Zoological Studies 56: 20 (2017) doi:10.6620/ZS.2017.56-20

Applying Benthic Foraminiferal Assemblage to Evaluate the Coral Reef Condition in Dongsha Atoll lagoon Chienhsun Chen1,2,* and Hui-Ling Lin1,2 1Taiwan Ocean Research Institute, National Applied Research Laboratories, 80143 Kaohsiung, Taiwan 2Department of Oceanography, National Sun Yat-sen University, 80424 Kaohsiung, Taiwan

(Received 29 March 2017; Accepted 27 June 2017; Published 20 July 2017; Communicated by Benny K.K. Chan)

Chienhsun Chen and Hui-Ling Lin (2017) Coral reefs in the South China Sea are threatened by environmental changes and anthropogenic disruptions. , a group of unicellular shelled protists, has been considered a reliable indicator of water quality and reef health. However, this indicator has not yet been used to study coral reefs in the South China Sea. In this study of foraminifera in the lagoon of Dongsha Atoll, both the assemblage diversity and the functional group composition were investigated. The FORAM index (FI), a numerical indicator based on functional group composition, was used to evaluate the condition of the coral reef of the Atoll lagoon. A typical assumption is that FI = 4 is the minimum index value corresponding to a suitable environment for the growth of calcifying organisms. Environments with FI values between 2 and 4 are unsuitable to marginal for recovery of coral communities after a mortality event. Data were recorded regarding a total of 287 foraminiferal species. Approximately 68% of the tests belonged to the porcelaneous taxa; the , , and Pseudomassilina species were well represented. Hyaline foraminifera were less abundant than porcelaneous foraminifera; the agglutinated foraminifera were the least abundant. Multivariate analyses revealed four clustering groups. The functional groups were classified according to FI’s definition; the heterotrophic group was the most abundant, accounting for 82% of foraminiferal abundance. The symbiont-bearing group was the second most abundant, with a relative abundance of 12%; and the stress-tolerant group was the least abundant. Two samples had FI values slightly higher than 4; Amphisorus and Calcarina were dominant, but the other symbiont-bearing foraminifera had lower values. These high FI values can be associated with seagrass meadows or relict shells in an altered environment. Eighty percent of the sediment samples had FI values lower than 4, indicating that most of the benthic habitats in the Dongsha lagoon are not suitable for coral growth and reef recovery. The present findings provide an alternative evaluation method based on foraminiferal assemblages for future studies on the environmental changes of coral reefs.

Key words: Benthic foraminifera, FORAM index, Coral reef, Dongsha Atoll, South China Sea.

BACKGROUND 40 years unless more effective management is implemented (Bellwood et al. 2004; Knowlton and Coral reefs are vital coastal ecosystems that Jackson 2008). provide crucial services and goods to maritime Foraminifera are the most abundant shelled tropical and subtropical nations (Costanza et al. microorganisms, which substantially contribute 1997). However, coral reefs are rapidly declining to the carbonate sediments in shallow-water globally because of various stressors, such as environments. Owing to their prolific abundance, climate change and anthropogenic disruptions short reproductive cycle, and sensitivity to environ- (reviewed in Richmond 1993; Hoegh-Guldberg mental changes, benthic foraminifera have been et al. 2007). Furthermore, 15% of the coral reefs used as exceptional bioindicators of marine coastal worldwide are currently predicted to be lost in 20- environments. They have been used to evaluate

*Correspondence: E-mail: [email protected]

