SEARCH

SEARCH BY CITATION

Keywords:

  • aviculture;
  • bird species;
  • captive breeding;
  • conservation priorities;
  • IUCN Red List;
  • threatened species;
  • zoos

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Given the increasing rapprochement between aviculture and conservation organizations and the escalating global crisis in species conservation, we enumerate the avian taxa that are subject to, or might most appropriately be considered for, conservation-breeding programmes. Although the overall total, at 257, is only 2·6% of the extant global avifauna, the role for zoos remains crucial. Of this total, captive breeding is judged ‘Necessary’ or ‘Integral’ to conservation efforts for 45 spp (18%); for the great majority, it is regarded as ‘Precautionary’ or ‘Prudent’ [192 spp (75%)], and for the remainder it is recommended either as a showcase for in situ efforts [3 spp (1%) – although this proportion could be larger] or to deflect pressure from wild populations by the market-driven supply of captive-bred individuals [17 spp (7%)]. For the 8–21% of these species for which captive populations may not already exist, more detailed assessment is required prior to attempting to establish ex situ populations. Avicultural institutions preparing to rise to these challenges should recognize that: (1) the taking of birds into captivity should not provide an excuse to developers to continue unchecked with whatever activity threatens the species in question; (2) species recovery programmes driven primarily by conservation-breeding interests may need a more holistic agenda that develops the in situ component; (3) success has so far been elusive in several ‘Necessary’ cases (in which failure would lead almost certainly to extinction); (4) a delicate balance is needed between leaving ex situ management too late and starting it too early; (5) choice of species will depend not only on biological need but also on factors relating to the individual institution; (6) our recommendations are simply to consider conservation breeding for the species listed here that are not already in programmes; (7) speed of reaction is of the essence once the decision is clear; (8) new priorities will constantly arise, in some cases deriving from taxonomic revisions.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

It is slightly disconcerting to discover that opinions about the value and relevance of captive breeding to bird conservation were in conflict as long as 80 years ago.

If all the survivors of a certain rare form were caged, their descendants … in a few generations probably would depart from natural conformation and colour to such an extent as not to be typical of the species. The latter would then be almost as truly extinct as if the last individual had perished in the wild. The place to save threatened species is in their native range … (McAtee, 1935; our italics).

Thus spake the Principal Biologist with the US Biological Survey in response to a proposal to establish aviaries for the captive breeding of parrots in California. He seems, in a sense, to have been well ahead of his time, for the place of captive breeding in conservation only became seriously controversial in the mid-to-late1980s and early 1990s, when institutions and individuals were settling their positions in relation to the steadily emerging authority of the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES), which (for example), although coming into force in 1975, only established its Animals Committee in 1987.

The advent of CITES, which for conservation purposes seeks to restrict the species and numbers of birds in commerce between nations, was a challenge to private aviculturists and the great majority of zoos to justify their interests and activities far more explicitly. Examining their various, usually piecemeal responses to it, conservationists pressed them further (e.g. Imboden, 1987; Snyder et al., 1996). The aviculturists, initially resistant and resentful, saw their cause suffer irreparable damage in the mid-1990s when two figures accorded iconic status by their respective avicultural communities (T. Silva, USA; H. Sissen, UK) went to prison for trafficking threatened parrots (Lowther et al., 2002). By contrast, zoos, confronted with their limitations and opportunities (e.g. Mallinson, 1991; Rahbek, 1993; Balmford et al., 1995, 1996; Sheppard, 1995), moved steadily towards a greater engagement with in situ conservation initiatives while beginning to embrace the role of public awareness and education (Conway, 2003; Tribe & Booth, 2003; Redford et al., 2012). In synergistic response, the conservation movement has started to interact much more comfortably and constructively with zoos, as exemplified by the programmes of Zoologische Gesellschaft für Arten- und Populationsschutz in Germany and Conservation des Espèces et des Populations Animales in France.

This growing rapprochement could hardly be more timely. The number of species of bird threatened with extinction is increasing every year (Butchart et al., 2004; BirdLife International, 2013); and there is a parallel growth in the perception that not all of these species can be saved, as McAtee (1935) maintained, ‘in their native range’. Ineluctable pressures from alien invasive species, hunters, trappers/traders and ‘developers’ in all their guises mean that in some cases the most appropriate conservation measure has been or may be to establish a population in captivity while the main threat to the species is, if feasible, addressed. Therefore, if aviculture (whether in public zoos or private establishments) is to play a significant conservation role, it is clearly of cardinal importance to establish which are the species it should be targeting for its ex situ programmes. This paper is intended as a further step on the way to identifying such species.

The term ‘conservation breeding’ was adopted in the 1990s to reflect the circumstance when captive breeding is undertaken for conservation purposes, and we use it in our title and conclusions. Nevertheless, even in contexts where conservation is the guiding principle, for the most part we continue to use the humbler term ‘captive breeding’ simply to distinguish the discipline and practice of nurturing animals successfully through the reproductive cycle in captivity. By dint of this definition, we exclude from this review swiftlet nest-farming, which involves providing buildings for wild birds (although it may alleviate pressure on natural cave colonies), and species subject to clutch manipulation, in which wild-laid eggs are taken and incubated, and the young reared until they can be safely released into the wild, as is practised with various species; for example, the kiwis Apterygidae of New Zealand, Piping plover Charadrius melodus in the Great Lakes and Mauritius olive white-eye Zosterops chloronothus (BirdLife International, 2012).

A final preliminary point to stress is that the identification here of species for potential ex situ management is not a blanket invitation to aviculture to deploy in force on their behalf. All initiatives to assist these species, including (and in particular) those involved in supplying a market demand, need to be scrupulously observant of ethical standards, local and national sensitivities, precise conservation needs and all relevant legal requirements. The issue of ownership of birds being taken into captivity, particularly if leaving the country of origin, is vital to settle transparently and equitably.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

As part of its evaluations of the extinction risk of all bird species for the International Union for Conservation of Nature (IUCN) Red List, BirdLife International codes up the priority actions required for all threatened species; that is, those in the IUCN Red List categories Critically Endangered (CR), Endangered (EN) and Vulnerable (VU), plus those classified as Extinct in the Wild (EW) and Near Threatened (NT), using the IUCN-Conservation Measures Partnerships (CMP) Conservation Actions Classification Scheme (http://www.iucnredlist.org/technical-documents/classification-schemes/conservation-actions-classification-scheme-ver2; Salafsky et al., 2008). We extracted the species for which captive breeding is coded as a priority action and cross-checked these against the text fields in the Red List assessments (updated annually at http://www.birdlife.org/datazone/species/search), which draw on King (1978–1979 1981), Collar & Stuart (1985), Collar et al. (1992, 2001) and Stattersfield & Capper (2000), adding any for which the coding had been inadvertently omitted. We supplemented this list through further literature review, including species action plans, recovery programme reports and relevant websites, particularly for threatened species that appeared to be potential candidates for captive breeding. [For all additional cases we found, updated text fields and coding will appear online at http://www.birdlife.org/datazone/species in the 2013 update to BirdLife International (2012)]. We scored these species as requiring captive breeding in all cases where we (or the authors of the Red List assessments) judged it likely that it would make a significant (i.e. recognizably important and relevant) contribution to their conservation in the short- to medium-term future. We did not consider additional species listed on CITES appendices or by Taxon Advisory Groups of the Association of Zoos and Aquariums (although there is potentially a place for such species in the ‘Motivational’ class: see Discussion); nor did we consider species for which captive breeding may have been important or useful in the past but is no longer required (e.g. Black robin Petroica traversi: Aikman et al., 2001). We also noted which of these species are already known from captivity, recording as uncertain a small proportion of cases where there was doubt, and excluding cases where the evidence suggested that numbers in captivity were very small and/or that the information was seemingly out of date. For obvious reasons, establishing that a species is not in captivity is far more difficult than the opposite.

