INTRODUCTION
The term ‘trophic cascade’ was first introduced by Paine in 1980, following his experimentation with sea stars (Pisaster spp) and their role in shaping intertidal communities (Paine, 1969). In pelagic marine systems, the effects of apex predators on lower trophic levels have been studied with much dispute and difficulty. This has been partly due to other oceanographic factors, such as currents and changes in ocean temperature due to global warming, showing correlations with population changes which can’t be ruled out (Steneck, 2012; Möllmann et al., 2008; Kirby et al., 2009). As well as this, overfishing has reduced populations of apex predatory species such as Atlantic cod and Bluefin Tuna to the FAO’s lowest category of fish stocks, “depleted” (FAO, 2011). Sharks (Subclass Elasmobranchii, Subdivision Selachii) (Helfman & Burgess, 2014) are iconic apex predators in many pelagic systems and can demonstrate how overexploitation and a lack of it’s sufficient recording, has complicated our understanding of the impacts fishing activity has on their top-down effects.
While most commercial fisheries do not intend on catching sharks for consumer purposes, they are commonly involved in fisheries bycatch, that is unintentional catch of non-target species that is either unused or unmanaged (Davies et al., 2009). A variety of gear types used by fisheries have resulted in shark bycatch, with pelagic longline, gillnets and trawls being the most significant (Oliver et al., 2015). In some cases, shark catches may still be commercially valuable e.g. longline fisheries in the North Atlantic have had a history with commercialising porbeagle sharks (Lamna nasus) (Helfman & Burgess, 2014) since the 1960s (Lewison et al., 2004; Helfman & Burgess, 2014) and the fin trade in parts of Asia has been found to acquire shark biomass almost four times higher than that shown in fishery shark catch figures globally (Clarke et al., 2006). There is a general census that shark populations have declined due to fishing activities (Bonfil, 1994; Burgess et al., 2005), but the extent of the declines is largely uncertain due to the lack of reliable and accurate long-term reporting from fisheries in regard to stocks and bycatch (Clarke et al., 2006; Ferietti et al., 2010; Jordan et al., 2013; Campana, 2016). Similarly, there is a general census that removal of marine apex predators has far reaching effects in whole ecosystems (Parsons, 1992; Jackson et al., 2001; Steneck, 2012), but the evidence of specific trophic events, particularly with shark species, is variable.
HAS OVERFISHING OF SHARK POPULATIONS CAUSED TROPHIC CASCADES?
There is a series of studies which may suggest a three-level trophic cascade of behavioural interactions between tiger Sharks (Galeocerdo cuvier), green sea turtles (Chelonia mudas) and seagrasses (Heithaus et al., 2014), particularly in Shark Bay, Western Australia (Heithaus et al., 2012). Early studies found that tiger sharks had a preference for shallower habitats in seagrass ecosystems and that this correlated with the abundance of their prey species such as dugongs, sea snakes, sea birds and sea turtles (Heithaus et al., 2002; Heithaus et al., 2006). Soon after, it was found that green sea turtle habitat uses also responded to variations in food quality and predation risk by tiger sharks (Heithaus et al., 2007). These findings are consistent with key features of simple three-level trophic cascades, where the tiger sharks behaviour at the top level is dependent on the green sea turtle as it’s prey, and the green sea turtles behaviour in the middle level is regulated by a bidirectional regulation from both its shark predator (top-down) and it’s own seagrass food resource (bottom-up) (Terborgh & Estes, 2010). Patterns involving declines of tiger sharks due to overfishing and extensive grazing of seagrasses by sea turtles might be occurring in other areas such as Bermuda (Baum, 2003; Fourqurean et al., 2010) and Indonesia (Ferretti et al., 2010; Lal et al., 2010), suggesting that overfishing of tiger sharks may be detrimental to the functioning seagrass systems (Heithaus et al., 2014). However, the extent of the trophic interactions in areas where tiger sharks are overfished is not as well studied as in Shark Bay. This could be attributed to the fact that Shark Bay has suffered little to no anthropogenic impact and relative populations of the tiger shark and green turtle have remained abundant and intact, allowing the system to function as normal (Heithaus et al., 2012). This would highlight how exploitation and removal of apex predators from ecosystems can make understanding the trophic interactions more difficult in the first place (Steneck et al., 2012). Furthermore, such exploitation has led to disagreements on the extent of shark declines and the cascading effects it has.