1 Zoological Studies 56: 20 (2017) page 2 of 16

a wide range of anthropogenic pollution (e.g. the 1998 worldwide bleaching event and frequent Resig 1960; Watkins 1961) and to assess the destructive fishing practices, coral reefs in the consequences of organic waste discharges (e.g. lagoon of Dongsha Atoll (hereafter referred to Alve 1995; Schafer 2000; Samir and El-Din 2001; as the Dongsha lagoon) were degraded (Morton Yanko et al. 2002). 2002; Dai 2006). Regular ecological surveys In the past decade, benthic foraminiferal were conducted after the degradation, but the assemblages have been employed for the rapid recovery of the reef in the Dongsha lagoon assessment of coral reef conditions (reviewed remains debatable. An effective assessment of in Cooper et al. 2009). Hallock et al. (2003) the status of this coral reef is required. Therefore, developed a numerical index to associate water this study investigated the assemblages of benthic quality with reef health, known as the Foraminifera foraminifera to provide an alternative assessment in Reef Assessment and Monitoring (FORAM) of the benthic environment in the Dongsha lagoon. index (FI). The FI uses benthic foraminiferal The present work is the first investigation assemblages to quantify the suitability of an to study the benthic foraminifera in the Dongsha environment to support the prolific growth of lagoon. This study aims (1) to assess the calcifying organisms that host endosymbiotic algae, composition and assemblages of the benthic such as zooxanthellate corals and larger benthic foraminifera in the Dongsha lagoon and (2) to use foraminifera. These endosymbionts aid in the fast-responding foraminifera to assess the present calcification and food production for foraminifera reef-building status of the lagoon environment. just as zooxanthellae aid corals (Hallock 2000). However, endosymbionts constrain the growth of symbiont-bearing foraminifera and corals MATERIALS AND METHODS within the photic zone, particularly in relatively clear and oligotrophic waters (Hallock 1999). Sampling When the nutrient supply increases, fleshy algae and sponges dominate the benthic community. Surface sediments from the Dongsha lagoon Consequently, foraminiferal assemblages (which were collected in September 2009, in May and consist of small and fast-growing species) can September 2010, and in August 2013. Evenly be measured to quantify environmental quality distributed sampling stations in the lagoon were with respect to reef health (Reymond et al. 2012). originally planned; however, some stations were Previous applications of the FI have revealed the relocated because of the uncertain weather and advantages of foraminifera as bioindicators of reef sea conditions. Field sampling and laboratory conditions in the Aegean Sea (Koukousioura et al. preparation of the samples were performed 2011), Brazil (Barbosa et al. 2009; Barbosa et al. following the methods described by Hallock et 2012), Colombia (Velásquez et al. 2011), Florida al. (2003) and Narayan and Pandolfi (2010), (Carnahan et al. 2009), Moorea, French Polynesia with minor modifications. Typically, scuba divers (Fajemila et al. 2016), and the Great Barrier Reef scooped the upper 1-2 centimeters of the surface (Schueth and Frank 2008; Uthicke and Nobes sediments into a plastic bag. Each sample was 2008). However, the FI has not yet been applied to treated with 4% neutral formaldehyde and stored evaluate coral reefs in the South China Sea (SCS). in a plastic bag until it was transported to the Dongsha Atoll is a coral atoll in the northern laboratory. Figure 1 and table 1 present the SCS. The atoll’s circular-shaped lagoon is 16 km sampling sites and the data obtained from the in width and provides a wide array of habitats, samples. including seagrass meadows and coral reefs. It has been recognized for its biodiversity and Laboratory preparation ecological significance in the northern SCS (Morton 2002; Dai 2006). Early surveys of the In the laboratory, each sample was examined, region examined a limited number of sites close and any algae and sea grass were removed. Each to the Dongsha Islands. For example, a survey sample was freeze-dried and agitated thoroughly. conducted in 1994 recorded abundant coral and According to the preliminary determinations of fish, high coral coverage (80%-95%), and well- ideal quantitative counts, 200-300 individuals, developed communities of large Acropora and approximately 10 g of freeze-dried sediment Porites colonies around Dongsha Island (Chen subsample was wet-sieved by using deionized et al. 1995; Dai et al. 1995). However, owing to water over a 125-μm mesh sieve. The samples Zoological Studies 56: 20 (2017) page 3 of 16

N

Fig. 1. Map of Dongsha Atoll showing main geomorphological features and sampling sites in this study. ■ Dongsha Island; Back and fore reefs; □ Reef flat; ● Sampling sites.

Table 1. Information on benthic foraminifera in the Dongsha lagoon, including GPS and depth of the sediment sample, relative percentage of foraminiferal taxa with different shell textures, diversity index, relative percentage of foraminiferal taxa of different functional groups and the FORAM index. Shell texture: relative percentage of foraminifera with porcelaneous (P), hyaline (Y), and agglutinated (A) shell texture. Diversity index: Margalef richness index (d), Simpson dominance index (D), and Shannon-Wiener index (H). Functional group: symbiont-bearing (S), stress-tolerant (O), and other small and heterotrophic taxa (H)

Sample GPS Depth Identified Shell texture (%) Diversity index Functional group (%) FORAM

(latitude, longitude) (m) species P Y A d D H S O H index

A 20°42.59'N, 116°45.91'E 5 69 76.8 21.9 1.3 12.4 0.06 3.6 35.9 5.1 59.1 4.8 B 20°43.38'N, 116°47.78'E 12 68 60.6 34.6 4.8 10.6 0.04 3.6 2.7 9.1 88.3 2.1 C 20°44.48'N, 116°50.68'E 13 77 71.9 17.3 10.8 10.8 0.05 3.4 13.6 4.3 82.1 3.0 D 20°41.65'N, 116°47.17'E 15 44 48.3 45.2 6.6 7.0 0.04 3.4 2.2 10.0 87.8 2.1 E 20°41.95'N, 116°50.53'E 15 98 77.9 22.1 0 17.2 0.02 4.2 11.7 4.3 84.0 2.9 F 20°42.48'N, 116°52.75'E 5 86 84.8 11.1 4.0 14.9 0.03 4.0 5.7 5.1 89.2 2.4 G 20°39.80'N, 116°46.21'E 10 88 40.0 60.0 0 15.4 0.06 3.7 44.3 9.6 46.1 5.4 H 20°40.52'N, 116°48.42'E 5 93 72.1 12.4 15.5 16.2 0.03 4.0 3.4 3.1 93.4 2.2 I 20°40.65'N, 116°52.98'E 12 93 60.8 31.2 8.0 13.3 0.04 3.8 2.1 3.5 94.4 2.1 J 20°37.85'N, 116°50.47'E 12 101 82.5 17.1 0.3 17.4 0.02 4.2 3.8 6.3 89.8 2.2

