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Fishes (Gobiidae and Labridae) associated with the mushroom coral Heliofungia actiniformis (Scleractinia: Fungiidae) in the Philippines

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Abstract

Fish associations with corals are relatively common, but the only fish known to be associated with the mushroom coral Heliofungia actiniformis has been the white pipefish Siokunichthys nigrolineatus. This is the first observations of fishes, other than S. nigrolineatus, associated with the mushroom coral H. actiniformis. Moreover, this is the first record of various fish species cohabiting in a single H. actiniformis individual, resembling cases involving various shrimp species in the same coral host and clown fishes in a single sea anemone.
Fishes (Gobiidae and Labridae) associated with the mushroom
coral Heliofungia actiniformis (Scleractinia: Fungiidae)
in the Philippines
Although the presence of fish on coral colonies and
individual polyps of the Anthozoa is relatively common
(e.g., Munday et al. 1997), the only fish known to be
associated with Heliofungia actiniformis is the white pipefish
Siokunichthys nigrolineatus (see Hoeksema et al. 2011).
Other fishes may hover over individuals of this large solitary
coral polyp, but without direct contact with the tentacles.
In an attempt to find S. nigrolineatus, I searched several
hundred polyps of H. actiniformis at 3–28 m depth in the
Davao Gulf between July 2010 and May 2011. Instead of
S. nigrolineatus, I regularly observed members of the
Gobiidae (Eviota lachdeberei,E. pellucida, and Trimma sp.,
Fig. 1a) and Labridae (Bodianus diana,Cirrhilabrus
exquisitus,Oxycheilinus celebicus, and O. orientalis) among
the tentacles of H. actiniformis. About every 15th coral polyp
was inhabited by one or two fish and, at a few occasions,
specimens of more than one fish species were present on a
single coral polyp (Fig. 1b). These fishes dwelled within the
coral canopy apparently without being adversely affected.
Although these fishes survive outside this coral microhabitat,
I repeatedly observed one specimen of E. lachdeberei
occupying the same coral polyp over a period of 5 days. The
representatives of the Gobiidae were mostly adult specimens,
whereas those of the Labridae were exclusively juveniles.
Small juveniles (£4 cm TL) resided among the tentacles,
whereas larger juveniles hovered over the tentacles or swam
along the coral periphery. This is the first observation of
fishes, other than S. nigrolineatus, associated with the mushroom coral H. actiniformis. Moreover, this is the first record of
various fish species cohabiting in a single H. actiniformis individual, resembling cases involving various shrimp species in the
same coral host (Hoeksema and Fransen 2011) and clown fishes in a single sea anemone (Bos 2011).
References
Bos AR (2011) Clownfishes Amphiprion clarkii and A. sandaracinos (Pomacentridae) coexist in the sea anemone Stichodactyla mertensii. Coral Reefs
30:369
Hoeksema BW, Fransen CHJM (2011) Space partitioning by symbiotic shrimp species cohabitating in the mushroom coral Heliofungia actiniformis at
Semporna, eastern Sabah. Coral Reefs 30:519
Hoeksema BW, van der Meij S, Fransen CHJM (2011) The mushroom coral as a habitat. J Mar Biol Assoc UK 91: doi:10.1017/S0025315411001445
Munday PL, Jones GP, Caley MJ (1997) Habitat specialisation and the distribution and abundance of coral-dwelling gobies. Mar Ecol Prog Ser
152:227–239
A. R. Bos (&)
The Netherlands Center for Biodiversity Naturalis, P.O. Box 9517, 2300 RA Leiden, The Netherlands
e-mail: arthurrbos@yahoo.com
A. R. Bos
Biology Department, American University Cairo, P.O. Box 74, New Cairo 11835, Egypt
Fig. 1 Gobies aTrimma sp. (undescribed species), bEviota pellucida and
E. lachdeberei, and the shrimp Cuapetes lacertae among tentacles of Heliofungia
actiniformis
123
Received: 23 July 2011 / Accepted: 7 October 2011/ Published online: 21 October 2011
Springer-Verlag 2011
Coral Reefs (2012) 31:133
DOI 10.1007/s00338-011-0834-3
Reef sites
... However, this shelter can become temporarily lost when the corals become buried or overturned (Bongaerts et al., 2012;Hoeksema and Bongaerts, 2016). Individuals of other associated symbiotic species, which may include many other invertebrates and various fish species, dwell on the external upper side of mushroom corals (Bos, 2012;Hoeksema and Farenzena, 2012;Hoeksema and Ten Hove, 2014;Bos andHoeksema, 2015, 2017;Montano et al., 2015). Hence, it is expected that mushroom corals may potentially offer different habitats to associated symbiotic copepods. ...
