Journal of Indonesia Reefs 1(1) (2011) 15-29 Printed ISSN : 2089-8231

Conservation Management of the in the Banggai Kepulauan District MPA - A Genetic Approach Samliok Ndobe 1.2* , Daduk Setyohadi1 1 , Endang Yuli Herawati1 1 , Soemarno 1 and Abigail Moore 2 1Faculty of Fisheries and Marine Science, Brawijaya University, Malang 2(Fisheries and Marine Science Institute), Palu

Abstrak Banggai cardinalfish (Pterapogon kauderni, Koumans 1933), sering disingkat BCF, adalah jenis ikan yang berasosiasi dengan ekosistem terumbu karang dan bersifat endemik di perairan dangkal (kedalaman 0 sampai 5 meter) di sekitar Kepulauan Banggai. Terdaftar sebagai spesies "Endangered" pada IUCN Red-List, dinilai terancam oleh perdagangan internasional sebagai ikan hias. Pada tahun 2007, diinisiasi suatu Rencana Aksi BCF berskala nasional, dan Kawasan Konservasi Perairan Daerah (KKPD) di Kabupaten Banggai Kepulauan dicanangkan melalui SK Bupati, yang terdiri atas jejaring 10 pulau. Konservasi P. kauderni merupakan sasaran utama khusus dua pulau di antaranya. Dengan mereview data filogenetik, genetika dan biogeografi yang tersedia, maka jejaring KKPD ditinjau dari aspek konservasi genetika P. kauderni. Tanpa fase pelagis dan dengan site fidelity tinggi, populasi Banggai cardinalfish menunjukkan tingkat struktur genetika sangat tinggi khusus ikan laut. Sejumlah sub-populasi yang berbeda nyata dari aspek genetika telah teridentifikasi, hal yang mengindikasikan bahwa seharusnya unit (satuan) pengelolaan didasarkan pada sub-populasi (stok) yang ditentukan berdasarkan karakter genetika. Sejumlah knowledge gaps dan prioritas riset teridentifikasi. Secara khusus disimpulkan bahwa diperlukan sebuah program penelitian bertujuan mengidentifikasi serta melakukan karakterisasi setiap unit (satuan manajemen) berdasarkan genetika tersebut dari aspek biologi (termasuk genetika), ekologi (misalnya /mikro-habitat) dan sosio- ekonomi (termasuk fishing grounds). Ditawarkan penyediaan management support melalui penggunaan spatial analysis tool MARXAN bersama dengan sebuah database SIG, untuk menghasilkan alternatif-alternatif zonasi berbasis sains dengan satuan/sasaran pengelolaan yang didasarkan atas struktur genetika populasi, Kata Kunci: Pterapogon kauderni, Jenis terancam punah, Konservasi keanekaragaman genetik, Unit pengelolaan, MARXAN

Abstract The Banggai cardinalfish (Pterapogon kauderni, Koumans 1933), often referred to as BCF, is a restricted range associated fish endemic to shallow waters (0-5m) around the Banggai Archipelago, Indonesia. Listed as "Endangered" in the IUCN Red-List, the international marine trade and habitat degradation are considered major threats. In 2007, a national BCF Action Plan was developed, and a District MPA was established by decree of the Banggai Kepulauan District Head, consisting of a network of 10 islands. For 2 of these P. kauderni conservation is the main management target. We reviewed available phylogenic, genetic and biogeographical data, and examined the MPA network from the viewpoint of P. kauderni genetic diversity conservation. With no pelagic phase and high site fidelity, the Banggai cardinalfish population exhibits a level of genetic structure unusual in a marine fish. Several genetically distinct sub-populations have been identified. It was concluded that management units should be based on genetically determined sub-populations (stocks). Critical knowledge gaps and several research priorities were identified. In particular, we conclude that a research programme is necessary for the identification and characterisation of these genetically determined units from biological (including genetic), ecological (e.g. habitat/micro-habitat) and socio-economic (including fishing ground) aspects. We propose to provide management support through the use of the spatial analysis tool MARXAN combined with a GIS database to produce science-based zoning options with management units/targets based on genetic population structure. Key words: Pterapogon kauderni, , Genetic diversity conservation, Management units, MARXAN

*Corresponding Authors : [email protected] Conservation Management of the Banggai Cardinalfish

