Trophodynamics of two interacting species of estuarine mysids, Praunus flexuosus and Neomysis integer, and their predation on the calanoid copepod Eurytemora affinis

Journal of Experimental Marine Biology and Ecology 308 (2004) 127 – 146 www.elsevier.com/locate/jembe

Trophodynamics of two interacting species of estuarine mysids, Praunus flexuosus and Neomysis integer, and their predation on the calanoid copepod Eurytemora affinis Gesche Winkler a,*, Wulf Greve b a

De´partement de Biologie, Universite´ Laval, Sainte-Foy, Que´bec, Canada G1K 7P4 b Forschungsinstitut Senckenberg, Notkestrahe 31, 22607 Hamburg, Germany

Received 1 September 2003; received in revised form 10 February 2004; accepted 26 February 2004

Abstract Community structure is shaped by external factors (i.e., habitat, temperature, and food) frequently modified by interactions among its members. This study focusses on trophic interactions between two sympatric mysids Praunus flexuosus and Neomysis integer of the Elbe Estuary, northern Germany. Based on an experimental approach, intraguild predation was evaluated. Predation rate of P. flexuosus on N. integer was positively related to predator size and temperature. Predation rate was significantly correlated with prey size, juvenile N. integer released just from the mysid marsupium being most vulnerable. However, adult P. flexuosus were able to gain more energy in terms of body carbon by catching larger N. integer, whereas immature P. flexuosus assimilated more energy by capturing large numbers of the small-sized N. integer. In contrast to N. integer, P. flexuosus showed an efficient escape behaviour that prevented all stages of N. integer from preying on any size class of P. flexuosus. When Eurytemora affinis was offered as prey, both N. integer and P. flexuosus increased predation rates with predator size and temperature. In mixed prey (N. integer and E. affinis) experiments at 10 jC, predation rates of adult P. flexuosus on N. integer released just from the marsupium declined from 17 F 8 to 6 F 4 N. integer mysid 1 day 1. We conclude that intraguild predation exists between the two species but is one sided with small N. integer being strongly suppressed. This heavy predation pressure is modified by the addition of alternative food resources, in this case, E. affinis. D 2004 Elsevier B.V. All rights reserved. Keywords: Age structure; Mysidacea; Eurytemora affinis; Intraguild predation; Neomysis integer; Praunus flexuosus

* Corresponding author. Tel.: +1-418-656-2131x6140; fax: +1-418-656-2339. E-mail address: [email protected] (G. Winkler). 0022-0981/$ - see front matter D 2004 Elsevier B.V. All rights reserved. doi:10.1016/j.jembe.2004.02.017

128

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

1. Introduction Food web complexity is a function of multiple factors including taxonomic diversity, life history strategy, and trophic specialization (Greve and Reiners, 1996). Detailed knowledge of interspecific trophic linkages provides a tempting descriptor of community structure and function (Paine, 1980). Therefore, we focussed on a particular aspect of trophic interactions by evaluating a simplified feeding guild in the Elbe estuary ecosystem in northern Germany. A guild, as defined by Root (1967) and Polis et al. (1989), describes a group of different species sharing the same habitat, environment, and food resources. Furthermore, in size-structured populations, different age classes can act as separate guild members, and their interactions play an important role in the organisation of their communities (Wissinger, 1992). In particular, intraguild predation, defined as the killing and eating of species that use similar resources (Polis et al., 1989), has been shown to be important for the distribution and survival of mysids (Wooldridge and Webb, 1988) and other crustacean populations (Greve, 1977; Dick and Platvoet, 1996). We chose to study intraguild predation in mysids as they occupy an important position in many food webs due to their high abundance, flexible foraging strategies, and their importance as a food resource for other animals. Mysids are omnivores (Blegvad, 1922) that adapt their feeding behaviour depending on the food availability (Depdolla, 1923; Siegfried and Kopache, 1980; Viitasalo et al., 1998) and as such form a link between benthos, nekton, and plankton (Mauchline, 1980; Fulton, 1982a,b). When herbivorous and detrivorous, they are filter feeders (Lasenby and Langford, 1973; Zelickman, 1974; Webb et al., 1987), but as carnivores, they switch to either a filter or raptorial feeding method depending on size and behaviour of the prey (Wooldridge and Webb, 1988; Viitasalo and Rautio, 1998). Predation of small zooplankton by mysids is well documented (e.g., Bowers and Vanderploeg, 1982; Grossnickle, 1982; Fulton, 1985), whereas interspecific predation within the taxon Mysidacea is only described for Rhopalophthalmus terranatalis and Mesopodopsis slabberi in South Africa (Wooldridge and Webb, 1988). Intraspecific predation is also documented (Kuhlmann, 1982; Jansen, 1985; Winkler, 2000). Mysids provide an important food resource for commercially exploited fishes such as herring, cod, flatfishes (Arndt and Jansen, 1986; Fiedler, 1991; Thiel, 1992), small benthic gobies (Zander and Hagemann, 1986, 1987), and shrimps (Winkler, 1994; Pezenburg, 1998). Commercial fisheries of mysids exist in Japan (Omori, 1978). In the Elbe Estuary, the macrozooplankton is characterised by six mysid species and one shrimp species (Ku¨hl, 1964; Ko¨pcke and Kausch, 1996). The calanoid copepod, Eurytemora affinis dominates the mesozooplankton, representing between 30% and 50% of total numbers depending on season. Less frequent are Acartia spp. (1– 8%), cyclopoid (5– 8%), and harpacticoid copepods (0.6 – 15%). Rotifers also form a frequent taxon (30 – 38%) of the mesozooplankton. Bosmina longirostris is the most abundant cladoceran (0.3 – 4%). Within the summer months, meroplankton such as cirripedia, polychaetes, gastropods, bivalves, echinoderms, and bryozoans (Koepcke, 2002) may represent up to 5.8% of mesozooplankton community. The most important primary producers are Chlorophyceae and Bacillariophyceae, although concentrations of these taxa are exceeded by micro- and macroaggregates (Wolfstein and Kies, 1995; Zimmermann-Timm, 2002).

