Commentary: using prey naïveté to inform ecological management

1. Introduction

Stockwell et al. [1] tell the unfortunate story of the pahrump poolfish (Empetrichthys latos). The poolfish—a relic of historically larger lakes in the American southwest—is threatened by several novel predators and larvivores. However, the poolfish is naïve to the novel predators and larvivores, possessing limited abilities to recognize them and respond appropriately, resulting in the poolfish's steady, and perhaps inevitable, decline. The poolfish shows stunting in a key sensory ability—the detection of conspecific alarm cues via epidermal club cells—which appears to drive its naïveté. Even more tragically, this naïveté is presumptively secondary in evolutionary terms, meaning that ancestors of the poolfish probably possessed a significant club cell response pathway, but evolved naïveté in the absence of predators owing to either drift or fitness cost.

We believe that, read correctly, the work of Stockwell et al. [1] should serve both as a warning sign and a source of inspiration for managers, particularly those of aquatic systems. It should serve as a warning sign, because—as we argue below—novel interactions between introduced predators and naïve prey are likely to increase in frequency during the Anthropocene. It should inspire managers to take an evolutionary perspective when predicting and reacting to threats from novel interactions, as evolution of naïveté may predestine some populations to success and others to failure. As many others (including Stockwell) have argued before [2–4], an evolutionary approach can also provide managers with clear recommendations for increasing the chance of population persistence—even within the confines of traditional management policies and tools—as long as we follow evidence rather than the status quo.

2. Novel interactions are becoming more common

An increasingly common hallmark of the Anthropocene is the movement of species into new geographical locations. Humans are accelerating these movements in two primary ways. First, organisms may be directly moved by humans. These direct introductions can be intentional or incidental [5]. The second, less immediately obvious way, is through geographical range shifts driven by anthropogenic environmental change. Anthropogenic change such as climate change and land-use change causes cascading effects that allow species to enter habitats from which they were previously excluded [6]. Shifts in species' geographical ranges towards higher latitudes and elevation is one of the most documented responses of organisms to global climate change [7]. As a result of these introductions and range shifts, novel interspecific interactions are becoming more prevalent [8].

Often the species that are most successful at establishing in new habitats following range shifts or human introductions are generalist consumers [9,10]. The wide-ranging diet of generalist consumers often prevents them from constraint by particular prey availability when they move into new habitats. Generalist consumers are by definition likely to generate numerous novel interactions in which they are the predator. Thus, the Anthropocene will increasingly involve native prey experiencing novel predators [9,11].

Novel interactions are observed in all manner of ecosystems, though not necessarily in equal frequency. Freshwater fishes are particularly notable in this regard, as humans intentionally introduce fishes at a particularly high rate [5]. Some fishes, like bass (Micropterus salmoides), are commonly introduced into new waterbodies for sport fishing [5]. Others, such as mosquitofish (Gambusia spp.), are widely introduced for pest control [12]. In many of these cases (including the above), the introduced fishes are generalist consumers that create numerous negative novel interactions. Moreover, there is substantial evidence that fishes with generalist and piscivorous diets are more likely to expand or shift their ranges in response to global climate change [13]. Together, these modes of introduction create a two-pronged threat by which native freshwater organisms are especially likely to experience novel predators.

3. Naïveté imperils prey species during novel interactions

A significant, worrying aspect of novel predator–prey interactions is prey naïveté. While novel predators may often be generalists, typically possessing the ability to recognize novel prey, the reciprocal is not always true for prey. Prey naïveté—the lack of appropriate recognition and response to novel predators—can spell doom for some prey species [14]. Naïveté is complex, as both the sensory pathways for recognizing predators and the defence mechanisms for avoiding depredation are diverse (including physiology, morphology, behaviour and life history) and often predator- and habitat-specific [14,15]. The evolution of naïveté is also complex and can result from two pathways. The first, more obvious pathway is naïveté of prey species never exposed to a specific predator in deep time [16] (i.e. primary naïveté). Second, prey populations with successful antipredator mechanisms may also evolve naïveté when a predator disappears from a predator–prey interaction (i.e. secondary naïveté), as postulated by Stockwell et al. [1]. Many antipredator mechanisms are costly to maintain thus, naïveté can provide a short-term fitness advantage in the absence of a predator, allowing selection for naïveté [14]. Additionally, drift or gene flow could also lead to the evolution of naïveté without selection.

Indeed, secondary naivete has been well-documented in aquatic environments, particularly those that are fragmented [16]. Fragmented aquatic populations are more likely to develop secondary naïveté owing to (i) limited recolonization by predators following predator loss, (ii) limited gene flow from non-naïve populations, and (iii) higher rates of genetic drift. Secondary naïveté may be increasing in frequency during the Anthropocene as humans extirpate native predator species [11]. Evolutionary rescue (rapid adaptive evolution in response to a source of population decline) from naïveté can save prey populations from extirpation in some cases, but evolutionary rescue is often significantly limited by standing genetic variation in populations of management concern [17].