Two minor modifications were made to the taxonomy of BirdLife International (2012), to account for the splitting of Houbara bustard into two species Chlamydotis undulata and Chlamydotis macqueenii, and the synonymizing of Vietnamese pheasant Lophura hatinhensis with Edwards's pheasant Lophura edwardsi. Both these revisions are due to appear in the 2013 update to BirdLife International (2012), with justifications.

We then identified a set of six classes of purpose or value by which captive breeding could be justified from a conservation perspective (Table 1) and assigned species to one of these classes, based on published information on their population size, trends, distribution, nature and intensity of threats, history and success (including ex situ in particular) of conservation interventions, and conservation capacity within their natural ranges. It should, however, be noted that both objectivity and accuracy of this classification diminish with order of class. While ‘Necessary’ is fairly rigidly defined by the fact that conservationists possess no alternative, the borders between ‘Integral’, ‘Precautionary’, ‘Prudent’ and even ‘Motivational’ are less clear, in part because of our own predictably incomplete knowledge of the programmes, and in part because the programmes themselves must constantly be adjusting and adapting to the progress and problems of both in situ and ex situ endeavours.

Table 1. Classes of conservation-breeding programmes with their definitions
ClassDefinition
Necessaryprogrammes without which species would have or will become extinct, because they are or were extinct in the wild or extremely close to being so; captive breeding is thus the primary conservation response
Integralprogrammes that make a key contribution to species conservation through supporting active or intended supplementation, reintroduction or benign introduction efforts
Precautionaryprogrammes that have deliberately been established as an insurance against future disaster, owing to the vulnerability of the species’ wild population, albeit without an explicit commitment to supplementation, reintroduction or benign introduction
Prudentprogrammes that manage or could manage a captive population as an insurance against future disaster, although not originally established for this purpose
Motivationalprogrammes that act as a showcase for in situ conservation projects, raising awareness and support for these, but contributing little or nothing directly
Commercialprogrammes that deflect trade pressure (e.g. capture for pets, falconry) from wild populations by the market-driven supply of captive-bred individuals; such captive breeding, although not typically practised by zoos or bird gardens, is not necessarily incompatible with their missions

The set of species was analysed in terms of IUCN Red List categories, landmass (distribution on continents, continental islands and oceanic islands), geographic regions and threats. The latter are coded in BirdLife International (2012) using the IUCN-CMP Threats Classification Scheme (http://www.iucnredlist.org/technical-documents/classification-schemes/threats-classification-scheme; Salafsky et al., 2008]) and are scored for timing, scope and severity, from which impact is calculated automatically (http://www.birdlife.org/datazone/info/spcthreat). Only ‘high-’ and ‘medium-’ impact threats were examined, and only the broad classes within the classification scheme were considered, with the exception of ‘biological resource use’, ‘natural system modifications’ and ‘invasive and other problematic species and diseases’, for which we considered the more specific types within the broad class.

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

Captive breeding is already under way or recommended for consideration as a conservation action for a total of 257 spp (2·6% of extant species; Table 2). For a relatively small proportion of these, captive breeding is classed as ‘Necessary’ [13 spp (5%)] or ‘Integral’ to conservation efforts [32 spp (13%)]; for the great majority, it is classed as ‘Precautionary’ [65 spp (25%)] or ‘Prudent’ [127 spp (49%)]; and for the remainder, it is recommended either as a showcase for in situ efforts [‘Motivational’, 3 exemplary species (1%)] or to deflect pressure from wild populations by the market-driven supply of captive-bred individuals [‘Commercial’, 17 spp (7%)] (Fig. 1). Among the first of these classes, it is apparent that captive breeding has been partly or solely responsible for preventing the extinction of nine species of bird (marked with an asterisk in Table 2) and that at least four others almost certainly depend entirely on this conservation tool for their survival (Table 2). In total, 181 (70%) of the species for which captive breeding is recommended are already known to be held in captivity, whereas 55 spp (22%) are not and 21 spp (8%) are unknown either way; these two latter groups are, as might be expected, more highly threatened than those known to be held in captivity [60 of 76 spp (78·9%) are CR or EN vs 103 of 181 spp (56·9%)] and are more likely to be from oceanic islands [55 of 76 spp (72·4%) vs 65 of 181 spp (35·9%)].

figure

Figure 1. Proportion of species for which captive breeding is recommended for different conservation purposes (n = 257 species).