Average 81.7 67.5 27.4 5.1 13.5 0.04 3.8 12.5 6.0 81.4 2.9 Zoological Studies 56: 20 (2017) page 4 of 16

separated from the >125-μm fraction were dried These indices were calculated for each sediment in an oven at 50°C overnight and stored at room sample. The raw count data were first tabulated temperature. All benthic foraminiferal specimens and transformed to RA percentages by dividing the from the >125-μm fraction were handpicked number of individuals of a species (n) by the total from each subsample and placed on microslides number of individuals (N), where RA = 100 × n/N. for identification under a standard dissecting Each RA was used to conduct basic descriptive microscope. We examined the total foraminiferal statistical analysis, including faunal composition assemblages in each sediment subsample. The and percentages of taxa with different wall total assemblages provided information about the compositions. overall conditions that had accumulated over time. Margalef richness index (d), which estimates If the number of foraminiferal specimens was lower species richness, and is independent of the sample than the ideal quantitative count for a sample, size, was calculated as follows: additional sediment subsamples were weighed and processed as previously described. d = (S - 1)/ln (N) The taxonomic assignments of the benthic foraminifera were determined under a dissecting where S is the number of species (Margalef microscope. The supraspecific identification 1958). Simpson dominance index is based on the was based on their test characteristics, such as probability that two individuals randomly selected wall material and structure, as well as chamber from a sample belong to the same species arrangement and aperture position, following (Simpson 1949). The Simpson dominance index, the classification criteria of Loeblich and Tappan ranging from 0 (equal distribution of individuals (1988). Taxonomic identification was performed among species) to 1 (dominance of one species in using taxonomic monographs of the SCS (Zheng the community), was calculated as follows: and Zheng 1978; Zheng 1979; Zheng 1980), 2 Australian (Nobes and Uthicke 2008; Debenay D = Σ (Pi) 2012) and Indo-Pacific regions (Cushman 1910, 1921; Jones 1994). Intact specimens that where Pi is the proportion of individuals belonging showed no signs of reworking and damage were to species i. The Shannon-Wiener diversity index included in the following analyses. A few abraded (H) was calculated on the basis of the RA data: specimens (1-18 individuals per sample station) were found in this study. For each representative H = −Σ [Pi × ln(Pi)] specimen, several images were captured from different focal lengths by using a digital camera It is a measure of heterogeneity considering the (Canon EOS 7D) mounted on a stereoscopic evenness of species abundance (Shannon 1948; microscope (Leica M205). The focus depths were Murray 1991). Differences in diversity indices subsequently enhanced and multiple images were between sediment samples were analyzed using merged digitally into one picture by using Helicon pairwise permutation tests with 9999 random Focus (Helicon Soft Ltd.), as illustrated in figure iterations. Calculations and statistical tests were 2. All samples and specimen illustrations were conducted using PAST 3.15 (Hammer et al. 2001). deposited in the micropaleontological collection of the Marine Core Repository and Laboratory at the Functional groups and the FORAM index Taiwan Ocean Research Institute, National Applied Research Laboratories. The FI, initially described by Hallock et al. (2003) for assessing whether a benthic Analysis of foraminiferal assemblages and the environment is hospitable to symbiont-bearing biodiversity index organisms (i.e., corals and reefal foraminifera), was calculated. The FI was calculated according The variability in the foraminiferal community to the foraminiferal composition by arranging the was quantitatively evaluated in terms of the foraminiferal genera into three functional groups, species relative abundance (RA); the number of namely: (1) taxa of large foraminifera that hosted identified species; and diversity indices, including algal symbionts, (2) pollution-tolerant opportunistic species richness (Margalef richness index, d), foraminifera that dominated high-stress dominance (Simpson dominance index, D), and environments, and (3) other small heterotrophic diversity (Shannon-Wiener diversity index, H). foraminifera. The FI was calculated as follows: Zoological Studies 56: 20 (2017) page 5 of 16

1 2 3 4 5a 5b

6 7a 7b 8a 8b 9a 9b

10a 11a 12a 13a

10b 11b

12b 13b

14a 15 16a 17a 18

16b 17b

14b

Fig. 2. Foraminifera from the Dongsha lagoon. 1. Calcarina mayori Cushman; 2. Pseudohauerina orientalis (Cushman); 3. Pseudolachlanella eburnea (d’Orbigny); 4. Bolivina variabilis (Williamson); 5. Amphisorus hemprichii Ehrenberg, a: lateral view, b: apertural view; 6. Spiroloculina attenuate Cushman, lateral view; 7. Dendritina striata Hofker, a: lateral view, b: aperatural view; 8. Miliolinella subrotunda (Montagu), a: lateral view, b: apertural view; 9. Elphidium crispum (Linn), a: lateral view, b, apertural view; 10. Cymbaloporetta bradyi (Cushman), a: dorsal view, b: ventral view; 11. Rosalina globularis d’Orbigny, a: dorsal view, b: ventral view; 12. Pyrgo denticulata (Brady), a: lateral view, b: apertural view; 13. Pseudomassilina pacificiensis Cushman, a: lateral view, b: apertural view; 14. Triloculina wiesneri Le Calvez and Le Calvez, a: lateral view, b: aperatural view; 15. Spirillina grosseperforata Zheng, lateral view; 16. Fijiella simplex (Cushman), a: apertural view, b: lateral view; 17. Reussella pacifica Cushman and McCulloch, a: apertural view, b: lateral view; 18. Textularia agglutinans d’Orbigny, side view. Scale bar = 100 µm. Zoological Studies 56: 20 (2017) page 6 of 16

