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Intensity-Dependent Mortality of Paracalliope Novizealandiae (Amphipoda: Crustacea) Infected by a Trematode: Experimental Infections and Field Observations

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Intensity-Dependent Mortality of Paracalliope Novizealandiae (Amphipoda: Crustacea) Infected by a Trematode: Experimental Infections and Field Observations Journal of Experimental Marine Biology and Ecology 311 (2004) 253–265 www.elsevier.com/locate/jembe Intensity-dependent mortality of Paracalliope novizealandiae (Amphipoda: Crustacea) infected by a trematode: experimental infections and field observations B.L. Fredensborga, K.N. Mouritsenb, R. Poulina,* a Department of Zoology, University of Otago, P.O. Box 56, Dunedin, New Zealand b Department of Marine Ecology, Institute for Biological Sciences, Aarhus University, Finlandsgade 14, DK-8200 Aarhus N, Denmark Received 15 December 2003; received in revised form 6 May 2004; accepted 14 May 2004 Abstract The impact of parasitism on population dynamics and community structure of marine animals is an area of growing interest in marine ecology. The effect of a microphallid trematode, Maritrema novaezelandensis on the survival of its amphipod host, Paracalliope novizealandiae,was investigated by a laboratory study combined with data from field collections. In the laboratory, the effect of infection level on host mortality was investigated. Four groups of individuals were exposed to 0 (control), 5 (low), 25 (moderate) and 125 (high) cercariae, respectively, and their survival was monitored during a 10-day period. The distribution and migration of unencysted cercariae within the host were examined during dissections 6 and 48 h post infection. Parasite- induced mortality under field conditions was investigated by quantifying the relationship between parasite load and host body size. In the laboratory experiment, a highly significant decrease in host survival was observed for amphipods in the moderate and high infection groups relative to that of control amphipods. Parasite-induced mortality was most pronounced in the first two days post infection suggesting that the increased mortality is due to penetration of host cuticula and migration of cercariae within the host. Field data showed a monotonic increase in the mean parasite load with the body size of the amphipods, indicating that M. novaezelandensis does not severely affect P. novizealandiae-populations under normal field conditions. However, a decrease in the variance-to- mean ratio for the largest size-classes indicates that heavily infected individuals are removed from the population as predicted by the experimental infections. The results from the laboratory study in conjunction with our knowledge of the transmission strategy of the parasite emphasize the potential * Corresponding author. Tel.: +64-3-479-7983; fax: +64-3-479-7584. E-mail address: [email protected] (R. Poulin). 0022-0981/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2004.05.011 254 B.L. Fredensborg et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 253–265 effect of M. novaezelandensis on its amphipod host population during episodes of high temperature causing the rapid and massive release of cercariae from snail intermediate hosts. D 2004 Elsevier B.V. All rights reserved. Keywords: Amphipoda; Maritrema; Paracalliope; Parasite; Trematoda 1. Introduction The importance of parasites in intertidal host ecology has received increasing attention from ecologists in recent years. Studies of parasites in their invertebrate hosts have often reported a significant impact on host survival, fecundity and growth (see Mouritsen and Poulin, 2002 and references therein). Furthermore, by affecting host species differently, parasites can mediate competitive interactions and predator–prey relationships (Minchella and Scott, 1991; Thomas et al., 1995c; Hudson and Greenman, 1998) and in turn affect the structure of the animal community and biodiversity in the intertidal ecosystem (Lauckner, 1987; Sousa, 1991; Poulin, 1999; Thomas et al., 1999; Mouritsen and Poulin, 2002). Yet, few studies have attempted to link parasite impacts measured in the laboratory with evidence from the field. A combination of the two methods is crucial in order to understand the impact of the parasite on its host population under normal field conditions, but also the potential effect of the parasite on host populations should optimal conditions for transmission occur. Trematodes belonging to the family Microphallidae typically have a three-host life cycle, including crustaceans as second intermediate hosts. Free-living cercariae, released from the snail first intermediate host, penetrate the cuticula of a crustacean in which they encyst as metacercariae. The life cycle of the parasite is completed when the infected host is eaten by an appropriate definitive host, in most cases a shorebird. The proportion of intertidal crustaceans infected by