Portal de Periódicos da CAPES

Opportunistic exploitation: an overlooked pathway to extinction

2013; Elsevier BV; Volume: 28; Issue: 7 Linguagem: Inglês

10.1016/j.tree.2013.03.003

1872-8383

Trevor A. Branch, Aaron Savio Lobo, Steven W. Purcell,

Coral and Marine Ecosystems Studies

•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 (US$23,895) 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. Leader-Williams N. A model of incentives for the illegal exploitation of black rhinos and elephants: poaching pays in Luangwa Valley, Zambia.J. Appl. Ecol. 1992; 29: 388-401Crossref Scopus (145) Google Scholar]. However, poachers could make a living by targeting elephants, which were ten times more abundant, while poaching black rhinoceroses when they were encountered [20Milner-Gulland E.J. Leader-Williams N. A model of incentives for the illegal exploitation of black rhinos and elephants: poaching pays in Luangwa Valley, Zambia.J. Appl. Ecol. 1992; 29: 388-401Crossref Scopus (145) Google Scholar]. By the end of the 20th century, black rhinoceroses were extinct not just in the Luangwa Valley, but in all of Zambia [21Chomba C. Matandiko W. Population status of black and white rhinos in Zambia.Pachyderm. 2011; 50: 50-55Google Scholar]. Similarly, hunters in the Indonesian island of Sulawesi use snares to trap abundant Sulawesi wild pigs (Sus celebensis), but this allows them simultaneously to poach another wild pig, the rare babirusa (Babyrousa celebensis) (Figure 3) [22Clayton L. et al.Bringing home the bacon: a spatial model of wild pig hunting in Sulawesi, Indonesia.Ecol. Appl. 1997; 7: 642-652Crossref Scopus (66) Google Scholar], which would otherwise not be profitable to hunt. Although the babirusa are legally protected, they are caught more easily by the snares and thus even a small amount of trapping of Sulawesi wild pigs can eliminate babirusa from an area. Rowcliffe et al. make use of wordplay to describe this example as 'piggyback extinction' [23Rowcliffe J.M. et al.A model of human hunting impacts in multi-prey communities.J. Appl. Ecol. 2003; 40: 872-889Crossref Scopus (68) Google Scholar]. Bushmeat hunting in Equatorial Guinea and Ghana also displays classic signs of opportunistic exploitation, with more abundant smaller animals maintaining profitable hunting while larger, rare, and more valuable animals are still hunted whenever they are encountered [24Bennett E. et al.Why is eating bushmeat a biodiversity crisis?.Conserv. Pract. 2012; 3: 28-29Google Scholar, 25Cowlishaw G. et al.Evidence for post-depletion sustainability in a mature bushmeat market.J. Appl. Ecol. 2005; 42: 460-468Crossref Scopus (135) Google Scholar]. Selective logging of big-leaf mahogany (Swietenia macrophylla) also exemplifies opportunistic exploitation. In the Brazilian Amazon, these highly valued lumber trees are found at low densities, but logging removes 93–95% of commercial-sized trees [26Grogan J. et al.What loggers leave behind: Impacts on big-leaf mahogany (Swietenia macrophylla) commercial populations and potential for post-logging recovery in the Brazilian Amazon.Forest Ecol. Manag. 2008; 255: 269-281Crossref Scopus (57) Google Scholar]. Further waves of logging for low-value species ensures that big-leaf mahogany missed during the first wave are eradicated [27Grogan J. et al.Over-harvesting driven by consumer demand leads to population decline: big-leaf mahogany in South America.Conserv. Lett. 2010; 3: 12-20Crossref Scopus (38) Google Scholar], leading to simplified forests containing only low-value species. There are likely to be many more terrestrial examples of opportunistic exploitation, from both the past and the present. Possible candidates include the present-day depletion of Madagascar rosewood (Dalbergia spp.) [28Barrett M.A. et al.CITES designation for endangered rosewood in Madagascar.Science. 2010; 328: 1109-1110Crossref PubMed Scopus (56) Google Scholar], the near-extinction of American bison (Bison bison) [29Lueck D. The extermination and conservation of the American bison.J. Legal Stud. 2002; 31: S609-S652Crossref Scopus (47) Google Scholar], and the extinctions of South African blue antelope (Hippotragus leucophaeus) [30Kerley G.I.H. et al.Extinction of the blue antelope Hippotragus leucophaeus: modeling predicts non-viable global population size as the primary driver.Biodivers. Conserv. 