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

Survey methodology

To obtain a comprehensive set of literature reports on interactions between predators and amphipod prey, we conducted a literature survey in the Scopus database, using the following keywords: D. villosus or gammarid or amphipod combined with the following: anti-predator response or predator impact or anti-predator behaviour or predator defence or predator kairomone or predation risk or prey response. We found 67, 115 and 927 articles, respectively, meeting the criteria, 11 of which were of our own authorship. Among these articles were chosen key papers related to defence strategies exhibited by native and invasive amphipods.

Prey–predator relationships in the context of biological invasions

Predation is one of the most powerful forces in nature, affecting the evolution of prey and predator species and modifying interactions among organisms (Mowles, Rundle & Cotton, 2011; Turner & Peacor, 2012). On the one hand, predators kill and consume prey individuals, removing them from the population and creating selective pressure, which results in so called “consumptive effects” of a predator (Werner & Peacor, 2003). On the other hand, prey species respond to the presence of predators by various forms of constitutive (permanent) and induced defences, stimulated by the presence of a predator. These defence mechanisms include behavioural (De Meester et al., 1999; Gliwicz, 2005), morphological (Pettersson, Nilsson & Brönmark, 2000; Dzialowski et al., 2003; James & McClintock, 2017), physiological (Slos & Stoks, 2008; Glazier et al., 2011) and life-history related (Ślusarczyk, Dawidowicz & Rygielska, 2005) changes aiming at reducing the probability and/or efficiency of a predator attack. Defence responses are displayed by a wide range of taxa, from protozoans (Wiackowski, Fyda & Ciećko, 2004) through virtually all invertebrate taxa (Koperski, 1997; Lass & Spaak, 2003; Thoms et al., 2007; Kobak, Kakareko & Poznańska, 2010) to vertebrates (Gliwicz, 2005). Anti-predation mechanisms can be quite costly, consuming energy designated for the construction of defensive structures and compromising the habitat quality and/or food abundance, which finally leads to the decrease in growth rate and reproduction (Gliwicz, 1994; Gliwicz, 2005; De Meester et al., 1999; Clinchy, Sheriff & Zanette, 2013). These energetic expenses are called “non-consumptive effects” of predator presence (Werner & Peacor, 2003) and sometimes generate losses comparable to those caused by consumptive predator effects (Preisser, Bolnick & Benard, 2005; Creel & Christianson, 2008). Therefore, the ability to adequately recognize the danger imposed by predators, depending on their feeding mode (Wudkevich et al., 1997; Wooster, 1998; Abjörnsson et al., 2000), present condition (e.g., satiation level) (Abjörnsson et al., 1997), abundance (Pennuto & Keppler, 2008) and size (Kobak, Kakareko & Poznańska, 2010) is crucial for avoiding unnecessary (leading to energy wasting) or maladaptive (increasing the probability of death) responses.

Biological invasions add a new and interesting aspect to predator–prey interactions. In old systems, where predator and prey coevolve together for a long time, both are well adjusted to each other. The responses of prey species can be fine-tuned to specific predators (Wudkevich et al., 1997; Weber, 2003; Boeing, Ramcharan & Riessen, 2006), but also predator preying modes allow them to feed efficiently on available victims (Gliwicz, 2005). However, alien species, just transported to their novel locations, face completely new, unknown communities, containing new predators and new prey. In accordance with the Enemy Release Hypothesis (Torchin et al., 2003), as a consequence of the loss of natural parasites and predators, introduced species suffer lower pressure than native species. At the same time, local consumers may be unfamiliar with alien prey and unable to forage on them efficiently (Meijer et al., 2016). On the other hand, alien species are also not adapted to their new, potential predators which may prevent them from employing efficient anti-predation mechanisms and lead to an evolutionary trap: inefficient or even maladaptive responses or the lack of reactions to a danger (Salo et al., 2007; Zuharah & Lester, 2010).