... However, this shelter can become temporarily lost when the corals become buried or overturned (Bongaerts et al., 2012;Hoeksema and Bongaerts, 2016). Individuals of other associated symbiotic species, which may include many other invertebrates and various fish species, dwell on the external upper side of mushroom corals (Bos, 2012;Hoeksema and Farenzena, 2012;Hoeksema and Ten Hove, 2014;Bos andHoeksema, 2015, 2017;Montano et al., 2015). Hence, it is expected that mushroom corals may potentially offer different habitats to associated symbiotic copepods. ...
... The finding of generalist symbionts living in association with various coral species across a range of fungiid genera is also reported for other taxa, such as coral-excavating mussels (Kleemann and Hoeksema, 2002;Owada and Hoeksema, 2011), coral barnacles , epitoniid snails (Gittenberger and Hoeksema, 2013), hydroids of the genus Zanclea (Montano et al., 2015), coral gall crabs (van der Meij and Hoeksema, 2013; Van der Meij et al., 2015;Hoeksema et al., 2018), sessile ctenophores (Alamaru et al., 2016(Alamaru et al., , 2017, and cryptobenthic fishes (Bos, 2012;Bos andHoeksema, 2015, 2017). Interestingly, some coral-dwelling polychaetes of the genus Spirobranchus, which are commonly found on large ranges of hosts (Molodtsova et al., 2016;Perry et al., 2017), are scarcely recorded from fungiid corals (Hoeksema and ten Hove, 2014). ...
... However, this shelter can become temporarily lost when the corals become buried or overturned (Bongaerts et al., 2012;Hoeksema and Bongaerts, 2016). Individuals of other associated symbiotic species, which may include many other invertebrates and various fish species, dwell on the external upper side of mushroom corals (Bos, 2012;Hoeksema and Farenzena, 2012;Hoeksema and Ten Hove, 2014;Bos andHoeksema, 2015, 2017;Montano et al., 2015). Hence, it is expected that mushroom corals may potentially offer different habitats to associated symbiotic copepods. ...
... However, this shelter can become temporarily lost when the corals become buried or overturned (Bongaerts et al., 2012;Hoeksema and Bongaerts, 2016). Individuals of other associated symbiotic species, which may include many other invertebrates and various fish species, dwell on the external upper side of mushroom corals (Bos, 2012;Hoeksema and Farenzena, 2012;Hoeksema and Ten Hove, 2014;Bos andHoeksema, 2015, 2017;Montano et al., 2015). Hence, it is expected that mushroom corals may potentially offer different habitats to associated symbiotic copepods. ...
... The finding of generalist symbionts living in association with various coral species across a range of fungiid genera is also reported for other taxa, such as coral-excavating mussels (Kleemann and Hoeksema, 2002;Owada and Hoeksema, 2011), coral barnacles , epitoniid snails (Gittenberger and Hoeksema, 2013), hydroids of the genus Zanclea (Montano et al., 2015), coral gall crabs (van der Meij and Hoeksema, 2013; Van der Meij et al., 2015;Hoeksema et al., 2018), sessile ctenophores (Alamaru et al., 2016(Alamaru et al., , 2017, and cryptobenthic fishes (Bos, 2012;Bos andHoeksema, 2015, 2017). Interestingly, some coral-dwelling polychaetes of the genus Spirobranchus, which are commonly found on large ranges of hosts (Molodtsova et al., 2016;Perry et al., 2017), are scarcely recorded from fungiid corals (Hoeksema and ten Hove, 2014). ...
