Next Article in Journal
A Rather Unusual ”Pearl”: Biological Observations of the Hidden Pearlfish Carapus acus (Brünnich, 1768) and Its First Report from Apulian Waters (Salento Peninsula, Southern Italy)
Next Article in Special Issue
First Documented Courtship Behavior between Mobula birostris and M. alfredi at a Coral Reef Cleaning Station in Misool, Raja Ampat
Previous Article in Journal
Diversity of Pleurostomatid Ciliates: Morphology, Taxonomy and Molecular Phylogeny of Freshwater Isolates Found in a Northern China Wetland, with a Description of Two New Species
Previous Article in Special Issue
Threats to a Temperate Kelp Forest Species, Ecklonia cava, through Tropical Fish Herbivory Associated with Sea Surface Warming in the East China Sea
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Diversity
Volume 16
Issue 5
10.3390/d16050295
diversity-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Interesting Images

Stony Corals and Their Associated Fauna Residing in Marine Lakes under Extreme Environmental Conditions

by
Leontine E. Becking
1,2,*,
Stephanie J. Martinez
1,2,
Ludi Parwadani Aji
2,3,
Awaludinnoer Ahmad
4,
Adriana Alzate
1,2,
Mainah Folkers
1,2,
Dea Fauzia Lestari
5,6,
Beginer Subhan
5,6 and
Bert W. Hoeksema
1,7,*
1
Marine Evolution and Ecology Group, Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, The Netherlands
2
Department of Animal Sciences, Wageningen University & Research, De Elst 1, 6700 AR Wageningen, The Netherlands
3
Research Center for Oceanography, Indonesian National Research and Innovation Agency (BRIN), Jl. Pasir Putih No. 1, Ancol, Jakarta 14430, Indonesia
4
Yayasan Konservasi Alam Nusantara (YKAN), Graha Iskandarsyah 3rd. Fl. Jl. Iskandarsyah Raya No. 66C, Jakarta 12160, Indonesia
5
Department of Marine Science and Technology, Faculty of Fisheries and Marine Science, IPB University, Bogor 16680, Indonesia
6
Enhancing Marine Biodiversity Research in Indonesia (EMBRIO), IPB University, Bogor 16680, Indonesia
7
Groningen Institute for Evolutionary Life Sciences, University of Groningen, P.O. Box 11103, 9700 CC Groningen, The Netherlands
*
Authors to whom correspondence should be addressed.
Diversity 2024, 16(5), 295; https://doi.org/10.3390/d16050295
Submission received: 14 April 2024 / Revised: 2 May 2024 / Accepted: 9 May 2024 / Published: 13 May 2024
(This article belongs to the Collection Interesting Images from the Sea)
Browse Figures
Versions Notes

Abstract

:
Tropical marine lakes are small land-locked marine waterbodies occurring in karstic coastal areas. During biodiversity surveys in 12 marine lakes in Raja Ampat, Southwest Papua province, Indonesia, we recorded at least 37 species belonging to 29 genera of hard corals. Their observed associated symbiont fauna consisted of bivalve molluscs and polychaete worms. Marine lake temperature ranged from 30.0 to 32.5 °C, acidity from pH 7.6 to 8.1, and salinity from 26.4 to 33.2 ppt. This study provides the first inventory of the marginal coral communities in the extreme habitat of marine lakes, under chronic extreme environmental conditions of higher temperatures, land-based nutrient loads, and sedimentation.

