Aquarium Trade Threat to Pterapogon kaudneri, the Bangaii cardinalfish

By Eric Borneman on behalf of Eric Borneman, Alex Vagelli, Frank Marini, Andrew Bruckner, and MASNA History

Allen GR (2000) Env Biol Fish 57:142

- First discovered in 1920, described in 1933 (Koumans 1933) - Forgotten until 1991 -“Rediscovered” in 1994-1995 (Allen and Steene 1995) - Proposed for IUCN red listing as threatened species in 1999, 2002 Range

32 of 57 islands in the Bangaii Archipelago

Total area of 5500km2

Potential : 34km2

Vagelli AA and Erdmann MV (2002) First comprehensive ecological survey of the Banggai cardinalfish, Pterapogon kauderni Env Biol Fish 63: 1-8 Estimated population

-No historical data – estimate 0.6 ind/m2

-Based on collection, retrofits to historical population of 20 million

- first estimate in 2001 -6 years after collection began - 2.2 - 2.4 million fish (2007) - Density 0.08 ind/m2

CITES, COP 14 2007) from Vagelli AA (2005) PhD dissertation Natural Habitat and Behavior

Associated with benthic invertebrates

May share habitat with other species (, urchins, , )

Usually in bays, <4.5m depth

Associate in groups of 2-500 individuals - average size 9.5-21 individuals

Very site attached

Associates with damselfish, clownfish, and wrasses

Carnivorous planktivore

Lifespan 1-3 years in wild

Vagelli and Erdmann (2002) Reproductive Issues

Endemic

Low to no dispersal or gene flow

Low fecundity (average 40-50 egg clutch size)

Direct development with long parental care, male mouthbrooding

Highly genetically isolated – two main groups (southwestern and the rest) - severe population bottlenecks, geographic isolation - genetic isolation in as little as 2km (same island, different reef) - largest natural spread of populations: 16km - Allee effects present

Vagelli AA and Volpedo AV (2004) Reproductive ecology of Pterapogon kauderni, an endemic apogonid from Indonesia with direct development Env Biol Fish 70: 235-245

Vagelli A (1999) The reproductive biology and early ontogeny of the mouthbrooding Banggai cardinalfish, Pterapogon kauderni (Perciformes, ) Env Biol Fish 56 79-92 Collection Issues

Trade began in 1992 (local) and 1995 (international)*1

2.4 million total population - 0.63m2 in non-collected area (pearl farm) 900% higher - poaching now occurring and density declining (0.63-0.47 ind/m2) - 0.08/m2 in collected areas - 0.03 increased to 0.06 at one site where collection banned for three years

2 have occurred (perhaps more)*2

Introduced populations expanding

Late 1990s to 2001 – 600,000 – 700,000 collected each year 2001-2004 700,000 – 900,000 collected each year 2004 – present exceeds 900,000 (>30% of population)

CITES, COP14 (2007), Vagelli pers. comm. Aquarium Collection Issues

- subject to nematodes, digenetic trematodes, isopods, iridovirus - impacting survival of collected individuals in past five years

- 60 fishermen, 3 operations* - CPUE declined 25-80% (1000 fish/hr to 25-330 fish/hr) - mortality 25-30% post collection - 15% rejection rates - 15% mortality post export

- Population decline estimated at 89% (greater than CITES II requirements)

- Population size distributions changed (fewer adults)

- likely within 10 years, genetic lines lost

CITES COP 14 (2007), Vagelli pers. comm. Collection Locations

Lunn KE and Moreau M-A (2004) Unmonitored trade in marine ornamental fishes: the case of Indonesia’s Banggai cardinalfish (Pterapogon kauderni) Reefs 23: 344-351

Aquarium Trade Structure

Original retail price $100-150 Today: $15-30

Wholesale prices - $3-7

Lunn and Moreau (2004) Trade Information

Lunn and Moreau (2004) Trade and Economics

Lunn and Moreau (2004) SomeSome individualsindividuals fromfrom thosethose groupsgroups diedie afterafter thethe firstfirst flightflight betweenbetween IndonesiaIndonesia andand Singapore,Singapore, andand othersothers uponupon arrivalarrival toto thethe USA,USA, EuropeEurope oror Asia.Asia.

InIn fact,fact, manymany timestimes entireentire shshipmentsipments ofof thosethose survivorssurvivors diedie soonsoon uponupon arrivalarrival toto aa wholesalerwholesaler facility.facility. TheThe realreal impactimpact ofof thethe BanggaiBanggai cardinalfishcardinalfish tradetrade inin thethe locallocal economy:economy:

TheThe totaltotal numbernumber ofof locallocal peoplepeople currentlycurrently activelyactively involvedinvolved inin thethe BanggaiBanggai cardinalfishcardinalfish collectingcollecting // tradetrade isis aboutabout 6060 fishersfishers, andand lessless thanthan 200200 peoplepeople areare collectingcollecting inin thethe entireentire region.region. Thus,Thus, << 0.1%0.1% ofof thethe BanggaiBanggai regionregion humanhuman populationpopulation (approximately(approximately 160,000)160,000) isis dedicateddedicated toto thisthis activity.activity. TheThe BanggaiBanggai cardinalfishcardinalfish isis notnot aa historicalhistorical // traditionaltraditional sourcesource ofof incomeincome forfor thethe locallocal people.people. nornor tthehe principalprincipal sourcesource ofof incomeincome forfor thethe collectors.collectors. Aquarium Trade Introductions

