Biology and Ecology,
462: 83–89.
Ferrari, M. C. O., Munday, P. L., Rummer, J. L., McCormick, M. I.,
Corkill, K., Watson, S. A., Allan, B. J. M. et al. 2015. Interactive effects of ocean acidification and rising sea temperatures alter predation rate and predator selectivity in reef fish communities.
Global Change Biology, 21: 1848–1855.
C. D. MacLeod
Fredensborg, B. L., Mouritsen, K. N., and Poulin, R. 2005. Impact of
trematodes on host survival and population density in the intertidal gastropod Zeacumantus subcarinatus. Marine Ecology
Progress Series, 290: 109–117.
Gaylord, B., Kroeker, K. J., Sunday, J. M., Anderson, K. M., Barry, J.
P., Brown, N. E., Connell, S. D. et al. 2015. Ocean acidification
through the lens of ecological theory. Ecology, 96: 3–15.
Gilardoni, C., Ituarte, C., and Cremonte, F. 2012. Castrating effects of
trematode larvae on the reproductive success of a highly parasitized population of Crepipatella dilatata (Caenogastropoda) in
Argentina. Marine Biology, 159: 2259–2267.
Guilloteau, P., Poulin, R., and MacLeod, C. D. 2016. Impacts of
ocean acidification on multiplication and caste organisation
of parasitic trematodes in their gastropod host. Marine Biology,
163: 96.
Hamilton, T. J., Holcombe, A., and Tresguerres, M. 2013. CO2induced ocean acidification increases anxiety in Rockfish via alteration of GABAA receptor functioning. Proceedings of the Royal
Society B: Biological Sciences, 281: 20132509–20132509.
Haraguchi, Y., and Sasaki, A. 1996. Host–parasite arms race in mutation modifications: indefinite escalation despite a heavy load?.
Journal of Theoretical Biology, 183: 121–137.
Harland, H., MacLeod, C. D., and Poulin, R. 2016. Lack of genetic
variation in the response of a trematode parasite to ocean acidification. Marine Biology, 163: 1.
Harland, H., MacLeod, C., and Poulin, R. 2015. Non-linear effects of
ocean acidification on the transmission of a marine intertidal
parasite. Marine Ecology Progress Series, 536: 55–64.
Harvell, C. D. 1999. Emerging marine diseases–climate links and anthropogenic factors. Science, 285: 1505–1510.
Hatcher, M. J., Dick, J. T., and Dunn, A. M. 2012. Diverse effects of
parasites in ecosystems: linking interdependent processes.
Frontiers in Ecology and the Environment, 10: 186–194.
Hay, K. B., Fredensborg, B. L., and Poulin, R. 2005. Trematodeinduced alterations in shell shape of the mud snail Zeacumantus
subcarinatus (Prosobranchia: Batillariidae). Journal of the Marine
Biological Association of the United Kingdom, 85: 989–992.
Honisch, B., Ridgwell, A., Schmidt, D. N., Thomas, E., Gibbs, S. J.,
Sluijs, A., Zeebe, R. et al. 2012. The geological record of ocean
acidification. Science, 335: 1058–1063.
Keeling, R. F., Körtzinger, A., and Gruber, N. 2010. Ocean
Deoxygenation in a Warming World. Annual Review of Marine
Science, 2: 199–229.
Kelly, M. W., and Hofmann, G. E. 2013. Adaptation and the physiology of ocean acidification. Functional Ecology, 27: 980–990.
Keppel, A., Breitburg, D., Wikfors, G., Burrell, R., and Clark, V. 2015.
Effects of co-varying diel-cycling hypoxia and pH on disease susceptibility in the eastern oyster Crassostrea virginica. Marine
Ecology Progress Series, 538: 169–183.
Kroeker, K. J., Kordas, R. L., Crim, R., Hendriks, I. E., Ramajo, L.,
Singh, G. S., Duarte, C. M. et al. 2013. Impacts of ocean acidification on marine organisms: quantifying sensitivities and interaction with warming. Global Change Biology, 19: 1884–1896.
Kroeker, K. J., Sanford, E., Jellison, B. M., and Gaylord, B. 2014.
Predicting the effects of ocean acidification on predator-prey
interactions: a conceptual framework based on Coastal Molluscs.
The Biological Bulletin, 226: 211–222.
Kuris, A. M., Hechinger, R. F., Shaw, J. C., Whitney, K. L., AguirreMacedo, L., Boch, C. A., Dobson, A. P. et al. 2008. Ecosystem energetic implications of parasite and free-living biomass in three
estuaries. Nature, 454: 515–518.
Labaude, S., Rigaud, T., and Cézilly, F. 2015. Host manipulation in
the face of environmental changes: Ecological consequences.
International Journal for Parasitology: Parasites and Wildlife, 4:
442–451.
A missing piece of the OA puzzle
Lafferty, K. D., and Kuris, A. M. 2009. Parasitic castration: the evolution and ecology of body snatchers. Trends in Parasitology, 25:
564–572.
Lefèvre, T., Lebarbenchon, C., Gauthier-Clerc, M., Missé, D., Poulin,
R., and Thomas, F. 2009. The ecological significance of manipulative parasites. Trends in Ecology and Evolution, 24: 41–48.
