Opportunistic Exploitation: An

Opinion

Opportunistic exploitation: an

overlooked pathway to extinction

1 2 3

Trevor A. Branch , Aaron S. Lobo , and Steven W. Purcell

School of Aquatic and Fishery Sciences, Box 355020, University of Washington, Seattle, WA 98195, USA

Nature Conservation Foundation, Gokulam Park, Mysore – 570 002, Karnataka, India

National Marine Science Centre, Southern Cross University, PO Box 4321, Coffs Harbour, NSW 2450, Australia

How can species be exploited economically to extinc- Chinese bahaba, Bahaba taipingensis, which possesses a

tion? Past single-species hypotheses examining the eco- swimbladder that is highly coveted by Asian consumers of

nomic plausibility of exploiting rare species have argued tonic soups for its supposed medicinal properties [7]. A

that the escalating value of rarity allows extinction to be single 60.5 kg Chinese bahaba caught in the Fujian and

proﬁtable. We describe an alternative pathway toward Guangdon Provinces was once sold for the same price

extinction in multispecies exploitation systems, termed (US$23,895) as a three-bedroom house [7]. However, the

‘opportunistic exploitation’. In this mode, highly valued 100–200 Taiping boats seeking this species must make

species that are targeted ﬁrst by ﬁshing, hunting, and their living off other species, because only a handful of

logging become rare, but their populations can decline Chinese bahaba are caught each year [7].

further through opportunistic exploitation while more

common but less desirable species are targeted. Effec-

tively, expanding exploitation to more species subsi- Glossary

dizes the eventual extinction of valuable species at

Accidental exploitation: this mode occurs when the exploited species has no

low densities. Managers need to recognize conditions

economic value but is killed while a target species is exploited. Cases include the

that permit opportunistic depletion and pass regulations deaths of sea snakes caught and discarded in trawl fisheries in Australia [47] and

accidental snare captures in Newfoundland of endangered marten (Martes

to protect highly desirable species when exploitation

americana) while snowshoe hares (Lepus americanus) are targeted [48].

can expand to other species.

Incidental exploitation: this mode involves the exploitation of less desirable

species when commingled with the target species (e.g., Figure 5 in [4]). In

Pathways to extinction by exploitation 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-

Humans are by far the biggest drivers of extinction, both

resilient species [49–52]. Speciﬁc examples include the incidental bycatch of

directly and indirectly [1]. Yet extinction through exploi- shark species in longline ﬁsheries for tuna and swordﬁsh [53] and the near

extirpation of common skate (Dipturus batis) in the Irish Sea when caught by

tation seems paradoxical: how can this be proﬁtable given

trawlers targeting more valuable and abundant species such as cod [42,54].

the exorbitant costs of targeting rare species? Two previous

Opportunistic exploitation: the exploitation of a scarce but desirable species,

hypotheses suggest ways in which this could be proﬁtable, when encountered while targeting other less desirable but more common

species. Exploitation is only proﬁtable because of the presence of the less

but here we expand on another exploitation mode termed

desirable species. The term was originally coined as ‘opportunistic depletion’

opportunistic exploitation (see Glossary) that arguably

[8]. Opportunistic exploitation allows for continued exploitation at densities

offers a much more widespread pathway to extinction. below the bioeconomic equilibrium [55], when proﬁt (income minus expenses)

is the same as from available alternatives. In the single-species case, humans

One previous hypothesis, the ‘economics of overexploi-

should logically cease exploitation at this point. However, where multiple species

tation’ [2], contends that when population growth rates are

can be exploited in the same habitat, humans will often ﬁrst deplete the most

low relative to monetary returns on investments, exploi- desirable species, depleting it to the point of bioeconomic equilibrium, before

switching to less desirable species. The crux of opportunistic exploitation is that

ters could maximize their net present value by catching the

at this point the sparse but desirable species can continue to be taken opportu-

entire population, banking the money, and living off the

nistically whenever it is encountered, providing an unexpected bonus to the

comparatively high interest. The applicability of this hy- exploiter. The deﬁnition of ‘opportunistic’ involves ‘exploiting circumstances or

opportunities to gain immediate advantage, rather than following a predeter-

pothesis has recently been challenged: even for very un-

mined plan. . .; especially with the implication of cynicism or a lack of regard to

productive species, catching the last individual would be principles’ (Oxford English Dictionary, http://www.oed.com). Thus, opportunistic

too costly to maximize net present value [3]. exploitation carries the dual connotations of being both unplanned and selﬁshly

targeting an already depleted species.

