Opportunistic exploitation: an overlooked pathway to extinction

•Opportunistic exploitation of high-value species may occur in multispecies systems. •Targeting common species subsidizes continued depletion of high-value species. •This pathway appears widespread but underappreciated, with many case studies. •Ecological parallels include apparent competition, hyperpredation, and predator pits. •Managers should protect high-value species exploited with other species. How can species be exploited economically to extinction? Past single-species hypotheses examining the economic plausibility of exploiting rare species have argued that the escalating value of rarity allows extinction to be profitable. We describe an alternative pathway toward extinction in multispecies exploitation systems, termed ‘opportunistic exploitation’. In this mode, highly valued species that are targeted first by fishing, hunting, and logging become rare, but their populations can decline further through opportunistic exploitation while more common but less desirable species are targeted. Effectively, expanding exploitation to more species subsidizes the eventual extinction of valuable species at low densities. Managers need to recognize conditions that permit opportunistic depletion and pass regulations to protect highly desirable species when exploitation can expand to other species. How can species be exploited economically to extinction? Past single-species hypotheses examining the economic plausibility of exploiting rare species have argued that the escalating value of rarity allows extinction to be profitable. We describe an alternative pathway toward extinction in multispecies exploitation systems, termed ‘opportunistic exploitation’. In this mode, highly valued species that are targeted first by fishing, hunting, and logging become rare, but their populations can decline further through opportunistic exploitation while more common but less desirable species are targeted. Effectively, expanding exploitation to more species subsidizes the eventual extinction of valuable species at low densities. Managers need to recognize conditions that permit opportunistic depletion and pass regulations to protect highly desirable species when exploitation can expand to other species. Humans are by far the biggest drivers of extinction, both directly and indirectly 1Diamond J. M. The present, past and future of human-caused extinctions. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 1989; 325: 469-477Crossref PubMed Google Scholar. Yet extinction through exploitation seems paradoxical: how can this be profitable given the exorbitant costs of targeting rare species? Two previous hypotheses suggest ways in which this could be profitable, but here we expand on another exploitation mode termed opportunistic exploitation (see Glossary) that arguably offers a much more widespread pathway to extinction. One previous hypothesis, the ‘economics of overexploitation’ 2Clark C. W. The economics of overexploitation. Science. 1973; 181: 630-634Crossref PubMed Scopus (379) Google Scholar, contends that when population growth rates are low relative to monetary returns on investments, exploiters could maximize their net present value by catching the entire population, banking the money, and living off the comparatively high interest. The applicability of this hypothesis has recently been challenged: even for very unproductive species, catching the last individual would be too costly to maximize net present value 3Grafton R. Q. et al. Economics of overexploitation revisited. Science. 2007; 318: 1601Crossref PubMed Scopus (176) Google Scholar. An alternative hypothesis is the ‘anthropogenic Allee effect’, which notes that humans place exaggerated value on species as they become rare, allowing profitable exploitation at very low population sizes 4Dulvy N. K. et al. Extinction vulnerability in marine populations. Fish Fish. 2003; 4: 25-64Crossref Scopus (690) Google Scholar, 5Courchamp F. et al. Rarity value and species extinction: the anthropogenic Allee effect. PLOS Biol. 2006; 4: e415Crossref PubMed Scopus (381) Google Scholar. For example, the traditional Chinese medicine market generates intense demand for products from rare fauna such as rhinoceroses and tigers 6Graham-Rowe D. Endangered and in demand. Nature. 2011; 480: S101-S103Crossref PubMed Scopus (57) Google Scholar. One instance of this demand is for the Chinese bahaba, Bahaba taipingensis, which possesses a swimbladder that is highly coveted by Asian consumers of tonic soups for its supposed medicinal properties 7Sadovy Y. Cheung W. L. Near extinction of a highly fecund fish: the one that nearly got away. Fish Fish. 2003; 4: 86-99Crossref Scopus (142) Google Scholar. A single 60. 