A case where this is evident is a highly cited and controversial paper by Myer’s et al. (2003) which suggested that a trophic cascade occurred most conspicuously between a decline in great sharks (Carcharodon carcharias) (argued as a result of fishing activity), an increase in cownose rays (Rhinoptera bonasus) and a decline in various species of bivalves. Limitations of the source of data here (research surveys and fisheries data) were highlighted in a paper published by the FAO, which mostly disagreed with a specific source used by Myer’s et al. (2003). It noted that Baum et al. (2003) only used logbook data based on longline surveys, which do not adequality sample all shark species, and that the extent of shark declines suggested here was over estimated, having been based on inadequate sample size and incomplete analysis (Burgess et al., 2005). More recently, a re-examination of the relevant data indeed revealed that changes in populations of the three trophic levels did not coincide and were not consistent with the trophic cascade (Grubbs et al., 2016). The major issue highlighted here is discrepancies with the data regarding the trends in shark populations and the extent in which they are being affected by the fishing activities described previously. Both under/over reporting and misidentification of shark species occurs in commercial fisheries logbooks (Burgess et al., 2005) resulting in only 15% of shark catches being recorded to species level (Clarke et al., 2006). Statistics provided by the FAO show that the number of global shark catches reported to them had tripled between 1950 and 1999, but again, misidentification and lack of sufficient recording is mentioned as a limitation of the data (Vannuccini, 1999). Therefore, even the most exhaustive data sources still vary in their reliability. Furthermore, the long-term decline in shark populations is hard to gage since historically, shark catches were not regularly recorded (Ferrietti et al., 2010). This makes understanding the effect of overfishing of sharks on the trophic relationships in their wider ecosystems very hard as there is little data on their function while populations are intact to compare to (Steneck, 2012).
Some of the setbacks discussed have emerged in the proposed cascade involving overfished tiger sharks in seagrass ecosystems where Heithaus et al., 2012 also used the same unreliable sources of data, e.g. Baum et al. (2003), in their discussions on areas like Bermuda. Additionally, it may also be argued that findings at Shark Bay alone are also not entirely conclusive of a trophic cascade between the proposed species. For example, where shark habitat preference correlated with abundance of prey species, stronger correlations were found for abundances of dugongs and sea snakes while those of sea turtles were much more variable (Heithaus et al., 2002). The impact that dugong grazing has on seagrass systems may be just as substantial as that of green turtles in bays of Australiia (Jackson et al., 2001) as their large herds graze in the same location for months, reducing seagrass biomass by 95% (Preen, 1995). Over exploitation of dugongs for their flesh and oil occurred in the early 20th century (Jackson et al., 2001) and though dugong catches in modern commercial fisheries is virtually unheard of, areas of Cambodia and Vietnam report that dugongs are highly profitable and hunted for their body parts or caught as bycatch and sold on (Hines et al., 2008). The evidence here might suggest that research into a trophic cascade between sharks, dugongs and seagrass, with a consideration for the exploitation of both sharks and dugongs, might be just as important as that which involves turtles. Furthermore, in seagrass systems where tiger shark populations are thought to have declined, such as Bermuda (Baum et al., 2003), and sea turtle foraging activity is severe (Fourqurean et al., 2010), no systematic study has specifically looked at the relationship of population changes between the three trophic levels and how overfishing of sharks here has effected the system as whole.
CONCLUSION
Shark Bay is a promising area for studies to understand marine trophic structures and how these might be meditated by apex predators. However, the pristine quality of Shark Bay also means that it is limited in providing evidence of how overfishing of top trophic level species might be having cascading effects. In areas where overfishing of tiger sharks is known to occur, the extent of exploitation is hard to gage based on restricted data from sources such as fishery stock reporting’s .Holistic studies are necessary to test the relationships between populations at different trophic levels and this should be done with a wide range of species at the middle level in the seagrass ecosystems. Overall, there is evidence of patterns occurring where overfishing of sharks as apex predators may be correlating to changes in lower trophic levels and these need to be investigated in order to understand the true extent that fishing activity has on trophic systems.
REFERENCES
Baum, J., Myers, R., Kehler, D., Worm, B., Harley, S. and Doherty, P., 2003. Collapse and Conservation of Shark Populations in the Northwest Atlantic. Science, 299(5605), pp. 389-392. https://doi.org/10.1126/science.1079777.