Thus, naïveté lies at the crux of why many species are imperiled by novel interactions. As such, a thorough case-specific understanding of naïveté is necessary to both predict and manage threatened prey. Naïveté and rescue therefrom are evolutionary processes, so management of naïve prey populations requires an evolutionary approach.

4. Using antipredator adaptation and naïveté

Below is a checklist for determining the risk of naïveté and the potential for adaptation, past or present, to aid a population of concern when a novel predator is introduced. This checklist can be used to assess risk to prey of novel predator-mediated extirpation before or after the introduction of the novel predator. Perhaps counterintuitively, the identity of a novel predator can often be known prior to introduction, either because a known invasion front is moving towards a population of concern, or because a specific novel predator is likely to be introduced intentionally (a common occurrence with fishes [5]). Even if no specific novel predators are anticipated, small populations of conservation concern could be assessed for general naïveté. This checklist leans heavily on knowledge of the natural history and phylogeny of the novel predator and potential prey. Often there may be gaps in knowledge about a specific prey or predator species, in which case evidence from closely related taxa may be carefully substituted:

• — has historical evolution set the prey population up for success?;
• (i) has the prey population coexisted consistently with established predators, particularly predators closely related to the novel predator?: tolerance of established predators can be a key indicator of prey success in the face of novel predators. This is particularly true if the established predators share similarities with novel predators, such as habitat use, feeding mode, kairomone patterns, and visual trait patterns [18]. These similarities increase the likelihood of recognizing and defending against the novel predator (see below). Such similarities are most likely exhibited among closely related predator taxa [16],
• (ii) does the prey population have sufficient mechanisms to recognize the novel predator?: cues for predator recognition are diverse and include various visual, audial and chemical cues [15]. These cues may involve recognition of the predator or depredation of con- or heterospecifics. Thus, the success of prey in the face of a novel predator involves possession of the mechanisms to receive the novel predator cues, which are themselves diverse. Furthermore, success in the face of a novel predator also requires the ability to learn to associate said cues with danger from the new predator, and
• (iii) does the prey population have sufficient defences to withstand the novel predator?: much as cues can be predator-specific, antipredator defences can also be predator-specific. Antipredator defences are extremely diverse, and span behaviour, morphology, physiology and life history [12,14]. Many of these defences are predator-specific—for example accelerated growth life histories may only prove useful against gape-limited predators. Other defences are context-specific—for example hiding behaviours may beget little use in open environments. Thus, risks from novel predators should take into account the ability of prey species to defend themselves against predators using appropriate defences;

• — is future evolution likely to rescue the prey population?;
• (i) does the prey population have sufficient sources of adaptive genetic variation to evolve defenses to the novel predator?: even some predator-naïve populations can successfully evolve antipredator defences in the face of novel predators, avoiding extirpation via evolutionary rescue. However, to do so, populations must possess significant adaptive genetic variation for natural selection to facilitate evolutionary rescue [17]. This genetic variation can come from the population itself (standing genetic variation) or from other populations (gene flow). Unfortunately, many of the most threatened and most naïve prey populations are also those with the lowest levels of standing genetic variation and gene flow [19].

(a) . Facilitating adaptation

When the answers to the above questions are ‘no’, all is not lost, and managers do have some options. Managers can work to introduce new, adaptive alleles by facilitating gene flow (translocations), assuming some other populations of the species exist. One caveat to translocations is that high levels of endemism in some species can limit the success of these efforts [19]. Increasing effective population size can also increase genetic variation by increasing the overall mutation rate [20]. However, increasing population size through captive propagation operations—a popular management tool—is generally counterproductive, as it can lead to further inbreeding, hatchery domestication, and significant maladaptation to wild environments [21]. Thus, facilitation of increased population size should be conducted in the wild whenever possible or in environments that mimic the wild as closely as possible. Such facilitation may include changes in habitat (e.g. refugia), ecological interactions, and land use. In many cases, facilitating evolutionary rescue in the face of prey naïveté may mimic more traditional management goals: increasing the quantity and quality of habitat and facilitating connectivity of prey (but not predator!) populations [2–4].

5. Conclusion

To many, the pahrump poolfish—with its evolved secondary naïveté and ensuing population decline in the face of a novel predator—will seem like a new, unique story. However, a broad view of Anthropocene trends compels us to consider cases like that of the poolfish are growing in frequency. Novel interactions are becoming more common. Prey naïveté and its evolutionary roots set many populations up for extirpation during novel interactions, but an evolutionary approach to management can use naïveté to predict population declines and manage recoveries. Thus, we implore managers to keep evolutionary management on the table when dealing with threatened prey species, and to keep in mind the evolutionary consequences of some management tools, such as captive propagation.

Data accessibility

No data were collected, created or analysed as part of this work.

Authors' contributions

Z.T.W.: conceptualization, writing—original draft and writing—review and editing; I.S.: conceptualization, writing—original draft and writing—review and editing.

Both authors gave final approval for publication and agreed to be held accountable for the work performed therein.

Conflict of interest declaration

The authors declare no competing interests.

Funding

The authors have no funding to report for this work.