5 kg Chinese bahaba caught in the Fujian and Guangdon Provinces was once sold for the same price (US23, 895) as a three-bedroom house 7Sadovy Y. Cheung W. L. Near extinction of a highly fecund fish: the one that nearly got away. Fish Fish. 2003; 4: 86-99Crossref Scopus (142) Google Scholar. However, the 100–200 Taiping boats seeking this species must make their living off other species, because only a handful of Chinese bahaba are caught each year 7Sadovy Y. Cheung W. L. Near extinction of a highly fecund fish: the one that nearly got away. Fish Fish. 2003; 4: 86-99Crossref Scopus (142) Google Scholar. Both the economics of overexploitation and the anthropogenic Allee effect hypotheses offer explanations of how exploitation focused on a single species (target exploitation) can lead to extinction. However, it is much more common for multiple species to be exploited together, offering more pathways to extinction. These pathways include accidental exploitation of species with no value and incidental exploitation of species with lower value while pursuing target species. We contend that a further pathway occurs when rare, high-value species are encountered during the exploitation of more common target species. We term this largely unrecognized mode opportunistic exploitation 8Purcell S. W. et al. Sea cucumber fisheries: global analysis of stocks, management measures and drivers of overfishing. Fish Fish. 2013; 14: 34-59Crossref Scopus (320) Google Scholar. This pathway allows critically sparse but valuable species to be profitably exploited when they are encountered while targeting abundant but lower-value species in the same habitat (Figure 1). Note that opportunistic exploitation is more pernicious than incidental or accidental exploitation, because the depleted species has high value, which results in stronger economic incentives for further exploitation. Opportunistic exploitation examples from disparate habitats, scales of exploitation, and trophic levels now provide compelling support for this extinction pathway. Antarctic blue whales were used as the key example exemplifying the economics of overexploitation by Colin Clark 2Clark C. W. The economics of overexploitation. Science. 1973; 181: 630-634Crossref PubMed Scopus (379) Google Scholar, but ironically exemplify opportunistic exploitation. As quoted within the original article 2Clark C. W. The economics of overexploitation. Science. 1973; 181: 630-634Crossref PubMed Scopus (379) Google Scholar: ‘Gulland pers. comm. has pointed out to me that fishing for the Antarctic blue whale probably would have become uneconomical several years earlier had it not been for the simultaneous occurrence of finback whales in the same area. ’ This view is even held by Clark himself in a recent book, where he writes that targeting Antarctic blue whales was effectively a zero-cost activity subsidized by the exploitation of fin whales 9Clark C. W. The Worldwide Crisis in Fisheries: Economic Models and Human Behavior. Cambridge University Press, 2006Google Scholar. The underlying story is that Antarctic blue whales were heavily depleted by pelagic whalers, who caught 28, 000 in 1930 but only 7000 in 1950 and fewer than 200 in 1963 as the population size plummeted 10Branch T. A. et al. Evidence for increases in Antarctic blue whales based on Bayesian modelling. Mar. Mamm. Sci. 2004; 20: 726-754Crossref Scopus (151) Google Scholar. However, this was not due to targeted exploitation, which would never have been profitable at such low population sizes. By the 1950s, profits flowed from less sought-after but more abundant species, particularly fin whales, whereas Antarctic blue whales comprised only 3% of all catches (Figure 2). Thus, it was opportunistic whaling that reduced the abundance of Antarctic blue whales to 0. 15% of pre-whaling levels 10Branch T. A. et al. Evidence for increases in Antarctic blue whales based on Bayesian modelling. Mar. Mamm. Sci. 2004; 20: 726-754Crossref Scopus (151) Google Scholar, before international regulations finally halted the slaughter. Multispecies trawl fisheries are also prone to opportunistic exploitation. For example, in India, trawl fisheries began by targeting valuable shrimp, cephalopods, and large fishes such as snapper and grouper in the 1950s, primarily for export. After these were depleted, trawlers shifted focus to lower-value fish such as croakers and sardines for domestic markets, including the traditionally discarded bycatch comprising small-bodied animals with lower consumer preference, called ‘trash fish’. In India and many other parts of South and Southeast Asia, trash fish are now processed to fishmeal and used as a protein supplement in the poultry and aquaculture industry. The