In recent years, there has been heightened interest in corals that live at the edge of their environmental limits as they can provide insights into how coral communities may survive and adapt to future scenarios of the marine environment [1]. Coral-populated extreme environments are considered possible resilience hotspots and climate-change refugia [1,2,3]. Within this line, marine lakes represent environments with elevated seawater temperatures, lower pH, and natural turbidity [4,5,6]. These small waterbodies are entirely surrounded by land but have a connection to the adjacent sea through subterranean channels and fissures or porous rock [4]. As such, marine lakes contain saline water and harbour marine species communities [6,7,8,9], some of which are anchialine as defined by Holthuis [10]. Marine lakes may contain endemic species of crustaceans [11,12], echinoderms [13,14], sponges [15,16,17], sea anemone [18,19], and benthic forams [20], some of which were observed to be involved in unique species interactions [18,19].
During biodiversity surveys in 2016, 2020, and 2023 in Raja Ampat, west of Bird’s Head Peninsula (Papua, Indonesia), we encountered hard coral species in 12 marine lakes (Figure 1). All marine lakes with coral fauna appeared to have well-developed connections to the sea. These allow frequent flushing of seawater with the adjacent coast and a high influence of terrigenous runoff, resulting in low-visibility waters despite low turbulence. The temperature across the 12 marine lakes ranged from 30.0 to 32.6 °C (Table 1), while in the nearby reefs it ranged from 29.2 to 30.9 °C. The salinity of the lakes also varied, with some of them representing brackish environments (26.4–29.1 ppt) and others that are only slightly lower in salinity (30.0–33.2 ppt) (Table 1) than coastal reefs (33.5–34.5 ppt).
The corals were mostly present at a depth range of 0.5–5 m. In four marine lakes (Papua11, Papua12, Papua15, and Papua24) hard corals represented 10–20% of the total benthic cover [23], resembling inshore and turbid reefs in the Indo-Pacific [24,25,26]. For comparison, the nearby reefs in Raja Ampat can range in coral cover from 10 to 86% [23] In some marine lakes, the corals formed small reefs (Figure 2d and Figure 3c,d), while in others, corals occurred in patches (Figure 2c). Most corals exhibit massive and encrusting growth forms. In some marine lakes, corals also exhibit foliose and branching growth forms, which contribute to increased structural habitat complexity. In the surveyed marine lakes with mangroves, the corals grow on and in between mangrove roots. Corals growing on mangrove roots is an uncommon feature, although there are reports from coastal areas in the Caribbean, such as in the U.S. Virgin Islands [27,28], Panama [29,30], and Florida [31], and also in the Indo-Pacific, such as the Great Barrier Reef [32,33].
Based on photographic evidence that was taken while snorkelling, 37 stony coral species of 29 genera could be distinguished, belonging to 11 scleractinian families and one hydrozoan family (Table 2; Figure 4 and Figure 5). They were identified with the help of Corals of the World [34], updated with the nomenclature of World List of Scleractinia [35]. These corals are generally known to be sediment-tolerant, such as those belonging to the genera Galaxea, Goniopora, Montipora, Pachyseris, Pavona, and Porites [36,37]. Most of the species have previously been reported from turbid reef or mangrove environments. For example, shallow-water branching Acropora spp., foliose Montipora spp., and large massive Porites spp. have been recorded in turbid nearshore coral communities in the Paluma Shoals Reef Complex in the Great Barrier Reef, Australia [26].
Hard corals have been reported in marine lakes before, but little information has been given on the species composition or their diversity. In Palau, which harbours numerous marine lakes, Hamner and Hamner [4] reported the presence of corals in the marine lake Ketau without further specification of species identities, coral cover or coral growth forms. The water in Lake Ketau was isothermal with an average temperature of 29.5 °C, with salinity around 30.5 ppt. Lake Ketau has the general appearance and fauna of the adjacent outside lagoon, with a high diversity of coral-reef fish and many species of corals found in the shallow areas near the islands [4]. Colin [5] reported on coral communities in Palau’s Heliofungia Lake and displayed images of a dense cover of free-living Heliofungia actiformis, as well as encrusting corals with large populations of Septifer mussels growing on them, and a foliose coral (Echinopora lamellosa) growing on a slope of the lake. In Ha Long Bay (Vietnam), four marine lakes have been reported to have coral, although specific species were not mentioned: Lake Dau Be (with a narrow strip of coral reef distributed sparsely around the lake), Lake Qua Bang (narrow strip of corals), Lake Bui Xam (a belt of massive corals), and Hang Du II Lake (the rocky shores of the lake are partially covered by a belt of corals) [38,39]. In Indonesia, Tomascik and Mah [40] reported the coral Alveopora tizardi from the marine Kakaban Lake in East Kalimantan province. However, we did not encounter this species in our surveys. Notably, no other coral species have previously been identified in Indonesian marine lakes.
It is striking that some corals in marine lakes are associated with high numbers of filter feeders (Figure 6 and Figure 7). Records of coral-associated animals can be relevant because of their role as possible bioindicators [41,42,43,44]. Since filter-feeding invertebrates generally appear to be most abundant in relatively shallow, eutrophic water [45], marine lakes could be favourable environments for these organisms.
Clusters of the box mussel bivalve, Septifer bilocularis (family Mytilidae), were present in high densities over the upper surface of massive coral colonies and inside crevices (Figure 6a–c). Boring mussels of the genus Leiosolenus (previously also known as Lithophaga) of the same family lived inside massive Porites corals, showing their characteristic orifices [46,47,48,49] scattered over their host’s surface (Figure 6d). The shell ribs of Septifer bilocularis resemble those of Brachidontes spp., which were also found to be abundant in the lakes but not in association with corals [22]. Since S. bilocularis has also been reported to occur in cryptic upper-sublittoral habitats in dead coral [50], its presence on live coral can perhaps be explained by settlement on small patches of dead surface area of the living host. Interestingly, no bivalves of the genus Pedum (family Pectiniidae) were observed, even though these scallops are commonly observed inside crevices in massive corals on coral reefs across the Indo-West Pacific [51,52,53], including eastern Indonesia [54,55].
Filter-feeding coral-associated tube worms were less abundant than the mussels in the lakes; they belonged to the polychaete families Sabellidae (Figure 7a–c) and Serpulidae (Figure 7d–g). The Sabellidae, popularly known as feather duster worms, have just recently been discovered to form associations with live corals in both the Indo-Pacific and in the Caribbean, where they may cause damage to their hosts [56,57]. Records of sabellids living on dead corals are more common than on live corals [58,59,60,61,62].
The only serpulid worm that could be identified was Floriprotis sabiuraensis (Figure 7d–f), a coral symbiont, which has been reported from various hosts and localities across the Indo-Pacific [49,63,64,65]. The calcareous tube of an unknown serpulid was found attached to the surface of a massive coral (Figure 7g). It does not show the ring-like structures (peristomes) of Floriprotis tubes [64,66] and also not the sharp spike at the tube opening, as seen in most Spirobranchus species [67,68]. It could be an individual belonging to the Sprirobranchus tetraceros species complex, such as in S. schmardi [69], which do not always develop such spikes (ten Hove, personal communication).
Boring sponges may also occur in marine lakes and have here only been recorded from limestone rock but not yet from corals [70,71], as those in open-sea reefs [71,72,73,74]. Other large, striking coral-associated fauna, such as worm snails [75,76,77], barnacles, and gall crabs [49,78,79], were also not observed in the marine lakes of Raja Ampat, and should therefore receive more attention in future studies.
In conclusion, the coral communities and their associated fauna that we have found in the marine lakes of Raja Ampat can be classified as extreme and marginal following the framework by Schoepf et al. [1]. The coral communities in marine lakes survive under chronic extreme environmental conditions of higher temperature, land-based nutrient loads, and sedimentation, and have a species diversity that is lower in comparison to clearwater coastal coral communities. The marine lakes in the current study that contained stony corals had an average temperature of 30.4 °C, which is markedly higher than the average temperatures of 27.9 to 28.5 °C recorded in the reefs of Raja Ampat since 2009 [80,81,82].
Our study is a first assessment of the stony coral diversity of marine lakes. The list of corals that we present here (Table 2) is a first qualitative compilation based on photographic evidence. Future work will require a systematic documentation of the coral biodiversity, which will likely result in additional species records. Further research will assess to what extent these marine lakes can serve as natural laboratories, where resident coral communities are experiencing conditions of future climate scenarios (high temperature and low pH) combined with local stressors on water quality (e.g., sedimentation and eutrophication).

Author Contributions

Conceptualization, L.E.B. and B.W.H.; investigation, L.E.B., S.J.M., A.A. (Awaludinnoer Ahmad), L.P.A., A.A. (Adriana Alzate), M.F., D.F.L., B.S. and B.W.H.; writing—original draft preparation, L.E.B.; writing—review and editing, L.E.B., S.J.M., A.A. (Awaludinnoer Ahmad), L.P.A., A.A. (Adriana Alzate), M.F., D.F.L., B.S. and B.W.H.; funding acquisition, L.E.B. and L.P.A. All authors have read and agreed to the published version of the manuscript.

