Numerically, meiofaunal prey dominated the diet of B. luteum and P. minutus in all seasons, was found seasonally in the diet of A. laterna and L. limanda and was absent in the diet of P. platessa between 10 and 20 cm body size. Thus, although sharing the same habitat, seasonal differences in meiofauna prey resources do exist between these small-sized demersal fish species. In terms of prey biomass, macrofaunal prey dominated in all fish diets reflecting the higher weight of macrofaunal compared to meiofaunal prey. For details on fish predation on macrofaunal prey groups, see Schückel et al. (2011) and Schückel et al. (2012).
Among different meiofaunal prey groups, harpacticoids were always of primary importance in the diet of each of the studied fish species during all seasons, whereas nematodes dominated the meiofauna community in the study area.
The meiofauna community in the study area
Nematodes were always the dominant meiofauna group in sediment samples in terms of abundance, while harpacticoids occurred most frequently. Seasonal differences were negligible for meiofaunal abundance but significant for biomass, due to a marked increase in harpacticoids in summer.
Previous research on meiofauna communities in the North Sea has also shown that nematodes are the dominant meiofauna group in terms of abundance accounting for at least 90 % of the total meiofauna (Juario 1975; Heip and Craeymeersch 1995). Their densities ranged from 61 to 4,167 ind./10 cm² and they were especially abundant in the southern North Sea (Huys et al. 1992). Harpacticoids ranked second in abundance, whereas other groups such as polychaetes, kinorhynchs, gastrotrichs, bivalves and ostracods were far less abundant (Juario 1975; Govaere et al. 1980; Heip et al. 1992; Heip and Craeymeersch 1995). Seasonally, meiofauna abundance generally peaks in spring and summer following an increase in food supply after the spring phytoplankton bloom, whereas abundance is low during autumn and winter, when most meiofauna groups live deeper in the sediment (Olafsson and Elmgren 1997). Only harpacticoids are known to occur most of the year, concentrated in the upper six centimetre of the sediment (Huys et al. 1986). However, in the area of investigation in the German Bight (“Box A”), seasonal changes of both abundance and occurrence of meiofauna groups were small. Only an increase in copepodite occurrence as well as of harpacticoid biomass was found during summer, probably triggered by reproductive activities of harpacticoid copepods and sufficient food supply due to phytoplankton sedimentation after the spring bloom (Rudnick et al. 1985).
Confirming previous results of the North Sea Benthos Survey (for details see Huys et al. 1992), epibenthic species belonging to the family Ectinosomatidae (mainly H. canaliculatum and P. minor) and Longipediidae (mainly L. coronata) dominated the harpacticoid community structure in the study area. The pelophilic species P. crassicornis (Ameiridae) as well as T. reducta (Idyanthidae) were also important in this community. In contrast, interstitial species were completely absent in the present study, although interstitial species belonging to the family Leptastacidae (mainly Leptastacus and Paraleptastacus) were described as characteristic species in previous studies (Heip et al. 1992). Leptastacus and Paraleptastacus are both known as interstitial sliders (Huys et al. 1992), probably able to penetrate deeper into the sediment than the first five centimetre, which were sampled here.
Seasonally, abundances of Ectinosomatidae and Longipediidae differed significantly, being highest for P. minor and H.
canaliculatum between October and May but lowest in July, whereas the reverse with a peak in abundance in July was found for L. coronata.
Such seasonal changes of harpacticoid densities are mostly observed in vertical distribution patterns, which are caused by migrations in response to seasonal fluctuations in environmental parameters (e.g. oxygen, salinity) and physiological adaption such as changes in growth rate and fecundity in response to environmental pressures. More details in terms of species-specific migration patterns in harpacticoids will be given in the section below directly related to its function as potential prey source for the studied demersal fish.
Meiofauna as prey source of demersal fish
Diets of B. luteum and P. minutus were numerically dominated by harpacticoids during all seasons. Such a dominance of harpacticoid prey throughout the seasons has also been reported for B. luteum in the Western Mediterranean (Tito de Morais and Bodiou 1984) and the Scottish coast (Nottage and Perkins 1983) and for several gobiid species in the North Sea (Zander 1979), in the Adriatic Sea (Kovačić 2001, 2007; Kovačić and la Mesa 2008) and in the Gulf of Mexico (Fitzhugh and Fleeger 1985). Other meiofaunal prey groups (juvenile bivalves, ostracods and nematodes) became important in their diets only in May, indicating a seasonal change in prey preferences during spring. Constrained by their small mouth gapes and a more sediment surface-orientated feeding strategy, B. luteum and gobiids catch very small benthic prey buried in the top few centimetres of the sediment or living very close to the sediment surface, which represents the habitat of most harpacticoids (Tito de Morais and Bodiou 1984; Darnaude et al. 2001). Furthermore, their caloric values are 35 % higher than those of most other meiofaunal groups (Gee 1989). Consequently, the relatively low costs of capturing harpacticoids and their relatively high caloric content turn them into a more energy-efficient prey. However, the seasonal trend to meet energy requirements in spring also by eating other meiofauna prey groups (e.g. bivalves) as well as macrofauna was also confirmed for P. minutus in the Baltic Sea, even though harpacticoids always comprised the most important prey group in each season (Aarnio and Bonsdorff 1993).