INTRODUCTION population numbers at a particular point in time, leading to genetic bottlenecks Indonesia is often called a (Bertorelle et al ., 2009). It is now widely "Megabiodiversity" country, and the Coral considered that, in the conservation Triangle is one of the three major global management of species with biodiversity regions, ranking alongside the reproductively (and therefore genetically) Amazon and Congo basins. Indonesia as a isolated populations, each such population signatory to the Convention on Biological or sub-population should be treated as a Diversity (CBD) is committed to biodiversity separate management unit. This is conservation, however the high level of specifically so in the case of marine fish, anthropogenic pressure (direct and indirect) where each such unit can be considered as means that an increasing number of species a separate stock (e.g. Reis et al ., 2009; are at risk of . There is a growing Rocha et al ., 2007). awareness that simply conserving parts of Sustainable management of marine an ecosystem or a certain number of fisheries resources, including the use of individuals of a species is often not enough. Marine Protected Areas (MPA) as a In addition, genetic diversity between fisheries management tool, should be individuals and between populations or sub- based on these genetic sub-populations or populations of a given species is also stocks (Palumbi, 2003), leading to a need important, as is acknowledged in the CBD for population genetics studies for their text. However in the Agenda 21 document identification and characterisation. As (produced at the 1992 United Nations pointed out by Hellberg (2007), such Conference on Environment & identification is now possible due to the Development held in Rio de Janeiro, Brazil) development of technology for genetic which was intended as a technical guideline (DNA) analysis, using a variety of for CBD implementation, genetic diversity is approaches. One powerful support tool is only discussed for terrestrial plants and GenBank, a global database of DNA and . other proteins, hosted by several sites, There is growing concern about aquatic including in particular the National Center species, including freshwater and marine for Biotechnology Information. Gen Bank organisms. Examples of this trend can be and a number of other tools (e.g. software seen in a recent review of the IUCN Red for genetic data analysis) can be accessed List (Vié et al. 2009), recent proposals to for free at http://www.ncbi.nlm.nih.gov/. CITES (see http://www.cites.org); species Other software for genetic and phylogenic added to the list of flora and fauna protected data analysis which are available on-line in Indonesia under the Appendix to Law PP and/or downloadable include GENEPOP No7 1999 (http://www.dephut (http://genepop.curtin.edu.au) and PAST .go.id/INFORMASI/UNDANG2/pp/L_7_99 (http://www.nhm.uio.no/norges/past/downl .htm); and the Census of Marine Life - oad.htm). CoML (http://www.coml.org). This concern One marine species of conservation is also increasingly extended to the concern is the Banggai cardinalfish conservation of genetic diversity within Pterapogon kauderni (Koumans, 1933), a species (e.g. Gray, 1997; Conover et al . small (maximum standard length around 65 (2006). mm SL) restricted range endemic species One factor which tends to affect genetic with an endemic distribution limited to the diversity within a species is the level of southern part of the Banggai Archipelago reproductive isolation between populations and a few nearby islands (Vagelli, 2005). which in extreme cases can be total, with no Traded internationally as a marine gene flow for many generations. Isolated ornamental since the 1980's . These sites populations or sub-populations tend to include Lembeh Straits (Erdman and become genetically distinct due to genetic Vagelli, 2001); Palu Bay (Moore and drift, site-specific selection and a variety of Ndobe, 2007a);dobe et al., 2005), stochastic factors such as founder effects introduced P. kauderni populations have and one-off or infrequent impacts which become established at several sites along can significantly reduce effective the long and complex trade routes.

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Sources: Vagelli (2005); Erdman and Vagelli (2001); Vagelli and Erdmann (2002); Moore and Ndobe (2007a); Ndobe et al. (2005); Lilley (2008): Moore et al, (2011) Fig. 1. Known endemic and introduced P. kauderni populations

Tumbak(Ndobe et al., 2005); North Bali fecundity and a suspected high rate of (Lilley, 2008) Kendari (Moore et al, ;2011 in mortality due to predation of recruits and theseproceedings); and Luwuk (Vagelli and juveniles, make this species especially Erdmann, 2002), though there has been vulnerable to extinction, with a particularly speculation that the Luwuk population high risk of local extinction due to the lack of might be a remnant of a once more natural dispersion mechanisms leading to extensive P. kauderni population on the an extremely low probability of natural re- Sulawesi mainland (Vagelli, 2005). colonisation The known P. kauderni endemic Considerable international attention has distribution and introduced population sites been focussed on the risk of extinction due are shown in Fig. 1, though it is likely there to the marine aquarium trade (e.g. Bruins et have been further as yet unpublished al ., 2004; Vagelli, 2008). Since 2007, introduced populations established. The management of the fishery has greatly endemic distribution area covers around improved but growing threats due to habitat 5,500 km2 , while the total area of available and especially micro-habitat loss have habitat has been estimated at around 30- been identified, in particular the increasing 34km2 and the total endemic population has consumption of sea and sea been estimated at around 2.4 million urchins. Though some other community (Vagelli,2005). It is considered likely that members are involved, the main there may have been further (as yet consumers are seaweed farmers who are unpublished) introduced populations tending to collect these and other established. invertebrates as a major source of protein A paternal with direct in their diets (Ndobe et al., 2008; Moore et development, there is no pelagic dispersal al ., 2011) phase in the P. kauderni life-cycle and Pterapogon kauderni is listed as recruits settle in the substrate near the site ENDANGERED in the IUCN Red List (Allen of their release (Vagelli, 1999). Despite an and Donaldson, 2007) and was proposed ontogenetic shift in micro-habitat use for CITES listing in 2007 (CITES, 2007a) by (Vagelli, 2005; Ndobe et al . 2008), P. the United States of America. However the kauderni exhibits a high site fidelity proposal was withdrawn (CITES, 2007b) thereafter (Kolm et al ., 2005). The shallow- whit Indonesia making a commitment to the water habitat (coral reefs, reef flats and sustainable management of this species beds under 5 m depth, mainly (Indrawan and Suseno, 2008; Moore and 0.5-3m) and sedentary habit make P. Ndobe 2007b). A multi-stakeholder, multi- kauderni extremely easy to catch. These year Banggai Cardinalfish Action Plan was factors, combined with relatively low

17 Conservation Management of the Banggai Cardinalfish developed, and a number of activities have METHODS been implemented to achieve the goals agreed (Ndobe and Moore, 2009; Moore et The state of knowledge regarding the al ., 2011). A District Marine Protected Area phylogeny, biogeography and genetic (MPA), or more accurately a Marine structure of the endemic Banggai Protected Area Network (MPAN) was cardinalfish (Pterapogon kauderni) was established by Decree of the Banggai assessed through a review of published Kepulauan District Head (SK Bupati scientific literature as well as "grey 540/2007). Two out of the ten islands listed literature", supplemented by direct (Pulau Banggai and Pulau Togong observation and key informant interviews Lantang) are designated specifically for the (primary data). The data and information conservation of the Banggai cardinalfish. thus obtained were analysed to evaluate This MPA is still in the planning stage. the MPA network from the viewpoint of P. The habitat and dispersal limitations kauderni genetic diversity conservation, in have resulted in a geographically particular in relation to the spatial planning discontinuous P. kauderni population process for the District MPA Network. distribution pattern, with a very low Specific aims were to identify critical likelihood of interbreeding between all but knowledge gaps and to propose a possible the closest of populations, separated by approach towards effective BCF shallow water with suitable habitat. It is conservation management from a genetic therefore considered likely that each of biodiversity standpoint. these geographically isolated populations is in fact a separate sub-population or stock RESULTS AND DISCUSSION with significant genetic divergence or differentiation between stocks. Local Pterapogon kauderni phylogeny and are likely to result in the total biogeography loss of genetic strains so that the identification of these stocks is important The Dutch naturalist Walter Kaudern for species conservation management, collected 2 (type) specimens of a new both from a fisheries management point of species from the coastal waters around view and in the context of MPA planning Banggai Island during an expedition in and management. 1917-1920. These were deposited with the