FI = (10 × Ps) + (Po) + (2 × Ph) Buliminida, and Rotaliida (Appendix 1). Of the 287 identified species, only 63 (22%) species where Ps, Po, and Ph represent the proportion consistently occurred and were found in more than of symbiont-bearing, stress-tolerant, and other half of the sediment samples (Appendix 1). When heterotrophic taxa, respectively. The FI is a single- all foraminiferal specimens of the 10 samples in the metric indicator of water quality that has already Dongsha lagoon were combined, approximately been applied in tropical coral reef communities 98% of the foraminiferal species had RA values of and subtropical estuarine environments (reviewed less than 3%. Only five species, Quinqueloculina in Hallock 2012; Reymond et al. 2012). A coral bosciana (RA = 3.5%), Pseudohauerina orientalis reef with FI > 4 is an oligotrophic environment (RA = 3.4%), Fijiella simplex (RA = 3.2%), Q. supporting calcifying mixotrophs. However, an FI debenayi (RA = 3.2%), and Textularia agglutinans between 2 and 4 indicates a marginal environment (RA = 3.1%), had RA values exceeding 3%. for calcifying foraminifera, and FI < 2 indicates Porcelaneous foraminifera were predominant environmental conditions that support substantial throughout the Dongsha lagoon (Appendix 1). For populations of stress-tolerant foraminifera (Hallock example, among the consistent species, 76.2% et al. 2003). were porcelaneous foraminifera (48 species), belonging to Pseudohauerina of Brebinidae; Multivariate statistics Planispirinella and Vertebralina of Fischerinidae; Miliolinella, Pseudolachlanella, Pseudomassilina, For determining the structures of the Pyrgo, Quinqueloculina, Schlumbergerina, foraminiferal assemblages, RA of a subset of Sigmamiliolonella, and Triloculina of ; the most abundant 23 foraminiferal genera that Dendritina of Peneroplidae; Amphisorus, accounted for approximately 85% of the total Parasorites, and Sorites of Soriitae; and population of the foraminifera was used. Q-mode Spiroloculina of Spiroloculinidae. Fourteen hyaline hierarchical clustering techniques were applied to species were consistent, including those belonging retrieve information and discover structural entities to Ammonia and Neorotalia of Rotaliidae, Fijiella within complex data sets (Parker and Arnold 1999). of Reussellidae, Epistomaroides of Alfredinidae, A nonmetric multidimensional scaling (nmMDS) Cibicides of Cibicididae, Cymbaloporetta of analysis was carried out to visualize and refine the Cymbaloporidae, Elphidium of Elphidiidae, grouping pattern among samples. The between- Heterostegina of Nummulitidae, and Rosalina group differences in foraminiferal composition were of Rosalinidae. Only one agglutinated species, tested by analysis of similarity (ANOSIM). The taxa belonging to the genus Textularia, consistently contributing most to the dissimilarity among groups occurred. were identified by similarity percentage analysis Porcelaneous foraminifera were the most (SIMPER). Distance and similarity measurements abundant foraminifera in the Dongsha lagoon, of the multivariate analyses were calculated based with RAs of approximately 40%-84.8% in our on the Bray-Curtis distance. For cluster grouping, sediment samples (Table 1). Quinqueloculina a paired grouping algorithm with a bootstrapping was the most abundant genus (RA = 28.1%) and procedure of 500 iterations was executed to was well-represented with Q. bosciana as the evaluate the stability of the clustering results. The most abundant species (RA = 3.5%), followed by ANOSIM was tested with 9999 permutations. Q. debenayi (RA = 3.2%) and Q. parkeri (RA = Calculations and statistical tests were conducted 2.9%). Triloculina and Pseudomassilina were the using PAST 3.15 (Hammer et al. 2001). second and third most abundant porcelaneous genera with RAs of 6.4% and 5.2%, respectively. Hyaline foraminifera, with an average RA of RESULTS 27.4%, were less abundant than porcelaneous foraminifera. Elphidium and Fijiella were the Benthic foraminiferal assemblage most abundant hyaline taxa, with RAs of 3.4% and 3.2% respectively. Agglutinated taxa were A total of 4,935 benthic foraminifera were the least abundant (average RA = 5.1%, Table 1) recognized, which accounted for 287 species and were recorded in only a total of 21 species. belonging to 111 genera distributed among the Textularia was the most abundant agglutinated orders Astrorehizida, Lituolida, Textulariina, genus (RA = 3.9%) and was well-represented with , Spirilinida, Lagenida, Robertinida, T. agglutinans (RA = 3.1%). Zoological Studies 56: 20 (2017) page 7 of 16

Biodiversity index (a)

In each sample, 44-101 species were identified, with a mean of 81.7 (Table 1). The least species, occurring in sample D, was the smallest value from the rest, but it was not a significant outlier (p > 0.05; Grubbs test, Z = 2.29). The Margalef richness index of the foraminiferal assemblages ranged between 7.0 and 17.4 (Table 1). The Margalef richness index of the foraminiferal assemblages was the highest in samples J and E and was on an average approximately 1.2 times higher than that in samples A, B, C, and D. Pairwise permutation testing revealed that the sediments from the east and southeast regions of the Dongsha lagoon had high species richness (b) (p < 0.001 with Bonferroni correction in all pairwise permutation tests, Fig. 3a). The Simpson dominance index ranged between 0.02 and 0.06 (Table 1). The north and west regions of the Dongsha lagoon showed high dominance index values of benthic foraminifera. Species, such as Amphisorus hemprichii (RA = 20.3% in sample A), Calcarina spp (RA = 29.7% in sample G), and Quinqueloculina debenayi (RA = 12.5% in sample C) were dominant at these stations. However, the RA of each foraminiferal species was lower than 10% in the remaining samples. The Shannon-Wiener diversity index ranged between 3.4 and 4.2 (Table 1). Pairwise (c) permutation analyses revealed higher foraminiferal diversity in samples collected from the east and southeast regions, such as samples J and E; the diversity was approximately 1.2 times higher than that in samples collected from the north and west regions (samples A, B, C, and D; Fig. 3c).

