Ecophysiological Studies of Corophium Volutator (Amphipoda) Infested by Microphallid Trematodes

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Ecophysiological Studies of Corophium Volutator (Amphipoda) Infested by Microphallid Trematodes MARINE ECOLOGY PROGRESS SERIES Vol. 202: 143–151, 2000 Published August 28 Mar Ecol Prog Ser Ecophysiological studies of Corophium volutator (Amphipoda) infested by microphallid trematodes Karin Meißner*, Thomas Schaarschmidt University of Rostock, Department of Zoology, Universitätsplatz 5, 18051 Rostock, Germany ABSTRACT: The impact of metacercaria infestation on the metabolic activity, thermal tolerance and freezing tolerance of Corophium volutator (Pallas, 1766) was investigated. Metabolic activity was measured by direct microcalorimetry at different temperatures and oxygen conditions. In 2 cases only, at 15°C/50% O2 and 10°C/100% O2, a positive correlation between infestation intensity and metabolic heat loss was found. At all temperatures examined, hypoxia down to 35% oxygen saturation did not have a significant effect on metabolic heat loss. With rising temperature, enhanced locomotory activity of C. volutator was observed during measurements, but an effect of infestation intensity was not found. According to the results of the thermal tolerance experiments, metacercaria infestation at studied intensities does not compromise infested hosts. In the freezing tolerance experiments, heavily infested C. volutator specimens survived better than specimens with lower infestation intensities. The results indicate a good adaptation of the parasite, because survival of the second intermediate host until consumed by the final host is essential for the completion of the life cycle of digenetic trematodes. It is concluded that under normal field conditions, changes of metabolic activity or reduced tolerance towards thermal stress and freezing as a result of metacercaria infestation should not be responsible for mass mortality events observed in the field. The role of the developmental stage of the metacer- caria and the possibly more severe impact caused by not yet or only recently encysted metacercariae, compared to metacercariae with multi-layered cyst walls, is discussed. KEY WORDS: Corophium volutator · Amphipoda · Microphallidae · Microcalorimetry · Thermal tolerance · Freezing tolerance · Parasitism Resale or republication not permitted without written consent of the publisher INTRODUCTION from the first intermediate host, a gastropod of the genus Hydrobia for example, and seek out the next The amphipod Corophium volutator (Pallas, 1766) is host, a crustacean. There the cercariae develop into a well-known inhabitant of coastal mudflats of Europe metacercariae and form metacercarial cysts of differ- and North America. The studies of several authors ent sizes. In a single C. volutator, for instance, up to have led to a greater understanding of the ecology and 100 metacercarial cysts can be found (Fig. 1). The life physiology of this species. During the last few years, cycle of these digenetic trematodes is completed when the discussion about population dynamics of C. voluta- the final host, a sea bird or wader, feeds on infested C. tor has resumed because of a new aspect: parasitism volutator specimens. (Lauckner 1986, 1990). Primarily involved are dige- The lowest values of the relative infestation intensity netic trematodes. In shallow water areas of the south- and prevalence among Corophium volutator specimens ern Baltic Sea, for example, C. volutator is used as a generally were recorded in May and June, when the second intermediate host by at least 2 microphallid offspring of individuals that had overwintered pre- trematode species: Maritrema subdolum (Jägerskiöld dominated within the population (Bick 1994, Meißner & 1908) and Levinseniella brachysoma (Creplin 1837) Bick 1997). Thereafter, increasing numbers of indi- (Reimer 1963). The cercariae of these species emerge viduals were infested with increasing frequency until autumn (Meißner & Bick 1997). A statistical analysis *E-mail: [email protected] revealed that C. volutator with high infestation inten- © Inter-Research 2000 144 Mar Ecol Prog Ser 202: 143–151, 2000 the possible synergistic effects of temperature, oxygen content of the water and infestation intensity on meta- bolic activity. Apart from effects on the metabolism, an impact on the general physiological fitness of the host is conceivable, possibly reflected in reduced tolerance towards extreme environmental conditions. As an in- habitant of intertidal and shallow water areas, C. volu- tator is exposed to great diurnal and seasonal fluc- tuations of temperature. Water temperature in the summer is usually above 30°C during the day in our investigation area, whereas in the winter the water is frozen solid to the bottom for several weeks. Hence, freezing and thermal stress tolerance experiments are relevant observations concerning potential conse- Fig. 1. Corophium volutator. Metacercarial cysts in the body quences of trematode infestation. cavity (thoracic region, appendages removed) MATERIAL AND METHODS sities (14 to 22 cysts ind.