2009; 18: 3235-3242Crossref Scopus (18) Google Scholar] and New Zealand moa species (Aves, Dinornithiformes) [31Anderson A. Mechanics of overkill in the extinction of New Zealand moas.J. Archaeol. Sci. 1989; 16: 137-151Crossref Scopus (62) Google Scholar]. Opportunistic exploitation might thus be a widespread but overlooked phenomenon wherever humans exploit multiple species together, with some ecological parallels in the general field of 'apparent competition' where the abundance of two prey species becomes linked through shared predators, affecting predator functional responses [32Holt R.D. Predation, apparent competition, and the structure of prey communities.Theor. Popul. Biol. 1977; 12: 197-229Crossref PubMed Scopus (1757) Google Scholar]. Multispecies models invoking apparent competition can explain how early hunters caused the mass extinction of large mammals in North America, whereas models based on a single prey species cannot [33Alroy J. A multispecies overkill simulation of the end-Pleistocene megafaunal mass extinction.Science. 2001; 292: 1893-1896Crossref PubMed Scopus (413) Google Scholar, 34Alroy J. Did human hunting cause mass extinction? Response.Science. 2001; 294: 1459-1462Google Scholar]. For instance, common forms of functional response in predators can act to keep one prey species in a low-abundance 'predator pit' [35Holling C.S. The functional response of predators to prey density and its role in mimicry and population regulation.Mem. Entomol. Soc. Can. 1965; 45: 5-60Google Scholar, 36Bakun A. Wasp-waist populations and marine ecosystem dynamics: navigating the "predator pit" topographies.Prog. Oceanogr. 2006; 68: 271-288Crossref Scopus (230) Google Scholar] whereby, if they increase, predators will start targeting them and keep their numbers depressed, but at low densities predators no longer maintain a search image for that species and switch to other prey species [37Smout S. et al.The functional response of a generalist predator.PLOS ONE. 2010; 5: e10761Crossref PubMed Scopus (73) Google Scholar]. Unlike most natural predators, however, humans maintain and even increase their desire to target high-value species when they are encountered at low densities [5Courchamp F. et al.Rarity value and species extinction: the anthropogenic Allee effect.PLOS Biol. 2006; 4: e415Crossref PubMed Scopus (381) Google Scholar], so there is no refuge in rarity. 'Hyperpredation' in natural systems is also somewhat analogous to opportunistic exploitation. Hyperpredation occurs when one prey source increases, subsidizing higher predator populations, which in turn cause declines in alternative prey populations [38Smith A.P. Quin D.G. Patterns and causes of extinctions and decline in Australian conilurine rodents.Biol. Conserv. 1996; 77: 243-267Crossref Scopus (288) Google Scholar]. This is typified by declines and extinctions of native Australian rodents, where feral cats and other predators subsidize their diets with introduced rabbits and mice [38Smith A.P. Quin D.G. Patterns and causes of extinctions and decline in Australian conilurine rodents.Biol. Conserv. 1996; 77: 243-267Crossref Scopus (288) Google Scholar], and by the declines of island foxes in the California Channel Islands due to introduced pigs providing a steady food source for predatory golden eagles [39Roemer G.W. et al.Golden eagles, feral pigs, and insular carnivores: how exotic species turn native predators into prey.Proc. Natl. Acad. Sci. U.S.A. 2002; 99: 791-796Crossref PubMed Scopus (302) Google Scholar]. However, whereas hyperpredation requires an increase in alternative prey, opportunistic exploitation can happen even when the abundance of alternative prey is constant or declining. Management and conservation policies need to identify species at risk of opportunistic exploitation and take steps to avoid their potential depletion and extinction. Past studies have focused on attributes of each species in isolation to predict their risk of extinction: factors such as life-history traits, overexploitation, loss of habitat, disease, rates of decline, abundance, and geographic range [4Dulvy N.K. et al.Extinction vulnerability in marine populations.Fish Fish. 2003; 4: 25-64Crossref Scopus (690) Google Scholar, 40Mace G.M. et al.Quantification of extinction risk: IUCN's system for classifying threatened species.Conserv. Biol. 2008; 22: 1424-1442Crossref PubMed Scopus (912) Google Scholar]. We argue that multispecies attributes are also important; the risk of opportunistic exploitation not only depends on the value of the species in question, but is also linked to the presence of co-occurring lower-value species that could subsidize continued exploitation. There are several specific management actions that can be taken to overcome opportunistic exploitation. One key realization is that private ownership of multispecies resources can lead to economically rational overexploitation. Managers should pay special attention to rare species that are highly valuable and institute protocols to limit and monitor trade. For example, Papua New Guinea has an export ban on seven species of birdwings, the largest butterflies in the world, due to their rarity and the global demand from collectors [41Slone