Erdmann and Vagelli 2001 (Coral Reefs) 20: 252-253

-Introduced population by the aquarium trade in 2000, 2002

-Established populations at four sites

- aquarium introduced populations at two sites within archipelago (Vagelli 2005, 2007) - Luwuk harbor

- aquarium introduced populations at numerous sites around Bali (Erdmann, pers comm) Indirect Pressures to Bangaiis

- Loss of habitat

- coral disease outbreaks

- destructive fishing techniques (cyanide, bomb-fishing)

- co-collection of other species (anemones, urchins, corals)

- collection damage to critical habitat (urchins, corals)

- general degradation - nutrients, sewage outfalls, siltation, pollution, agriculture - coral algal, fungal, bacterial cover making unsuitable habitat

- earthquakes

- Iridovirus CITES COP 14 (2007) VulnerabilityVulnerability FactorsFactors: Shallow ; Sedentary behavior VulnerabilityVulnerability FactorsFactors: Group formation; Benthic attachment VulnerabilityVulnerability FactorsFactors: Elevated early mortality VulnerabilityVulnerability FactorsFactors: Habitat degradation

Deforestation , Contamination Commercial collecting of benthic organisms

Cyanide used for other ornamentals VulnerabilityVulnerability FactorsFactors: Habitat degradation

CoralCoral DiseasesDiseases VulnerabilityVulnerability FactorsFactors: Habitat degradation DynamiteDynamite FishingFishing PredatorsPredators

Pterois volitans (Scorpaenidae)

Laticauda colubrina (Elapidae)

Epinephelus merra (Serranidae) ParasitesParasites VulnerabilityVulnerability FactorsFactors: Easy collection Conservation Efforts

- Voluntary village protection and private pearl farm

- only Bangaii villagers can fish (permits)

- no international or domestic protection legislation

- No MPA’s or local breeding efforts in place or planned

- no population management, monitoring

- CITES COP14, rejected

CITES COP 14 (2007) Solutions

- Aquarium or source-based captive breeding programs

- IUCN red list as threatened species in 2007 as endangered

- Development of management plan with enforcement

- Protection and conservation of critical habitat

- Reduction of post-capture mortality

- CITES Appendix II listing to regulate trade, develop sustainable trade, without affecting local economy (0.1% population, not historical fishery, not primary source of income

- ESA listing to stop commercial trade without permit

CITES COP 14 (2007) The Good News!...... Breeding

Breeding at 6-9 months of age

Clutch size – 40-90 eggs

Lunar breeding females monthly males 6x/year sex ratio: 1:1 (more males = more broods, but more aggression) no sexual dimorphism

Male mouth broods eggs for 20 days, plus 10 before release

Fertilization rate averages 40-60% (unfertilized or lost during clutch transfer)

Clutch size averages (25-29) in captivity, 18 in wild

References: Marini, Vagelli and Volpedo, Bernardo and Vagelli (2004), et al. Breeding

- cannibalism post-release

- marketable fish within 100-130 days

- survivorship from 66-95%

- currently many local breeders with little effect on market, little entry to market

- extremely easy fish to breed, intentionally or accidentally

- concept of cooperatives to gain entry to marketplace

References: Marini, Vagelli and Volpedo, Bernardo and Vagelli (2004), et al. Captive Breeding WhatWhat cancan thethe hobbyistshobbyists dodo toto help?help? To realize that they have the power of deciding the future of this , which carries a high degree of responsibility. If neither the conservation agencies nor the host Country are willing to protect it, what will determine the future of this species is the decision on whether or not to buy wild capture specimens.

Statement by ALEX VAGELLI, delivered 1pm today by email to MACNA I would urge the hobbyist community to avoid acquiring wild capture Banggais until proper protective measures / trade regulations are in place (CITES or equivalent).

I believe that most hobbyists will be willing to pay a few extra $ for captive bred individuals, knowing that they can have the enjoyment of keeping this amazing fish without contributing to the demise of its natural populations.

The demand for captive bred specimens will give incentives to the aquaculture industry to increase significantly its production, which currently it is not very profitable.

Statement by ALEX VAGELLI, delivered 1pm today by email to MACNA Position Statement

The aquarium trade is almost solely responsible for the rediscovery, subsequent precipitous decline, and potential extinction of an endemic species.

The species is unique and its loss would be of great ecological impact

The role of the aquarium trade in its extirpation would be highly detrimental to the continued existence of the marine ornamental trade.

The U.S. is by far the leading consumer of the species and as such should play a leading role in its continued existence and conservation.

This is a unanimously agreed upon goal in the mission statement of MASNA and MASNA member aquarium societies. Final Statement

It is the position of this group to no longer support the purchase or collection of Pterapogon kaudneri, the Bangaii cardinalfish, for the ornamental trade except for use by ornamental breeders (to be registered with MASNA) until adequate measures are employed by Indonesia and the ornamental supply chain to ensure its sustainable collection and conservation of existing populations in the wild Acknowledgements

Dr. Andrew Bruckner, NOAA Fisheries, Living Oceans Foundation

Dr. Alex Vagelli

Dr. Frank Marini

Dr. Mark Erdmann, Conservation International

IUCN

Species Survival Network

CITES

MASNA board, and especially Cheri Phillips

Steve Pro, Matt Wittenrich