Functional groups and the FORAM index

According to the functional groups defined by Hollock et al. (2003), the heterotrophic group was predominant, which comprised approximately 81.4% of the foraminifera in the benthic environment of the Dongsha lagoon (Table 1). Among the 93 heterotrophic genera, 10, including Fijiella, Miliolinella, Pseudohauerina, Fig. 3. Diversity index of benthic foraminifera from surface Pseudomassilina, Quinqueloculina, Reussella, sediments of the Dongsha Atoll lagoon: (a) Margalef richness Spirillina, Spiroloculina, Textularia, and Triloculina, index; (b) Simpson dominance index; and (c) Shannon - Wiener had RA values > 5% at more than two stations. diversity index. Error bars indicate the upper and lower limits Symbiont-bearing foraminifera were not of 9999 bootstrap iterations. Horizontal lines under the x-axis indicate no significant differences among the sampling sites abundant, with an average RA of 12.5% (Table (p > 0.001, pairwise comparison with 9999 random permutation 1). Thirteen genera were classified as symbiont- iterations). Sampling sites refer to table 1 and figure 1. bearing foraminifera, including Alveolinella of Zoological Studies 56: 20 (2017) page 8 of 16

Alveolinidae; Amphistegina of Amphisteginidae; levels of symbiont-bearing foraminifera, such as A. Baculogypsina and Calcarina of Calcarinidae; hemprichii and Calcarina species. The prevalence Heterostegina and Operculina of Nummulitidae; of other symbiont-bearing foraminifera, including A. Coscinopira and Dendritina of Peneroplidae; sauronensis, Heterostegina depressa, Parasorites Neorotalia of Rotaliidae; and Amphisorus, orbitolitoides, and Sorites orbiculus, was minimal. Marginopora, Parasorites, and Sorites of Soritidae Quinqueloculinids constituted approximately (Table 2). Only Calcarina had RA values >5% 13.6% and 24.9% of clusters 1 and 2, respectively. in two samples. Stress-tolerant foraminifera Other thick-shelled miliolids, such as Miliolinella constituted the least abundant group, with an subrotunda, Pseudohauerina involute, Pyrgo average RA of 6% (Table 1); this group included depressa, Spiroloculina antillarum, and Triloculina Bolivina and Bolivinellina of Bolivinidae, Elphidium wiesneri, occurred in minimal proportions. of Elphidiidae, Ammonia of Rotaliidae, and Opportunistic taxa, such as Elphidium, were Ammobaculite of Lituolidae (Table 2). abundant in sample G (RA = 7.1%). The FI ranged between 2.1 and 5.4 and was Cluster 3 mostly consisted of samples from typically low in the Dongsha lagoon (Table 1). the northeast region of the Dongsha lagoon, Eighty percent of the samples had FI values < 4. including samples C, E, F, H, and J. Sixty-five The FI exceeded 4 for samples A (FI = 4.8) and G percent of similarity and a moderate bootstrap (FI = 5.4), where Amphisorus (RA = 24.1%) and support (56%) indicated potential subgroups Calcarina (RA = 29.6%) were dominant. within this cluster. This cluster included a diverse assemblage of 222 species of benthic foraminifera. Multivariate analyses It was characterized by a high abundance of Quinqueloculina (RA = 31.7%-45.8%), which was Cluster analysis comparing the compositions represented by 55 species, and it constituted and RAs of foraminiferal species in all samples 41.4% of all specimens collected from the revealed four clusters at 65% similarity, with a high sampling stations. The agglutinated taxon of cophenetic coefficient (0.90) and robust support Textularia, accounting for 6.8% of all specimens, (bootstrap value > 50%; Fig. 4). However, the was the second most predominant taxon. The results of cluster analysis were not consistent with proportion of symbiont-bearing foraminifera, such the geological affinity of the samples. as Coscinospira hemprichii and Dendritina striata, Clusters 1 and 2 were observed in samples was moderate in sample C (RA = approximately G and A, respectively. These samples were 6%) but minimal in the other samples (RA = 0%- characterized by median to coarse sand and high 2.2%). The prevalence levels of other miliolids,

Table 2. Generic categorization of functional groups of foraminifera in the Dongsha lagoon. Stars indicate the selected 23 genera of benthic foraminifera included in cluster analyses

