Temporal changes in lipid condition and parasitic infection by digenean metacercariae of young-of-year common sole Solea solea (L.) in an Atlantic nursery ground (Bay of Biscay, France)

Abstract

Little attention has been paid to flatfish parasitism as a potential factor of variation in year-class strength. The aim of this study was to evaluate the relationship between parasitic infection and nutritional condition of young-of-year (YOY) common sole. Sole were collected monthly from May (early settlement) to November 2004 in a mussel pole culture area, using a push-net or a trawl, and dissected for parasite identification and counts. Total lipids were extracted from the whole body and lipid classes quantified. Triacylglycerols to sterols (free form) ratio (TAG/ST) was used as an index of nutritional status. Digenean metacercariae infection, characterized by two dominant genera, displayed clear seasonal dynamics and the highest records yet reported for sole. Prevalence (P%) and mean abundance (Ab ± SE) increased for Timoniella spp. (Acanthostomidae) from May (P% = 22%; Ab = 1.9 ± 1.1) to August (P% = 100%; Ab = 51.2 ± 10.4), and for Prosorhynchus spp. (Bucephalidae) from June (P% = 8%; Ab = 0.1 ± 0.0) to August (P% = 100%; Ab = 19.5 ± 1.7). Epidemiological values reached a plateau after August. In this shellfish-dominated nursery area, YOY sole accumulated metacercariae in the presence of the first intermediate hosts which live in the same habitat. Total lipids decreased significantly from May to June and then remained constant until autumn, indicating a change in the proximate composition of YOY during this high growth period. Mean (± SD) TAG/ST ratio increased from very low values in May–July (0.10 on average) to a peak in September (0.57 ± 0.31) and then fell back to values as low as before. YOY sole only stored energy as TAG prior to autumn. No relationship was found between YOY parasitic infection levels and lipid condition indices. However, the poor nutritional status and heavy infection level observed in November could dramatically lower over-winter survival of the YOY remaining in this shallow part of the nursery.

Introduction

Coastal areas, such as estuaries and shallow water bays, serve as nurseries for juveniles of many marine fish species and especially flatfishes. Growth and survival of juvenile flatfish in these essential habitats is generally good, due to abundant food, low predation risks and higher temperatures than in offshore areas (Bergman et al., 1988, Gibson, 1994). Nevertheless, nursery grounds are subject to highly variable environmental and anthropogenic factors (Yamashita et al., 2001). Conditions encountered by juveniles in coastal nurseries are therefore thought to greatly influence their growth and survival, via physiological mechanisms, and thus influence recruitment in the adult population (Gibson, 1994, Van der Veer et al., 1994, Yamashita et al., 2001). Fundamental factors - such as temperature, oxygen, salinity, food availability, density, predation, river plume extension and pollutants - are known to affect growth, condition and survival, and are therefore taken into account when estimating nursery quality (Gibson, 1994, Van der Veer et al., 1994, Van der Veer et al., 2001, Nash and Geffen, 2000, Yamashita et al., 2001, Le Pape et al., 2003a).

Parasites have been shown to be able to regulate host populations (Anderson and May, 1978, May and Anderson, 1978). They can affect both physiology and ecology of their hosts (growth, condition, survival, fecundity, behaviour) and thus their fitness (Combes, 2001). However, despite the importance of parasitism in ecology, this factor is rarely taken into account in fish ecology and even less in flatfish ecology. Like other small fishes, young flatfishes are subjected to parasitism in nursery grounds, especially from digenean trematodes for which they can act as second intermediate hosts. Digeneans have a complex life cycle, which in marine environment follows the general scheme of having molluscs as first intermediate hosts, small fishes as second intermediate hosts and piscivorous fishes as definitive hosts (Cribb et al., 2001). Cercariae actively penetrate the skin of their second intermediate host and encyst as metacercariae in the body. Transmission to the definitive host then occurs through predation. Metacercariae, like all parasitic stages, are metabolically dependent on their host and use some of their host's energy for their own development and maintenance. Although studies on the effects of digenean metacercariae on fish are scarce, some have shown a clearly negative impact of these parasites on growth, condition and survival of freshwater fishes (Lemly and Esch, 1984, Coleman and Travis, 1998, Johnson and Dick, 2001, Collyer and Stockwell, 2004). Parasitism is thus a factor that could potentially influence habitat quality of juvenile flatfishes.

Common sole is a commercially important and widely distributed flatfish of the North-East Atlantic. Parasitic infection of juvenile sole by Prosorhynchus spp. (Digenea, Bucephalidae) metacercariae has recently been reported in the Pertuis Charentais (Laffargue et al., 2004). This area represents an important nursery ground for the common sole stock of the Bay of Biscay, both in terms of density and potential surface area (Le Pape et al., 2003b). However, Le Pape et al. (2003c) also showed that juveniles in this nursery ground had a lower mean size during winter, which indicates the poor quality of the area.

Changes in nutritional status and growth of juveniles may reflect their probability of survival in the nursery grounds. Lipid depletion has been identified as a general metabolic response to stress and a response to parasites also (Lemly and Esch, 1984, Lemly, 1997). Total lipid content of a fish is an easy estimation of its physiological condition, but fractionation into individual lipid classes provides a more sensitive measurement of metabolically available lipids and energy allocation (Norton et al., 2001). Lipid class composition has therefore been used to measure the nutritional status of fish at early life stages (Fraser, 1989, Häkanson, 1989, Lochmann et al., 1995, Norton et al., 2001). A nutritional index based on the ratio between quantities of triacyglycerols (TAG: lipid reserves) and free sterols (ST: structural lipids) (TAG/ST) has been used to investigate the nutritional status of sole larvae (Galois et al., 1990, Amara et al., 2000, Amara and Galois, 2004).

In this study, we used both morphometric (Fulton's K) and biochemical condition indices (total lipid content and TAG/ST) to investigate the effect of parasitism on young-of-year (YOY) sole condition in the Pertuis Charentais. Our aims were to simultaneously analyze changes in infection by digenean metacercariae and the condition of YOY sole from the early settlement period until the onset of winter in the nursery.