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

129

Based on this plankton community, this study focuses on predation between the two dominant co-occuring members of the macrozooplankton, Praunus flexuosus and Neomysis integer and the dominant copepod species, E. affinis. P. flexuosus and N. integer have different life history traits. They have different sequences of generations based on development time and size, maturity timing, and the number and size of offspring (Winkler and Greve, 2002). However, both species are known to be omnivorous. Filamentous algae, fragments of macroalgae, diatoms, and detritus occurred in the stomachs of both species, but these food items are less important than animal food. The dominant portion of their diet consists of crustaceans, especially copepods such as E. affinis (P. flexuosus: Blegvad, 1922; Mauchline, 1971; Viitasalo and Rautio, 1998; N. integer: Kinne, 1955; Jansen, 1985; Fockedey and Mees, 1999). Cannibalism was also found in both species (Kuhlmann, 1982; Winkler, 2000). Similar feeding habits between the two species indicate a high niche overlap in their food resources and lead us to hypothesise intraguild predation behaviour. In this study, the guild consisted of several cohorts of both of P. flexuosus and N. integer. Due to its dominance in mysid diet, we chose E. affinis as the common animal food resource. The purpose of this paper is to investigate the amount of predation between two sympatric mysid species in relation to their ontogeny, behaviour, and an alternative food resource. We initiated a laboratory-based investigation to evaluate possible food web interactions between different developmental stages of N. integer and P. flexuosus and one of their most common prey species, E. affinis. Three trophic interaction experiments were carried out: (1) interspecific predation experiments with P. flexuosus as predator and N. integer as prey; (2) separate feeding experiments with mysids as predators and E. affinis as prey; and (3) mixed feeding experiments with P. flexuosus and both prey species present With this design we describe the most contrasting conditions. In the absence of E. affinis, we expect intraguild predation to be maximal, whereas in the presence of high densities of a further food resource, minimum potential of predation for a special prey – predator combination may be shown. We then interpreted the trophic relationships between guild members and their food resource in terms of relative importance to population dynamics of both mysid species in their natural habitat.

2. Materials and methods Specimens of P. flexuosus and N. integer were caught in the outer Elbe Estuary using a 1-m-diameter plankton net (1000 Am mesh) and a Tucker trawl (500 Am) from the research ¨ RN of the Biologische Anstalt Helgoland in April, June, and August 1998. vessel UTHO To minimise damage to the mysids, each haul lasted only 3– 5 min. The net was towed horizontally approximately 4 m above the bottom. The mysids were concentrated in 30l plastic containers, and then rapidly transported to the laboratory. In the laboratory, the mysids were acclimated to experimental conditions in Plexiglas culturing jars with a rotating water jet to retain any mysid that jumped out of the water. A sand and gravel filter was used to regenerate the circulating water. The mysids were kept in 20 psu salinity

130

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

seawater at temperatures of 10 and 15 jC. These reflect spring/autumn and summer conditions respectively in the outer Elbe Estuary. The mysids were fed surplus levels of newly released (1– 3 days old) Artemia salina, frozen pieces of mysids and live E. affinis, the dominant copepod prey in the Elbe Estuary. E. affinis for feeding experiments was caught using a 0.5-m-diameter plankton net (330 Am mesh) from a quay in the estuary near Brunsbu¨ttel and was acclimated in the manner described above. These catches consisted mainly of E. affinis copepodid stages III –VI. 2.1. P. flexuosus predation on N. integer Preliminary predation experiments on 34 different combinations of size classes of P. flexuosus/N. integer demonstrated trophic interaction between the two species (Winkler, 2000). However, N. integer was not able to feed on any size class of P. flexuosus due to the avoidance reflex of newly released P. flexuosus, which is already completely developed (Berrill, 1971). On this basis, we designed our predation experiments exclusively with P. flexuosus as predator. A semi-continuous design was chosen; one predator and five prey organisms were maintained in a 1-l beaker for 12 h. We re-established the original prey density every 2 h. Jerling and Wooldridge (1995) observed an increase in filtration rate of zooplankton which decreased at a container size of 500 ml and stayed constant in containers of 1000 ml. Experimental containers of these sizes are commonly used in predation experiments with mysids (Fulton, 1982a,b; Aaser et al., 1995; Viitasalo et al., 1998, 2001). Prey densities of five N. integer were chosen based on the results of Wooldridge and Webb (1988). They found constant clearance rates in R. terranatalis and M. slabberi, with initial prey densities of 5 – 10 juvenile mysids l 1. Gorokhova and Hansson (1997) showed constant consumption rates of Mysis mixta after 10 h so that we conducted our experiments over 12 h. The predator/prey ratio was found to be up to 1:10 at the sampling station, but densities appeared to be one magnitude lower in the estuary than in the experiments (Winkler, unpublished data). Our experimental design is simplified such as it excludes turbidity and turbulence, common factors in the Elbe Estuary, which are likely to have an effect on prey encounter rates. We could not observe any wall effect due to beaker size which had influenced capture or escape activities of predator and prey. To discriminate ontogenetic changes in predation, two developmental stages of P. flexuosus were observed; immature (9– 16 mm) and adult (17 – 25 mm) individuals. Juveniles ( < 9 mm) were excluded because they did not prey on N. integer in preliminary experiments (Winkler, 2000). To investigate the predation rate of P. flexuosus as a function of prey size, we presented six size classes of N. integer ranging from newly released juveniles to immature individuals (2.0 – 2.9 mm; 3.0– 3.9 mm; 4.0– 4.9 mm; 5.0– 5.9 mm; 6.0– 6.9 mm; and 7.0 –7.9 mm). At the beginning of each experiment, size classes of both predators and prey were sorted by eye and their precise lengths were measured at the end of each experiment. The number of replicates ranged from 4 to 37. Some experimental predator – prey – temperature combination were missing due to a lack of specimens in these size classes (Table 1). The effect of temperature on predation rates were evaluated by conducting experiments at 10 and 15 jC.

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

131

Table 1 Number of experimental replicates of prey (N. integer) size class per developmental stage of the predator (P. flexuosus) and two temperatures Number of replicates P. P. P. P.

flexuosus flexuosus flexuosus flexuosus

N. integer (mm)

immature mature immature mature

2.0 – 2.9

3.0 – 3.9

4.0 – 4.9

5.0 – 5.9

6.0 – 6.9

7.0 – 7.9

Temperature (jC)

11 19 16 23

11 20 14 37

6 11 10 5

5 m 8 25

m 19 m 17

m m m 4

10 10 15 15

‘‘m’’ indicates that in combination of developmental stage/temperature, no experiments were carried out.