T.H. et al.A comparison of price, rarity and cost of butterfly specimens: Implications for the insect trade and for habitat conservation.Ecol. Econ. 1997; 21: 77-85Crossref Scopus (34) Google Scholar]. Another useful policy is to develop shortlists 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], instead of imposing species bans that inevitably are developed too late to avoid depletion from opportunistic exploitation. The shortlists could include common exploitable species but exclude threatened high-value species and others that are not targeted to preserve ecosystem functioning. Used in this manner, shortlists would prevent the future expansion of exploitation to new species before they can be assessed. Naturally, trade restrictions and shortlists should be based on sound taxonomy, to ensure that the diagnosis of extinction risk is not clouded by cryptic species that are part of undetected species complexes [42Iglésias S.P. et al.Taxonomic confusion and market mislabelling of threatened skates: important consequences for their conservation status.Aquat. Conserv.: Mar. Freshwat. Ecosyst. 2010; 20: 319-333Crossref Scopus (131) Google Scholar]. Another pitfall to avoid is a group quota for the exploitation of multiple similar species. The International Whaling Commission initially set an annual quota on the weighted catch of all species of large whales combined, which contributed greatly to the decline of individual species, including Antarctic blue whales. Instead, sustainable individual-species quotas should be set wherever quotas can be practically established, monitored, and enforced. Related to the idea of individual quotas for species is the proposal for balanced fisheries exploitation, where catches are spread broadly across a range of species while care is taken to ensure that exploitation rates for individual species remain in proportion to their productivity [43Zhou S. et al.Ecosystem-based fisheries management requires a change to the selective fishing philosophy.Proc. Natl. Acad. Sci. U.S.A. 2010; 107: 9485-9489Crossref PubMed Scopus (274) Google Scholar, 44Garcia S.M. et al.Reconsidering the consequences of selective fisheries.Science. 2012; 335: 1045-1047Crossref PubMed Scopus (334) Google Scholar]. Fishers are capable of applying this approach in multispecies fisheries, provided there are sufficient incentives to target and avoid particular species, but this requires near-100% enforcement and monitoring [45Branch T.A. Hilborn R. Matching catches to quotas in a multispecies trawl fishery: targeting and avoidance behavior under individual transferable quotas.Can. J. Fish. Aquat. Sci. 2008; 65: 1435-1446Crossref Scopus (104) Google Scholar]. The danger of the balanced-exploitation approach is that expanding catches to new species acts as a subsidy for the continued exploitation of current species, as seen in our example of multispecies trawl fisheries in India. In addition to these specific policy ideas to mitigate opportunistic exploitation, there are a number of familiar policies that are also needed. For instance, ideally, species should be regulated by limiting the amount exploited and not the amount of effort expended (a surprisingly common regulation in fisheries). Terrestrial and marine reserves should be set aside where no extractive exploitation is allowed, to serve as a refuge against opportunistic exploitation. Finally, all regulations are moot without effective monitoring and enforcement to deter illegal exploitation. Examples from fishing, hunting, and logging demonstrate that opportunistic exploitation is a pervasive pathway to depletion and extinction wherever multiple species are exploited. We anticipate that further examples of opportunistic exploitation, both historically and in the present, will come to light wherever humans exploit natural resources. For example, opportunistic exploitation might arise in spear-fishing, in trapping, and in the process of collecting bird eggs, orchids, mushrooms, insects, shells, and ornamental corals [46Salafsky N. et al.A standard lexicon for biodiversity conservation: unified classifications of threats and actions.Conserv. Biol. 2008; 22: 897-911Crossref PubMed Scopus (513) Google Scholar]. Policy efforts should focus on conserving rare, high-value species exploited within multispecies systems, to avoid scenarios where subsidy by lower-value species allows a profitable pathway that drives species toward extinction.GlossaryAccidental exploitation: this mode occurs when the exploited species has no economic value but is killed while a target species is exploited. Cases include the deaths of sea snakes caught and discarded in trawl fisheries in Australia [47Rasmussen A.R. et al.Marine reptiles.PLOS ONE. 2013; 6: e27373Crossref Scopus (99) Google Scholar] and accidental snare captures in Newfoundland of endangered marten (Martes americana) while snowshoe hares (Lepus americanus) are targeted [48Thompson I.D. Could marten become the spotted owl of eastern Canada?.Forest. Chron. 