Pterapogon kauderni, a unique species

Text & photos: José María Cid Ruiz

Pterapogon kauderni is a good paradigm about how ornamen- tal fish farming could have a posive impact on the survival of certain , offering to the market of aquariuma qu arium fishes, specimens born in capvity which would alallevle viiateate pres- sure on the wild populaons.

The "Banggai cardinal fish" ( PterapogonPt erapogon kauderni. Koumans,Ko umans, 1933), is a small tropicalal marinem arine species with a very rrestrictestricteded range in nature. ThisT hi s species is mainly located in the arcarchipelagohi pe la go of which are namedn am ed (Banggai Islands, Sulawesi,Sulawes i, Indonesia),I nd on es ia ), bbeingei ng countedd aroundar ou nd 74 points of localizaonlocaliza o n in thirtyt hi rt y islanis la nddss (Vagelli,(V ag el li , 2005).20 05 ). IItsts addiona dd i on tot o the set of speciesspeci es keptk ep t in aquara qu ar ium,iu m, did not occur unlun l 1995,1 99 5, whenw he n Dr.Dr . G. Allen,A ll en , introducedin tr od uc ed themt he m that year duringdu ring the MACNAM AC NA VIIV II Congress.C on gr ess.

Thee speciessp ecie s barelyba re ly measuresm ea su re s 8 cm iinn totalto tal length and ppresentsresents a DiademaDi ad em a and Tripneustes ), the fact is that them also are located under the protecon of lar- very aaracver ac v e papaerne rn ooff cocoloraon:lo ra o n: wwithit h a silver body aandnd three ge aanemones and between the branches of hard and so (Allen, 2000 y Vagelli et al, large vercalr ca l blacblackk babands,nd s, highlighngh ig hl ig h ng a smalls ma ll constellac on stellaonon of 2004). P. kauderni is a diurnal that feeds on small pelagic organisms, mainly white spotsot s betweenbetwee n theth e secondse co nd anda nd the thirdt hi rd band,b an d, asa s we can crustaceans. But its diet is wider, being idenfied in their stomach contents: annelids, mo- see in the images.ma ge s. OnlyO nl y twotw o speciessp ec ie s sharesh are the genusgenu s PterapogonPt erap og on : lluscs and fish larvae. the one in quesons on anda nd thet he AustralianAustr al ia n P. mirificam irifica . Breeding in capvity In nature the speciesie s livesli ve s in smalls mall groups,gro up s, usuallyusu al ly is present in areas of calm and shallowal lo w waterswa te rs (between(betw ee n 1 and 6 meters) in The species has the reputaon of "easy to reproduce in capvity." But the truth is that when beds, reef coralor al oorr sasandnd bbooms.o om Although cited living moving from theory to pracce, there are various difficules to successfully complete the under the protecon of thehe longl on g spines of sea urchins (genera process. My personal experience in keeping and breeding this species in for two

Pterapogon kauderni, a unique species 1 All rights reserved: ©José María Cid 2014

years can be summarized as follows: "not too much difficult spe- cies at the phase to form pairs, easy to in capvity with proper food, but not so easy to get more than 15% of healthy adult individuals from spawning".