Recognition of a predator may be based on variable stimuli, including chemical, visual and/or mechanical cues. In the aquatic environment, due to its relative darkness and high density of the medium, chemical recognition is regarded as the most important (Brönmark & Hansson, 2000). This general rule also applies to gammarids detecting their predators (Wisenden et al., 2009; Hesselschwerdt et al., 2009; Jermacz, Dzierżyńska-Białończyk & Kobak, 2017). Prey organisms can potentially recognize three sources of chemical predation cues: alarm cues produced by wounded conspecifics (Czarnołeski et al., 2010; Kobak & Ryńska, 2014; Jermacz, Dzierżyńska-Białończyk & Kobak, 2017), scents of consumed conspecifics included in predator faeces (Ślusarczyk & Rygielska, 2004; Jermacz, Dzierżyńska-Białończyk & Kobak, 2017) or other exudates and/or direct predator metabolites, independent of their diet (Kobak, Kakareko & Poznańska, 2010; Jermacz, Dzierżyńska-Białończyk & Kobak, 2017). The first two options can be potentially utilized by alien organisms to detect unknown predators. Moreover, alien organisms can recognize predators taxonomically related to those living in their native range (Sih et al., 2010) or use learning to associate new predator scents with the perceived danger cues (Chivers, Wisenden & Smith, 1996; Wisenden, Chivers & Smith, 1997; Martin, 2014). The latter approach is commonly exhibited by fish (Korpi & Wisenden, 2001), whereas in invertebrates predator recognition is often innate, displayed also by naïve individuals (Dalesman, Rundle & Cotton, 2007; Ueshima & Yusa, 2015).

Predator recognition by D. villosus

For a perfect invasive species, the mechanism of predator detection should be universal, enabling the recognition and subsequent response to a novel predator without a common evolutionary history. As a consequence of an improper identification of a predator signal, prey species are exposed to higher predation due to the lack of responses or maladaptive responses (Abjörnsson, Hansson & Brönmark, 2004; Banks & Dickman, 2007). Such a scenario was presented by Pennuto & Keppler (2008) who demonstrated that a native Gammarus fasciatus is able to avoid a narrower range of potential predators than an invasive Echinogammarus ischnus. Moreover, ineffective recognition of danger could result in costly defence reactions when the predation risk is low (Lima & Dill, 1990; Dunn, Dick & Hatcher, 2008) as was experimentally shown for Gammarus minus responding to a predatory fish Luxilus chrysocephalus (Wooster, 1998). Therefore, appropriate predation risk assessment is crucial for an adequate response and optimization of energy expenditure.

Laboratory experiments demonstrated the ability of D. villosus to recognize diverse fish predators, including bottom dwellers: the racer goby Babka gymnotrachelus (Jermacz et al., 2017; Jermacz, Dzierżyńska-Białończyk & Kobak, 2017), European bullhead Cottus gobio (Sornom et al., 2012) and spiny-cheek crayfish Orconectes limosus (Hesselschwerdt et al., 2009), as well as fish swimming in the water column: the Eurasian perch Perca fluviatilis, Amur sleeper Perccottus glenii (Ł Jermacz & J Kobak, pers. obs., 2015–2016) and red-bellied piranha Pygocentrus nattereri (Jermacz, Dzierżyńska-Białończyk & Kobak, 2017). Among these species, the goby, bullhead and perch have co-occurred with the gammarid in its home range, the Amur sleeper and crayfish were met several dozen years ago in its novel areas, whereas the piranha had no previous contact with D. villosus. The above-mentioned studies indicate a universal method of predator recognition exhibited by D. villosus, effective with regard to both native and novel predatory species. A situation when potential naïve prey recognizes and responds to a novel predator can be explained by several mechanisms. For example, conspecifics can be present in the predator diet, providing information about predation risk (Chivers & Smith, 1998), as was demonstrated for another invasive gammarid Pontogammarus robustoides (Jermacz, Dzierżyńska-Białończyk & Kobak, 2017). Moreover, the novel predator can be closely related to some native predators (Ferrari et al., 2007; Sih et al., 2010) and therefore release similar signals.

