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Diver Fear Effects and Other Human Alterations of Predation Risk in Marine Systems

  • Author(s): Ridlon, April Danielle
  • Advisor(s): Gaines, Steven D
  • Warner, Robert R
  • et al.
Abstract

Humans have altered the ocean on a global scale. From large-scale extractive activities such as fishing, to the unintentional introduction and spread of invasive species via shipping vessels, human activities shape marine communities worldwide, having myriad effects on ecosystem functions and resilience. Even recreational activities that are assumed to have lesser impacts, such as SCUBA diving, are intensifying and becoming increasingly concentrated inside marine protected areas. Research into a wide range of direct and obvious human impacts has informed the effective management of marine systems for both conservation goals and human uses. However, understanding the more nuanced pathways for the effects of human disturbance is critical, especially in systems facing multiple stressors, as they may serve to tip the balance between healthy ecosystems and degraded ones. In particular, there is recent and growing evidence that human activities are altering predation risk in marine systems. When humans change the abundance, distribution, or behavior of marine predators, whether through fishing or other forms of disturbance, those changes can ripple through marine ecosystems due to the comparatively large effects that predators have on other trophic levels. Predators exert both consumptive and non-consumptive effects on prey populations, and can thus influence other species interactions and trigger cascades that can result in the fundamental restructuring of marine systems. However, although risk effects have been well studied in terrestrial systems, these effects have been largely neglected in marine systems. In this thesis, I explore two different pathways for the effects of human alteration of predation risk. My first two chapters examine the non-consumptive, or fear effects of recreational spearfishing, diving, and snorkeling to marine fish. My third chapter examines the consumptive effects of an introduced predator on both a native and an invasive prey population, and the dynamics between them.

Chapters One and Two: Diver fear effects

The ecology of fear is based on evidence demonstrating that predation risk is a strong motivating factor in individual prey behavior, and has consequences at the population, community and ecosystem level. While predator escape theory was developed with natural predators in mind, humans can act as predators (e.g. while fishing) or mimic predators (e.g. while diving). The recent testing of predator escape theory by the measurement of flight initiation distance (FID) - the distance at which a fish flees from approaching diver - represents a promising new avenue for future research on diver fear effects to marine fish and in marine ecosystems. My synthesized review of the available empirical evidence suggested that fish react to divers with increases in vigilance and flight where they are exposed to spearfishers as compared to areas where they are protected from fishing. In contrast, I found that the effects of recreational diving on the flight and vigilance behavior of fish have not been well studied or effectively measured to date. In order to explore the effects of long-term recreational diving on the behavior of a common reef fish, I conducted a series of experiments on reefs in the Cayman Islands where recreational diving activity has been consistent and spearfishing has been banned for decades. By measuring the FID and vigilance behavior of over 250 individual Stoplight Parrotfish (Sparisoma viride), I found evidence for habituation to divers by this species in areas where recreational diving is most concentrated. The near lack of a flight response in fish exposed to chronic diving activity represents the lowest FID recorded for the species in either protected or fished areas elsewhere in the world. The significant decrease in flight and vigilance in individuals in the highly dived area in comparison to those in less frequently dived areas also suggests that the frequency of diving activity drives this response. However, significant declines in the bite rates and frequency of cleaning interactions of individuals in the immediate presence of a diver also suggested that there may be fitness costs associated with recreational diver encounters, even for habituated fish. I therefore used these decreased bite rates to estimate a cumulative cost of daily diver encounters to an individual fish in terms of lost feeding. Where habituation to divers was extreme at my study site, estimated feeding loss for an individual fish was low. For scenarios in which I simulated lower levels of fish habituation and different diver behavior, estimated feeding loss due to diver encounters were much higher. This suggests that the cumulative costs of recreational diver encounters may be significant if, for example, larger flight distances must be maintained due to the occasional or nearby presence of spearfishers. Based on my findings, I make recommendations for future research into the behavioral effects of spearfishing, recreational diving, and the potential interaction of these two activities on the behavior of marine fish. I also recommend the incorporation of these behavioral effects into marine spatial planning and management for multiple human uses, particularly where spearfishing and recreational diving co-occur.

Chapter Three: Predation effects of an introduced predator

As multiple invasions accumulate in marine systems, identifying the species traits and interactions that affect invasion success is critical for predicting the outcomes of multiple species introductions. Facilitation is a major mechanism for invasion success that can increase the magnitude of impact of an existing invasion. Marine predators can facilitate invasions and may be more likely to tip the balance of dynamics between species in an invaded system via top-down effects. I examined the effect of predation by an introduced crab, Carcinus maenas, on the native snail Cerithidea californica and the invasive snail Ilyanassa obsoleta. These two common snail species co-occur in the San Francisco Bay estuary, where there is evidence for the competitive displacement of the native snail by the invasive. Laboratory experiments revealed that Carcinus maenas predation was strongly and significantly greater on the native species as compared to the invasive. While the frequency of crab attacks was not significantly different between snail species, the predator was 5.45 times more successful at killing the native C. californica than the invasive I. obsoleta given an attack. This differential predation success drives the higher overall mortality in native snails. In light of the competitive displacement of the native snail by the invasive in this system,these results demonstrate that the introduced predator C. maenas can have both direct negative impacts on native species and indirect positive impacts on other invaders via facilitation. My results provide unique information about a predator’s potential to indirectly influence the success of an invasion, and contribute to our understanding of the role of introduced predators in influencing the dynamics of multiple invasions in marine systems.

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