microphallid trematodes in any given locality can occasionally reach high levels (Bick, 1994; Mouritsen et al., 1997, Meissner and Bick, 1997; Fredensborg, 2001; Meissner, 2001; Pung et al., 2002) and laboratory studies indicate that survival of infected individuals is generally negatively influenced by the parasite (Mouritsen and Jensen, 1997; Jensen et al., 1998; Meissner and Bick, 1999a,b). Direct measures of the survival of infected animals from field studies are, however, difficult to obtain and thus are rare in the ecological literature. Instead, indirect methods such as assessing the shape of the relationship between mean parasite load or variance-to- mean ratio and host size-class are often used to infer parasite-induced mortality. The reasoning behind this is that if parasites accumulate in the host over time with no density- dependence, intensity-dependent host mortality will be detectable as a flattening of the infection intensity versus host size curve (Anderson and Gordon, 1982). The oldest and most heavily infected individuals will thus be removed from the population, leaving a convex relationship between both mean parasite load and variance-to-mean ratio and host size (Anderson and Gordon, 1982; Rousset et al., 1996). This method has been used once to demonstrate amphipod mortality induced by microphallid trematodes in the field (Thomas et al., 1995c). B.L. Fredensborg et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 253–265 255 Recently, Maritrema novaezelandensis, a new microphallid trematode, has been described from the Otago Harbour, South Island, New Zealand. Its life cycle includes a snail first intermediate host (Zeacumantus subcarinatus), several species of amphi- pods and crabs as second intermediate hosts, and the red-billed gull (Larus hollan- diiae scopulinus) as a definitive host (Martorelli et al., 2004). One of its amphipod hosts, Paracalliope novizealandiae (Dana, 1853), is an abundant and widespread species in the soft-bottom littoral zone, occupying beds of eelgrass (Zostera novae- zelandensis) and patches of sea lettuce (Ulva lactuca), where it mainly feeds on epiphytic diatoms and fine detritus (Barnard, 1972; Cummings et al., 1995). Because of its abundance, it is believed to be an important component of the food web, serving as food for several fish species using the shallow intertidal areas as nursery grounds and for shorebirds. In this study, direct measurements on the survival of P. novizealandiae in relation to intensity of infection by M. novaezelandensis were obtained from a laboratory experiment. Furthermore, mean parasite load and variance-to-mean ratio were estimated for field- collected amphipods to investigate whether infection intensity-dependent mortality occurs under field conditions. Possible pathological mechanisms involved in parasite-induced mortality and the potential impact of M. novaezelandensis on P. novizealandiae-population dynamics are discussed in relation to the results obtained and the transmission strategy of the parasite. 2. Materials and methods 2.1. Field collections A large sample of amphipods was collected on two sampling occasions in late summer (March) and spring (October) 2003 from Lower Portobello Bay (LPB) and in March 2003 from Hoopers Inlet (HI) on the Otago Peninsula, South Island, New Zealand (45j52VS, 170j42VE). Both localities are intertidal (tidal range = 2 m), and the sediment consists mainly of fine sand and mud. The two localities were selected based on the probability of finding Maritrema-infected amphipods known from earlier samples. In LPB the density of M. novaezelandensis-infected Z. subcarinatus is known to be relatively high and preliminary studies have confirmed the presence of Maritrema-infected amphipods at this locality (Fredensborg, unpublished data). In HI, on the other hand, the snail first intermediate host is absent and amphipods are therefore not expected to harbour any M. novaezelandensis metacercariae. Amphipods were randomly sampled during low tide from shallow pools (5 cm deep) 50 m from MHWL. The pools are isolated during low tide (10–12 h per day) and contain eelgrass (Z. novaezelandensis) and sea lettuce (U. lactuca). A plankton-net was dragged through the water and the animals captured were transferred to a plastic container (25 Â 15 Â 15 cm) half-filled with seawater. In addition, in LPB, a large sample of Z. subcarinatus snails was collected by hand from the same tidal pools, stored in a separate container and returned to the laboratory for use in the experiments described below. 256 B.L. Fredensborg et al. / J. Exp. Mar. Biol. Ecol. 311 (2004) 253–265 2.2. Field study For each of the sampling occasions, approximately 300 amphipods from LPB were randomly taken from the field-collected samples, measured (rostrum to telson), sexed and the number of parasites they harboured counted. Extra amphipods were selected to ensure that all available size classes were represented
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