Oecologia (1998) 115:188±195
Ó Springer-Verlag 1998
Robert E. Sorensen á Dennis J. Minchella
Parasite in¯uences on host life history: Echinostoma revolutum parasitism of Lymnaea elodes snails
Received: 5 September 1997 / Accepted: 19 November 1997
Abstract Using ®eld surveys and experimental infections, we investigated the in¯uence of a trematode parasite on life history traits of adult Lymnaea elodes snails. We found that parasitism signi®cantly aected the growth, fecundity, and survival of host snails. Within ®ve of the six natural L. elodes populations we sampled, shell length of echinostome-infected hosts was signi®cantly greater than for uninfected conspeci®cs. Furthermore, we show that gigantism occurs among experimentally infected snails due to an accelerated growth rate and size-selective mortality following an Echinostoma revolutum infection. The fecundity of infected snails sharply decreased beginning at 3 weeks post exposure (PE) and all egg production eventually ceased for most hosts by 5±6 weeks PE. Energy constraints, imposed by parasite development, alter the host energy budget. Early in the infection, parasite depletion of host energy reserves reduces host reproduction, but sucient resources remain to allow accelerated host growth. Mortality was increased among host snails at two distinct stages: shortly after exposure and several weeks after cercariae were ®rst released. We did not observe tissue degradation in snails during the ®rst 4 weeks after exposure to the parasite, but destruction of host tissues was noted among snails dying later in the infection. Key words Host life history á Parasitism á Gigantism á Echinostoma á Lymnaea
Introduction An organism's dierential investment into growth, reproduction, and survival de®nes its life history strategy. Allocation trade-os exist between these processes such
R.E. Sorensen (&) á D.J. Minchella Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA E-mail:
[email protected]; Fax: +1-765-494-0876
that energy channeled to any one of them is unavailable to the remaining two components (Stearns 1976, 1992). The lifetime reproductive success of an organism is a manifestation of the life history traits expressed by that organism throughout its life. Interspeci®c interactions, such as predation (Crowl and Covich 1990) and competition (Brown 1982), in¯uence life history traits; likewise, parasitism shapes individual host life history strategies (Sousa 1983; Minchella 1985). Price (1980) elegantly emphasized the potential relationship between parasitism and host life history strategies, but researchers have just begun to elucidate this interaction during the last decade (Esch and Fernandez 1994; Michalakis and Hochberg 1994). By utilizing ®eld collections and experimental trematode infections of Lymnaea elodes, a common freshwater snail, we assessed parasite in¯uences on host growth, fecundity, and survival. Parasites impose direct ®tness costs on their hosts by stealing nutrients normally used for host life processes (Toft 1991). Trematodes are a diverse group of endoparasites requiring at least two hosts: a mollusc and a vertebrate. Intramolluscan trematode parasitism is frequently associated with the alteration of a host's growth, fecundity, or survival; yet, few clear patterns exist (reviewed in Thompson 1997). The results vary depending upon several factors, including: (1) the speci®c hostparasite combination (Minchella and LoVerde 1983; Schrag and Rollinson 1994), (2) host age (Loker 1979; Kuris 1980; Keas and Esch 1997), (3) the life span and typical reproductive pattern of the host (Sousa 1983; Curtis 1995), and (4) whether the experiments were conducted in a laboratory or in the ®eld (McClelland and Bourns 1969; Fernandez and Esch 1991). However, in the midst of these host response variations, there appears to be one common outcome among molluscs following trematode infection: an eventual elimination of host reproductive output, often termed ``parasitic castration'' (Wright 1971; Malek and Cheng 1974). For uninfected freshwater snails, the production of energetically expensive egg masses occurs at the expense of body growth (Geraerts and Joosse 1984) and adult life
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span (Calow 1978). To a larval trematode, host reproduction diverts resources away from its own development, and potentially limits the size and stability of the parasite's habitat (Bayne and Loker 1987); thus, it is not surprising that trematodes castrate their snail hosts. The intrinsic interdependence existing among the growth, fecundity, and survival components of a life history strategy suggests that parasitic castration could aect the resulting growth and survival of individual hosts. Increased host size, termed ``gigantism,'' commonly coincides with trematode parasitism (Keymer and Read 1991). Parasitic castration typically begins 2±3 weeks after infection. The cause of this reduction in fecundity may depend upon the type of intramolluscan larval stages that prevail in the trematode life cycle. There are two types of intramolluscan stages of trematodes, sporocysts and rediae, both of which function to produce additional life cycle stages asexually within the host mollusc. Sporocysts lack ambulatory musculature and absorb host nutrients via their tegument. Rediae, with their muscular pharynx and primitive gut, actively consume and digest host tissues while moving throughout infected hosts. Most detailed studies of life history consequences for infected snails have focused on trematodes that possess sporocysts as the ®nal intramolluscan stage (Pan 1965; McClelland and Bourns 1969; Minchella and LoVerde 1981; Schrag and Rollinson 1994); therefore, relatively little is known about host life history traits associated with trematodes using redial larvae. This study utilizes L. elodes snails and Echinostoma revolutum, a ubiquitous old world trematode that develops rediae stages in pulmonate snails belonging to the genus Lymnaea (Kanev 1994). We address three questions. (1) Do natural populations of echinostome-infected L. elodes show evidence of gigantism? (2) In controlled laboratory infections, does E. revolutum impact the growth, fecundity and/or survival of L. elodes snails? (3) If parasitic infection alters host life history traits, what is the temporal pattern of this change; furthermore, can life history trade-os explain this outcome?
