Anti‐predator mechanisms in evolutionarily predator‐naïve vs. adapted fish larvae

Abstract

It is a fundamental feature of evolution that natural selection acts on individuals to adapt to predation pressure via the development of anti‐predator mechanisms. As such mechanisms are costly in terms of energy and time, species living in habitats where predators are rare or absent were expected to show reduced predator responses. Such a reduction was expected for larvae of the native whitefish (Coregonus wartmanni) in Upper Lake Constance, as these pass their initial stage in a historically predator‐free pelagic habitat and only start to encounter predators in a later ontogenetic stage during which they shift to littoral habitat. However, a recent invader of the pelagic waters of the lake, the three‐spined stickleback (Gasterosteus aculeatus), is implicated in a severe decline in whitefish recruitment through larval predation. The predator‐naivety effect and its consequences on predation were experimentally tested by comparing predator defenses of different age classes of whitefish with those of roach (Rutilus rutilus) and perch (Perca fluviatilis), two species whose larvae grow up in a predator‐holding habitat. As predator, the three‐spined stickleback (Gasterosteus aculeatus) was selected. Sticklebacks actively hunted all prey species but predation was high on whitefish only. The addition of zooplankton (Daphnia) as alternative prey for sticklebacks in the experimental setup did not reduce predation on the whitefish larvae, indicating a clear preference for whitefish in this invasive predator. The escape responses of roach and perch were found to be clearly more complex and diverse to those of the predator‐naïve whitefish larvae. Particularly striking was that whitefish often did not show any apparent behavioral response to the approaching predator. Only large whitefish larvae (Table 1: length = 40.8 ± 0.6 mm) appeared capable of escaping predation, and this was correlated with a change in complexity of predator escape responses. Thus, differences in predation pressure for the different larvae species were highly related to the observed interspecific differences in predator defenses, and with the ontogenetic intraspecific change in whitefish from poor and inefficient predator escape responses to complex and more efficient predator escape responses. The evolutionary consequences of stickleback as an invasive predator on whitefish larvae behavior are discussed.

Threespine Stickleback in Lake Constance: The Ecology and Genomic Substrate of a Recent Invasion

“…The massive recent increase in stickleback abundance coincides with a sharp decline in pelagic whitefish (Coregonus wartmanni, Bloch, 1784) yields, both in the number of individuals caught, and their weight-at-age (Rösch et al, 2017). Previous work has speculated that the invasive stickleback population could have a negative impact on whitefish growth and abundance, and shows that stickleback will prey on whitefish larvae in laboratory foraging experiments (Roch et al, 2018;Ros et al, 2019) or following stocking (Roch et al, 2018). However, the first stickleback population expansion during the eutrophication period in Constance coincides with population size increase in whitefish (Numann, 1972), so the relationship between whitefish and stickleback abundances is either mediated by some other factors in the environment, or it is not causal.…”

“…However, the first stickleback population expansion during the eutrophication period in Constance coincides with population size increase in whitefish (Numann, 1972), so the relationship between whitefish and stickleback abundances is either mediated by some other factors in the environment, or it is not causal. It has been proposed that either competition for pelagic zooplankton resources such as Daphnia -that have declined in abundance with the re-oligotrophication of Lake Constance (Straile and Geller, 1998;Stich and Brinker, 2010;Rösch et al, 2017) -or direct predation on whitefish eggs and larvae (Roch et al, 2018;Ros et al, 2019) are responsible for this reduction in yield. Predation by sticklebacks on eggs and juveniles of their own species occurs frequently (Whoriskey and FitzGerald, 1985;Hyatt and Ringler, 1989;Smith and Reay, 1991;Foster and Bell, 1994;Manica, 2002;Mehlis et al, 2010) along with predation on larvae of other fish species (Hynes, 1950;Manzer, 1976;Delbeek and Williams, 1988;Kean-Howie et al, 1988;Gotceitas and Brown, 1993;Nilsson, 2006;Kotterba et al, 2014;Byström et al, 2015), while previous studies on stickleback populations in the Baltic Sea have suggested that intraguild predation on eggs and juvenile fish is responsible for the observed declines in perch (Perca fluviatilis, Linnaeus, 1758) and pike (Esox lucius, Linnaeus, 1758) recruitment (Nilsson, 2006;Bergström et al, 2015;Byström et al, 2015;Nilsson et al, 2019;Eklöf et al, 2020).…”

The hunter and the hunted—A 3D analysis of predator-prey interactions between three-spined sticklebacks (Gasterosteus aculeatus) and larvae of different prey fishes

“…As an opportunistic species, the ability of sticklebacks to adapt to different and multiple food sources plays a significant role across the different life stages [ 31 ]. It was recently shown that the success of stickleback predation on fish larvae depends upon the size and species of prey [ 32 , 33 ]. Quantitative examination of predation on roach ( Rutilus rutilus ), perch ( Perca fluviatilis ) and whitefish ( Coregonus wartmannii ) larvae shows a particularly high toll on small-sized whitefish larvae which historically grew up in habitat without predators, in comparison to similar-sized larvae of the other two species which have co-evolved with predators in their environment [ 32 , 34 ].…”

“…Sticklebacks have recently increased strongly in abundance in the pelagial of Lake Constance prompting concern that predation on whitefish larvae may be of ecological importance [ 34 ]. Stickleback hunting success has been shown to decrease with prey size and with increasing variation in predator avoidance strategies shown by prey [ 33 ], but it has not been analysed thus far whether these differences might be related to larval swimming performance as well.…”

“…Important performance criteria in predator-prey interactions include the response time of the prey, the speed and efficacy of evasive behaviour vs . hunting behaviour, and factors that prompt the predator to abort the hunt [ 33 , 35 , 36 ]. Questions about the decisions that predators and prey may or must make during a hunt can be addressed using detailed analysis of high-definition video recordings [ 37 , 38 ].…”