Fraser (1972) dalam Gows dan Gon (2009 ), di olah Source: Fraser (1972) in Gouws & Gon (2009)

Fig. 2. A Simplified phylogeny of the

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Leiden Museum and later described by thin high body unlike the horizontal stripes Frederick Koumans. Placed in the Family and elongated rounded body more Apogonidae (cardinalfishes), several common in cardinalfishes. While the unusual features warranted the differences are striking to ichthyologists establishment of a new Pterapogon, familiar with both species, this superficial while the species name kauderni was given resemblance has lead to cases of mistaken in recognition of the discovery by Walter identity, with several reports of P. kauderni Kaudern (Koumans, 1933). Commonly sightings which on examination by local used local names are bebese tayung (Bajo scientists familiar with P. kauderni turned language) and capungan (Banggai out to be nemtopterus. The language) while other trade names include behaviour and habitat of the two species the abbreviation BCF, capungan Banggai are quite different, S. nemptopterus being and high-fin cardinalfish (Ndobe et al ., relatively mobile and favouring mid-water 2005). The classification of Pterapogon habitat around almost any form of structure kauderni in the global database FishBase (natural or man-made), while P. kauderni is (http://www.fishbase.org) is as follows: benthic and sedentary. Superclass: Osteichthyes (bony fishes) Advances in genetic analysis Class: (ray-finned fishes) (technology, software) have lead to the Order: Perciformes (perch-like fishes) development of phylogeny based on DNA Family: Apogonidae (cardinalfishes) with more detailed and/or accurate studies Sub family: of evolutionary/phylogenic relationships Genus: Pterapogon between taxa at many levels Genetic Species:Pterapogon kauderni studies of Apogonidae published to date (Koumans, 1933) (e.g. Gouws & Gon, 2009; Thacker & Roje, Common name: Banggai 2009) still cover relatively few taxa. Despite cardinalfish this limitation, the results of these studies According to Gavin and Gows (2009), question previous classifications based on the Cardinalfishes or Apogonidae are morphometric, biogeographical & small, carnivorous fish. The majority are ecological considerations, and phylogenic reef-associated, while some live in relationships within the Apogonidae are deepwater, estuarine or freshwater under revision. Based on the analysis of 3 . There are two generally types of mitochondrial DNA, Thacker recognised Sub-families, the Apogoninae (2009) placed the Family Apogonidae in and Pseudaminae with around 23 Genera Sub-order Apogonoidei, as a sister clade and over 250 species, with the highest alongside the Gobioidei and Kurtoidei in diversity being found in the Indo-Pacific the Order of Gobiiformes. Thacker and region. The most complete phylogeny to Roje (2009) developed this analysis to date was compiled by Fraser (1972), and is produce a phylogenic tree shown in Fig. 3. shown in a simplified schematic form in Fig. Thacker (2009) and Thacker and Roje 2. Based on osteology & morphology, (2009) considered that the theory of a close Frazer (1972) ordered the Apogonidae relationship (relatively recent common based on what were considered the most ancestry) between the Apogonidae and basic to the mostadvanced traits. P. Gobioidei is supported by data, including kauderni was placed in the same Clade as data from the fields of morphometry, the Genus Sphaeramia, while the two biogeography, ecology, and reproductive neighbouring Clades ( & biology. Vagelli (2009) postulated that the ) were both considered ancestral species of the Gobiiformes, monophyletic. including the Apogonidae, could be There is a physical resemblance freshwater fish from Australasian plate, between Sphaeramia nemtopterus (a which evolved before the fragmentation widespread cosmopolitan species) and P. and subsequent movement of the various kauderni. Both have vertical stripes and a plate fragments as shown in Fig. 4.

19 Conservation Management of the Banggai Cardinalfish

DNA analysis: subunit NADH- dehydrogenase one and two: ND1, Nd2; cytochrome· oxidase subunit one: COI Bayesian Consensus (probability nodes >90%)

Source: Thacker & Roje (2009) Fig. 3. Phylogenic Tree based on 3 types of mitochondrial DNA

According to this theory, P. kauderni thereafter. Several species known to would have evolved during the northwest exhibit traits rare in marine fish but not movement of the plate comprising the uncommon in freshwater fish, in particular Banggai Islands and western Taliabu. a similar reproductive biology (large egg Thus, when eventually the plates attained s i z e , m o u t h b r o o d e r w i t h d i r e c t their current positions, P. kauderni would development) include P. kauderni, Quinca have been present on this plate fragment (or Pterapogon) mirifica, the Genus but not on any of the adjacent plates. With and Genus . Vagelli no planctonic dispersal phase and a (2009) considered that these traits could be sedentary habit, the species would have explained by this theory of common globoid been unlikely to spread far (if at all) ancestor.