Funding

This work was financially supported by the Dutch Research Council (NWO) project VI.Vidi.193.137 for L.E. Becking and by the Endowment Fund for Education (LPDP) Scholarship from the Ministry of Finance of the Republic of Indonesia for L.P. Aji. A. Alzate has received funding from the European Union’s Horizon 2020 research and innovation programme under the Marie Skłodowska-Curie grant agreement No 101061723, from the KNAW Ecology Fund of the Royal Netherlands Academy of Arts and Sciences with a KNAW Ecology Fund Grant (2023045), and from the Treub-Maatschappij (Society for the Advancement of Research in the Tropics).

Acknowledgments

The authors are very grateful to Pak Syafrie (UPTD BLUD), Purwanto (CTC), Lukas Rumetna (YKAN), Fitry Pakiding (UNIPA), Augy Syahailatua (BRIN), Udhi Hernawan (BRIN), Fredinan Yulianda (IPB), Mala Nurilmala (IPB), Christiaan de Leeuw, Diede Maas, Agustin Capriati, Max Ammer, Andi and Marit Miners, Misool Foundation, Raja Ampat Research and Conservation Center (RARCC), Misool Eco Resort, and Papua Diving for assistance during the fieldwork. Research permits were provided by RISTEK in 2016 and 2020, and BRIN in 2023. We are grateful to Maria Ana Tovar-Hernández (Universidad Autónoma de Nuevo León, Mexico) and Harry A. ten Hove (Naturalis Biodiversity Center, The Netherlands) for their assistance in the identification of the tube worms, and Carden Wallace for help with the species identification of the Acropora species. We want to thank five anonymous reviewers for their constructive comments, which helped us to improve the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Schoepf, V.; Baumann, J.H.; Barshis, D.J.; Browne, N.K.; Camp, E.F.; Comeau, S.; Cornwell, C.E.; Guzmán, H.M.; Riegl, B.; Rodolfo-Metalpa, R.; et al. Corals at the edge of environmental limits: A new conceptual framework to re-define marginal and extreme coral communities. Sci. Total Environ. 2023, 884, 163688. [Google Scholar] [CrossRef]
  2. Cacciapaglia, C.; van Woesik, R. Climate-change refugia: Shading reef corals by turbidity. Glob. Chang. Biol. 2016, 22, 1145–1154. [Google Scholar] [CrossRef]
  3. Sully, S.; van Woesik, R. Turbid reefs moderate coral bleaching under climate-related temperature stress. Glob. Chang. Biol. 2020, 26, 1367–1373. [Google Scholar] [CrossRef]
  4. Hamner, W.M.; Hamner, P. Stratified marine lakes of Palau (Western Caroline Islands). Phys. Geogr. 1998, 19, 175–220. [Google Scholar] [CrossRef]
  5. Colin, P.L. Marine Environments of Palau; Coral Reef Research Foundation: Koror, Palau, 2009; pp. ix, 414. [Google Scholar]
  6. Becking, L.E.; Renema, W.; Santodomingo, N.K.; Hoeksema, B.W.; Tuti, Y.; de Voogd, N.J. Recently discovered landlocked basins in Indonesia reveal high habitat diversity in anchialine systems. Hydrobiologia 2011, 677, 89–105. [Google Scholar] [CrossRef]
  7. Tomascik, T.; Mah, A.J. The ecology of “Halimeda lagoon”: An achialine lagoon of a raised atoll, Kakaban Island, East Kalimantan, Indonesia. Trop. Biodivers. 1994, 2, 385–399. [Google Scholar]
  8. Tomascik, T.; Mah, A.J.; Nontji, A.; Moosa, M.K. The Ecology of the Indonesian Seas; Periplus: Singapore, 1997. [Google Scholar]
  9. Maas, D.L.; Capriati, A.; Ahmad, A.; Erdmann, M.V.; Lamers, M.; de Leeuw, C.A.; Prins, L.; Putri, A.P.; Tapilatu, R.F.; Becking, L.E. Recognizing peripheral ecosystems in marine protected areas: A case study of golden jellyfish lakes in Raja Ampat, Indonesia. Mar. Pollut. Bull. 2020, 151, 110700. [Google Scholar] [CrossRef]
  10. Holthuis, L.B. Caridean shrimps found in land-locked salt-water pools at four Indo-West Pacific localities (Sinai Peninsula, Funafuti Atoll, Maui and Hawaii Islands), with the description of one new genus and four new species. Zool. Verh. 1973, 128, 1–48. [Google Scholar]
  11. Ng, P.K.L.; Tomascik, T. Orcovita saltatrix, a new genus and species of anchialine varunine crab (Crustacea: Decapoda: Brachyura: Grapsidae) from Kakaban Island, Indonesia. Raffles Bull. Zool. 1994, 42, 937–948. [Google Scholar]
  12. Fransen, C.H.J.M.; Tomascik, T. Parhippolyte uveae Borradaile, 1899 (Crustacea: Decapoda: Hippolytidae) from Kakaban Island, Indonesia. Zool. Meded. 1996, 70, 227–233. [Google Scholar]
  13. Massin, C.; Tomascik, T. Two new holothurians (Echinodermata: Holothuroidea) from an anchialine lagoon of an uplifted atoll, Kakaban Island, East Kalimantan, Indonesia. Raffles Bull. Zool. 1996, 44, 157–172. [Google Scholar]
  14. Setiadi, A. A new genus and two new species of sea stars (Family Asterinidae) from Indonesian marine lakes, with notes on habitat and feeding ecology. Zootaxa 2019, 4712, 392–402. [Google Scholar] [CrossRef] [PubMed]
  15. Becking, L.E. Revision of the genus Placospongia (Porifera, Demospongiae, Hadromerida, Placospongiidae) in the Indo-West Pacific. ZooKeys 2013, 298, 39–76. [Google Scholar] [CrossRef] [PubMed]
  16. Santodomingo, N.; Becking, L.E. Unravelling the moons: Review of the genera Paratetilla and Cinachyrella in the Indo-Pacific (Demospongiae, Tetractinellida, Tetillidae). ZooKeys 2018, 791, 1–46. [Google Scholar] [CrossRef] [PubMed]
