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Ecological Impacts of Declining Global Elasmobranch Populations Due to Anthropogenic Influences Amanda Flannery Miami University Oxford, OH April 19, 2017

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Ecological Impacts of Declining Global Elasmobranch Populations Due to Anthropogenic Influences Amanda Flannery Miami University Oxford, OH April 19, 2017 Ecological Impacts of Declining Global Elasmobranch Populations Due to Anthropogenic Influences Amanda Flannery Miami University Oxford, OH April 19, 2017 Abstract In the past century, marine ecosystems worldwide have seen sharp declines in elasmobranch populations. Recent assessments by the International Union for Conservation of Nature (IUCN) revealed nearly 25% of elasmobranchs are vulnerable to extinction. They exhibit k-species characteristics which leave them highly susceptible to anthropogenic influences. Human influences, such as habitat degradation or loss, climate change, as well as fishing and finning, are the most likely causes of the steep population declines in elasmobranchs over the past century. Physical destruction of habitats leaves juveniles vulnerable to predation and starvation from low prey availability. Due to elasmobranchs’ slower life history characteristics they are the most vulnerable to climate change effects, especially those residing in estuarine and reef habitats. With prices for shark fins increasing to nearly US$400 per kilogram on the Hong Kong market and increased demand from the Asian markets, sharks are ​ harvested for their fins alone. It is estimated that if fishing mortality rates increase to 20% of the initial population per year, some species could decline to 1% of their population in the next 10 to 39 years. There have been documented cases of trophic cascades and meso-predator release as marine ecosystems have seen sharp declines in large bodied elasmobranch populations. Keywords: elasmobranchii, elasmobranchs, ecology, conservation, population decline, ​ ​ sharks, rays, climate change, habitat destruction, fishing, finning, apex predator, meso-predator, trophic cascade Introduction Elasmobranchii is a subclass of Chondrichtyes, or cartilaginous fishes, which include sharks, skates, and rays that debuted in the fossil record in the Devonian era nearly 400 million years ago (Fowler et al., 2005). In their evolutionary past, elasmobranchs have faced fived mass extinctions (Parker, 2008), however, recent assessments by the International Union for Conservation of Nature (IUCN) revealed nearly 25% of elasmobranchs are vulnerable to extinction (Magiera, 2014). Unlike bony fishes, which exhibit r-species characteristics, reaching sexual maturity quickly and have a high rate of reproduction or fecundity, sharks and rays exhibit k-species characteristics which can make them susceptible to changes in their environment (Fowler et al., 2005). They have long life spans with slow growth rates, reaching sexual maturity late in life, and usually have low fecundity (Chin, Kyne, Walker, & McAuley, 2010), which leave them highly susceptible to anthropogenic influences. Human influences, such as habitat degradation or loss, climate change, as well as fishing and finning, are the most likely causes of the steep population declines in elasmobranchs over the past century (Knip, Heupel, & Simpfendorfer, 2010; Ward-Paige et al., 2010). Dramatic population declines in elasmobranchs can have devastating effects on marine ecosystems (Baum & Worm, 2009; Heupel, Knip, Simpfendorfer, & Dulvy, 2014; Mumby et al., 2007). Habitat Degradation or Loss In 2010, it was estimated that 60% of the global population lived within 100 km of a coastline. By 2020 it’s estimated that number will increase to nearly 75% (Knip et al., 2010). As one may imagine, the increase in population comes with a price for the environment. The acts of dredging, construction, and deforestation, which go hand in hand with increased coastal development, are detrimental to nearshore areas (Knip et al., 2010). While it is adult sharks who have been exploited in the fisheries markets, juveniles of some shark species are at the greatest risk for habitat loss due to the encroachment of humans through coastal development (Heupel et al., 2007). For many species, mangroves provide nearshore nursery habitats for juvenile sharks, offering safety from predation and an abundant food supply (Knip et al., 2010) (Appendix Figure 1). In the last 25 years, mangrove habitats worldwide have decreased by nearly 35% due to clearing, cutting for development, and lumber (Valiela, Bowen, & York, 2001). Around Bimini island in the Bahamas, juvenile lemon sharks (Negaprion brevirostris) (Appendix ​ ​ Figure 2) utilize mangroves to hone their hunting skills and to evade predators (Jennings, Gruber, Franks, Kessel, & Robertson, 2008). However, these mangroves have been threatened by recent resort development. A study of the region saw a direct correlation between the decrease of