Impacts of Ocean Acidification on Multiplication and Caste Organisation of Parasitic Trematodes in Their Gastropod Host
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Mar Biol (2016) 163:96 DOI 10.1007/s00227-016-2871-5 FEATURE ARTICLE Impacts of ocean acidification on multiplication and caste organisation of parasitic trematodes in their gastropod host Pauline Guilloteau1 · Robert Poulin1 · Colin D. MacLeod1 Received: 1 December 2015 / Accepted: 8 March 2016 © Springer-Verlag Berlin Heidelberg 2016 Abstract Ocean acidification is predicted to impact the may also impact transmission success and parasite abun- structure and function of all marine ecosystems in this cen- dance of some trematodes, with possible consequences for tury. As focus turns towards possible impacts on interac- marine communities and ecosystems. tions among marine organisms, its effects on the biology and transmission potential of marine parasites must be evaluated. In the present study, we investigate two marine Introduction trematode species (Philophthalmus sp. and Parorchis sp., both in the family Philophthalmidae) infecting two marine Since the preindustrial period, emissions of CO2 in the gastropods. These trematodes are unusual in that their asex- atmosphere have increased drastically, with atmospheric ually multiplying stages within snails display a division levels rising each year by 0.5 % (Solomon et al. 2007). As of labour, with two distinct castes, a large-bodied morph oceans play a major role in the processes driving the natu- producing infective stages and a smaller morph playing a ral carbon cycle, the current input of atmospheric CO2 is defensive role against other competing parasites. Using a buffered by oceanic uptake, amounting to nearly a third potentiometric ocean acidification simulation system, we of carbon added to the atmosphere from human activity in test the impacts of acidified seawater (7.8 and 7.6 pH) on the past 200 years (Fabry et al. 2008; Doney et al. 2009). the production of free-living infective stages (cercariae), Due to the equilibrium between atmospheric CO2 and dis- the size and survival of encysted resting stages (metacercar- solved oceanic CO2 at the water surface, the non-negligible iae), and the within-host division of labour measured as the input of dissolved CO2 is modifying seawater chemistry by ratio between numbers of the two morphs. In general, low changing the balance of different chemical reactions (Dick- pH conditions caused an increase in cercarial production son et al. 2007). These chemical changes lead to a reduc- and a reduction in metacercarial survival. The ratio of the tion in carbonate ion concentrations, but an increase in two castes within snail hosts tended to shift towards more concentrations of bicarbonate ions and hydrogen ions, thus of the smaller defensive morphs under low pH. However, lowering pH (i.e. pH log [H+]), a phenomenon known = − the observed effects of reduced pH were species specific as ocean acidification (OA). The main consequences for and not always unimodal. These results suggest that ocean marine ecosystems are a reduction in average seawater acidification can affect the biology of marine parasites and pH and a decline in the availability of calcium carbonate (CaCO3) used by many groups of marine organisms, such as molluscs, echinoderms, crustaceans, corals, and many Responsible Editor: T. Reusch. species of plankton that synthesise calcified structures (Orr Reviewed by A. Kostadinova and an undisclosed expert. et al. 2005). Moreover, the increase in hydrogen ions in seawater affects acid–base homoeostasis in several marine * Robert Poulin organisms (Pörtner et al. 2004), leading to more energy [email protected] required for maintenance of intra- and extra-cellular bal- 1 Department of Zoology, University of Otago, PO Box 56, ances. Surface-ocean pH has fallen by approximately 0.1 Dunedin 9054, New Zealand units to its present 8.1 pH value (Doney et al. 2009; Fabry 1 3 96 Page 2 of 10 Mar Biol (2016) 163:96 et al. 2008; Riebesell et al. 2010) and is predicted to drop labour, with the small rediae acting as ‘soldiers’ defending to approximately 7.6 by the year 2100 and to 7.4 by 2300 the redial colony against other parasites trying to establish (Intergovernmental Panel on Climate Change (IPCC) in the same snail host, and the large reproductive rediae 2014). produce cercariae that will leave the snail to complete the Research on the effects of OA is now founded on precise life cycle (Hechinger et al. 2011; Leung and Poulin 2011; understanding of carbonate chemical reactions and the use Lloyd and Poulin 2012, 2014; Mouritsen and Halvorsen of realistic OA simulation systems (Riebesell et al. 2010). 