2.2. Predation of P. flexuosus and N. integer on the calanoid copepod E. affinis Predation on E. affinis copepodids (stages III – VI, 0.6– 1.2 mm pleon length) was determined for several developmental stages of P. flexuosus and N. integer at both 10 and 15 jC. Experiments for juvenile N. integer at 10 jC were not conducted because no juvenile individuals were available. Beaker size was chosen based on predator size. Juvenile P. flexuosus and all size classes of N. integer were placed in 500-ml beakers, while 1000-ml beakers were used for immature and adult P. flexuosus. In experiments with P. flexuosus, each beaker contained one predator and was replicated 7 –27 times per age class and temperature (Table 2). Five juvenile, three immature and one adult N. integer were added to experimental containers (500 ml), based on the ability to detect low feeding rates of the smallest individuals. Numbers of replicates varied from 5 to 29 (Table 2). A mean density of 440 ( F 40 S.D.) E. affinis l 1 were introduced into each experimental beaker at the beginning of the experiments. To determine maximum predation rates in relatively small experimental beakers, experimental densities represented double the maximum observed field abundance. In the Elbe Estuary, maximum abundance of copepodids and adults occur in April and September with ca. 200 individuals l 1 (Koepcke, 2002). The experiments continued for 24 h. Table 2 Predator densities, beaker size, and number of replicates for P. flexuosus and N. integer on E. affinis at two temperatures Predator density (individuals beaker

1

)

Beaker size (ml)

Number of replicates 10 jC

15 jC

P. flexuosus (mm) Juveniles (5.0 – 8.9) Immatures (11.0 – 16.9) Adults (17.0 – 25.9)

1 1 1

500 1000 1000

15 7 15

21 27 23

N. integer (mm) Juveniles (4.0 – 4.9) Immatures (5.0 – 6.9) Adults (8.0 – 16.9)

5 3 1

500 500 500

m 6 29

6 5 13

‘‘m’’ indicates that in combination of developmental stage/temperature, no experiments were carried out.

132

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

2.3. Predation of P. flexuosus on a mixed N. integer and E. affinis prey assemblage Each experiment was run for 12 h in a 1000-ml beaker containing 1 predator (P. flexuosus), 5 juvenile N. integer, and 440 ( F 40 S.D.) E. affinis at a water temperature of 10 jC. Density of N. integer was re-established every 2 h, but the prey density of E. affinis was not manipulated as in the earlier experiments. We tested predation of two P. flexuosus size classes, immature and adult (as described above), with the 2– 2.9 mm size class of N. integer. Bigger prey of 5– 5.9 mm was presented only to adult P. flexuosus. To validate

Fig. 1. Predation expressed first (axis left) as predation rates (individuals mysid 1 day 1; mean F S.D.) of P. flexuosus and second (axis right) as predation pressure on N. integer (% loss to predation; mean F S.D.) in relation to (A) temperature and (B) prey size (N. integer). ‘‘0’’ indicates that no predation occurred. Different letters indicate significant LS-means differences ( p < 0.05).

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

133

possible predation of E. affinis by the second prey species N. integer, three control experiments were carried out for each N. integer size class (excluding P. flexuosus). For newly released N. integer (2 – 2.9 mm) observed at 10 jC over 12 h, we did not detect any predation on E. affinis, presumably because most of the E. affinis copepodids were too big IV – VI. Predation rates of immature N. integer in the control experiments were low (10 F 8 E. affinis N. integer 1 12 h 1), and we corrected the predation rates of P. flexuosus in the mixed experiments by the predation rate of immature N. integer. 2.4. Data analysis Predation rates (individuals mysid 1 day 1), specific ingestion rates (% body carbon (C) mysid 1 day 1), and predation pressure (% loss to predation) are described as means F S.D. We used three-way factorial ANOVA with unbalanced replication with rank data (Zar, 1996) to compare predation rates, specific ingestion rates, and predation pressure of P. flexuosus in relation to predator size (P. flexuosus), prey size (N. integer), and temperature (10 and 15 jC). We excluded predation experiments of largest prey size (7.0 – 7.9 mm) from the ANOVA, since only a single predator stage – temperature combination was tested for this prey size class (Table 1). P. flexuosus and N. integer predation on E. affinis and mixed prey experiments were compared with two-way factorial ANOVA with rank data. Post hoc comparisons were carried out with least square means. All ANOVA’s were processed with the SAS-System (Zar, 1996). Table 3 Comparison of (A) predation rate (individuals mysid 1 day 1) and (B) specific ingestion rate (% body C day of P. flexuosus on several size classes of N. integer by a three-way factorial ANOVA with rank data

1

)

Source of variation

df

MS

F value

p

(A) Predation rate on N. integer Temperature (10 jC, 15 jC) Predator: P. flexuosus (im, ad) Prey: N. integer (size classes: 2 – 6) Temperature  Predator Temperature  Prey Predator  Prey Temperature  Predator  Prey Error Corrected total

1 1 4 1 4 4 1 224 240

6763.28 106,774.16 104,808.18 10.32 2682.29 3692.90 64.18 1410.34

4.80 75.71 74.31 0.01 1.90 2.62 0.05

0.030 < 0.0001 < 0.0001 0.932 0.111 0.036 0.833

(B) Specific ingestion rate Temperature (10 jC, 15 jC) Predator: P. flexuosus (im, ad) Prey: N. integer (size classes: 2 – 6) Temperature  Predator Temperature  Prey Predator  Prey Temperature  Predator  Prey Error Corrected total

1 1 4 1 4 4 1 224 240

3436.47 1191.53 18,952.39 12,417.71 5710.04 21,110.16 979.95 3136.86

1.10 0.38 6.04 3.96 1.82 6.73 0.31

0.296 0.538 < 0.0001 0.048 0.126 < 0.0001 0.577

Developmental stages are represented by im: immature and ad: adult.

134

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

We used length/weight regression equations established by Winkler (2000) for N. integer (dry weight = 0.0016 total length3.086; R2 = 0.97; N = 201) and P. flexuosus (dry weight = 0.0015 total length3.062; R2 = 0.97; N = 180) to calculate dry weight. Carbon content was estimated to be 30% of the dry weight of the mysids (Raymont et al., 1964). We used carbon content to calculate specific ingestion rates (% body carbon (C) mysid 1 day 1) to compare the quantity of food intake between size classes and species. We

Fig. 2. Specific ingestion rates (% body C mysid 1 day 1; mean F S.D.) of two developmental stages of P. flexuosus in relation to (A) temperature and (B) prey size (N. integer). ‘‘0’’ indicates that no predation occurred. Different letters indicate significant LS-means differences ( p < 0.05).

