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Sharkbites Saturday

Small but perhaps not so mighty: The second edition of the epaulette shark saga

In the first post of Sharkbites Saturday, I told the story of a little tropical shark that has some wildly unique abilities. To recap, the epaulette shark (Hemiscyllium ocellatum) is a small bottom dwelling species in the shallow pools of the Great Barrier Reef and beyond. However in addition to what some would call its “cute” factor (Figure 1), the epaulette shark has the physiological ability to live without oxygen for hours on end in addition to having a pair of modified pectoral fins it uses to walk. With the combination of these cool evolutionary traits the epaulette shark is seemingly unstoppable. If it doesn’t favor an area, it can simply walk away. However, in my last post I also emphasized that epaulette sharks, like 40% of shark species, lay eggs, which can’t just walk away. Eggs are laid in one spot and stay in place as the embryo gestates for 3-4 months depending on water temperature. Therefore, embryos must be able to tolerant the environment they are deposited in, otherwise they may not survive.

Figure 1. Epaulette sharks have an inherently high “cuteness” factor in the world of sharks (PC: C. Gervais & T. Nay).

With global sea surface temperatures rising from climate change, especially in the tropics where epaulette sharks inhabit, we asked the question, how will these embryos survive the warming? Changes in water temperature in general for fish can cause stress. In terms of metabolism, they have to dedicate more energy to maintaining homeostasis over other important life processes like foraging for food, growth, and reproduction. These can not only cause stress and mortality to individual animals, but impact whole populations, potentially shifting an ecosystem off balance. When thinking about our epaulette shark eggs, thermal stress could cause large issues for the developing embryos because they cannot escape it, so how do they fair? It was hypothesized they may tolerate the heat well, given their amazing tolerances to other environmental stressors. However, we are finding out we may have been really wrong. Isn’t science fun?!

Figure 2. Normal pattern development of a neonate epaulette shark (i.e., defined epaulette spot) reared in ovo (28 °C) at 14 days post-hatch (a)and 120 days post-hatch (c) in contrast to patterns of a neonate reared in ovo at 32 °C at 14 days post-hatch (b) and then transitioned to 28 °C (at 30 days post-hatch) until 120 days post-hatch (d). Figure directly from Johnson et al. 2016.

Thermal stress exhibited very visible effects on epaulette sharks in some preliminary work conducted by my lab cohort in Australia, led by Dr. Jodie Rummer at the ARC Centre of Excellence for Coral Reef Studies based at James Cook University. As seen in Johnson et al. (2016), epaulette shark egg cases were raised in an ambient temperature (28ᵒC/82ᵒF) and an elevated temperature predicted for the end of the century (32ᵒC/90ᵒF), and the results were astounding. In Figure 2A and 2C we see the pup from an egg case raised in current temperatures. Note that the dark black name-sake epaulette spot is well developed right immediately after hatching as well as after 4 months have passed. In comparison, in Figure 2B, we see a pup from an egg raised in an elevated temperature. Notice how the spot is not black, but a brown smudge. Even after being transitioned back to the cooler temperature, the spot does not develop properly (Figure 2D). This visual difference was our first indication that epaulette sharks may not tolerate heat very well. If proper patterns and coloration are not developing, this could have implications for survival, where these markings may help epaulette sharks be disgusted from predators.

Figure 2. (A) A light is directed on the back of the egg case during candling. (B) An epaulette shark embryo attached to its yolk within the egg case (PC: C. Gervais).

Sparked from these preliminary results, within the last month I embarked on a new project to further quantify some of these thermal stress effects seen in Johnson et al. 2016. This work is being conducted at the New England Aquarium with the help of many staff, interns, and volunteers. The idea is to raise epaulette sharks in an ambient temperature that they would currently experience in the wild (27ᵒC/81ᵒF) to temperatures predicted to occur over the next century (29ᵒC/84ᵒF; 31ᵒC/88ᵒF; 33ᵒC/91ᵒF). Throughout the 3-4 month gestation we are collecting various data on growth, development, and physiological performance to better understand the effects of thermal stress. Similar to a chicken, the embryo of an epaulette shark is attached to a yolk that decreases as the embryo consumes it over time. In an act called candling, we can shine a light through the egg case and observe the activities on the inside with harming the embryo (Figure 3). This technique allows us to collect measurements like embryo and yolk sizes, as well as other cool metrics like how often the embryo is beating its tail or ventilating its gills. With these types of measurements taken on eggs raised in various temperatures, we hope to observe differences in growth rates or activity that could suggest the future of these little sharks. For example, it has been observed in other shark species that warmer temperatures can cause eggs to hatch faster, but the emerging pups are smaller in size. These types of changes could cause issues for the newly hatched pup’s abilities to hide from predators or forage for food. Additionally, if temperatures rise above a threshold point, embryos may not even survive to hatching. Results of this nature could mean detrimental impacts to this species in the wild in the future.

In addition to studying growth and development by candling, my research is also studying the oxygen consumption rates of the epaulette shark embryos and pups, we call this physiological performance. This type of data is similar to an athlete being monitored while running on a treadmill. We can understand how much oxygen an organism is using, which can tells us about metabolism, or the sum of all the chemical processes occurring in the body (Figure 4). For example, a fast metabolism requires and burns a lot of energy, where a slow one does not. Warmer temperatures are universally known to increase metabolism in fish, so our results could indicate if an epaulette shark’s body is using more energy for maintenance because of increased temperature.

Overall, the results of my research will allow scientists to have a better understanding of the growth, development, and physiological performance of epaulette sharks into the future. Given the preliminary results from Johnson et al. 2016, we should perhaps already be concerned about these potential temperature related problems. Moreover, if a relatively tolerant species like the epaulette sharks is struggling, what will happen with less tolerant species? To answer this question, my research is not only being conducted on epaulette sharks, but coral cat sharks (Atelomycterus marmoratus) (Figure 4). This species is another egg-laying shark that has similar size and tropical distribution in the wild, but does not have hypoxia tolerance and the ability to walk. Therefore at the end of the project, we will be able to make comparisons no only within one species, but two. This project is currently in the egg case phase, so you will have to stay tuned for more information on the fate of the embryos and pups as well as the outcomes we find! This research is featured along with other cool shark research and facts in the New England Aquarium’s new exhibit The Science of Sharks, check it out this summer!

Figure 4. A coral cat shark hanging out in the New England Aquarium’s new exhibit The Science of Sharks.

Reference:

Gervais C, Mourier J, Rummer JL (2016) Developing in warm water: irregular colouration and patterns of a neonate elasmobranch. Mar Biodiv doi: 10.1007/s12526-015-0429-2.

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