Contributions to Zoology, 81 (4) 199-221 (2012)

Evolutionary trends in onshore-offshore distribution patterns of mushroom (: )

Bert W. Hoeksema1, 2 1 Department of Marine Zoology, Naturalis Biodiversity Center, P.O. Box 9517, 2300 RA Leiden, The Netherlands 2 E-mail: [email protected]

Key words: competitive exclusion, ecophylogenetics, environmental gradients, habitat partitioning, niche differen- tiation, phylogenetic ecology

Abstract Species co-occurrences based on abundance and incidence data ...... 209 A phylogenetically based comparative analysis of onshore-off- Ordination of species co-occurrences ...... 209 shore distribution patterns of mushroom coral species (Sclerac- Discussion ...... 214 tinia: Fungiidae) was made to reconstruct an evolutionary sce- Onshore-offshore patterns ...... 214 nario for differentiation in fungiid shelf habitats. This phylo- Spatial partitioning and co-existence ...... 214 ecological study integrates data on fungiid distribution patterns Phylogenetic ecology ...... 215 along environmental gradients on the Spermonde Shelf, SW Acknowledgements ...... 217 Sulawesi, with a recently published phylogeny reconstruction of References ...... 217 the Fungiidae. A mushroom coral fauna of 34 species was used to compare their distributions by use of 50-m2 belt quadrats in transects (1) from the mainland to the shelf edge, (2) around reefs with regard to predominant wind directions, and (3) over Introduction bathymetrical reef zones. Species association ordinations were made for each of the four shelf zones using both abundance and Most studies on biotic changes of marine faunas along incidence data to examine whether closely related species co- onshore-offshore gradients concern the evolution and occurred. Some closely related species or even sister species extinction of taxa as represented in the fossil record. appeared to show very similar distribution patterns and to co- exist in high abundances. These results indicate that there may The general scenario is that marine faunas in the Phan- not be community saturation and competitive exclusion among erozoic originated in shallow coastal seas and expanded mushroom species, most of which are free-living. In re- from there into deep offshore ecosystems, but also that constructions of fungiid habitat evolution, offshore reef slopes some of the younger lineages may have originated in appear to be original (ancestral), whereas onshore habitats, less stable nearshore environments (Jablonski and Val- shallow reef flats, and deep sandy reef bases seem to be derived. The latter is in contrast with an earlier hypothesis, in which entine, 1981; Jablonski et al., 1983; Valentine and Ja­ deep sandy substrates were considered ancestral mushroom blonski, 1983; Jablonski and Bottjer, 1988, 1990; Sepko- coral habitats. ski, 1991; Jacobs and Lindberg, 1998). With an increas- ing availability of phylogeny reconstructions based on molecular methods it is also possible to use recent taxa Contents in studies on evolutionary trends in habitat preferences. Only few examples are known from the marine realm. Introduction ...... 199 For instance, Lindner et al. (2008) found that recent sty- Material and methods ...... 201 lasterid corals (Hydrozoa: Stylasteridae), the second Study area ...... 201 largest group of hard corals, evolved mainly in the deep Data sampling ...... 201 Phylogeny reconstruction ...... 202 sea, and invaded shallow waters from there. Evolution of onshore-offshore and bathymetric Studies of onshore-offshore distribution patterns distribution ranges ...... 204 of recent coral reef species usually concern shallow, Species co-occurrences: cluster analyses of tropical shelf seas, with various examples known abundance and incidence data ...... 204 from the Great Barrier Reef (Done, 1982; Williams, Ordination of species co-occurrences ...... 204 Results ...... 205 1982; Dinesen, 1983; Williams and Hatcher, 1983; Onshore-offshore distributions ...... 205 Russ, 1984; Wilkinson and Trott, 1985; Preston and Evolutionary trends in cross-shelf distributions ...... 205 Doherty, 1990, 1994; DeVantier et al., 2006) and the

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Spermonde Archipelago in southwest Sulawesi (Moll, come available, which enabled an evolutionary study 1983; de Beer, 1990; Hoeksema, 1990, 2012; Verheij of their life history traits (Gittenberger et al., 2011) and and Prud’homme van Reine, 1993; Troelstra et al., their associated fauna (Hoeksema et al., 2012). In ad- 1996; de Voogd et al., 1999, 2006; Renema et al., 2001; dition, field data on the cross-shelf bathymetric distri- Cleary et al., 2005; Becking et al., 2006; Cleary and bution patterns of 34 mushroom coral species were de Voogd, 2007; Hoeksema and Crowther, 2011). To obtained on the Spermonde shelf (Hoeksema, 2012). study the evolutionary history of cross-shelf distribu- Use of their phylogenetic relations may help to clarify tion patterns, it would be ideal to use a phylogenetic the evolution of their habitat preferences along envi- ecological model in which detailed information on ronmental gradients, like depth (reflected in reef zona- onshore-offshore distributions can be combined with tion) and increasing distance from the mainland in a a phylogeny reconstruction of a monophyletic species direction from onshore to offshore. group abundantly represented in various shelf habitats. Mushroom corals are suitable for such studies be- A recent molecular phylogenetic study of 50 mush- cause most species have an adult free-living (antho- room coral species (Scleractinia: Fungiidae) has be- cyathus) phase in their life history (Wells, 1966;

o 119 5‘ 10‘ 15‘ 20‘ 25‘ 30‘ 4A

5o 2A

N 4B 3A

1A

2B 5‘ 3B 3C 1B

Tello 2C 1C 1D 100 m 2D MAKASSAR STRAIT 1D Makassar

10‘

Jene Berang

Zone 4Zone3 Zone2 Zone 1 5 km

Fig. 1. The locations of 52 transects around coral reefs in four zones on the central section of the Spermonde Shelf where mushroom coral abundances were measured. The names of the reefs are listed in Table 1. After Hoeksema (2012).

0 10 20

Depth (m) 30 40 o shore o shore onshore 50 60 Zone 4 Zone 3 o shore Zone 2 Zone 1

40 30 20 10 0 Distance o shore (km)

Fig. 2. Schematic cross-section of the central Spermonde Shelf (approximately W-E) from the Makassar Strait to the mainland. After Hoeksema (2012).

