Abstract
Game theory is commonly used by ecologists to understand complex biological relationships in which the outcome depends on the strategies used by both sides implicated in the interaction, such as between predators and prey. Different strategies result in different payoffs, that is, the net gain or loss incurred based on the energy invested in, and the benefits obtained from, such strategies. Interactions between predators and prey start with the search for prey and escalate through a series of stages from encounter, detection, attack, and capture. Prey may proactively avoid its predators to minimize the rate of encounters. For instance, many shark species are known to aggregate in discrete habitats during their first months of life mainly to avoid predators (e.g., nursery habitats). However, such spatiotemporal patterns of habitat use can easily be predicted by predators. Therefore, predators can capitalize on the needs of the prey to increase fitness by minimizing the energy spent searching (e.g., increasing the net gain from their hunting strategy). Most studies have argued that nursery habitats are beneficial for juvenile prey since predator access is restricted and therefore energy can be spent in other fitness related activities (e.g., foraging). This view overlooks the escape strategies of prey assuming that prey are passive victims. An alternative view is that prey can strategically use habitats where certain habitat features enhance their escape tactics for their advantage despite the presence of predators. Therefore, the overarching goal of this thesis was to improve our ability to define the use of essential nursery habitats by juvenile sharks, by focusing on their escape tactics and how habitat features can maximize their escape performance.
Newborn blacktip reef (Carcharhinus melanopterus) and sicklefin lemon (Negaprion acutidens) sharks were selected as the model species given their high site attachment to coastal shallow fringing reef habitats. The island of Mo'orea, in French Polynesia, was selected as the study system because large numbers of newborns of both species are commonly found in the shallow reefs along the coastline during parturition months, but predation is seemingly high. To investigate escape tactics in newborn sharks, I looked at (1) the behaviour and kinematics of their antipredator escape responses, (2) the role of chemoreception on predator detection, and (3) aerobic exercise capacity associate to a predatory chase. To investigate how habitat features can benefit their escape tactics, I explore the biomechanical advantages of competing with larger predators and manoeuvring in shallow and complex environments. Further, I determined escape and aerobic thermal performance in blacktip reef shark newborns and correlated these results with observed habitat thermal regimes. Through this behavioural, kinematic, and physiological approach, I provide a framework to determine essential habitats for newborn sharks.
In chapter II, I investigated the accelerative manoeuvres, known as fast-starts, in both species of tropical reef shark. Behavioural and kinematic variables were measured using two- dimensional, high-speed videography analysis of mechano-acoustically stimulated newborn blacktip reef (n=12), and sicklefin lemon (n=8) sharks. I predicted (1) high manoeuvrability, given their high flexibility, but (2) low propulsive locomotion owing to the drag costs associated with pectoral fin extension during escape responses. Further, based on previous work on dogfish, Squalus suckleyi, I predicted (3) long reaction times (as latencies longer than teleosts, >20 ms). In line with predictions on manoeuvrability, newborn sharks showed remarkably high turning rates (faster than expected for their size) and tight turning radii (3- 11% of body length) that provides them with the advantage of manoeuvring in structurally complex environments (e.g., coral reefs). These results anticipated that manoeuvring in shallow waters will provide a further antipredator advantage for fish that are smaller than their predators given the biomechanical and hydrodynamical limitation that larger animals incur when manoeuvring in waters too shallow for their size. Interestingly, contrary to my predictions, newborn sharks also displayed extraordinarily fast reaction times (< 20 ms) suggesting that the neurophysiological system of sharks may not be limited to long response times. Together, these results show that fast-starts are a crucial escape tactic employed by newborn tropical sharks. In particular, these results provide the first quantitative assessment of the traits associated with the antipredator strategy of newborn tropical reef sharks (i.e., survival traits).