Source: modified from Vagelli (2009) Fig. 4. The theory of plate dispersal and the Australian origin of P. kauderni

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We consider that this theory, consistent Pterapogon kauderni genetic with historical bathymetry and other population structure geophysical data, could provide a Two methods have been developed for reasonable explanation for the current P. P. kauderni genetic analysis. Bernardi and kauderni distribution. It is well known that Vagelli (2004) used mitochondrial DNA the meeting of plates, each bearing (mtDNA) haplotypes. Hoffman et al . (2004) distinctive flora and fauna, contributed to identified 11 polymorphic microsatellite the high biodiversity of Sulawesi Island. DNA loci. These have been registered in Examples of speciation in freshwater fish GenBank, and used in genetic analysis by due to isolation include the ricefishes of the Hoffman et al . (2005); Vagelli et al . (2009) Sulawesi ancient lake complex described and Kolm et al . (2005). Sampling sites for in Parenti and Soeroto (2004). However as the analysis by Bernardi and Vagelli (2004) yet it seems that there are no published and Hoffman et al . (2005) are shown in Fig. data on the genetics of Quinca (or 5. Vagelli et al . (2009) also collected Pterapogon) mirifica or on the Glossamia samples at 12 sites for a fine-scale analysis and Vincentia species so that the proposed of P. kauderni population genetics around evolutionary phylogenic relationships the island of Bangkulu (synonym between P. kauderni and these species Bangkurung), on the western edge of the P. (based on geology and reproductive kauderni distribution. The genetic analysis biology) remain unproven by genetic in Kolm et al . (2005) was at an extremely research methods.

Table 1. Characteristics of 11 polymorphic micro-satellite loci in P. kauderni DNA

Annealing Clone GenBank No. 1 Sequences temp. 2 3 Locus n Repeat size Ho He Accession (5′−3′) Alleles (°C) (bp) No.

Pka 03 32 *GCTTGATACAACAGTGACAGA 54 (GATA) 8 73 6 0.781 0.715 Ay530932 GCGACTGGCAATTTTATAC

Pka 06 36 *AAGGTTCCACTTCCATCTACT 53.5 (GATA) 6 218 10 0.722 0.774 AY530933 TCGGTCTTCCACCAATAA Pka 07 28 *CAAGGATTGAGCTATTAACAT 49.5 (GATA) 24 230 14 0.786 0.883 AY530934 AGGGAGAAGGAATTACAGA Pka 09 29 *TGTGTGAAAATTCTAGTG 49.5 (GATA) 14 179 10 0.621 0.67 AY530935 GGTGAATAGAGAAAACAA Pka 11 27 56 (GT)12 A(GATA) 5 288 2 0.111 0.107 AY530936 *CACACGCACTGATGTTT CGCAGTATCTTAGCTGTTC Pka 13 36 54 (GATA) 24 209 15 0.833 0.853 AY530937 *AATGGCTACCTTTACAACTAC AAGGATGGAGGACAGATG Pka 16 32 51 (GATA) 23 153 12 0.656 0.873 AY530938 *GGAGCACAGGAACCCCTTTATAC CACCGCACCTGGAACAGA Pka 19 37 54 (CTAT) 11 199 11 0.73 0.815 AY530939 *GGCTTGGGTTTGAGTTCT CCAGGCTGTGAGTTTGAGAC Pka 21 35 48 (GATA) 15 185 4 0.8 0.655 AY530940 *CGCTGAACGAGACTAGATAC

Pka 24 25 TTTGGTATGCTTTTGAATATC 51 (GATA) 12 171 2 0.4 0.47 AY530941 *TCTCCCTGGAAATGTCTC

Pka 25 30 TTCGGACACAGCCAATA 51 (GATA) 20 203 15 0.933 0.928 AY530942 *ATCCCATTGTTCTGAATAA AGGGAGTTTACTGTAGTCTAAT

*5′ fluorescent-labelled primer. 1 n, number of individuals screened from the population, 2 3 Ho , observed heterozygosity, He , expected heterozygosity

21 Conservation Management of the Banggai Cardinalfish

-

Sources: adapted from Bernardi and Vagelli (2004); Hoffman et al. (2005) Fig. 5. Sampling locations for P. kauderni genetic analysis (2004-2005) fine scale, aiming to identify the level of a n d o b s e r v e d h e t e r o z y g o s i t y, kinship within groups of adult P. kauderni. Hardy–Weinberg equilibrium (HWE) and The analysis of genetic distance based genetic distance between populations. on mtDNA data by Bernardi and Vagelli FSTAT V.2.9.3.2 was used to test the level (2004) indicated a reproductive isolation of significance. Based on an analysis of all period of around 800,000-160,000 years 11 microsatellite loci, a high level of genetic between the islands of Bangkulu and structure was revealed with significant Banggai. This was based on molecular divergence between sites. These clocks developed for fish mitochondrial differences were considered most likely control regions with a rate of 10–2% per due to highly restricted gene flow million years (McMillan and Palumbi, 1997, (reproductive isolation) rather than natural Terry et al ., 2000 and Bargelloni et al ., 2003 selection. A synopsis of the results for two in Bernardi and Vagelli, 2004). Based on micro-satellite loci considered to represent historical sea level data (Voris, 2000 in a significant proportion of the genetic Bernardi and Vagelli, 2004), this distance is diversity are shown in Fig. 6. consistent with known sea level variation. The genetic data give a strong indication During periods before this genetic isolation that the Luwuk population was introduced is estimated to have occurred, most of the rather than being a remnant population. It known P. kauderni distribution, including can be seen in Fig. 6. that the genetic data the two islands of Banggai and Bangkulu, for of the Tolokibit (site H) and Luwuk (site would have been joined by shallow waters R) populations are very similar. This finding suitable as Banggai cardinalfish habitat. concurs with social survey data reported in However it is likely that they would have Ndobe et al . (2005). Although no longer been separated by deeper waters from active in 2004, there had been a trade route most nearby areas where P. kauderni is not from Tolokibit, the southernmost sampling currently found. site in Fig. 6. This route began in the 1980's Hoffman et al . (2005) analysed data and passed through Luwuk, Banggai from 7 sampling sites using the software cardinalfish were indeed released in Luwuk GENEPOP V.3.3. to calculate expected harbour by the traders involved.