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Hoeksema, 1989), which enables them to inhabit vari- itats could indeed have been representative for the ear- ous kinds of substrata, including sandy reef bases liest mushroom corals. (Goreau and Yonge, 1968; Fisk, 1983; Chadwick, 1988; Hoeksema 1988, 2012; Chadwick-Furman and Loya, 1992). Initially, mushroom corals are attached to a Material and methods hard substratum, but individuals of free-living species eventually detach themselves (Yamashiro and Yamaz- Study area ato, 1987a, b, 1996; Hoeksema, 1989; Hoeksema and Yee­min, 2011). About 20% of all mushroom coral spe- Mushroom coral distribution patterns were studied on cies remain attached after settlement on a solid sub- the central part of the Spermonde Shelf, off southwest strate. They belong to the genera Cantharellus (n=3), Sulawesi in the southern Makassar Strait, which bears Cyclo­seris (n=3), (n=2), and Podabacia a large group of cay-crowned reefs and shoals known (n=4) (see Hoeksema, 1989, 1993a, 2009; Benzoni et as the Spermonde Archipelago (Fig. 1). The reefs are al., 2012). arranged in parallel rows in N-S direction, in between Mushroom corals usually occur in mixed multi- the coastline of SW Sulawesi and the outer barrier species assemblages (Pichon, 1974; Claereboudt, 1988; reef, which is situated about 40 km from the mainland Hoeksema and Moka, 1989; Hoeksema 1991b, 2012; in the study area (Hoeksema, 1990, 2012). The shelf Latypov, 2007; Elahi, 2008; Hoeksema and Koh, 2009; can be divided into four zones from the coastline to the Hoeksema and Matthews, 2011). High concentrations westward shelf edge (Figs 1-2). Zone 1 is 5 km wide of mushroom corals can be the result of either sexual where the sea floor reaches a maximum depth of 20 m. or asexual reproduction (Nishihira and Poung-In, Zone 2 ranges 5-12.5 km away from the coastline, 1989; Yamashiro et al., 1989; Krupp et al., 1992; Kra- where the depth of the sea floor varies approximately marsky-Winter and Loya, 1996; Littler et al., 1997; between 20 and 30 m. Zone 3 is 12.5 to 30 km offshore Colley et al. 2002; Gilmour 2002, 2004; Hoeksema, with a sea floor at 30-50 m depth and many submarine 2004; Knittweis et al., 2009a; Hoeksema and Gitten- shoals and some reefs that are crowned by sand cays. berger, 2010; Hoeksema and Waheed, 2011; Hoeksema Zone 4 is the outer rim, which includes the barrier reef, and Yeemin, 2011). Asexual reproduction strategies ranging 30 to 40 km away from the shoreline. To the are applied by various mushroom coral species on the east, the depth reaches 40-50 m, while to the west the Spermonde shelf (Hoeksema, 2012). submarine contours drop immediately to below 100 m. Data on onshore-offshore distribution patterns Some of the reefs on the ridge following the outer shelf within a monophyletic group of sympatrically occur- edge have islets on top of them. ring marine species is rarely available, usually because of identifiation problems. Therefore a taxonomic revi- Data sampling sion of the scleractinian mushroom coral family Fungiidae (Hoeksema, 1989), a recent phylogenetic The survey was conducted in 1984-1986 on 13 reefs analysis (Gittenberger et al., 2011), and a descriptive by snorkeling and SCUBA diving (Hoeksema, 2012). study of their cross-shelf distributions in the Spermon- The abundance data of 34 fungiid species was record- de Archipelago (Hoeksema, 2012), make them ideal as ed around 13 reefs in the four shelf zones (Tables 1-2). a model group for a study on the evolution of distribu- Since the mushroom coral fauna in onshore zone 1 dif- tion patterns along onshore-offshore environmental fered distinctly from those of the other three zones gradients, as reflected in reef zonation (depth) and on- (Table 2; Hoeksema, 2012: Fig. 11), corals observed shore-offshore distribution patterns. in this particular zone were classified as having an Based on their (poorly studied) fossil record, small Onshore (On) range, while those in zones 2-4 were size, simple morphology, and wide geographic range it categorized as Offshore (Off). was assumed that the earliest members of the Fungii- To compare mushroom coral distributions with dae were Cycloseris species, which were known to live wind speed frequencies, transect sites were selected on shallow reefs and on sandy bottoms down to about around each of the 13 reefs, mainly at the N, W, S and 120 m deep (Wells, 1966). Other genera were consid- E side in 565 belt quadrats (50×1 m²) over 52 transects ered as derived. The present study, which is based on (Table 1). If eastward reef sides were generally sandy recent information regarding the phylogeny and ecol- with little coral cover, additional transects at the ESE ogy of the Fungiidae, will examine whether these hab- or SE were selected in shelf zones 2 and 3.

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Table 1. List of 13 reefs in four reef Shelf Reef Transect direction with maximum depth (m) zones on the Spermonde Shelf with the Zone position of 52 transects (Fig 1). In each N NW W SW S SE ESE E transect mushroom coral abundances were recorded in 50-m2 belt transects Zone 1 A. Barang Baringang 6 - 9 - - - 9 - with 3 m depth intervals down to the B. Gusung Trabanusu 9 - 15 - 15 - - 9 maximum depth where mushroom corals C. Lae-Lae Keke - - 12 - - - 9 occurred or where the bottom became D. Lae-Lae - - 12 - 12 - - 9 horizontal. Zone 2 A. Bone Batang 30 - 24 - 24 - 21 24 B. Barang Caddi 24 - 24 - 24 - 21 27 C. Samalona 21 - 24 - 24 - 18 24 D. Bone Baku - - 21 - - - - 18 Zone 3 A. Bone Tambung 36 - 36 - 36 - 36 33 B. Kapodasang - - 33 - - - - 27 C. Kudingareng Keke 30 30 30 33 36 24 24 24 Zone 4 A. Lanyukang 6 - 24 - 15 - - 18 B. Langkai 6 - 18 - 18 - - 30

In each transect, species abundances were meas- sified as such during the fieldwork, i.e., the encrusting ured at various depths. On the reef flats, mushroom species Cycloseris explanulata (van der Horst, 1922), coral inventories were conducted at 3 m depth and at 5, and C. wellsi (Veron and Pichon, 1980). Although their 10, 20 and 50 m distance away from the 3 m isobaths position in the Fungiidae was recognized and correct- in the direction of the reef centre, where the depths ed recently Benzoni et al. (2007, 2012), they could not were ca. 2.5, 2, 1.5 and 1 m, respectively. On reef be included in the present analysis without proper dis- slopes and reef bases, inventories were made at 3 m tribution data. depth intervals, from 6 m deep down to the depth Many of the Spermonde reefs are inhabited by where the bottom became horizontal or no mushroom people and are situated in close proximity of the capi- corals were encountered anymore, which was 39 m tal of South Sulawesi, Makassar, which may have im- deep in the third shelf zone, meaning that depths over pact on the coral populations here (Knittweis et al., 36 m were not included. Northward and southward 2009b; Knittweis and Wolff, 2010; Ferse et al., 2012, reef bases in shelf zone 4 were generally shallow as in press). Since the survey was conducted in 1984- they were based on the barrier, which is mostly cov- 1986, the distributions may have changed over time ered by fine sand on its top. due to human impact (Hoeksema and Koh, 2009; van For each transect, three reef zones were distin- der Meij et al., 2010; Hoeksema et al., 2011). For the guished, i.e., the reef flat, the reef slope and the reef present study such changes are not considered relevant. base (Hoeksema, 2012). The bottom inclination on the reef flats was < 15° and the substratum consisted pre- Phylogeny reconstruction dominantly of coral and rubble, except for the sandy E sides. The bottom inclination of the reef slopes usually The cladogram used as basis for the reconstruction of varied between 15° and 45° and the substratum con- a phylo-ecological scenario involving mushroom cor- sisted mostly of hard coral. Some westward slopes als present in the Spermonde Archipelago has been were partly covered by rubble and most eastward presented by Gittenberger et al. (2011: Fig. 9), for which slopes consisted entirely of sand. At the reef base, the DNA-samples of mushroom corals were collected at inclination was also < 15° and the sea-floor itself con- various Indo-Pacific regions. Soft tissue samples were sisted of sand or silt and contained little coral cover. removed from the corals for amplification of the ITS Descriptions of the recorded species (Table 2) are (Internal Transcribed Spacers I & II) and a part (from given by Hoeksema (1989) and their updated classifi- the 3’-end) of the COI (Cytochrome Oxidase I) re- cation by Gittenberger et al. (2011). Corals that could gions, for which Fungiid DNA-specific COI primers not be identified in situ were collected for further ex- were made. The COI and ITS sequences were aligned amination and were deposited in the collection (RMNH with ClustalW Multiple alignment by use of BioEdit Coel.) of Naturalis. Two fungiid species were present 7.0.1, for which default parameters were used (Hall, in the Spermonde Archipelago but they were not clas- 1999). The COI data set consisted of 63 sequences of

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Table 2. Presence (1) absence (0) data of 34 fungiid species recorded in four parallel shelf zones of the Spermonde Archipelago. The shelf zones were oriented in N-S direction, parallel to the coastline. The onshore-offshore distribution (On-Off) is indicated as well as the predominant reef zonation (F = Flat, S = Slope, B = Base). Numbers of individuals per species are indicated (n) as well as the abun- dance ranking of each species from most common to most rare (1-34).

