s3-us-west-2.amazonaws.com · befne

INTRODUCTIONThe Banggai cardinalfish Pterapogon kauderni

Koumans 1933 is a small and visually attractive shallow-water reef fish popular in the marine aquarium trade The

known endemic distribution is extremely limited fora marine fish with plusmn30 km2 of habitat spread over around 32small islands within an area of plusmn5500 km2 (Vagelli 2008)Introduced populations have become established along

ACTA ICHTHYOLOGICA ET PISCATORIA (2013) 43 (3) 237ndash250 DOI 103750AIP201343308

Correspondence Ir Samliok Ndobe MSi Fakultas Peternaken dan Perikanan Universitas Tadulako Kampus Bumi Tadulako Palu 94118 Sulawesi TengahIndonesia phone +624514744436 fax +624514131334 e-mail samndobeyahoocom (soemarnoyahoocoid eyulihyahoocoid dsetyohadiyahoocomabigail2105yahoocom mpalomaresfisheriesubcca dpaulyfisheriesubcca)

LIFE HISTORY OF BANGGAI CARDINALFISH PTERAPOGON KAUDERNI(ACTINOPTERYGII PERCIFORMES APOGONIDAE) FROM BANGGAI ISLANDS

AND PALU BAY SULAWESI INDONESIA

Samliok NDOBE 1 2 SOEMARNO 1 Endang Y HERAWATI 1 Daduk SETYOHADI 1Abigail MOORE 3 Maria LD PALOMARES 4 and Daniel PAULY 4

1 Faculty of Marine and Fisheries Science Brawijaya University Malang Indonesia2 Faculty of Animal Husbandry and Fisheries Tadulako University Palu 94118 Indonesia

3 Fisheries and Marine Science Institute (STPL) Palu 94118 Indonesia4 Sea Around Us Project Fisheries Centre University of British Columbia Vancouver Canada

Ndobe S Soemarno Herawati EY Setyohadi D Moore A Palomares MLD Pauly D 2013 Life his-tory of Banggai cardinalfish Pterapogon kauderni (Actinopterygii Perciformes Apogonidae) inBanggai Islands and Palu Bay Sulawesi Indonesia Acta Ichthyol Piscat 43 (3) 237ndash250

Background The paternal mouthbrooding Banggai cardinalfish Pterapogon kauderni Koumans 1933 has anexceptionally restricted endemic range for a marine fish is traded internationally as a marine ornamental and list-ed as endangered in the IUCN Red List This paper aims to contribute to the body of knowledge regarding thebiology of this species based on studies on the endemic population in the Banggai Archipelago and the intro-duced population in Palu Bay Central Sulawesi Province IndonesiaMaterials and methods Length frequency data collected over the period 2004ndash2012 (n = 23 230) were analysedusing the ELEFAN approach (FiSAT software) A lengthndashweight relation was derived from measurements of1002 individuals from the Banggai Archipelago Specimens from the Palu Bay population were used to studyreproductive parameters (n = 80) morphometric relations (n = 54) and feeding habits (n = 30)Results The ELEFAN analysis suggested an annual recruitment peak (September to December) and VBGFparameter estimates of Linfin = 71 cm (SL) K = 074 yearndash1 and t0 = ndash011 year suggesting first maturity at 1 yearand longevity of 3ndash5 years Total mortality (Z) and natural mortality (M) estimates of 44 yearndash1 and 22 yearndash1

yielded fishing mortality F = 22 yearndash1 and exploitation rate E = 05 Lengthndashweight relation parameters werea = 018 b = 215 There was no significant morphological difference between sexes Gonad maturation beganat 29ndash35 cm SL all specimens ge 42 cm SL were sexually mature Mean observed fecundity (59 n = 21) andnumber of eggs brooded by males (59 n = 17) were similar Observed sex ratio was 167 males per female Gutcontent indicated an omnivorous predominantly carnivorous diet Copepods and decapod larvae were the mostabundant components in adult (SL ge 42 cm) and sub-adult (SL le 42 cm) diets respectively Adult diet appearedto be more varied No empty guts were observedConclusion This study provides data for a major reassessment of Pterapogon kauderni life history parameters inFishBase the global database of fishes P kauderni spawning is associated with the lunar cycle the seasonalrecruitment peak is probably related to improved reproductive success during the calm season With strong indi-cations of a decline in the endemic population due to habitat degradation and loss (independent of fishing pres-sure) current exploitation levels may be unsustainable Research is required to further refine life-history param-eters (eg sex ratio) and elucidate issues such as fasting in brooding male Banggai cardinalfish and ontogeneticdifferences in diet

Keywords growth mortality length-frequency ELEFAN lengthndashweight relation maturity reproduction dietand feeding habits

several trade routes including at least two sites in PaluBay (Moore and Ndobe 2007) The Banggai cardinalfishis a paternal mouth-brooder with direct development andwithout pelagic dispersal phase as the larvae on releaseswiftly seek refuge in nearby substrate (Vagelli 1999)Post-release Banggai cardinalfish maintain a sedentarylifestyle with high site fidelity (Kolm et al 2005)

Considered at risk of extinction in the wild due toover-exploitation for the marine aquarium trade (Lunnand Moreau 2004) and habitat degradation (Moore et al2011 2012) international concern has led to listing of theBanggai cardinalfish as endangered in the IUCN(International Union for the Conservation of Nature) RedList (Allen and Donaldson 2007) While a number ofstudies have been published on various aspects ofPterapogon kauderni biology and ecology literature onspecific Banggai cardinalfish life-history traits both in itsendemic distribution area and for the introduced popula-tions remains limited as reflected by the paucity of lifehistory data in FishBase (Froese and Pauly 2013) Thispaper presents data on life-history parameters of P kaud-erni including growth mortality reproduction and dietbased on research carried out over 8 years (2004ndash2012) inthe Banggai Archipelago and in Palu Bay CentralSulawesi Province Indonesia This information will con-tribute to the knowledge base for conservation manage-ment of the species

MATERIALS AND METHODSSampling Banggai cardinalfish Pterapogon kaudernispecimens were captured at Bone Baru Banggai Islandand in Palu Bay (Fig 1) using a lsquocangrsquo-style mobile fykenet such as used in the ornamental fishery The dates andcoordinates for each site as well as the number of fish cap-tured post-capture treatment and use in this study aregiven in Table 1 and the habitats defined as followsbull Coral reef (CR) coral reef area near the reef crest or

upper slopebull Reef flat (RF) flat or slightly sloping areas shoreward

from the reef crest substrate dominated by coral or deadcoral and rubble

bull Seagrass (SG) areas shoreward from the reef crest sub-strate usually predominantly sandy with visually obvi-ous seagrass cover some coral andor rubble

bull Mangrove (MG) between the prop roots of Rhizophorasp mainly below the low-tide line

Length-frequency data were also obtained from belttransect surveys (transect size 20 m times 5 m = 100 m2 cen-sus of fish within transect) carried out over the period2004ndash2012 The number of fish month and year areshown in Table 1 The sea surface temperature (SST) andother environmental parameters at the sampling sites aregiven in Table 2Growth and mortality The available length frequencydata were regrouped into 6 mm classes (0ndash59 6ndash119 etcwith class mid-lengths [ML] at 3 9 etc see Table 3) thenanalysed using the FISAT II software (Gayanilo et al 2005)to obtain estimates of the parameters of the von

Bertalanffy Growth Function (VBGF) of the formLt = Linfin middot (1 ndash endashK(t ndash t