An alternative hypothesis is the ‘anthropogenic Allee

Targeted exploitation: this is the most common mode, which occurs when one or

effect’, which notes that humans place exaggerated value a few species are the primary subjects of resource extraction. Examples include

trophy hunting for wild goats (subfamily Caprinae) [5] and diving for black-lip

on species as they become rare, allowing proﬁtable exploi-

abalone (Haliotis rubra) in Australia [56].

tation at very low population sizes [4,5]. For example, the

traditional Chinese medicine market generates intense

Key differences between exploitation modes

demand for products from rare fauna such as rhinoceroses

Exploitation mode Value of species Primary target?

and tigers [6]. One instance of this demand is for the

Opportunistic Higher than target No

Targeted Proﬁtable Yes

Corresponding author: Branch, T.A. ([email protected]). Incidental Lower than target No

0169-5347/$ – see front matter Accidental No value No

Trends in Ecology & Evolution, July 2013, Vol. 28, No. 7 409

Opinion Trends in Ecology & Evolution July 2013, Vol. 28, No. 7

50 World War II Humpback Subsidy from other species 40 No subsidy from other species Sperm 30

OE 0 20 Fin Economic rent

EB Total catch (thousands) 10 Antarcc blue Loss Proﬁt

Stock biomass 0 1940 1950 1960 TRENDS in Ecology & Evolution

Year

Figure 1. Economics of opportunistic exploitation (OE). Curves show hypothesized

TRENDS in Ecology & Evolution

changes in economic rent (revenue minus costs) at varying biomass levels of high-

value species in multispecies (top curve) and single-species (lower curve)

Figure 2. Opportunistic exploitation of the Antarctic blue whale (Balaenoptera

exploitation systems. Subsidy from other species permits opportunistic

musculus intermedia) demonstrated by the number of whales caught annually by

exploitation of the high-value stock because there is no bioeconomic equilibrium

pelagic whalers in the Southern Hemisphere from 1932 to 1963. During this period,

(EB) at which exploitation is unprofitable.

whalers shifted their focus from Antarctic blue whales to target lower-value and

more abundant species, particularly fin whales (Balaenoptera physalus) and sperm

whales (Physeter macrocephalus). Although Antarctic blue whales were too scarce

to support a target whaling industry, they were targeted opportunistically

Both the economics of overexploitation and the anthro-

whenever they were encountered, resulted in depletion to near-extinction. Small

pogenic Allee effect hypotheses offer explanations of how

catches of other species have been excluded. The comparative scale of the whale

exploitation focused on a single species (target exploita- drawings is indicative. Whale drawings reproduced with permission from

Greennature.

tion) 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 fewer than 200 in 1963 as the population size plum-

and incidental exploitation of species with lower value meted [10]. However, this was not due to targeted exploi-

while pursuing target species. We contend that a further tation, which would never have been proﬁtable at such low

pathway occurs when rare, high-value species are encoun- population sizes. By the 1950s, proﬁts ﬂowed from less

tered during the exploitation of more common target spe- sought-after but more abundant species, particularly ﬁn

cies. We term this largely unrecognized mode opportunistic whales, whereas Antarctic blue whales comprised only 3%

exploitation [8]. This pathway allows critically sparse but of all catches (Figure 2). Thus, it was opportunistic whaling

valuable species to be proﬁtably exploited when they are that reduced the abundance of Antarctic blue whales to

encountered while targeting abundant but lower-value 0.15% of pre-whaling levels [10], before international reg-

species in the same habitat (Figure 1). Note that opportu- ulations ﬁnally halted the slaughter.

nistic exploitation is more pernicious than incidental or Multispecies trawl ﬁsheries are also prone to opportu-

accidental exploitation, because the depleted species has nistic exploitation. For example, in India, trawl ﬁsheries

high value, which results in stronger economic incentives began by targeting valuable shrimp, cephalopods, and

for further exploitation. Opportunistic exploitation exam- large ﬁshes such as snapper and grouper in the 1950s,

ples from disparate habitats, scales of exploitation, and primarily for export. After these were depleted, trawlers

trophic levels now provide compelling support for this shifted focus to lower-value ﬁsh such as croakers and

extinction pathway. sardines for domestic markets, including the traditionally

discarded bycatch comprising small-bodied animals with

Marine examples of opportunistic exploitation lower consumer preference, called ‘trash ﬁsh’. In India and