Turning now to the details will have to start by sayinay in g that P. kauderni as many other apogonidae, is a mouthbroodermo ut hbrooder (m(males)ales) with no apparent sexual dimorphism. To address its rreproduc-eproduc- on in capvity, should be starngng fromf rom a group of yoyoung.ung. The procedure used in my case, hhasas been to allocate groups of 6-7 individuals in specific aquariumsa qu ariums of 450 L. Well fed and withwithoutou t compeon fromom othero th er species, it is usual that a domind om in antan t cou-co u- ple is formedd aera er a me of two to four weeks (also(als o I haveha ve oob-b- served tthehe formaon of couples in communcommunityit y aquariumaq ua ri um s).s) . Des-De s- pipitete to have a roomy aquarium (because(becau se theyt he y arear e juvenileju ve niless just with 5 -6 cm of length), it is usualu su al thatt ha t theth e newlyne wl y formedfo rm ed ccouplouplee exextendstends its territory araroundou nd thet he tankt an k andan d beginbe gi n to sshowhow an daily feedings. TheTh specimens in these condions, grow and mature very quickly and aer agaggressivegr es sive behaviour aagainstga in st thet he restr es t of the group, wwhosehose quali- a period ofo f twotw to three months will begin to produce the first courtship and spawning. ty ooff lifeli fe isi s degradeddegrad ed veryv er y ququickly.ic kl y. AtA t that point, we proceed mo- EnEnvironmentalvi ro condions: T:27 -28,5 ºC, pH: 8,2, S: 33 -35 g/L. The spawns have always oc- vivingng thet he recentlyr ec en tl y formformeded couple to a 200L specific aquarium.aquarium. cucurred during the day, most oen early in the morning. AAerer tthis,hi s, tthehe rrestes t of tthehe group is recovered in a shortshort me and ooenen a seconds ec on d pairpa ir is formedfo rm ed in just two weeks, which is again The reproducve process observed in the aquarium differs slightly from that takes place in rerelocated,lo ca te d, aass ththee firfirst,st , in anothera no th er aquarium of 200L.200 L. nature where as has been previously described (Vagelli, 2004), a gravid female chooses a male from the group several days prior to starng the courtship. The couple leaves the Again, ffoodoo d andan d waterwa te r quality arear e keyke y to the rapidrap id growg ro th and group and defends a small territory, driving out the other specimens that get too close. In mamaturaontu ra o n of the specimens.s pe ci me ns. The food providedpro vi de has been based (200 -400L) inhabited only by pairs or small groups, as soon the dominant cou- on a porridgepor ri dg e withwi th freshf re sh seafoods ea fo od includinginclu di ng several species of al- ple is formed (me before the first spawning happen), proceeds to drive out the rest of gae anandd someso me vitaminv itamin ssupplements.up pl em en ts This diet has been supple- the group. If the couple and the rest of the group are kept in the same aquarium, the cou- menteded bbyy MyMysissi s sp. and frfrozenoz en red mosquito larvae. Periodical- ple stays together and the female always spawn with the same male. ly they hahaveve bbeenee n fed wiwithth Artemia salina alive. Two to three

Pterapogon kauderni, a unique species 2 All rights reserved: ©José María Cid 2014

In the aquarium, we can see some change in behavior in the couple, two or three days before they spawn. The Courtship itself is iniated by the female, who displays behaviors that include body vibraon, "posioning" in parallel with the male, and also occasional touches flank against flank. During this same period, the male can perform certain characteriscs c "yawns". Spawning is very fleeng, personally I haven'tav en 't been able to watch it, but is described (Petersen,, 2013)20 13) tthathat “the female spawns a mass of about 40 -70 eeggsgg s and the male, very close to it, proceeds to ferlize theth e egg mass as thetheyy are being expelled and subsequently introducedin tr oduced into the mouth, all in about three seconds. " The eggs showw an orange color and are large, with a diamdi am eteret er close to 3 mmm m and remain grouped by means of adhesiva dh es iv es ccho-ho - rionicon ic filaments. AAerer sspawning,pa wning, the female fofollowsll ow s nextne xt tot o theth e malema le for several even breathing rate lolooksok different (slightly faster). Considering the hypothesis that hohoursur s or evene ve n all thet he dayd ay (we canc an slls l l seese e sporadicsp or adic pphysicalhysical ththisis event coincidescoinc id es with the hatching of larvae inside the male's mouth, I have recor- cocontactsnt ac ts betweenb et we en both). Meanwhile,M ea nw hi le , theth e male focuses on in- dededd a me betweenbe 18 and 21 days unl embryonic development is completed. cucubangba n g eggs.eg gs . DuringDu ri ng the periodper io d of embryonic developdevelopment,ment, OnceOn ce they hatch, the larvae remain in the oral cavity of the male about ten days more ococcasionallyca si on al ly youy ou canc an sees ee thet he malem ale projecng outward from his (occasionally I have registered for this period unl twelve days, with previous paral momouthuth theth e eggeg g massma ss forf or a moment,m om en t, driving out non -viable eggs expulsions of fry). Under these condions the larvae connues to evolve, thanks to en- andan d reintroducingreintr od uc in g "the"t he block"b lo ck " of eggse gg s aliveal ive promptly. In the dogenous food provided by their large yolk sac. In the literature, several authors con- oralor al cavity of thet he malem al e embryoem br yo developmentd ev el op me nt connues unl template mes ranging from a minimum of 18 and a maximum of 28 days for the enre compleon.mp le o n. InI n theth e processespr oc es se s of incubaonincub a on I haveh ave beenbe en able to process. be monitoredon itored ini n my tanks,tan ks , thereth er e comesco mes a me whwhen a slight changes canca n be appreciateda pp re ciated ini n theth e oral cavityc av it y and the degree of During the days of the whole process, from spawning to the expulsión of the larvae, opening in thet he gillg il l coversco ve rs (both areas lookl oo slightly bulkier), the male does not feed. The female does it normally.