The avoidance reactions of D. villosus were studied by Jermacz, Dzierżyńska-Białończyk & Kobak (2017) in a flow-through Y-maze allowing gammarids to select an arm with or without the scent of predators fed on different diets. This study indicated that the avoidance of predators was induced in the presence of kairomones emitted by hungry predators (starving for 3 days), including totally allopatric, tropical P. nattereri (Jermacz, Dzierżyńska-Białończyk & Kobak, 2017). The avoidance response of D. villosus to another hungry predator, American spiny-cheek crayfish, was noted by Hesselschwerdt et al. (2009). Thus, the predator identification system of D. villosus seems to be independent of the presence of conspecifics in the predator’s diet. Nevertheless, it should be noted that D. villosus did also recognize the predator diet and used it as an additional source of information about the predator status and current level of predation risk, though its responses to satiated predators did not include avoidance (see the chapter “Positive response of D. villosus to the predation cue” below) (Jermacz, Dzierżyńska-Białończyk & Kobak, 2017). Avoidance of a hungry predator, which is most determined to obtain food, and modifications of the responses to satiated predators suggest that D. villosus is capable of effective risk assessment and flexible responses, adjusted to the current situation. A similar relationship between the level of predator satiation and prey response was observed in the case of a water beetle Acilius sulcatus, responding only to hungry perch, but not to satiated fish (Abjörnsson et al., 1997).

The versatility of the predator detection mechanism of D. villosus could be related to the fact that active components of kairomones emitted by unrelated predators are often very similar (Von Elert & Pohnert, 2000). Therefore prey can react to diverse predators, including those which evolved in isolated ecosystems. In temperate European water bodies, fish usually have broad diet ranges and most of them feed on invertebrate food at least at particular life stages (Wootton, 1990; Gerking, 1994). Thus, a general response to hungry fish of particular size seems beneficial under such conditions. D. villosus is an invasive species characterized by a high dispersal rate. During the dispersal, the probability of meeting a novel predator is high, therefore species exhibiting universal defence mechanisms and/or the capability of quick adaptations are more likely to be successful invaders.

Anti-predator defence mechanisms of D. villosus

Positive response of D. villosus to the predation cue

In general, a chemical signal indicating predator presence induces a defence response responsible for the reduction in predation risk (Brönmark & Hansson, 2000; Ferrari, Wisenden & Chivers, 2010). However, in the case of omnivorous species, capable of feeding on predator faeces or their dead bodies, or partly sharing their diet, a predation signal does not always indicate only a danger and, as a consequence, does not always induce a defence response. Such a unique situation takes place in the case of D. villosus as it actively avoided the scent of hungry predators in a Y-maze, but did not exhibit an avoidance reaction to the predation cues emitted by predators fed with chironomids or other gammarids (including conspecifics) (Jermacz, Dzierżyńska-Białończyk & Kobak, 2017). On the contrary, it showed an active preference, moving towards the scent of satiated predators in a Y-maze (Jermacz, Dzierżyńska-Białończyk & Kobak, 2017). A similar response was induced by the presence of cues released by crushed conspecifics and other gammarid species. This reaction suggests that this omnivorous and cannibalistic species is able to use such a signal not as a predation cue, but as a source of information about the location of a feeding ground. As shown in the above sections of this review, D. villosus is characterized by an effective defence strategy (Kobak, Jermacz & Płąchocki, 2014; Błońska et al., 2015; Błońska et al., 2016; Jermacz et al., 2017), therefore being relatively safe in the presence of predators, especially when alternative prey items are available in the vicinity (Jermacz et al., 2015a; Błońska et al., 2016). In such a situation, D. villosus may follow a predator to feed on its faeces or sense wounded invertebrates as being its potential prey. A similar trade-off between predator avoidance and foraging was observed in the case of Gammarus pulex, which in the presence of food did not respond to the predation signal, contrary to the situation when it was exposed only to predator kairomones (Szokoli et al., 2015).