Antarctic blue whales were used as the key example many other parts of South and Southeast Asia, trash ﬁsh

exemplifying the economics of overexploitation by Colin are now processed to ﬁshmeal and used as a protein

Clark [2], but ironically exemplify opportunistic exploita- supplement in the poultry and aquaculture industry.

tion. As quoted within the original article [2]: ‘Gulland The extra subsidy received from these former discards

[pers. comm.] has pointed out to me that ﬁshing for the (Figure 3) has allowed trawlers to further deplete high-

Antarctic blue whale probably would have become uneco- value species whenever they are encountered [11].

nomical several years earlier had it not been for the Opportunistic exploitation also occurs in small-scale sea

simultaneous occurrence of ﬁnback whales in the same cucumber ﬁsheries where multiple species are targeted [8].

area.’ This view is even held by Clark himself in a recent Sea cucumbers feature prominently in Asian medicinal

book, where he writes that targeting Antarctic blue whales markets and banquet dishes [12]. In sea cucumber ﬁsher-

was effectively a zero-cost activity subsidized by the ex- ies, one or two high-value species are often ﬁshed to low

ploitation of ﬁn whales [9]. The underlying story is that levels before ﬁshers shift to lower-value species in the same

Antarctic blue whales were heavily depleted by pelagic grounds and then the high-value species continue to be

whalers, who caught 28,000 in 1930 but only 7000 in 1950 ﬁshed while lower-valued species are targeted. In unﬁshed

410

Opinion Trends in Ecology & Evolution July 2013, Vol. 28, No. 7

(A) (B) (C)

(D) (E) (F)

TRENDS in Ecology & Evolution

Figure 3. Case studies demonstrating opportunistic exploitation. (A) Poachers caused the extinction of the black rhinoceros (Diceros bicornis) in Zambia despite focusing

mainly on elephants. Photograph (from Namibia) by Rob Wilkinson (www.Wilkinsonsworld.com). (B) Formerly discarded, trash fish caught in Indian shrimp trawl fisheries

are now auctioned in piles at the dock, effectively subsidizing continued exploitation of rarer high-value species. Photograph by Aaron Lobo. (C) Illegal trapping of babirusa

(Babyrousa celebensis) while the more common Sulawesi wild pig is targeted has depleted babirusa populations to vulnerable levels. Photograph by Pauli Hien. (D) The

prickly redfish (Thelenota ananas), one of many high-value coral reef sea cucumber species collected in small-scale multispecies fisheries, has been depleted

opportunistically from East Africa to the Central Pacific. Photograph by Steven Purcell. (E) Reductions by 93–95% of big-leaf mahogany (Swietenia macrophylla) by initial

logging are exacerbated by subsequent waves of loggers targeting the remaining species. Photograph by James Grogan. (F) The Antarctic blue whale (Balaenoptera

musculus intermedia) was depleted to less than 1% of its original numbers by opportunistic whaling by whalers targeting more abundant but less valuable fin whales and

other species. Photograph by Isabel Beasley.

areas, high-value sea cucumber species (Figure 3) are the 1980s, despite an economic analysis showing this was

naturally common and widely distributed, but in areas unproﬁtable due to their rarity [20]. However, poachers

subject to multispecies sea cucumber ﬁsheries they are could make a living by targeting elephants, which were ten

often critically overﬁshed [13]. Conversely, in single-spe- times more abundant, while poaching black rhinoceroses

cies sea cucumber ﬁsheries in Alaska, Iceland, New Zeal- when they were encountered [20]. By the end of the 20th

and, British Columbia, Newfoundland and Labrador, century, black rhinoceroses were extinct not just in the

Washington, and eastern Russia, where there are no other Luangwa Valley, but in all of Zambia [21].