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

135

estimated dry weight of various copepodid stages of E. affinis by measuring cephalothorax length and using biometrics of E. affinis (dry weight = 10(2.44 log(cephalothorax length) 6.095)) (Escaravage and Soetaert, 1993). Carbon content was estimated to be 50% of dry weight (Lenz, 1974).

3. Results 3.1. P. flexuosus predation on N. integer Results of a three-way factorial ANOVA with rank data indicated that temperature affected predation rates (Fig. 1A; Table 3A). P. flexuosus predation as a function of prey size showed that immature P. flexuosus had a maximum predation rate on 2 mm N. integer.

Fig. 3. Predation rate (individuals mysid 1 day 1; mean F S.D.) on E. affinis (A) of two developmental stages of P. flexuosus and of two developmental stages of N. integer in relation to temperature. Specific ingestion rates (% body C mysid 1 day 1; mean F S.D.) on E. affinis (B) by two developmental stages of P. flexuosus and two developmental stages of N. integer in relation to temperature. ‘‘m’’ indicates that in this developmental stage no experiments were carried out. Different letters indicate significant LS-means differences ( p < 0.05).

136

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

Rates of consumption of N. integer >3-mm were very low, indicating their inability to capture older developmental stages (Fig. 1B). In contrast, adult P. flexuosus were able to prey on a broader size range of N. integer (2 to 6 mm) than immature stages (Fig. 1B). In general, predation rates of P. flexuosus decreased significantly with increasing prey size (Fig. 1B). Predation rates of adult P. flexuosus were significantly greater than those of immature individuals, except predation rate on 6-mm prey, which was low in both developmental stages of P. flexuosus (Fig. 1B). Predation pressure at 10 jC was significant lower that at 15 jC (Fig. 1A, three-way factorial ANOVA with ranks: F16,240 = 37.46 p < 0.001; temperature: F1 = 4.8, p < 0.029) and small specimens are more affected than larger N. integer. However, immature P. flexuosus disproportionately impacted 2- and 3mm N. integer, while the effect of adults declined linearly with increasing prey size (Fig. 1B). Maximum predation pressure was caused by adult P. flexuosus on 2-mm N. integer. We calculated specific ingestion rates to quantify the nutritional benefit expressed as carbon of P. flexuosus obtained by preying on different sizes of N. integer (Fig. 2). ANOVA on the specific ingestion rates of P. flexuosus found significant interactions between both predator size and temperature and predator size and prey size (Table 3B). Higher temperature positively affected the specific ingestion rate of adult P. flexuosus, but Table 4 Comparison of (1) predation rate (individuals mysid 1 day 1) of (A) P. flexuosus and (B) N. integer and (2) specific ingestion rate (% body C day 1) of (C) P. flexuosus and (D) N. integer on E. affinis by a two-way factorial ANOVA with rank data Source of variation (1) Predation on E. affinis (A) P. flexuosus Temperature (10 jC, 15 jC) Developmental stage (ju, im, ad) Temperature  Developmental stage Error (B) N. integer Temperature (10 jC, 15 jC) Developmental stage (ju, im, ad) Temperature  Developmental stage Error Corrected total (2) Specific ingestion rate (C) P. flexuosus Temperature (10 jC, 15 jC) Developmental stage (ju, im, ad) Temperature  Developmental stage Error (D) N. integer Temperature (10 jC, 15 jC) Developmental stage (ju, im, ad) Temperature  Developmental stage Error Corrected total

df

MS

F value

p

1 2 2 94

17,471.41 13,012.61 2420.67 170.61

102.40 76.26 14.19

< 0.0001 < 0.0001 < 0.0001

1 2 1 55 59

3490.51 4385.40 300.52 92.32

37.81 48.76 3.26

< 0.0001 < 0.0001 0.078

1 2 2 94

2774.81 25,749.71 723.53 207.39

102.40 76.26 14.19

< 0.0001 < 0.0001 < 0.0001

1 2 1 55 59

12,021.65 96.79 1499.80 61.11

37.81 48.76 3.26

< 0.0001 < 0.0001 0.078

Developmental stages are represented by ju: juvenile, im: immature and ad: adult.

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

137

that of immature P. flexuosus did not increase significantly in warmer conditions (Fig. 2A). The expected influence of temperature on specific ingestion of juveniles was not significant mostly due to lower n than for adult P. flexuosus and higher variances. The

Fig. 4. Specific ingestion rates (% body C mysid 1 day 1; mean F S.D.) of P. flexuosus on E. affinis and N. integer in mixed prey experiments. The pie diagrams show the proportion of carbon of each prey of the ingested diet. ‘‘m’’ indicates that in this developmental stage no experiments were carried out.

138

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

response of specific ingestion rate to prey size was different depending on predator size. Immatures preferred the smallest size (2- and 3-mm), with specific ingestion rate depressed significantly with prey sizes greater than 3 mm (Fig. 2B). Adults gained more carbon by feeding on fewer but larger prey (3-, 4-, and 5-mm). 3.2. Consumption of E. affinis in relation to predator species, predator size, and temperature Higher temperature increased the predation rate of all developmental stages (juveniles, immatures, and adults) of P. flexuosus (Fig. 3A; Table 4A). From the juvenile to the adult stage P. flexuosus increased predation rate on E. affinis by three times at 10 jC and by four times at 15 jC. Temperature affected overall predation on E. affinis of N. integer (Table 4B). Predation rate also increased significantly with the ontogenetic development of N. integer (Table 4B; Fig. 3A). Highest predation rates were found at 15 jC for adult N. integer. The effect of temperature on carbon ingestion was opposite to that of the predation rate; the specific ingestion rate was greater for juveniles than for adults in both species (Fig. 3B; Table 4C,D). 3.3. Intraguild predation in the presence of E. affinis Feeding experiments with a choice of prey revealed that P. flexuosus preferred E. affinis over either size class of N. integer (Fig. 4). The ratios of E. affinis and 2-mm N. integer in

Fig. 5. Comparison of P. flexuosus predation rates (individuals mysid 1 day 1; mean F S.D.) on N. integer in the presence and absence of E. affinis at 10 jC. Different letters indicate significant LS-means differences ( p < 0.05).