0)) [1]

where Linfin is the mean length the fish would attain is theywere to live indefinitely K (timendash1) is the rate at which Linfin isapproached and t0 the predicted lsquoagersquo at a length (orweight) of zero (Pauly 1984) Specifically Linfin was esti-mated from a Wetherall Plot (Wetherall 1986) as imple-mented in FiSAT II K was estimated by its lsquoscanning forK routinersquo and t0 was estimated by solving equation [1]for a size at known age once Linfin and K had been estimat-ed (see below) Note also that longevity (tmax) if it isassumed to be the age at which fish reach 95 of Linfin canbe approximated by tmax asymp 3 middot Kndash1 (Pauly 1984)

Comparisons between pairs of Linfin and K estimates wereperformed using an index of growth performance (oslashrsquo)defined by the formula proposed by Pauly (1983 2010)oslashrsquo = log(K) + 2 middot log(Linfin) [2]

Natural mortality (M) was estimated from the empiri-cal equation (Pauly 1980)log(M) = ndash00066 ndash 0279 middot log(Linfin) + 06543 middot log(K)+ 04634 middot log(T) [ 3 ]where Linfin is expressed in cm K is in yearndash1 and T is themean water temperature in degC

Total mortality (Z) was then estimated using a length-converted catch curve (Pauly and Ingles 1981) thusallowing fishing mortality (from Z ndash M = F) and exploita-tion rate (from E = F middot Zndash1) to be estimated as wellLengthndashweight relation and other morphometrics Theparameters lsquoarsquo and lsquobrsquo of a lengthndashweight relation of the formW = a middot Lb [4]where W is the wet weight in g and L is the standardlength (SL) in cm were determined from the analysis of1002 Banggai cardinalfish specimens collected fromBone Baru in the Banggai Archipelago The length (L) ofeach specimen was measured to the nearest millimetre(mm) The specimens were then weighed to the nearest01 g and the weights averaged within each mm lengthclass A linear regression was then fitted to the log-trans-formed variables ie L and the corresponding (mean)weights which leads to an equation of the formlog(W) = log(a) + b middot log(L) [5]

Fifty four specimens from Kadongo in Palu Bay weremeasured to the nearest mm to relate their standard lengthto a number of other morphometric features (Fig 2) Theratios of each measurement to standard length were thencalculated and averaged for females (n = 27) males(n = 27) and for the entire sample (n = 54) The ratios forfemales and males were compared using one-way analysisof variance (ANOVA) Linear regression was performedfor the ratio of total length to standard length (TL middot SLndash1)Reproductive biology Each specimen (n = 80) was dis-sected and the gonad removed and weighed The gonado-somatic index (GSI) was calculated fromGSI = Wg middot Wndash1 [6]where Wg is the gonad weight and W is the total bodyweight Eggs were counted in both females (in developingegg masses) and males (in their buccal cavities) In juve-nile specimens where sex was not visually apparent his-

Ndobe et al238

See Sulawesi Case StudymdashBanggai Kepulauan (Bangkep) Pp 5ndash143 and pp169ndash228 In Indonesian ornamental fish trade Case studies and options for improvinglivelihoods while promoting sustainability in Banggai and Banyuwangi The international seafood trade Supporting sustainable livelihoods among poor aquaticresource users in Asia (EC Prep Project EPRO3R14) Available from httpaquaticcommonsorg22471IndonesianOrnamentalFishTrade_optpdf

tological preparations were made and examined undera binocular microscope (4 times 20 magnification) The eggscontained in the egg sacs were clearly visible besidemature and maturing ovaries this yielded fecundity (num-ber of eggs in female specimens) This was complement-ed by effective fertility (number of eggs brooded bymales) size at first maturity and sex ratio (number ofmales times number of femalesndash1) of the sampleFeeding habits Specimens from the Palu Bay populationused in the feeding study (n = 30) were measured andweighted (see above) and their gut tract was thenremoved and assessed as to its fullness which rangedfrom very full to near empty (there were no empty guts)

Each gut tract was then weighed (to the nearest 001 g)and the gut contents separated using 70 alcohol(4 drops) and prepared for examination under a (4 times 10magnification) binocular microscope Food item identifi-cation was based mainly on Sachlan (1972)

RESULTSEnvironmental parameters All specimens of Pterapogonkauderni were collected from shallow (maximum 6 m)coastal waters mainly embayments or lagoons or otherhabitats sheltered from strong wave action (eg mangrovestands) Environmental parameter values at the sites whereP kauderni samples were collected are given in Table 2

Life history of Banggai cardinalfish Pterapogon kauderni 239

Fig 1 Map of Central Sulawesi showing the locations of the sampling sites mentioned in the text and tables of thiscontribution

The observed water temperature range was 26ndash31ordmCDespite a preponderance of readings of 29ordmC the averagetemperature in P kauderni habitat is probably 28ordmC giventhat temperatures are lower at night when few sampleswere taken Salinity was in the PSS 29ndash35 range at allsites and in all seasons where measurements were takenGrowth and mortality The largest specimen found inthis study also seems to be the largest specimen ofPterapogon kauderni reported to date This specimena female provided a valueofLmax = 66 cm (SL) and 86 cm (TL)and a weight of 113 g

The analysis of the length-frequency data in Table 3yielded SLinfin = 71 cm (or TLinfin = 107 cm Table 4) and

K = 074 yearndash1 (Fig 3) Given these parameter valuessolving the VBGF [equation 1] for a length of 4 cm at1 year (taken to be the mean length and age at first matu-rity respectively see below) yields an estimated t0 asymp ndash011Thus the growth in SL of P kauderni can be described byLt = 71 middot (1 ndash expndash(074(t + 011))) [7]which implies a longevity of 3ndash5 years

Total mortality Z was 44 yearndash1 (Fig 4) Subtracting Mestimated for a temperature of 28ordmC as 22 yearndash1 yieldsan estimate of F as 22 yearndash1 and an E of 05Lengthndashweight relation and other morphometrics The1002 Banggai cardinalfish Pterapogon kauderni in thisstudy ranged from 1 cm to 6 cm The 48 log-transformed

Ndobe et al240

Date [DMY](time) Sampling site Latitude

Longitude Fish sampled Field treatment Primary use

291008(1000ndash1300)

Mamboro(Palu Bay)

0deg47prime51primeprimeS119deg52rsquo14rdquo E 30 Preserved in 70 alcohol Diet study

120509240509170709310709(0900ndash1200)

Kadongo(Palu Bay)

0deg44prime51primeprimeS119deg51prime21primeprimeE

20202020

Preserved in 70 alcohol Reproductivebiology

261211(1500ndash1700) Bone Baru 1ordm31prime53primeprimeS

123ordm29prime35primeprimeE 1003Fixed in formalin(4 for 24 h)then preservedin 70 alcohol

Growthparameters

S

Table 1Details on samples of Banggai cardinalfish Pterapogon kauderni

collected from 2008 to 2011 in Central Sulawesi

Site MonthYear

Time of day[GMT + 8]

SST[ordmC]

Depth[m]

Salinity[psu]

HabitatEcosystem

Popisi

122011

0800 28 05ndash15 34 CR RF SGBone Baru 0700

15002829 05ndash3 32 CR RF SG

Paisulimukon 1100 29 05ndash3 34 CRTinakin Laut 0830 28 1ndash2 33ndash34 RF SGMonsongan 1130 29 1ndash2 34 RF SGTolokibit 1100 29 1ndash2 30ndash32 RF SGMatanga 1300 29 1ndash2 m 31ndash32 RF SGTinakin Laut 042007 0830ndash1730 30ndash31 05ndash3 32ndash35 CR RF SGTanjung Nggasuang

062012

1000 29 1ndash3 33 LagoonKokudang 0830 29 1ndash3 34 CR RF SGToropot 1230 29 1ndash2 mdash SGMbuang-Mbuang 1200 29 1ndash2 mdash SG sandToado 1000 29 1ndash2 33 MG RFBone Bone 0930 29 05ndash3 mdash RF SG sandP Bandang 1040 28 05ndash6 mdash CR RF SG

