GOMBESSA IV Expedition – Revealing reef shark behaviour as never seen before!

After the success of GOMBESSA II Expedition in 2014 (results published in Current Biology; Mourier et al. 2016) which focused on the role and functioning of grouper spawning aggregations in providing subsidies to maintain an inverted trophic pyramid led by the biggest grey reef shark aggregation, here we come again!!!

The same team (including Laurent Ballesta and colleagues from Andromede Oceanologie) joined by other international researchers (including Yannis Papastamatiou, Charlie Huveneers, Damien Sonny or Eric Parmentier) went back to Fakarava for a new expedition GOMBESSA IV from June to July 2017. This expedition of course will lead to a nice documentary but one of the main aim is to conduct a cutting-edge shark science project! And trust me, all ingredients were involved to produce amazing science and better understand the behaviour of the biggest grey reef shark aggregation in the world!

In June 7th, I arrived in Fakarava with Charlie Huveneers (Flinders University) to help me install an array of Vemco VR2W acoustic receivers in the famous South pass of Fakarava. The idea was to cover the entire channel to better monitor shark movements in the channel. We conducted detection range tests to evaluate at which distance receivers can detect an acoustic tag. Our tests confirmed what I found previously (Mourier et al. 2016) that detection rate clearly dropped from 50 m. So we decided to install receivers 100 m apart. As such, 25 receivers were installed in the pass.

Later, in mid-June, another shark expert Yannis Papastamatiou (Florida International University) joined us to start catching and tagging grey reef sharks. We tested a new capture and tagging technique this year. Indeed, instead of hooking sharks, Laurent and his team was catching sharks underwater, putting them into tonic immobility, attaching a rope around the caudal fin linked to the boat so that we could bring the shark back to us. The shark was then placed into a stretcher alongside the boat to be measured, given a biopsy for isotope analysis and fin clipped for genetic analysis. A transmitter was inserted into its peritoneal cavity and sutured using a surgical stapler. These transmitters not only give the position of the shark within the array of receivers but also important additional data: depth and acceleration! With depth, we will be able to model the 3D movement patterns of sharks in the pass and with accelerometry we will be able to investigate and map activity of sharks and how they monitor energy expenditure especially during hunting phases!

Charlie left us after 2 weeks and Yannis also brang a great gadget to play with: a CatCam which is an animal-borne camera, i.e. a camera we attached to the dorsal fin of a shark and which detached after 2 or 3 days. During the deployment, the logger not only film what the shark see during the day but also record important fine scale behavioural data such as fine accelerometry in the 3 axes. In combination with the acoustic tags, we will better understand how shark hunt and how the manage their energy balance. We succeeded to deploy 4 CatCams and recovered all of them! While some detached earlier than expected, others revealed long-range excursions in open ocean.

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After Yannis left our team on June 1st, I finished the tagging program to reach an impressive total of 38 grey reef sharks which will provide us with great data for a year. At the end of the trip, the team retrieved the receivers to download preliminary data and redeployed them the day after. During a day, I worked on analyzing the data and build a small animation showing all tagged sharks moving simultaneously in the pass (note that I used 32 individuals here because some sharks were tagged at the end of the trip so they did not provide enough data yet).

 

Of course this year, I also conducted several shark count surveys like in 2014 in which I drifted as fast as possible in the school of sharks to count them and avoid them to come back in frame (i.e. avoiding repeated count of same individuals).

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During this expedition, we also used other tools to study sharks. For example, we used the 3 CCTV cameras from the previous expedition to monitor in real-time from our dry office what sharks were doing but also which potential preys are present.

But the year, Damien Sonny (ProFish) brang us a new interesting tool to monitor sharks not only during the day but also at night; a BlueView acoustic camera! It provide images like an echography but have the advantages to provide the same image at night, so ideal to compare the behaviour and activity of sharks and their prey between day and night.

And of course we conducted many night dives in the channel in order to record hours of shark hunting and better understand predator-prey interactions. These drifting dives into >500 sharks were conducted in all hours of the night and will inform us about the periods and locations of maximum hunting activities. Analyzing the slow-motion videos of predation will allow us to identify prey species and in combination with stable isotope analyses will allow us to better understand the trophic position of grey reef sharks in the pass of Fakarava.

 

 

Finally, with Eric Parmentier (University of Liege) we will investigate the sound produced by fishes at night and how it influences their probability of being predated.

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There and Back again: PJs are definitely not boring and travel a lot!

Who would have expected that Port-Jackson sharks can travel long distance when seeing these little guys resting in the bottom of New South Wales in Sydney Harbour or Jervis Bay during winter months?

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The BEEF lab from Macquarie University led by Prof Culum Brown has been studying these little mysterious creatures, endemic of Aussie waters, for years now and have investigated their long-term movement patterns using acoustic telemetry. Every winter the team went to Jervis Bay where PJs are forming large aggregations and caught sharks to implant them an acoustic transmitter. When the tagged shark passes in proximity of a receiver its identity is recorded allowing to follow them in time and space. The movements of these littles guys can then be tracked along a huge Australian network of receivers.

I was fortunate to participate in this project by analysing the data during my post doc at Culum’s lab last year. And the results are available in a Special Issue of Marine and Freshwater Research.

What the team found was surprising and exciting!!!!

These small benthic sharks not only come to NSW every winter but they were tracked as far as Tasmania, swimming >1,000 km after leaving their mating aggregation in Jervis Bay!

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Moreover, they not only conducted long distances but they also came back every single year to exactly the same reef in Jervis Bay after their > 2,000 km travel (round-trip), becoming an astonishing migrating species with strong site fidelity and philopatry!

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In summary, they forage in southern Australia and move to NSW to reproduce in winter, with males arriving earlier than females at the mating aggregation sites.

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All this little sharks are aggregating in great numbers and are socialising for mating. We are now tracking their interactions and investigating their social network. How? Wait for a few more days as we have a paper accepted for publication on this!

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The paper can be found at:

Bass N, Mourier J, Day J, Knott N, Guttridge T, Brown C (2017) Long-term migration patterns and bisexual philopatry in a benthic shark speciesMarine and Freshwater Research 68(8): 1414-1421.

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