  17. Calcinai, B.; Cerrano, C.; Núñez-Pons, L.; Pansini, M.; Thung, D.C.; Bertolino, M. A new species of Spongilla (Porifera, Demospongiae) from a karst lake in Ha Long Bay (Vietnam). J. Mar. Sci. Eng. 2020, 8, 1008. [Google Scholar] [CrossRef]
  18. Fautin, D.G.; Fitt, W.K. A jellyfish-eating sea anemone (Cnidaria, Actiniaria) from Palau: Entacmaea medusivora sp. nov. Hydrobiologia 1991, 216, 453–461. [Google Scholar] [CrossRef]
  19. Hoeksema, B.W.; Tuti, Y.; Becking, L.E. Mixed medusivory by the sea anemone Entacmaea medusivora (Anthozoa: Actiniaria) in Kakaban Lake, Indonesia. Mar. Biodivers. 2015, 45, 141–142. [Google Scholar] [CrossRef]
  20. Kawagata, S.; Yamasaki, M.; Jordan, R.W. Acarotrochus lobulatus, a new genus and species of shallow-water benthic foraminifer from Mecherchar Jellyfish Lake, Palau, NW equatorial Pacific Ocean. J. Foram. Res. 2005, 35, 44–49. [Google Scholar] [CrossRef]
  21. de Leeuw, C.A.; Peijnenburg, K.T.C.A.; Gillespie, R.G.; Maas, D.L.; Hanzawa, N.; Tuti, Y.; Toha, A.H.A.; Aji, L.P.; Becking, L.E. First come, first served: Possible role for priority effects in marine populations under different degrees of dispersal potential. J. Biogeogr. 2020, 47, 1649–1662. [Google Scholar] [CrossRef]
  22. Aji, L.P.; Goud, J.; van der Steeg, S.; Tapilatu, R.; Maas, D.L.; Becking, L.E. The diversity of molluscan faunas in marine lakes of Raja Ampat, West Papua, Indonesia. Contrib. Zool. 2023, 92, 391–430. [Google Scholar] [CrossRef]
  23. Aji, L.P.; Maas, D.L.; Capriati, A.; Ahmad, A.; de Leeuw, C.; Becking, L.E. Shifts in dominance of benthic communities along a gradient of water temperature and turbidity in tropical coastal ecosystems. PeerJ 2024, 12, e17132. [Google Scholar] [CrossRef]
  24. Cleary, D.F.R.; Polónia, A.R.M.; Renema, W.; Hoeksema, B.W.; Wolstenholme, J.; Tuti, Y.; de Voogd, N.J. Coral reefs next to a major conurbation: A study of temporal change (1985–2011) in coral cover and composition in the reefs of Jakarta, Indonesia. Mar. Ecol. Prog. Ser. 2014, 501, 89–98. [Google Scholar] [CrossRef]
  25. Cleary, D.F.R.; Polónia, A.R.M.; Renema, W.; Hoeksema, B.W.; Rachello-Dolmen, P.G.; Moolenbeek, R.G.; Budiyanto, A.; Yahmantoro; Tuti, Y.; Draisma, S.G.A.; et al. Variation in the composition of corals, fishes, sponges, echinoderms, ascidians, molluscs, foraminifera and macroalgae across a pronounced in-to-offshore environmental gradient in the Jakarta Bay–Thousand Islands coral reef complex. Mar. Pollut. Bull. 2016, 110, 701–717. [Google Scholar] [CrossRef] [PubMed]
  26. Morgan, K.M.; Perry, C.T.; Smithers, S.G.; Johnson, J.A.; Daniell, J.J. Evidence of extensive reef development and high coral cover in nearshore environments: Implications for understanding coral adaptation in turbid settings. Sci. Rep. 2016, 6, 29616. [Google Scholar] [CrossRef] [PubMed]
  27. Rogers, C.S. A unique coral community in the mangroves of Hurricane Hole, St. John, US Virgin Islands. Diversity 2017, 9, 29. [Google Scholar] [CrossRef]
  28. Rogers, C.S. Immediate effects of hurricanes on a diverse coral/mangrove ecosystem in the US Virgin Islands and the potential for recovery. Diversity 2019, 11, 130. [Google Scholar] [CrossRef]
  29. Stewart, H.A.; Kline, D.I.; Chapman, L.J.; Altieri, A.H. Caribbean mangrove forests act as coral refugia by reducing light stress and increasing coral richness. Ecosphere 2021, 12, e03413. [Google Scholar] [CrossRef]
  30. Stewart, H.A.; Wright, J.L.; Carrigan, M.; Altieri, A.H.; Kline, D.I.; Araújo, R.J. Novel coexisting mangrove-coral habitats: Extensive coral communities located deep within mangrove canopies of Panama, a global classification system and predicted distributions. PLoS ONE 2022, 17, e0269181. [Google Scholar] [CrossRef]
  31. Flowers, K.; Golembeski, P.; Ross, B.; Karp, R.F.; Baker, A.C. Visual surveys reveal coral growth in mangrove fringe in a subtropical metropolis. Bull. Mar. Sci. 2023, 99, 145–146. [Google Scholar] [CrossRef]
  32. Yates, K.K.; Rogers, C.S.; Herlan, J.J.; Brooks, G.R.; Smiley, N.A.; Larson, R.A. Diverse coral communities in mangrove habitats suggest a novel refuge from climate change. Biogeosciences 2014, 11, 4321–4337. [Google Scholar] [CrossRef]
  33. Camp, E.F.; Edmondson, J.; Doheny, A.; Rumney, J.; Grima, A.J.; Huete, A.; Suggett, D.J. Mangrove lagoons of the Great Barrier Reef support coral populations persisting under extreme environmental conditions. Mar. Ecol. Prog. Ser. 2019, 625, 1–14. [Google Scholar] [CrossRef]
  34. Veron, J.E.N. Corals of the World; Australian Institute of Marine Sciences and CRR Qld Pty Ltd.: Townsville, Australia, 2000.
  35. Hoeksema, B.W.; Cairns, S. Word List of Scleractinia. Available online: https://www.marinespecies.org/scleractinia/ (accessed on 14 March 2024).
  36. Zweifler, A.; O’Leary, M.; Morgan, K.; Browne, N.K. Turbid coral reefs: Past, present and future—A review. Diversity 2021, 13, 251. [Google Scholar] [CrossRef]
  37. Rosedy, A.; Ives, I.; Waheed, Z.; Hussein, M.A.S.; Sosdian, S.; Johnson, K.; Santodomingo, N. Turbid reefs experience lower coral bleaching effects in NE Borneo (Sabah, Malaysia). Reg. Stud. Mar. Sci. 2023, 68, 103268. [Google Scholar] [CrossRef]