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

139

Table 5 Comparison of predation rate (individuals mysid 1 day 1) of two developmental stage of P. flexuosus on N. integer in present and absence of alternative prey (Eurymora affinis) by a two-way factorial ANOVA Source of variation

df

MS

F value

p

Predation rate on N. integer Developmental stage (immature, adult) Alternative prey: E. affinis (present, absent) Developmental stage  Alternative prey Error Corrected total

1 1 1 64 67

15.03 671.43 356.64 29.38

0.51 22.85 12.14

0.477 < 0.0001 < 0.001

terms of ingested carbon were 93:7 and 97:3 for immatures and adults, respectively. In the case of adult P. flexuosus preying on E. affinis and 5-mm N. integer, a lower ratio of 84:16 was observed. P. flexuosus reached high specific ingestion rates of 50 –100% body C day 1 by feeding on E. affinis. During the same experiment, specific ingestion rates were 3 –16% body C day 1 when ingesting 2- or 5-mm N. integer. In Fig. 5, we compare predation on N. integer in the presence and absence of E. affinis. Predation rates on N. integer by adult P. flexuosus showed a significant decrease in the presence of an alternative prey item (Table 5). E. affinis was highly abundant and apparently easier to catch compared to juvenile N. integer. However, we could not find a significant difference in predation rates of immature P. flexuosus (Fig. 5).

4. Discussion 4.1. Trophic interactions between N. integer and P. flexuosus We found evidence of interspecific predation among N. integer and P. flexuosus which co-occur in the Elbe Estuary. N. integer was not able to catch newly released P. flexuosus, but was able to prey on newly released conspecifics (Winkler, 2000). This was not a function of size because juvenile size overlaps between the species, but of behavioural differences in susceptibility to predation. The avoidance reflex in mysids is already developed when the individuals hatch (Berrill, 1971; Rademacher and Kils, 1996) and P. flexuosus may have a more powerful avoidance reflex. In our experiment, N. integer was capable of preying only on E. affinis, whereas both immature and adult P. flexuosus were efficient predators on juvenile N. integer. Furthermore, we showed that predation success was determined by developmental stage of the predator, prey size, and temperature. Price (1988) suggested four important factors, encounter, pursuit, capture, and ingestion in determining predation success. The probability of encountering a prey item is dependant on predator and prey density which were held constant in our study. In an estuary, factors such as turbulence and turbidity are likely to alter encounter rates, but we did not evaluated these conditions in our experiments. The other three factors are typically controlled by the interaction of predator and prey sizes; bigger prey are more difficult to pursue, capture, and ingest even though mature predators are usually more efficient at these actions (Ramcharan and Sprules, 1986). Our results suggest that bigger P. flexuosus took advantage of

140

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

being faster and more powerful in their attacks than smaller P. flexuosus. Growth of the prey made it more visible for the predator but at the same time the prey seemed better able to escape predator attacks. Predation rates of N. integer by P. flexuosus were higher than reported in the only other study of interspecific predation in mysids previously published. Wooldridge and Webb (1988) found that R. terranatalis sized 12– 15 mm caught a mean of 3 individuals mysid 1 day 1 of M. slabberi (2 –3 mm), whereas P. flexuosus in the same size class (immature) caught three times more N. integer (2 – 3 mm). Our experiments with replacement of prey lasted 12 h, whereas Wooldridge and Webb (1988) used higher predator densities and ran their study over 24 h without prey replacement, all of which could have lowered the reported predation pressure. It was more advantageous, in terms of ingested carbon, for immature P. flexuous to attack small (2– 3 mm) N. integer than bigger prey. However, adult P. flexuous increased their energy intake by feeding on larger juveniles (3– 5 mm). The specific ingestion rates for immatures and adults from our experiments were between 3% and 15% and between 3% and 10% body C mysid 1 day 1, respectively, depending on prey size. Similar values of total average daily carbon rations have been reported for Mesopodopsis wooldridgei (3– 7% body C mysid 1 day 1) and M. relicta (2 –7% body weight mysid 1 day 1) (Bowers and Vanderploeg, 1982; Froneman, 2001a,b). Compared to mysids, copepods in temperate estuaries are found to require around 35% body C day 1 with increases during egg production to 61% body C day 1 (Froneman, 2000, 2001a,b). In contrast, krill only needed 0.8 –2.8% body C day 1 for basic metabolic demand. Including growth, moulting, and reproduction, this rose to between 5% and 15% body C day 1 (Atkinson and Sny¨der, 1997; Perissinotto et al., 1997). Metabolic costs scale to size and thus metabolic costs of mysids may be placed between copepods and krill due to their intermediate size, so that mysids need approximately 10% body C day 1 to meet basic metabolic requirements (Froneman, 2000). Based on our observations, carbon derived from the predation of N. integer alone was just sufficient to meet the basic metabolic costs of only immature P. flexuosus. Adult P. flexuosus barely reached the 10% body C day 1 by the predation of larger juveniles (3– 5 mm). This suggests that in nature, more ingested carbon must be derived from several sources to meet metabolic requirements. We observed an increased specific ingestion up to 350% body C day 1 for juvenile P. flexuosus and up to 50% body C day 1 for adults when feeding on E. affinis. These high daily rations of E. affinis seemed to exceed the energy requirement cited earlier. The high amount of ingested carbon might be converted into energy reserves or passed inefficiently through the digestive system. In our mixed prey assemblage experiments, specific ingestion rates of P. flexuosus ranged from 60% to 100% body C day 1 and were derived from E. affinis/N. integer ratios that ranged between 97:3 and 84:16. These were sufficient to cover all daily energy demands of P. flexuosus. To quantify the impact of predation on prey species, we evaluated the predation pressure on N. integer. Losses to predation due to adult P. flexuosus were very high for juvenile N. integer and somewhat less due to immature P. flexuosus, up to 40% and 23% in the 2-mm-size class, respectively. While there was little bioenergetic benefit for the predator to feed on N. integer, the cost for N. integer was higher; one adult P. flexuosus was able to consume 30 newly released N. integer, which corresponds to the reproduction