Functional groups Genera of benthic foraminifera

Symbiont-bearing Alveolinella, Amphisorus*, Amphistegina, Baculogypsina, Calcarina*, Coscinospira*, Dendritina*, Heterostegina, Marginopora, Neorotalia, Operculina, Parasorites, Sorites Opportunistic Ammobaculites*, Ammonia, Bolivina*, Bolivinellina, Elphidium* Heterotrophic Acervulina, Acupeina, Adelosina, Alliatina, Alliatinella, Ammomassilina, Anomalinella, Anomalinoides, Articulina, Ashbrookia, Baggina, Bronnimannia, Buliminoides, Cancris, Caribeanella, Cibicides, Cibicidoides, Cibicorbis, Clavulina, Conicospirillinoides, Cornuspira, Cymbaloporella*, Cymbaloporetta, Discorbinella, Epistomaroides, Eponides, Fijiella*, Fissuripolymorphina, Fontbotia, Fursenkoina, Gyroidina, Hanzawaia, Hauerina, Haynesina*, Heterolepa, Hyperammina, Inaequalina, Laryngosigma, Lenticulina, Melonis, Miliammina*, Miliola, Miliolinella*, Millettiana, Mychostomina, Neocassidulina, Neoconorbina, Neoeponides, Nodobaculariella, Nonion, Nonionoides, Nummulopyrgo, Pararotalia, Parrina, Planispirillina, Planispirinella, Planogypsina, Planorbulinella, Planulina, Poroeponides, Porosononion, Pseudohauerina*, Pseudolachlanella*, Pseudomassilina*, Pseudotriloculina, Pyrgo*, Pyrgoella, Quinqueloculina*, Reophax, Reussella*, Rosalina*, Rotorbis, Saintclairoides, Schlumbergerina, Sigmamiliolinella, Sigmavirgulina, Sigmoilinella, , Siphogenerina, Siphonina, Siphotextularia, Spirillina*, Spiroloculina*, Spirosigmoilina, Textularia*, Triloculina*, , Ungulatelloides, Uvigerina, Valvulineria, Vertebralina, Wiesnerella, Zoyaella Zoological Studies 56: 20 (2017) page 9 of 16 such as Pseudohauerina orientalis (RA = 1.4%- in approximately the same manner as that of 5.3%) and Pseudomassilina robusta (RA = 0%- cluster analysis (Fig. 5). On an nmMDS plot the 11.4%) and species of Miliolinella (RA = 0%- distance between two points corresponds to 2.8%), Spiroloculina (RA = 0%-3.1%), and their similarity in composition. Different clustering Triloculina (RA = 0%-2.8%) were moderate to groups were distributed in various quadrants of minimal. Opportunistic taxa, such as Bolivina and the plot with a fair goodness of fit (Fig. 5; stress = Elphidium, occurred in minimal quantities. 0.10). Results of the ANOSIM analyses showed Cluster 4 comprised samples B, D, and I, and significant differences in foraminiferal assemblage consisted of 153 species of benthic foraminifera. composition between clusters 3 and 4 (R = 0.98, The thick-shelled miliolids were prominent in p = 0.02 with 9999 permutations). Because each this cluster. The prevalence of quinqueloculinids of clusters 1 and 2 had only one sediment sample, was 13.7% at these sites, followed by Miliolinella clusters 1 and 2 were excluded from the ANOSIM (7.1%), Reussella (RA = 6.9%), Pseudomassilina test. Results of SIMPER analyses indicated that (RA = 6.8%), Triloculina (RA = 6.2%), Spirillina overall dissimilarities ranged from 49% to 59.9% (RA = 6.0%), Fijiella (RA = 5.9%), Spiroloculina (Table 3). In most of the pairwise comparisons, (RA = 5.8%), and Pseudohauerina (RA = 5.1%). abundant genera were the taxa contributing most Symbiont-bearing taxa were rare and accounted to the between-group differences. For example, for only 2% of all foraminifera. Calcarina and Amphisorus contributed most to the An nmMDS ordination plot based on between-group dissimilarity of clusters 1 and 2, same data set grouped the sampling stations respectively (Table 3).

Relative abundance : 0 - 0.9 : 1 - 4.9 : 5 - 9.9 : 10 - 19.9 : 20 - 39.9 : >40

Similarity 0.42 0.48 0.54 0.60 0.66 0.72 0.78 0.84 0.90 0.96 Amphisorus Calcarina Coscinospira Dendritina Miliammina Textularia Pseudohauerina Miliolinella Pseudolachlanella Pseudomassilina Pyrgo Quinqueloculina Triloculina Spiroloculina Spirillina Fijiella Reussella Cymbaloporetta Haynesina Rosalina Ammobaculites Bolivina Elphidium G Cluster 1 C

56 E Cluster 3 F

J

H

A Cluster 2 100 B

77 D Cluster 4 I

Fig. 4. Dendrogram of the sampling sites plotted by cluster analysis by using Bray-Curtis similarity based on the subset dataset of 23 foraminiferal genera. Values on the dendrograms indicate the > 50% supporting value of 500 bootstrap iterations. Zoological Studies 56: 20 (2017) page 10 of 16

C 0.24 I H 0.16

0.08 F E

-0.40 -0.32 -0.24 -0.16 J -0.08 0.08 0.16 0.24 0.32 D B Axis 2 -0.08

-0.16

A -0.24

-0.32

-0.40 G

-0.48 Stress: 0.10 Axis 1

Fig. 5. Nonmetric multidimensional analysis of foraminiferal assemblages in the Dongsha lagoon. Symbols indicate different groups in the cluster analysis: △, Cluster 1; ○, Cluster 2; □, Cluster 3; X, Cluster 4. Sediment samples refer to table 1 and figure 1.