1991; 67: 136-140Google Scholar].Incidental exploitation: this mode involves the exploitation of less desirable species when commingled with the target species (e.g., Figure 5 in [4Dulvy N.K. et al.Extinction vulnerability in marine populations.Fish Fish. 2003; 4: 25-64Crossref Scopus (690) Google Scholar]). In fisheries, it has long been recognized that, in such a situation, maximizing catches from all species combined will result in the depletion or extirpation of less-resilient species [49Ricker W.E. Maximum sustained yields from fluctuating environments and mixed stocks.J. Fish. Res. Board Can. 1958; 15: 991-1006Crossref Google Scholar, 50Paulik G.J. et al.Exploitation of multiple stocks by a common fishery.J. Fish. Res. Board Can. 1967; 24: 2527-2537Crossref Google Scholar, 51Hilborn R. Optimal exploitation of multiple stocks by a common fishery: a new methodology.J. Fish. Res. Board Can. 1976; 33: 1-5Crossref PubMed Google Scholar, 52Worm B. et al.Rebuilding global fisheries.Science. 2009; 325: 578-585Crossref PubMed Scopus (1608) Google Scholar]. Specific examples include the incidental bycatch of shark species in longline fisheries for tuna and swordfish [53Megalofonou P. et al.Incidental catch and estimated discards of pelagic sharks from the swordfish and tuna fisheries in the Mediterranean Sea.Fish. Bull. 2005; 103: 620-634Google Scholar] and the near extirpation of common skate (Dipturus batis) in the Irish Sea when caught by trawlers targeting more valuable and abundant species such as cod [42Iglésias S.P. et al.Taxonomic confusion and market mislabelling of threatened skates: important consequences for their conservation status.Aquat. Conserv.: Mar. Freshwat. Ecosyst. 2010; 20: 319-333Crossref Scopus (131) Google Scholar, 54Brander K. Disappearance of common skate Raia batis from Irish Sea.Nature. 1981; 290: 48-49Crossref Scopus (250) Google Scholar].Opportunistic exploitation: the exploitation of a scarce but desirable species, when encountered while targeting other less desirable but more common species. Exploitation is only profitable because of the presence of the less desirable species. The term was originally coined as 'opportunistic depletion' [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 densities below the bioeconomic equilibrium [55Gordon H.S. The economic theory of a common-property resource: the fishery.J. Polit. Econ. 1954; 62: 124-142Crossref Google Scholar], when profit (income minus expenses) is the same as from available alternatives. In the single-species case, humans should logically cease exploitation at this point. However, where multiple species can be exploited in the same habitat, humans will often first deplete the most desirable species, depleting it to the point of bioeconomic equilibrium, before switching to less desirable species. The crux of opportunistic exploitation is that at this point the sparse but desirable species can continue to be taken opportunistically whenever it is encountered, providing an unexpected bonus to the exploiter. The definition of 'opportunistic' involves 'exploiting circumstances or opportunities to gain immediate advantage, rather than following a predetermined plan…; especially with the implication of cynicism or a lack of regard to principles' (Oxford English Dictionary, http://www.oed.com). Thus, opportunistic exploitation carries the dual connotations of being both unplanned and selfishly targeting an already depleted species.Targeted exploitation: this is the most common mode, which occurs when one or a few species are the primary subjects of resource extraction. Examples include trophy hunting for wild goats (subfamily Caprinae) [5Courchamp F. et al.Rarity value and species extinction: the anthropogenic Allee effect.PLOS Biol. 2006; 4: e415Crossref PubMed Scopus (381) Google Scholar] and diving for black-lip abalone (Haliotis rubra) in Australia [56Leiva G.E. Castilla J.C. A review of the world marine gastropod fishery: evolution of catches, management and the Chilean experience.Rev. Fish Biol. Fish. 2002; 11: 283-300Crossref Scopus (130) Google Scholar].Tabled 1Key differences between exploitation modesExploitation modeValue of speciesPrimary target?OpportunisticHigher than targetNoTargetedProfitableYesIncidentalLower than targetNoAccidentalNo valueNo Open table in a new tab Accidental exploitation: this mode occurs when the exploited species has no economic value but is killed while a target species is exploited. Cases include the deaths of sea snakes caught and discarded in trawl fisheries in Australia [47Rasmussen A.R. et al.Marine reptiles.PLOS ONE. 2013; 6: e27373Crossref Scopus (99) Google Scholar] and accidental snare captures in Newfoundland of endangered marten (Martes americana) while snowshoe hares (Lepus americanus) are targeted [48Thompson I.D. Could marten become the spotted owl of eastern Canada?.Forest. Chron. 