Sharks show flexibility in trophic interactions in response to competition

Coral reef ecosystems are increasingly threatened by global changes, especially the shorelines where most of human activities are concentrated. These areas serve as nursery areas for several species of sharks and are important in maintaining populations. But how does competition in these restricted areas influence foraging ecology of sharks?

A study in collaboration between Centre de Recherches Insulaires et Observatoire de Environnement (CRIOBE USR3278, PSL Research University: EPHE – CNRS – UPVD) and Florida International University, published in Marine Environmental Research investigated how sharing nursery areas between species influences trophic interactions in juvenile sharks.

We therefore investigated this question using a long-term monitoring program on juvenile sicklefin lemon sharks (Negaprion acutidens) and blacktip reef sharks (Carcharhinus melanopterus) led by CRIOBE over the past 10 years on Moorea Island (French Polynesia) 1, 2. Moorea represents a useful experimental ground to test the influence of competition in juvenile sharks because this island has numerous nurseries sheltering either only one or both of the two species of sharks. In examining stable isotope values of carbon and azote in juvenile sharks, we demonstrated that sharing a nursery with another species led the species to trophic niche partitioning. While they feed on a similar trophic level when they are alone in a nursery, lemon sharks appear to feed on prey with higher trophic level than blacktip reef sharks when they share the same nursery. This partitioning allows the co-existence of both predator species during the first life stages. This plasticity show the capacity of sharks to adapt to competition and more broadly to their environment.

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The paper can be found at :

Matich J, Kiska JJ, Mourier J, Planes S & Heithaus MR (2017) Species co-occurrence affects the trophic interactions of two juvenile reef shark species in tropical lagoon nurseries in Moorea (French Polynesia). Marine Environmental Research 127: 84-91.


Previous papers from juvenile shark monitoring in nurseries of Moorea:
  1. Mourier J, Buray N, Schultz JK, Clua E, Planes S (2013) Genetic network and breeding patterns of a sicklefin lemon shark (Negaprion acutidens) population in the Society Islands, French PolynesiaPLoS ONE8(8): e73899.
  2. Mourier J., Planes S (2013) Direct genetic evidence for reproductive philopatry and associated fine-scale migrations in female blacktip reef sharks (Carcharhinus melanopterus) in French PolynesiaMolecular Ecology22 (1): 201-214.

Smart Sharks Have Robust Social Networks

The role that an individual shark plays within its social network not only serves to maintain cohesion within the population, but it can enhance the network’s resilience to environmental and anthropogenic disturbances. Researchers from Centre de Recherche Insulaire et Observatoire de l’Environnement (CRIOBE USR3278, PSL Research University: EPHE – CNRS – UPVD) recently published a study in the journal Biology Letters that examined the social network of a population of blacktip reef sharks (Carcharhinus melanopterus) in French Polynesia (Figure 1). With support from a researcher at Macquarie University in Australia, the team demonstrated that the interactions between sharks within the social network made the network robust to shark removal. This study also suggested that sharks were able to quickly learn from capture questioning the use of capture-recapture model frameworks for these species.

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Figure 1: Blacktip reef sharks networking in the lagoon of Moorea (Photo credit: Lauric Thiault)

In a previous study published in the journal Animal Behaviour (Mourier et al. 2012), the team discovered that blacktip reef sharks could form preferred associations in the wild. ‘Sharks have social networks too! Even though their social structure is not as complex as that of most mammals, sharks can display an affinity for one another’ explains Dr. Johann Mourier, the principal investigator of the study.

To study the social network of sharks, Mourier used the patterns found on the dorsal fins (Figure 2) – which are unique to the individual and can be likened to fingerprints in humans – to identify each individual shark. Such patterns allow researchers to track individuals in space and through time.

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Figure 2: The patterns on a shark’s dorsal fin are likened to a human’s fingerprint, and allow researchers to track individual sharks in space and time.

‘Through a global analysis of sharks present together, we were able to build their social network using social science-based methods’, explains Mourier. ‘Capture-release-recapture surveys were simultaneously conducted after each dive to calculate individual probabilities of being captured’.

Investigating the blacktip reef shark’s social network has revealed that not all individuals are equal in terms of maintaining the connectivity between social clusters. Researchers ran simulations, where individual sharks were removed from the network, and what they found was that up to 50% of the population could be removed before the entire network collapsed. In addition to this surprising result, Mourier also noticed that the sharks he had already caught were now nearly impossible to catch as they were avoiding his fishing gear. ‘A shark’s ability to learn from previous negative experiences results in a network that is more robust to removal from fishing.