Table 3. SIMPER analysis of foraminiferal assemblages in the Dongsha lagoon. Above diagonal: average dissimilarity (%) between clusters; below diagonal: five taxa contributing most to between-cluster dissimilarity; the contribution (%) to the total dissimilarity of each taxon is given in brackets

Grouping Cluster 1 Cluster 2 Cluster 3 Cluster 4

Cluster 1 51.0 53.9 56.2 Cluster 2 Calcarina (33.9) 49.0 59.9 Amphisorus (27.9) Quinqueloculina (11.5) Elphidium (7.7) Pseudomassilina (3.9) Cluster 3 Calcarina (38.2) Amphisorus (29.7) 51.4 Quinqueloculina (25.1) Quinqueloculina (15.7) Textularia (5.7) Pseudomassilina (8.6) Elphidium (5.7) Calcarina (6.8) Pseudomassilina (5.2) Textularia (6.0) Cluster 4 Calcarina (36.7) Amphisorus (24.6) Quinqueloculina (27.7) Reussella (7.9) Quinqueloculina (10.9) Reussella (8.4) Spirillina (6.6) Reussella (7.5) Pseudomassilina (8.0) Fijiella (6.3) Spirillina (6.2) Spirillina (7.1) Pseudomassilina (5.9) Fijiella (5.9) Fijiella (5.8) Zoological Studies 56: 20 (2017) page 11 of 16

DISCUSSION 1995), foraminifera (Langer and Lipps 2003), and other metazoans (Gosliner 1993; Roberts et al. Species diversity of foraminifera in the 2002). Dongsha lagoon Foraminiferal assemblages in the Dongsha Bicchi et al. (2002) proposed that the species lagoon richness of benthic foraminifera in an atoll lagoon can be influenced by the extent of seawater Quinqueloculina, Triloculina, and exchange between the lagoon and peripheral Spiroloculina, with 58, 18, and 16 species oceanic environments. An atoll lagoon with a high respectively, constitute the bulk of the lagoonal degree of aperture has a high influx of ocean assemblages. This pattern is similar to that water, thus increasing the probability of a higher observed in some atoll lagoons and back-reef number of colonizers in the lagoon (Hatcher habitats in the Indo-Pacific region (Bicchi et al. 1997; Adjeroud et al. 2000). However, Dongsha 2002; Uthicke et al. 2010; Makled and Langer Atoll has a low degree of lagoonal aperture; 2011; Parker and Gischler 2011; Fajemila et al. therefore, it has a limited number of colonizers. 2016). Uthicke et al. (2010) reported that these The exchanges between the lagoonal and oceanic heterotrophic miliolids are dominant in sediments waters are mainly through two wide channels on with high organic content and in localities with the northwest and southwest of the atoll, driven by low light availability in the Great Barrier Reef. the semidiurnal tides (Chang 2012). Only 10% of Their high abundance can be mostly attributed to lagoonal water was replaced by introduced oceanic turbid environments in the Dongsha lagoon. The water during the high tide (Chang 2012). Moreover, suspended particles reduce the amount of light low numbers of planktonic foraminifera found in reaching the shallow benthic system, and increase this study might indicate a limited penetration of the organic matter load of the sediments. the Dongsha lagoon by planktonic forms, including Amphisteginids are few in the Dongsha planktonic stages of benthic colonizers. lagoon, although they typically dominate warm Habitat age is considered a main factor that and shallow-water environments (Hallock 1981; can influence the benthic foraminiferal diversity Baccaert 1987). Different Amphistegina species in an atoll lagoon (Bicchi et al. 2002). A deeper show distinct depth zonation, with a reduced lagoon that was flooded earlier has a longer laminar thickness to adapt to attenuated light with colonization period during postglacial transgression water depth even in some deep atoll lagoons than a shallower lagoon that was inundated later. (Hallock and Hansen 1979; Parker and Gischler Regarding Dongsha Atoll, a study of geological 2011). Our unpublished data revealed that A. drilling proposed that the Holocene atoll developed lessonii and A. lobifera were predominant in reef- on an antecedent platform of Pleistocene flat and fore-reef environments in Dongsha Atoll, limestone 7300 years ago (Gong and Wang 2013). respectively. Their absence could be due to the low The average depth of the Dongsha lagoon is 16 m, light levels in turbid environments in the Dongsha indicating a medium-water environment and young lagoon. habitat compared with other atoll lagoons in the Dendritina species, symbiont-bearing Pacific and Indian oceans (Bicchi et al. 2002). peneroplids, typically dwell in low-energy A possible explanation is that the Dongsha conditions, such as back-reef and lagoonal Atoll had received abundant colonizers from environments (Lidz and Rose 1989; Culver 1990; nearby coastal and coral reefs compared with Murray 2006; Gischler and Moder 2009). They are other remote atolls. The distance from nearby mainly distributed at the lagoon’s northeast and coastal and reef environments to the Dongsha east regions, where tide-induced current is the Atoll is 340-450 km, which is 3-20 times closer lowest. than the distance during occasional long-distance Calcarina species are common and diverse colonization in remote atolls. The constraints on in the Indo-Pacific region and have been typically the colonization distance resulting from diluting associated with Amphistegina, Baculogypsina, effects could be low in the Dongsha Atoll. In Baculogypsinoides, and Schlumbergerella addition, Dongsha Atoll is located at the margin of (Rottger and Kriiger 1990; Yamano et al. 2000; the coral triangle. The rich diversity of species in Murray 2006; Renema 2008). Baculogypsina, this study is consistent with the pronounced central Baculogypsinoides, and Schlumbergerella have Indo-Pacific center of diversity in scleractinia (Veron restricted distribution in the west Pacific and Indo- Zoological Studies 56: 20 (2017) page 12 of 16