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... To generate the comprehensive list of marine fishes present in southern Mindanao, we supplemented the fish market survey with data from: (1) underwater fish visual census (CL Nañola, AC Eballe, GS Gumanao, and RB Sobradil) conducted in Davao Gulf from 2019 to 2022; and (2) published literature on Pujada Bay (Nañola et al. 2011, Eballe 2014, Davao Gulf (Motomura et al. 2001, Alcala et al. 2008, Nañola et al. 2011, Bos 2012, Bos and Gumanao 2013, Bucol and Alcala 2015, Gumanao et al. 2016, Bos and Hoeksema 2015, Cabasan et al. 2017, Elumba et al. 2019, Gumanao et al. 2022, Labrador et al. 2022, Gumanao et al. 2023, Fortaleza et al. 2024, and Sarangani Bay (Alcala et al. 2008, Nañola et al. 2011, Tea et al. 2018; and (3) the National Stock Assessment Program (NSAP) of the Bureau of Fisheries and Aquatic Resources (BFAR) published by Emperua et al. (2018) and Villanueva (2018). ...
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The Philippines has been long known for its multispecies fisheries, and while there is a growing effort to document fish diversity, collections-based species inventories remain insufficient in southern Mindanao. Market survey efforts conducted in Pujada Bay, Davao Gulf, and Sarangani Bay in the last ten years resulted in documenting 556 species of marine fishes from 82 families, while underwater fish visual census (FVC) surveys conducted in Davao Gulf from 2019 to 2022 revealed 365 species in 42 families. Combining the data from market surveys, FVC, and published literature, we present 771 species of marine fishes (770 teleosts, 1 elasmobranch) belonging to 94 families. Of the 771 species documented, 130 are deep reef and deepwater species, while 20 species await further taxonomic investigations for species-level identifications.Moreover, 498 cytochrome oxidase I (COI) genetic barcodes were produced representing 357 species from 59 families, which covers 46% of the total number of species reported and 63% of the market survey data. Genetic distances based on taxonomic ranks were concordant with other barcoding studies on marine fishes. Samples (20 species) with pairwise genetic distances that did not conform with the expected intra- and interspecific threshold suggest cases that also need to be investigated further (e.g., incomplete lineage sorting, introgressive hybridization, crypticspeciation). All market survey data used in genetic barcoding correspond to tissue samples, live-color photographs, and preserved specimens. This work complements the DNA barcode libraries reported recently in the country, and this serves as an additional reference for future biodiversity management and conservation efforts.
... Scleractinian corals are known to host a variety of organisms belonging to different phyla [1][2][3][4][5][6]. Among coral ectosymbionts, the acoel flatworms of the genus Waminoa (Order Acoela, Family Convolutidae) have been studied only recently. ...
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... Selain itu Hoeksema dan Fransen (2011) mengungkapkan bahwa tujuh spesies udang ditemukan pada spesies ini. Beberapa jenis ikan cryptobenthic seperti Eviota pellucida dan E. Lachdeberei juga menggunakan tentakel Heliofungia actiniformis sebagai mikro habitat (Bos 2012). ...
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... obs.); [42] Acanthaster (Bos et al., 2013) and Drupella (Gumanao, pers. obs.); [43] a conservative estimate based on the presence of 56 scleractinian genera and 35 mushroom coral species(Gumanao, 2009;Bos and Hoeksema, 2017); [44]Nañola and Ingles (2003),Bos (2012Bos ( , 2014, Gumanao (2012, 2013),Bos and Smits (2013), Hoeksema (2015, 2017), Gumanao et al. (2016), Bos et al. (2018); [45] Mancao et al. (2008), Horigue et al. (2012), Cabral et al. (2014); [46] Wood (1977, 1979); [47] Aripen et al. (2002); [48] Spait (2001), Jakobsen et al. (2007); [49] Abdul-Hadi et al. (2013), Gallagher et al. (2016); [50] Ali et al. (2014); [51] Ali et al. (2015); [52] Mathias and Langham (1978), Pilcher and Cabanban (2000), Spait (2001), Theng et al. (2003), Waheed et al. (2007); [53] Adnan et al. (2015), Mobilik et al. (2016); [54] Woodman et al. (2004), Reef Check Malaysia (2010); [55] Cabanban and Nais (2003); [56] Phillips (1979); [57] Waheed and Hoeksema (2014); [58] Spait (2001); [59] in 2012 and 2016 (Aw and Syed Hussein, 2012; Waheed pers. obs.); [60] Syed Hussein and Nooramli (2016); [61] Nyanti and Johnston (1992), Waheed et al. (2011), Huang et al. (2015), Waheed and Hoeksema (2014); [62] Townsend (2015); [63] Pang et al. (2016); [64] Tunkul Abdul Rahman Park (Nyanti and Johnston, 1992); [65] the population of the Brunei-Muara District conglomerate is much larger; [66] Chou et al. (1987), DeVantier and Turak (2009), Turak and DeVantier (2009); [67] Turak and DeVantier (2009), Lane and Lim (2013); [68] De Silva (1987); [69] Yong et al. (2006), most reports are about Brunei Bay and not about the offshore reefs (e.g. ...