  38. Cerrano, C.; Azzini, F.; Bavestrello, G.; Calcinai, B.; Pansini, M.; Sarti, M.; Thung, D.C. Marine lakes of karst islands in the Ha Long Bay (Vietnam). Chem. Ecol. 2006, 22, 489–500. [Google Scholar] [CrossRef]
  39. Ngai, N.D.; Thao, D.V.; Thung, D.C.; Thuy, L.T.; Tien, D.D.; Quan, N.V.; Chien, P.V. Biological community in submerged caves and marine lakes in ha Long-Cat Ba Area, Vietnam. J. Life Sci. 2015, 9, 541–548. [Google Scholar] [CrossRef]
  40. Tomascik, T.; Mah, A.J. Presence of Alveopora tizardi (Scleractinia: Acroporidae) as an epibiont on molluscan shells in an anchialine lake of a raised atoll, Kakaban Island, East Kalimantan, Indonesia: An opportunist or a survivor? Galaxea J. Coral Reef Stud. 2023, 25, 9–10. [Google Scholar] [CrossRef]
  41. Risk, M.J.; Heikoop, J.M.; Edinger, E.N.; Erdmann, M.V. The assessment ‘toolbox’: Community-based reef evaluation methods coupled with geochemical techniques to identify sources of stress. Bull. Mar. Sci. 2001, 69, 443–458. [Google Scholar]
  42. Fonseca, E.A.C.; Dean, H.K.; Cortés, J. Non-colonial coral macro-borers as indicators of coral reef status in the south Pacific of Costa Rica. Rev. Biol. Trop. 2006, 54, 101–115. [Google Scholar] [CrossRef]
  43. Scaps, P.; Denis, V. Can organisms associated with live scleractinian corals be used as indicators of coral reef status? Atoll Res. Bull. 2008, 566, 1–21. [Google Scholar] [CrossRef]
  44. Lymperaki, M.M.; Hill, C.E.; Hoeksema, B.W. The effects of wave exposure and host cover on coral-associated fauna of a centuries-old artificial reef in the Caribbean. Ecol. Eng. 2022, 176, 106536. [Google Scholar] [CrossRef]
  45. van der Schoot, R.J.; Hoeksema, B.W. Abundance of coral-associated fauna in relation to depth and eutrophication along the leeward side of Curaçao, southern Caribbean. Mar. Environ. Res. 2022, 181, 105738. [Google Scholar] [CrossRef] [PubMed]
  46. Kleemann, K.H. Boring bivalves and their host corals from the Great Barrier Reef. J. Molluscan Stud. 1980, 46, 13–54. [Google Scholar] [CrossRef]
  47. Wong, K.T.; Tsang, R.H.L.; Ang, P. Did borers make corals more susceptible to a catastrophic disease outbreak in Hong Kong? Mar. Biodivers. 2016, 46, 325–326. [Google Scholar] [CrossRef]
  48. Hoeksema, B.W.; Smith-Moorhouse, A.; Harper, C.E.; van der Schoot, R.J.; Timmerman, R.F.; Spaargaren, R.; Langdon-Down, S.J. Black mantle tissue of endolithic mussels (Leiosolenus spp.) is cloaking borehole orifices in Caribbean reef corals. Diversity 2022, 14, 401. [Google Scholar] [CrossRef]
  49. van der Schoot, R.J.; Hoeksema, B.W. Host specificity of coral-associated fauna and its relevance for coral reef biodiversity. Int. J. Parasitol. 2024, 54, 65–88. [Google Scholar] [CrossRef] [PubMed]
  50. Arnaud, P.M.; Thomassin, B.A. Habits and morphological adaptations of mytilids (Mollusca: Bivalvia) from coastal and reefal environments in southwest Malagasia (Indian Ocean). In The Bivalvia—Proceedings of a Memorial Symposium in Honour of Sir Charles Maurice Yonge, Edinburgh, 1986; Morton, B., Ed.; Hong Kong University Press: Hong Kong, China, 1990; pp. 333–344. [Google Scholar]
  51. Kleemann, K. The pectinid bivalve Pedum spondyloideum (Gmelin 1791): Amount of surface and volume occupied in host corals from the Red Sea. Mar. Ecol. 2001, 22, 111–133. [Google Scholar] [CrossRef]
  52. Chan, B.K.; Tan, J.C.; Ganmanee, M. Living in a growing host: Growth pattern and dwelling formation of the scallop Pedum spondyloideum in massive Porites spp. corals. Mar. Biol. 2020, 167, 95. [Google Scholar] [CrossRef]
  53. Scaps, P. Association between the scallop Pedum spondyloideum (Bivalvia: Pteriomorphia: Pectinidae) and scleractinian corals from Nosy Be, Madagascar. Cah. Biol. Mar. 2020, 61, 73–80. [Google Scholar] [CrossRef]
  54. Scaps, P.; Denis, V.; Berhimpon, S.; Kaligis, F. Coral associations and space competitors of Pedum spondyloideum (Gmelin, 1791) (Bivalvia, Pteriomorphia: Pectiniidae) from the northeast coast of Sulawesi. Basteria 2005, 69, 157–166. [Google Scholar]
  55. Scaps, P.; Denis, V. Association between the scallop, Pedum spondyloideum, (Bivalvia: Pteriomorphia: Pectinidae) and scleractinian corals from the Wakatobi Marine National Park (Southeastern Sulawesi, Indonesia). Raffles Bull. Zool. 2007, 55, 371–380. [Google Scholar]
  56. Tovar-Hernández, M.A.A.; García-Garza, M.E.; de León-González, J.A. Sclerozoan and fouling sabellid worms (Annelida: Sabellidae) from Mexico with the establishment of two new species. Biodivers. Data J. 2020, 8, e57471. [Google Scholar] [CrossRef] [PubMed]
  57. Hoeksema, B.W.; Timmerman, R.F.; Spaargaren, R.; Smith-Moorhouse, A.; van der Schoot, R.J.; Langdon-Down, S.J.; Harper, C. Morphological modifications and injuries of corals caused by feather duster worms (Sabellidae: Anamobaea sp.) in the Caribbean. Diversity 2022, 14, 332. [Google Scholar] [CrossRef]
  58. Capa, M.; López, E. Sabellidae (Annelida: Polychaeta) living in blocks of dead coral in the Coiba National Park, Panamá. J. Mar. Biol. Assoc. UK 2004, 84, 63–72. [Google Scholar] [CrossRef]