Species Zone Onshore- Reef n Abundance offshore zone rank

1 2 3 4

01. Ctenactis albitentaculata Hoeksema, 1989 0 1 1 1 -Off - S - 66 27 02. Ctenactis crassa (Dana, 1846) 0 1 1 1 -Off - S - 159 23 03. Ctenactis echinata (Pallas, 1766) 1 1 1 1 On-Off FS - 1509 5 04. Cycloseris costulata (Ortmann, 1889) 1 1 1 1 On-Off - SB 1051 10 05. Cycloseris cyclolites (Lamarck, 1816) 0 1 1 0 -Off - SB 17 31 06. Cycloseris distorta (Michelin, 1842) 0 0 1 0 -Off - S - 1 34 07. Cycloseris fragilis (Alcock, 1893) 0 1 1 1 -Off - SB 424 17 08. Cycloseris mokai (Hoeksema, 1989) 0 1 1 1 --Off - S - 254 21 09. Cycloseris sinensis (Milne Edwards and Haime, 1851) 0 1 1 1 -Off - SB 471 16 10. Cycloseris somervillei (Gardiner, 1909) 0 1 1 1 -Off - - B 38 30 11. Cycloseris tenuis (Dana, 1846) 0 1 1 1 -Off - S - 938 11 12. Cycloseris vaughani (Boschma, 1923) 0 1 1 1 -Off - - B 46 29 13. horrida (Dana, 1846) 1 1 1 1 On-Off FS - 1256 9 14. (Klunzinger, 1879) 1 1 1 1 On-Off FS - 1264 8 15. fungites (Linnaeus, 1758) 1 1 1 1 On-Off FS - 3909 2 16. Halomitra pileus (Linnaeus, 1758) 0 1 1 1 -Off - S - 151 24 17. (Quoy and Gaimard, 1833) 1 1 1 1 On-Off - S - 342 19 18. Heliofungia fralinae (Nemenzo, 1955) 0 1 1 1 -Off - S - 625 13 19. Herpolitha limax (Esper, 1797) 1 1 1 1 On-Off FS - 1398 6 20. Lithophyllon concinna (Verrill, 1864) 1 1 1 1 On-Off FS - 2904 3 21. Lithophyllon repanda (Dana, 1846) 1 1 1 1 On-Off FS - 6588 1 22. Lithophyllon scabra (Döderlein, 1901) 1 1 1 1 On-Off FS - 556 15 23. Lithophyllon spinifer (Claereboudt and Hoeksema, 1987) 0 0 1 0 -Off - SB 2 33 24. Lithophyllon undulatum Rehberg, 1892 0 1 1 1 -Off - S - 148 26 25. Lobactis scutaria (Lamarck, 1801) 0 1 1 1 -Off FS - 363 20 26. granulosa (Klunzinger, 1879) 0 1 1 1 -Off - S - 828 12 27. Pleuractis gravis (Nemenzo, 1955) 0 1 1 1 -Off - S - 254 22 28. Pleuractis moluccensis (Van der Horst, 1919) 1 1 1 1 On-Off - SB 1311 7 29. Pleuractis paumotensis (Stutchbury, 1833) 1 1 1 1 On-Off FS - 1907 4 30. Podabacia crustacea (Pallas, 1766) 1 1 1 1 On-Off - S - 150 25 31. Polyphyllia talpina (Lamarck, 1801) 1 1 1 1 On-Off FS - 421 18 32. Sandalolitha dentata Quelch, 1884 0 1 1 1 -Off - S - 63 28 33. Sandalolitha robusta (Quelch, 1886) 1 1 1 1 On-Off FS - 558 14 34. Zoopilus echinatus Dana, 1846 0 0 1 0 -Off - S - 7 32

500 bases each, not including any gaps or stop codons. cally variable base positions included. The combined The ITS data set consisted of 45 sequences with COI+ITS data set without intraspecific variation re- lengths varying between 604 and 618 bases. The phy- sulted in the lowest number of most parsimonious logenetic analyses were performed on six data sets, i.e. trees, i.e. 36 instead of 791 when intraspecific varia- the COI data set, the ITS data set and the combined tion is included. Therefore the latter was selected as COI+ITS data set, all of which with and without in- basis for the eventual phylogeny reconstruction.To fill traspecifically varying base positions. In all cases the in gaps concerning species not included in the molecu- consistency index of the most parsimonious trees was lar analysis, data from a morphology-based cladogram higher for the data set without the intraspecifically are used, which overall agrees much with the one variable base positions, which resulted in less most based on molecular data (Hoeksema 1989, 1991a; Git- parsimonious trees than the data sets with intraspecifi- tenberger et al., 2011).

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Evolution of onshore-offshore and bathymetric distri- 50-m2 SUs (sample units = belt quadrats) were ana- bution ranges lyzed separately for each of the four shelf zones. For every zone, a data matrix was constructed in which the The onshore-offshore and bathymetric distribution observed species were arranged in columns and the ranges of the mushroom coral species were projected SUs containing fungiids in rows. The data of the four onto a cladogram (phylogeny reconstruction) to ex- shelf zones were analyzed separately because the plore how frequently invasion of a particular habitat by zones differ in the number and composition of species a species may have resulted from either 1) synapomor- and in the number of SUs. An overall analysis of the phy in a common lineage or 2) homoplasy (conver- shelf would be biased by the dominance of the zone gence), and also 3) whether there were reversals in with the highest number of SUs. Moreover, separate ecological traits (cf. Hoeksema, 1991a; Gittenberger et analyses enable interzonal comparisons of the inter- al., 2011). Each species was assigned a cross-shelf and specific affinities. a reef zonation distribution type, as follows: The R-mode analyses of the ecological species af- Cross-Shelf zonation: Onshore-offshore (On-Off) finities are performed with SPASSOC (Ludwig and as derived from the commonly inherited Offshore Reynolds, 1988), which gives a variance ratio test VR (Off) only. Onshore (On) only was not observed. for each analysis, which suggests positive overall as- Reef zonation: Flat - Slope (FS), Slope - Base (SB), sociation when VR > 1 and negative net association or Base only (B) as derived from the commonly inher- when VR < 1. An accompanying test statistic W de- ited Slope (S). notes whether deviations from 1 are significant (Schlu­ These characters were projected onto the clad- ter, 1984). Furthermore, the analysis indicates whether ogram of Gittenberger et al. (2011: Fig. 9), which dif- the association is positive or negative per species pair ferentiates between lineages with and without molecu- and a chi-square statistic is given, which highlights lar support. When an entire clade is restricted to a bias caused by a too low species representation. The particular ecological zone (cross-shelf or bathymetric), chi-square is computed from a pair-wise species 2×2 it may be assumed that it originated within that zone contingency table, which is considered biased when (Davis et al., 2005; Ricklefs, 2006). any cell in the table has an expected frequency < 1 or if more than two of the cells have expected frequencies Species co-occurrences: cluster analyses of abun- < 5 (Zar, 1974: 49). In case of a biased chi-quadrat dance and incidence data value the Yates correction factor for continuity was employed. SPASSOC supplies three interspecific co- Multivariate analyses of both abundance and presence/ occurrence coefficients which serve as measures for absence data of mushroom coral species were con- ducted to determine the extent of their co-occurrences the degree of association. In the present study Ochiai’s in the belt quadrats for each of the four shelf zones (1957) index, IO, was selected because, compared to using the Plymouth Routines in Multivariate Ecologi- other indices it is little affected by the frequency of cal Research (PRIMER) version 6 software (Clarke occurrence (Jackson et al., 1989), making interzonal and Warwick, 2001; Clarke and Gorley, 2006). Group- comparisons of species associations more reliable. averaged hierarchical clustering dendograms were Only significant associations, i.e. those with (cor- generated from Bray-Curtis resemblance matrices to rected) chi-quadrats > 3.84, were admitted to the anal- show the degree of species co-existence. The Bray- yses. The IO-values representing positive and negative Curtis similarity measure was used with regard to spe- associations were arranged as symbols in trellis dia- cies abundance data (square root transformed) and in- grams (Green, 1979). Species names listed in the upper cidence data (presence/absence). In the latter case the right triangle have been reordered in the lower left tri- Bray-Curtis similarity index is equivalent to the So- angle to achieve the greatest possible number of high renson similarity index (Clarke and Gorley, 2006). similarity values nearest to the principal diagonal Similarity profiles (SIMPROF) were derived from the (McIntosh, 1978; Legendre and Legendre, 1983). Since dendogram to show significant groupings of the sites. each species is arranged next to its closest associates, the concentrations of high associations close to the Ordination of species co-occurrences diagonal resemble clusters. Arranged thus, the sum of the products of each IO-value by its distance to the To study to what degree mushroom coral species co- diagonal (measured by the numbers of intermediate existed, the presence-absence data of the species in the columns and rows) should be minimal. This can be