sea cucumber species to support opportunistic exploita- Similarly, hunters in the Indonesian island of Sulawesi

tion, even high-value sea cucumber species have not been use snares to trap abundant Sulawesi wild pigs (Sus

heavily depleted [8]. In other words, economic value must celebensis), but this allows them simultaneously to poach

be coupled with the presence of more abundant but less another wild pig, the rare babirusa (Babyrousa celebensis)

desirable species to subsidize the chronic depletion of sea (Figure 3) [22], which would otherwise not be proﬁtable to

cucumber stocks. hunt. Although the babirusa are legally protected, they

Given these examples, we argue that this switch from are caught more easily by the snares and thus even a small

targeted exploitation to opportunistic exploitation [14] is amount of trapping of Sulawesi wild pigs can eliminate

probably widespread in marine and freshwater environ- babirusa from an area. Rowcliffe et al. make use of word-

ments. For example, overﬁshing of Napoleon wrasse (Chei- play to describe this example as ‘piggyback extinction’

linus undulatus) [15], white abalone (Haliotis sorenseni) [23]. Bushmeat hunting in Equatorial Guinea and Ghana

[16], and freshwater populations of lake trout (Salvelinus also displays classic signs of opportunistic exploitation,

namaycush) and walleye (Stizostedion vitreum) [17] were with more abundant smaller animals maintaining proﬁt-

all likely to have been exacerbated because ﬁshing could able hunting while larger, rare, and more valuable ani-

continue on other species in the same habitat. We also mals are still hunted whenever they are encountered

speculate that examples of opportunistic exploitation [24,25].

might include the extinctions of Steller’s sea cow (Hydro- Selective logging of big-leaf mahogany (Swietenia

damalis gigas) [18] and the Caribbean monk seal (Mon- macrophylla) also exempliﬁes opportunistic exploitation.

achus tropicalis) [19]. In the Brazilian Amazon, these highly valued lumber trees

are found at low densities, but logging removes 93–95% of

Terrestrial case studies commercial-sized trees [26]. Further waves of logging for

Terrestrial systems also provide examples of opportunistic low-value species ensures that big-leaf mahogany missed

exploitation. For instance, black rhinoceroses (Figure 3) during the ﬁrst wave are eradicated [27], leading to sim-

were illegally poached in the Luangwa Valley, Zambia in pliﬁed forests containing only low-value species.

411

Opinion Trends in Ecology & Evolution July 2013, Vol. 28, No. 7

There are likely to be many more terrestrial examples of resources can lead to economically rational overexploita-

opportunistic exploitation, from both the past and the tion. Managers should pay special attention to rare species

present. Possible candidates include the present-day de- that are highly valuable and institute protocols to limit and

pletion of Madagascar rosewood (Dalbergia spp.) [28], the monitor trade. For example, Papua New Guinea has an

near-extinction of American bison (Bison bison) [29], and export ban on seven species of birdwings, the largest

the extinctions of South African blue antelope (Hippotra- butterﬂies in the world, due to their rarity and the global

gus leucophaeus) [30] and New Zealand moa species (Aves, demand from collectors [41]. Another useful policy is to

Dinornithiformes) [31]. develop shortlists of allowed species [8], instead of impos-

ing species bans that inevitably are developed too late to

Parallels in ecological theory avoid depletion from opportunistic exploitation. The short-

Opportunistic exploitation might thus be a widespread but lists could include common exploitable species but exclude

overlooked phenomenon wherever humans exploit multi- threatened high-value species and others that are not

ple species together, with some ecological parallels in the targeted to preserve ecosystem functioning. Used in this

general ﬁeld of ‘apparent competition’ where the abun- manner, shortlists would prevent the future expansion of

dance of two prey species becomes linked through shared exploitation to new species before they can be assessed.

predators, affecting predator functional responses [32]. Naturally, trade restrictions and shortlists should be based

Multispecies models invoking apparent competition can on sound taxonomy, to ensure that the diagnosis of extinc-

explain how early hunters caused the mass extinction of tion risk is not clouded by cryptic species that are part of

large mammals in North America, whereas models based undetected species complexes [42]. Another pitfall to avoid

on a single prey species cannot [33,34]. For instance, is a group quota for the exploitation of multiple similar

common forms of functional response in predators can species. The International Whaling Commission initially

act to keep one prey species in a low-abundance ‘predator set an annual quota on the weighted catch of all species of

pit’ [35,36] whereby, if they increase, predators will start large whales combined, which contributed greatly to the

targeting them and keep their numbers depressed, but at decline of individual species, including Antarctic blue

low densities predators no longer maintain a search image whales. Instead, sustainable individual-species quotas

for that species and switch to other prey species [37]. should be set wherever quotas can be practically estab-