Mackenzie, C. L., Lynch, S. A., Culloty, S. C., and Malham, S. K.
2014. Future oceanic warming and acidification alter immune response and disease status in a commercial shellfish species,
Mytilus edulis L. PLoS One, 9: e99712.
Mackenzie, K. 1999. Parasites as pollution indicators in marine ecosystems: a proposed early warning system. Marine Pollution
Bulletin, 38: 955–959.
MacLeod, C. D., and Poulin, R. 2012. Host–parasite interactions: a
litmus test for ocean acidification? Trends in Parasitology, 28:
365–369.
MacLeod, C. D., and Poulin, R. 2015a. Interactive effects of parasitic
infection and ocean acidification on the calcification of a marine
gastropod. Marine Ecology-Progress Series, 537: 137–150.
MacLeod, C. D., and Poulin, R. 2015b. Differential tolerances to
ocean acidification by parasites that share the same host.
International Journal for Parasitology, 45: 485–493.
MacLeod, C. D., and Poulin, R. 2016a. Parasitic infection alters the
physiological response of a marine gastropod to ocean acidification. Parasitology, 143: 1397–1408.
MacLeod, C. D., and Poulin, R. 2016b. Parasitic infection: a buffer
against ocean acidification? Biology Letters, 12: 20160007.
Marcogliese, D. J., and Cone, D. K. 1997. Food webs: a plea for parasites. Trends in Ecology and Evolution, 12: 320–325.
Mouritsen, K. N., and Poulin, R. 2002. Parasitism, climate oscillations and the structure of natural communities. Oikos, 97:
462–468.
Pan, T. C. F., Applebaum, S. L., and Manahan, D. T. 2015.
Experimental ocean acidification alters the allocation of metabolic
energy. Proceedings of the National Academy of Sciences of the
United States of America, 112: 4696–4701.
Perdiguero-Alonso, D., Montero, F. E., Raga, J., and Kostadinova, A.
2008. Composition and structure of the parasite faunas of cod,
Gadus morhua L. (Teleostei: Gadidae), in the North East Atlantic.
Parasites and Vectors, 1: 23.
Poulin, R., Blasco-Costa, I., and Randhawa, H. S. 2016. Integrating
parasitology and marine ecology: Seven challenges towards greater
synergy. Journal of Sea Research, 113: 3–10.
933
Poulin, R., Krasnov, B. R., Pilosof, S., and Thieltges, D. W. 2013.
Phylogeny determines the role of helminth parasites in intertidal
food webs. Journal of Animal Ecology, 82: 1265–1275.
Probst, S., and Kube, J. 1999. Histopathological effects of larval
trematode infections in mudsnails and their impact on host
growth: what causes gigantism in Hydrobia ventrosa (Gastropoda:
Prosobranchia)? Journal of Experimental Marine Biology and
Ecology, 238: 49–68.
Queir
os, A. M., Fernandes, J. A., Faulwetter, S., Nunes, J., Rastrick, S.
P. S., Mieszkowska, N., Artioli, Y. et al. 2015. Scaling up experimental ocean acidification and warming research: from individuals to the ecosystem. Global Change Biology, 21: 130–143.
Reipschl€ager, A., and Pörtner, H. 1996. Metabolic depression during
environmental stress: the role of extracellular versus intracellular
pH in Sipunculus nudus. Journal of Experimental Biology, 199:
1801–1807.
Reusch, T. B. H. 2016. Trematodes on acid: editorial comment on the
feature article by Guilloteau et al. Marine Biology, 163: 96.
Sato, T., Watanabe, K., Kanaiwa, M., Niizuma, Y., Harada, Y., and
Lafferty, K. D. 2011. Nematomorph parasites drive energy flow
through a riparian ecosystem. Ecology, 92: 201–207.
Shaw, J., Korzan, W., Carpenter, R., Kuris, A., Lafferty, K., Summers,
C., and Overli, O. 2009. Parasite manipulation of brain monoamines in California killifish (Fundulus parvipinnis) by the trematode Euhaplorchis californiensis. Proceedings of the Royal Society
B: Biological Sciences, 276: 1137–1146.
Shinn, A. P., Pratoomyot, J., Bron, J. E., Paladini, G., Brooker, E. E.,
and Brooker, A. J. 2015. Economic costs of protistan and metazoan parasites to global mariculture. Parasitology, 142: 196–270.
Studer, A., Lamare, M. D., and Poulin, R. 2012. Effects of ultraviolet
radiation on the transmission process of an intertidal trematode
parasite. Parasitology, 139: 537–546.
Thieltges, D. W., Amundsen, P. A., Hechinger, R. F., Johnson, P. T.
J., Lafferty, K. D., Mouritsen, K. N., Preston, D. L. et al. 2013.
Parasites as prey in aquatic food webs: implications for predator
infection and parasite transmission. Oikos, 122: 1473–1482.
Thomas, F., Renaud, F., De Mee^
us, T., and Poulin, R. 1998.
Manipulation of host behaviour by parasites: ecosystem engineering in the intertidal zone? Proceedings of the Royal Society of
London. Series B: Biological Sciences, 265: 1091–1096.
Handling editor: Howard Browman