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

141

of 20 females with a mean reproduction rate of 1.4 young per day at 15 jC (Winkler and Greve, 2002). While laboratory experiments are likely to overestimate natural predation levels, this suggests a strong potential impact of P. flexuosus on sympatric populations of N. integer. Wooldridge and Webb (1988) also found high predation pressure on M. slabberi from R. terranatalis in laboratory experiments, which would be sufficient to keep net reproduction of Me. slabberi at zero. Since Me. slabberi and R. terranatalis still occur sympatrically in the estuary, various mechanisms such as spatial segregation, different behaviour as well as a large plasticity of the diet may reduce predation pressure. We have also shown in our mixed prey assemblage experiments that predation pressure due to adult P. flexuosus was significantly depressed in the presence of E. affinis. 4.2. Role of E. affinis Predation on E. affinis by N. integer and P. flexuosus was positively related to predator size and temperature. The predation rates on E. affinis that we obtained were similar to predation rates reported for N. integer (Aaser et al., 1995). Even higher predation rates of N. integer on E. affinis were reported by studies in Hickling Broad, a brackish shallow water lake in UK (Irvine et al., 1990, 1993, 1995). Differences in feeding rates among these studies may be due to prey densities used and to experimental design. Our prey densities of 400 E. affinis l 1 and feeding experiment times of 24 h were greater compared to 100 –300 individuals l 1 and feeding times of 2 h of other studies of N. integer (Irvine et al., 1990, 1993; Aaser et al., 1995). Thus, predation rates measured in the laboratory are highly variable depending on experimental design. Therefore, extrapolation to natural situations should be carried out with caution. However, our experiments illustrated clearly the predation potential of P. flexuosus and N. integer on copepod prey. Based on the results of our experiments and the literature on the effect of mysid predators on copepod populations in the field, we conclude that N. integer and P. flexuosus together are able to exploit zooplankton aggregations efficiently, potentially influencing copepod distribution patterns. Due to the fact that predation is dependant on size of the predator, the potential impact on prey organisms of adult P. flexuosus is higher than of adult N. integer. In future work, controlled feeding experiments with multiple-species prey combined with field observations should provide a better image of the predation rates of mysids. 4.3. Intraguild predation in the presence of E. affinis Combined predation experiments confirmed P. flexuosus predation on N. integer and E. affinis. Further, it was shown that predation on high densities of smaller-sized prey was greater than on less abundant juvenile N. integer. Most of the ingested carbon was derived from consumption of E. affinis. This suggests that P. flexuosus conforms to an optimal foraging model (Begon et al., 1991), choosing high numbers of the small but easily captured E. affinis, as opposed to a selective predation model (i.e., searching out low density but highly nutritious juvenile mysids). This is consistent with the findings of Viitasalo and Rautio (1998) who showed that P. flexuosus fed mainly opportunistically; suspension feeding on cladocerans was preferred over raptorial feeding on copepods due to the fact that cladocerans are easier and faster to handle and ingest than copepods.

142

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

Our experiments represented two specific situations: In the absence of E. affinis, P. flexuosus showed maximum intraguild predation while, in the presence of high numbers of E. affinis, predation was depressed due to the presence of an abundant alternative food resource. These two experimental situations thus represented the two extreme cases of possible interactions. In the natural environment, we would expect situations between these extremes. 4.4. Intraguild predation model for mysids in the Elbe Estuary We exploited the intraguild predation concept (Root, 1967; Polis et al., 1989) to summarise the interspecific interactions documented in this study. Our model consisted of two age structured mysid species, N. integer and P. flexuosus, which competed for the same food resource, E. affinis (Fig. 6). Immature and adult P. flexuosus expanded

Fig. 6. Conceptual diagram of intraguild predation within the age structured mysid guild of the Elbe Estuary. Relative importance of energy flow is indicated by arrow thickness for the two studied cases; (A) the common food resource, E. affinis is absent and (B) E. affinis is present (grey solid arrows).

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

143

their diet by preying on juvenile and immature N. integer. Although it is not clear what value preying on juvenile N. integer has for P. flexuosus, it is obvious that predation has the potential to cause high size-specific mortality in the N. integer population. Juvenile N. integer up to 4 mm, representing the first 15 days after release from the marsupium at 15 jC and the first 50 days at 10 jC (Winkler and Greve, 2002), are particularly at risk of predation by P. flexuosus. Life history characteristics of both species should influence the strength of predation. N. integer is an r-strategist with short generation times, high brood size and multiple subsequent broods, whereas P. flexuosus represents more closely a k-strategy. So we would expect predation to be more pronounced and favourable for P. flexuosus during high N. integer reproduction in summer, when they may comprise up to 16% of the P. flexuosus energy budget as found in the mixed prey experiments. Wooldridge and Webb (1988) found an increase in predation on M. slabberi by R. terranatalis with increasing prey density. Thus, density dependant predation by P. flexuosus may also influence predation. Availability of alternative prey reduced predation. As such, the proportion of N. integer juveniles and E. affinis will also determine the extent of predation. At the individual level, nutritional condition and escape behaviour also influences intraguild predation (Polis and Holt, 1992). In the present case, N. integer was not able to catch and feed on juvenile P. flexuosus because the escape behaviour in juvenile P. flexuosus was too strong. The intraguild predation model could be further improved with more information on the role of resource partitioning to consider omnivory of both species and the effect of density dependence of predator and prey.

5. Conclusion Our results indicate that intraguild predation may be an important mortality factor affecting the size structure of the population of N. integer. The extent of predation is dependant of the age structure and abundance of both guild members, P. flexuosus and N. integer, as well as the quantity of alternative food sources. Predation may be mediated by the temporal and spatial distribution of both mysid species as seen in R. terranatalis and Neomysis mercedis (Murtaugh, 1981; Wooldridge and Webb, 1988) and by the separation of different life stages by aggregation of individuals of similar size (McLusky and Heard, 1971; Wissinger, 1992). Regarding the complex dynamic of predation in N. integer and P. flexuosus, we suggest that there may be a critical predator population size which has not been exceeded in the Elbe Estuary and/or shared prey populations that permit the co-existence of the sympatric populations of P. flexuosus and N. integer.

Acknowledgements Special thanks are extended to the crew members of the Utho¨rn, K. Broeg, A. Cugat, J. Nast, N. Peters, U. Pein, M. Pezenburg, and S. Prinage for their assistance in the field and the laboratory. We thank U. Wilhelmsen for helpful discussions and A. Casper, M. Rautio, and