Bonfil, R. ,1994. Overview of world elasmobranch fisheries. FAO Fisheries Technical Paper, 341, 119 pp.
Burgess, G., Beerkircher, L., Cailliet, G., Carlson, J., Cortés, E., Goldman, K., Grubbs, R., Musick, J., Musyl, M. and Simpfendorfer, C., 2005. Is the collapse of shark populations in the Northwest Atlantic Ocean and Gulf of Mexico real? Fisheries, 30(10), pp. 19-26. https://doi.org/10.1577/1548-8446(2005)30[19:ITCOSP]2.0.CO;2.
Campana, S., 2016. Transboundary movements, unmonitored fishing mortality, and ineffective international fisheries management pose risks for pelagic sharks in the Northwest Atlantic. Canadian Journal of Fisheries and Aquatic Sciences, 73(10), pp. 1599-1607. https://doi.org/10.1139/cjfas-2015-0502.
Clarke, S., McAllistair, M., Milner-Gulland, E., Kirkwood, G., Michielsens, C., Agnew, D., Pikitch, E., Nakano, H and Shivji, M., 2006. Global estimates of shark catches using trade records from commercial markets. Ecology Letters, 9(10), pp. 1115-1126. https://doi.org/10.1111/j.1461-0248.2006.00968.x.
Davies, R., Cripps, S., Nickson, A. and Porter, G., 2009. Defining and estimating global marine fisheries bycatch. Marine Policy, 33(4), pp. 661-672. https://doi.org/10.1016/j.marpol.2009.01.003.
(FAO) United Nations Food and Agricultural Union, 2011. Review of the state of world marine Fishery resources. FAO Fisheries and Aquaculture Technical Paper, 569. Rome: FAO. 334 pp.
Ferretti, F., Worm, B., Britten, G., Heithaus, M. and Lotze, H., 2010. Patterns and ecosystem consequences of shark declines in the ocean. Ecology Letters, 13(8), pp. 1055-1071. https://doi.org/j.1461-0248.2010.01489.x.
Fourqurean, J., Manuel, S., Coates, K., Kenworthy, W. and Smith, S., 2010. Effects of excluding sea turtle herbivores from a seagrass bed: overgrazing may have led to loss of seagrass meadows in Bermuda. Marine Ecology Progress Series, 419, pp. 223–232. https://doi.org/10.3354/meps08853.
Grubbs, R., Carlson, J., Romine, J., Curtis, T., McElroy, W., McCandless, C., Cotton, C. and Musick, J., 2016. Critical assessment and ramifications of a purported marine trophic cascade. Scientific Reports (Nature Publisher Group), 6(1). https://doi.org/10.1038/srep20970.
Hall, M., 1996. On bycatches. Reviews in Fish Biology and Fisheries, 6, pp. 319-352. https://doi.org/10.1007/BF00122585.
Heithaus, M., Alcoverro, T., Arthur, R., Burkholder, D., Coates, K., Christianen, M., Kelkar, N., Manuel, S., Wirsing, A., Kenworthy, W., et al., 2014. Seagrasses in the age of sea turtle conservation and shark overfishing. Frontiers in Marine Science, 1. https://doi.org/10.3389/fmars.2014.00028.
Heithaus, M., Dill, L., Marshall, G. and Buhleier, D., 2012. Habitat use and foraging behavior of tiger sharks (Galeocerdo cuvier) in a seagrass ecosystem. Marine Biology, 140(2), pp. 237-248. https://doi.org/10.1007/s00227-001-0711-7.
Heithaus, M., Frid, A., Wirsing, A., Dill, L., Fourqurean, J., Burkholder, D., Thomson, J and Bejder, L., 2007. State‐dependent risk‐taking by green sea turtles mediates top‐down effects of tiger shark intimidation in a marine ecosystem. Journal of Animal Ecology, 76(5), pp. 837-844. https://doi.org/10.1111/j.1365-2656.2007.01260.x.
Heithaus, M., Hamilton, I., Wirsing, A. and Dill, L., 2006. Validation of a randomization procedure to assess animal habitat preferences: microhabitat use of tiger sharks in a seagrass ecosystem. Journal of Animal Ecology, 75(3), pp.666-676. https://doi.org/10.1111/j.1365-2656.2006.01087.x.
Heithaus, M., Wirsing, A. and Dill, L., 2012. The ecological importance of intact top-predator populations: a synthesis of 15 years of research in a seagrass ecosystem. Marine and Freshwater Research, 63(11), pp. 1039-1050. https://doi.org/10.1071/MF12024.