Download figure to PowerPoint

Table 2. Bird species for which conservation breeding is already under way or recommended for consideration. Taxonomy and nomenclature follow BirdLife International (2012). The list excludes recently unencountered species for which captive breeding has been advocated if any wild populations can be found. * Species for which captive breeding prevented extinction; † species for which the recommendation is in our view particularly tentative, for a variety of reasons; n, no; y, yes. IUCN Red List categories: CR, Critically Endangered (PE, Possibly Extinct; PEW, Possibly Extinct in the Wild); EN, Endangered; EW, Extinct in the Wild; NT, Near Threatened; VU, Vulnerable. Threats: AG, agriculture & aquaculture; CC, climate change & severe weather; DW, dams & water management/use; EM, energy production & mining; FI, fire & fire suppression; HD, human disturbance; HT, hunting & trapping; IA, invasive alien species/diseases; LO, logging & wood harvesting; PO, pollution; PN, problematic native species/diseases; RC, residential & commercial development; TR, transportation & service corridors; OT, other. Upper-case abbreviations indicate high/medium impact threats; for those species lacking these, low/negligible/unknown impact threats are indicated with lower-case abbreviations. Region: AF, Africa; AS, Asia; CA, Caribbean; CE, Central America; EU, Europe; Middle East & Central Asia; NA, North America; OC, Oceania; SA, South America
SpeciesCurrently known to be held in captivity2012 IUCN Red list CategoryThreatsRegion
NECESSARY (13 spp)    
Alagoas curassow    
 Mitu mitu*yEWag, htSA
Edwards's pheasant    
 Lophura edwardsiyCRAG, HT, LOAS
Hawaiian goose    
 Branta sandvicensis*yVUag, cc, hd, iaOC
Madagascar pochard    
 Aythya innotatayCRPOAF
California condor    
 Gymnogyps californianus*yCRht, ia, trNA
Guam rail    
 Gallirallus owstoni*yEWIAOC
Socorro dove    
 Zenaida graysoni*yEWIA, PNNA
Kakapo    
 Strigops habroptila*yCRiaOC
Spix's macaw    
 Cyanopsitta spixii*yCR (PEW)AG, HT, IASA
Javan green magpie    
 Cissa thalassinayCRAG, HT, LOAS
Hawaiian crow    
 Corvus hawaiiensis*yEWIA, PNOC
Bali starling    
 Leucopsar rothschildi*yCRHTAS
Black-winged starling    
  Sturnus melanopterusyCRHTAS
INTEGRAL (32 spp)    
White-winged guan    
 Penelope albipennisyCRAG, HT, LO, PNSA
Blue duck    
 Hymenolaimus malacorhynchosyENIAOC
Hawaiian duck    
 Anas wyvillianayENHD, IAOC
Campbell Islands teal    
 Anas nesiotisyENcc, iaOC
Northern bald ibis    
 Geronticus eremitayCRAG, HT, PN, RCAF, EU
Asian crested ibis    
 Nipponia nipponyENht, lo, ot, poAS
Mauritius kestrel    
 Falco punctatusyVUag, ia, lo, poAF
Cape vulture    
 Gyps coprotheresyVUAG, HTAF
Philippine eagle    
 Pithecophaga jefferyiyCRAG, LO, POAS
African houbara bustard    
 Chlamydotis undulatayVUAG, HTAF, EU
Asian houbara bustard    
 Chlamydotis macqueeniiyVUAG, HTAS, EU
Kagu    
 Rhynochetos jubatusyENFI, IAOC
Lord Howe woodhen    
 Gallirallus sylvestrisyENCC, IAOC
Takahe    
 Porphyrio hochstetteriyENag, cc, hd, ht, iaOC
Whooping crane    
 Grus americanayENTRNA
Black stilt    
 Himantopus novaezelandiaeyCRIA, PNOC
Shore plover    
 Thinornis novaeseelandiaeyENag, cc, hd, iaOC
Spoon-billed sandpiper    
 Eurynorhynchus pygmeusyCRHD, HT, IA, RCAS
Pink pigeon    
 Nesoenas mayeriyENIAAF
Negros bleeding-heart    
 Gallicolumba keayiyCRAG, LOAS
Mariana fruit-dove    
 Ptilinopus roseicapilla?ENAG, IAOC
Kaka    
 Nestor meridionalisyENIAOC
Malherbe's parakeet    
 Cyanoramphus malherbi?CRIAOC
Orange-bellied parrot    
 Neophema chrysogasteryCRAG, IA, RCOC
Mauritius parakeet    
 Psittacula equesyENIAAF
Puerto Rican amazon    
 Amazona vittatayCRCC, PNCA
Visayan hornbill    
 Penelopides paniniyENHTAS
Eastern bristlebird    
 Dasyornis brachypterus?ENFIOC
Blue-crowned laughingthrush    
 Garrulax courtoisiyCRHT, TRAS
Saddleback    
 Philesturnus carunculatusyNTiaOC
Puaiohi    
 Myadestes palmeriyCRcc, iaOC
Palila    
 Loxioides bailleui?CRCC, IAOC
PRECAUTIONARY (65 spp)    
Trinidad piping-guan    
 Pipile pipilenCRAG, HT, LOCA
Blue-billed curassow    
 Crax albertiyCRAG, EM, HT, RCSA
Red-billed curassow    
 Crax blumenbachiiyENAG, HTCE
Djibouti francolin    
 Francolinus ochropectusnCRAG, CC, HD, LO, POAF
Western tragopan    
 Tragopan melanocephalusyVUag, ht, lo, otAS, EU
Bornean peacock-pheasant    
 Polyplectron schleiermacheriyENag, ht, fi, loAS
Congo peafowl    
 Afropavo congensisyVUAG, HTAF
Laysan duck    
 Anas laysanensisyCRCC, IAOC
Meller's duck    
 Anas melleriyENAG, HD, HT, LOAF
Madagascar teal    
 Anas bernieriyENAG, HT, LOAF
Brown teal    
 Anas chlorotisyENCC, TROC
Brazilian merganser    
 Mergus octosetaceusyCRAG, DW, EM, HD, LOCE
Junin grebe    
 Podiceps taczanowskiinCRCC, DW, POCE
Hooded grebe    
 Podiceps gallardoinCRIACE
Dwarf olive ibis    
 Bostrychia bocageinCRHTAF
Madagascar fish-eagle    
 Haliaeetus vociferoidesnCRAG, HT, LOAF
White-rumped vulture    
 Gyps bengalensisyCRPOAS, EU
Indian vulture    
 Gyps indicusyCRPOAS, EU
Slender-billed vulture    
 Gyps tenuirostrisyCRPOAS
Okinawa rail    
 Gallirallus okinawaeyENag, cc, dw, ia, lo, rcAS
Siberian crane    
 Leucogeranus leucogeranusyCRAG, DW, RCAS, EU
Grenada dove    
 Leptotila wellsinCRAG, HD, IA, RCCA