Downloaded from Brill.com10/04/2021 01:37:58PM via free access Contributions to Zoology, 81 (4) – 2012 205 accomplished by manual pair-wise switching of rows the 34 fungiid species recorded in the belt quadrats, 19 and columns of two species that have neighbouring were not recorded in zone 1 and were therefore catego- positions, which has to be continued in each newly re- rized as species with a predominantly offshore distri- ordered matrix. Eventually, convergence is obtained bution (Off), whereas 15 that were also present in zone when for each species pair the column-row combina- 1 were categorized as having an onshore-offshore tion closest to the principal diagonal has the highest range (On-Off). Likewise, with regard to their bathym- total of IO-values. etric distributions (Hoeksema, 2012), the zonation pat- terns of the 34 species (see Table 2) were classified by their occurrence in the reef zones “flat” (F), “slope” Results (S), and “base” (B), as FS (n=12), S (n=14), SB (n=6), or B (n=2). Apparently there were no species with F or Onshore-offshore distributions FSB ranges. Furthermore, the total numbers of speci- mens per species and, consequently, their order of Mushroom corals were abundant in multi species as- abundance are indicated, with for instance Lithophyl- semblages (>500 individuals per 50-m2 belt quadrat) in lon repanda, Fungia fungites, L. concinna, Pleuractis shelf zones 1-3, whereas the highest number counted paumotensis, and Ctenactis echinata ranking as the in zone 4 was only 195 (Hoeksema, 2012). Hence, five most common species, respectively (Table 2). proximity to the mainland and river outlets per se did not limit overall mushroom coral abundance. The Evolutionary trends in cross-shelf distributions highest mushroom coral concentrations were observed in W, N, NW, and SW transects, at the sides most By plotting the onshore-offshore distribution ranges strongly exposed to winds from the west, whereas indicated in Table 2 on the phylogenetic model pre- fungiids were absent from several transects on east- sented by Gittenberger et al. (2011) a scenario can be ward reef slopes (E or ESE) with a sand cay nearby, reconstructed in which evolutionary trends can be dis- from where sand can easily be transported over the cerned (Fig. 3). Since all mushroom coral species on reef flat (Hoeksema, 2012). In contrast, submerged the Spermonde shelf had an offshore component, it is reefs and reefs with breakwaters on their top had high assumed that the common ancestor of the Fungiidae mushroom densities in their eastward transects. Fungi- also occurred offshore (cf. Davis et al., 2005; Ricklefs, ids were absent from wide, wave-exposed westward 2006). Offshore habitats remote from terrigenous im- reef flats in shelf zone 4, where storm-driven waves pact are common on oceanic reefs and have always may prevent coral settlement. remained available during sea level fluctuations. In 12 Reefs in zone 3 had the greatest vertical ranges of species lineages (represented by 15 species) an on- mushroom coral presence, up to 36 m depth (Table 1). shore component was found (Fig. 3). This indicates For the shallower-based reefs in shelf zones 2 and 1, that an onshore-offshore shelf range (with a compo- mushroom corals extended down to 27 m and 15 m nent of terrigenous impact) appeared to have evolved depth respectively. The sea floor in zone 1 (15 m) con- 12 times from a predominant offshore distribution sisted of fine silt (without any life cover) and mush- only. Herpolitha limax, Lithophyllon scabra, and room corals were only observed down the reef slope to Pleuractis paumotensis were the only species showing 12 m depth. On zone 4 reefs, fungiids were often rela- their highest concentrations in shelf zone 1 (Hoekse- tively sparse, probably because many of the reefs sit on ma, 2012). Of these, L. scabra was the least abundant top of a sandy bank (the barrier), but they extend deep- on the most offshore reefs in shelf zone 4, while it was est on the reefs of the western margin where the bot- a dominant species in some reef zones in shelf zone 1. tom merges into the Makassar Strait drop-off. Nearly all mushroom coral species on the Sper- Based on detailed results presented earlier (Hoek- monde shelf inhabited reef slopes or had sister species sema, 2012) distinction among species can be made (phylogenetically most closely related) with a reef with regard to their onshore-offshore distributions by slope distribution. Therefore it is assumed that the their occurrence in the four reef zones (Table 2). Indi- common ancestor of the Fungiidae also inhabited reef viduals of species only counted once in a zone were slopes which, unlike reef flats, remained available dur- considered exceptional and not included, such as sin- ing sea level fluctuations. The bathymetric range of gle specimens of Cycloseris cyclolites, Lithophyllon nine species lineages (involving 10 species) included undulatum and Lobactis scutaria in zone 1. Among reef flats, suggesting that mushroom coral species

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Fig. 3. Cladogram of the Fungiidae based on the phylogeny reconstruction by Gittenberger et al. (2011: Fig. 9). Species lineages repre- sented by solid lines are supported by molecular analysis, while those that are not supported by the molecular analyses or have re- mained uncertain are indicated by a broken line. Cross-shelf distributions (onshore-offshore) and reef zonation distributions (indicated in Table 2) have been superimposed on the cladogram and are based on the sharing of these traits by the species within the species lineages. Their appearance in the phylogeny have been reconstructed accordingly: onshore-offshore (On-Off) as derived from offshore only (Off); reef flat - slope (F-S), reef slope - base (S-B), or reef base only (B) as derived from reef slope only (S).

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Fig. 4. Alternative evolutionary scenarios of cross-shelf distributions when three kinds of reversals are included: retreat from onshore, retreat from reef flats and retreat from reef bases. A. Cycloseris clade is more parsimonious: five reef base colonizations have been reduced to one but two retreats from reef bases have been added. B1-B2. Ctenactis-Herpolitha-Polyphyllia clade shows equal numbers of transformations (total six) if besides extensions to onshore habitats and colonization of reef flats also retreat from onshore reefs and reef flats are added. C. Lobactis-Danafungia-Halomitra-Fungia clade shows equal number of transformations (total four) if retreat from onshore reefs is added and an extension to onshore is not included. D1-D2. Lithophyllon clade shows one supernumerous trans- formation (six instead of five) if retreat from onshore is built-in and therefore this alternative is considered less plausible.