Helfman, G. and Burgess, G., 2014. Sharks: The Animal Answer Guide. Baltimore:
Johns Hopkins University Press.
Hines, E., Adulyanukosol, K., Somany, P., Ath, L., Boonyanate, P. and Hoa, N., 2008. Conservation needs of the dugong Dugong dugon in Cambodia and Phu Quoc Island, Vietnam. Oryx, 42(1), pp. 113-121. https://doi.org/10.1017/S0030605308000094.
Jackson, J., Kirby, M., Berger, W., Bjorndal, K., Botsford, L., Bourque, B., Bradbury, R., Cooke, R., Erlandson, J., Estes, J. et al., 2001. Historical Overfishing and the Recent Collapse of Coastal Ecosystems. Science, 293(5530), pp. 629-637. https://doi.org/10.1126/science.1059199.
Jordan, L., Mandelman, J., McComb, D., Fordham, S., Carlson, J. and Wener, T., 2013. Linking sensory biology and fisheries bycatch reduction in elasmobranch fishes: a review with new directions for research. Conservation Physiology, 1(1). https://doi.org/10.1093/conphys/cot002.
Kirby, R., Beaugrand, G. and Lindley, J., 2009. Synergistic effects if Climate and Fishing in a Marine Ecosystem. Ecosystems, 12, pp. 548-561. https://10.1007/s10021-009-9241-9.
Lal, A., Arthur, R., Marbà, N., Lill, A. and Alcoverro, T., 2010. Implications of conserving an ecosystem modifier: increasing green turtle (Chelonia mydas) densities substantially alters seagrass meadows. Biological Conservation, 143(11), pp. 2730–2738. https://doi.org/10.1016/j.biocon.2010.07.020.
Lewison, R., Crowder, L., Read, A. and Freeman, S., 2004. Understanding impacts of fisheries bycatch on marine megafauna. Trends in Ecology & Evolution, 19(11), pp. 598-604. https://doi.org/10.1016/j.tree.2004.09.004.
Möllmann, C., Müller-Karulis, B., Kornilovs, G. and St John, M., 2008. Effects of climate and overfishing on zooplankton dynamics and ecosystem structure: regime shifts, trophic cascade, and feedback loops in a simple ecosystem. ICES Journal of Marine Science, 65(3), pp. 302-310. https://doi.org/10.1093/icesjms/fsm197.
Myers, R., Baum, J., Shepherd, T., Powers, S. and Peterson, C., 2007. Cascading Effects of the Loss of Apex Predatory Sharks from a Coastal Ocean. Science, 315(5820), pp. 1846-1850. https://doi.org/10.1126/science.1138657.
Oliver, S., Braccini, M., Newman, S. and Harvey, E., 2015. Global patterns in the bycatch of sharks and rays. Marine Policy, 54, pp. 86-97. https://doi.org/10.1016/j.marpol.2014.12.017.
Paine, R., 1969. The Pisaster-Tegula Interaction: Prey Patches, Predator Food Preference, and Intertidal Community Structure. Ecology, 50(6), pp 950-961. https://doi.org/10.2307/1936888.
Paine, R., 1980. Food Webs: Linkage, Interaction Strength and Community Infrastructure. Journal of Animal Ecology, 48(3), pp. 666-685. https://doi.org/10.2307/4220.
Parsons, T., 1992. The removal of marine predators by fisheries and the impact of trophic structure. Marine Pollution Bulletin, 25(1-4), pp. 51-53. https://doi.org/10.1016/0025-326X(92)90185-9.
Preen, A., 1995. Impacts of dugong foraging on seagrass habitats: observational and experimental evidence for cultivation grazing. Marine Ecology Progress Series, 124(1-3), pp. 201-213. https://doi.org/10.3354/meps124201.
Steneck, R., 2012. Apex predators and trophic cascades in large marine ecosystems: Learning from serendipity. Proceedings of the National Academy of Sciences of the United States of America, 109(21), pp. 7953-7954. https://doi.org/10.1073/pnas.1205591109.
Terborgh, J. and Estes, J., 2010. Trophic Cascades: Predators, Prey, and the Changing Dynamics of Nature. Washington, DC: Island Press.
Vannuccini, S., 1999. Shark Utilization, Marketing and Trade. FAO fisheries technical paper, 389.