Mamboro 112006102008 Monitoring (24 h) 26ndash31 05ndash4 29ndash34 CR SG

Kadongo 052009072009 1030 29 1ndash3 32 CR RF SG

M

Table 2Environmental parameters at Banggai cardinalfish Pterapogon kauderni

sample collection sites (Central Sulawesi)

GMT = Greenwich mean time SST = sea surface temperature CR = coral reef RF = reef flat SG = seagrass MG = mangrove

data pairs used for the analysis are shown in Fig 5 alongwith the linear regression log(W) = 2151 middot log(SL) ndash0744 (r = 0993) from which the relation W = 018 middot L215

can be derived Thus the growth in (wet) weight ofP kauderni can be described byWt = 122 middot (1 ndash expndash(074(t+011)))215 [8]

Figure 6 illustrates the growth in length and weight ofP kauderni as inferred from the data presented so far

Morphometric parameters and weight of the speci-mens measured in this study are given in Table 4 forfemales and males Differences between males andfemales in average values of the ratios calculated were notsignificant (F lt Fcrit α = 005 = 403) except for the mouthgape (MG) to standard length ratio (F = 752 gt Fcrit α = 001= 715 P = 00083) There was no significant differencebetween the TL middot SLndash1 ratio for males and females


ML 2004 2006 2007 2009 2011 2012[mm] Oct Nov Nov Dec Apr Jul Oct Sep Sep Dec Jun 3 0 0 0 0 0 0 0 0 0 0 0 9 14 9 77 21 76 72 75 13 84 542 68515 17 10 141 194 161 59 101 21 89 581 98921 12 8 151 177 355 84 112 86 98 1301 258627 11 7 109 96 291 70 89 69 91 1213 187433 9 6 39 46 153 67 78 36 79 409 132539 7 8 48 35 118 114 69 49 98 533 57745 9 17 94 84 296 129 64 84 39 567 117451 13 19 135 91 248 147 125 91 40 396 217357 3 7 25 10 57 9 39 5 6 38 16563 0 0 0 0 1 0 0 0 0 0 6Total 95 91 819 754 1756 751 752 454 624 5580 11554

P

Table 3Standard length-frequency data of Banggai cardinalfish Pterapogon kauderni sampledin the Banggai Archipelago over the period of 2004ndash2012 based on 6-mm size classes

ML = class mid- length (n = 23230)

Fig 2 Schematic representation of a specimen of Banggaicardinalfish Pterapogon kauderni illustrating wheremeasurements were taken TL = total length SL =standard length HH = head height BH = body heightCF = caudal fin length DF1 = anterior dorsal finlength DF2 = posterior dorsal fin length VF = ventralfin length AF = anal fin length PL = pectoral finlength (not shown) and MG = mouth gape (not shown)

Fig 3 Output of the ELEFAN software routine scanningfor the optimal estimates of K for Banggai cardinal-fish Pterapogon kauderni given SLinfin = 71 cm andthe length-frequency data in Table 3 The best esti-mate of K = 074 yearndash1 corresponding to a longevityof 3ndash5 years

(F = 0007 lt Fcrit α = 005 = 403) The mean value of theratio of TL to SL plusmn SD expressed in percentage points wasasymp 150 plusmn 12 and linear regression of TL versus SL yieldeda slope plusmn SE of 15 plusmn 01 with an r2 of 099 (n = 54) Themean aspect ratio (standard length divided by bodyheight) plusmn SE was 207 plusmn 002 for the total sample (N = 54)and was not significantly correlated with length(r2 = 0001) or sex (F = 101 lt Fcrit α = 005 = 403)Reproductive biology A synopsis of the data on femalePterapogon kauderni gonad development is shown inTable 5 (n = 30) The (single) gonad shape and size wassimilar in male and female P kauderni varying in colour(paler in males) and texture (granulose in females)Developing masses encased in an egg envelope were pres-ent in most adult female specimens Mature male andfemale P kauderni gonads photographed during thisstudy are shown in Fig 7

Effective fertility based on numbers of eggs or larvaebrooded by male specimens (13 specimens collected fromBone Baru and 4 brooding males collected at Kadongo)ranged from 45 to 99 eggs with a mean value plusmn SE of59 plusmn 27 eggs or larvae Several other males captured duringthe lengthweight study were also brooding however the eggsor larvae were released on capture and could not be recov-ered for counting The smallest of these had an SL of 42 cm

A regression of fecundity and fertility against bodysize (SL or W) showed no significant trend (P gt 005r2 lt 01) and thus fecundity in adult P kauderni can be

summarized by their mean fecundity plusmn SE (58 plusmn 4 eggsper female) The similarity between fertility estimatesbased on numbers of eggs in female gonads andeggslarvae brooded by male P kauderni indicates thatfew (if any) eggs are lost in the process of fertilisation andtransfer to the male buccal pouch The sex ratio of the(random) sample (n = 80) was 167 ie heavily biasedtowards males

Table 6 shows the percentages of occurrence of vari-ous stages of gonad development in male P kauderniMale gonad development began at SL asymp 3 cm and all male

Ndobe et al242

ParameterAdult Male P kauderni

(n = 27 SL 43ndash54 cm)Adult Female P kauderni(n = 27 SL 41ndash57 cm) ANOVA

ndashAverage SD SE Average SD SE

SL [cm] 486 033 006 487 043 008 nsW [g] 489 123 024 478 134 026 nsc

TL middot SLndash1 [] 15043 1238 238 15017 1050 202 nsDF1 middot SLndash1 [] 3603 614 118 3384 518 100 nsDF2 middot SLndash1 [] 7423 1525 294 6685 1809 348 nsPF middot SLndash1 [] 2649 618 119 2510 355 068 nsVF middot SLndash1 [] 4534 465 090 4430 388 075 nsAF middot SLndash1 [] 3859 638 123 3841 691 133 nsCF middot SLndash1 [] 4973 726 140 4684 627 121 nsHH middot SLndash1 [] 3713 678 130 3719 487 094 nsMG middot SLndash1 [] 2789 277 053 2551 358 069 vsTL middot BHndash1 []a 306 029 006 314 028 005 nsSL middot BHndash1 []b 204 019 004 209 016 003 nsMG middot SLndash1 range 2273ndash3265 1951ndash3333

M

Table 4Standard length (SL) weight (W) and 13 morphometric ratios (expressed as percentages)

for 27 male and 27 female Banggai cardinalfish Pterapogon kauderni and significance levelsof a one-way analysis of variance (ANOVA) for male () versus female () specimens

SD = standard deviation SE = standard error ns = not significant (F lt Fcritα = 005 = 403) vs = very significant (F = 752gt Fcritα = 001 = 715 P = 000835 lt 001 n = number of fish measured TL = total length SL = standard length DF1 = ante-rior dorsal fin DF2 = posterior dorsal fin PF = pectoral fin AF = anal fin CF = caudal fin HH = head height MG = mouthgape BH = body height a average aspect ratio for TL (n = 54) = 310 (SD = 028 SE = 004) b average aspect ratio for SL(n = 54) = 207 (SD = 018 SE = 002) c ANOVA male vs female for SL3 middot Wndash1 was also not significant

Fig 4 Length-converted catch curve for Banggai cardi-nalfish Pterapogon kauderni as used to estimateZ = 44 yearndash1 from the 3 largest length classes

specimens with a SL of 4 cm or above were either repro-ductively active (brooding andor spent) or appearedphysically capable of reproduction Female gonad devel-opment was less well documented due to sample size(Table 5) However both female specimens in the SL31ndash35 cm size class had gonads in the early stages ofdevelopment and all female P kauderni over 4 cm SL