–1) were distinctly less common in September than theoretically expected (infestation Collection and storage of Corophium volutator. The assumed to be a random event and subsequent infesta- Corophium volutator specimens used in the experiments tions independent of previous ones) (Meißner & Bick were collected in a shallow water area in the southern 1997). Laboratory studies showed that severe in- part of the Mecklenburger Bucht, Baltic Sea. The col- festation through microphallid trematodes (>60 meta- lected crustaceans were held in aerated aquaria with cercarial cysts or ~40 not yet encysted metacercariae) is seawater and heat-treated sediment from the biotope for detrimental to C. volutator and finally leads to the death about 4 wk. In addition, mudsnails of the genus Hydro- of the host (Jensen et al. 1998, Meißner & Bick 1999a). bia were placed in some of the aquaria with C. volutator Moreover, these parasites are possibly responsible for to induce higher microphallid infestation intensities of mass mortality events in C. volutator populations the crustacean. Sieved sediment (200 µm mesh) from the (Lauckner 1987, Jensen & Mouritsen 1992, Meißner & uppermost sediment layer in the biotope was added into Bick 1997). However, there is still little known about the the aquaria to induce the growth of algae on the sedi- kind of impairment that occurs. Metacercarial cysts can ment layer and glass panes of the aquaria, serving as be found in almost every part of the body, but particu- foodstuff for the specimens. In addition a few ml of a lary in the posterior thorax region (Mouritsen & Jensen culture solution of the diatom Thalassiosira fluviatilis 1997). Histological examinations of infested C. voluta- were introduced into the aquaria weekly. tor revealed that the cysts are located in the mixocoel After this period, Corophium volutator was trans- without any real contact to the host’s organs (R. ferred to the adaptation aquaria and kept under con- Bochert, Univ. Rostock, pers. comm.). Galaktionov et al. stant conditions for at least 2 wk until the start of the (1996) investigated the developmental changes in the experiments (Table 1). During this adaptation period, tegument of 4 microphallid species in the second inter- storage conditions were identical to the ones described mediate host and concluded that recently encysted above, but without the mudsnails. metacercaria of the species Levinseniella brachysoma Experimental design. Metabolic heat loss measure- and Maritrema subdolum absorb nutrients and other ments: Metabolic heat loss in Corophium volutator was substances from the haemolymph of their host Gam- measured by direct microcalorimetry using a TAM marus oceanicus during a period of up to 35 d. It is also (Thermal Activity Monitor 2277, Thermometric AB, conceivable that metacercarial cysts exert a mechanical Sweden). Perfusion cells with 4 ml ampoule in twin impact on the tissues and organs of the host. arrangement (1 sample and 1 reference system for With this background knowledge, it is possible that each channel) were used. Thermal calibration was per- differences exist in the physiology and autecology of formed using the internal calibration unit of the TAM. infested and non-infested Corophium volutator. To test The specimen chambers were prepared with a thin this assumption, we conducted measurements of meta- layer of washed, sieved and ashed (500°C) sediment bolic heat dissipation as a measure of metabolic activ- from the sample location. Continous water flow (aver- ity in C. volutator specimens with different infestation age of 14 ml h–1) was applied by means of a peristaltic intensities. Metabolic heat loss was measured at differ- pump. To minimize bacterial growth and contamina- ent temperatures and oxygen combinations to examine tion, the water was filtered before use (0.45 µm mem- Meißner & Schaarschmidt: Ecophysiological studies of Corophium volutator 145 Table 1. Laboratory conditions during the adaptation period of Corophium volutator before the start of the experiments Experiment Date of specimen Temperature Light period L/D Salinity Adaptation period collection (mo/yr) (°C) (‰) Freezing tolerance 10/96 3 11 h/13 h 13.3 4 wk Thermal tolerance 7/97 20 14 h/10 h 14.0 ≥2 wk Metabolic 1 3/98–4/98 10 12 h/12 h 14.0 ≥2 wk heat loss 2 9/96–2/97 15 14 h/10 h 14.0 ≥2 wk 3 7/97–2/98 19 and 25 14 h/10 h 14.0 ≥2 wk + 4 d (25°C) brane filter). Defined oxygen saturation in the water perature (36, 36.5 or 38.5°C), a single Corophium volu- was generated by controlled flow of air and nitrogen tator specimen was placed in the jar. At the end of an (combined
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