of reproduction (Eisenberg 1970; Brown et al. 1985); however, the life history traits of this species vary with population density, nutrient availability, and habitat permanence (Eisenberg 1966; Hunter 1975; Brown et al. 1985). Voltinism, growth rate, and size at maturity increase in permanent productive habitats, whereas, life span and reproductive rate are greatest in vernal, densely populated habitats. Because L. elodes is simultaneously hermaphroditic, it can reproduce through either self-insemination or outcrossing. The trematode, E. revolutum, has a complex three-host life cycle and adults use avian species, primarily waterfowl, as de®nitive hosts (Kanev 1994). E. revolutum adults, occupying the posterior digestive tract of infected birds, produce eggs that give rise to a free-living stage, called a miracidium, that infects L. elodes snails in northern Indiana, USA (Sorensen et al. 1997). Miracidia of E. revolutum that successfully infect L. elodes produce three distinct asexual stages of the parasite, a mother sporocyst and two subsequent redial stages. The second redial generation produces an infective, free-living cercarial stage that exits the host snail and forms metacercariae in another aquatic host, typically another snail (Beaver 1937). Metacercariae develop into adults when ingested by a suitable vertebrate host. Field survey studies Between 12 July and 9 August 1995, we collected L. elodes from six wetlands in northern Indiana to assess the prevalence of echinostome parasitism within various snail populations. Five of these sites ± pond A, pond B, pond 39, Merry Lea Pond, and Garwood Pond ± are located within Whitley County, Ind., whereas Shock Lake is in Kosciusko County, Ind. These six wetlands present a range of size, permanence, predominant vegetation, and nutrient productivity characteristics (Table 1). Two of these sites (pond A and pond B) have been previously studied (Brown et al. 1985; Minchella et al. 1985). L. elodes tend to reside on vegetation and detritus near the water surface, so we surveyed each study population using a single, haphazard collection of adult-sized L. elodes found on submerged and emergent subtrates. The number of snails collected at each site varied between 24 and 482 depending upon their abundance at the time of collection. All collected snails were isolated in small Syracuse dishes for 12 h under 700 ft-c of illumination to check for emerging echinostome cercariae (see Minchella et al. 1985). We also measured snail size, from the tip of the spire to the base of the body whorl to the nearest 0.01 mm with a digital caliper because shell length was shown to be a reliable indicator of snail condition in previous studies (Hunter 1975; Rollo and Hawryluk 1988). Snail life history traits following experimental infections
Materials and methods Snail and trematode descriptions The snail L. elodes ( L. palustris Stagnicola palustris S. elodes) is a common, freshwater pulmonate snail that inhabits a variety of ephemeral and permanent lentic systems. L. elodes is typically described as an annual species with a semelparous pattern
Table 1 Environmental characteristics of the six sites where echinostome-infected and uninfected Lymnaea elodes snails were collected during 1995 in northern Indiana, USA
E. revolutum cercariae were obtained from the infected snails collected during the survey portion of this study in order to experimentally infect snails in the laboratory. Parasites were maintained in the laboratory by passage through chickens (Gallus gallus dom.) and their natural host snails (Sorensen et al. 1997). We collected 500 L. elodes snails, ranging in size from 12 to 23 mm, on 17 June 1996 from Shock Lake. These snails were individually isolated under illumination twice (18±20 June and 2±3
Pond
Hectares
Permanence
Vegetation type
Productivity
Pond B Merry Lea Pond 39 Garwood Pond A Shock Lake
2 mm larger at 10 weeks PE. Altered growth patterns were also observed among EBU snails beyond 5 weeks PE. Mean shell length of EBU snails was always greater than that of CTL snails (Fig. 4). At week 9 PE, EBU snails were signi®cantly larger than CTL snails (time treatment, F1,9 2.674,
Discussion Parasitism by E. revolutum has a signi®cant in¯uence on L. elodes growth, fecundity, and survival. We found that snails exposed to E. revolutum suered increased mortality compared to control snails. Furthermore, infected
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snails showed size-speci®c mortality favoring larger individuals, grew faster early in the infection, and displayed reduced fecundity relative to uninfected snails. Snail infection and mortality Both exposure to and infection by E. revolutum markedly reduced L. elodes survival as also demonstrated in several other freshwater trematode-snail systems (Anderson and May 1979; Loker 1979; Kuris 1980; Minchella and LoVerde, 1981). We detected two phases of host mortality: during the prepatent stage (weeks 0±4), and several weeks postpatency (Fig. 2). Host mortality during the prepatent stage may have resulted from increased energetic demands of host defense, or from starvation, because tissue degradation was not obvious. In contrast, mortality of older snails involved tissue degradation. Superinfection with metacercariae is another potential cause of reduced survival in host snails during the late stages of infection; however, little is known about the relationship between metacercariae burden and mortality (Beaver 1937).The function of host immune responses was not investigated here, but initiation of these responses must be energetically demanding and the cost may depend upon the number of miracidia or metacercariae that enter the snail (Bayne and Loker 1987). Snail fecundity Trematode parasitism typically decreases the fecundity of hosts during the patent stages of an infection. Our results demonstrate that ``parasitic castration'' occurs in this parasite-host system (Fig. 3). The precise cause of this reduction is unknown, but it seems unlikely that physical destruction of host tissues is the sole mechanism (Wilson and Denison 1980), since few (