Mindoro bleeding-heart    
 Gallicolumba platenaenCRHT, LOAS
Polynesian ground-dove    
 Gallicolumba erythroptera?CRAG, IAOC
Tooth-billed pigeon    
 Didunculus strigirostris?ENIAOC
Yellow-crested cockatoo    
 Cacatua sulphureayCRHT, LOAS
Philippine cockatoo    
 Cacatua haematuropygiayCRAG, CC, HT, LOAS
Uvea parakeet    
 Eunymphicus uvaeensisyENag, cc, ht, ia, loOC
Antipodes parakeet    
 Cyanoramphus unicoloryVUcc, iaOC
Norfolk Island parakeet    
 Cyanoramphus cookiiyCRIAOC
Night parrot    
 Pezoporus occidentalisnENag, ia, otOC
Socorro parakeet    
 Aratinga brevipesyENAG, IANA
Marquesan kingfisher    
 Todiramphus godeffroyinCRIA, LOOC
Tuamotu kingfisher    
 Todiramphus gambierinCRIAOC
Sulu hornbill    
 Anthracoceros montaninCRHT, LOAS
Mindoro hornbill    
 Penelopides mindorensisnENHT, LOAS
Rufous-headed hornbill    
 Aceros waldeniyCRHTAS
Stitchbird    
 Notiomystis cinctayVUag, iaOC
Crow honeyeater    
 Gymnomyza aubryananCRIA, PNOC
Regent honeyeater    
 Xanthomyza phrygiayCRAG, LO, PN, RCOC
Yellowhead    
 Mohoua ochrocephalayENIAOC
Kokako    
 Callaeas cinereusyENIAOC
Reunion cuckooshrike    
 Coracina newtoninCRHT, IAAF
Fatuhiva monarch    
 Pomarea whitneyinCRIAOC
Mariana crow    
 Corvus kubaryiyCRAG, HT, IA, PN, RCOC
Nightingale reed-warbler    
 Acrocephalus lusciniusnCRIAOC
Black-and-white laughingthrush    
 Garrulax bicoloryVUHT, LOAS
Rota bridled white-eye    
 Zosterops rotensisnCRAG, CC, IA, POOC
White-chested white-eye    
 Zosterops albogularisnCRIAOC
Golden white-eye    
 Cleptornis marcheiyCRIAOC
Floreana mockingbird    
 Mimus trifasciatus?CRCC, IASA
Socorro mockingbird    
 Mimus graysoninCRIANA
Olomao    
 Myadestes lanaiensisnCR (PE)IAOC
Mauritius fody    
 Foudia rubrayENIAAF
Nihoa finch    
 Telespiza ultimanCRCC, IAOC
Ou    
 Psittirostra psittaceanCR (PE)IAOC
Maui parrotbill    
 Pseudonestor xanthophrysnCRIAOC
Nukupuu    
 Hemignathus lucidusnCR (PE)IAOC
Akikiki    
 Oreomystis bairdi?CRIAOC
Oahu alauahio    
 Paroreomyza maculatanCR (PE)ag, cc, ia, rc, trOC
Akekee    
 Loxops caeruleirostrisnCRCC, IAOC
Akepa    
 Loxops coccineusyENIAOC
Akohekohe    
 Palmeria doleiyCRIAOC
Bahama oriole    
 Icterus northropinCRIACA
Montserrat oriole    
 Icterus oberiyCRCC, IA, PNCA
PRUDENT (127 spp)    
Southern brown kiwi    
 Apteryx australisyVUIAOC
Cauca guan    
 Penelope perspicaxyENHTSA
Black-fronted piping-guan    
 Pipile jacutingayENAG, DW, HTSA
Rufous-headed chachalaca    
 Ortalis erythropterayVUAG, HTSA
Horned guan    
 Oreophasis derbianusyENAG, HT, LOCE, SA
Wattled curassow    
 Crax globulosayENHTSA
Helmeted curassow    
 Pauxi pauxiyENHTSA
Blyth's tragopan    
 Tragopan blythiiyVUag, em, ht, lo, rc, trAS
Cabot's tragopan    
 Tragopan cabotiyVUag, ht, ia, loAS
Sclater's monal    
 Lophophorus sclateriyVUHTAS
Chinese monal    
 Lophophorus lhuysiiyVUia, otAS
Crestless fireback    
 Lophura erythrophthalmayVUAG, FI, HT, LOAS
Crested fireback    
 Lophura ignitayNTag, ht, fi, loAS
Wattled pheasant    
 Lophura bulweriyVUAGAS
Brown eared-pheasant    
 Crossoptilon mantchuricumyVUag, hd, lo, rcAS
Cheer pheasant    
 Catreus wallichiyVUAG, FI, HT, LOAS, EU
Reeves's pheasant    
 Syrmaticus reevesiiyVUHT, LO,AS
Mountain peacock-pheasant    
 Polyplectron inopinatumyVUag, cc, rc, trAS
Hainan peacock-pheasant    
 Polyplectron katsumataeyENHT, LO,AS
Malayan peacock-pheasant    
 Polyplectron malacenseyVUAGAS
Palawan peacock-pheasant    
 Polyplectron napoleonisyVULOAS
Green peafowl    
 Pavo muticusyENAG, HD, HTAS
West Indian whistling-duck    
 Dendrocygna arboreayVUAG, CC, LO, POCA
Lesser white-fronted goose    
 Anser erythropusyVUAG, DW, HTAS, EU
White-winged duck    
 Cairina scutulatayENDW, HD, LOAS
Auckland Islands teal    
 Anas aucklandicayVUiaOC
Baer's pochard    
 Aythya baeriyCRAG, CC, HTAS
Steller's eider    
 Polysticta stelleriyVUcc, em, ht, ia, po, trNA, AS, EU
Oriental stork    
 Ciconia boycianayENAG, HD, POAS
Greater adjutant    
 Leptoptilos dubiusyENHT, POAS, EU
Madagascar sacred ibis    
 Threskiornis bernieriyENHT, LO, POAF
Southern bald ibis    
 Geronticus calvusyVUag, em, hd, ht, ia, po, rc, trAF
Flightless cormorant    
 Phalacrocorax harrisinVUCCSA
Steller's sea-eagle    
 Haliaeetus pelagicus?VUem, ht, lo, ot, po, rcAS
Egyptian vulture    
 Neophron percnopterusyENAG, EM, HD, PO, PN, TRAF, AS, EU
Red-headed vulture    
 Sarcogyps calvusyCRAG, HT, POAS
Cinereous vulture    
 Aegypius monachusyNTHTAF, AS, EU
Ridgway's hawk    
 Buteo ridgwayinCRAG, HT, LOCA
Harpy eagle    
 Harpia harpyjayNTHT, LO,NA, CE, SA
Spanish imperial eagle    
 Aquila adalbertiyVUIAAF, EU
Great Indian Bustard    
 Ardeotis nigricepsnCRIA, TRAS, EU
Inaccessible rail    
 Atlantisia rogersinVUIAAF
Grey crowned-crane    
 Balearica regulorumyENAG, TRAF
Sarus crane    
 Grus antigoneyVUAG, HD, HT, PO, TRAS, EU, OC
Blue crane    
 Anthropoides paradiseusyVUAG, HT, TRAF
Wattled crane    
 Bugeranus carunculatusyVUag, cc, dw, em, fi, hd, ht, ot, po, trAF
Red-crowned crane    
 Grus japonensisyENAG, RCAS
Buff-breasted buttonquail    
 Turnix olivii?ENag, fi, iaOC
Chatham snipe    
 Coenocorypha pusillayVUcc, iaOC
Tolima dove    
 Leptotila conoverinENagSA
Tuxtla quail-dove    
 Geotrygon carrikeriyENAG, LONA
