Łukasz Jermacz

Effectiveness of zebra mussels to act as shelters from fish predators differs between native and invasive amphipod prey

Biological invasions cause organisms to face new predators, but also supply new anti-predator shelters provided by alien ecosystem engineers. We checked the level of anti-predator protection provided to three gammarid species by an invasive Ponto-Caspian zebra mussel Dreissena polymorpha, known for its habitat modification abilities. We used gammarids differing in their origin and level of association with mussels: Ponto-Caspian aliens Dikerogammarus villosus (commonly occurring in mussel beds) and Pontogammarus robustoides (not associated with mussels), as well as native European Gammarus fossarum (not co-occurring with dreissenids). The gammarids were exposed to predation of two fish species: the racer goby Babka gymnotrachelus (Ponto-Caspian) and Amur sleeper Perccottus glenii (Eastern Asian). This set of organisms allowed us to check whether the origin and level of association with mussels of both prey and predators affect the ability of gammarids to utilize zebra mussel beds as shelters. We tested gammarid survival in the presence of fish and one of five substrata: sand, macrophytes, stones, living mussels and empty mussel valves. D. villosus survived better than its congeners on all substrata, and its survival was highest in living dreissenids. The survival of the other gammarids was similar on all substrata. Both fish species exhibited similar predation efficiency. Thus, D. villosus, whose affinity to dreissenids has already been established, utilizes them as protection from fish predators, including allopatric predators, more efficiently than other amphipods. Therefore, the presence of dreissenids in areas invaded by D. villosus is likely to help the invader establish itself in a new place.

The impact of zebra mussel (Dreissena polymorpha) periostracum and biofilm cues on habitat selection by a Ponto-Caspian amphipod Dikerogammarus haemobaphes

Dikerogammarus haemobaphes is one of several Ponto-Caspian gammarids invading Europe in recent decades. Previously, it exhibited active preferences for habitats associated with another Ponto-Caspian alien, zebra mussel. Now we tested gammarid preferences for living mussels and their empty shells with biofilm and/or periostracum present or absent, to find the exact cues driving gammarid responses. We observed a strong preference of gammarids for biofilmed shells, even if the biofilm was relatively young (2-day old). However, the biofilm quality, related to the substratum on which it had developed (shells with or without the periostracum, or coated with nail varnish) did not affect their behaviour. In the absence of biofilm, gammarids positively responded to the shell periostracum. Furthermore, they clearly preferred living zebra mussels over old empty shells, independent of the presence or absence of biofilm, confirming the importance of a periostracum-associated cue in their substratum recognition. On the other hand, shells obtained shortly after mussels’ death were preferred over living bivalves. Thus, the attractant is associated with fresh mussel shells, rather than with living mussels themselves. The ability of alien gammarids to locate sites inhabited by zebra mussels may contribute to their invasion success in novel areas inhabited by this habitat-forming bivalve.

Keep calm and don’t stop growing: Non-consumptive effects of a sympatric predator on two invasive Ponto-Caspian gammarids Dikerogammarus villosus and Pontogammarus robustoides

Predators shape prey populations by elimination of individuals (consumptive effects) and by inducing modifications in prey behaviour, physiology or morphology (NCE—non-consumptive effects). Due to the resource allocation to defence, decreased feeding and higher stress, the costs of predator NCEs can be considerable. Therefore, the resistance to NCEs may be crucial for population growth and interspecific competition. We tested the resistance of Ponto-Caspian gammarids Dikerogammarus villosus and Pontogammarus robustoides to NCEs imposed by their predator, the racer goby Babka gymnotrachelus. As D. villosus is often avoided by predators in the presence of alternative food, we hypothesised that it would bear lower behavioural and physiological costs of anti-predator responses. We tested gammarid feeding in short-time experiments (2–4 h) with food (chironomid larvae) located at various distances from the stony shelter (to enforce food searching, Experiment I) or in the direct gammarid proximity (no searching needed, Experiment II). Moreover, we checked the predator effect on gammarid growth in a 2-week Experiment III. Both gammarids exposed to predators reduced feeding efficiency outside the shelter (Experiment I). Contrary to our expectations, the response of D. villosus was stronger. When food was provided in their direct proximity (Experiment II), the feeding of both species was unaffected by predators, indicating that a shelter supplied with food can reduce predator NCEs. The growth of P. robustoides was reduced in the presence of predators (Experiment III), whereas that of D. villosus was unaffected. Although D. villosus has a more effective defence strategy than P. robustoides, it bears similar or even higher behavioural costs of NCEs. However, it exhibits the higher resistance to the long-term predator presence, sustaining its growth rate under such conditions. This may be one of the factors contributing to the great invasion success of D. villosus, currently taking place in European fresh waters.