Finally, results from this study highlight that extreme care must be taken before applying capture-release-recapture models for shark population studies because individual sharks do not have equal probability of being caught.

This original work highlights the complexity of relationships between individuals in the wild and has implications for shark conservation, where it is now imperative that we consider the relative contribution of an individual to the overall resilience of the population.

REFERENCE
Mourier, J., Brown, C. and S. Planes. 2017. Learning and robustness to catch-and-release fishing in a shark social network. Biol. Lett. 2017 13 20160824; DOI: 10.1098/rsbl.2016.0824. Published 15 March 2017

CONTACT
Johann MOURIER (Perpignan, France)

When a massive reef shark aggregation relies on delivery

Our work was recently published in the journal Current Biology and even made the cover of the journal.CURBIO_26_15.c1.indd

Mourier J, Maynard J,  Parravicini V, Ballesta L, Clua E, Domeier ML, Planes S (2016) Extreme Inverted Trophic Pyramid of Reef Sharks Supported by Spawning GroupersCurrent Biology 26(15): 2011-2016

It is becoming increasingly difficult to understand what a coral reef ecosystem should look like in areas characterized by low human influence, simply because these areas are becoming increasingly rare. Most of the ocean reefs are facing increasing anthropogenic pressure, especially overfishing and habitat degradation. Therefore, our view of the ocean is often not accurate as we get used to overexploited ecosystems in which the top of the food web has been extirpated. Scientists therefore need to use bait or increase hours of observations to sight any large predator. However, rare healthy reefs still exist and may help us to better understand coral reef ecosystem functioning in health conditions, which is critical to help global conservation management of coral reefs.

In this paper we first quantify the abundance and density of an aggregation of reef sharks in the pass of Fakarava, an atoll of the Tuamotu archipelago in French Polynesia. French Polynesia host healthy populations of sharks as they have never been targeted by local human population and have been protected by law under fishing bans since 2006 within which is one of the largest worldwide shark sanctuary! Our work allowed to estimate the population size of this aggregation to reach up to 900 reef sharks (700 grey reef sharks) in a tiny and narrow channel (density 2-3 times what have been found in other health reefs), making for the moment the largest aggregation of reef sharks ever documented.

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Figure above: Up to 700 grey reef sharks live in the pass of Fakarava, a narrow channel in French Polynesia

We therefore questioned how such a high biomass of predator can survive in such a restricted area.

One of the first question was to determine if there were enough fish in the pass to feed such a number of sharks… and the response was obviously NO!

The second question was therefore to understand if these sharks are resident or if it happens that they feed outside the pass. Using acoustic telemetry, we found that sharks were more present and abundant during the winter months while they were roaming in and out of the pass during summer. So how during these winter months this massive number of sharks can be supplied if they don’t search for food outside the pass?

During June and July, camouflage groupers form dense spawning aggregations in the pass as well as less other fish species. Although relatively ephemeral, these spawning aggregations represent a large amount of biomass into the pass. Indeed, this grouper aggregation accounted for more than 17,000 fishes representing about 30 tonnes of potential food, freely brought to the sharks. Sharks use these inputs as trophic subsidies and do not need to conduct costly foraging excursion outside the pass.

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Figure above: Fish spawning aggregations represent important subsidies for sharks.

While they are generally resting in the strong current during the day, our underwater nocturnal observations showed that they were actively hunting in the pass at night, targeting at least 14 species of fish including groupers.

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Figure above: Sharks are hunting at night on spawning grouper as well as up to 13 other fish species.

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Figure above: Nocturnal hunting of grey reef sharks in Fakarava

Generally, typical ecosystem should be represented as a classic pyramid with broad base of primary producer and decreasing biomass as higher trophic levels are being reached. Biological energy flow is lost when predator consume their prey and therefore there is a requirement for more prey than predators. In the pass of Fakarava, the huge abundance of resident reef sharks and lower relative abundance of prey makes the trophic pyramid inverted; a paradox in which predators outnumber their prey which is not supported by the physical laws of thermodynamics.