2015). As in social insects like ants and termites (Oster and From an ecological perspective, there is growing interest Wilson 1978), the ratio of small-to-large rediae is likely to in the more indirect effects of OA, for instance, effects on be optimised to yield maximum fitness, i.e. cercarial out- interspecific interactions such as predation, competition and put, for the colony. Earlier research has shown that external parasitism (Kroeker et al. 2013; McCormick et al. 2013; stressors can indeed affect the caste ratios of social trema- MacLeod and Poulin 2015). Parasites are often neglected in tode colonies (Lloyd and Poulin 2013). marine ecological research because of their small size. How- The present study investigates two trematode species, ever, parasites are diverse and abundant, and now known to both of the family Philophthalmidae: Philophthalmus sp. impact host population dynamics, interspecific interactions, (Martorelli et al. 2008) and Parorchis sp. (O’Dwyer et al. community structure, food web complexity and ecosystems 2014), which use the New Zealand gastropods Zeacumantus energetics (Sousa 1991; Poulin 1999; Mouritsen and Poulin subcarinatus and Austrolittorina cincta, respectively, as first 2002; Thompson et al. 2005; Kuris et al. 2008). There are intermediate host. Both are very common parasites of gas- many reasons to believe OA could impact parasites either tropods in New Zealand intertidal habitats, and their rediae directly or indirectly through their hosts, in ways that could infect the gonad and digestive tissue of the host, leading to change their interactions with their hosts and their influence its castration (Fredensborg et al. 2005). Both species display on ecosystems (MacLeod and Poulin 2012). a division of labour inside the first intermediate host (Leung In intertidal environments, parasitic trematodes are par- and Poulin 2011; Lloyd and Poulin 2012; Kamiya and Pou- ticularly abundant and known to affect the biology of the lin 2013; O’Dwyer et al. 2014). Cercariae of Philophthal- two or three host species involved in their complex life mus sp. and Parorchis sp. do not use a second intermediate cycle. Typically, adult worms live in the gut of a verte- host but instead leave the snail to encyst on a hard substrate, brate definitive host, such as a bird or fish, from where they such as the shell of other gastropods or seaweed (Lei and release eggs in host faeces (Galaktionov and Dobrovolskij Poulin 2011; Neal and Poulin 2012; O’Dwyer et al. 2014), 2003). Snails serve as first intermediate host, becoming in the process losing their tail and becoming metacercariae. infected after accidentally ingesting eggs or by free-swim- The survival of cercariae of both species, and metacercariae ming larvae hatched from eggs. Following asexual (clonal) at least in the case of Philophthalmus sp., is significantly multiplication within the snail host, free-swimming infec- lower under conditions of reduced pH (MacLeod and Poulin tive stages, or cercariae, emerge from snails in large num- 2015). However, the effects of OA on caste ratio and overall bers and seek a second intermediate host, which they pen- trematode colony fitness in these trematodes with division etrate and in which they encyst as metacercariae, to await of labour remain unexplored. ingestion by a suitable definitive host, in which they develop The main objective of this study was to experimentally into adult worms. In some trematode species, however, there assess the impact of OA on colony organisation and fitness is no second intermediate host; cercariae encyst on various in these two trematodes. Specifically, we test the effects of substrates and become metacercariae, awaiting ingestion by OA on cercarial output, metacercarial size, metacercarial a definitive host (Galaktionov and Dobrovolskij 2003). Mul- survival, and within-host colony structure measured as the tiple studies have documented how sensitive cercariae and relative numbers (ratio) of the two castes. Cercarial pro- metacercariae attached to external substrates are to abiotic duction and metacercarial survival are key steps in parasite conditions, such as temperature (Studer et al. 2010; Mor- transmission, and thus, our results have bearing not only ley and Lewis 2013), salinity (Lei and Poulin 2011) and pH on the social biology of these trematodes, but also on the (Koprivnikar et al. 2010; MacLeod and Poulin 2015). infection risk they pose for birds and snails. Here, we focus on how OA affects a recently discovered facet of trematode biology. In some species, the asexually multiplying stages within a snail intermediate host, known Methods as rediae, come in two morphotypes representing distinct castes: a larger-bodied reproductive caste and a smaller Snail collection and parasite identification non-reproductive caste (Hechinger et al. 2011; Leung and Poulin 2011; Miura 2012; Nielsen et al. 2014). Much In February and March 2015, Z. subcarinatus and A. cincta evidence indicates that this represents a true division of snails were collected by hand at low tide on the intertidal 1 3 Mar Biol (2016) 163:96 Page 3 of 10 96 mudflat of Lower Portobello Bay (LPB), Otago Harbour, 2-amino-2-hydroxy-1,3-propanediol (TRIS) and 2-ami- South Island, New Zealand (45°80′S, 170°66′E). Prior nopyridine (AMP), prepared in accordance with Dickson to the study, all snails were maintained in well-aerated 2 et al. (2007). To maintain appropriate seawater chemistry, L seawater aquaria (20 °C, >95 % oxygen, 8.05 pH) and i.e.