Unlike most natural predators, however, humans main- lished, monitored, and enforced.

tain and even increase their desire to target high-value Related to the idea of individual quotas for species is the

species when they are encountered at low densities [5], so proposal for balanced ﬁsheries exploitation, where catches

there is no refuge in rarity. are spread broadly across a range of species while care is

‘Hyperpredation’ in natural systems is also somewhat taken to ensure that exploitation rates for individual spe-

analogous to opportunistic exploitation. Hyperpredation cies remain in proportion to their productivity [43,44].

occurs when one prey source increases, subsidizing higher Fishers are capable of applying this approach in multispe-

predator populations, which in turn cause declines in cies ﬁsheries, provided there are sufﬁcient incentives to

alternative prey populations [38]. This is typiﬁed by target and avoid particular species, but this requires near-

declines and extinctions of native Australian rodents, 100% enforcement and monitoring [45]. The danger of the

where feral cats and other predators subsidize their diets balanced-exploitation approach is that expanding catches

with introduced rabbits and mice [38], and by the declines to new species acts as a subsidy for the continued exploi-

of island foxes in the California Channel Islands due to tation of current species, as seen in our example of multi-

introduced pigs providing a steady food source for preda- species trawl ﬁsheries in India.

tory golden eagles [39]. However, whereas hyperpredation In addition to these speciﬁc policy ideas to mitigate

requires an increase in alternative prey, opportunistic opportunistic exploitation, there are a number of familiar

exploitation can happen even when the abundance of policies that are also needed. For instance, ideally, species

alternative prey is constant or declining. should be regulated by limiting the amount exploited and

not the amount of effort expended (a surprisingly common

Implications for conservation and policy regulation in ﬁsheries). Terrestrial and marine reserves

Management and conservation policies need to identify should be set aside where no extractive exploitation is

species at risk of opportunistic exploitation and take steps allowed, to serve as a refuge against opportunistic exploi-

to avoid their potential depletion and extinction. Past tation. Finally, all regulations are moot without effective

studies have focused on attributes of each species in isola- monitoring and enforcement to deter illegal exploitation.

tion to predict their risk of extinction: factors such as life-

history traits, overexploitation, loss of habitat, disease, Concluding remarks

rates of decline, abundance, and geographic range [4,40]. Examples from ﬁshing, hunting, and logging demonstrate

We argue that multispecies attributes are also important; that opportunistic exploitation is a pervasive pathway to

the risk of opportunistic exploitation not only depends on depletion and extinction wherever multiple species are

the value of the species in question, but is also linked to the exploited. We anticipate that further examples of opportu-

presence of co-occurring lower-value species that could nistic exploitation, both historically and in the present, will

subsidize continued exploitation. come to light wherever humans exploit natural resources.

There are several speciﬁc management actions that can For example, opportunistic exploitation might arise in spear-

be taken to overcome opportunistic exploitation. One key ﬁshing, in trapping, and in the process of collecting bird eggs,

realization is that private ownership of multispecies orchids, mushrooms, insects, shells, and ornamental corals

412

Opinion Trends in Ecology & Evolution July 2013, Vol. 28, No. 7

potential for post-logging recovery in the Brazilian Amazon. Forest

[46]. Policy efforts should focus on conserving rare, high-

Ecol. Manag. 255, 269–281

value species exploited within multispecies systems, to avoid

27 Grogan, J. et al. (2010) Over-harvesting driven by consumer demand

scenarios where subsidy by lower-value species allows a

leads to population decline: big-leaf mahogany in South America.

proﬁtable pathway that drives species toward extinction. Conserv. Lett. 3, 12–20

28 Barrett, M.A. et al. (2010) CITES designation for endangered rosewood

Acknowledgments in Madagascar. Science 328, 1109–1110

29 Lueck, D. (2002) The extermination and conservation of the American

The authors thank Daniel Schindler, Ray Hilborn, Jim Kitchell, and

bison. J. Legal Stud. 31, S609–S652

Nicholas Dulvy for helpful comments on earlier drafts that greatly

30 Kerley, G.I.H. et al. (2009) Extinction of the blue antelope Hippotragus

improved the manuscript.