Meiofauna was more important as a seasonal prey source in the diet of A. laterna and small-sized L. limanda. Meiofauna mainly characterized the diet of A. laterna during winter, dominated by harpacticoids in terms of occurrence as well as abundance. In contrast, harpacticoids dominated the diet of L. limanda spring and summer. Similar to both fish species discussed before, juvenile bivalves became an important prey group in spring. On the basis of their mouth morphology, it can be assumed that A. laterna and L. limanda are able to feed on larger and hence more energetically valuable prey (Piet et al. 1998; Schückel et al. 2011, 2012). Consequently, mainly macrofaunal prey (e.g. crustaceans and polychaetes) comprised the diets of both fish species, whereas meiofaunal prey seems to be of less diet importance. Confirming this, preferential feeding on macrofauna was also found in previous diet studies for both fish species (e.g. Gibson and Ezzi 1980; Bayan et al. 2008; Schückel et al. 2011) and furthermore, was already found in relatively small fish (L
T’s < 10 cm; Schückel et al. 2012).
However, a reduced feeding activity of A. laterna in winter resulting in low stomach functions and low mobility, together with a reduced availability of larger benthic prey in the field, may have caused the observed increasing numbers of harpacticoids in the January stomachs. Assuming for dab a rather weak condition in spring after the winter feeding pause and the spawning period (Knust 1986; Hinz et al. 2005), harpacticoids may also provide an easily available and nutritious prey to fulfil energy requirements.
Increasing abundances of juvenile bivalves in all fish diets in May indicated a match with spawning periods of bivalves in this area (Beukema et al. 1998; Reiss and Kröncke 2004). The subsequent decrease of juvenile bivalves in occurrence, abundance and biomass in the field during summer might be due to predation pressure of the studied fish species. Similar results of a strong predation pressure on juvenile bivalves after spawning was also found for small plaice in the Baltic Sea (Olafsson and Elmgren 1997) and for gobiids in the Adriatic Sea (Kovačić and la Mesa 2008). Thus, seasonal changes of meiofauna in the diet composition of small demersal fish could be the result of seasonal availability of suitable meiofaunal prey (see Tables 2, 3).
Although nematodes represented, depending on season, between 93 and 98 % of the total number of individuals in the sediment, they were completely absent in the flatfish diets but, interestingly, they occurred in almost each season in the diet of P. minutus (see Table 5). This agrees well with the literature showing that harpacticoids are usually the most abundant prey group in the fish diets, whereas nematodes dominate the sediment (e.g. Gee 1989 and references therein). Food selection of demersal fish depends on the availability of the prey, which is mainly determined by its density, visibility, accessibility and mobility (Nelson and Coull 1989). Feeding of the studied fish on meiofauna was mainly focused on harpacticoids living on or near the sediment surface, whereas nematodes have a deeper vertical distribution (Aarnio and Bonsdorff 1993; Aarnio 2000). Another factor that may explain the absence of nematodes in the stomachs could be differences in digestion rates for these two taxa. Harpacticoids have an exoskeleton that is slowly digested and remains in the gut for several hours after ingestion, while nematodes are soft-bodied and are digested rapidly (Alheit and Scheibel 1982; Scholz et al. 1991), thus probably giving a false impression of diet composition. A third explanation implies that physical disturbance caused by searching fish in the sediment may have suspended nematodes from the uppermost sediment layer or swept them away (Fitzhugh and Fleeger 1985; Gee 1989). This last explanation, regarding our study, also indicates best why, on the one hand, nematodes are absent in the flatfish diets, but on the other hand, are a dominant prey item in the goby diet. Similar findings of nematodes in gobiid stomachs were also reported for P. minutus and P. lozanoi in the North Sea (Fonds 1973) as well as for two closely related gobiids in the Gulf of Mexico (Fitzhugh and Fleeger 1985). The latter assumed that gobies graze sediments more or less indiscriminately in addition to sight feeding for larger prey. This rather passive feeding strategy in searching prey may contradict with a more active visual feeding strategy of flatfish remaining motionless on the bottom at first, and then periodically lunging rapidly forward, causing the upper sediment layers to float in suspension (de Groot 1971; Hoghue and Carey 1982). Also morphological differences (e.g. body shape, mouth gape) between gobiids and pleuronectids may enable P. minutus to penetrate in deeper sediments.
Prey selectivity
Fish predation on harpacticoids was highly selective for the two species Pseudobradya spp. and Longipedia spp. Pseudobradya spp. was found almost exclusively in fish stomachs in winter, whereas Longipedia spp. dominated the stomach contents between spring and autumn.
