Sharks: the World’s Custodians of Fisheries

Today’s post comes from Salvador Herrando-Pérez (who, incidentally, recently submitted his excellent PhD thesis).

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Three species co-occurring in the Gulf of Mexico and involved in the trophic cascade examined by Myers et al. (8). [1] Black-tips (Carcharhinus limbatus) are pelagic sharks in warm and tropical waters worldwide; they reach < 3 m in length, 125 kg in weight, with a maximum longevity in the wild of ~ 12 years; a viviparous species, with females delivering up to 10 offspring per parturition. [2] The cownose ray (Rhinoptera bonasus) is a tropical species from the western Atlantic (USA to Brazil); up to 2 m wide, 50 kg in weight, and 18 years of age; gregarious, migratory and viviparous, with one single offspring per litter. [3] The bay scallop (Agropecten irradians) is a protandric (hermaphrodite) mollusc, with sperm being released a few days before the (> 1 million) eggs; commonly associated with seagrasses in the north-western Atlantic; shells can reach up to 10 cm and individuals live for < 2 years. In the photos, a black-tip angled in a bottom long-line off Alabama (USA), a school of cownose rays swimming along Fort Walton Beach (Florida, USA), and a bay scallop among fronds of turtle grass (Thalassia testudinum) off Hernando County (Florida, USA). Photos by Marcus Drymon, Dorothy Birch and Janessa Cobb, respectively.

The hips of John Travolta, the sword of Luke Skywalker, and the teeth of Jaws marked an era. I still get goose pimples with the movie soundtrack (bass, tuba, orchestra… silence) solemnizing each of the big shark’s attacks. The media and cinema have created the myth of man’s worst friend. This partly explains why shark fishing does not trigger the same societal rejection as the hunting of other colossuses such as whales or elephants. Some authors contend that we currently live in the sixth massive extinction event of planet Earth (1) 75 % of which is strongly driven by one species, humans, and characterized by the systematic disappearance of mega-animals in general (e.g., mammoths, Steller’s seacow), and predators in particular, e.g., sharks (2, 3).

The selective extirpation of apex predators, recently coined as ‘trophic downgrading’, is transforming habitat structure and species composition of many ecosystems worldwide (4). In the marine realm, over the last half a century, the main target of the world’s fisheries has turned from (oft-large body-sized) piscivorous to planctivorous fish and invertebrates, indicating that fishery fleets are exploiting a trophic level down to collapse, then harvesting the next lower trophic level (5-7).

Myers et al. (8) illustrate the problem with the fisheries of apex-predator sharks in the northeastern coast of the USA. Those Atlantic waters are rife with many species of shark (> 2 m), whose main prey are smaller chondrichthyans (skates, rays, catsharks, sharks), which in turn prey on bottom fishes and bivalves. Myers et al. (8) found that, over the last three decades, the abundance of seven species of large sharks declined by ~ 90 %, coinciding with the crash of a centenary fishery of bay scallops (Agropecten irradians). Conversely, the abundance of 12 smaller chondrichthyes increased dramatically over the same period of time. In particular, the cownose ray (Rhinoptera bonasus), the principal predator of bay scallops, might today exceed > 40 million individuals in some bays, and consume up to ~ 840,000 tonnes of scallops annually. The obvious hypothesis is that the reduction of apex sharks triggers the boom of small chondrichthyans, hence leading to the break-down of scallop stocks.

Trophic cascade linked to overfishing of large sharks in the Northeastern coast of USA (8). Graphs show catches of blacktip shark (blue, Carcharhinus limbatus) and bay scallop (red, Agropecten irradians), and censuses of cownose ray (grey, Rhinoptera bonasus) between 1970 and 2004. Relative abundances are standardized to a maximum of 1. In this trophic chain, sharks eat rays, and rays eat scallops. As can be seen, extirpation of sharks has occurred gradually as rays thrived and scallop catches plummeted. Those trends are supported across the assemblage of chondrichthyans in the region (8), while heavy ray predation on scallops has been demonstrated experimentally (17).

Eating and being eaten

Trophic downgrading is an example of a trophic cascade. In simple terms, a trophic cascade represents a predator-prey (or parasite-host) relationship, the balance of which affects the abundance, biomass or productivity of a third species (9). Thus, fish species in a freshwater lake might enhance local pollination of  terrestrial plants if, by feeding on aquatic larvae of dragonfly, diminish the abundance of adults of dragonfly that forage on pollinating bees (10).

Trophic cascades can originate from human action (e.g., trophic downgrading), natural factors, or both. Thus, at the beginning of last century, overhunting of Alaskan sea otters (Enhydra lutris) brought the species to the brink of extinction, but provoked the explosion of their preferred prey, sea urchins, which devoured kelp forests. Subsequently, kelp forests recovered after several decades of otter protection (11). Now some authors suggest that killer whale (Orcinus orca) predation on sea otters might jeopardize kelp forests again (12-14).

Most importantly, trophic cascades result not only from direct mortality of prey species, but due to change in prey behavior avoiding their enemies (15). In Australia, tiger sharks (Galeocerdo cuvier) can shape local distribution and abundance of seagrass beds, because dugongs (Dugong dugon) avoid the lush shallow-water seagrass, in favour of deeper waters with less food, yet lower risk of shark encounters (16).

Globally, trophic cascades brought about by extirpation or introduction of predators or megaherbivores promote or exacerbate a range of severe, long-term environmental impacts such as wild fires, invasion of foreign species, disease bouts, CO₂ emissions, water hypoxia or impoverishment of species richness (4). Those outcomes manifest the complexity of trophic chains, and the need to account for species’ ecological functions in our (largely failed) endeavour of regulating our encroachments on nature and ecosystem services.

References

1. D. B. Wake, V. T. Vredenburg, Proc. Natl. Acad. Sci. USA 105, 11466 (2008)
2. J. K. Baum et al., Science 299, 389 (2003)
3. F. Ferretti, R. A. Myers, F. Serena, H. K. Lotze, Conserv. Biol. 22, 952 (2008)
4. J. A. Estes et al., Science 333, 301 (2011)
5. B. Bhathal, D. Pauly, Fish. Res. 91, 26 (2008)
6. D. Pauly, V. Christensen, J. Dalsgaard, R. Froese, F. Torres, Science 279, 860 (1998)
7. T. E. Essington, A. H. Beaudreau, J. Wiedenmann, Proc. Natl. Acad. Sci. USA 103, 3171 (2006)
8. R. A. Myers, J. K. Baum, T. D. Shepherd, S. P. Powers, C. H. Peterson, Science 315, 1846 (2007)
9. M. L. Pace, J. J. Cole, S. R. Carpenter, J. F. Kitchell, Trends Ecol. Evol. 14, 483 (1999)
10. T. M. Knight, M. W. McCoy, J. M. Chase, K. A. McCoy, R. D. Holt, Nature 437, 880 (2005)
11. J. A. Estes, D. O. Duggins, Ecol. Monog. 65, 75 (1995)
12. M. Schrope, Nature 445, 703 (2007)
13. A. M. Springer et al., Proc. Natl. Acad. Sci. USA 100, 12223 (2003)
14. A. M. Springer et al., Mar. Mamm. Sci. 24, 414 (2008)
15. M. R. Heithaus, A. Frid, A. J. Wirsing, B. Worm, Trends Ecol. Evol. 23, 202 (2008)
16. A. J. Wirsing, M. R. Heithaus, L. M. Dill, Oecologia 153, 1031 (2007)
17. C. Peterson, J. Fodrie, H. Summerson, S. Powers, Oecologia 129, 349 (2001)

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