leucophaeus: modeling predicts non-viable global population size as the

primary driver. Biodivers. Conserv. 18, 3235–3242

References 31 Anderson, A. (1989) Mechanics of overkill in the extinction of New

1 Diamond, J.M. (1989) The present, past and future of human-caused Zealand moas. J. Archaeol. Sci. 16, 137–151

extinctions. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 325, 469–477 32 Holt, R.D. (1977) Predation, apparent competition, and the structure of

2 Clark, C.W. (1973) The economics of overexploitation. Science 181, prey communities. Theor. Popul. Biol. 12, 197–229

630–634 33 Alroy, J. (2001) A multispecies overkill simulation of the end-

3 Grafton, R.Q. et al. (2007) Economics of overexploitation revisited. Pleistocene megafaunal mass extinction. Science 292, 1893–1896

Science 318, 1601 34 Alroy, J. (2001) Did human hunting cause mass extinction? Response.

4 Dulvy, N.K. et al. (2003) Extinction vulnerability in marine Science 294, 1459–1462

populations. Fish Fish. 4, 25–64 35 Holling, C.S. (1965) The functional response of predators to prey

5 Courchamp, F. et al. (2006) Rarity value and species extinction: the density and its role in mimicry and population regulation. Mem.

anthropogenic Allee effect. PLOS Biol. 4, e415 Entomol. Soc. Can. 45, 5–60

6 Graham-Rowe, D. (2011) Endangered and in demand. Nature 480, 36 Bakun, A. (2006) Wasp-waist populations and marine ecosystem

S101–S103 dynamics: navigating the ‘‘predator pit’’ topographies. Prog.

7 Sadovy, Y. and Cheung, W.L. (2003) Near extinction of a highly fecund Oceanogr. 68, 271–288

ﬁsh: the one that nearly got away. Fish Fish. 4, 86–99 37 Smout, S. et al. (2010) The functional response of a generalist predator.

8 Purcell, S.W. et al. (2013) Sea cucumber ﬁsheries: global analysis of PLOS ONE 5, e10761

stocks, management measures and drivers of overﬁshing. Fish Fish. 14, 38 Smith, A.P. and Quin, D.G. (1996) Patterns and causes of extinctions and

34–59 decline in Australian conilurine rodents. Biol. Conserv. 77, 243–267

9 Clark, C.W. (2006) The Worldwide Crisis in Fisheries: Economic Models 39 Roemer, G.W. et al. (2002) Golden eagles, feral pigs, and insular

and Human Behavior. Cambridge University Press carnivores: how exotic species turn native predators into prey. Proc.

10 Branch, T.A. et al. (2004) Evidence for increases in Antarctic blue Natl. Acad. Sci. U.S.A. 99, 791–796

whales based on Bayesian modelling. Mar. Mamm. Sci. 20, 726–754 40 Mace, G.M. et al. (2008) Quantiﬁcation of extinction risk: IUCN’s

11 Lobo, A.S. et al. (2010) Commercializing bycatch can push a ﬁshery system for classifying threatened species. Conserv. Biol. 22, 1424–1442

beyond economic extinction. Conserv. Lett. 3, 277–285 41 Slone, T.H. et al. (1997) A comparison of price, rarity and cost of

12 Clarke, S. (2004) Understanding pressures on ﬁshery resources butterﬂy specimens: Implications for the insect trade and for

through trade statistics: a pilot study of four products in the habitat conservation. Ecol. Econ. 21, 77–85

Chinese dried seafood market. Fish Fish. 5, 53–74 42 Igle´sias, S.P. et al. (2010) Taxonomic confusion and market

13 Friedman, K. et al. (2011) Management of sea cucumber stocks: mislabelling of threatened skates: important consequences for their

patterns of vulnerability and recovery of sea cucumber stocks conservation status. Aquat. Conserv.: Mar. Freshwat. Ecosyst. 20,

impacted by ﬁshing. Fish Fish. 12, 75–93 319–333

14 Kim, J. (2010) Opportunistic versus target mode: prey choice changes in 43 Zhou, S. et al. (2010) Ecosystem-based ﬁsheries management requires

central-western Korean prehistory. J. Anthropol. Archaeol. 29, 80–93 a change to the selective ﬁshing philosophy. Proc. Natl. Acad. Sci.

