Multi-trophic native and non-native prey naïveté shape marine invasion success

Katherine J Papacostas,Amy L Freestone,Peter Eklöv

doi:10.1371/journal.pone.0221969

Abstract

Invasive predators have caused rapid declines in many native prey species across the globe. Predator invasion success may be attributed to prey naïveté, or the absence of anti-predator behavior between native and non-native species. An understanding of the effects of naïveté at different timescales since introduction and across multiple trophic levels is lacking, however, particularly in marine systems. Given the central role of trophic interactions in invasion dynamics, this knowledge gap limits the ability to predict high impact predator invasions. Naïveté was examined across three trophic levels of marine invertebrates: a native basal prey (hard clam), two non-native intermediate predators (the recently-introduced Asian shore crab and the long-established European green crab), a native intermediate predator (juvenile blue crabs), and a native top predator (adult blue crab). We hypothesized that naïveté would be more pronounced in trophic interactions involving the recently-introduced non-native predator in comparison to the long-established non-native and native intermediate predators. We further hypothesized that the recently-introduced intermediate predator would both benefit from naïveté of the native basal prey and be hindered by higher mortality through its own naïveté to the native top predator. To test these hypotheses, three laboratory experiments and a field experiment were used. Consistent with our hypotheses, basal prey naïveté was most pronounced with the recently-introduced intermediate predator, and this increased the predator’s foraging success. This recently-introduced intermediate predator, however, exhibited an ineffective anti-predator response to the native top predator, and was also preyed upon more in the field than its long-established and native counterparts. Therefore, despite direct benefits from basal prey naïveté, the recently-introduced intermediate predator’s naïveté to its own predators may limit its invasion success. These results highlight the importance of a multi-trophic perspective on predator-prey dynamics to more fully understand the consequences of naïveté in invasion biology.

Highlights

Predator-prey interactions are often attributed to coevolution [1, 2], but a lack of shared evolutionary history between native and non-native species alters these interactions substantially and can contribute to the success of non-native species [3]
M. mercenaria did not exhibit anti-predator behavior when exposed to H. sanguineus chemical cues, and M. mercenaria burrowing depth was no different in the presence of H. sanguineus than the control treatment with no predators
The clams burrowed deepest in the presence of C. sapidus, clearly recognizing the native intermediate predator as a threat

Summary

Introduction

Predator-prey interactions are often attributed to coevolution [1, 2], but a lack of shared evolutionary history between native and non-native species (i.e. naïvete) alters these interactions substantially and can contribute to the success of non-native species [3]. There has been far less empirical attention, given to naïvetein marine systems This gap in the literature may be due to limited data on marine predator invasions [12] or the idea that the increased connectivity in marine systems compared to terrestrial and freshwater systems make marine prey naïvetemuch less likely [6, 13]. This inference about limited naïvetein marine environments, is largely based on pelagic systems ([6], see [13] for an estuarine example). Existing marine studies conducted in coastal systems have shown that naïvetecan occur (e.g. [4, 14]) and can have significant impacts on coastal communities (e.g. [15])

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