Predator diet, origin or both? Factors determining responses of omnivorous amphipods to predation cues

Detection of chemical cues of predators and food resources is a key for the behaviour of many species in aquatic ecosystems. We checked whether predator origin and diet, containing potential food and/or alarm signals, affect the behaviour of omnivorous prey partly sharing their diet with a top predator. We conducted y-maze experiments to study the responses of invasive omnivorous and cannibalistic amphipods (Dikerogammarus villosus and Pontogammarus robustoides) to chemical cues of fish predators, injured amphipods and chironomid larvae (common amphipod food). As the predators, we used the goby Babka gymnotrachelus (sympatric with the amphipods) and piranha Pygocentrus nattereri (allopatric to the amphipods). The fish were either starved or fed amphipods or chironomids. D. villosus preferred predators fed chironomids and conspecifics as well as crushed conspecifics and chironomids, but avoided both hungry predators. Thus, D. villosus may perceive the presence of a top predator as an indication of both food resource and predation risk. P. robustoides avoided predators fed both amphipods (particularly conspecifics) and their alarm substances. The responses of both species depended more on the predator diet than on its species, which is likely to facilitate the recognition of allopatric predators and survival in newly invaded areas.

Zebra mussel beds: an effective feeding ground for Ponto-Caspian gobies or suitable shelter for their prey?

Aggregations of the Ponto-Caspian invasive zebra mussel (Dreissena polymorpha) constitute a suitable habitat for macroinvertebrates, considerably increasing their abundance and providing effective antipredator protection. Thus, the overall effect of a mussel bed on particular predator species may vary from positive to negative, depending on both prey density increase and predator ability to prey in a structurally complex habitat. Alien Ponto-Caspian goby fish are likely to be facilitated when introduced into new areas by zebra mussels, provided that they are capable of utilizing mussel beds as habitat and feeding grounds. We ran laboratory experiments to find which prey (chironomid larvae) densities (from ca. 500 to 2,000 individuals m−2) in a mussel bed make it a more beneficial feeding ground for the racer goby Babka gymnotrachelus (RG) and western tubenose goby Proterorhinus semilunaris (WTG) compared to sandy and stone substrata (containing the basic prey density of 500 ind. m−2). Moreover, we checked how food availability affects habitat selection by fish. Mussel beds became more suitable for fish than alternative mineral substrata when food abundance was at least two times higher (1,000 vs. 500 ind. m−2), regardless of fish size and species. WTG was associated with mussel beds regardless of its size and prey density, whereas RG switched to this habitat when it became a better feeding ground than alternative substrata. Larger RG exhibited a stronger affinity for mussels than small individuals. WTG fed more efficiently from a mussel bed at high food abundances than RG. A literature review has shown that increasing chironomid density, which in our study was sufficient to make a mussel habitat an attractive feeding ground for the gobies, is commonly observed in mussel beds in the field. Therefore, we conclude that zebra mussels may positively affect the alien goby species and are likely to facilitate their establishment in novel areas, contributing to an invasional meltdown in the Ponto-Caspian invasive community.

The Braveheart amphipod: A review of responses of invasive Dikerogammarus villosus to predation signals

Predator pressure is a fundamental force driving changes at all levels of the community structure. It may protect native ecosystems from alien species. Therefore, resistance to diverse predators resulting from a universal anti-predator strategy seems crucial for invasion success. We present a comprehensive review of the responses of an invasive amphipod Dikerogammarus villosus to sympatric and allopatric predator signals. We summarize diverse aspects of the gammarid anti-predator strategy, including predator identification, morphological and behavioural adaptations, effectiveness of shelter use and resistance to indirect predator effects. The response of D. villosus is independent of predator species (including totally allopatric taxa), which assures the high flexibility of its predator recognition system. It has a harder exoskeleton and better capability of utilizing shelters compared to other gammarids, resulting in relatively high resistance to predators. Therefore, it can use predator kairomones as indirect food signals (sharing the diet with the predator) and follow the predator scent. This resistance may allow D. villosus to reduce the costs of its physiological responses to predators and sustain growth in their presence. This might facilitate invasion success by increasing its competitive advantage.