Seasonal dynamics of trematode infection in the first and the second intermediate hosts: A long-term study at the subarctic marine intertidal

Highlights

• At the White Sea intertidal molluscan hosts are infected with trematodes year-round.

• Composition of rediae and daughter sporocyst groups had different seasonal dynamics.

• Peaks of parthenitae groups activity and host infection with metacercariae coincided.

• Maximal mussel infection with metacercariae was timed for seabirds autumn migration.

• Climate warming may intensify trematode transmission in Subarctic seas.

Abstract

The purpose of this study was to reveal seasonal reorganizations in groups of parthenitae (rediae or daughter sporocysts) of trematodes in the first intermediate hosts (1IH) and of their larvae (metacercariae) in the second intermediate hosts (2IH) in the nearshore ecosystems of the White Sea. The study involved two trematode species parasitizing seabirds, Himasthla littorinae (Himasthlidae) and Cercaria parvicaudata (Renicolidae), and was based on long-term seasonal monitoring of populations of 1IH (snails Littorina spp.) and 2IH (mussels Mytilus edulis) at two intertidal sites (66°N). We discovered that groups of H. littorinae rediae in the molluscan host were self-sustaining and could function for more than one warm season. Groups of daughter sporocysts of C. parvicaudata caused the death of the molluscan host in the course of a year. Parthenitae groups of both trematode species spend the cold season (7–8 months a year) in the state of developmental arrest. After the water warms up in spring, the surviving mature groups of sporocysts of C. parvicaudata start to emit cercariae, but their molluscan hosts die soon. Most of the mature rediae in groups of H. elongata die in autumn-winter; in spring young overwintered rediae mature and produce cercariae over the next warm period. The maximum prevalence of mature parthenitae groups of H. littorinae and C. parvicaudata in periwinkles was observed in the warmest period, July-August, when they produced and emitted numerous cercariae ensuring mass infection of mussels. Though metacercariae occurred in mussels all year round, the mean abundance usually reached the highest values in summer–autumn. In winter-spring the level of infection decreased because heavily infected molluscs died out and new molluscs were not infected as cercarial emergence from 1IH had stopped. We discuss the components of the transmission success of H. littorinae and C. parvicaudata in the Subarctic and suggest that the parasites’ transmission may intensify owing to the prolongation of the period of functional activity of parthenitae groups under conditions of a warming climate.

Introduction

A regular alternation of cold and warm seasons in temperate and high-latitude regions determines the annual cycles of life activity of all organisms, and parasites are no exception. The transmission of digenetic trematodes (Trematoda, Digenea)—a species-rich subclass of parasitic flatworms with a complex life cycle (Cribb et al., 2003; Galaktionov and Dobrovolskij, 2003; Littlewood et al., 2015)—is confined to the warm season. At that time, all the hosts are present and active in the biotope, and the temperature is sufficient for the normal functioning of the parasitic stages in ectothermic hosts (sporocysts and rediae, metacercariae and, in some cases, adults) and of the dispersive larvae (miracidia and cercariae) in the environment (reviewed in Galaktionov and Dobrovolskij, 2003; Galaktionov, 2017). The final vertebrate hosts, in which adult flukes producing eggs with developing or mature miracidia are formed, are also available during the warm season (Galaktionov, 2017).