144

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

J.J. Dodson for critical reading and correcting the language of the manuscript. This project was financially supported by the German Science Foundation (DFG : GR 382/3-1). [RW] References Aaser, H., Jeppesen, E., Sondergaard, M., 1995. Seasonal dynamics of the mysid Neomysis integer and its predation on the copepod Eurytemora affinis in a shallow hypertrophic brackish lake. Mar. Ecol. Prog. Ser. 127, 47 – 56. Arndt, E.A., Jansen, W., 1986. Neomysis integer (Leach) in the chain of Boddens south of Darss/Zingst (Western baltic): ecophysiology and population dynamics. Ophelia 4, 1 – 15. Atkinson, A., Sny¨der, R., 1997. Krill – copepod interactions at South Georgia, Antarctica: I. Omnivory by Euphausia superba. Mar. Ecol. Prog. Ser. 160, 63 – 76. ¨ kologie. Individuen, Populationen und Lebensgemeinschaften. Begon, M., Harper, J.L., Townsend, C.R., 1991. O Birkha¨user, Berlin, p. 1024. Berrill, M., 1971. The embryonic development of the avoidance reflex of Neomysis americana and Praunus flexuosus. Anim. Behav. 19, 707 – 713. Blegvad, H., 1922. On the biology of some danish gammarids and mysids. Rep. Dan. biol. Stn. 28, 1 – 103. Bowers, J.A., Vanderploeg, H.A., 1982. In situ predatory behaviour of Mysis relicta, Lake Michigan. Hydrobiologia 93, 121 – 131. Depdolla, P., 1923. Nahrung und Nahrungserwerb bei Praunus flexuosus (Mu¨ll.). Biol. Zentralbl. 43, 534 – 546. Dick, J., Platvoet, D., 1996. Intraguild predation and species exclusions in amphipods: the interaction of behaviour, physiology and environment. Freshw. Biol. 36, 375 – 383. Escaravage, V., Soetaert, K., 1993. Estimating secondary prodution for the brackish Westerschelde copepod population Eurytemora affinis (Poppe) combining experimental data and field observations. Cah. Biol. Mar. 34, 201 – 214. Fiedler, M., 1991. Die Bedeutung von Makrozoobenthos und Zooplankton der Unterelbe als Fischnahrung. Ber. Inst. Meereskd. Kiel 204, 226. Fockedey, N., Mees, J., 1999. Feeding of the hyperbenthic mysid Neomysis integer in the maximum turbidity zone of the Elbe, Westernschelde and Gironde estuaries. J. Mar. Syst. 22, 207 – 228. Froneman, P.W., 2000. Feeding studies on selected zooplankton in a temperate estuary, South Africa. Estuar. Coast. Shelf Sci. 51, 543 – 552. Froneman, P.W., 2001a. Feeding ecology of the mysid, Mesopodopsis wooldridgei, in a temperate estuary along the eastern seaboard of South Africa. J. Plankton Res. 23 (9), 999 – 1008. Froneman, P.W., 2001b. Seasonal changes in zooplankton biomass and grazing in a temperate estuary, South Africa. Estuar. Coast. Shelf Sci. 52 (5), 543 – 553. Fulton, R.S., 1982a. Preliminary results of an experimental study of the effects of mysids predation on estuarine zooplankton community structure. Hydrobiologia 93, 79 – 84. Fulton, R.S., 1982b. Predatory feeding of two marine mysids. Mar. Biol. 72, 183 – 191. Fulton, R.S., 1985. Predator – prey relationships in an estuarine littoral copepod community. Ecology 66 (1), 21 – 29. Gorokhova, E., Hansson, S., 1997. Effects of experimental contitions on the feeding rate of Mysis mixta (Crustacea, Mysidacea). Hydrobiologia 355, 167 – 172. Greve, W., 1977. Interspecific interaction: the analysis of complex structures in carnivorous zooplankton populations. Helgol. Wiss. Meeresunters. 30, 83 – 91. Greve, W., Reiners, F., 1996. A multiannual outbreak of the turbellarian Alaurina composita Mecznikow 1865 in the German Bight. J. Plankton Res. 18, 157 – 162. Grossnickle, N.E., 1982. Feeding habits of Mysis relicta—an overview. Hydrobiologia 93, 101 – 107. Irvine, K., Bales, M.T., Moss, B., Stansfield, J.H., Snook, D., 1990. Trophic relations in Hickling Broad—a shallow and brackish eutophic lake. Verh. Int. Vereinsbl. Limnol. 24, 576 – 579. Irvine, K., Moss, B., Bales, M., Snook, D., 1993. The changing ecosystem of a shallow, brackish lake, Hickling Broad, Norfolk, U.K.: I. Trophic relationships with special reference to the role of Neomysis integer. Freshw. Biol. 29, 119 – 139.