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Fig. 5. Evolutionary scenario of mushroom coral habitats (marked by thick lines covering reefs) based on the Spermonde Shelf as a model area. A. Original situation in which mushroom corals and/or their ancestors inhabited offshore reef slopes, especially exposed ones. B. Present situation in which mushroom corals also inhabit nearshore reefs, shallow reef flats and deep, sandy reef bases. C. Past situations when the sea level was lower than the shelf during glacial periods and corals lived on fringing reefs that were not shelf-based and possibly more oceanic.

ranges in those lineages expanded from reef slopes reef base colonizations have been reduced to one but into reef flats during periods when these flats were two retreats from reef base have been added (Fig. 4A). available (Fig. 3). Many of the most common species The Ctenactis-Herpolitha-Polyphyllia clade shows even showed most of their highest densities in shallow equal numbers of transformations (total six) if besides reef zones: Ctenactis echinata, Fungia fungites, Her- extensions to onshore habitats and colonization of reef politha limax, Lithophyllon concinna, L. repanda, flats also retreats from onshore and reef flats are pos- Pleuractis paumotensis, Polyphyllia talpina, and San- sible, which yields two extra scenarios (Fig. 4A-B). dalolitha robusta (Hoeksema, 2012). On the other The Lobactis-Danafungia-Halomitra-Fungia clade hand, in seven species lineages (involving eight spe- shows equal number of transformations (total four) if cies) reef bases were added to the bathymetrical distri- retreat from onshore is added and one extension to on- bution or even had replaced the reef slope (Fig. 3). The shore is excluded (Fig. 4C). The Lithophyllon clade replacement concerns two separate lineages, each with shows one extra transformation (six instead of five) if one species, i.e., Cycloseris somervillei and C. vaugha- retreat from onshore is built-in; this alternative is con- ni, both of which showed to be restricted to sandy sub- sidered less parsimonious and therefore less likely strates (Hoeksema, 2012). (Fig. 4D). Alternative scenarios concerning the evolution of All possible scenarios combined indicate that cross-shelf distributions can be considered when three mushroom corals initially inhabited offshore reef kinds of reversals are included: retreat from onshore, slopes and most abundantly on exposed ones; see retreat from reef flats and retreat from reef bases (Fig. Hoeksema, 2012; Fig 5A) and from there evolved into 4). The Cycloseris clade is more parsimonious by two onshore habitats and moved into either shallow or deep transformations less by the inclusion of reversals: five reef zones as in the present situation (Fig. 5B). How-

Downloaded from Brill.com10/04/2021 01:37:58PM via free access Contributions to Zoology, 81 (4) – 2012 209 ever, when sealevels were much lower during glacial Overall it is remarkable that some pairs of sister periods, they could only retreat to the steep outward species appear to show very similar cross-shelf distri- reef slope on the barrier (Fig. 5C). bution patterns by grouping closely together, although not significantly, in cluster analyses for most of the four Species co-occurrences based on abundance and in- shelf zones, especially with regard to the species pairs cidence data Danafungia horrida - D. scruposa and Lithophyllon concinna - L. repanda. Other sister species pairs, such Cluster analyses of abundance and incidence data for as Ctenactis albitentaculata – C. echinata, Heliofungia mushroom coral species recorded in zone 1 show re- actiniformis – H. fralinae and Pleuractis moluccensis markable patterns with regard to co-occurrence or dif- – P. paumotensis were consistent by showing dissimilar ferences among closely related species, especially distributions across all four shelf zones. when sister species pairs are indicated, i.e. species that are phylogenetically most closely related (Fig. 6). Ordination of species co-occurrences Pleuractis gravis, Cycloseris cyclolites and Lobactis scutaria were outliers that showed significantly differ- The ordination of co-occurrence among species in trel- ent distribution patterns from the other species be- lis diagrams based on presence-absence data in the belt cause they were rare in zone 1, each represented by a quadrats (SUs) for each shelf zone enables direct com- single specimen only (see Hoeksema, 2012): parisons of all species directly with each other (Fig. 10). Some pairs of sister species showed very similar Samples of sister species pairs are indicated and show distributions patterns, especially the very abundant that within such pairs of very closely related species species Lithophyllon concinna and L. repanda for much overlapping in distribution patterns occurs. both abundance and incidence data and Danafungia On shelf zone 1, 19 species encountered in 69 SUs horrida and D. scruposa for abundance data (Fig. 6). (see Hoeksema, 2012) showed 61 pair-wise combina- These high similarities in species co-existence were tions of significant co-occurrence and three of signifi- not significant. The sister species Pleuractis moluc- cant non-co-occurrence (Table 3, Fig. 10A). The high- censis and P. paumotensis showed significantly differ- est IO-values (IO > 0.80) were found for the species ent patterns. pairs Cycloseris cyclolites - Lobactis scutaria, Litho- The cluster analyses for species in zone 2 did not phyllon repanda - Ctenactis echinata, and Pleuractis show outliers (Fig. 7). Again, Lithophyllon concinna paumotensis - Herpolitha limax. The three species and L. repanda clustered close together, indicating their pairs representing negative associations (non-co-oc- very similar distributions, but not significantly. The sis- currence) were Polyphyllia talpina - Ctenactis echi- ter species Danafungia horrida and D. scruposa clus- nata, P. talpina - Fungia fungites, and P. talpina - tered close together with regard to their incidence data. Lithophyllon concinna, which clustered along the left Other pairs of closely related species did not show much margin in the re-arranged diagram (Fig. 10A). Of significant similarity in their distributions. these, species of the combination Cycloseris cyclolites The cluster analyses for zone 3 showed three rare - Lobactis scutaria were each represented by a single species that acted as outliers: Lithophyllon spinifer, specimen co-occurring in the same SU. They did not Cycloseris cyclolites, and Zoopilus echinatus (Fig. 8). show significant associations with any other species The sister species pairs Lithophyllon concinna - L. and therefore became ordered at the end of the se- repanda and Danafungia horrida - D. scruposa showed quence. Among the sister species pairs Danafungia much resemblance in abundance distributions. All horrida - D. scruposa (IO> 0.60), Lithophyllon con­ four species grouped together with regard to indidence cinna - L. repanda (IO> 0.40), and Pleuractis moluc- data. Other sister species pairs did not show such sim- censis - P. paumotensis (IO> 0.60) there were no high ilarities. IO-values for co-occurrences (Fig. 10A). Zone 4 distribution patterns (Fig. 9) showed one out- On shelf zone 2, 31 fungiid species were encoun- lier among the clusters, i.e. Cycloseris sinensis, which tered in 137 SUs containing Fungiidae (Hoeksema, occurred in a high abundance in a single belt quadrat all 2012). In the analysis, 264 species pairs showed sig- by itself (Hoeksema, 2012). Danafungia horrida and D. nificantly positive associations and five significantly scruposa showed much similarity with regard to both negative ones (Table 3, Fig. 10B). Thirteen species their abundance and incidence distribution data, which pairs involving ten species had IO-values > 0.80. Li­ cannot be said for other sister species pairs. thophyllon repanda and Danafungia scruposa were