Pterapogon kkauderni,au de a unique species 3 All rights reserved: ©José María Cid 2014

Among my pairs of P. kauderni, has been prevalent in their first spawnings, that the male disrupts incubaon in the first week, usually on the 4th or 5th day. Has not been possible objecfy if the cause of interrupng the process is movated by reasons of infer- lity in the spawns or perhaps for reasons of stress in the newly for- med couples. Addionally, two adult males with several incuba- ons already made, stopped the process and expelled the egeggsgs when they were disturbed (they are very sensive duriningg this pe- riod to any work on the aquarium).

When the larvae are finally released (usuallyal ly I've detedetectedcted them early in the morning), we can see thatat theyt hey are already ny replicas of their parents (without havingng gone through any larvlarvalal pelagic stage). In nature, larvae seseekek protecon in the vicinityvicinity of the tenta-te nt a- cles of an oro r between the spines of a sea urcur chhin,in , whilewh il e in the aquarium theyt he y try to adapt to anything that givesgi ve s tthhemem a ssafeaf e shelter. Larvaear va e have presented a size between 7 anandd 8m m LTLT.. TheyTh ey are trtranslucent,an slucent, but show many melmelanophoresan op ho re s andan d finsfin s strongronglyly It wwasas offered as first foodfood,, newbornne nauplii Artemia salina enriched with essenal fay pigmentedpi gm ented in black. Larvae presentp re se nt ono n itsit s flanksfla nk s twotw o vveercalr cal stripes, acacids:ids: the Ω-3 HUFA. docosahexaenoicdo a. (DHA) and eicosapentaenoic a. (EPA) and the Ω-6. theth e firfirstst at eye level and the sesecondco nd ata t theth e beginninbe gi nn ingg of the dorsal arachidonic acid (ARA).( AR An effecve way to enrich the nauplius is to wait unl the first moult fin.fin . MorphologicallyMo rp ho lo gi ca ll y theyth ey are a faithfulf ai th fu l refleconre fle con in miminiatureniature of the (a(aboutbout 6 -8 hohours aer hatching) and then proceed to provide a mixture of unicellular algae: adultad ul t specimens.sp ec im en s. They are vigorous,vi go ro us , photophilic and rremainemain close IsocIsochrysishr ys is sp. (66%) and Nannochloropsis sp. (33%). Before that me the nauplius don't to tthehe surfaces ur fa ce anda nd closec lo se to theth e light source. They araree always posio- bebegingi to feed by filtering of suspended parcles. Isochrysis sp . presents together with Pavlo- nenedd in anglea ng le withw it h respectre sp ec t to thet he water surface, with tthehe head direc- va sp. one of the nutrient profiles with higher levels of DHA between phytoplankton species tedte d totowardwa rd it.i t. TheyT he y do notn ot seems ee m especially frightenedfrightened.. ConsideriConsideringng commonly cultured. Complementarily, Nannochloropsis sp . has a high level of EPA. For the theth e full sets et ofo f my experiences,e xp er ie nc es , the numbernu mb er of larvae finally expelledex pe first two or three days, I have preferred to use Artemia cysts of medium size (nauplius with hasha s rangedrang ed fromf ro m a minimummi ni mu m of fourf ou r andan d a maximumma ximum of ten.t en 450 μ of length). The food is accepted from the first moment. The larvae are very acve du- The larvaela rvae area re ccollectedol le cted aandnd transferredt ra nsferred for its develd ev opment to an ring the day in mid -water. They are provided with a long photoperiod, with just 6 hours of aquariumum of aboutab ou t 10 L. simplysi mp ly equippede quipped withwi th a line of gentle aera- night. During the night, they stay in the mid -water aquarium. (nauplii and semi - on and variousva riou s objectsob je cts on thet he boom,bo om simulang "arficial sea adults) are an excellent alternave to A. salina nauplii, given that unlike Artemia, directly urchins". provide certain levels of DHA and EPA.