Our research provides an empiric example demonstrating that inverted trophic pyramids, where predators outnumber their prey, is only possible at local scales if predators find a way of optimizing the exploitation of both spatial and temporal subsidies.

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Figure above: Sharks exploit both spatial (in summer) and temporal (in winter) subsidies.

Finally, our study revealed important considerations for coral reef conservation. Indeed, protection of vulnerable spawning aggregation is important, not only for the fish themselves but also for predators that depend on them for trophic subsidies.

You can also watch our Video Abstract to better understand our findings.

you can also watch our documentary “The Grouper Mystery” that was produced during our scientific project.

Read also Colin Simpfendorfer and Michelle Heupel dispatch related to our study here.

Increase in sea temperature can affect development of coloration in a benthic shark

Here are some interesting but bad news findings about the impact of climate change on the development of young sharks from an experiment conducted by Connor Gervais at the Rummer Lab:

“Small benthic shark may not develop their coloration patterns under predicted end-of-centery temperature (32°C)”

Epaulette sharks (Hemiscyllium ocellatum) are small (70–90 cm), oviparous long-tailed carpet sharks commonly found on reef flats from Papua New Guinea to Australia. Sharks reared at annual summer average temperatures (~28 °C; 24.114° S, 152.717° E) develop distinct colouration and patterning in ovo (n=16). Upon hatching (n = 11), their namesake epaulettes are clearly defined (Fig. 1a). But sharks hatching from eggs reared at predicted end-of-century temperatures (32 °C) displayed irregular colouration and patterning (Fig. 1b). All except for one 32 °C hatchling died after 3 days, and none had developed the distinct epaulette observed in control sharks. The surviving hatchling was maintained
at 32 °C for 30 days post-hatch and then slowly transitioned to control temperatures (28 °C). Even after 120 days post-hatch, the neonate’s patterns were still not properly developed (Fig. 1d).

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The left panels are current day temperatures, and the right panels are sharks that developed under temperatures predicted to occur on the Great Barrier Reef Marine Park by 2100.

These patterns are important for the ecology and survival of these small benthic sharks. Inded it can further affect their camouflage ability to hide from predators or alternatively impact their social behaviour. Further research is needed but this is certainly a bad news for this species for which it was found good abilities to deal with increasing CO2 (see published paper here).

Paper:

Gervais C, Mourier J, Rummer J (in press) Developing in warm water: Irregular colouration and patterns of a neonate elasmobranch. Marine Biodiversity. Link to PDF

 

Sharks have increadible healing abilities

Following a nice collaboration with Andrew Chin and Jodie Rummer from James Cook University (Australia), we recently published an article documenting a range of diverse wounds and injuries on the blacktip reef shark (Carcharhinus melanopterus) and demonstrating how quickly sharks were able to heal and recover from these injuries. This healing ability has different implications and application to understanding of shark’s ecology.

We first documented the rapid healing of this species following an internal tagging procedure involving a small incision in the belly of the shark to implant the transmitter. This not only shows that sharks are healing quickly but also that they are robust to this tagging procedure which is important to know as a scientist when you work with free-living animal.

 

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The same kinds of incisions/open-wounds are present in neonate sharks from viviparous species such as the blacktip reef shark. Just after birth, an open umbilical scar is visible but it quickly close and heals. It is then important to assess the speed of healing in ecology as it can inform the approximate date of birth when the juvenile is caught in its nursery. Small umbilical wounds in neonates decreased in surface area by 71% in less than a week and were barely detectable after 24 days.

 

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The same rate of healing is helpful when females are bitten by males during mating. Indeed, as it is really rare to observe shark copulation, we can indirectly infer when mating occurred using the fresh bite wounds on female’s body. Inferring the speed of healing of these wounds can therefore tell us exactly when mating occurred.

 

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Blacktip reef sharks can also have other sources of injuries. For example, larger sharks or other conspecifics can bite them during agonistic/dominance behaviour or predation attempt by larger predators, and healing quickly is therefore important.

 

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Anthropogenic activities can injure sharks (e.g. boat propellers). We report here an unbelievable healing case of a shark surviving a serious deep wound that might have been inflicted by a boat propeller in Moorea lagoon. I less than a month the wound closed completely.

 

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Finally, we reported two cases of survival after fin removal due to targeted shark-finning in which the basal wound of fin removal healed well and the sharks were observed alive a while after injury, swimming without their dorsal fin. However, even if they survive for un unknown time, the removal of the dorsal fin may greatly affect their daily life and in turn their fitness (and most of finned sharks may not survive).