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Fig. 6. Dendrogram (group average, Bray Curtis similarity) Fig. 7. As Fig. 6, but for shelf zone 2. showing clustering of mushroom coral species recorded in belt quadrats in shelf zone 1 based on abundance data by square root transformation and incidence data (presence/absence). Bold lines: significant groupings based on similarity profiles (SIM- PROF). Starlike symbols indicate sister species pairs. overall species association proved to be positive and highly significant (Table 3). Some sister species pairs showed high IO-values for co-occurrences: Danafun- gia horrida - D. scruposa (IO> 0.80) and Lithophyllon part of five and four of these pairs, respectively, while concinna - L. repanda (IO> 0.80). The latter became Cycloseris tenuis, Danafungia horrida, Pleuractis re-arranged close to each other in the trellis diagram paumotensis and Herpolitha limax were combined in (Fig. 10B). Other sister species pairs, such as Heliofun- three of such pairs. Fungia fungites was highly associ- gia actiniformis – H. fralinae (IO> 0.40) and Pleurac- ated with two species, whereas Ctenactis echinata, tis moluccensis - P. paumotensis (IO> 0.50) showed Cycloseris costulata, and Lithophyllon concinna were little similarity in their distributions (Fig. 10B). each highly associated with only one other species. Shelf zone 3 had the highest species number, 34 in The five negative associations involved Fungia fun- a total of 162 belt quadrats with fungiids (Hoeksema, gites (2×), Pleuractis moluccensis (2×), Lithophyllon 2012; Table 3). A total of 311 species pairs showed a repanda (1x) and Sandalolitha dentata (1×), which in significant positive association and 48 displayed a sig- the re-arranged trellis diagram appeared in two col- nificant negative association (Fig. 10C). The analysis umns at the left side (Fig. 10B). Each of the species of zone 3 contained 13 species pairs with IO-values > was positively associated with at least one other. The 0.80, involving seven species: Lithophyllon repanda

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Fig. 8. As Fig. 6, but for shelf zone 3. Fig. 9. As Fig. 6, but for shelf zone 4.

(6×), Herpolitha limax (5×), Danafungia scruposa pairs, such as Heliofungia actiniformis – H. fralinae (4×), Pleuractis paumotensis (4×), Lithophyllon con­ (IO> 0.50), showed little similarity in their distribu- cinna (3×), Danafungia horrida (3×) and Fungia fun- tions (Fig. 9-3). The pair Pleuractis moluccensis - P. gites (1×). In the negative associations four species paumotensis showed no significant association. were involved: Cycloseris somervillei (16×), C. vau­ In shelf zone 4, 49 SUs contained fungiids, which ghani (13×), C. fragilis (11×) and C. sinensis (6×). In belonged to 29 species (Table 3); 93 species pairs had the re-arranged diagram, the negative associations significant positive associations, while no significant clustered in the left corner below (Fig. 10C). Due to negative associations occurred (Fig. 10D). Ten species their low abundance, Cycloseris distorta and C. cyclo- pairs showed high IO-values (>0.80), in which seven lites showed no significant association with any other species were involved: Cycloseris somervillei (2×), C. species. The net species association is positive (since fragilis (2×), C. vaughani (2×), Lithophyllon repanda VR > 1) and highly significant (Table 3). (1×), Danafungia horrida (1×), Fungia fungites (1×) and The sister species pairs Danafungia horrida - D. Herpolitha limax. C. sinensis and L. scabra were less scruposa (IO> 0.80) and Lithophyllon concinna - L. common and therefore showed no significant associa- repanda (IO> 0.80) showed high IO-values for co-oc- tions with other species. The overall species association currences, and became re-arranged close to each other was significantly positive (Table 3). The sister species in the trellis diagram (Fig. 10C). Other sister species pairs Danafungia horrida - D. scruposa (IO> 0.70) and

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Fig. 10. Trellis diagrams with IO-values calculated to indicate significant fungiid species associations. Negative associations are indi- cated by a minus sign. For each shelf zone (A= zone 1, B = zone 2, C = zone 3, D = zone 4) a set of two matrices is given: the upper right triangle shows species in alphabetical / taxonomic order (gaps indicate absent species); the lower left one is the rearranged simi- larity matrix with seriated order in species co-occurrences. Star-like symbols indicate sister species pairs.

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Fig. 10. (continued).

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Table 3. Interspecific association of Fungiidae in 50×1 Shelf SUs with Number VR, overall W, test Association m² SUs in each of the four Spermonde shelf zones. The zone fungiids of species association statistic (+ or ) presence absence data of species are compared by R- mode analysis for SUs having at least one species rep- 1 69 19 4.8 329 + resented. When VR, the variance ratio, > 1, there is a 2 137 31 8.4 1153 + possible possitive overall association which proves to 3 162 34 8.8 1424 + be significant when the test statistic W approximates a 4 49 29 7.2 352 + chi-square distribution (Schluter, 1984).

Lithophyllon concinna - L. repanda (IO> 0.50) did not to the reef bases of reefs further offshore (Hoeksema, show highest IO-values for co-occurrences (Fig. 10D). 2012). In zone 1, depths > 15 m do not exist on the reef Other sister species pairs, such as Heliofungia actini- slope because the sea floor surrounding the reefs is formis – H. fralinae and Pleuractis moluccensis - P. relatively shallow (deepest SU at 15 m) and it consists paumotensis showed no significant association at all. of fine sediment deposited by fluvial discharge. There- It is remarkable that among some sister species, fore, species with predominant deep offshore distribu- such as Danafungia horrida with D. scruposa, and tions that prefer oceanic conditions are absent here. Lithophyllon concinna with L. repanda, distributions Similar patterns of onshore-offshore distributions for patterns appear to be very similar, showing much co- particular mushroom coral species were found in occurrence, especially in shelf zones 2 and 3 where northern Papua New Guinea, East Kalimantan and mushroom corals are most abundant. In other sister eastern Sabah (Hoeksema, 1993a; Hoeksema et al., species pairs, the species show very different patterns 2004; Waheed and Hoeksema, 2013). and little co-existence. Species with a more off-shore biased distribution are best represented in zone 3, and to a minor degree in zone 2. Here, the presence or absence of a sand cay Discussion seems to exert an important influence on the fungiid fauna. Shelf zone 4 is less rich in species than zone 3 Onshore-offshore patterns because the reefs in zone 4 sit upon a shallow sand ridge (the barrier), which lacks dense coral cover, ex- Three major environmental gradients are considered cept along some stretches of narrow reef flope (Hoek- important for fungiid distribution patterns on the sema, 2012). Spermonde Shelf (1) reefs varying in distance off- shore, away from terrigenous impact (2) position of Spatial partitioning and co-existence sites around reefs with regard to predominant wind direction, and (3) depth zonation over reef flats, slopes Because many coral species have broad ranges with and bases (Hoeksema, 2012). Substantial environmen- respect to depth distribution and the location of the tal differences may exist across tropical continental reefs they occupy, habitat partitioning is not necessar- shelves with regard to the physiography of coral reefs ily important in the maintenance of coral reef diversity (Hopley, 1982; de Klerk, 1983). Consequently, more (Connell, 1978). With the application of molecular oceanic, peripheral habitats on a shelf differ physically techniques in the of reef corals it has been and biologically from inshore habitats (Done, 1982), discovered that what used to be considered species such differences being considered of considerable rel- may actually consist of species complexes, which may evance to biogeographic and speciation patterns and imply that these ecological ranges are split up and nar- processes (Jablonski and Valentine, 1981; Valentine rower than previously assumed (Knowlton and Jack- and Jablonski, 1983; Potts, 1983, 1984, 1985). son, 1994). In the present analyses of species co-occur- Fungiid faunas on near-shore reefs on the Sper- rences on the Spermonde shelf, most fungiids appear monde shelf (Zone 1) are distinct from the rest (Hoek- to show much overlap regarding their onshore-off- sema, 2012). The fungiids here are not nearshore spe- shore, circum-reef and depth distributions as presented cialists, but rather a subset of species that are widely by Hoeksema (2012). distributed across the shelf (Table 1; Hoeksema, 2012). Among the 34 mushroom coral species encountered For example the predominantly deep-living Cycloseris in belt quadrats, many show much similarity regarding species (rare or absent in zone 1) are mostly restricted their presence and abundance over reef flats, slopes and