extra subsidy received from these former discards (Figure 3) has allowed trawlers to further deplete high-value species whenever they are encountered 11Lobo A. S. et al. Commercializing bycatch can push a fishery beyond economic extinction. Conserv. Lett. 2010; 3: 277-285Crossref Scopus (32) Google Scholar. Opportunistic exploitation also occurs in small-scale sea cucumber fisheries where multiple species are targeted 8Purcell S. W. et al. Sea cucumber fisheries: global analysis of stocks, management measures and drivers of overfishing. Fish Fish. 2013; 14: 34-59Crossref Scopus (320) Google Scholar. Sea cucumbers feature prominently in Asian medicinal markets and banquet dishes 12Clarke S. Understanding pressures on fishery resources through trade statistics: a pilot study of four products in the Chinese dried seafood market. Fish Fish. 2004; 5: 53-74Crossref Scopus (96) Google Scholar. In sea cucumber fisheries, one or two high-value species are often fished to low levels before fishers shift to lower-value species in the same grounds and then the high-value species continue to be fished while lower-valued species are targeted. In unfished areas, high-value sea cucumber species (Figure 3) are naturally common and widely distributed, but in areas subject to multispecies sea cucumber fisheries they are often critically overfished 13Friedman K. et al. Management of sea cucumber stocks: patterns of vulnerability and recovery of sea cucumber stocks impacted by fishing. Fish Fish. 2011; 12: 75-93Crossref Scopus (80) Google Scholar. Conversely, in single-species sea cucumber fisheries in Alaska, Iceland, New Zealand, British Columbia, Newfoundland and Labrador, Washington, and eastern Russia, where there are no other sea cucumber species to support opportunistic exploitation, even high-value sea cucumber species have not been heavily depleted 8Purcell S. W. et al. Sea cucumber fisheries: global analysis of stocks, management measures and drivers of overfishing. Fish Fish. 2013; 14: 34-59Crossref Scopus (320) Google Scholar. In other words, economic value must be coupled with the presence of more abundant but less desirable species to subsidize the chronic depletion of sea cucumber stocks. Given these examples, we argue that this switch from targeted exploitation to opportunistic exploitation 14Kim J. Opportunistic versus target mode: prey choice changes in central-western Korean prehistory. J. Anthropol. Archaeol. 2010; 29: 80-93Crossref Scopus (14) Google Scholar is probably widespread in marine and freshwater environments. For example, overfishing of Napoleon wrasse (Cheilinus undulatus) 15Sadovy Y. J. Vincent A. C. J. Ecological issues and the trades in live reef fishes. in: Sale P. F. Coral Reef Fishes: Dynamics and Diversity in a Complex Ecosystem. Academic Press, 2002: 391-420Crossref Google Scholar, white abalone (Haliotis sorenseni) 16Hobday A. J. et al. Over-exploitation of a broadcast spawning marine invertebrate: decline of the white abalone. Rev. Fish Biol. Fish. 2001; 10: 493-514Crossref Scopus (119) Google Scholar, and freshwater populations of lake trout (Salvelinus namaycush) and walleye (Stizostedion vitreum) 17Post J. R. et al. Canada's recreational fisheries: the invisible collapse? . Fisheries. 2002; 27: 6-17Crossref Google Scholar were all likely to have been exacerbated because fishing could continue on other species in the same habitat. We also speculate that examples of opportunistic exploitation might include the extinctions of Steller's sea cow (Hydrodamalis gigas) 18Anderson P. K. Competition, predation, and the evolution and extinction of Steller's sea cow, Hydrodomalis gigas. Mar. Mamm. Sci. 1995; 11: 391-394Crossref Scopus (40) Google Scholar and the Caribbean monk seal (Monachus tropicalis) 19McClenachan L. Cooper A. B. Extinction rate, historical population structure and ecological role of the Caribbean monk seal. Proc. Biol. Sci. 2008; 275: 1351-1358Crossref PubMed Scopus (83) Google Scholar. Terrestrial systems also provide examples of opportunistic exploitation. For instance, black rhinoceroses (Figure 3) were illegally poached in the Luangwa Valley, Zambia in the 1980s, despite an economic analysis showing this was unprofitable due to their rarity 20Milner-Gulland E. J. A of incentives for the exploitation of black and in Luangwa Valley, 29: Scopus Google Scholar. 