(n = 28) were either currently producing egg masses(n = 24) including the smallest female over 4 cm SL(41 cm SL) or appeared to have recently spawned (n = 4)Overall this suggests that mean length at first maturity ofmale and female P kauderni is about 4 cm SL asassumed above for the estimation of t0Feeding habits Quantitative gut content data for the sub-


Fig 5 Data points and log transformed lengthndashweight relation in Banggai cardinalfish Pterapogon kauderni ielog(W) = ndash0744 + 2151 middot (logL) with r2 = 0993 n = 1002 Standard error SE of slope = 0025

Fig 6 Estimated mean growth curves in length and weight of Banggai cardinalfish Pterapogon kauderni

adult (SL lt 42cm n = 9) and adult (SL ge 42 cm n = 21)specimens are shown in Tables 7 and 8 Trophic levelcould not be calculated due to the lack of volumeweightdata and the substantial proportion of unidentified items

DISCUSSIONEnvironmental parameters Water quality parameterswere within normal limits for tropical marine fishes andcoral reef ecosystems The observed salinity (PSS 29ndash35)

was within the range for which growth and survival ofPterapogon kauderni juveniles reared in captivity wasacceptable but higher than the value (PSS 27) for whichgrowth and survival were highest (Madinawati et al 2009)Growth mortality and life cycle The estimated asymp-totic length of 71 cm (SL) is higher than the longest fishrecorded by the authors ie 66 cm in Palu Bay butappears reasonable for this species Overall the growthparameters and M that were estimated here suggest that

Ndobe et al244

Moon phase(date) Sample no SL

[cm]W[g] Fecundity Wg

[g] GSI

Full Moon(12 May)

1 450 366 57 023 005 2 450 403 92 032 007 3 460 345 49 027 006 4 470 445 51 028 006 5 480 440 mdash 001 000 6 500 540 50 040 008 7 530 552 mdash 004 001 8 560 668 77 064 011

Mean 488 470 6267 027 006

Dark Moon (24 May)

9 410 384 30 001 00010 540 683 53 006 00111 540 598 60 006 00112 540 678 50 019 00413 660 1130 85 027 004

Mean 636 789 6813 017 003

Waxing (17 July)

14 330 208 mdash 003 00115 340 213 mdash 002 00116 450 494 mdash 008 00217 450 516 45 009 00218 460 437 46 008 00219 460 554 mdash 009 00220 490 539 60 014 00321 540 614 19 009 00222 570 773 86 019 003

Mean 454 483 5120 009 002

Waning (31 July)

23 520 313 64 029 00624 500 495 42 009 00225 490 325 39 011 00226 420 375 102 028 00727 440 292 28 009 00228 470 423 50 007 00129 480 352 55 013 00330 490 393 64 016 003

Mean 476 371 5550 015 003Overall mean 504 511 5887 017 003

S

Table 5Gonad development and fecundity of female Banggai cardinalfish Pterapogon kauderni

in Palu Bay (n = 30)

SL = standard length W = whole body weight Wg = gonad weight GSI = gonadosomatic index = Wg middot Wndash1


Fig 7Mature (single) gonads of male (A) and female (B) Banggai cardinalfish Pterapogon kauderni the white arrowindicates a developing egg mass

A

B

Banggai cardinalfish Pterapogon kauderni hasa longevity of 3ndash5 years and that first maturity is reachedin a year at a size of about 4 cm SL (Table 6 Fig 7)

There are few estimates of growth parameters in car-dinalfishes (Family Apogonidae) with which to compareour results FishBase (Froese and Pauly 2013) providesgrowth parameters for only 5 lsquostocksrsquo in 2 apogonidspecies Apogon imberbis (L) and A lineatus Temmincket Schlegel 1842 (Table 9) However the mean value ofoslashrsquo (see Equation 2) that can be calculated from these5 LinfinK pairs (oslashrsquo = 1911) matches almost exactly the val-ues of oslashrsquo = 1928 computed from the growth parametersestimated for P kauderni (Table 9) and hence our growthcurves are compatible with what little is known of thegrowth of cardinalfishes

Spawning occurs throughout the year but may bemore intensive around SeptemberndashOctober This being

the calm season in most of the Banggai ArchipelagoP kauderni appears to behave as predicted by the lsquotriadhypothesisrsquo of Bakun (1996) as modified by Pauly andNavaluna (1983) which states that fish reproduction inmonsoon-dominated tropical areas peaks in the lullsbetween the monsoons Abesamis and Russ (2010) reporta similar pattern for reef fish in the Philippines withldquopeaks in density and species richness of recruits duringthe [] periods of the year when temperatures were high-est and [] winds were weakrdquo This pattern would explainwhy recruits have been more commonly observed duringfield expeditions in OctoberndashDecember (for example dur-ing the collection of much of the data used in this analy-sis) compared expeditions in the early part of the yearsuch as that reported by Vagelli and Erdmann (2002)

This pattern would also suggest that a cohort ofP kauderni hatched in October would reach first maturi-

Ndobe et al246

SL[cm]

Gonad development stagen

Undeveloped Developing Well developed Mature Spent21ndash25 100 00 00 00 00 126ndash30 750 00 250 00 00 431ndash35 667 167 00 167 00 636ndash40 00 700 200 100 00 1041ndash45 00 00 125 625 250 846ndash50 00 00 67 600 333 1551ndash55 00 00 00 667 333 6

Table 6Male Banggai cardinalfish Pterapogon kauderni gonad development in Palu Bay (n = 50) with bold percentage

values for each size class highlighting the relation between size (standard length) and maturation stage

Values shown are the percentage of the age-class sample in each gonad development stage SL = standard length Wg = gonadweight [g] n = number of specimens in each size class Undeveloped = (Wg lt 02 g) Developing = (Wg ge 02 g) Well devel-oped = (Wg ge 03 g) Mature = (Wg ge 05 g)

Food item Total No of occurrences

Percentage of guts ApproximateSub-adult Adult Overall trophic level

Copepods 120 667 476 533 22ndash32a

Cypris nauplii 105 889 238 467 22ndash26b

Conochilus volvox 90 444 524 500 2a

Planktothrix agardhii 70 111 333 267 1a

Enteromorpha spp 45 111 190 167 1a

Nitzschia spp 25 111 95 100 1a

Asterionella spp 25 0 190 133 1a

Euglena spp 25 0 238 167 1a

Allogromia spp 20 0 95 67 asymp 2Diadema spp 20 111 143 133 24b

Desmidium baileyi 5 0 48 33 1a

Unidentified matter 105 556 571 567 mdash

G

Table 7Food items identified in the guts of sub-adult and adult Banggai cardinalfish Pterapogon kauderni

Sub-adult = (SL lt 42cm n = 9) adult = (SL ge 42cm n = 21) a Anonymous (2008) b Pauly and Christensen (1995)

ty in September of the following year (see also Fig 6)notwithstanding suggestions that P kauderni reaches firstmaturity in about 9 months (Vagelli 1999) Indeeda 9-month lag between hatching and first maturity is hardto conceive for fishes living in the wild as it would causesuccessive cohorts to be out of phase with recurrent annu-al events every 3 out of 4 years

There are strong indications from the most recent surveys(December 2011 and June 2012 Ndobe et al unpublished)that mostP kauderni populations in the Banggai Archipelagoare declining due to habitat degradation and loss added to thestrong fishing pressure quantified here Monitoring andmanagement of the fishery as well as addressing habitatloss and degradation (especially the loss of microhabitatsee Moore et al 2012) are crucial to ensure the conserva-tion of P kauderni which is at risk of extinctionLengthndashweight relation other morphometrics andreproductive biology Growth of Pterapogon kauderniexhibits a negative allometry (b lt 3) The equationW = 018 middot L215 obtained for P kauderni is close to the valuepredicted by the empirical equation for short and deep bod-ied fish in Froese (2006) log a = ndash1358 middot b + 2322A regression using data from 216 mainly juvenile or sub-adult specimens from Kadongo in Palu Bay (Mooreunpublished data) yielded a value of b = 232 which isalso strongly allometric negative and close to the predict-ed value from Froese (2006)