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Pie chart Legen d Sampling site

Locus Pka11: right orange/brown/pink Locus Pka06: left

blue/purple/white

Each shade represents an allele at the locus

The size of the pie chart segments represents the frequency of each allele in the population Source: Hoffman et al. (2005)

Fig. 6. Genetic variation of 2 loci (Pka 11 and Pka 06) at 7 sampling site

The shortest distance between Bangkurung (synonym names). The populations (sites) with significantly software GENEPOP was used, different genetic characteristics in a pair- supplemented by assignment tests using wise analysis by Hoffman et al . (2005) was Doh Program (location "fingerprinting"). 2km. The two sites in question were Three sub-populations or genetically separated by a gap in suitable P. kauderni distinct stocks were identified on Bangkulu habitat (discontinuous P. kauderni Island, corresponding to: (1) the northern distribution). indication of recent bottleneck and eastern sites, (2) the most southern effects (poor/very poor genetic diversity). sites and (3) some small islands off west Hoffman et al . (2005) highly recommended coast. Most of the western coast was further genetic population structure reported to have sheer coastline research as a basis for conservation and/or topography with little or no suitable habitat sustainable fisheries management. A for P. kauderni. similar minimum distance between At the overall population level, a high genetically distinct populations was rate of re-assignment was reported by reported by Vagelli et al . (2009). Analysis of Vagelli et al . (2009), except for the Luwuk the genetic diversity within populations or and Lembeh introduced populations. The sites (using the software BOTTLENECK) hypothesis was put forward that most gave no indication of recent bottleneck mating and most recruitment of juveniles effects (poor/very poor genetic diversity). occurs within the site of origin, with a very Hoffman et al . (2005) highly recommended few individuals moving over short further genetic population structure distances. Marked genetic population research as a basis for conservation and/or structure with significant genetic distance sustainable fisheries management. A between islands was reported. similar minimum distance between It was concluded that available data are genetically distinct populations was consistent, and both collectively and reported by Vagelli et al . (2009). severally indicate a high level of genetic Vagelli et al . (2009) carried out a more structure. Genetic isolation due to habitat detailed study of population genetics based gaps recent in geological and evolutionary on the loci Pka06 and Pka11 identified by timescales seems to have resulted in Hoffman et al. (2004). This study combined significant genetic distance between P. a re-analysis of samples used in the kauderni populations on separate islands. previous mtDNA study (Bernardi and In addition, there are proven examples of Vagelli, 2004) with intensive sampling of genetically distinct populations (stocks) on Bangkulu Island which is also known as the same island, separated by gaps in

23 Conservation Management of the Banggai Cardinalfish suitable habitat. At least two cases have stages of planning process. Priority needs been reported (Ndobe et al., 2005 and include the establishment of definitive Vagelli, 2005) where P. kauderni boundaries and zonation. populations extirpated from isolated sites We consider that the MPA network had not been recolonised after a period of design is poor from the P. kauderni genetic several years even though there were diversity aspect. Much of the known P. healthy P. kauderni populations nearby, but kauderni distribution is not represented in separated by relatively deep water. In the the MPA. In particular, at least 12 areas case of an islet near Liang Harbour on already known to have genetically distinct Peleng Island (Ndobe et al ., 2005), severe populations (stocks) are not represented. habitat degradation from coral mining and a Furthermore, of the 10 islands included in one-off incident of severe overfishing were the MPA, only 2 are designated for Banggai implicated. Based on the available genetic cardinalfish protection: Banggai Island, the data, it is considered that such local major P. kauderni fishing ground, and extinctions are likely to result in the total Togong Lantang (Tolobundu). Data on loss (extinction) of genetic strains. Togong Lantang is limited and contradictory. At least 3 other islands within Application to P. kauderni conservation the MPA have P. kauderni populations, in the banggai Kepulauan district MPA known or suspected to be genetically distinct stocks, but do not have P. kauderni The Decree of the Banggai Kepulauan conservation as a conservation target. District Head (SK Bupati 540/2007) Despite these limitations, on Banggai established the legal basis of a District Island alone it is clear that there are at least MPA, or more accurately an MPA network, two and possibly four or more genetically consisting of 10 islands (see Table 2). The distinct populations. This factor should be a main conservation target for two of these is key management consideration, conservation of the endemic Banggai particularly in zonation both for core zones cardinalfish. In view of the data presented (no-take conservation approach) and above, it is important that the design of the restricted use or buffer zones (sustainable District MPA should take into account P. fishery). The planning approach we kauderni genetic diversity and population propose below should enable optimisation structure. The MPA has an office (as yet of genetic conservation benefits for the unmanned) in Bone Baru, the main islands included in the MPA, and could be Banggai cardinalfish trading village on extended to other areas of the P. kauderni Banggai Island, but is still in the early distribution.

Table 2 . The Island in the Banggai District MPA

Site/Island (alternative/ Main Conservation In known BCF Fishing No BCF Population synonym name) targets* distribution? Ground survey(s) 1. PulauTolobundu BCF, CR, SG, M yes yes c 1 site, not founda (P Togong Lantang) a 2. Pulau Bandang Besar CR, SG, M, MT yes yes b,c yes, found b,c 3. Pulau Makaliu CR, SG no no a yes, not found 4. Pulau Lesapuang CR, SG no no b,c 5. Pulau Togong Sagu M, CR no 2 sites, not founda (P. Sago) No data (highly 6. Pulau Panteh M, CR yes unlikely) yes, foundd 7. Pulau Maringkih M, CR no yes, not found d 8. Pulau Peposo CR no no b,c yes, not founda 9. Pulau Sonit (P. Masoni) M, CR, A yes no data yes, found a 10. Pulau Banggai BCF, M, CR yes yesb,c yes a,b Sources: SK Bupati 540/2007; Vagelli (2005); Ndobe et al ..(2005); Latupono (2009) Artiawan (pers. com, 2011) * BCF = Banggai cardinalfish; CR = coral reef; SG = seagrass; M = ; MT = marine tourism; A = abalone