White-throated ground-dove    
 Gallicolumba xanthonurayNTOTOC
Santa Cruz ground-dove    
 Gallicolumba sanctaecrucisnENIAOC
Western crowned-pigeon    
 Goura cristatayVUHT, LO,AS
Victoria crowned-pigeon    
 Goura victoriayVUHTAS, OC
Southern crowned-pigeon    
 Goura scheepmakeriyVUHTAS, OC
Rapa fruit-dove    
 Ptilinopus huttoni?VUFI, IA, LOOC
Makatea fruit-dove    
 Ptilinopus chalcurus?VUcc, em, iaOC
Polynesian imperial-pigeon    
 Ducula aurorae?ENPNOC
Marquesan imperial-pigeon    
 Ducula galeata?ENHTOC
Christmas Island imperial-pigeon    
 Ducula whartoninNTcc, em, ht, iaOC
Carnaby's black-cockatoo    
 Calyptorhynchus latirostrisyENAG, IAOC
Red-and-blue lory    
 Eos histrioyENHTAS
Rimatara lorikeet    
 Vini kuhlii?ENIAOC
Henderson lorikeet    
 Vini stepheninVUIAOC
Ultramarine lorikeet    
 Vini ultramarina?ENAG, FI, IAOC
Horned parakeet    
 Eunymphicus cornutusyVUIAOC
Swift parrot    
 Lathamus discoloryENAG, LO, RC, TROC
Green racquet-tail    
 Prioniturus luconensis?VULOAS
Blue-winged racquet-tail    
 Prioniturus verticalisnCRHT, LO,AS
Black-cheeked lovebird    
 Agapornis nigrigenisyVUAG, CC, HTAF
Hyacinth macaw    
 Anodorhynchus hyacinthinusyENHTSA
Lear's macaw    
 Anodorhynchus leariyENAG, FI, HTSA
Blue-throated macaw    
 Ara glaucogularisyCRHTSA
Military macaw    
 Ara militarisyVUHT, LO, RC, TRCE, SA
Great green macaw    
 Ara ambiguusyENAG, HT, LOCE, SA
Red-fronted macaw    
 Ara rubrogenysyENAG, HTSA
Blue-winged macaw    
 Primolius maracanayNTAG, RCSA
Thick-billed parrot    
 Rhynchopsitta pachyrhynchayENAG, HT, LOSA
Maroon-fronted parrot    
 Rhynchopsitta terrisiyENAG, CC, FINA
Golden parakeet    
 Guaruba guaroubayENLOSA
Cuban parakeet    
 Aratinga euopsyVUAG, HTCA
Sun parakeet    
 Aratinga solstitialisyENHTSA
Grey-breasted parakeet    
 Pyrrhura griseipectusyCRAG, HTSA
Grey-cheeked parakeet    
 Brotogeris pyrrhopterayENAG, HT, LOSA
Yellow-billed amazon    
 Amazona collariayVUAG, EM, LOCA
Hispaniolan amazon    
 Amazona ventralisyVUAG, HT, LOCA
Black-billed amazon    
 Amazona agilisyVUAG, EM, LO, PNCA
Red-crowned amazon    
 Amazona viridigenalisyENAG, HTNA
Red-browed amazon    
 Amazona rhodocorythayENAG, HT, LO, RCSA
Red-tailed amazon    
 Amazona brasiliensisyVUAG, HT, LO, RCSA
Yellow-shouldered amazon    
 Amazona barbadensisyVUHTCA, SA
Yellow-headed amazon    
 Amazona oratrixyENAG, HTNA, CE
Yellow-naped amazon    
 Amazona auropalliatayVUAG, HTNA, CE
Vinaceous-breasted amazon    
 Amazona vinaceayENAG, HT, RCSA
St Lucia amazon    
 Amazona versicoloryVUCC, HT, LOCA
Red-necked amazon    
 Amazona arausiacayVUag, cc, htCA
St Vincent amazon    
 Amazona guildingiiyVUag, cc, ht, lo, ot, trCA
Imperial amazon    
 Amazona imperialisyENag, cc, htCA
Bannerman's turaco    
 Tauraco bannermaninENAG, FI, LOAF
Bay-breasted cuckoo    
 Coccyzus rufigularisnENAG, HTCA
Anjouan scops-owl    
 Otus capnodesnCRAGAF
Philippine eagle-owl    
 Bubo philippensisyVUAG, LOAS
Blakiston's fish-owl    
 Ketupa blakistoni?ENAG, LOAS
Spotted owl    
 Strix occidentalisyNTLO, PNNA
Christmas Island hawk-owl    
 Ninox natalisnVUEM, IAOC
Great hornbill    
 Buceros bicornisyNTAG, HT, LOAS
Gurney's pitta    
 Pitta gurneyinENAG, HT, LOAS
Mao    
 Gymnomyza samoensisnENAG, IAOC
Black-eared miner    
 Manorina melanotisyENCC, FI, PNOC
Mauritius cuckooshrike    
 Coracina typicanVUcc, ia, poAF
Oahu Elepaio    
 Chasiempis ibidisnENAG, IA, RCOC
Tahiti monarch    
 Pomarea nigranCRCC, IAOC
Marquesan monarch    
 Pomarea mendozaenENCC, FI, IAOC
Taiwan bulbul    
 Pycnonotus taivanus?VUPNAS
Mauritius black bulbul    
 Hypsipetes olivaceusnVUIAAF
Bonin white-eye    
 Apalopteron familiarenVUag, cc, ia, rcAS
San Cristobal mockingbird    
 Mimus melanotis?ENIASA
Seychelles fody    
 Foudia sechellarumyNTcc, ht, ia, loAF
Anianiau    
 Hemignathus parvusnVUIAOC
Akiapolaau    
 Hemignathus munroinENAG, IA, LO, PNOC
Hawaii creeper    
 Oreomystis manayENIAOC
Martinique oriole    
 Icterus bonananVUPNCA
Jamaican blackbird    
 Nesopsar nigerrimusnENAG, EMCA
Red-bellied grackle    
 Hypopyrrhus pyrohypogaster?VUag, ht, ia, loSA
Mangrove finch    
 Camarhynchus heliobatesnCRcc, iaSA
Black-cheeked ant-tanager    
 Habia atrimaxillarisnENag, loCE
MOTIVATIONAL (3 spp)    
African penguin    
 Spheniscus demersusyENCC, PNAF
Salmon-crested cockatoo    
 Cacatua moluccensisyVUHT, LOAS
White cockatoo    
 Cacatua albayVUHT, LOAS
COMMERCIAL (17 spp)    
Saker falcon    
 Falco cherrugyENAG, HTAF, AS, EU
Black-winged lory    
 Eos cyanogeniayVUag, htAS
Chattering lory    
 Lorius garrulusyVUHTAS
Purple-naped lory    
 Lorius domicellayENDW, HTAS
Grey parrot    
 Psittacus erithacusyVUHTAF
Straw-headed bulbul    
 Pycnonotus zeylanicusyVUAG, HTAS
Green avadavat    
 Amandava formosayVUAG, HT, POAS
Royal parrotfinch    
 Erythrura regiayVULOOC
Gouldian finch    
 Erythrura gouldiaeyNTFIOC
Java sparrow    
 Padda oryzivorayVUHTAS
Timor sparrow    
 Padda fuscatayNTAG, HTAS
Yellow-faced siskin    
 Carduelis yarrelliiyVUHTSA
Red siskin    
 Carduelis cucullatayENAG, HTCA, SA
Marsh seedeater    
 Sporophila palustrisyENAG, HTSA
Chestnut seedeater    
 Sporophila cinnamomeayVUAG, HTSA
Yellow cardinal    
 Gubernatrix cristatayENHTSA
Seven-coloured tanager    
 Tangara fastuosayVUAG, HT, LOSA