Costs of the anti-predator responses of D. villosus

Anti-predatory defences of prey organisms usually result in considerable energetic costs of the development of additional structures, selection of suboptimal habitats and/or decreased feeding due to the higher vigilance focused on predator detection (Hawlena & Schmitz, 2010; Sheriff & Thaler, 2014). This may result in growth reduction (Janssens & Stoks, 2013), weaker condition (Slos & Stoks, 2008) and/or finally even mortality (McCauley, Rowe & Fortin, 2011). The impact of the presence of predators on the feeding of D. villosus was checked by Jermacz & Kobak (2017). The gammarids considerably limited their feeding in the presence of predators (by 95% and 74% depending on the location of food, placed in the direct vicinity of shelters or away from them, respectively). Surprisingly, this response was even stronger than that of the related species P. robustoides (77% and 33%, respectively), though the latter seems to be more susceptible to predation pressure. On the other hand, no decrease in feeding was observed when single gammarids did not have to search for their food, having it available directly in their shelters. This shows that the aforementioned limitation of feeding in the open field resulted from the limited activity of gammarids (when food was located close to the shelter) or their increased vigilance in the open field (when food was distant from the shelter and no reduction in the search time was observed).

Nevertheless, the most important result of the study by Jermacz & Kobak (2017) was the demonstration that the growth rate of D. villosus supplied with food in their shelters (over a period of 2 weeks) was unaffected by the presence of predators. On the other hand, P. robustoides under the same conditions significantly reduced its growth rate by ca. 60% when exposed to predation cues (Jermacz & Kobak, 2017). Reduction in growth under predation risk was also observed in an amphipod Hyalella azteca, accompanying its induced morphological adaptations resulting in lower predator pressure (James & McClintock, 2017). This confirms the relatively high resistance of D. villosus to non-consumptive predator effects and shows that it may thrive in a good physiological condition under predatory pressure.

Resistance of D. villosus to predator non-consumptive effects was also confirmed by Richter et al. (2018), who did not observe any disturbance of gammarid feeding behaviour under the pressure of a benthivorous fish, the European bullhead (Cottus gobio). In contrast, another gammarid species (G. pulex) reduced its consumption in the presence of C. gobio kairomones (Abjörnsson et al., 2000). Lagrue, Besson & Lecerf (2015) have shown that the abundance of armoured detritivore prey did not decrease in the presence of predators, in contrast to that of non-armoured species. D. villosus is more armoured than other gammarids (Błońska et al., 2015), and thus the consequence of trade-offs between behavioural and morphological defences, such as the cost of the anti-predator responses of D. villosus seems to be less pronounced than that of other gammarids.

Ecological significance of the anti-predator strategy of D. villosus

We have shown that D. villosus is capable of flexible predator recognition (Jermacz, Dzierżyńska-Białończyk & Kobak, 2017) allowing the species to respond to both novel and known dangers. It seems unlikely that it may benefit from the naïvety of local predators in central and western Europe, as they are used to preying on native gammarids (MacNeil, Dick & Elwood, 1999; MacNeil, Elwood & Dick, 1999) and not very selective with regard to their benthic food, consuming also large quantities of alien amphipods (Rezsu & Specziár, 2006; Eckmann et al., 2008). Moreover, predators of Ponto-Caspian origin, sympatric to the gammarids, such as several species of gobiid fish, have also invaded the same regions and co-occur with D. villosus in most of its current range, and include it in their diet (Grabowska & Grabowski, 2005; Borza, Eros & Oertel, 2009; Brandner et al., 2013). Therefore, its ability to easily recognize potential dangers may be one of the traits facilitating its establishment in invaded areas.