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Systematic MPA design should take into It was considered that the MARXAN account the conservation of biodiversity at application would be appropriate as a ecosystem, species and genetic levels as planning tool for the Banggai Kepulauan well as economic and social factors and District MPA, in particular in the context of vested interests (Ardron et al ., 2010). In P. kauderni conservation. order to facilitate this process, data on When using MARXAN as a planning conservation targets (ecosystems, tool, the study area (the proposed or communities, species, populations/sub- potential MPA area) is divided into planning populations etcetera) need to be available units, which are usually hexagonal in in a user-friendly spatial format, and shape. Each of these units is assigned combined with other spatial data (e.g. land attributes which will be used to evaluate it's use). Maps are the most common media for effectiveness in terms of the potential presenting spatial data. In this Information contribution to conservation if it is Technology (IT) era, maps are commonly a conserved (FEATURES) and the outlay or part of as well as products of an electronic loss to other sectors associated with spatial database or Geographical conserving it (COSTS). Key definitions are Information System (GIS). given in Table 2. A number of other A GIS Database has many uses in MPA parameters can be set in order to enable planning (Ehler and Douvere, 2009). In the MARXAN model to be more realistic or particular a GIS can be a powerful tool for run more efficiently. stakeholder consultation, planning and The Output of each RUN is an option of a implementing effective conservation specific set of priority hexagons to be management, including the development included in the MPA in order to attain of sustainable use patterns. Geographical conservation targets with minimum costs. Information System (GIS) software Repeated MARXAN runs with same packages are increasingly numerous. ArcGIS (ESRI) products are often used for data/parameters may provide a range of MPA planning and implementation, options. The more the input parameters are including ArcView 3.x: developed in the refined, the more likely that the options 1990s which has many compatible from different runs will be similar to one applications. MARXAN (Marine Reserve another. The options produced are a Design using Spatially Explicit Annealing) scientific basis which can inform is an MPA planning software stakeholder discussions and planning (http://www.uq.edu.au/ MARXAN/; Ardron decisions. Once the key sites have been et al ., 2010). The MARXAN software is agreed, the hexagons will most likely need compatible with ArcView 3.x. via CLUZ to be squared or rounded off to produce application. Both MARXAN & CLUZ are workable MPA boundaries. free (non-commercial) software packages The proposed use of MARXAN for the which have been used successfully in conservation of within species genetic many countries (Loos, 2006). In Indonesia diversity will be a new application of the examples include the Wakatobi National MARXAN tool. Each sub-population will Marine Park (http://www.reefresilience.org/ form a separate MARXAN FEATURE and Toolkit_Coral/C8_ Wakatobi.html) and the ArcView GIS layer, with a conservation Lesser Sunda region (Wilson et al., 2008). target expressed as a minimum area or a

Table 3. Key MARXAN Definitions

FEATURES LOCKIN COSTS LOCKOUT What is to be conserved Features which must Other interests (e.g. Areas which must (e.g.Ecosystems, habitats, beconserved (e.g. Aquaculture, fishing not be within the species). Each must have Spawning grounds) grounds, harbours, core conservation zone values (weighted) and touristattractions). Each (e.g. Harbours) conservation targets must comprise spatial (area orpercent) data and values (weighted).

25 Conservation Management of the Banggai Cardinalfish

Fig. 7. MARXAN hexagons and proposed sampling sites for a P. kaudeni genetic population analysis within the Banggai Kepulauan District MPA

percentage of the feature area. The area to will be necessary to carry out this analysis. be included is limited to shallow water These include biophysical data layers (e.g. coastal ecosystems (coral reefs/reef flats, habitat & microhabitat) and socio- seagrass) which provide known or potential economic data layers (e.g. fishing grounds, Banggai cardinalfish habitat within the key infrastructure, coastal development, known P. kauderni distribution. Therefore aquaculture). Once these have been the survey and analysis will not include compiled into the MPA database, MARXAN coasts with sheer drop-offs such as much RUNS can provide science-based options of the East coast of Banggai Island. for achieving the conservation targets The Banggai Kepulauan District MPA which are set or suggested by managers. can be divided into hexagons, as shown in Initial runs will provide a basis for a Fig. 7. In this example the diameter of the discussion and consultation process. hexagons was set at 2km based on the Suggestions from any stakeholders can be smallest known distance between entered into the GIS and factored in to genetically distinct P. kauderni sub- further RUNS to predict the effects of populations or stocks. Genetic analysis specific choices on a conservation targets - should enable the identification specifically on conservation of BCF genetic andcharacterisation of each sub- diversity – or indeed to test the costs and population or stock. Combining genetic, benefits associated with changes in the geological and ecological data, it should be conservation targets themselves. possible to determine the boundaries Thereafter, the GIS can be updated with between stocks, so that each hexagon can new data and information (e.g. additional be allocated to a specific stock or sub- surveys or genetic analysis, planned population. Fig. 7 also shows the locations infrastructure development etc), before and with existing P. kauderni genetic data and after the management plan and proposed sampling sites in order to enable management mechanisms are in place, such a genetic population analysis for the specifically including data from monitoring islands within the District MPA. programs. This will make the GIS a In addition to genetic sampling and valuable tool for adaptive management as analysis, other FEATURE and COST data well as planning.