The morphological data also confirm the results ofVagelli and Volpedo (2004) that there is no significantexternal morphological difference between male andfemale P kauderni The only parameter with a statistical-ly significant difference between male and female P kaud-erni was the mouthgape (MGSL) ratio Despite the highconfidence level (99) yielded by the ANOVA the rangeof values for adult male P kauderni was contained withinthe range for adult female specimens The high level ofoverlap and individual variability in MGSL values pre-clude the use of this characteristic for sex determination

However subtle sexual dimorphism may be maskedby the relatively high variance associated with fin meas-urements in P kauderni itself due to the fact that thesefins are extremely vulnerable to damage especially the

caudal and dorsal ones Indeed fin damage is the main rea-son for rejection of market-sized specimens by buyers inthe ornamental fish trade at the lowest (fishermen) tradinglevel and the reason why standard- rather than totallength is the reference length throughout this study

The sex ratio of the sample of 167 males for everyfemale confirmed Vagelli and Volpedo (2004) whowhile finding no significant difference in sex ratio alsohad a sample in which the number of males exceeded thatof females A greater number of males would potentiallyimprove reproductive capacity at population level whilefemale P kauderni are capable of producing eggs ona monthly basis male P kauderni require a period torecuperate after brooding for almost a month or in thewords of Kolm (2002) ldquofemales produce eggs faster thanmales can lsquoprocessrsquo themrdquo

Because of the pair-forming inherent in P kaudernispawning sexual maturity does not guarantee participa-tion in reproductive activity The gonad development datacoupled with field observations suggest that reproductivesuccess in P kauderni may tend to be delayed relative tophysical sexual maturity (gonad development) especiallyin males whose gonad development appears to take placeat a smaller sizeearlier age than brooding Kolm (2001)reports that P kauderni females seem to have a preference


Species (sex) TLinfin[cm]

K[yearndash1] oslashrsquo Location Source

Apogon lineatus (F) 85 123 1949Off Niigata Prefecture Kume et al (2003)

Apogon lineatus (M) 95 050 1654Apogon lineatus (F) 87 112 1928

Tokyo Bay Kume et al (2003)Apogon lineatus (M) 119 037 1719Apogon imberbis (both) 150 090 2306 Mediterranean Pauly (1978) Mean mdash mdash 1911 mdashPterapogon kauderni (M F) 107 074 1928 Central Sulawesi this study

Table 9Growth parameter comparison in three species of cardinalfishes (see text)

based on data in Garnaud (1962) TLinfin = total asymptotic length K = rate at which asymptotic length is approached in the VBGF(Von Bertalanffy Growth Function) oslashrsquo = index of growth performance in terms of total length (TL) = log(K) + 2 middot log(TLinfin)

Groupclass No of food itemsper gut

No of food typesper gut

Sub-Adult 183 plusmn 88 30 plusmn 10

Adult 224 plusmn 123 31 plusmn 11

Overall 218 plusmn 113 31 plusmn 099

Brooding males 300 plusmn 141 35 plusmn 07

S

Table 8Food items and food types in the guts

of individual groupsclassesof Banggai cardinalfishPterapogon kauderni

Values are mean plusmn standard deviation sub-adult = (SL lt 42 cmn = 9) adult = (SL ge 42cm n = 21)

Ndobe S Moore A Salanggon AIM Muslihudin Setyohadi D Herawati EY Soemarno Pengelolaan Banggai cardinalfish (Pterapogon kauderni) melaluiKonsep Ecosystem-Based Approach [Banggai cardinalfish (Pterapogon kauderni) Management - an Ecosystem-Based Approach] [In Indonesian] Article accepted forpublication in Jurnal Marine Fisheries (httpjournalipbacidindexphpjpspindex)

for (and produce larger eggs for) larger males BothVagelli (1999) and Kolm (2001) report that femaleP kauderni are active in the courtship process both inattracting and selecting a mate This is likely to mean thatin a situation where there are sufficient males smallermales may have to wait (and grow) before mating even ifthey are adults in terms of their gonad development

Spawning does not guarantee reproductive success asit is not uncommon for male P kauderni to fail to broodto term In addition many factors affect recruit survival(Moore et al 2012 Moore et al unpublished) Theseinclude the availability of microhabitat especially seaanemones and Diadema sp sea urchins and the preva-lence of predation including cannibalism (observed bothin the wild and in captivity Moore et al 2012) Recruitand juvenile survival seems to correlate negatively withadult P kauderni density (Moore et al unpublished)most likely due to increased levels of cannibalism Seaanemones (an effective refuge against cannibalism) andsea urchins are being exploited at an unprecedented ratedue to recent (over the last 3ndash6 years) changes in humanconsumption patterns and their decline seems to havecaused sharp declines in the P kauderni populationincluding at unfished sites wherever these key microhab-itats have been substantially reduced (Moore et al 20112012 Moore et al unpublished)

In view of the complexity of these issues the biologi-cal parameters related to reproductive output (eg fecun-dityfertility and spawning frequency) are not sufficient toestimate the true resilience or the ability of the species towithstand exploitation It should be remembered that withno pelagic dispersal stage sedentary habit and depth-restricted habitat populations lost through whatever set ofcircumstances are unlikely to ever recoverreturn natural-ly A population on an island off Liang which had beenreduced to 13 individuals by 2004 has not recovered andwas locally extinct at this site in June 2012 (Ndobe et alunpublished) The high level of genetic population struc-ture over distances as short as 2ndash5 km (Hoffman et al 2005Vagelli et al 2009) mean that local extinctions can resultin the total loss of entire genetic strains and make re-stock-ing a controversial issue (Ndobe et al 2012)Feeding habits None of the specimens observed had anempty stomach two brooding males had stomachs thatwere half full and full which appears to be incompatiblewith the assumption (Vagelli 1999) that male Pterapogonkauderni fast while brooding the eggs (around 20 days)and larvae (around 9 days) This phenomenon requiresfurther research however this should be based on speci-mens of opportunity as the sacrifice of large numbers ofbrooding males could have a significant impact on thepopulation of this endangered species

The results in Tables 7 and 8 are consistent with thefindings of Vagelli and Erdmann (2002) who based ongut content analysis of P kauderni collected in theBanggai Archipelago stated that ldquoP kauderni is a gener-alist planktivorendashcarnivore [whose diet includes] repre-sentatives from the benthic and neustonic communitiesrdquo

and compatible with the estimated trophic level ofP kauderni plusmn SE of 33 plusmn 041 currently indicated inFishBase (Froese and Pauly 2013) However a surprising-ly large number of phytoplankton food items were alsoobserved in the gut tracts of adults though such itemswere rare in the gut tracts of sub-adults (Tables 7 and 8)

While crustaceans dominated gut content in terms ofvolume and number of items in both sub-adult and adultP kauderni decapods (cypris stage larvae) were moreimportant in sub-adult gut content and copepods in adultgut content Adult P kauderni in Palu Bay appeared tofeed on a wider variety of food items than sub-adults(Tables 7 and 8) but this could be an artefact of samplesize (21 as opposed to 9 individuals)

Though several taxa recorded by Vagelli and Erdmann(2002) in gut samples from the P kauderni endemic region(Banggai Archipelago) were not observed during thisstudy one taxon reported here apparently for the first timein the diet of P kauderni is a sea urchin most likely thelong-spined sea-urchin Diadema setosum In the BanggaiArchipelago sea urchins are abundant and groups ofDiadema setosum provide the most common microhabitator refuge for P kauderni though it has also been observedassociated with other urchins of the Family Diadematidaein particular Echinothrix sp (Moore et al 2012)