Seven families, only one of them passerine, have more than ten species that are recommended for captive breeding [Psittacidae (58 spp), Columbidae (20 spp), Phasianidae (20 spp), Anatidae (16 spp), Fringillidae (15 spp), Accipitridae (13 spp) and Cracidae (11 spp)], whereas a substantial proportion of species in the Gruidae [7 of 15 spp (47%)], Threskiornithidae [5 of 35 spp (14%)] and Otididae [3 of 25 spp (12%)] are recommended for captive breeding. The 257 spp comprise 13 spp from North America including Mexico (5%), 11 spp from Central America (4%), 20 spp from the Caribbean (8%), 39 spp from South America (15%), 75 spp from Asia (29%), 82 spp from Oceania including Hawaii (32%), 33 spp from Africa (13%), and 17 spp from Europe, the Middle East and Central Asia (7%) (NB: some species occur in multiple regions, thus a value >100%). This approximately matches the distribution of all species but with half the number expected from Africa (which holds 23·4% of all species) and twice the number expected from Oceania (which holds 15·8% of all species). The latter reflects the predominance of island species: of the 257 spp recommended for captive breeding, 120 spp occur on oceanic islands (47%), 41 spp on continental islands (16%) and 110 spp on continents (43%).

Unsurprisingly, the species recommended for captive breeding are not distributed equally across IUCN Red List categories. Approximately one-third fall into each of the categories of CR, EN and VU, with a total of 6·2% considered EW or NT (Fig. 2). Hence the proportion of all species in each category that are recommended for captive-breeding ranges from 100% for EW to 38% of CR down to just 1% of NT species (Fig. 3). A similar trend is found when considering the proportion of species recommended for captive breeding in each Red List category against the six classes of captive breeding (Fig. 4). By definition, captive breeding is ‘Necessary’ for the conservation of all EW species in the immediate future, and for CR species it is ‘Necessary’, ‘Integral’ or ‘Precautionary’. For most other species, captive breeding is considered ‘Prudent’, with an increasing proportion (up to one-fifth of the relevant NT species) listed because of the role that it can play in supplying birds to meet demands from the cage-bird trade.

figure

Figure 2. Proportion of species for which captive breeding is recommended in different International Union for Conservation of Nature Red List categories (n = 257 species): CR, Critically Endangered; EN, Endangered; EW, Extinct in the Wild; NT, Near Threatened; VU, Vulnerable.

Download figure to PowerPoint

figure

Figure 3. Percentage of species in each International Union for Conservation of Nature (IUCN) Red List category for which captive breeding is recommended: CR, Critically Endangered (75 of 197 spp); EN, Endangered (88 of 389 spp); EW, Extinct in the Wild (4 of 4 spp); NT, Near Threatened (12 of 880 spp); VU, Vulnerable (78 of 727 spp).

Download figure to PowerPoint

figure

Figure 4. Percentage of species for each purpose (for which captive breeding is recommended) in each International Union for Conservation of Nature (IUCN) Red List category (n = 257 species): CR, Critically Endangered; EN, Endangered; EW, Extinct in the Wild; NT, Near Threatened; VU, Vulnerable.

Download figure to PowerPoint

Finally, the pattern of the most significant threats impacting species for which captive breeding is recommended (Fig. 5) largely matches the pattern for all threatened species but with a higher proportion impacted by hunting and trapping (38·3% vs 16·2%) and invasive alien species (27·7% vs 16%).

figure

Figure 5. Percentage of species for which captive breeding is recommended (n = 257 species) that are impacted by different threats, compared with the pattern for all threatened species (n = 1313).

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

The evidence assembled in this review demonstrates clearly that aviculture has a small but significant past and present role, and potentially a mainstream future, in the conservation of avian diversity. How mainstream that future is will depend in large part on how closely the avicultural institutions adopt the priorities that conservation biologists have identified (our primary purpose here is to present these priorities as fully and dispassionately as possible), but it must also depend on the quality and appropriateness of the concept and execution of the intervention. This inevitably implies a careful integration of ex situ skills with in situ strategy: zoos cannot be expected to possess much expertise in conservation biology (although some do), but they can be expected to seek such expertise elsewhere and harness it (or harness themselves to it) for the greater good of the species or issues they are addressing. With conservationists clearly insufficiently resourced to service all the pressing cases presented by the growing number of threatened species, partnerships with and leadership from zoos and like-minded institutions could become an increasingly important and standard way of seeking to prevent extinctions and restore populations for the subset of species for which this is appropriate. Even so, a number of qualifications are needed to provide perspective and commentary on the role of zoos in the future conservation of avian diversity.

First – this caveat applies particularly to those species for which no captive population already exists – it is crucial that the taking of a species into captivity should not provide an excuse for the threat(s) to that species to continue unaddressed. Vested interests ranging from government through corporates to the local unemployed may readily batten onto captive breeding as a solution to any seeming impasse between conservation requirements and economic development, commonly with the assumption that animals standing in the way of projects can simply be moved elsewhere. When hotel/residential developments were recently threatening the last tiny stronghold of the Grenada dove Leptotila wellsi, the pressure to establish an ex situ population was considerable, but several conservation organizations resisted the measure for fear it would be seen as a green light to the developers. Following the modification of the building plans, we feel it relatively safe now to include the Grenada dove in Table 2, but the key element in any move to establish a reserve population in captivity is that this forms part of a coherent strategy for the long-term security of the species in question and, therefore, is fully integrated with any in situ programme.

Second, there are of course existing and potential cases where an in situ programme is greatly needed but not yet in existence or sufficiently advanced. Examples where captive breeding is already integral to the conservation effort but where in situ management remains underdeveloped and unengaged include the Philippine eagle Pithecophaga jefferyi, both species of Houbara bustard, Negros bleeding-heart Gallicolumba keayi and Blue-crowned laughingthrush Garrulax courtoisi, for all of which the future conservation endeavour for the species appears to lie de facto with those who breed them in captivity and who appear to exhibit the greatest motivation over their survival. Credit in these cases clearly belongs to aviculture but with the proviso that, in the absence of input from ecologists, biologists, managers and other groups, the conservation agenda for certain species may sometimes acquire unusual (and debatable) emphases, as in the case of the two Houbara bustards where the release of large numbers of captive-bred birds receives greater attention than managing habitat in order to optimize productivity and carrying capacity (pers. obs).

Third, captive breeding is, as its practitioners know better than anyone, by no means an easy solution, whether for biological or other reasons. There are still indeed some species for which captive breeding, even though identified here as their sole hope, has yet to achieve real breakthrough results. One is the Socorro dove Zenaida graysoni, ‘saved’ by aviculture almost by chance back in the 1950s and 1960s but then commonly hybridized and even now making painfully slow progress towards population stability and eventual reintroduction (BirdLife International, 2012). Another is Spix's macaw Cyanopsitta spixii, held in a small number of private collections but in desperate need of rapid population increase and a coherent recovery plan with genuine all-party engagement (Donald et al., 2010). A third is the Bali starling Leucopsar rothschildi, for which a number of initiatives now exist but with no overarching strategy or biological-monitoring programme to guide them (BirdLife International, 2012). Then there is Edwards's pheasant, a species for which no recent evidence exists of its continued survival in the wild, leaving its fate perhaps entirely in the hands of an as yet unorganized network of mostly European enthusiasts (BirdLife International, 2012). These examples indicate that individual enthusiasms, vital as they are, are no substitute for fully integrated, well-funded and biologically led recovery programmes, such as those that serve the California condor Gymnogyps californianus (Walters et al., 2010).

Fourth, as noted under Results, captive breeding decreases sharply in relevance and value with decreasing levels of endangerment. Because moving individuals of a species into ‘protective captivity’ can be a relatively risky and expensive step, it is typically only taken when the species in question reaches a point of crisis. Naturally, however, there are various risks associated with allowing in situ conditions to deteriorate too far before stepping in with ex situ support. For example, one recent study suggests that species that can increase faster in captivity than in the wild should be taken entirely into captivity when the total number of ♀♀ falls below 20 (Tenhumberg et al., 2004); another suggests that successful ex situ intervention typically requires 15 unrelated founders and a captive population of 100 individuals in order to avoid inbreeding (Witzenberger & Hochkirch, 2011). On the other hand, there are equal risks in moving too early with ex situ support, thereby expending and possibly wasting resources that could more judiciously be directed to more deserving causes. The balance to be struck in this regard is a particularly delicate one.