 

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In summary, this study suggests that elasmobranchs may be resilient to injuries, showing rapid healing from minor wounds and long-term survival from even major mechanical injuries. These are positive findings for elasmobranch conservation, especially considering that up to a quarter of all shark and ray species worldwide are threatened with extinction. Despite this incredible ability, we encourage minimal handling time and stress when releasing sharks after fishing or by-catch, which could include cutting a line near the hook instead of repeatedly attempting to remove the hook. Anglers should also be made aware that sharks can recover from mechanical injury; therefore, sharks should be released even if the animal sustains injuries during the capture process.

 

The paper is Open Access and available at:

Chin A, Mourier J, Rummer J (2015) Blacktip reef sharks (Carcharhinus melanopterus) show high capacity for wound healing and recovery following injury. Conservation Physiology 3(1): cov062

What is known about effects of provisoning on sharks and ray and how future research should investigate different scales?

We recently published a paper that review the research that has been conducted so far on the effect of shark and ray provisioning on the animal’s ecology, behaviour and health.

Shark and ray provisioning is a rapidely growing indstry that offers tourist with an increased probability of interaction with elusive animals buy attracting them with food or even feeding them to habituate them to visit the diving site. This activity is widespread around the world and involve different species.

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We reviewed the 22 available studies on this topic involving 14 shark and 3 ray species targeted by artificial provisioning to investigate their behavioral, physiological, and ecological response.

We first report similar individual response by sharks and rays, including change in horizontal movements or emergence of an anticipatory response. However, all studies demonstrate that the propensity to respond to provisioning operations varies both among elasmobranch species and among individuals within each species. The effect on diet and foraging behaviour is yet to be better investigated as this topic has been understudied so far; the 2 availaible studies showing contrasting patterns that might be due by different provisioning practices.

We also investigated the potential effects at the group scale. We report a number of studies showing an aggregation effect with an increased abundance of the targeted species at the feeding site. Provisioning operations can influence group composition in terms of species and genders that are aggregated. It can aggregate naturally gregarious species but also solitary species creating an artificial interacting zone. However, most studies indicate that there is unlikely an effect on the natural cycle of the species involved, as for example, most species appear to keep conducting their breeding migrations despite the possibility to stay at the provisioning site. On the other hand, aggregation at a specific site can promote intra-specific aggression or competition.

We also reported the community-scale effects, including the effects of distribution of predators and prey or chnaging elasmobranch communities at the feeding site.

Although the effect on elasmobranch health has been yet underinvestigated, we discuss the potential effects that may impact animal’s health and body condition.

While a growing number of ecologists is investigating the potential effects of provisioning on sharks and rays, we took the opportunity to suggest a framework that take into account multi-scales when studying this topic. Until now, most of the studies have only been context dependent and focused on only one or two effects (e.g., effects on abundance or on movement patterns), but we highlight teh fact that scientists should now intergrate multiple effects and their interactions within their study. Indeed, most individual, group and community effects are not isolated and actively interact. A broader framework could therefore study the cascading affects accross the scales.

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Such a framework could benefit our understanding of the real effects and their strenght and importance on shark and rays health and behaviour.

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While the review was based on the potential effects of provisioning on sharks and rays, we also show that it is context dependent and not necessarily negative. This activity can have positive effect for conservation and awareness, or even null effects on some aspects. The strenght of negative effects is often related to the practices of the industry. If some operations are already conscious on the benefit of good practices to secure the durability of their activity and the health of populations of the species they target (http://globalsharkdiving.org/ , http://sustainablesharkdiving.com/), others only think about short-term financial benefit of the practice and do not adapt their practices to good code of conduct which is likely to negatively impact the industry.

Note also that the reported negative effects are nothing compared to other threats that sharks are facing every day (e.g. overfishing, habitat degradation, climate change…).

We hope our review will provide a good summary of the different effects that have already been studied in sharks and rays but also that it will encourage future researcher to use a broader framework to investigate the response of these marine animals to provisioning.

Our study is available here:

Brena PF, Mourier J, Planes S, Clua E (2015) Shark and ray provisioning : functional insights into behavioral, ecological and physiological responses across multiple scales. Marine Ecology Progress Series 538: 273-283.PDF icon