Downloaded from Brill.com10/04/2021 01:37:58PM via free access Contributions to Zoology, 81 (4) – 2012 215 bases within transects around reefs across the shelf. For it may be risky for mushroom corals to get into contact a better understanding of niche differentiation and spe- with sedentary organisms that are known to produce cies co-existence it is important to compare distribution toxins, such as sponges (de Voogd et al., 2005). When patterns of phylogenetically closely related species, that happens, they may use their ability to move away, preferably sister species. Although there is in general either by their own force or by wave action (Abe, 1939; much overlap in distribution patterns of closely related Horridge, 1957; Hubbard, 1972; Jokiel and Cowdin, species, their distributions are usually not similar. 1976; Chadwick, 1988; Hoeksema, 1988; Chadwick- Therefore, the co-existence of sister species show- Furman and Loya, 1992; Yamashiro and Nishira, ing very similar distribution patterns in high densities is 1995; Hoeksema and de Voogd, 2012). exceptional, like Lithophyllon concinna with L. repan- da, and Danafungia horrida with D. scruposa. These Phylogenetic ecology are typical examples of niche conservatism (sensu Wiens and Graham, 2005; Holland and Zaffos, 2011; When historical, causal explanations are sought in Mouquet et al., 2012), in which sister species share sim- biological comparisons, a phylogenetic foundation is ilar habitat traits that did not change during and after essential (Bock, 1989), especially since adaptations speciation. The co-existence of similar species is not of an organism to its environment may be limited by unique though and various ecological explanations have phylogenetic constraints (Gans, 1989; McKitrick, 1993). been suggested (Scheffer and van Nes, 2006). Because of their independence from morphological The four mushroom species in question have wide- character state transformations, molecular phylogeny ly overlapping Indo-West Pacific geographic ranges reconstructions are ideal to detect evolutionary trends and a fossil records that can be traced back to either in morphology, life history traits, and associated fau- the Miocene or Pliocene (Hoeksema, 1989). Because na of corals (Gittenberger et al., 2011; Hoeksema et of their ecological similarities, there is no clear indica- al., 2012). In the present study they are applied to de- tion for sympatric speciation and if they originated by tect evolutionary causes for species distributions and allopatric speciation, it is unclear where and how that abundances. process started. Furthermore, with regard to their as- In evolutionary ecology, historical causes are sought sociated fauna, only both Danafungia species show a behind ecological adaptations when the autoecologies clear difference, i.e., the presence of dissimilar endo­ of species in a community are compared (Orians, 1962; symbiotic Leptoconchus snails (Gittenberger and Git- Lack, 1965). However, evolutionary ecology is not nec- tenberger, 2011; Hoeksema et al., 2011). Spatial parti- essarily restricted to comparisons within monophyletic tioning may not have occurred among mushroom cor- groups because it does not take phylogeny reconstruc- als if there was sufficient geographic and ecological tions into account. Hence, for comparative historical space to expand into, especially in the case of free- ecological studies with a phylogenetic approach the living species. term ‘phylogenetic ecology’ is used (Hoeksema, 1990; The range overlaps shown by the co-occurrence Westoby, 2006), which can also be referred to as ‘phylo- analyses reflect what also can be seen in dense mixed ecology’ or ‘ecophylogenetics’. This approach is gain- mushroom coral assemblages in situ, with specimens ing support in community ecology, which implies aban- of various species literally being piled on top of each doning localized concepts of communities and adopting other (Littler et al., 1997; Hoeksema and Matthews, a historical perspective with respect to the evolution of 2010; Hoeksema, 2012). There appears to be no visible diversity within larger regions (Losos, 1996; Ricklefs, effect of community saturation or competitive exclu- 1996, 2006; Schluter et al., 1997; Webb et al., 2002; sion, especially because of the ability of many free- Johnson and Stinchcombe, 2007; Cavender-Bares et al., living mushroom coral species to occupy different 2009; Mouquet et al., 2012). kinds of substrates and to escape burial in sand The present evolution models of cross-shelf distri- (Schuhmacher, 1977, 1979; Bongaerts et al., 2012). butions and depth ranges in the Fungiidae (Figs 3-4) Furthermore, mushroom corals are known to be ag- suggest that their ancestral species occurred on off- gressive towards other corals (Sheppard 1979, 1981; shore reef slopes, which is plausible because they con- Cope, 1981; Thomason and Brown, 1986; Hildemann stitute the most diverse habitat for many coral species et al., 1975a, b; Chadwick-Furman and Loya, 1992; on the Spermonde Shelf (Moll, 1983; Hoeksema, Jokiel and Bigger, 1994; Abelson and Loya, 1999), but 2012). The ancestor of the Fungiidae was probably an they appear not to harm each other. On the other hand, Acrosmilia-like scleractinian, which in overall shape