The efficient defence mechanisms of D. villosus make this species relatively resistant to predation (Kobak, Jermacz & Płąchocki, 2014; Jermacz et al., 2017; Jermacz, Dzierżyńska-Białończyk & Kobak, 2017), which may help it in its competition with other gammarids (Jermacz et al., 2015a; Beggel et al., 2016). Other, less resistant and more often consumed species are preferentially removed from the environment by predators and must spend more energy and time on anti-predator vigilance, whereas D. villosus, as the least preferred potential food, may thrive in the presence of predators with no negative effect on its growth (Jermacz & Kobak, 2017). Moreover, its aggressive behaviour may force competing gammarid species to less suitable habitats (Platvoet et al., 2009; Jermacz et al., 2015a) or make them swim more often in the water column, which further exposes them to fish predation (e.g., Jermacz et al., 2015a; Beggel et al., 2016). In addition to direct intra-guild predation and competition for food, this displacement from shelter is likely to be another factor making D. villosus an efficient competitor displacing other species from the areas in which it appears. Negative interactions with D. villosus make other gammarids avoid the presence of the stronger competitor, increasing their migrations to new areas and switching to different habitats (Dick, Platvoet & Kelly, 2002; Hesselschwerdt, Necker & Wantzen, 2008; Platvoet et al., 2009; Jermacz et al., 2015a; Kobak et al., 2016).

Nevertheless, the nature of interactions between D. villosus and its related species is far more complex. The presence of predators does have an impact on D. villosus behaviour (Jermacz, Dzierżyńska-Białończyk & Kobak, 2017; Kobak et al., 2017; Jermacz et al., 2017) and may reduce its interspecific aggression, allowing the competing species to stay in its presence. Jermacz et al. (2015a) have demonstrated that another gammarid P. robustoides is easily displaced from habitats preferred by both species in a safe environment, but the presence of predatory fish changes the situation, allowing P. robustoides to stay in the area co-occupied by D. villosus. It is difficult to distinguish whether this is due to the reduction in D. villosus aggression or the higher substratum affinity of P. robustoides in the presence of predators (selecting the vicinity of the stronger competitor as the lesser evil), or both. Nevertheless, individuals of both species can take advantage of staying in a group and reduce the probability of a successful predator attack (Jermacz et al., 2017). This also shows how important it is to consider the effect of predators when studying competitive interactions between species because the consequences of competition in a predator-free situation, which is very unlikely in the wild, may be easily overestimated.

Moreover, as the reduction in the feeding rate of D. villosus in the presence of predators was observed by Jermacz & Kobak (2017), it is likely that the predatory impact of this gammarid on the local community can also be lower than expected on the basis of experiments conducted in fishless conditions. This confirms the results of the field studies in the River Rhine (Hellmann et al., 2015; Hellmann et al., 2017; Koester, Bayer & Gergs, 2016) and can explain their discrepancy with some laboratory experiments, indicating the strong predatory impact of D. villosus on invertebrates (Dick & Platvoet, 2000; MacNeil & Platvoet, 2005).

Unexpectedly, despite the high consumption of D. villosus commonly observed in the field (Kelleher et al., 1998; Grabowska & Grabowski, 2005; Eckmann et al., 2008; Borza, Eros & Oertel, 2009; Brandner et al., 2013; Czarnecka, Pilotto & Pusch, 2014), it was experimentally demonstrated that its dominance may in fact decrease the quality of food conditions for fish due to the higher difficulty of capturing and handling, leading to poor growth on a diet based on this species, compared to the diets consisting of native gammarids or chironomid larvae (Błońska et al., 2015). Thus, although fish feed on D. villosus in the areas invaded by this species, it seems they would have thrived much better if this invasion had not occurred and other gammarid species (usually displaced by the invader) had been available as alternative food (Błońska et al., 2015).