Fifth, questions of cost, public appeal and institutional tradition exert an inevitable sway on the choice of project to pursue. The disproportionate number of oceanic species that are identified here as potential targets for captive breeding is correlated with susceptibility of island birds to the effects of invasive alien species, a problem that habitat management alone (usually the most important requirement in species conservation, at least on continents) does not address. However, oceanic islands are typically expensive places to travel to, to work in (in most cases the birds will incur the additional cost of being caught, as many will have no pre-existing captive populations: see Results) and, especially, to remove deleterious invasives from. Zoos anxious to become involved in species conservation therefore have to weigh the costs and benefits of one potential choice against all others, review how they would expect these choices to play with their public and other supporters, and in addition consider the capacity of their staff and the general orientation of their themes and interests.

Sixth, the list of species identified here for conservation breeding should not be interpreted as a comprehensive and watertight review of candidates. Table 2 merely synthesizes evidence and opinion from a range of sources, and there may well be other species that on further reflection (perhaps prompted by this compilation) will need to be added. All nominations have a degree – often high – of authority and sense behind them, but this is not to say that they should be accepted uncritically; moreover, a small number represent our own speculation rather than a previously published recommendation and may be judged inappropriate choices for practical or political reasons (e.g. Sulu hornbill Anthracoceros montani, which is subject to much hunting pressure, may be far too rare now to attempt to catch – none is known to be in captivity – as well as being confined to a tiny range inside a personnel security-risk area). Each species should therefore be considered for captive breeding only after a fresh, careful and comprehensive review of the evidence; each should be treated as recommended simply for consideration of captive breeding rather than anything more authoritative. As an example, current interest in the captive breeding of the Rufous-fronted laughingthrush Garrulax rufifrons, based on evidence of a potentially catastrophic collapse in its numbers (Collar et al., 2012), depends on first establishing how many (and in what condition) populations persist within its current known range in West Java (Collar & van Balen, 2013).

Seventh, once the need for conservation breeding is firmly established, it is important for aviculture to move expeditiously. Speedy interventions repay the investment (Martin et al., 2012). Even supposedly long-lived species, such as parrots, have recently been shown to have relatively constrained reproductive lifetimes (Young et al., 2012). The standard conservation response for threatened species is to establish protected areas for them, given that the commonest threat is habitat destruction driven by unsustainable agriculture, logging and development (BirdLife International, 2013). However, the disproportionate frequency of exploitation and invasive alien species affecting species recommended for ex situ management (see Fig. 5) is a recognition that these threats – which are particularly grave for large-bodied, slow-breeding species (Owens & Bennett, 2000) – are unimpeded by protected area boundaries. In such circumstances, the urgency of the conservation-breeding option clearly increases. Recent, as yet unpublished disquiet over the status of the Tooth-billed pigeon Didunculus strigirostris, if justified by more concerted searches, should trigger very rapid intervention, because the only plausible cause of its disappearance is likely to be an invasive predator or competitor (we include it in Table 2, as the evidence of its disappearance appears to be significantly more compelling at this stage than for the Rufous-fronted laughingthrush discussed above).

Eighth, circumstances and hence priorities can change rapidly. At the most basic level, this can be the result of new taxonomic insights. For example, the seemingly intractable complex of Pyrrhura parakeets that have traditionally been treated as two species, Painted parakeet Pyrrhura picta and White-eared parakeet Pyrrhura leucotis, was recently recommended to be broken into no fewer than 14 species (Arndt, 2008), and the Mealy amazon Amazona farinosa broken into two (Wenner et al., 2012), with new implications for potential avicultural interventions. Moreover, new priorities for ex situ management can emerge with remarkable speed, cases in point being the White-bellied heron Ardea insignis (RSPN, 2013) and Spoon-billed sandpiper Eurynorhynchus pygmeus (Pain et al., 2011), two species that as recently as 2010 were nowhere considered appropriate targets for captive breeding.

Apart from these caveats, there are several observations to be made relating to the classes ‘Motivational’ and ‘Commercial’. ‘Motivational’ species are expected to have broad popular appeal, thereby allowing zoos to capitalize freely on the conservation stories associated with them. Most such species may not be threatened: Table 2 contains only three examples where the conservation breeding of threatened birds – a penguin and two cockatoos – could be considered mainly in terms of public motivation. However, there are clearly a number of highly attractive species for which conservation concern has been registered through their listing on CITES appendices and which could be used to good effect as ambassadors for conservation: examples include Harpy eagle Harpia harpyja, Horned guan Oreophasis derbianus, Palm cockatoo Probosciger aterrimus, Great hornbill Buceros bicornis and Helmeted hornbill Rhinoplax vigil (all species on CITES Appendix I and all among the most charismatic representatives of their rainforest habitat). Even Least Concern and non-CITES species with great popular appeal, such as White stork Ciconia ciconia, various colonial waterbirds, Barn owl Tyto alba, Eurasian eagle-owl Bubo bubo and Great blue turaco Corythaeola cristata, can be harnessed very effectively to the conservation cause through their various associations (migration, wetlands, farmland and forests).

The main conservation response on behalf of species affected by the international bird trade is to seek to suppress or manage levels of exploitation through the mechanisms of CITES. An alternative strategy, however, might be to seek to meet the demand for certain species through breeding them in commercial volume. Normally, any such enterprise would fall outside the remit of a zoo but, for example, Loro Parque in the Canary Islands is principal supporter of the non-profit Loro Parque Foundation, which supplies captive-bred parrots to the global market and uses 100% of the funds generated for in situ conservation of threatened parrot species (Waugh, 2000). Clearly, there are issues of scale and geography that may render this model unsuitable for many of the species listed under ‘Commercial’ in Table 2, but scope for national initiatives remains, especially as in many cases the consumption is largely domestic and therefore beyond the reach of CITES. Various risks exist, to do with laundering wild-caught birds and creating markets instead of supplying them, but with appropriate legal and administrative superintendence these difficulties might be obviated and outweighed.

A final observation to be made here simply acknowledges the primacy of non-passerines over passerines in Table 2. With 5913 out of 9934 bird species (BirdLife International, 2012), passerines form very nearly 60% of the global avifauna (and 47% of threatened bird species), but with 69 out of 257 spp, they only form around 27% of birds being treated by or recommended for possible ex situ management. This bias is perhaps explicable partly because larger-bodied birds are generally more extinction-prone than smaller- bodied species (Bennett & Owens, 1997) and partly because zoos tend to hold more large- bodied than small-bodied species, as the former make a better public spectacle and live longer (Speakman, 2005). The families with disproportionate numbers of species for which conservation breeding is recommended for consideration here tend to be those that breed more easily in captivity and that are highly threatened by either capture for the bird trade (e.g. parrots) or hunting for food (e.g. pheasants and waterbirds).