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... Data of the present study, and those published by Gumanao et al. actiniformis, were firstly found to be associated with mushroom corals (Bos, 2012;Bos & Hoeksema, 2015 Eye migration is genetically controlled (Palmer, 2016) and individuals usually follow the same orientation; hence 'right-eyed flounders', the common name for the Pleuronectidae. However, a few exceptions of mixed populations do exist. ...
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... They can cause damage to the host coral by eroding its skeleton or by smothering its New interspecific associations have been discovered recently by targeting specific corals in order to examine their possible role as host, involving a shrimp, a worm and snail in the Caribbean (Brinkmann and Fransen 2016;Hoeksema et al. 2017;Potkamp, Vermeij, and Hoeksema in press). Many associates, including new species, have been found in or near Indo-Pacific mushroom corals: (1) hiding underneath corals, such as snails and sessile ctenophores (Alamaru, Brokovich, and (Cheng et al. 2016;Hoeksema and Farenzena 2012;Fransen and Rauch 2013);(5) in between the tentacles, like shrimps and fishes (Bos 2012;Hoeksema and Fransen 2011). Branching corals can offer shelter in between their branches (Stella, Jones, and Pratchett 2010) and some associates of octocorals use camouflage as hiding strategy, as demonstrated by pygmy seahorses (Figure 2; Lourie and Kuiter 2008;Reijnen, van der Meij, and van Ofwegen 2011) and ovulid snails (Reijnen 2010;Sánchez et al. 2016). ...
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Coexistence of clownfish has been observed in several host anemones, usually combined with aggressive behavior among the fish due to the territorial instinct of damselfish. This is the first observation of Amphiprion clarkii and A. sandaracinos in the sea anemone Stichodactylus mertensii, where fish do not perform aggressively towards one another, but rather accept each others presence. Moreover, this coexistence was preferred above the migration to nearby available anemones.
The mushroom coral as a habitat Habitat specialisation and the distribution and abundance of coral-dwelling gobies The Netherlands
  • Hoeksema
  • Bw
  • Van
  • S Meij
  • Fransen
  • Jones Pl Gp Munday
  • Caley
  • Mj
Hoeksema BW, van der Meij S, Fransen CHJM (2011) The mushroom coral as a habitat. J Mar Biol Assoc UK 91: doi:10.1017/S0025315411001445 Munday PL, Jones GP, Caley MJ (1997) Habitat specialisation and the distribution and abundance of coral-dwelling gobies. Mar Ecol Prog Ser 152:227–239 A. R. Bos (&) The Netherlands Center for Biodiversity Naturalis, P.O. Box 9517, 2300 RA Leiden, The Netherlands
The Netherlands Center for The Netherlands e-mail: arthurrbos@yahoo.com A. R
  • A R Bos
  • Ra Leiden
A. R. Bos (&) The Netherlands Center for Biodiversity Naturalis, P.O. Box 9517, 2300 RA Leiden, The Netherlands e-mail: arthurrbos@yahoo.com A. R. Bos Biology Department, American University Cairo, P.O. Box 74, New Cairo 11835, Egypt Fig. 1 Gobies a Trimma sp. (undescribed species), b Eviota pellucida and E. lachdeberei, and the shrimp Cuapetes lacertae among tentacles of Heliofungia actiniformis 123