Downloaded from Brill.com10/04/2021 01:37:58PM via free access 216 Hoeksema – Evolution of cross-shelf mushroom coral distributions resembled the attached anthocaulus-stage of the Fungii- wave action and temperature fluctuations.Fungia fun- dae (Wells, 1966). From this coral, displaying a seden- gites is able to reach high densities here and may be tary turbinate shape and a vertical corallum wall, best adapted to live in shallow reef habitats. In order to evolved a free-living coral with a more horizontal wall achieve this shallow depth range, the planula larvae by the broadening of the oral surface and the develop- have to settle in shallower depth zones. During periods ment of the detachment process (see Yamashiro and of transgression this could have been an advantage for Yamazato 1987a, b, 1996; Hoeksema and Yeemin, species that needed to keep pace with the rising sea- 2012). This evolutionary sequence resembles the suc- level. New species may even have evolved along the cession in the first post-settlement stages of the fungiid outward side of shelves (Fig. 5C) or around oceanic life cycle (Wells, 1966; Hoeksema, 1989). Little is islands that became isolated during transgressions known about the ecology of Acrosmilia corals but be- (Potts, 1983, 1984, 1985; Rosen, 1984; Hoeksema, 1989). cause of their sedentary attached growth form, they pre- Furthermore, free-living adults had to maintain shal- sumably lived on hard substrates, like on reef slopes. low positions on steep reef slopes. Many species that In post-larval stage, ancestral fungiids also settled expanded upwards in bathymetric range show large on such hard substrata but by becoming free-living septo-costal ornamentations which may provide addi- they were also able to colonize unconsolidated sub- tional resistance on exposed steep reef slopes and pre- strates, such as sand and rubble (Wells, 1966). On reef vent them to slide downwards too quickly (Hoeksema, slopes, they could become part of and move with coral 1989, 1991a, 1993b). On the other hand, by not depart- debris, decreasing the risk of becoming buried (Hoek- ing from deeper reef slopes entirely, species were able sema, 1988). On the other hand, in 12 mushroom coral to survive during sea level regressions, when shallow species the ability to become free-living has been lost shelf habitats disappeared (Fig. 5C; Hoeksema, 2007). and they remain secondarily attached (Hoeksema, In other lineages, mushroom coral species ap- 1991a, 2009; Gittenberger et al., 2011; Benzoni et al., peared to have migrated downward, enabling them to 2012). In some areas attached fungiids have become colonize deep sandy bottoms offshore (Fig. 3). Some quite common or even dominant (Cope, 1981, 1982; free-living Cycloseris species have become special- Hoeksema, 2009). However, if corals of these species ized in this kind of habitat, which is remote from the accidently break, their fragments are able to survive as ancestral situation. In this way they have become free-living corals as well. The ultimate reversal to- nearly independent from hard substrates, especially wards the sedentary shape is found in three poly­ when they apply fragmentation as a reproductive stomatous encrusting Cycloseris species (Gittenberger mechanism (Ya­mashiro and Nishihira, 1994, 1998; et al., 2011; Benzoni et al., 2012), some of which in- Colley et al., 2002; Hoeksema and Waheed, 2011). habit the sides of dead coral at the border of reef slope This model is in contrast with a previous evolution and reef base where sedimentation may be high. Be- scenario (Wells, 1966), in which it was assumed that cause of their vertical attached position and the pos- these small, free-living mushroom corals with simple session of multiple mouths, they may also be adapted skeleton structures (Cycloseris spp.) were the least to free themselves from sediments (Chadwick-Furman evolved and that their deep sandy substrates repre- and Loya, 1992; Erftemeijer et al., 2012). sented ancestral habitats among Recent fungiids. The In various species lineages, fungiids have colonized present model suggests that these corals have devel- nearshore habitats but they have not become specialized oped a small size and simple structures in order to be in onshore distributions. They are just more eurytopic, more mobile and to be more resistant to sedimenta- by tolerating the proximity of river mouths, which sug- tion. Mushroom corals with fine ornamentations on gests that they are more resistant to freshwater. Perhaps their septa are more capable of shedding sediments this was an advantage for populations that remained in (Schuhmacher, 1977, 1979), and it is likely that a fine isolated sea basins during sea level regressions (Mc- ornamentation does not hinder their movements over Manus, 1985). These seas were probably deprived from sandy substrates (Hoeksema, 1988, 1993b; Yamashi- oceanic influence and therefore affected by river dis- ro and Nishihira, 1995). charge from the surrounding shores. Alternative evolutionary scenarios are obtained if In several species lineages, mushroom corals ap- reversals are included in the habitat transformations: peared to have migrated upward, which enabled them retreats from onshore reefs, reef flats, and reef bases to live on shallow reef flats (Figs 3-4). Here they can (Fig. 4). This model is most parsimonious with regard receive more light but they are also more exposed to to the Cycloseris clade (Fig. 4A). Alternative scenarios

Downloaded from Brill.com10/04/2021 01:37:58PM via free access Contributions to Zoology, 81 (4) – 2012 217 for other clades do not result in more parsimonious References solutions when reversals are introduced (Fig. 4B-D). The alternative scenarios do not change the notion that Abe N. 1939. Migration and righting reaction of the coral, Fun- offshore reef slopes were the most likely original gia actiniformis var. palawensis Döderlein. Palao Tropical Biological Station Studies 4: 671‑694. mushroom coral habitat. Abelson A, Loya Y. 1999. Interspecific aggression among stony The application of a phylogenetic model for recon- corals in Eilat, Red Sea: a hierarchy of aggression ability structing the evolution of mushroom coral habitats over and related parameters. Bulletin of Marine Science 65: 851- environmental gradients appears to give insight in 860. adaptive shifts that occurred in various independent Becking LE, Cleary DFR, de Voogd NJ, Renema W, de Beer M, van Soest RWM, Hoeksema BW. 2006. Beta-diversity of species lineages over time. The model shows how gra- tropical marine assemblages in the Spermonde Archipelago, dients of species richness could have evolved on shelf- Indonesia. Marine Ecology 27: 76-88. based reef systems through diversification from an Beer M de. 1990. Distribution patterns of regular sea urchins ancestral ecological zone of origin (offshore slopes (Echinodermata: Echinoidea) across the Spermonde Shelf, used by Fungiidae ancestors) combined with homo- SW Sulawesi (Indonesia). Pp. 165-169 in: de Ridder C, Du­ bois P, Lahaye MC, Jangoux M, eds, Echinoderm Research. plastic adaptive shifts leading to the colonisation of Rotterdam: Balkema. new ecological zones, i.e. onshore habitats, reef flats Benzoni F, Stefani F, Stolarski J, Pichon M, Mitta G, Galli P. and reef bases. The present high mushroom coral di- 2007. Debating phylogenetic relationships of the scleractin- versity found on offshore slopes in shelf zone 3, con- ian Psammocora: molecular and morphological evidences. firms the assumption that cross-shelf gradients of di- Contributions to Zoology 76: 35-54. Benzoni F, Arrigoni R, Stefani F, Reijnen BT, Montano S, versity have been established with the highest species Hoeksema BW. 2012. Phylogenetic position and taxonomy richness in environments that are older, more wide- of Cycloseris explanulata and C. wellsi (Scleractinia: spread, or less stressful (Ricklefs, 2006). 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Competition and locomotion in a free- diversity. living fungiid coral. Journal of Experimental Marine Biol- ogy and Ecology 123: 189-200. Chadwick-Furman NE, Loya Y. 1992. Migration, habitat use, and competition among mobile corals (Scleractinia: Fungii- Acknowledgements dae) in the Gulf of Eilat, Red Sea. Marine Biology 114: 617- 623. The research was financed by the Netherlands Foundation for Clarke KR, Gorley RN. 2006. PRIMER v6: User Manual/Tuto- the Advancement of Tropical Research (WOTRO, grant W77- rial. PRIMER-E, Plymouth 96) as part of a PhD project, for which the fieldwork (as part of Clarke KR, Warwick RM. 2001. Change in marine communi- the Buginesia Programme) was supervised by Dr. M.R.R.B. ties: an approach to statistical analysis and interpretation, Best (National Museum of Natural History, Leiden) and Prof. 2nd edition. PRIMER-E, Plymouth Dr. J.H.J. Terwindt (Department of Physical Geography, Utre- Claereboudt M. 1988. Spatial distribution of fungiid coral pop- cht University) and the thesis by Prof. Dr. E. Gittenberger (Na- ulation on exposed and sheltered reef slopes in Papua New tional Museum of Natural History and Leiden University) and Guinea. Proceedings of the 6th International Coral. Reef Prof. Dr. K. Bakker (Leiden University). The research permit Symposium, Townsville, Australia 2: 715-720. was granted through the Indonesian Institute of Sciences Cleary DFR, de Voogd NJ. 2007. Environmental determination (LIPI), Jakarta. The Research Centre for Oceanography of sponge assemblages in the Spermonde Archipelago, Indo- (PPO‑LIPI) at Jakarta and Hasanuddin University at Makassar nesia. Journal of the Marine Biological Association of the acted as sponsor. I am grateful to rector and staff of Hasanuddin United Kingdom 87: 1669-1676. University at Makassar for their hospitality and assistance, es- Cleary DFR, Becking LE, de Voogd NJ, Renema W, de Beer M, pecially vice rector prof. Hardjoeno and my colleague Drs. W. van Soest RWM, Hoeksema BW. 2005. Variation in the di- Moka at the Marine Biology laboratory. Zarinah Waheed per- versity and composition of benthic taxa as a function of dis- formed the cluster analyses with Primer. I want to thank Dr. T.J. tance offshore, depth and exposure in the Spermonde Archi- Done and four anonymous reviewers for critical comments on pelago, Indonesia. Estuarine Coastal and Shelf Science 65: the manuscript. 557-570.

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