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One key is that of multispecies resources can lead to economically Managers should to rare species that are highly valuable and to and For example, New has an on species of the in the due to their rarity and the global demand from et of rarity and of for the trade and for habitat Scopus Google Scholar]. is to of allowed species 8Purcell S. W. et al. Sea cucumber fisheries: global analysis of stocks, management measures and drivers of overfishing. Fish Fish. 2013; 14: 34-59Crossref Scopus (320) Google Scholar, of species that are too to depletion from opportunistic exploitation. The could include common species but high-value species and that are not targeted to in this would the future of exploitation to species before they can be trade and should be based on to that the of extinction is not by species that are of species et and market of for their 2010; 20: Scopus Google Scholar]. to is a for the exploitation of multiple species. 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The of the is that expanding catches to species as a subsidy for the continued exploitation of species, as in example of multispecies trawl fisheries in In to these to opportunistic exploitation, there are a of that are also For instance, species should be by the exploited and not the of common in Terrestrial and marine should be where no exploitation is to as a opportunistic exploitation. all regulations are and to exploitation. from fishing, hunting, and logging that opportunistic exploitation is a pathway to depletion and extinction multiple species are We that further examples of opportunistic exploitation, both and in the present, to humans For example, opportunistic exploitation might in in and in the of and et for of and Biol. 2008; PubMed Scopus Google Scholar]. should focus on rare, high-value species exploited within multispecies systems, to where subsidy by lower-value species allows a profitable pathway that species toward this mode occurs when the exploited species has no economic value but is while a target species is include the of sea caught and discarded in trawl fisheries in et 2013; Scopus Google Scholar] and accidental in Newfoundland of while are targeted become the of eastern this mode the exploitation of less desirable species when with the target species in 4Dulvy N. 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PLOS Biol. 2006; 4: e415Crossref PubMed Scopus (381) Google Scholar] and for abalone (Haliotis in A of the marine evolution of management and the Fish Biol. Fish. 2002; 11: Scopus Google exploitation of than than in a this mode occurs when the exploited species has no economic value but is while a target species is include the of sea caught and discarded in trawl fisheries in et 2013; Scopus Google Scholar] and accidental in Newfoundland of while are targeted become the of eastern this mode the exploitation of less desirable species when with the target species in 4Dulvy N. K. et al. Extinction vulnerability in marine populations. Fish Fish. 2003; 4: 25-64Crossref Scopus (690) Google In fisheries, it has been in such a catches from all species in the depletion or of species from and Fish. Google Scholar, et of multiple stocks by a common Fish. Google Scholar, R. exploitation of multiple stocks by a common a Fish. PubMed Google Scholar, et global 325: PubMed Scopus Google Scholar. examples include the incidental bycatch of species in fisheries for and et and discards of pelagic from the and fisheries in the Scholar] and the of common in the Sea when caught by trawlers targeting more valuable and abundant species such as et and market of for their 2010; 20: Scopus Google Scholar, K. of common from Scopus Google the exploitation of a but desirable species, when encountered while targeting other less desirable but more common species. is only profitable because of the presence of the less desirable species. The term was as ‘opportunistic 8Purcell S. W. et al. Sea cucumber fisheries: global analysis of stocks, management measures and drivers of overfishing. Fish Fish. 2013; 14: 34-59Crossref Scopus (320) Google Scholar. Opportunistic exploitation allows for continued exploitation at the The economic of a the Google Scholar], when is the same as from In the single-species humans should exploitation at this However, where multiple species can be exploited in the same humans often first deplete the desirable species, it to the of before to less desirable species. The of opportunistic exploitation is that at this the sparse but desirable species can continue to be whenever it is an to the The of or to than a with the of or a of to Thus, opportunistic exploitation the of both and targeting an depleted this is the common mode, which occurs when one or a species are the of include for F. et al. Rarity value and species extinction: the anthropogenic Allee effect. PLOS Biol. 2006; 4: e415Crossref PubMed Scopus (381) Google Scholar] and for abalone (Haliotis in A of the marine evolution of management and the Fish Biol. Fish. 2002; 11: Scopus Google exploitation of than than in a The and for on earlier that the