Synergistic impacts by an invasive amphipod and an invasive fish explain native gammarid extinction

Abstract

Background: Worldwide freshwater ecosystems are increasingly affected by invasive alien species. In particular, Ponto-Caspian gobiid fishes and amphipods are suspected to have pronounced effects on aquatic food webs. However, there is a lack of systematic studies mechanistically testing the potential synergistic effects of invasive species on native fauna. In this study we investigated the interrelations between the invasive amphipod Dikerogammarus villosus and the invasive fish species Neogobius melanostomus in their effects on the native amphipod Gammarus pulex. We hypothesized selective predation by the fish as a driver for displacement of native species resulting in potential extinction of G. pulex. The survival of G. pulex in the presence of N. melanostomus in relation to the presence of D. villosus and availability of shelter was analyzed in the context of behavioural differences between the amphipod species.

Results: Gammarus pulex had a significantly higher susceptibility to predation by N. melanostomus compared to D. villosus in all experiments, suggesting preferential predation by this fish on native gammarids. Furthermore, the presence of D. villosus significantly increased the vulnerability of G. pulex to fish predation. Habitat structure was an important factor for swimming activity of amphipods and their mortality, resulting in a threefold decrease in amphipods consumed with shelter habitat structures provided. Behavioral differences in swimming activity were additionally responsible for higher predation rates on G. pulex. Intraguild predation could be neglected within short experimental durations.

Conclusions: The results of this study provide evidence for synergistic effects of the two invasive Ponto-Caspian species on the native amphipod as an underlying process of species displacements during invasion processes. Prey behaviour and monotonous habitat structures additionally contribute to the decline of the native gammarid fauna in the upper Danube River and elsewhere.

Keywords: Anti-predator behaviour; Dikerogammarus villosus; Gammarus pulex; Neogobius melanostomus; Selective predation; Species displacement.

Fig. 1

Influence of fish sex on gammarid predation depending on absence or presence of substratum. Index of stomach fullness (ISF) confirms a generally higher predation rate in absence of substratum. No differences between female (white) and male (grey) N. melanostomus were observed. [Asterisks indicate significant differences at p < 0.05 (*), p < 0.01 (**), p < 0.001 (***)]. Boxplots represent 25 to 75 % (boxes ) and 5 to 95 % percentiles (whiskers). Circles represent outliers (exceeding 1.5 interquartile range). n = 14: female/substratum absent; n = 8: male/substratum absent; n = 12: female/substratum present; n = 10: male/substratum present)

Fig. 2

Predation of N. melanostomus on amphipods within a 3 h time-period where either single species (white, n = 11) or a combination of both species (grey, n = 22) were tested. a Substratum absent. b Substratum present. [Asterisks indicate significant differences at p < 0.05 (*), p < 0.01 (**), p < 0.001 (***)]. Boxplots represent 25 to 75 % (boxes) and 5 to 95 % percentiles (whiskers). Circles represent outliers (exceeding 1.5 interquartile range)

Fig. 3

Predation of N. melanostomus within a 3 h time-period on G. pulex (grey) and D. villosus (white). Gammarus pulex mean size (± SD) 11.8 ± 1.5 mm and D. villosus 18.3 ± 2.4 mm. [Asterisks indicate significant differences at p < 0.05 (*), p < 0.01 (**), p < 0.001 (***)]. Boxplots represent 25 to 75 % (boxes) and 5 to 95 % percentiles (whiskers). Circles represent outliers (exceeding 1.5 interquartile range); n = 12 per substratum trial)

Fig. 4

Prey selectivity of N. melanostomus. Mean values ± SE of electivity index are presented. Positive values represent preferred prey species in presence (open circles and squares) or absence (black circles and squares) of substratum. Dashed line indicates no selectivity. a Same size class of G. pulex and D. villosus. b Larger size class of D. villosus. Asterisks indicate significant differences to zero at p < 0.05 (repeated measures ANOVA): (*), p < 0.01 (**), p < 0.001 (***)

Fig. 5

Mean number (± SD) of individual amphipods swimming actively in the water column within a timeframe of 15 min in absence (grey) and 15 min in presence (black) of a single N. melanostomus specimen. (n = 5 per species)