Pterapogonap og on kkauderni,au de a unique species 4 All rights reserved: ©José María Cid 2014

Larvae constantly look for food near the surface and mid - water. Well fed the growth is appreciated right away. When compleng the first week of free swimming (about 17 days aer birth), the specimens measures 1 cm LT of average and have completed their pigmentaon. Somemes, I have obser- ved a peculiar behavior: "if the light of its aquarium suddenly switch on, without going through a state of so light, then they go into shock and fall down laterally on the substrate and re-e- main moonless as if dead during 20 -30 seconds, aerer wwhichhich go to mid -water normally ". Similar behaviors hass beenbe en descri- bed by other authors (Vagelli, 2004) who haveav e linked those aab-b- normal behaviours to deficiencies of essenales se nal fay acidacidss in the diet. When compleng three weeksee ks of free swimming, thirtythirt y days post hatching (30 dph),ph ), theyt he y maintain a remarkable growth rate, averagingng 11.5.5 cm LT. At this stage of itsits devdevelop-el op - ment significant sizesi ze differences are seen between diffd iff ererenten t specimens. AtA t this point, changes are introduced intoi nt o theth e didiet,et , providingid in g both CyclopsCy clops sp. lyophilizedly ophilized as differentd iff er en t porridgepo rr id ge ofo f At ffourou r months they averageaver ag e 3,3,1 cm TL, to the five months their size reach 3,4 cm and marinema ri ne mmolluscsolluscs and crustaceancrustaceanss finelyfin el y sieved.si ev ed . TheTh e realire al ittyy is whwhenen they are seven momonths old are near of 4,5 cm TL. In the literature are cited some thatth at theyt he y arear e very selecve wiwithth tthehe nnewew ffoodsoo ds aandnd becausebecause ooff developments fasterf as te than what I've registered in my experience. Sexual maturity is this,th is , remainre ma in asa s theirth ei r mainma in food,f oo d, thet he naupliin au pl ii and metanaumetanaupliupliu reached ababoutou nine months old. enrichedenri ch ed ofo f ArtemiaAr te mi a salisalinana . Promptly,Pr om pt ly , theyth ey are moved to a se- cond aquariuma qu ar iu m of 303 0 L equippedeq uipp ed with a filtraon systemsystem,, which BaBasicsi c maintenance during development includes daily siphoning the boom of the bre- generatesge ne ra te s a cucurrentrr en t agagainstai ns t whwhichic h the young of P. kauderni eding tank and two water changes per week. In the eleven full developments of fry per- swimsw im incessantly.inc es sa nt ly . TheTh e photoperiodph ot op er io d waswa s reduced to 14 hh.. When formed, has been observed in some cases, the appearance of a specimen that has pre- theyth ey reach ttwowo mmonthson th s theth e growthgr ow th raterat e reremainsma ins high, the lar- sented defects such as "deformed operculum". Usually these abnormal specimens have gestst sspecimenspe cime ns mmeasuredea su re d 2.2.22 cm LT. OverO ve r mmee the growgrowthth rate not reached adulthood. In all developments, the number of larvae expelled by breeding is somewhatew ha t lower,lo we r, averaginga vera gi ng 22.7.7 cm when they rereachac h three males has been much less than the mass of spawned eggs (between 10 and 25%). months oldo ld (at thist hi s mem e the dietdi et includesi nc ludes frozenfroz en crustaceans and small crushedcr ushe d drydr y food).fo od ). The contrasted longevity of the species in aquarium is about five years.

Pterapogonog on kkauderni,au de rni, a uuniqueni species 5 All rights reserved: ©José María Cid 2014