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

145

Irvine, K., Snook, D., Moss, B., 1995. Life histories of Neomysis integer, and its copepod prey, Eurytemora affinis, in a eutrophic and brackish shallow lake. Hydrobiologia 304, 59 – 76. Jansen, W., 1985. Stellung von Neomysis integer (Leach) (Crustacea, Mysidacea) als Konsument im Nahrungsgefu¨ge der Darh-Zingst Bodenkette (su¨dliche Ostsee). Fisch. Forsch. Wiss. Schriftenr. 23, 55 – 59. Jerling, H.L., Wooldridge, T.H., 1995. Feeding of two mysid species on plankton in a temperate South African estuary. J. Exp. Mar. Biol. Ecol. 188, 243 – 259. Kinne, O., 1955. Neomysis vulgaris, eine auto¨kologische Studie. Biol. Zent. Bl. 74, 160 – 202. Ko¨pcke, B., 2002. Die Bedeutung der Nebenelben und Flachwasserbereiche fu¨r den Populationserhalt von Eurytemora affinis (Poppe, 1880). Dissertation, University of Hamburg, Hamburg, p. 302. Ko¨pcke, B., Kausch, H., 1996. Distribution and varibility in abundance of Neomysis integer and Mesopodopsis slabberi in relation to environmental factors in the Elbe Estuary. Arch. Hydrobiol., Suppl. 110, 263 – 282. Ku¨hl, H., 1964. Die Mysideen der Elbmu¨ndung. Abhandlungen und Verhandlungen des Naturwissenschaftlichen vereins in Hamburg. Hamburg 8, 167 – 178. Kuhlmann, D., 1982. Die Biologie von Neomysis integer Leach unter dem Aspekt ihrer Zucht als Futterorganismus. Dissertation, University of Kiel, Kiel, p. 151. Lasenby, D.C., Langford, R.R., 1973. Feeding and assimilation of Mysis relicta. Limnol. Oceanogr. 18, 280 – 285. Lenz, J., 1974. On the amount and size distribution of suspended matter in Kiel Bight. Ber. Dtsch. Wiss. Komm. Meeresforsch. 23, 209 – 225. Mauchline, J., 1971. The biology of Praunus flexuosus and P. neglectus Crustacea Mysidacea. J. Mar. Biol. Assoc. U.K. 51, 641 – 652. Mauchline, J., 1980. The biology of Mysids and Euphausids (Crustracea, Mysidacea). Adv. Mar. Biol. 18, 3 – 317. McLusky, D.S., Heard, V., 1971. Some effects of salinity on the mysid Praunus flexuosus. J. Mar. Biol. Assoc. U.K. 51, 709 – 715. Murtaugh, P.A., 1981. Selective predation by Neomysis mercedis in Lake Washington. Limnol. Oceanogr. 26 (3), 445 – 453. Omori, M., 1978. Zooplankton fisheries of the world: a review. Mar. Biol. 48, 199 – 205. Paine, R.T., 1980. Food webs: linkage, interaction strength and community infrastructure. The third Tansley lecture. J. Anim. Ecol. 49 (3), 667 – 685. Perissinotto, R., Pakhomov, E.A., McQuaid, C.D., Froneman, P.W., 1997. In situ grazing rates and daily ration of Antarctic krill Euphausia superba feeding on phytoplankton at the Antarctic Polar Front and the Marginal Ice Zone. Mar. Ecol. Prog. Ser. 160, 77 – 91. Pezenburg, M., 1998. Nahrungskonsumption und Nahrungsselektivita¨t der Dorngarnele Palaemon longirostris H. Milne Edwards, 1837 (Crustacea, Decapoda, Natantia). Diplomarbeit, Universita¨t Hamburg, Hamburg, p. 61. Polis, G.A., Holt, R.D., 1992. Intraguild predation: the dynamics of complex trophic interactions. TREE 7 (5), 151 – 154. Polis, G.A., Myers, A., Holt, R.D., 1989. The ecology and evolution of intraguild predation: potential competitors that eat each other. Ann. Rev. Ecolog. Syst. 20, 297 – 330. Price, H.J., 1988. Feeding mechanisms in marine and freshwater zooplankton. Bull. Mar. Sci. 43, 327 – 343. Rademacher, K., Kils, U., 1996. Predator/prey dynamics of fifteen-spined stickleback (Spinachia spinachia) and the mysid Neomysis integer. Arch. Fish. Mar. Res. 43 (2), 171 – 181. Ramcharan, C.W., Sprules, G.W., 1986. Visual predation in Mysis relicta Loven. Limnol. Oceanogr. 31, 414 – 420. Raymont, J.E.G., Austin, J., Linford, E., 1964. Biochemical studies on marine zooplankton: I. The biochemical composition of Neomysis integer. J. Cons.-Perm. Int. Explor. Mer. 28, 354 – 363. Root, R., 1967. The niche exploitation pattern of the blue-grey gnat catcher. Ecol. Monogr. 37, 317 – 350. Siegfried, C.A., Kopache, M.E., 1980. Feeding of Neomysis mercedis (HOLMES). Biol. Bull. 159, 193 – 205. Thiel, R., 1992. Quantitative estimation of mysids Neomysis integer, (Leach,1814) and their production within a typical southern Baltic Bay. In: Ko¨hn, V.J., Jones, M.B., Moffat, A.M. (Eds.), Taxonomy, biology and ecology of (Baltic) mysids (Mysidacea: Crustacea). International expert conference, Hiddensee, Germany. Rostock University Press, Rostock, pp. 73 – 78.

146

G. Winkler, W. Greve / J. Exp. Mar. Biol. Ecol. 308 (2004) 127–146

Viitasalo, M., Rautio, M., 1998. Zooplanktivory by Praunus flexuosus (Crustacea : Mysidacea): functional responses and prey selection in relation to prey escape responses. Mar. Ecol. Prog. Ser. 174, 77 – 87. Viitasalo, M., Kiorboe, T., Flinkman, J., Pedersen, L.W., Visser, A.W., 1998. Predation vulnerability of plantonic copepods: consequences of predator foraging strategies and prey sensory abilities. Mar. Ecol. Prog. Ser. 175, 129 – 142. Viitasalo, M., Flinkman, J., Viherluoto, M., 2001. Zooplanktivory in the Baltic Sea: a comparison of prey selectivity by Clupea harengus and Mysis mixta, with reference to prey escape reactions. Mar. Ecol. Prog. Ser. 216, 191 – 200. Webb, P., Perissinotto, R., Wooldridge, T.H., 1987. Feeding of Mesopodopsis slabberi (Crustacea, Mysidacea) on naturally occurring phytoplankton. Mar. Ecol. Prog. Ser. 38, 115 – 123. Winkler, G., 1994. Zur Populationdynamik und Erna¨hrungsbiologie von Crangon crangon L. (Crustacea; Crangonidae) in der Lu¨becker Bucht (Su¨dwestliche Ostsee). Diplomarbeit, Universita¨t Hamburg, Hamburg, p. 90. Winkler, G., 2000. Zur Oekologie zweier interagierender Mysidaceenarten Neomysis integer (Leach, 1814) und Praunus flexuosus F. Mueller 1776 (Peracarida, Mysidacea). Dissertation, Universita¨t Hamburg, Hamburg, p. 145. Winkler, G., Greve, W., 2002. Laboratory studies of the effect of temperature on growth, moulting and reproduction in the co-occurring mysids Neomysis integer and Praunus flexuosus. Mar. Ecol. Prog. Ser. 235, 177 – 188. Wissinger, S.A., 1992. Niche overlap and the potential for competition and intraguild predation between sizestructured populations. Ecology 73 (4), 1431 – 1444. Wolfstein, K., Kies, L., 1995. A case study on the oxygen budget in the freshwater part of the Elbe estuary: 3. Variations in phytoplankton pigments in the Elbe estuary before and during the oxygen minima in 1992 and 1993. Arch. Hydrobiol., Suppl. 110 (1), 39 – 54. Wooldridge, T.H., Webb, P., 1988. Predator – prey interactions between two species of estuarine mysid shrimps. Mar. Ecol. Prog. Ser. 50, 21 – 28. Zander, C.D., Hagemann, T., 1986. Fluctuatuion of prey, abundance and biomass of gobies (Goviidae, Teleostei) in a shallow habitat of the western Baltic Sea. Zool. Anz. 216, 289 – 304. Zander, C.D., Hagemann, T., 1987. Predation impact and ecological efficiengy of Pomatoschistus minutus (Gobiidae, Pisces) from a clay/sand ecotone of the western Baltic Sea. Zool. Anz. 218, 33 – 48. Zar, J.H., 1996. Biostatistical Analysis, 3rd edn. Prentice-Hall, Upper Saddle River, NJ. Zelickman, E.A., 1974. Group orientation in Neomysis mirabilis Mysidacea Crustacea. Mar. Biol. 24, 251 – 258. Zimmermann-Timm, H., 2002. Characteristics, dynamics and importance of aggregates in rivers—an invited review. Int. Rev. Hydrobiol. 87 (2 – 3), 197 – 240.