15 Sadovy, Y.J. and Vincent, A.C.J. (2002) Ecological issues and the trades U.S.A. 107, 9485–9489

in live reef ﬁshes. In Coral Reef Fishes: Dynamics and Diversity in a 44 Garcia, S.M. et al. (2012) Reconsidering the consequences of selective

Complex Ecosystem (Sale, P.F., ed.), pp. 391–420, Academic Press ﬁsheries. Science 335, 1045–1047

16 Hobday, A.J. et al. (2001) Over-exploitation of a broadcast spawning 45 Branch, T.A. and Hilborn, R. (2008) Matching catches to quotas in a

marine invertebrate: decline of the white abalone. Rev. Fish Biol. Fish. multispecies trawl ﬁshery: targeting and avoidance behavior under

10, 493–514 individual transferable quotas. Can. J. Fish. Aquat. Sci. 65, 1435–1446

17 Post, J.R. et al. (2002) Canada’s recreational ﬁsheries: the invisible 46 Salafsky, N. et al. (2008) A standard lexicon for biodiversity

collapse? Fisheries 27, 6–17 conservation: uniﬁed classiﬁcations of threats and actions. Conserv.

18 Anderson, P.K. (1995) Competition, predation, and the evolution and Biol. 22, 897–911

extinction of Steller’s sea cow, Hydrodomalis gigas. Mar. Mamm. Sci. 47 Rasmussen, A.R. et al. (2013) Marine reptiles. PLOS ONE 6, e27373

11, 391–394 48 Thompson, I.D. (1991) Could marten become the spotted owl of eastern

19 McClenachan, L. and Cooper, A.B. (2008) Extinction rate, historical Canada? Forest. Chron. 67, 136–140

population structure and ecological role of the Caribbean monk seal. 49 Ricker, W.E. (1958) Maximum sustained yields from ﬂuctuating

Proc. Biol. Sci. 275, 1351–1358 environments and mixed stocks. J. Fish. Res. Board Can. 15, 991–1006

20 Milner-Gulland, E.J. and Leader-Williams, N. (1992) A model of 50 Paulik, G.J. et al. (1967) Exploitation of multiple stocks by a common

incentives for the illegal exploitation of black rhinos and elephants: ﬁshery. J. Fish. Res. Board Can. 24, 2527–2537

poaching pays in Luangwa Valley, Zambia. J. Appl. Ecol. 29, 388–401 51 Hilborn, R. (1976) Optimal exploitation of multiple stocks by a common

21 Chomba, C. and Matandiko, W. (2011) Population status of black and ﬁshery: a new methodology. J. Fish. Res. Board Can. 33, 1–5

white rhinos in Zambia. Pachyderm 50, 50–55 52 Worm, B. et al. (2009) Rebuilding global ﬁsheries. Science 325, 578–585

22 Clayton, L. et al. (1997) Bringing home the bacon: a spatial model of 53 Megalofonou, P. et al. (2005) Incidental catch and estimated discards of

wild pig hunting in Sulawesi, Indonesia. Ecol. Appl. 7, 642–652 pelagic sharks from the swordﬁsh and tuna ﬁsheries in the

23 Rowcliffe, J.M. et al. (2003) A model of human hunting impacts in Mediterranean Sea. Fish. Bull. 103, 620–634

multi-prey communities. J. Appl. Ecol. 40, 872–889 54 Brander, K. (1981) Disappearance of common skate Raia batis from

24 Bennett, E. et al. (2012) Why is eating bushmeat a biodiversity crisis? Irish Sea. Nature 290, 48–49

Conserv. Pract. 3, 28–29 55 Gordon, H.S. (1954) The economic theory of a common-property

25 Cowlishaw, G. et al. (2005) Evidence for post-depletion sustainability in resource: the ﬁshery. J. Polit. Econ. 62, 124–142

a mature bushmeat market. J. Appl. Ecol. 42, 460–468 56 Leiva, G.E. and Castilla, J.C. (2002) A review of the world marine

26 Grogan, J. et al. (2008) What loggers leave behind: Impacts on big-leaf gastropod ﬁshery: evolution of catches, management and the Chilean

mahogany (Swietenia macrophylla) commercial populations and experience. Rev. Fish Biol. Fish. 11, 283–300

413