Malay Archipelago (Langer and Hottinger 2000; broad ecological response of their functional Bicchi et al. 2002; Parker and Gischler 2011). trophic groups and the ecological record they Their rarity and absence in the present study leave in the sediments can enable identification and at other reef islands in the SCS (Zheng and of the duration and timing of eutrophication in Zheng 1978; Zheng 1979) are in accordance with coral reef ecosystems (Hallock et al. 2003). A previous predictions. However, Zheng (1980) second advantage of using foraminifera in reef reported abundant Baculogypsina spinosa in the assessment is their short life span. Measurement submerged bank of the Zhongsha Islands. The of foraminiferal assemblages can facilitate varying distribution patterns of these three genera differentiation between long-term reef decline remain unclear. The differences may result from associated with water quality and episodic the high dispersal ability of the longer zygotic stress events (Hallock et al. 2003). In addition, stage of Calcarina (Lessard 1980; Bicchi et al. foraminifera are more sensitive than coral to 2002). Alternatively, Parker and Gischler (2011) water quality changes (Uthicke et al. 2010). The suggested that Calcarina has a longer expansion communities and coverage of corals and algae period than other genera of calcarinids because are influenced by numerous factors, such as coral Calcarina is known to be from the Middle Miocene, diseases, tropical storms, herbivorous predation, and the other genera are much younger. and light attenuation (Jackson and Knowlton Discoidal soritids, known as the most common 2001). Foraminifera are not affected by the same foraminifera in coral reef environments, were not diseases as corals, and their assemblages recover dominant in the Dongsha lagoon. During field quickly after bleaching events and storms. A sampling, A. hemprichii was observed to attach foraminiferal community is largely influenced by itself to the leaves of seagrass and to encrust water quality (Uthicke et al. 2010). coralline algae of coral rubble. This is in agreement According to the total foraminiferal with its known optimal habitat in coral reef assemblages, most FIs were between 2 and 3 environments in the Pacific Ocean (Hohenegger in the Dongsha lagoon. A basic premise for the 1994; Saraswati 2002). High abundances of formula for the FI is that 100% heterotrophic taxa Amphisorus and Calcarina can be associated with give an index of 2, and additions of symbiont- seagrass meadows that are densely distributed in bearing taxa increase the FI to 10 (Hallock et al. the shallow and western regions of the Dongsha 2003). The low index was caused by the high lagoon (Lin et al. 2005). abundance of heterotrophic taxa that made up Although stress-tolerant species of Bolivina, 82% of the benthic foraminiferal assemblages in Ammonia, and Elphidium were common in the the Dongsha lagoon. Dongsha lagoon, their prevalence was low. An FI between 2 and 4 represents a marginal These species are typically found in lagoons with environment for mixotrophs and is unsuitable for low to normal salinity (Murray 2006). Their low coral growth and recovery after a stress event abundance indicates that environmental pollution is (Hallock et al. 2003). The low FI is in accordance rare in the Dongsha lagoon. Human activities, such with live reef assemblages in the Dongsha lagoon. as sewage disposal, fish farming, and uncontrolled These sampling stations have low coral cover (on tourism, do not contribute to the degradation of the average, approximately 12.6%), with stress-tolerant Dongsha lagoon. These foraminiferal associations corals, such as solitary fungiids, massive faviids, can potentially be used to monitor anthropogenic and Porites, as well as foliaceous Turbinaria (C. ecological changes of the Dongsha lagoon. A. Chen, personal communication). Studies have reported no significant correlation between the FI Applying the FORAM index in the Dongsha and coral or algae cover in some reefs (Barbosa et lagoon al. 2009; Velásquez et al. 2011). The discrepancy can be attributed to diverse controlling factors Although numerous indicators have been influencing the community composition of coral and applied to evaluate the condition and resilience benthic foraminifera (Narayan and Pandolfi 2010; of reef environments, the use of foraminifera is Uthicke et al. 2010). Thus, the low FI shows that being applied with remarkable success (reviewed water quality does not support calcifying symbiosis in Hallock 2012; Reymond et al. 2012). A major in most benthic environments in the Dongsha advantage of using foraminifera in reef assessment lagoon, suggesting that coral communities exist is that their functional groups represent various but are not likely to recover after a stress event. trophic states of the benthic environment. The Applying benthic foraminifera to evaluate Zoological Studies 56: 20 (2017) page 13 of 16 different habitats of an atoll has not yet been fully Acknowledgments: We thank the Southern explored in the SCS in the literature. Symbiont- Coastal Patrol Office of the Coast Guard bearing foraminifera should be dominant in Administration, Dongsha Atoll National Park, and the fore-reef environment where most coral Dongsha Atoll Research Station for providing calcification occurs. For example, Fajemila field assistance in the Dongsha Atoll; Marine et al. (2016) found that symbiont-bearing Core Repository and Laboratory of Taiwan Ocean foraminifera generally live in the fore- and back- Research Institute, National Applied Research reef environments of Moorea. Our unpublished Laboratories for laboratory tasks; CA Chan and data revealed that fore-reef environments his team member for providing coral community have abundant symbiont-bearing foraminifera, information; and anonymous referees for constituting approximately 70% of the RA in the constructive comments. This study was supported Dongsha Atoll (manuscript in preparation). by grants from the National Science Council The ecological and environmental Grant (NSC-102-2621-B-492-001) and Ministry applications of the FI have been surprising of Science and Technology (MOST) (MOST 103- since its introduction. Hallock et al. 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Appendix 1. Foraminiferal species list. Stars indicate consistently occurring species that were found in more than half of sampling locations. (download)