In chapter III, I studied the use of predator chemical cues in newborn blacktip reef sharks. I used high-speed videography in combination with static respirometry to test changes in their activity level, fast-start escape performance, and oxygen uptake rates following the exposure to conspecific predator diet cue. Postdigestion cues (or diet cues) are released into the environment from the predator’s digestive system and can be used by prey as kairomones. The chemosensory system of sharks is well developed. Olfaction, in particular, is remarkably sensitive in sharks. Sharks can detect molecules from the sub-nanomolar to the micromolar scales. Therefore, sharks’ detection and determination of the origin of odours is extraordinary. However, what is more interesting is that sharks are able to predict odorant distribution in space and time. This is known as the “olfactory spatial” hypothesis. This chemical spatiotemporal sense of their environments is key for assessing predation risk. Many reef fishes use a variety of predator chemical cues to inform on the level of risk so that they can modulate their behaviours accordingly to manage the perceived level of risk. Our understanding of the chemical ecology of the antipredator strategies in sharks is, however, very limited. Given the purported high predation pressure in the reef flats used by newborn blacktip reef sharks around Mo'orea, it was hypothesized that wild newborns would respond to the presence of the conspecific diet cues. Specifically, I hypothesized that upon exposure to conspecific diet cues, newborn blacktip reef sharks will (1) show a significant change in their activity level, (2) increase the strength of their fast-start responses, and (3) show a significant change in their oxygen uptake rates. Wild-caught newborn blacktip reef sharks were exposed to adult conspecific faeces, teleost faeces, and a seawater control. I measured (1) their activity level (n = 36) immediately after cue exposure for five minutes; after the five minutes exposure sharks were startled and (2) fast-start escape performance (n = 36) measured in the same way as in Chapter II; a subset of sharks was used to (3) measure their oxygen uptake rates (n = 12) upon cue exposure as proxies for antipredator response. In line with predictions, sharks swam at slower speeds when exposed to predator cues, compared to controls. Interestingly, contrary to predictions, sharks decreased their fast-start escape performance following the exposure to predator cues. It was likely possible that sharks were able to use the chemical information presented, in addition to vision, to assess the situation as low-risk given the absence of predators visually detected, and responded accordingly to minimize the energy spent. Unfortunately, given the small sample size (only four individuals per treatment), I was unable to determine with certainty if their increase in oxygen uptake rate corresponded to a hyper- vigilance response. These results are paramount to understand how sharks manage predation risk, both pre- and post-encounter with a predator, and to explain their patterns of habitat use when the risk of predation is imminent.
Finally, in chapter IV, I exposed blacktip reef sharks, ex situ, to their natural thermal regime and tested their escape and aerobic performance under a range of ecologically relevant temperatures (25oC, 27oC, 29oC or 31oC). I predicted that newborn blacktip reef sharks are able to capitalise on the thermal conditions of their environment to ensure high escape performance (i.e., both fast-start and endurance). Also, I anticipated that given the high level of performance of their antipredator tactics (i.e., fast-starts and endurance combined) sharks will be subject to a high recovery cost. Fast-start escape performance was measured using the same protocol as in chapter II using all sharks from temperature treatments (12 per treatment, n = 48). Oxygen uptake rates were measured using static respirometry for 24 hours following an exhaustive predatory chase to obtain an aerobic thermal performance curve and a recovery curve using all sharks excluding the 25oC group (n = 36). The results from the laboratory experiments were combined with filed observations of daily habitat thermal fluctuations. I predicted that the habitat used by newborn blacktip reef sharks provide thermal condition that allow for a high escape performance. Historical temperature records (from seasons 2019-2020, 2020-2021, and 2021-2022) were used to build diel thermal cycles of four representative habitats used by newborn sharks. The results showed that under Mo'orea’s thermal conditions, sharks display both maximal escape and aerobic performance. Turning rate and acceleration increased within the thermal range observed in the wild and thermal quotients (Q10) values indicated that escape performance is likely at a maximum level. The optimal temperature for peak aerobic performance (29.2oC) was similar to the average habitat temperature observed during the parturition months. The breadth for performance was narrow but also similar to the range of temperatures observed during a 24-h cycle. That is, under Mo'orea’s thermal conditions, sharks show aerobic performance ≥ 80%. Therefore, newborn sharks likely use these habitats as an antipredator advantage. Nonetheless, although recovery was not affected by temperature, the cost was high (i.e., long recovery periods and large oxygen debt). Further, I recorded warm extreme event in the habitats that would lower their aerobic performance below 80%. In conclusion, the use of warm habitats can be a strategy to maximize escape performance but relying on these habitats makes newborns sharks susceptible to marine heatwaves.
Sharks’ nursery ecology has strongly relied on the idea that avoidance of predators is the main antipredator strategy but has widely overlooked their escape tactics. My work is the first to study how shark escape tactics correlate with habitat feature. The use of shallow, structurally complex, and warm terrestrial reef flats can be seen as a strategy to maximize the probability to survive a predator attack. Therefore, given this high ecological benefit, Mo'orea’s terrestrial reef flats can function as a nursery system essential for the local population of blacktip reef and sicklefin lemon sharks. Together the results of this study will help improve our ability to define essential nursery habitats for sharks.