  59. Capa, M.; Murray, A. A taxonomic guide to the fanworms (Sabellidae, Annelida) of Lizard Island, Great Barrier Reef, Australia, including new species and new records. Zootaxa 2015, 4019, 98–167. [Google Scholar] [CrossRef] [PubMed]
  60. Tovar-Hernández, M.A.; ten Hove, H.A.; Vinn, O.; Zatoń, M.; de León-González, J.A.; García-Garza, M.E. Fan worms (Annelida: Sabellidae) from Indonesia collected by the Snellius II Expedition (1984) with descriptions of three new species and tube microstructure. PeerJ 2020, 8, e9692. [Google Scholar] [CrossRef] [PubMed]
  61. Capa, M.; Kupriyanova, E.; Nogueira, J.M.d.M.; Bick, A.; Tovar-Hernández, M.A. Fanworms: Yesterday, today and tomorrow. Diversity 2021, 13, 130. [Google Scholar] [CrossRef]
  62. Veeraiyan, B.; Tovar-Hernández, M.A.; Palanivel, P.S.; Palanisamy, S.; Perumal, M. New records of sclerozoan fan worms in Acropora sp. from the Gulf of Mannar, south-eastern coast of India (Annelida: Sabellidae). J. Nat. Hist. 2022, 56, 1365–1381. [Google Scholar] [CrossRef]
  63. Nishi, E. Serpulid polychaetes associated with living and dead corals at Okinawa Island, Southwest Japan. Publ. Seto Mar. Biol. Lab. 1996, 36, 305–318. [Google Scholar] [CrossRef]
  64. ten Hove, H.A.; Kupriyanova, E.K. Taxonomy of Serpulidae (Annelida, Polychaeta): The state of affairs. Zootaxa 2009, 2036, 1–126. [Google Scholar] [CrossRef]
  65. Kupriyanova, E.; ten Hove, H.A.; Rouse, G.W. Phylogeny of Serpulidae (Annelida, Polychaeta) inferred from morphology and DNA sequences, with a new classification. Diversity 2023, 15, 398. [Google Scholar] [CrossRef]
  66. Humann, P.; Deloach, N. Reef Creature Identification: Tropical Pacific, 1st ed.; New World Publications: Jacksonville, FL, USA, 2017; pp. 1–497. [Google Scholar]
  67. Perry, O.; Bronstein, O.; Simon-Blecher, N.; Atkins, A.; Kupriyanova, E.; ten Hove, H.; Levy, O.; Fine, M. On the genus Spirobranchus (Annelida, Serpulidae) from the northern Red Sea, and a description of a new species. Invertebr. Syst. 2018, 32, 605–626. [Google Scholar] [CrossRef]
  68. Kupriyanova, E.K.; Flaxman, B.; Burghardt, I. A puzzle no more: The identity of Spirobranchus tetraceros (Schmarda, 1861) (Annelida, Serpulidae) is revealed. Rec. Aust. Mus. 2022, 74, 201–214. [Google Scholar] [CrossRef]
  69. Hoeksema, B.W.; Wels, D.; van der Schoot, R.J.; ten Hove, H.A. Coral injuries caused by Spirobranchus opercula with and without epibiotic turf algae at Curaçao. Mar. Biol. 2019, 166, 60. [Google Scholar] [CrossRef]
  70. Azzini, F.; Calcinai, B.; Cerrano, C.; Bavestrello, G.; Pansini, M. Sponges of the marine karst lakes and of the coast of the islands of Ha Long Bay (North Vietnam). In Porifera Research: Biodiversity, Innovation and Sustainability; Série Livros 28; Custodia, M.R., Lobo-Hajdu, G., Hajdu, E., Muricy, G., Eds.; Museu Nacional: Rio de Janeiro, Brazil, 2007; pp. 157–164. [Google Scholar]
  71. Becking, L.E.; Cleary, D.F.R.; de Voogd, N.J. Sponge species composition, abundance, and cover in marine lakes and coastal mangroves in Berau, Indonesia. Mar. Ecol. Prog. Ser. 2013, 481, 105–120. [Google Scholar] [CrossRef]
  72. Ward, P.; Risk, M.J. Boring pattern of the sponge Cliona vermifera in the coral Montastrea annularis. J. Paleontol. 1977, 51, 520–526. [Google Scholar]
  73. Schönberg, C.H.L.; Wilkinson, C.R. Induced colonization of corals by a clionid bioeroding sponge. Coral Reefs 2001, 20, 69–76. [Google Scholar] [CrossRef]
  74. de Bakker, D.M.; Webb, A.E.; van den Bogaart, L.A.; van Heuven, S.M.A.C.; Meesters, E.H.; van Duyl, F.C. Quantification of chemical and mechanical bioerosion rates of six Caribbean excavating sponge species found on the coral reefs of Curaçao. PLoS ONE 2018, 13, e0197824. [Google Scholar] [CrossRef] [PubMed]
  75. Adhavan, D.; Prakash, S.; Kumar, A. Tube dwelling gastropod an indicator of coral reef status at the tropical reef of Palk Bay region, southeast coast of India. Ind. J. Geo Mar. Sci. 2021, 50, 585–587. [Google Scholar]
  76. Hoeksema, B.W.; Harper, C.E.; Langdon-Down, S.J.; van der Schoot, R.J.; Smith-Moorhouse, A.; Spaargaren, R.; Timmerman, R.F. Host range of the coral-associated worm snail Petaloconchus sp. (Gastropoda: Vermetidae), a newly discovered cryptogenic pest species in the southern Caribbean. Diversity 2022, 14, 196. [Google Scholar] [CrossRef]
  77. Bieler, R.; Collins, T.M.; Golding, R.; Granados-Cifuentes, C.; Healy, J.M.; Rawlings, T.A.; Sierwald, P. Replacing mechanical protection with colorful faces twice: Parallel evolution of the non-operculate marine worm-snail genera Thylacodes (Guettard, 1770) and Cayo n. gen. (Gastropoda: Vermetidae). PeerJ 2023, 11, e15854. [Google Scholar] [CrossRef]
  78. Chan, B.K.K.; Wong, K.J.H.; Cheng, Y.R. Biogeography and host usage of coral-associated crustaceans: Barnacles, copepods, and gall crabs as model organisms. In The Natural History of the Crustacea: Evolution and Biogeography of the Crustacea; Thiel, M., Poore, G.C., Eds.; Oxford University Press: Oxford, UK, 2020; Volume 8, pp. 183–215. [Google Scholar]