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CONCLUSION (Quinca/ Pterapogon mirifica, Genus Vincentia and Genus Glossamia). As for most of the Family Apogonidae, there are many questions regarding the REFERENCES phylogeny of the Genus Pterapogon and Allen G.R. and T.J. Donaldson. (2007). species P. kauderni, including the Pterapogon kauderni. In: IUCN 2009. IUCN relationship of P. kauderni to several taxa Red List of Threatened Species. Version 2009.1. (http://www.iucnredlist.org, from the Australian plaque. Knowledge and downloaded 11 July 2009) techniques for P. kauderni genetic (DNA) Ardron J.A., H.P. Possingham and C.J. Klein analysis which can be used for effective (eds). (2010). Marxan Good Practices genetic population structure analysis have Handbook, Version 2. Pacific Marine been developed, and genetically distinct Analysis and Research Association, Victoria, BC, Canada sub-populations have been identified at Bernardi G. and A. Vagelli (2004). Population distances as little as 2-5 km apart, within structure in Banggai cardinalfish, coastal waters of the same island as well as Pterapogon kauderni, a coral reef species between islands. Each genetically distinct lacking a pelagic larval phase. Marine sub-population or stock should be Biology (2004) 145: 803–810 Bertorelle G., M.W. Bruford, H.C. Hauffe, A. considered as a separate management Rizzoli and C. Vernesi (2009). Population unit. There are big gaps in the geographical Genetics for Conservation. coverage of P. kauderni genetic population Cambridge University Press, Cambridge, data, in particular within the Banggai UK. Kepulauan District MPA. Bruins E.B.A., M.A. Moreau, K.E. Lunn, A.A. Vagelli and H. Hall (2004). 10 Years after Recommendations for MPA planning rediscovering the Banggai Cardinalfish. include: (i) the establishment of genetic Musée Océanographique, Monaco. Bulletin sub-populations (stocks) as a spatial de l'Institut Océanographique 2004, vol. 77, management unit in the planning and no1446, pp. 71-81 management of P. kauderni conservation in CITES (2007a). COP 14 Prop. XX. Convention on the International Trade in Endangered the Banggai Kepulauan District MPA, Species, Fourteenth meeting of the including specifically in the zonation Conference of the Parties, The Hague process, and as far as practicable (most (Netherlands), 3-15 June 2007, likely excluding areas where significant Consideration of Proposals for Amendment of Appendices I and II. Proposal: Inclusion of introductions and mixing have taken place) the Banggai cardinalfish (Pterapogon for fisheries management; (ii) research to kauderni, Koumans 1933) in Appendix II of complete the identification of P. kauderni CITES. (http://www.cites.org, downloaded genetic sub-populations and the 21 January, 2007) geographical boundaries between them, CITES (2007b). Summary record of the 10th session of Committee I. E14-Com-I-Rep-10. the first priority being the two islands (http://www.cites.org, downloaded 24 June designated for BCF conservation (Banggai 2007) and Togong Lantang); (iii) establish Conover D. O., L.M. Clarke, S.B. Munch. and conservation targets for each sub- G.N. Wagner. (2006). Spatial and temporal population within the MPA (e.g. as scales of adaptive divergence in marine fishes and the implications for conservation. FEATURES in MARXAN) Journal of Fish Biology 69 (Supplement General recommendations include: (i) C):21–47 extreme care in re-stocking or in-situ Ehler C. and F. Douvere. (2009). Marine Spatial breeding/culture to avoid/minimise the Planning: a step-by-step approach toward ecosystem-based management. mixing of BCF sub-populations as this Intergovernmental Oceanographic could affect population genetic diversity Commission and Man and the Biosphere and/or fitness; (ii) the development and Programme. IOC Manual and Guides No. implementation of a P. kauderni population 53, ICAM Dossier No. 6. UNESCO, Paris, dynamics model and fisheries France. Erdmann M.V. and A.A. Vagelli (2001). Banggai management tools at genetic sub- Cardinalfish Invade Lembeh Strait. Coral population (stock) level, not only for the Reefs 20:252-253. endemic population as a whole; (iii) further Frazer T.H. (1972). Comparative osteology of research into P. kauderni phylogeny & the shallow water cardinalfishes reproductive biology, including the [Perciformes: Apogonidae] with reference to the systematics and evolution of the family. relationship with Apogonidae from Australia Ichthyological bulletin 34:1-105