Studies of seasonal dynamics of trematode infection in animal hosts have a long history, and there are numerous publications on this topic (reviewed in Kube et al., 2002; Galaktionov and Dobrovolskij, 2003). Most of them, however, analyse only changes in the total prevalence of a particular trematode species in the host. For instance, the prevalence of trematodes in the first intermediate molluscan hosts was established based on cercarial emergence (without dissecting the molluscs) (Brassard et al., 1982; Muhoho et al., 1997; Morley et al., 2004; Kazibwe et al., 2006) or based on the presence of parthenitae (daughter sporocysts or rediae) containing fully-formed cercariae in the dissected molluscs. These studies, made on both freshwater (e.g. Campbell, 1973; Rantanen et al., 1998; Sturrock et al., 2001; Kazibwe et al., 2006; Peterson, 2007; Zemmer et al., 2017) and marine (e.g. Robson and Williams, 1970; Lang and Dennis, 1976; Allison, 1979; Lauckner, 1980; Hughes and Answer, 1982; Field and Irwin, 1999) molluscs, made it possible to identify the general pattern of seasonal dynamics of the prevalence of trematode intramolluscan stages. This pattern is as follows: infection, inconsiderable in spring, grows steadily throughout the summer and, having reached a peak in late summer/autumn, starts to decrease, and decreases gradually until spring.

While the conclusions made in the studies cited above are correct in many respects, the data given in them reflect only the phenology of the seasonal dynamics of the infection of molluscs, without elucidating the processes behind it. We mean, first of all, seasonal reconstructions of the composition of groups of different stages of the parasite’s life cycle in the hosts. This is especially important for parthenitae (usually called asexual stages) of trematodes, for which temporal reorganisations of the composition of sporocyst and rediae groups are known (e.g. Dönges, 1971; Théron, 1981; Touassem and Théron, 1986; Dönges and Götzelmann, 1988; Ataev and Dobrovolskij, 1990; Galaktionov et al., 2014). The few studies where different stages of the development of parthenitae were taken into consideration show that seasonal changes in the prevalence of their mature cercariae-producing groups in molluscs do not provide a clear picture of the seasonal dynamics of the infection (Køie, 1975; Machkevsky, 1982; Rusanov and Galaktionov, 1984; Ataev, 1991; Taskinen et al., 1994; Abdul-Salam et al., 1997; Ataev et al., 2002; Sendersky et al., 2002; Kube et al., 2002; Galaktionov et al., 2006; Korniychuk, 2008a; Averbuj and Cremonte, 2010; Fermer et al., 2010; Prinz et al., 2010; Nikolaev, 2012; Ataev and Tokmakova, 2015). The aspects remaining unclear include the lifespan of parthenitae groups, the character of their development and recruitment with young individuals, seasonal changes in the composition and dynamics of cercarial production. These processes have a considerable impact on the transmission of cercariae and in the long run determine the character of their infection of populations of the second intermediate hosts.

It is fairly evident that seasonal dynamics of component populations (all the individuals of a given life cycle phase at a particular space and time [Bush et al., 1997]) of metacercariae are mostly determined by the character of cercarial emergence in different seasons as well as by the biology and the dynamics of abundance and age composition of the host population. Therefore, we may expect the general course of the seasonal changes of the trematode infection to be similar in the first and the second intermediate hosts. This similarity indeed transpires from the data on the dynamics of infection of the second intermediate hosts both in freshwater (Stromberg et al., 1978; Chubb, 1979; Lemly and Esch, 1984; Ménard and Scott, 1987; Marcogliese et al., 2001; Sandland et al., 2001; Wang et al., 2001; Jiménez-Garcia and Vidal-Martinez, 2005) and marine (Bowers and James, 1967; MacKenzie, 1985; Goater, 1993; Faliex and Morand, 1994; Meißner and Bick, 1997; Svårdh, 1999; Desclaux et al., 2006; Korniychuk, 2008b; Fermer et al., 2010) ecosystems. As a rule, this dynamics is described by a unimodal or a bimodal curve with a maximum in summer or in autumn, which coincides with the period of maximum cercarial emergence.

It is important that studies of seasonal dynamics of infection of intermediate hosts with trematode parthenitae and larvae usually do not exceed 1 or 2 years, exceptions being rare (Kennedy, 1981; Marcogliese et al., 1990; Esch et al., 1997; Ataev et al., 2002; Negovetich and Esch, 2007; Magalhães et al., 2020). The picture of the seasonal changes derived from such a (relatively) short study period might be distorted for two reasons: interannual variations (e.g. an anomalously hot or cold summer, an early or a late onset of the cold season etc.) and the impossibility to determine the duration of functional activity and existence of parthenitae groups in the infected molluscs. Besides, an overwhelming majority of studies of seasonal dynamics of parthenitae and metacercariae have been made in temperate and subtropical regions.