seagrass (Thalassia testudinum) and the decrease ​ ​ in survival rates of lemon shark juveniles (Jennings et al., 2008). Not only does coastal development lead to direct removal of habitat space, but it also leads to increased terrestrial runoff. When terrestrial runoff in an area introduces an excessive amount of nutrient richness there is an increased risk of algae blooms which can smother other organisms by reducing the available oxygen levels. These eutrophication events cause dead zones in aquatic environments (Knip et al., 2010). Many species of elasmobranchs have been leaving regions during periods of anoxia, like leopard sharks (Triakis semifasciata) (Appendix Figure 3) (Carlisle & Starr, 2009). ​ ​ Terrestrial runoff can also cause health problems in other ways for elasmobranchs. Organochlorines, a pesticide containing chlorinated hydrocarbons used generously in the 1940’s through ‘60’s for mosquito control and agriculture, has been shown to cause infertility in bonnethead sharks (Sphyma tiburo) (Appendix Figure 4) in coastal waters ​ ​ (Delaware Health and Social Services, 2010; Gelsleichter et al., 2005). Not all species of elasmobranchs are coastal. Many, like whitetip reef sharks (Triaenodon obesus), spotted eagle rays (Aetobatus narinari), bluespotted stingrays ​ ​ ​ ​ ​ (Taeniura lymma), yellow stingrays (Urobatis jamaicensis), nurse sharks ​ ​ ​ ​ ​ (Ginglymostoma cirratum), epaulette sharks (Hemiscyllium ocellatum) (Appendix Figure ​ ​ ​ ​ ​ 5), and many others all inhabit coral reefs which are mostly found between 23.4°N and 23.4°S of the Equator between the Tropics of Cancer and Capricorn (Appendix Figure 6). While corals represent only 0.1% of the sea floor, corals are estimated to sustain 25% of life in the ocean (Riegl, Purkis, Al-Cibahy, Abdel-Moati, & Hoegh-Guldberg, 2011). As the global climate continues to rise each year, the ocean temperatures also rise and coral bleaching epidemics have spread across many areas (Riegl et al., 2011)., Available habitats for reef species dwindles as degradation of coral habitats continues (Chin et al., 2010). Elasmobranch reef species are often highly mobile, sometimes traveling hundreds, or even thousands, of miles every year to find food and mates (Hammerschlag, Gallagher, & Lazarre, 2011; Wilson, Polovina, Stewart, & Meekan, 2006; Wilson, Taylor, & Pearce, 2001). This can often require a network of reef habitats to be available to them to make these journeys each year. As coral patches continue to die off, fewer networks become available for these migratory animals and they are forced to find new networks of reefs to make these journeys possible (Duncan & Holland, 2006; Robbins, Hisano, Connolly, & Choat, 2006). For some species of reef shark, even if new suitable coral habitats can be reached, it may be possible that they will be unable to establish a stable population due to competition or predation events (Duncan & Holland, 2006). Climate Change It has been estimated that by 2050, with minimal climate-warming changes, approximately 18% of terrestrial species will be committed to extinction due to rapid global temperature increases (Thomas et al., 2004). Species that express r-strategy life histories are generally able to respond and adapt the quickest to climate change (Perry, Low, Ellis, & Reynolds, 2005). However, k-strategy species, like elasmobranchs, are more vulnerable to climate change effects (Perry et al., 2005). Climate change has been known to effect sharks and rays in two distinct ways: as direct effects and indirect effects (Chin et al., 2010). Direct effects influence the physiochemical environment which a shark or ray inhabits. These effects can include water temperature changes, freshwater input from streams or rain fall, and ocean acidification (Chin et al., 2010). Indirect effects influence the geophysical, ecological, and biological processes occurring within the habitats, as well as the health of the environment. Indirect effects can also include air temperature, ultraviolet radiation, ocean circulation, and severe weather events (Chin et al., 2010). Both direct and indirect effects can have significant impacts on elasmobranch populations. It has been suggested that round stingrays (Urobatis halleri) (Appendix Figure 7) and leopard ​ ​ sharks (Triakis semifasciata) (Appendix Figure 3) use behavioral thermoregulation, ​ ​ aggregating in warmer waters to optimize their physiological and metabolic processes including reproduction (Hight & Lowe, 2007; Hoisington IV & Lowe, 2005). If conditions are not met for these animals they will not be able to meet their physiological requirements necessary for reproduction which could have a detrimental impact on their populations (Hight & Lowe, 2007). In a recent study of elasmobranchs in six ecological habitats along Australia’s Great Barrier Reef (Appendix Figure 8), ocean circulation changes, temperature, and freshwater input were the greatest influential factors due to
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