Anthropogenic Impacts

Marine predators are increasingly threatened by anthropogenic pressures which can potentially modify their ecology, physiology and behaviour.

Of these pressures, we find the tourism activities that are in rapid development and include artificial food provisioning for predators and all environmental pressures caused by climate change.

1) Effects of artificial food provisioning on marine predators

The feeding of wildlife has become a popular means by which tourists and tourism operators can facilitate close observation and interaction with wildlife. Compared to marine pollution, coastal habitat degradation, over-exploitation and intensive fishery, shark-feeding seems of little concern. However this practice is widespread throughout tropical and subtropical seas of the world and gives rise to controversy with little consensus on how it should be managed. Shark-feeding is probably one of the most impressive activity tourists can experience underwater. Deliberate and long-term shark feeding is suspected to alter natural behaviour patterns of shark populations, engender dependency and habituation, increasing aggression towards humans by conditioning them to associate humans with food, and to have adverse effects on surrounding communities. On the other hand, tour operators defend the practice as a mean to spread awareness and promote conservation. Despite this controversy, there are few comprehensive reports that consider the impacts of the shark-feeding while the practice is widespread and growing.

Overview of the existing shark and ray provisioning operations in the world (Brena et al. 2015)

Provisioning can have interacting and cascading effect on the behaviour, ecology and physiology on sharks at different scales (individual, group, community; Brena et al. 2015)

If the effect of provisioning can vary between species and location, most studies have found little major long-term changes in the ecology of sharks due to this activity, with important processes such as reproduction, migrations and natural predation being maintained. However, we found that on site attached species such as the blacktip reef sharks (Carcharhinus melanopterus), it can cause important shifts in habitat use, although it is unclear how it can influence the fitness of individuals and long-term population dynamics.

Effects of provisioning on blacktip reef shark residency, split by habitat type, diurnal activity or sex. Effect sizes and their 95% confidence intervals are shown. Statistically significant effects (95 % CI not overlapping 0) are presented in red for positive effects and in blue for negative effects. Non-significant effects (95% CI overlapping 0) are presented in grey. (Mourier et al. 2021)

The tourism activities linked to artificial provisioning of blacktip reef sharks (Carcharhinus melanopterus) and pink whiprays (Pateobatis fai) on a specific site in French Polynesia were suddenly and completely stopped due to a COVID-19 lockdown that lasted 6 weeks from March 20 until April 30, 2020. This was an opportunity to investigate how species are affected by provisioning activities. Using both drone footage and underwater counting, we were able to track the abundance of those two species before, during, and after reopening. The absence of any stimulus during this long period resulted in almost total desertion of the site by the elasmobranchs. However, 1 day prior to reopening, some individuals of both species positively reacted to the single acoustic stimulus of an engine boat, showing the resilience of conditioning, and some elasmobranchs reacted to acoustic and olfactive stimuli linked to the provisioning practice from the first day after reopening. Pre-lockdown abundance levels were considered restored 1 and 2 months after reopening for blacktip reef sharks and pink whiprays, respectively. These findings improve our capacity to better understand the potential effects of artificial provisioning tourism on the abundance of elasmobranchs by showing that conditioning is resilient for several weeks, suggesting that intermittent interruption of elasmobranchs feeding would not really help to decrease its impact on animal welfare.

Photographs from drone surveys showcasing representative abundance of sharks (red circles) and rays (yellow circles) at the Tiahura feeding site on (a) 04/29/2020 (2 days before re-opening) showing the presence of one shark; (b) 04/30/3030 (1 day before re-opening) showing the presence of four sharks and three rays; (c) 05/02/2020 (1 day after re-opening) showing the presence of eleven sharks and five rays; (d) 06/01/2020 (31 day after re-opening), showing the presence of 20 sharks and 9 rays. (Séguine et al. 2022)

2) Response of elasmobranchs to climate change

This research area was conducted as part of my contribution to a collaboration with Dr. Jodie Rummer from PHYSIOSHARK project.

The Physioshark project, led by Dr. Jodie Rummer from James Cook University in Australia, investigates how climate change impacts the physiology of newborn and juvenile reef sharks. Sharks that are born today represent adult shark populations of the future. Understanding how human and environmental impacts affect these sharks is crucial knowledge for developing effective shark conservation strategies.

The fieldwork is based at the CRIOBE Research Center on Moorea, French Polynesia. The project investigates the physiological energetics (i.e., costs/benefits) of newborn blacktip reef and sicklefin lemon sharks living in the 11 potential nursery areas identified around the island. For instance, the research team is investigating how well newborn sharks cope with hot water temperatures in these nurseries and how the cost of growing up in these nurseries will change with increased human disturbances like coastal development and climate change.

I have been involved in several publications led by Jodie.

• Thermal tolerance

Temperature and oxygen limit the distribution of marine ectotherms. Haematological traits underlying blood-oxygen carrying capacity are thought to be correlated with thermal tolerance in certain fishes, and this relationship is hypothesised to be explained by oxygen supply capacity. We tested this hypothesis using reef shark neonates as experimental models because they live near their upper thermal limits and are physiologically sensitive to low oxygen conditions. We first described in situ associations between temperature and oxygen at the study site (Moorea, French Polynesia) and found that the habitats for reef shark neonates (Carcharhinus melanopterus and Negaprion acutidens) were hyperoxic at the maximum recorded temperatures. Next, we tested for in situ associations between thermal habitat characteristics and haematological traits of neonates. Contrary to predictions, we only demonstrated a negative association between haemoglobin concentration and maximum habitat temperatures in C. melanopterus. Next, we tested for ex situ associations between critical thermal maximum (CT_Max) and haematological traits, but only demonstrated a negative association between haematocrit and CT_Max in C. melanopterus. Finally, we measured critical oxygen tension (p_crit) ex situ and estimated its temperature sensitivity to predict oxygen-dependent values of CT_Max. Estimated temperature sensitivity of p_crit was similar to reported values for sharks and skates, and predicted values for CT_Max equalled maximum habitat temperatures. These data demonstrate unique associations between haematological traits and thermal tolerance in a reef shark that are likely not explained by oxygen supply capacity. However, a relationship between oxygen supply capacity and thermal tolerance remains to be demonstrated empirically.

Graphical abstract from Bouyoucos et al. 2021

• Ocean acidification and pH

Anthropogenic ocean acidification (OA) is a threat to coral reef fishes, but few studies have investigated responses of high-trophic-level predators, including sharks. We tested the effects of 72-hr exposure to OA-relevant elevated partial pressures of carbon dioxide (pCO₂) on oxygen uptake rates, acid–base status, and haematology of newborn tropical blacktip reef sharks (Carcharhinus melanopterus). Acute exposure to end-of-century pCO₂ levels resulted in elevated haematocrit (i.e. stress or compensation of oxygen uptake rates) and blood lactate concentrations (i.e. prolonged recovery) in the newborns. Conversely, whole blood and mean corpuscular haemoglobin concentrations, blood pH, estimates of standard and maximum metabolic rates, and aerobic scope remained unaffected. Taken together, newborn blacktip reef sharks appear physiologically robust to end-of-century pCO₂ levels, but less so than other, previously investigated, tropical carpet sharks. Our results suggest peak fluctuating pCO₂ levels in coral reef lagoons could still physiologically affect newborn reef sharks, but studies assessing the effects of long-term exposure and in combination with other anthropogenic stressors are needed.

Respiratory chambers used to quantified sharks’ oxygen uptake rates (MO₂, in mg O₂ kg⁻¹ h⁻¹) as proxies of metabolic rates (Rummer et al. 2020).