Selective feeding on harpacticoid species seems to be common in many fish species. For instance, Alheit and Scheibel (1982) showed exclusive feeding on L. helgolandica by predatory fishes in a Bermudan lagoon. Hicks (1984), in his study of flatfish feeding on intertidal sandflats in New Zealand, also found exclusive feeding on one harpacticoid species (P. megarostrum). For B. luteum from the Mediterranean, a marked preference for Pseudobradya beduina was described, whereas the goby D. quadrimaculatus from the same habitat fed exclusively on H. canaliculatum (Tito de Morais and Bodiou 1984).
Firstly, by comparing the meiofauna community in the sediment with that in the fish stomachs, it becomes clear that the studied fish species fed almost exclusively on the most abundant harpacticoids in the sediment. Thus, fish predation on Pseudobradya spp. in winter and Longipedia spp. in summer may merely reflect their high prey densities in the field. Contradictory to this, Ivlev’s high selection values for all studied fish species on both harpacticoids clearly suggested a positive prey selection.
Secondly, harpacticoids differ in vertical distribution within the sediment. By dwelling in the uppermost sediment layers, Pseudobradya spp. and Longipedia spp. are more vulnerable to predation compared to deeper interstitial or burrowing species (Gee 1987). Consequently, interstitial species, such as B. aemula (also known to build a tube into which it retreats when disturbed; Huys et al. 1986) and E. propinquum, were negatively selected. Only the upward migration in the sediment of B. aemula during summer leads to an increase in fish predation (Huys et al. 1986), explaining the positive prey selection for this harpacticoid in the diet of B. luteum only in July.
Moreover, Pseudobradya spp. and Longipedia spp. are both emergers, swimming into the overlying water (typically during the night) and returning to the seabed during the day (Sedlacek and Thistle 2006). Thus, Pseudobradya is classified as a moving water emerger during all seasons, whereas Longipedia moves in the water column mainly in summer (Thistle 2003), leading to a greater susceptibility of Longipedia sp. for visual predators during summer. Diets of the studied fish species changed towards an intensively feeding on Longipedia spp. in July, even though Pseudobrayda spp. also occurred in high abundances in the sediment. In this context, prey selection on Longipedia spp. could also be prey size dependent. Longipedia spp. is significantly larger (mean length, 0.9 mm; own data), compared to Pseudobradya spp. (mean length, 0.4 mm; own unpubl. data), and consequently more favourable as a source of energy compared to Pseudobrayda spp. Such a prey size selection was also found by McCall (1992) for juvenile flounder, mainly feeding on the largest available harpacticoids.
Size aspects
The relative contribution of meiofauna and macrofauna to the diet composition of fish depends mostly on predator size (e.g. Gee 1989; Kovačić and la Mesa 2008; Schückel et al. 2012). On the basis of the optimal foraging theory, smaller fish eat smaller prey and switch usually to larger prey to maximize their net energy gain as fish length increases (Schoener 1971). Confirming this, harpacticoids as the prevalent meiofaunal prey rapidly decreased in terms of frequency of occurrence as well as numerical abundance in the diets of all studied fish species with increasing fish size. Interestingly, threshold lengths at which the importance of harpacticoid prey decreased differed for the studied species. The abundance of harpacticoid prey decreased already at relatively small individual size in A. laterna and P. minutus (3–4 cm L
T), whereas they were still abundant prey for B. luteum also at larger fish sizes (8 cm L
T). Similar results were described for gobies B. affinis in the Adriatic Sea (Kovačić and la Mesa 2008) and for P. minutus in the Baltic Sea (Aarnio and Bonsdorff 1993), indicating significant differences between the diet of large- and small-sized individuals, switching from meiofaunal to macrofaunal prey at approximately 3–4 cm L
T, respectively. Harpacticoids in the diet of the goby D. quadrimaculatus, still constituting 50 % in the total diet at 3 cm fish length, decrease to almost 0 % in individuals up to a fish length of 5 cm (Tito de Morais and Bodiou 1984). Predominant feeding on harpacticoids was also found in A. laterna as well as for the closely related A. thorni with L
T’s between 5 and 6 cm, but changing rapidly towards polychaetes and fish prey at larger size (Bayan et al. 2008). In contrast, for a B. luteum population on the Scottish coast, harpacticoids were still an important prey in the diets of individuals reaching fish lengths of 8 cm L
T (Nottage and Perkins 1983). Mainly morphological constraints (e.g. mouth gape, jaw structures) determine the threshold length for fish below which meiofauna are of no value as prey. In most flatfish species and gobiids, this threshold length is about 3 cm (total fish length). Above this size, macrofauna are always the dominant prey, whereas below this size, harpacticoids can constitute between 20 and 100 % (Gee 1989). Mouth gape widths differed between the studied fish species, being generally larger for P. minutus and A. laterna and smaller for B. luteum (Piet et al. 1998). Consequently, harpacticoids as prey resource were also used by B. luteum at larger fish sizes.