  79. Vimercati, S.; Terraneo, T.I.; Marchese, F.; Eweida, A.A.; Rodrigue, M.; Pieribone, V.; Benzoni, F. Diversity and distribution of coral gall crabs associated with Red Sea mesophotic corals. Front. Mar. Sci. 2024, 11, 1305396. [Google Scholar] [CrossRef]
  80. Purwanto, M.; Wilson, J.; Ardiwijaya, R.; Mangubhai, S. Coral Reef Monitoring in Kofiau and Boo Islands Marine Protected Area, Raja Ampat, West Papua, 2009–2011; Report 6/12; The Nature Conservancy, Indo-Pacific Division: Jakarta, Indonesia, 2012; pp. xiii, 43. [Google Scholar]
  81. Nugraha, A.P.; Purba, N.P.; Sunarto, J. Ocean currents, temperature, and salinity at Raja Ampat islands and the boundaries seas. World Sci. News 2018, 110, 197–209. [Google Scholar]
  82. Patty, S.I.; Rizqi, M.P.; Huwae, R.; Kainama, F. Water quality status of Raja Ampat Island Natural Marine Reserve based on the seawater physical parameters. Jurnal Ilmiah PLATAX 2020, 8, 95–101. [Google Scholar] [CrossRef]
Diversity 16 00295 g001
Figure 1. (a) Locations of 12 marine lakes with coral communities in Raja Ampat, Indonesia. (b–d) Aerial images of marine lakes: (b) Papua24, (c) Papua06, and (d) Papua25. See Table 1 for location codes (Photo credits: Christiaan de Leeuw).
Figure 1. (a) Locations of 12 marine lakes with coral communities in Raja Ampat, Indonesia. (b–d) Aerial images of marine lakes: (b) Papua24, (c) Papua06, and (d) Papua25. See Table 1 for location codes (Photo credits: Christiaan de Leeuw).
Diversity 16 00295 g001
Diversity 16 00295 g002
Figure 2. Impressions of coral cover and coral formations at shallow depths in marine lakes: (a) corals growing among and on mangrove roots; (b) foliose and vase-shaped corals as habitats for butterflyfishes in shallow water; (c) encrusting merulinid coral with the grey encrusting sponge Lamellodysidea herbacea and the green macroalga Halimeda sp.; (d) pillar reef formations of Galaxea.
Figure 2. Impressions of coral cover and coral formations at shallow depths in marine lakes: (a) corals growing among and on mangrove roots; (b) foliose and vase-shaped corals as habitats for butterflyfishes in shallow water; (c) encrusting merulinid coral with the grey encrusting sponge Lamellodysidea herbacea and the green macroalga Halimeda sp.; (d) pillar reef formations of Galaxea.
Diversity 16 00295 g002
Diversity 16 00295 g003
Figure 3. Impressions of coral cover and coral formations on upper reef slopes of marine lakes: (a) massive merulinid coral colonies and an encrusting Porites overtopped by a free-living mushroom coral, Danafungia scruposa (arrow); (b) encrusting and massive coral colonies; (c) foliose colonies of an unidentified Montipora species; (d) foliose colonies of an unidentified Montipora species next to a patch of Pavona cactus.
Figure 3. Impressions of coral cover and coral formations on upper reef slopes of marine lakes: (a) massive merulinid coral colonies and an encrusting Porites overtopped by a free-living mushroom coral, Danafungia scruposa (arrow); (b) encrusting and massive coral colonies; (c) foliose colonies of an unidentified Montipora species; (d) foliose colonies of an unidentified Montipora species next to a patch of Pavona cactus.
Diversity 16 00295 g003
Diversity 16 00295 g004
Figure 4. Selection of stony coral species observed in marine lakes: (a) Acropora cf. rudis, (b) Montipora sp., (c) Pavona decussata, (d) Coeloseris mayeri, (e) Galaxea astreata, (f) Heliofungia actiniformis, (g) Lobophyllia sp., and (h) Pectinia paeonia.
Figure 4. Selection of stony coral species observed in marine lakes: (a) Acropora cf. rudis, (b) Montipora sp., (c) Pavona decussata, (d) Coeloseris mayeri, (e) Galaxea astreata, (f) Heliofungia actiniformis, (g) Lobophyllia sp., and (h) Pectinia paeonia.
Diversity 16 00295 g004
Diversity 16 00295 g005
Figure 5. Selection of stony coral species observed in marine lakes (continued): (a) Dipsastraea sp., (b) Echinopora sp., (c) Goniastrea sp., (d), Millepora tenera, (e) Pachyseris speciosa, (f) Plerogyra sinuosa, (g) Porites cylindrica, and (h) Porites rus.
Figure 5. Selection of stony coral species observed in marine lakes (continued): (a) Dipsastraea sp., (b) Echinopora sp., (c) Goniastrea sp., (d), Millepora tenera, (e) Pachyseris speciosa, (f) Plerogyra sinuosa, (g) Porites cylindrica, and (h) Porites rus.
Diversity 16 00295 g005
Diversity 16 00295 g006
Figure 6. Coral-associated mytilid bivalves: (a) single specimen of Septifer bilocularis settled in between two merulinid corals; (b,c) clusters of S. bilocularis settled inside crevices and patches of dead surface areas of scleractinian corals; (d) characteristic orifices (arrows) of boring mussels (Leiosolenes sp.) in a massive Porites colony.
Figure 6. Coral-associated mytilid bivalves: (a) single specimen of Septifer bilocularis settled in between two merulinid corals; (b,c) clusters of S. bilocularis settled inside crevices and patches of dead surface areas of scleractinian corals; (d) characteristic orifices (arrows) of boring mussels (Leiosolenes sp.) in a massive Porites colony.