At the Mamboro site (Palu Bay) where P kauderniwas introduced sea urchins (including Diadema sp) arerare It would therefore be reasonable to assume that thefact they were eaten by over 13 of the P kauderni sam-ple could indicate a positive preference However the nat-ural abundance of Diadema setosum and other membersof the Diadematidae in the Banggai Archipelago wouldindicate that this predation if it does indeed occur theredoes not seriously affect the sea urchin population undernatural conditions

The condition of the items recorded as ldquounidentifiedmatterrdquo in Tables 7 and 8 was such that these items couldnot be precisely identified with the resources availableHowever in almost all cases small fragments includingsmall fish bones (mostly broken) were visible While notquantifiable these observations indicate that small fish doform part of the P kauderni diet confirming observationsof predation of new recruits by adult P kauderni immedi-ately or shortly after release both in captivity and in thewild (Moore et al 2012) Detailed bone studies andorgenetic (DNA) studies on the gut content of P kauderni(preferably specimens of opportunity) could no doubt fur-ther elucidate the incidence of piscivory including canni-balism in the species Such a study would also contributeto an informed evaluation of the trophic level of P kaud-erni and in general to the further definition of its niche

ACKNOWLEDGEMENTSThe research presented forms part of the dissertation by

S Ndobe at the Doctoral Program in the Marine Sciencesand Fisheries Faculty Brawijaya University Malang(Indonesia) S Ndobe acknowledges support from theDirectorate of Higher Education of the Ministry of Education

Ndobe et al248

Moore A Ndobe S Siddik J Zamrud M Salanggon AIM Rahman A Population status of the endangered endemic marine ornamental Banggai cardinalfishlinked to societal and environmental factors Paper presented at the International Conference on Marine Sciences 4ndash6 June 2013 IPB International Convention CentreBogor Indonesia See footnote on page 247

and Culture of the Republic of Indonesia in the form ofa travel scholarship to the University of British Columbia(UBC) under the Sandwich Program 2012 BrawijayaUniversity Malang (Indonesia) Tadulako UniversityPalu (Indonesia) the Fisheries Centre at UBC Vancouver(Canada) and the College of Fisheries and MarineScience (Sekolah Tinggi Perikanan dan KelautanSTPL)Palu (Indonesia) provided in kind support during theresearch andor the preparation of this paperML Palomares and D Pauly acknowledge support fromthe Sea Around Us Project a research collaborationbetween UBC and the Pew Environment Group Theauthors thank two anonymous reviewers for their com-ments and Ms Evelyn Liu for the artwork

REFERENCESAbesamis RA Russ GR 2010 Patterns of recruitment of

coral reef fishes in a monsoonal environment Coral Reefs29 (4) 911ndash921 DOI 101007s00338-010-0653-y

Allen GR Donaldson TJ 2007 Pterapogon kauderni InIUCN 2009 IUCN Red List of Threatened Species Version20091 ltwwwiucnredlistorggt [Accessed 22 August 2009]

Anonymous 2008 Lesser Antilles Pelagic Ecosystem (LAPE) proj-ect Trophic levels FI Institutional Websites FAO Fisheries andAquaculture Department [online] Rome Updated 28November 2008 httpwwwfaoorgfisherytopic4210en[Accessed 6 August 2013]

Bakun A 1996 Patterns in the ocean ocean processes andmarine population dynamics California Sea Grant CollegeSystem National Oceanic and Atmospheric Administrationin cooperation with Centro de Investigaciones Bioloacutegicasdel Noroeste

Froese R 2006 Cube law condition factor and weightndashlengthrelationships history meta-analysis and recommendationsJournal of Applied Ichthyology 22 (4) 241ndash253 DOI101111j1439-0426200600805x

Froese R Pauly D (eds) 2013 FishBase [version 062013]httpwwwfishbaseorg

Hoffman EA Kolm N Berglund A Arguello JR JonesAG 2005 Genetic structure in the coral-reef-associatedBanggai cardinalfish Pterapogon kauderni MolecularEcology 14 (5) 1367ndash1375 DOI 101111j1365-294X200502538x

Garnaud J 1962 Monographie de lrsquoApogon meacutediterraneacuteenApogon imberbis (L) 1758 Bulletin de lrsquoInstitutoceacuteanographique de Monaco No 1248

Gayanilo FC Sparre P Pauly D 2005 FAO-ICLARMstock assessment tools II (FiSAT II) Revised version userrsquosguide FAO Computerized Information Series (Fisheries)No 8 revised version Food and Agriculture Organisationof the United Nations (FAO) Rome

Kolm N 2001 Females produce larger eggs for large males ina paternal mouthbrooding fish Proceedings of the RoyalSociety Part B Biological Sciences 268 (1482)2229ndash2234 DOI

Kolm N 2002 Male size determines reproductive output ina paternal mouthbrooding fish Animal Behaviour 63 (4)727ndash733 DOI 101006anbe20011959

Kolm N Hoffman EA Olsson J Berglund A Jones AG2005 Group stability and homing behavior but no kin groupstructures in a coral reef fish Behavioral Ecology 16 (3)521ndash527 DOI 101093behecoari022

Kume G Yamaguchi A Aoki I 2003 Variation in life histo-ry parameters of the cardinalfish Apogon lineatus FisheriesScience 69 (2) 249ndash259 DOI 101046j1444-2906200300615x

Lunn KE Moreau A-M 2004 Unmonitored trade in marineornamental fishes the case of Indonesiarsquos Banggai cardinal-fish (Pterapogon kauderni) Coral Reefs 23 (3) 344ndash341DOI 101007s00338-004-0393-y

Madinawati Ndobe S Gamgulu A 2009 Growth of Banggaicardinalfish Pterapogon kauderni reared at different salinityin a controlled system Jurnal Akuakultur Indonesia 8 (2)193ndash198

Moore A Ndobe S 2007 Discovery of an introduced Banggaicardinalfish population in Palu Bay central SulawesiIndonesia Coral Reefs 26 (3) 569 DOI 101007s00338-007-0227-9

Moore A Ndobe S Salanggon A-I Ederyan Rahman A2012 Banggai cardinalfish ornamental fishery The impor-tance of microhabitat Proceedings of the 12th InternationalCoral Reef Symposium ldquo13C Ecological effects of habitatdegradationrdquo 9ndash13 July 2012 Cairns Australia [5 unnum-bered pages]

Moore A Ndobe S Zamrud M 2011 Monitoring theBanggai cardinalfish an endangered restricted range endem-ic species Journal of Indonesia Coral Reefs 1 (2) 99ndash103

Ndobe S Setyohadi D Herawati EY Soemarno Moore A2012 An ecological and social approach to Banggai cardi-nalfish conservation management Proceedings of the 12thInternational Coral Reef Symposium ldquo17A Science to sup-port the coral triangle initiativerdquo 9ndash13 July 2012 CairnsAustralia [5 unnumbered pages]

Pauly D 1978 A preliminary compilation of fish length growthparameters Berichte des Institut fuumlr Meereskunde an derUniversitaumlt Kiel No 55

Pauly D 1980 On the interrelationships between natural mor-tality growth parameters and mean environmental temper-ature in 175 fish stocks ICES Journal of Marine Science 39(2) 175ndash192 DOI 101093icesjms392175

Pauly D 1983 Some simple methods for the assessment oftropical fish stocks FAO Fisheries Technical Paper No 234Food and Agriculture Organisation of the United Nations(FAO) Rome

Pauly D 1984 Fish population dynamics in tropical watersa manual for use with programmable calculators ICLARMStudies and Reviews 8 ICLARM Manila Philippines

Pauly D 2010 Gasping fish and panting squids Oxygen tem-perature and the growth of water-breathing animalsExcellence in Ecology Book 22 International EcologyInstitute OldendorfLuhe Germany

Pauly D Christensen V 1995 Primary production required tosustain global fisheries Nature 374 (6519) 255ndash257 DOI101038374255a0

Pauly D Ingles J 1981 Aspects of the growth and natural mor-tality of exploited coral reef fishes Pp 89ndash98 In Gomez ED


Birkeland CE Buddemeier RW Johannes RE Marsh JAjrTsuda RT (eds) Proceedings of the 4th International CoralReef Symposium Vol 1 18ndash22 May 1981 ManilaPhilippines

Pauly D Navaluna NA 1983 Monsoon-induced seasonalityin the recruitment of Philippine fishes Pp 823ndash833In Sharpe GD Csirke J (eds) Proceedings of the expertconsultation to examine changes in abundances and species ofneritic fisheries resources FAO Fisheries Report No 291 (3)Food and Agriculture Organisation of the United Nations(FAO) Rome

Sachlan M 1972 Planktonology Direktorat Jenderal PerikananDepartemen Pertanian Jakarta Indonesia [In Indonesian]

Vagelli A 1999 The reproductive biology and early ontogenyof the mouthbrooding Banggai cardinalfish Pterapogonkauderni (Perciformes Apogonidae) EnvironmentalBiology of Fishes 56 (1ndash2) 79ndash92 DOI 101023A1007514625811

Vagelli AA 2008 The unfortunate journey of Pterapogonkauderni A remarkable apogonid endangered by the inter-national ornamental fish trade and its case in CITES SPCLive Reef Fish Information Bulletin 18 17ndash28

Vagelli AA Burford M Bernardi G 2009 Fine scale dis-persal in Banggai cardinalfish Pterapogon kauderni a coralreef species lacking a pelagic larval phase MarineGenomics 1 (3ndash4) 129ndash134 DOI 101016jmargen200901001

Vagelli AA Erdmann MV 2002 First comprehensive eco-logical survey of the Banggai cardinalfish Pterapogonkauderni Environmental Biology of Fishes 63 (1) 1ndash8 DOI101023A1013884020258

Vagelli AA Volpedo AV 2004 Reproductive ecology ofPterapogon kauderni an endemic apogonid from Indonesiawith direct development Environmental Biology of Fishes70 (3) 235ndash245 DOI 101023BEBFI000003333811355f9

Wetherall JA 1986 A new method for estimating growth andmortality parameters from length-frequency data Fishbyte(ICLARM) 4 (1) 12ndash14

Received 11 April 2013Accepted 10 September 2013

Published electronically 30 September 2013

Ndobe et al250

several trade routes including at least two sites in PaluBay (Moore and Ndobe 2007) The Banggai cardinalfishis a paternal mouth-brooder with direct development andwithout pelagic dispersal phase as the larvae on releaseswiftly seek refuge in nearby substrate (Vagelli 1999)Post-release Banggai cardinalfish maintain a sedentarylifestyle with high site fidelity (Kolm et al 2005)

Considered at risk of extinction in the wild due toover-exploitation for the marine aquarium trade (Lunnand Moreau 2004) and habitat degradation (Moore et al2011 2012) international concern has led to listing of theBanggai cardinalfish as endangered in the IUCN(International Union for the Conservation of Nature) RedList (Allen and Donaldson 2007) While a number ofstudies have been published on various aspects ofPterapogon kauderni biology and ecology literature onspecific Banggai cardinalfish life-history traits both in itsendemic distribution area and for the introduced popula-tions remains limited as reflected by the paucity of lifehistory data in FishBase (Froese and Pauly 2013) Thispaper presents data on life-history parameters of P kaud-erni including growth mortality reproduction and dietbased on research carried out over 8 years (2004ndash2012) inthe Banggai Archipelago and in Palu Bay CentralSulawesi Province Indonesia This information will con-tribute to the knowledge base for conservation manage-ment of the species

MATERIALS AND METHODSSampling Banggai cardinalfish Pterapogon kaudernispecimens were captured at Bone Baru Banggai Islandand in Palu Bay (Fig 1) using a lsquocangrsquo-style mobile fykenet such as used in the ornamental fishery The dates andcoordinates for each site as well as the number of fish cap-tured post-capture treatment and use in this study aregiven in Table 1 and the habitats defined as followsbull Coral reef (CR) coral reef area near the reef crest or

upper slopebull Reef flat (RF) flat or slightly sloping areas shoreward

from the reef crest substrate dominated by coral or deadcoral and rubble

bull Seagrass (SG) areas shoreward from the reef crest sub-strate usually predominantly sandy with visually obvi-ous seagrass cover some coral andor rubble

bull Mangrove (MG) between the prop roots of Rhizophorasp mainly below the low-tide line

Length-frequency data were also obtained from belttransect surveys (transect size 20 m times 5 m = 100 m2 cen-sus of fish within transect) carried out over the period2004ndash2012 The number of fish month and year areshown in Table 1 The sea surface temperature (SST) andother environmental parameters at the sampling sites aregiven in Table 2Growth and mortality The available length frequencydata were regrouped into 6 mm classes (0ndash59 6ndash119 etcwith class mid-lengths [ML] at 3 9 etc see Table 3) thenanalysed using the FISAT II software (Gayanilo et al 2005)to obtain estimates of the parameters of the von

Bertalanffy Growth Function (VBGF) of the formLt = Linfin middot (1 ndash endashK(t ndash t

0)) [1]

where Linfin is the mean length the fish would attain is theywere to live indefinitely K (timendash1) is the rate at which Linfin isapproached and t0 the predicted lsquoagersquo at a length (orweight) of zero (Pauly 1984) Specifically Linfin was esti-mated from a Wetherall Plot (Wetherall 1986) as imple-mented in FiSAT II K was estimated by its lsquoscanning forK routinersquo and t0 was estimated by solving equation [1]for a size at known age once Linfin and K had been estimat-ed (see below) Note also that longevity (tmax) if it isassumed to be the age at which fish reach 95 of Linfin canbe approximated by tmax asymp 3 middot Kndash1 (Pauly 1984)

Comparisons between pairs of Linfin and K estimates wereperformed using an index of growth performance (oslashrsquo)defined by the formula proposed by Pauly (1983 2010)oslashrsquo = log(K) + 2 middot log(Linfin) [2]

Natural mortality (M) was estimated from the empiri-cal equation (Pauly 1980)log(M) = ndash00066 ndash 0279 middot log(Linfin) + 06543 middot log(K)+ 04634 middot log(T) [ 3 ]where Linfin is expressed in cm K is in yearndash1 and T is themean water temperature in degC

Total mortality (Z) was then estimated using a length-converted catch curve (Pauly and Ingles 1981) thusallowing fishing mortality (from Z ndash M = F) and exploita-tion rate (from E = F middot Zndash1) to be estimated as wellLengthndashweight relation and other morphometrics Theparameters lsquoarsquo and lsquobrsquo of a lengthndashweight relation of the formW = a middot Lb [4]where W is the wet weight in g and L is the standardlength (SL) in cm were determined from the analysis of1002 Banggai cardinalfish specimens collected fromBone Baru in the Banggai Archipelago The length (L) ofeach specimen was measured to the nearest millimetre(mm) The specimens were then weighed to the nearest01 g and the weights averaged within each mm lengthclass A linear regression was then fitted to the log-trans-formed variables ie L and the corresponding (mean)weights which leads to an equation of the formlog(W) = log(a) + b middot log(L) [5]

Fifty four specimens from Kadongo in Palu Bay weremeasured to the nearest mm to relate their standard lengthto a number of other morphometric features (Fig 2) Theratios of each measurement to standard length were thencalculated and averaged for females (n = 27) males(n = 27) and for the entire sample (n = 54) The ratios forfemales and males were compared using one-way analysisof variance (ANOVA) Linear regression was performedfor the ratio of total length to standard length (TL middot SLndash1)Reproductive biology Each specimen (n = 80) was dis-sected and the gonad removed and weighed The gonado-somatic index (GSI) was calculated fromGSI = Wg middot Wndash1 [6]where Wg is the gonad weight and W is the total bodyweight Eggs were counted in both females (in developingegg masses) and males (in their buccal cavities) In juve-nile specimens where sex was not visually apparent his-

Ndobe et al238

See Sulawesi Case StudymdashBanggai Kepulauan (Bangkep) Pp 5ndash143 and pp169ndash228 In Indonesian ornamental fish trade Case studies and options for improvinglivelihoods while promoting sustainability in Banggai and Banyuwangi The international seafood trade Supporting sustainable livelihoods among poor aquaticresource users in Asia (EC Prep Project EPRO3R14) Available from httpaquaticcommonsorg22471IndonesianOrnamentalFishTrade_optpdf










Ndobe et al240



291008(1000ndash1300)

Mamboro(Palu Bay)


120509240509170709310709(0900ndash1200)

Kadongo(Palu Bay)


20202020




Growthparameters

S



Site MonthYear


SST[ordmC]

Depth[m]

Salinity[psu]

HabitatEcosystem

Popisi

122011


15002829 05ndash3 32 CR RF SG


062012




M










P










Ndobe et al242




SL [cm] 486 033 006 487 043 008 nsW [g] 489 123 024 478 134 026 nsc


M













Ndobe et al244



[g] GSI

Full Moon(12 May)

1 450 366 57 023 005 2 450 403 92 032 007 3 460 345 49 027 006 4 470 445 51 028 006 5 480 440 mdash 001 000 6 500 540 50 040 008 7 530 552 mdash 004 001 8 560 668 77 064 011

Mean 488 470 6267 027 006

Dark Moon (24 May)

9 410 384 30 001 00010 540 683 53 006 00111 540 598 60 006 00112 540 678 50 019 00413 660 1130 85 027 004

Mean 636 789 6813 017 003

Waxing (17 July)


Mean 454 483 5120 009 002

Waning (31 July)

23 520 313 64 029 00624 500 495 42 009 00225 490 325 39 011 00226 420 375 102 028 00727 440 292 28 009 00228 470 423 50 007 00129 480 352 55 013 00330 490 393 64 016 003


S






A

B






Ndobe et al246

SL[cm]



















G
























S
















Ndobe et al248










































Ndobe et al250










Ndobe et al240



291008(1000ndash1300)

Mamboro(Palu Bay)


120509240509170709310709(0900ndash1200)

Kadongo(Palu Bay)


20202020




Growthparameters

S



Site MonthYear


SST[ordmC]

Depth[m]

Salinity[psu]

HabitatEcosystem

Popisi

122011


15002829 05ndash3 32 CR RF SG


062012




M










P










Ndobe et al242




SL [cm] 486 033 006 487 043 008 nsW [g] 489 123 024 478 134 026 nsc


M













Ndobe et al244



[g] GSI

Full Moon(12 May)

1 450 366 57 023 005 2 450 403 92 032 007 3 460 345 49 027 006 4 470 445 51 028 006 5 480 440 mdash 001 000 6 500 540 50 040 008 7 530 552 mdash 004 001 8 560 668 77 064 011

Mean 488 470 6267 027 006

Dark Moon (24 May)

9 410 384 30 001 00010 540 683 53 006 00111 540 598 60 006 00112 540 678 50 019 00413 660 1130 85 027 004

Mean 636 789 6813 017 003

Waxing (17 July)


Mean 454 483 5120 009 002

Waning (31 July)

23 520 313 64 029 00624 500 495 42 009 00225 490 325 39 011 00226 420 375 102 028 00727 440 292 28 009 00228 470 423 50 007 00129 480 352 55 013 00330 490 393 64 016 003


S






A

B






Ndobe et al246

SL[cm]



















G
























S
















Ndobe et al248










































Ndobe et al250







P










Ndobe et al242




SL [cm] 486 033 006 487 043 008 nsW [g] 489 123 024 478 134 026 nsc


M













Ndobe et al244



[g] GSI

Full Moon(12 May)

1 450 366 57 023 005 2 450 403 92 032 007 3 460 345 49 027 006 4 470 445 51 028 006 5 480 440 mdash 001 000 6 500 540 50 040 008 7 530 552 mdash 004 001 8 560 668 77 064 011

Mean 488 470 6267 027 006

Dark Moon (24 May)

9 410 384 30 001 00010 540 683 53 006 00111 540 598 60 006 00112 540 678 50 019 00413 660 1130 85 027 004

Mean 636 789 6813 017 003

Waxing (17 July)


Mean 454 483 5120 009 002

Waning (31 July)

23 520 313 64 029 00624 500 495 42 009 00225 490 325 39 011 00226 420 375 102 028 00727 440 292 28 009 00228 470 423 50 007 00129 480 352 55 013 00330 490 393 64 016 003


S






A

B






Ndobe et al246

SL[cm]



















G
























S
















Ndobe et al248










































Ndobe et al250






Ndobe et al242




SL [cm] 486 033 006 487 043 008 nsW [g] 489 123 024 478 134 026 nsc


M













Ndobe et al244



[g] GSI

Full Moon(12 May)

1 450 366 57 023 005 2 450 403 92 032 007 3 460 345 49 027 006 4 470 445 51 028 006 5 480 440 mdash 001 000 6 500 540 50 040 008 7 530 552 mdash 004 001 8 560 668 77 064 011

Mean 488 470 6267 027 006

Dark Moon (24 May)

9 410 384 30 001 00010 540 683 53 006 00111 540 598 60 006 00112 540 678 50 019 00413 660 1130 85 027 004

Mean 636 789 6813 017 003

Waxing (17 July)


Mean 454 483 5120 009 002

Waning (31 July)

23 520 313 64 029 00624 500 495 42 009 00225 490 325 39 011 00226 420 375 102 028 00727 440 292 28 009 00228 470 423 50 007 00129 480 352 55 013 00330 490 393 64 016 003


S






A

B






Ndobe et al246

SL[cm]



















G
























S
















Ndobe et al248










































Ndobe et al250









Ndobe et al244



[g] GSI

Full Moon(12 May)

1 450 366 57 023 005 2 450 403 92 032 007 3 460 345 49 027 006 4 470 445 51 028 006 5 480 440 mdash 001 000 6 500 540 50 040 008 7 530 552 mdash 004 001 8 560 668 77 064 011

Mean 488 470 6267 027 006

Dark Moon (24 May)

9 410 384 30 001 00010 540 683 53 006 00111 540 598 60 006 00112 540 678 50 019 00413 660 1130 85 027 004

Mean 636 789 6813 017 003

Waxing (17 July)


Mean 454 483 5120 009 002

Waning (31 July)

23 520 313 64 029 00624 500 495 42 009 00225 490 325 39 011 00226 420 375 102 028 00727 440 292 28 009 00228 470 423 50 007 00129 480 352 55 013 00330 490 393 64 016 003


S






A

B






Ndobe et al246

SL[cm]



















G
























S
















Ndobe et al248










































Ndobe et al250



A

B






Ndobe et al246

SL[cm]



















G
























S
















Ndobe et al248










































Ndobe et al250






Ndobe et al246

SL[cm]



















G
























S
















Ndobe et al248










































Ndobe et al250






















S
















Ndobe et al248










































Ndobe et al250












Ndobe et al248










































Ndobe et al250









































Ndobe et al250

s3-us-west-2.amazonaws.com · befne

Documents