Current status of the species: threats and opportunies

As the abundant literature on this unique and beauful species has repeatedly pointed out, several aspects of its biology ma- kes it a highly vulnerable species . It should first be noted that this is a species whose ontogenesis does not provide a pelagic larval stage, so the species does not have great capabilies of expansion towards new areas. Secondly, we have their repep ro- ducve strategy based on oral incubaon with spawnswn s of jjustust 40 -70 eggs, which represents a very low potenalen a l of ferlity.ferlity. Its popularity in the marine aquarium hass generatedge nerated an intensi- ve capture since almost a decade, whwhichic h has resulted in a signi- ficant decrease of their wild populaonsp op ul aons according to various field surveys (Lunn and MoreauM or eau 2004 Vagelli 2005). DuDuee to all of those circumstances,nc es , the species is found since 2200007,7, iinclu-nc lu - ded in the Reded ListL is t of Threatened Species IUCN withwit h ththee ststatusat us "EN" v3.11 (A(Allen,llen, 2007). The situaon worsened evene ve n momorere whenen in 2012 it began to be detecteddetect ed in navena v e specimsp ec im ensen s im- poported,rt ed , an increased incidenceinciden ce ofo f a viralvi ra l diseasedi se as e (irido(i ri do vivirus)ru s) In thist hi s sense, different instuonsins tu o and public aquariums have launched several bre- cacapablepa bl e of killing a large numbern um be r of individualsi nd iv id ua ls of thithiss species ededinging programs in rerecentce nt years. Although the key to its final success will depend largely in a shorts ho rt me. me . on good interninternaonala on coordinaon and appropriate stance of marine aquarists, in the sense of vverifyinger if yi the origin of the specimens prior to purchase. HoHowever,we ve r, tthehe ffactac t ththatat its ccapveap ve breeding is feasiblefeasible and rela- vvelyel y sisimplermp le r thanth an othero th er tropicaltro pi cal marine species kept in aqua- AnAnotherot he possibility would be, some kind of controlled reproducon of this species in ririumum createsc re at es a ggreatre at oopportunitypp or tu ni ty to improve the expexpectaonsectaons "fish farms" located in natural microhabitats. In this regard it is noteworthy that the of mediummed iu m-tetermrm ssurvivalur vi va l of thet he species.s pe ci es . This opportunity for species was arficially introduced in 2000 in the Lembeh Strait, North Sulawesi, outside bebecomingcoming a reality,r ea lity, haveha ve to be aablebl e intoin to thet he trade of orornamen-na me its natural range (Allen, 2007). Subsequent scans have verified that this subpopulaon tall fishes,fis he s, ofo f replacingre pl ac in g theth e P. kauderni spspecimensec im ens takenta ke from has prospered. © the wiwildld by specimenssp ec im ens bredbr ed in capvity.ca pvity. For more informaon or contact with the author : www.aquacnotes.com

Pterapogonap og on kkauderni,au de rn i, a unique species 6 All rights reserved: ©José María Cid 2014

Works cited Allen, G.R. and R.C. Steene, 1995. Notes on the ecology and behaviour of the Indonesian cardinalfishfis h (Apogonidae(A pogonidae)) PterapogonPter ap og kauderni Kou- mans. Rev. Fr. Aquariol. 22(1 -2):7 -10.

Allen, G.R & Donaldson, T.J. 2007. Pterapogon kauderni. In: IUCN 2013. IUCN Red List ooff ThreatenedTh reatened Species. VVersionersion 2013.2. Lunn, K. E.; Moreau, M. -A. 2004 Unmonitored trade in marine ornamental fishes:he s: the case of Indonesia’s Banggai cardinalfishcardi na lfi sh (Pterapogon( Pt er ap kau- derni). Reefs, 2004, vol. 23, no 3, p. 344 -351. Bernardi, G., & Vagelli, A. (2004). Populaon structure in Banggai cardinalfish,c ar dinalfish, Pterapogon kauderni, a coral rer eeeff spspeciesec ie s llackingac king a pepelagicla gi c larval phase. Marine Biology, 145(4), 803 -810. Vagelli, A. (2004). Significant Increase in Survival of Capve-bredap ve-bred Juvenile Banggai CardinalfishCardinalfis h PterapogonPt er ap og on kaudernk au dernii withwi th ana n E ssenalss en a l FayFa y Acid-A ci d- Enriched Diet. Journal of the World Aquacultureur e SocieSo ciety,ty, 35(1), 61 -69.69 . Vagelli, A. (2011). The Banggai Cardinalfish:fis h: Natural HisHistory,tory, Conservaon, and CCultureul tu re ofo f PterapogonPt er ap og on kaudernikau de rn i (Wiley,2011),il ey ,2 01 1) , Pedersen,M. (2013). “Banggai bbreedingre ed ing 101”. Coral magazinemagazine 10 -11.20111.20133

Pterapogon kauderni, a unique species 7 All rights reserved: ©José María Cid 2014