1991; 67: 136-140Google Scholar].Incidental exploitation: this mode involves the exploitation of less desirable species when commingled with the target species (e.g., Figure 5 in [4Dulvy N.K. et al.Extinction vulnerability in marine populations.Fish Fish. 2003; 4: 25-64Crossref Scopus (690) Google Scholar]). In fisheries, it has long been recognized that, in such a situation, maximizing catches from all species combined will result in the depletion or extirpation of less-resilient species [49Ricker W.E. Maximum sustained yields from fluctuating environments and mixed stocks.J. Fish. Res. Board Can. 1958; 15: 991-1006Crossref Google Scholar, 50Paulik G.J. et al.Exploitation of multiple stocks by a common fishery.J. Fish. Res. Board Can. 1967; 24: 2527-2537Crossref Google Scholar, 51Hilborn R. Optimal exploitation of multiple stocks by a common fishery: a new methodology.J. Fish. Res. Board Can. 1976; 33: 1-5Crossref PubMed Google Scholar, 52Worm B. et al.Rebuilding global fisheries.Science. 2009; 325: 578-585Crossref PubMed Scopus (1608) Google Scholar]. Specific examples include the incidental bycatch of shark species in longline fisheries for tuna and swordfish [53Megalofonou P. et al.Incidental catch and estimated discards of pelagic sharks from the swordfish and tuna fisheries in the Mediterranean Sea.Fish. Bull. 2005; 103: 620-634Google Scholar] and the near extirpation of common skate (Dipturus batis) in the Irish Sea when caught by trawlers targeting more valuable and abundant species such as cod [42Iglésias S.P. et al.Taxonomic confusion and market mislabelling of threatened skates: important consequences for their conservation status.Aquat. Conserv.: Mar. Freshwat. Ecosyst. 2010; 20: 319-333Crossref Scopus (131) Google Scholar, 54Brander K. Disappearance of common skate Raia batis from Irish Sea.Nature. 1981; 290: 48-49Crossref Scopus (250) Google Scholar].Opportunistic exploitation: the exploitation of a scarce but desirable species, when encountered while targeting other less desirable but more common species. Exploitation is only profitable because of the presence of the less desirable species. The term was originally coined as 'opportunistic depletion' [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 densities below the bioeconomic equilibrium [55Gordon H.S. The economic theory of a common-property resource: the fishery.J. Polit. Econ. 1954; 62: 124-142Crossref Google Scholar], when profit (income minus expenses) is the same as from available alternatives. In the single-species case, humans should logically cease exploitation at this point. However, where multiple species can be exploited in the same habitat, humans will often first deplete the most desirable species, depleting it to the point of bioeconomic equilibrium, before switching to less desirable species. The crux of opportunistic exploitation is that at this point the sparse but desirable species can continue to be taken opportunistically whenever it is encountered, providing an unexpected bonus to the exploiter. The definition of 'opportunistic' involves 'exploiting circumstances or opportunities to gain immediate advantage, rather than following a predetermined plan…; especially with the implication of cynicism or a lack of regard to principles' (Oxford English Dictionary, http://www.oed.com). Thus, opportunistic exploitation carries the dual connotations of being both unplanned and selfishly targeting an already depleted species.Targeted exploitation: this is the most common mode, which occurs when one or a few species are the primary subjects of resource extraction. Examples include trophy hunting for wild goats (subfamily Caprinae) [5Courchamp F. et al.Rarity value and species extinction: the anthropogenic Allee effect.PLOS Biol. 2006; 4: e415Crossref PubMed Scopus (381) Google Scholar] and diving for black-lip abalone (Haliotis rubra) in Australia [56Leiva G.E. Castilla J.C. A review of the world marine gastropod fishery: evolution of catches, management and the Chilean experience.Rev. Fish Biol. Fish. 2002; 11: 283-300Crossref Scopus (130) Google Scholar].Tabled 1Key differences between exploitation modesExploitation modeValue of speciesPrimary target?OpportunisticHigher than targetNoTargetedProfitableYesIncidentalLower than targetNoAccidentalNo valueNo Open table in a new tab The authors thank Daniel Schindler, Ray Hilborn, Jim Kitchell, and Nicholas Dulvy for helpful comments on earlier drafts that greatly improved the manuscript.