In the Arctic and the Subarctic (>60°N), where seasonal changes of the environment are the sharpest, studies of this kind are few and involve a limited number of trematode species (Rumyantsev, 1975; Rusanov and Galaktionov, 1984; Valtonen and Gibson, 1997; Galaktionov, 1992, Galaktionov, 1993; Galaktionov et al., 2006). Besides, in these regions there have been no attempts to find correlations between the seasonal dynamics of parasite prevalence in the first and the second intermediate hosts, that is, to explain the seasonal dynamics of infection of the second intermediate hosts with metacercariae on the basis of the analysis of (also seasonal) changes in the functioning of parthenitae groups in the first intermediate hosts. The scarce studies of this kind have been made only in freshwater (Etges, 1953; Campbell, 1973; Dronen Jr., 1978; Herrmann and Sorensen, 2009; Urabe et al., 2009; Flores et al., 2010) and marine ecosystems of the temperate (Kesting et al., 1996; Machkevsky et al., 1997; Fermer et al., 2010; Studer and Poulin, 2012; de Montaudouin et al., 2016) and subtropical (Al-Kandari et al., 2007) climatic belts.

The above gaps were an incentive for our long-term study aimed at revealing the features of the seasonal dynamics of parthenitae and metacercariae in, correspondingly, the first and the second intermediate hosts, accompanied by a detailed analysis of the composition of the parthenitae groups. Trematodes transmitted in the intertidal ecosystems of the White Sea near the polar circle were chosen as the objects. Information from this study area is important in the light of the ongoing climatic changes, which are especially pronounced in the Arctic and the Subarctic (Symon et al., 2005; Stocker et al., 2013). The determination of the main parameters of seasonal changes of the parasites’ transmission would allow an objective assessment of the impact of the forecasted climatic oscillations on these processes. Besides, there are reasons to believe that the seasonal changes in the infection levels would be more pronounced in the Subarctic than in temperate seas. This conjecture is based on the results of the studies of the same trematode species transmitted under different climatic conditions. For instance, the prevalence of sporocysts of Bacciger bacciger in molluscs Donax trunculus does not change seasonally in the subtropics (Ramadan and Ahmad, 2010) but shows pronounced seasonal fluctuations in the boreal waters (Delgado and Silva, 2018). The same pattern is observed for the prevalence of metacercariae of trematodes Proctoeces spp. in gastropod and bivalve molluscs: it changes seasonally in the temperate region (Lang and Dennis, 1976) but does not differ much throughout the year in the subtropics (Shimura, 1980; Calvo-Ugarteburu and McQuaid, 1998; Bretos and Chihuailaf, 1993).

Our study, spanning 11 years, was made on trematodes Himasthla littorinae Stunkard, 1966 and Cercaria parvicaudata Stunkard and Shaw, 1931. These species, which belong to the phylogenetically distant families Himasthlidae (Echinostomatoidea) and Renicolidae, correspondingly, are quite different in respect of morphology and biology of all life cycle stages but use the same host species (Stunkard and Shaw, 1931; Stunkard, 1966; Lauckner, 1983; our data). Their first intermediate hosts are molluscs from the genus Littorina (represented in our study by L. saxatilis and L. obtusata, common at the White Sea intertidal). The parthenitae developing in periwinkles produce cercariae. The latter leave the molluscan host and, in order to develop further, have to infect the second intermediate hosts, mussels (Mytilus edulis). The final hosts, seagulls, are infected by eating mussels containing infective metacercariae. Adult flukes formed in the gulls produce eggs with miracidia. The eggs are spread with the faeces, and the larvae hatching from them are the source of infection of the first intermediate hosts.