27 Conservation Management of the Banggai Cardinalfish

the family. Ichthyological bulletin 34:1-105 ornamental fishery. Proceedings of the 11th Gouws G. and O. Gon, (2009). A preliminary International Coral Reef Symposium, Ft. molecular phylogeny of and related Lauderdale, Florida, 7-11 July 2008 genera. Paper presented at the 8th Indo- pp.1026-1029 Pacific Fish Conference, 1-5 June 2009. Ndobe S., Madinawati and Moore A. (2008). (http://www.ipfc2009asfb.com/pdf/speaker_ Pengkajian Ontogenetic Shift pada Ikan presentations/Gouws,Gavin.pdf, Endemik Pterapogon kauderni. Jurnal Mitra downloaded 26 August, 2009) Bahari. Vol 2 No.2: 32-55 Gray J.S. (1997). Marine Biodiversity: Patterns, Ndobe S., Moore A. & Supu A. (2005). Sulawesi Threats and Conservation Needs. Case Study - Banggai Kepulauan. Pages 5- Biodiversit and Conservation 6:153-175 143 & 165-229 in The Indonesian Hellberg M.E. (2007). Footprints on water: the Ornamental Fish Trade: Case Studies and genetic wake of dispersal among reefs. Coral Options for Improving Livelihoods while Reefs, DOI 10.1007/s00338-007-0205-2. Promoting Sustainability in Banggai and Hoffman E.A., Arguello J.R., Kolm N., Berglund Banyuwangi. The International Seafood A. and Jones A.G. (2004). Eleven Trade: Supporting Sustainable Livelihoods polymorphic microsatellite loci in a coral reef Among Poor Aquatic Resource Users in Asia fish, Pterapogon kauderni. Molecular (EC Prep Project EP/RO3/R14). Poseidon Ecology Notes (2004) 4 pp. 342-344 and Network of Aquaculture Centres in Asia Hoffman E.A., Kolm N., Berglund A., Arguello (NACA) STREAM. J.R. and Jones A.G. (2005). Genetic Palumbi S.R. (2003). Population Genetics, structure in the coral-reef-associated Demographic Connectivity, and the Design Banggai cardinalfish, Pterapogon kauderni. of Marine Reserves. Ecological Applications, Blackwell Publishing Ltd.Molecular Ecology 13(1) Supplement: S146–S158 (2005) 14, 1367–1375. Parenti L.R. and Soeroto B. (2004). Indrawan M. and Suseno (2008). The Adrianichthys roseni and Oryzias complications of CITES inclusion of endemic nebulosus, two new ricefishes species in Indonesia: Lessons learned from (Atherinomorpha: Beloniformes: an in-country deliberation on protecting the Adrianichthyidae) from Lake Poso, Banggai cardinalfish, Pterapogon kauderni. Sulawesi, Indonesia. Ichthyol Res 51: SPC Live Reef Fish Information Bulletin 10–19 #18:13-16 Reiss H., Hoarau G., Dickey-Collas. M and Wolf Kolm N., Hoffman E.A., Olsson J., Berglund A., W.J. (2009). Genetic population structure of and Jones A.G. (2005). Group stability and marine fish: mismatch between biological homing behaviour but no kin group and fisheries management units. Fish and structures in a coral reef fish. Behavioural Fisheries 10:361–395 Ecology 16:521–527 Rocha L.A., Craig M.T. and Bowen B.W. (2007). Koumans, F. P. 1933. On a new genus and Phylogeography and the conservation of species of Apogonidae. Zoologische coral reef fishes. Coral Reefs, DOI Mededeelingen (Leiden) 16 (1-2): 78, Pl. 1. 10.1007/s00338-007-0261-7 Latupono F. (2009). Data Enumerator BCF Thacker C.E. (2009). Phylogeny of Gobioidei Tahun 2009 (Excel file) and Placement within Acanthomorpha, with Lilley R. (2008). The Banggai cardinalfish: An a New Classification and Investigation of overview of conservation challenges. SPC Diversification and Character Evolution. Live Reef Fish Information Bulletin #18:3-12 Copeia, 2009(1):93-104. 2009 Loos S.A. (2006). Exploration of MARXAN for Thacker C.E. and Roje D.M. (2009). Phylogeny Utility in Marine Protected Area Zoning. A of cardinalfishes (Teleostei: Gobiiformes: Thesis Submitted in Partial Fulfilment of the Apogonidae) and the evolution of visceral Requirements for the Degree of Master of bioluminescence. Molecular Phylogenetics Science in the Department of Geography, and Evolution 52:735–745 University of Victoria, Canada. Vagelli A. (1999). The Reproductive biology and Moore A. and Ndobe S. (2007a). Discovery of an early ontogeny of the mouthbrooding introduced Banggai Cardinalfish population Banggai Cardinalfish, Pterapogon kauderni in Palu Bay, Central Sulawesi, Indonesia. (Perciformes, Apogonidae). Environmental Coral Reefs 26:569. Biology of Fishes 56:79-92 Moore A. and Ndobe S. (2007b). The Banggai Vagelli A.A. & Erdmann M.V. (2002). First Cardinalfish and CITES – a local Comprehensive Survey of the Banggai perspective. Reef Encounters Vol.38:15-17. Cardinalfish, Pterapogon kauderni. Moore A., Ndobe S. and Zamrud M. (2011). Environmental Biology of Fishes 63:1-8 Monitoring the Banggai Cardinalfish, an Vagelli A.A. (2005). Reproductive Biology, Endangered Restricted Range Endemic Geographic Distribution and Ecology of the Species. Paper presented at the 2nd Coral Banggai Cardinalfish Pterapogon kauderni Reef Management Symposium on Coral Koumans, 1933 (Perciformes, Apogonidae), Triangle Area. with Considerations on the Conservation Ndobe S. and Moore A. (2009). Banggai Status of this Species on its Natural Habitat. cardinalfish: towards a sustainable PhD. Dissertation, University of Buenos Aires, Argentina

28 Ndobe et al./JICoR vol. 1 (1) (2011): 15-29

Vagelli A.A. (2008). The unfortunate journey of Pterapogon kauderni: A remarkable apogonid endangered by the international ornamental fish trade, and its case in CITES. SPC Live Reef Fish Information Bulletin #18:17-28 Vagelli A.A. (2009). The reproductive biology of Quinca mirifica (Apogonidae). Can it help to clarify the evolution of direct development and intergeneric relation ships in apogonids? Paper presented at the 8th Indo - Pacific Fish Conference, 1-5 June 2009. (http://www.ipfc2009asfb.com/pdf/speaker_ presentations/Vagelli,Alejandro.pdf, downloaded 26 August, 2009) Vagelli A.A., Burford M. and Bernardi G. (2009). Fine scale dispersal in Banggai Cardinalfish, Pterapogon kauderni, a coral reef species lacking a pelagic larval phase. Marine Genomics 1:129–134. Vié, J.-C., Hilton-Taylor, C. and Stuart, S.N. (eds.) (2009). Wildlife in a Changing World – An Analysis of the 2008 IUCN Red List of Threatened Species. Gland, Switzerland: IUCN Wilson J., Darmawan A., Subijanto J., Green A., and Sheppard S. (2011). Scientific design of a resilient network of marine protected areas. Lesser Sunda Ecoregion, Coral Triangle. The Nature Conservancy Asia Pacific Marine Program. Report 2/11. http://conserveonline.org/workspaces/tncc oral triangle/documents/resilient-mpa- networklesser-sunda-ecoregion/ (downloaded 22 July 2011)

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