Acknowledgements

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References

N.J.C. would like to thank the European Association of Zoos and Aquaria for the initial invitation to assemble a presentation on this subject at its Mid-Year Bird TAG meeting in April 2012, and Cathy King and Geer Scheres (Weltvogelpark Walsrode) for their facilitation and financing of his attendance at the meeting. We are most grateful to two referees for their constructive comments on this paper.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. Acknowledgements
  8. References
  • Aikman, H., Davis, A., Miskelly, C., O'Connor, S. & Taylor, G. (2001): Chatham Islands threatened birds: recovery and management plans. Wellington, New Zealand: Department of Conservation.
  • Arndt, T. (2008): Anmerkungen zu einigen Pyrrhura-Formen mit der Beschreibung einer neuen Art und zweier neuer Unterarten. Papageien 8/2008: 278286.
  • Balmford, A., Leader-Williams, N. & Green, M. J. B. (1995): Parks or arks: where to conserve threatened mammals? Biodiversity & Conservation 4: 595607.
  • Balmford, A., Mace, G. M. & Leader-Williams, N. (1996): Designing the Ark: setting priorities for captive breeding. Conservation Biology 10: 719727.
  • Bennett, P. M. & Owens, I. P. F. (1997): Variation in extinction risk among birds: chance or evolutionary predisposition? Proceedings of the Royal Society of London 264: 401408.
  • BirdLife International (2012): IUCN Red List for birds. Cambridge: BirdLife International. Available at http://www.birdlife.org (accessed 11 April 2013).
  • BirdLife International (2013): State of the world's birds. Cambridge: BirdLife International.
  • Butchart, S. H. M., Stattersfield, A. J., Bennun, L. A., Shutes, S. M., Akçakaya, H. R., Baillie, J. E. M., Stuart, S. N., Hilton-Taylor, C. & Mace, G. (2004): Measuring global trends in the status of biodiversity: Red List Indices for birds. Public Library of Science Biology 2: 22942304.
  • Collar, N. J. & van Balen, S. (2013): Notes for the conservation of the rufous-fronted laughingthrush Garrulax rufifrons. Forktail 29: 1518.
  • Collar, N. J. & Stuart, S. N. (1985): Threatened birds of Africa and related islands: the ICBP/IUCN Red Data Book (3rd edn, part 1). Cambridge: International Council for Bird Preservation, and International Union for Conservation of Nature and Natural Resources.
  • Collar, N. J., Gonzaga, L. P., Krabbe, N., Madroño Nieto, A., Naranjo, L. G., Parker, T. A. & Wege, D. C. (1992): Threatened birds of the Americas: the ICBP/IUCN Red Data Book (3rd edn, part 2). Cambridge: International Council for Bird Preservation.
  • Collar, N. J., Andreev, A. V., Chan, S., Crosby, M. J., Subramanya, S. & Tobias, J. A. (2001): Threatened birds of Asia: the BirdLife International Red Data Book (3rd edn, part 3). Cambridge: BirdLife International.
  • Collar, N. J., Gardner, L., Jeggo, D. F., Marcordes, B., Owen, A., Pagel, T., Pes, T., Vaidl, A., Wilkinson, R. & Wirth, R. (2012): Captive breeding and the most threatened birds in Asia. BirdingASIA 18: 5057.
  • Conway, W. G. (2003): The role of zoos in the 21st century. International Zoo Yearbook 38: 713.
  • Donald, P. F., Collar, N. J., Marsden, S. J. & Pain, D. J. (2010): Facing extinction: the world's rarest birds and the race to save them. London: T. & A. D. Poyser.
  • Imboden, C. (1987): The captive breeding controversy. World Birdwatch 9: 67.
  • King, W. B. (1978–1979): Red Data Book 2. Aves (2nd edn). Morges, Switzerland: International Union for Conservation of Nature and Natural Resources. Reprinted in 1981 as King, W. B. (Compiler) (1981): Endangered birds of the world: the ICBP Bird Red Data Book. Washington, DC: Smithsonian Institution.
  • Lowther, J., Cook, D. & Roberts, M. (2002): Crime and punishment in the wildlife trade. Godalming, Surrey: WWF TRAFFIC.
  • Mallinson, J. J. C. (1991): Partnerships for conservation between zoos, local governments and non-governmental organizations. Symposia of the Zoological Society of London No. 62: 5774.
  • Martin, T. G., Nally, S., Burbidge, A. A., Arnall, S., Garnett, S. T., Hayward, M. W., Lumsden, L. F., Menkhorst, P., McDonald-Madden, E. & Possingham, H. (2012): Acting fast helps avoid extinction. Conservation Letters 5: 274280.
  • McAtee, W. L. (1935): Preservation of species in aviaries. Auk 52: 128129.
  • Owens, I. P. F. & Bennett, P. M. (2000): Ecological basis of extinction risk in birds: habitat loss versus human persecution and introduced predators. Proceedings of the National Academy of Sciences of the United States of America 97: 1214412148.
  • Pain, D., Green, R. & Clark, N. (2011): On the edge: can the spoon-billed sandpiper be saved? British Birds 104: 350363.
  • Rahbek, C. (1993): Captive breeding – a useful tool in the preservation of biodiversity? Biodiversity & Conservation 2: 426437.
  • Redford, K. H., Jensen, D. B. & Breheny, J. J. (2012): Integrating the captive and the wild. Science 338: 11571158.
  • RSPN (2013): White-bellied heron conservation. Lhado Lam, Thimphu, Bhutan: Royal Society for Protection of Nature. Available at http://www.rspnbhutan.org/programs/endangered-species/white-bellied-heron.html
  • Salafsky, N., Salzer, D., Stattersfield, A. J., Hilton-Taylor, C., Neugarten, R., Butchart, S. H. M., Collen, B., Cox, N., Master, L. L., O'Connor, S. & Wilkie, D. (2008): A standard lexicon for biodiversity conservation: unified classifications of threats and actions. Conservation Biology 22: 897911.
  • Sheppard, C. (1995): Propagation of endangered birds in US institutions: how much space is there? Zoo Biology 14: 197210.
  • Snyder, N. F. R., Derrickson, S. R., Beissinger, S. R., Wiley, J. W., Smith, T. B., Toone, W. D. & Miller, B. (1996): Limitations of captive breeding in endangered species recovery. Conservation Biology 10: 338348.
  • Speakman, J. R. (2005): Body size, energy metabolism and lifespan. Journal of Experimental Biology 208: 17171730.
  • Stattersfield, A. J. & Capper, D. R. (Eds) (2000): Threatened birds of the world. Cambridge: BirdLife International, and Barcelona: Lynx Edicions.
  • Tenhumberg, B., Tyre, A. J., Shea, K. & Possingham, H. P. (2004): Linking wild and captive populations to maximize species persistence: optimal translocation strategies. Conservation Biology 18: 13041314.
  • Tribe, A. & Booth, R. (2003): Assessing the role of zoos in wildlife conservation. Human Dimensions of Wildlife 8: 6574.
  • Walters, J. R., Derrickson, S. R., Fry, D. M., Haig, S. M., Marzluff, J. M. & Wunderle Jr, J. M. (2010): Status of the California condor (Gymnogyps californianus) and efforts to achieve its recovery. Auk 127: 9691001.
  • Waugh, D. R. (2000): Parrot conservation and Loro Parque Fundación, Puerto de la Cruz. International Zoo Yearbook 37: 288298.
  • Wenner, T. J., Russello, M. A. & Wright, T. F. (2012): Cryptic species in a Neotropical parrot: genetic variation within the Amazona farinosa species complex and its conservation implications. Conservation Genetics 13: 14271432.
  • Witzenberger, K. A. & Hochkirch, A. (2011): Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodiversity & Conservation 20: 18431861.
  • Young, A. M., Hobson, E. A., Bingaman Lackey, L. & Wright, T. F. (2012): Survival on the ark: life-history trends in captive parrots. Animal Conservation 15: 2843.