Diversity 16 00295 g006
Diversity 16 00295 g007
Figure 7. Coral-associated tube worms. Sabellidae: (a) Acromegalomma sp. (red arrow); (b,c) colour varieties of Sabelastarte sp. (possibly S. spectabilis) in massive Porites colonies (yellow arrows). Serpulidae: Floriprotis sabiuraensis with (d,e) tubes almost entirely implanted in a Dipsastraea host coral (yellow arrows), both with extended arioles (d) and retracted (e), and another one (f) showing its tube partially embedded and its ariole partially retracted; (g) tube of an unknown serpulid, possibly Spirobranchus sp.
Figure 7. Coral-associated tube worms. Sabellidae: (a) Acromegalomma sp. (red arrow); (b,c) colour varieties of Sabelastarte sp. (possibly S. spectabilis) in massive Porites colonies (yellow arrows). Serpulidae: Floriprotis sabiuraensis with (d,e) tubes almost entirely implanted in a Dipsastraea host coral (yellow arrows), both with extended arioles (d) and retracted (e), and another one (f) showing its tube partially embedded and its ariole partially retracted; (g) tube of an unknown serpulid, possibly Spirobranchus sp.
Diversity 16 00295 g007
Table 1. Environmental characteristics of 12 marine lakes with hard coral fauna in Raja Ampat, Indonesia. Code names for marine lakes follow those of earlier studies [21,22,23]. Averages (and ranges in brackets) of temperature, salinity, and pH are based on five sites within each marine lake. Measurements were made at 1 m intervals in the depth range that the corals were observed (1–5 m). n.a. = not available.
Table 1. Environmental characteristics of 12 marine lakes with hard coral fauna in Raja Ampat, Indonesia. Code names for marine lakes follow those of earlier studies [21,22,23]. Averages (and ranges in brackets) of temperature, salinity, and pH are based on five sites within each marine lake. Measurements were made at 1 m intervals in the depth range that the corals were observed (1–5 m). n.a. = not available.
Marine Lake CodeTemperature (°C)Salinity (ppt)pHSurface Area (m2)Maximum Depth (m)Mangrove Presence
Papua0631.9 (30.8–32.5)28.3 (26.7–29.1)7.9 (7.9–8.0)295012No
Papua1130.7 (30.1–31.0)27.6 (26.4–29)8.1 (8.0–8.1)27,3009Yes
Papua1231.2 (30.2–31.8)32.7 (32.6–32.8)n.a.716012Yes
Papua1330.6 (29.0–31.3)32.8 (32.7–32.9)n.a.21003.5Yes
Papua1530.6 (30.3–31.2)30.1 (29.1–30.4)8.1 (8.0–8.1)10,30034Yes
Papua1631.2 (31.1–31.6)30.0 (29.5–30.1)8.1 (8.0–8.1)21,10019No
Papua1731.7 (31.1–32.0)n.a.n.a.6500n.a.Yes
Papua1831.5 (29.9–32.6)28.4 (27.2–29.1)7.7 (7.6–7.8)70004.5Yes
Papua2430.3 (30.0–31.1)30.7 (30–31.1)7.9 (7.8–7.9)42006No
Papua2531.7 (31.1–32.1)29.6 (27.2–30)7.8 (7.7–7.8)21,5008.5Yes
Papua2630.6 (30.0–31.5)29.7 (29.1–30.2)8.1 (8.0–8.1)167004.5Yes
Papua3330.4 (30.0–30.6)33.0 (32.8–33.2)n.a.11,70027No
Table 2. Coral taxa (Scleractinia and Milleporidae) observed in 12 marine lakes of Raja Ampat, Indonesia (Figure 1).
Table 2. Coral taxa (Scleractinia and Milleporidae) observed in 12 marine lakes of Raja Ampat, Indonesia (Figure 1).
FamilySpecies
AcroporidaeAcropora cf. rudis, Montipora spp. (2×)
AgariciidaeGardineroseris planulata, Pavona cactus, P. decussata
EuphylliidaeCoeloseris mayeri, Euphyllia glabrescens, Galexea astreata
FungiidaeDanafungia scruposa, Fungia fungites, Heliofungia actiniformis, Lithophyllon repanda
LeptastreidaeLeptastrea sp.
LobophylliidaeLobophyllia sp.
MerulinidaeCyphastrea sp., Dipsastraea spp. (2×), D. rotumana, D. speciosa, Echinopora sp., Favites spp. (2×), Goniastrea sp., Hydnophora rigida, Leptoria phrygia, Oulophyllia crispa, Pectinia paeonia
MilleporidaeMillepora tenera
PachyseridaePachyseris speciosa
PlerogyridaePlerogyra sinuosa
PocilloporidaePocillopora damicornis, Seriatopora hystrix, Stylophora pistillata
PoritidaePorites sp., P. cylindrica, P. rus
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Becking, L.E.; Martinez, S.J.; Aji, L.P.; Ahmad, A.; Alzate, A.; Folkers, M.; Lestari, D.F.; Subhan, B.; Hoeksema, B.W. Stony Corals and Their Associated Fauna Residing in Marine Lakes under Extreme Environmental Conditions. Diversity 2024, 16, 295. https://doi.org/10.3390/d16050295

AMA Style

Becking LE, Martinez SJ, Aji LP, Ahmad A, Alzate A, Folkers M, Lestari DF, Subhan B, Hoeksema BW. Stony Corals and Their Associated Fauna Residing in Marine Lakes under Extreme Environmental Conditions. Diversity. 2024; 16(5):295. https://doi.org/10.3390/d16050295

Chicago/Turabian Style

Becking, Leontine E., Stephanie J. Martinez, Ludi Parwadani Aji, Awaludinnoer Ahmad, Adriana Alzate, Mainah Folkers, Dea Fauzia Lestari, Beginer Subhan, and Bert W. Hoeksema. 2024. "Stony Corals and Their Associated Fauna Residing in Marine Lakes under Extreme Environmental Conditions" Diversity 16, no. 5: 295. https://doi.org/10.3390/d16050295

APA Style

Becking, L. E., Martinez, S. J., Aji, L. P., Ahmad, A., Alzate, A., Folkers, M., Lestari, D. F., Subhan, B., & Hoeksema, B. W. (2024). Stony Corals and Their Associated Fauna Residing in Marine Lakes under Extreme Environmental Conditions. Diversity, 16(5), 295. https://doi.org/10.3390/d16050295

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop