The distribution of meiofauna on back‐reef sandy platforms in the Maldives (Indian Ocean)

ORIGINAL ARTICLE

The distribution of meiofauna on back-reef sandy platformsin the Maldives (Indian Ocean)Federica Semprucci1, Paolo Colantoni2, Giuseppe Baldelli2, Marco Rocchi1 & Maria Balsamo1

1 Dipartimento di Scienze dell’Uomo, dell’Ambiente e della Natura (DiSUAN), Universita di Urbino ‘Carlo Bo’, Urbino, Italy

2 Dipartimento di Scienze Geologiche, Tecnologie Chimiche e Ambientali (DiGeoTeCA), Universita di Urbino ‘Carlo Bo’, Urbino, Italy

Problem

In tropical regions, most meiofauna research has been

carried out in the Pacific Ocean (Ndaro & Olafsson 1999;

Raes et al. 2007 and references within). Given the pres-

ence of heterogeneous coral reef structures and carbonate

sediments, atolls offer a wide variety of micro-habitats for

meiofauna. Despite this, relatively few quantitative studies

have been published on the shallow sublittoral sandy sedi-

ments of atolls (Netto et al. 1999a,b; Guo et al. 2007 and

references within).

Determinant variables that can influence the meioben-

thic assemblage include: mean sediment grain size, sort-

ing, oxygen content, position of the redox potential

Keywords

Back-reef platforms; free-living nematodes;

Maldives; meiofauna; sediment grain size.

Correspondence

Federica Semprucci, Dipartimento di Scienze

dell’Uomo, dell’Ambiente e della Natura

(DiSUAN) Universita di Urbino ‘Carlo Bo’, loc.

Crocicchia – 61029 Urbino, Italy.

E-mail: [email protected]

Accepted: 6 April 2010

doi:10.1111/j.1439-0485.2010.00383.x

Abstract

The Maldivian archipelago comprises some of the most characteristic and

significant world atoll systems, but the meiobenthic assemblages of these

islands continue to be largely unknown. To investigate variations in meiofaunal

spatial distribution and biodiversity in back-reef platforms, three transects were

studied, two at Felidhoo (the north and east sides) and one at South Male. The

sedimentological features of the samples obtained were also analyzed to further

current knowledge on the relationships that exist between sediments and meio-

fauna. Our results reveal that the meiofaunal assemblage at these locations is

well diversified and includes 20 major taxa. Nematodes and copepods are dom-

inant, together forming 68% of the total meiofauna, followed by platyhelmin-

thes, polychaetes and ostracods. The nematode assemblage is very rich and

composed of 34 families and 123 genera – 96 of which (78%) set new records

for the Maldives. The structures of the meiofaunal and nematode assemblages

are relatively similar on the ‘large-scale’ level (i.e. when the different platforms

are compared) and reveal a low b-diversity. However, significant dissimilarities

were detected within each platform, emphasizing that such ‘small-scale’ differ-

ences are the main factors determining the structure of the meiofauna and, in

particular, the nematode assemblages. Although significant differences were not

detected between the transects, greater levels of dissimilarity were recognized at

North Felidhoo. Here, the building of inclined deposit layers plays a significant

role in increasing the heterogeneity of the platform habitats and sediments,

confirming the great importance of sediment granulometry as an environmen-

tal variable. Indeed, a close relationship is observed between meiofauna (espe-

cially for the nematodes) and grain size, which appears to control the

structure, diversity and trophic composition of the Maldivian meiofauna

assemblages, thus highlighting the high biodiversity existing in the medium-

coarse sands.

Marine Ecology. ISSN 0173-9565

592 Marine Ecology 31 (2010) 592–607 ª 2010 Blackwell Verlag GmbH

discontinuity (RPD) layer within the sediment, organic

content, the extent of bioturbation by the macrobenthos,

macrofaunal competition and predation, and water depth

(see Giere 2009 for review). Nematodes are usually the

dominant and ubiquitous meiofaunal taxonomic group,

with high densities, especially in fine sediments. Cope-

pods, on the other hand, become progressively more

abundant as grain size increases (Heip et al. 1985).

Accordingly, in tropical coarse sands with low silt con-

tent, harpacticoids usually constitute the most dominant

group, although polychaetes and oligochaetes may also be

present to a substantial degree (see Netto et al. 1999a).

The sediment composition may also play an important

role in controlling meiofaunal assemblage structure. Many

other, often rare, taxa may also occur in carbonate sands.

Indeed, temporary meiofauna and specialized members of

permanent meiofauna are more frequently found in these

sediments, which have been defined by Giere (2009) as ‘a

bonanza of fascinating meiofauna’. These biogenic sedi-

ments are structurally complex, relatively unsorted and

possess high porosity. The permeability of calcareous sand

has been proved to be markedly higher than that of sili-

ceous sand. High permeability favours the absorption of

nutrients, which gives rise to rich organic matter and

large quantities of microorganisms, two important feeding

resources for the meiofauna (Wild et al. 2005; Dahms

et al. 2007).

The Maldive Islands form the central part of the Cha-

gos-Maldives-Laccadive ridge in the Central Indian Ocean

and comprise some of the most characteristic and signifi-

cant atoll systems (Risk & Sluka 2000); their back-reef

platforms consist entirely of carbonate sediments, unlike

those of the Pacific Atolls. In spite of the great interest in

this archipelago, the information available about its meio-

fauna is mostly taxonomic (Gerlach 1961, 1962, 1963a,b,

1964; De Zio Grimaldi et al. 1999; Gallo et al. 2007). For

these reasons, a study of the meiofaunal and nematode

assemblages from three Maldivian back-reef sandy plat-

forms was conducted. Meiofauna were collected from

different geographical locations that are also characterized

by different geomorphological features: two transects were

placed on the Felidhoo atoll (north and east sides) and

one on South Male. The aims of the study were: (i) to

investigate the spatial patterns of the meiofaunal assem-

blages and biodiversity on a ‘small’ and ‘large’ scale in the

Maldives (i.e. within and between the platforms, respec-

tively) and (ii) to improve our understanding of the rela-

tionships that exist between meiofauna and sediment

types.

Study Area

The Maldive Islands rise up in the tropical Indian Ocean,

south-west of India, as a shallow carbonate system com-

posed of a chain of atolls which extend for approximately

800 km along the 73� meridian, between 7�06¢ N and

0�42¢ S (Fig. 1A,B). Their geological history is marked by

a complicated succession of sea-level changes, construc-

tions and erosions (Aubert & Droxler 1992) which have

given rise to carbonate sediment deposits that are over

A

B C

D

E

Fig. 1. Geographic location of the study

area and the sampling transects.

Semprucci, Colantoni, Baldelli, Rocchi & Balsamo Meiofaunal distribution in Maldives

Marine Ecology 31 (2010) 592–607 ª 2010 Blackwell Verlag GmbH 593

2000 m thick above an ancient and subsided volcanic

substratum (Duncan & Hargraves 1990). Seismic reflec-

tion profiles (Aubert & Droxler 1996) and the presence of

widespread terraces, notches and caves (Bianchi et al.

1996; Colantoni et al. 2003) reveal that the eroded sur-

faces, formed during the last Pleistocene glacial sea-level

low-stand, largely govern the shape of the present reef

formations. At the top of many of them, the reef flats are

wide or stunted, but are always accompanied by biogenic

sand and rubble, which accumulate and form ribbons and

low islands, especially during high energy wave-generated

events (Kench et al. 2005).

Sampling operations were carried out between 19 and 21

May 2005, during a scientific cruise organized by Albatros

Top Boat. Samples were collected in the South Male and Fe-

lidhoo Atolls (Central Eastern Maldives Archipelago) along

three transects located on their eastern rims (see Fig. 1).

The South Male transect (T1) (3�52.396¢ N–

73�27.531¢ E) ran seawards (direction 90�N) from the tip

of the narrow island of Maadhoo, which lies at the north

end of a large reef (Maadhoo Falhu) in the South Male

Atoll (Fig. 1C). This island was once one of the largest and

most populated islands of the Atoll, but it has now been

almost completely washed away (Godfrey 1996). Going off-

shore from the narrow beach, and furrowed by eroded

notches, a strip of outcropping beach rock was present. The

short foreshore, ending with scattered patches of elevated

sea grass beds (Cymodocea spp.), is followed by a large and

gentle sub-tidal sandy plain which reaches the reef flat as

far as 900 m from the shore. Samples were taken from six

stations positioned along this transect (Fig. 2A).

The North Felidhoo transect (T2) (3�33.600¢N–73�29.859¢ E) started at a sandy cay (or finolhu) on

Kudadhiggaru Falhu, a wide reef in the vicinity of the

large island of Alimathaa, near the southern edge of a pass

(kandu). Proceeding in a direction 50� N, T2 reached the

outside rim of the Felidhoo Atoll (Fig. 1D), and crossed

the sandy floor of a wide depression that is in the process

of being filled by advancing inclined coarse sandy layers.

Seven stations were analyzed along this transect (Fig. 2B).

A

B

C

Fig. 2. Section of the three transects and station locations.

Meiofaunal distribution in Maldives Semprucci, Colantoni, Baldelli, Rocchi & Balsamo


The East Felidhoo transect (T3) (3�28.888¢N–73�42.200¢ E) crossed the Fotteyo Finolhu, a sandy

body 105 m from the reef edge on the northern side of

the pass, between Dhiggaru and Fotteyo Falhu, at the

eastern end of the Felidhoo Atoll (Fig. 1E). At this point,

the drop-off is only 1.5 m deep and is characterized by a

gentle rocky slope with blocks (Fig. 2C). Five stations

were sampled along this transect.

Material and Methods

Sample processing

At each station, samples for the quantitative analysis of

the meiofauna were collected by a SCUBA diver using a

hand-held piston corer (surface area 6 cm2) driven to a

depth of 5 cm and collected in triplicate. A fourth sam-

ple, intended for sediment analysis, was collected at each

station. Samples destined for meiofaunal analysis were

narcotized with a 7% magnesium chloride aqueous solu-

tion, fixed using a 4% formaldehyde solution (in buffered

seawater), stained with Rose Bengal and stored for subse-

quent processing.

The meiofauna were obtained by sieving the samples

through a 42-lm-mesh net, and animal extraction was

performed by flotation and multiple decantations. Centri-

fugation through a silica gel gradient (Ludox HS 30, den-

sity 1.18 gÆcm)3) was only carried out for samples with

fine sediments (Pfannkuche & Thiel 1988). The animals

were then transferred to a ‘Delfuss’ Petri dish with a

checkered bottom (200 squares, to make counting easier),

sorted into their major taxa under a Leica G26 stereomi-

croscope, and counted. About 100 nematode specimens

from each replicate were picked at random, placed in

glycerine and mounted as permanent slides. Identification

at the genus level was performed using a light microscope

equipped with Nomarski optics (Optiphoto-2 Nikon) and

aided by the pictorial keys of Platt & Warwick (1983,

1988), Warwick et al. (1998), the NeMys online identifi-

cation key (Deprez et al. 2004), and papers published by

Gerlach (1962, 1963a,b, 1964). Nematode trophic groups

were also defined according to Wieser (1953): 1A, selec-

tive deposit feeders; 1B, non-selective deposit feeders; 2A,

epistratum feeders; 2B, predators ⁄ omnivores.

Grain size analysis was performed on the collected sedi-

ments using a vibro-siever for fractions larger than 63 lm

and an X-ray analyzer for those smaller than 63 lm.

Using the percentages of each granulometric class

(defined at intervals of 1 u as the )log2 d mm; Krumbein

1934), histograms and cumulative curves were created,

from which percentiles were calculated; these measure-

ments were subsequently used to provide a statistical

characterization of the samples (according to Folk &

Ward 1957). The sediments were classified in accordance

with the Wentworth scale (Buchanan 1984).

Data analysis

Non-metric multi-dimensional scaling (nMDS) ordina-

tions derived from Bray–Curtis similarity matrices were

used to view differences in the structures of meiofaunal

and nematode assemblages between the stations located

in the different transects (on � transformed data). A two-

way nested ANOSIM (analysis of similarities) was used to

assess the statistical significance of any differences

between the transects and the stations. The SIMPER test

(cut-off of 50%) was utilized to determine the contribu-

tion of each meiofaunal taxa or nematode genus to the

total dissimilarity. Shannon’s diversity (H¢) and evenness

(J) indices (log2) were calculated to describe the nema-

tode assemblage structure. b-diversity (i.e. turnover diver-

sity, estimated as a % of Bray–Curtis dissimilarity; see

Gray 2000) was estimated using SIMPER and nMDS anal-

yses to provide a measure of genera dissimilarity between

the different transects and stations; a two-way nested

ANOSIM was used to assess the statistical significance of

any differences identified. All absolute data were pres-

ence ⁄ absence-transformed for the estimation of b-diver-

sity. An additional visual representation of diversity was

provided by a k-dominance curve, in which the abun-

dance of each genus was ranked in decreasing order of

dominance and cumulatively plotted. To evaluate the sig-

nificance of the differences in the meiofaunal and nema-

tode assemblages in relation to the sediment types

(irrespective of the station or transect of origin), a one-

way ANOSIM was used (on � transformed data). All of

the analyses referred to above were performed using the

software package PRIMER v. 5 (Clarke & Gorley 2001;

Clarke & Warwick 2001). Possible differences in the uni-

variate measures (Shannon, H¢, and Pielou, J, indices)

and in the abundance of nematode trophic groups were

evaluated using an analysis of variance (ANOVA). Prior

to statistical analysis, the logarithmic transformation

log(1 + x) was performed to normalize the data. Tukey’s

multiple-comparison tests were used when significant dif-

ferences (P < 0.05) were detected. Spearman’s correlation

analysis was utilized to test for significant correlations

between the various biological and sediment parameters

(SPSS v. 12 program).

Results

Sediment distribution

At South Male, the samples collected from St. 1 ⁄ 1(located on the foreshore) contained moderately sorted,



very coarse sands; those from St. 1 ⁄ 2 (situated amongst

the sea grasses) contained coarse and poorly sorted sand

(Fig. 2A; Table 1). Turning seawards, all of the remaining

stations (St. 1 ⁄ 3, 1 ⁄ 4, 1 ⁄ 5 and 1 ⁄ 6) were characterized by

poorly sorted, medium and coarse sands, with a ‘tail’ of

coarser material that is highlighted by their negative

asymmetries (Table 1). The sub-tidal beach of the finolhu

at North Felidhoo (St. 2 ⁄ 1 and 2 ⁄ 2) contained poorly

sorted, gravelly sands (Fig. 2B; Table 1). The deeper

depression which followed was covered by fine sands (St.

2 ⁄ 3 and 2 ⁄ 4), while the infilling inclined layers (St. 2 ⁄ 6)

were composed of moderately sorted, very coarse sands.

Towards the reef (St. 2 ⁄ 7, 2 ⁄ 8), the sea floor was covered

by coarse and medium sand (Table 1). Between the

finolhu and the reef top of East Felidhoo (St. 3 ⁄ 1 and

3 ⁄ 2), poorly sorted, medium sands were present, whilst

towards the lagoon (St. 3 ⁄ 4, 3 ⁄ 5 and 3 ⁄ 6), the sands were

coarse and poorly sorted (Fig. 2C; Table 1).

Meiofaunal and nematode assemblages

The North Felidhoo transect contained the greatest meio-

faunal abundances (on average 2463.62 ± 657.88

indÆ10 cm)2), whereas the values detected at the South

Male and East Felidhoo transects were lower and similar

(on average 1270.69 ± 375.70 and 1355.71 ± 353.34 indÆ10 cm)2, respectively) (Fig. 3). Overall, the meiofaunal

community appeared to be rich, with a total of 20 major

taxa present (Table 2). Copepods (adults and nauplii) and

nematodes were dominant in all transects and together

accounted for an average of 68% of the total meiofauna.

Other prevalent taxa were platyhelminthes, polychaetes

and ostracods, each one accounting for more than 3% of

the total assemblage (Fig. 4). Nematodes were only clearly

dominant at St. 2 ⁄ 3 and 2 ⁄ 4 (accounting for 89% and

63% of total assemblages, respectively), whereas the cope-

pods were particularly dominant at St. 2 ⁄ 6 and 2 ⁄ 1 (89%

and 77% of total assemblages, respectively), and, to a

lesser extent, at St. 1 ⁄ 6 and 1 ⁄ 1 (76% and 60%, respec-

tively) (Fig. 4A,B).

There were greater differences in the meiofaunal assem-

blage between the stations than between the transects

(ANOSIM, R = 0.61; P = 0.001, and R = 0.18; P = 0.023

for stations and transects, respectively). This phenomenon

is also visible in the nMDS plot of the meiofaunal assem-

blage (Fig. 5A), where the three transects did not appear

to be clearly separate despite the stations of the North

Felidhoo transect being the most scattered. Differences

between the meiofaunal assemblages relating to sediment

type were also found (ANOSIM, R = 0.34; P = 0.001)

(Table 3). The nematode community was well diversified

(H¢ from 4.62 to 2.16; J from 0.94 to 0.68) (Fig. 6), with

Table 1. Grain size parameters at each station.

station water depth (m) gravel % sand % pelite % mode Md mean size Mz sorting d skewness Sk1 kurtosis KG

1 ⁄ 1 0.50 15.32 83.02 1.66 0 0.00 1.08 0.10 0.98

1 ⁄ 2 0.90 6.49 86.21 7.30 1 1.03 1.78 0.27 1.31

1 ⁄ 3 0.60 3.49 94.41 2.10 2 0.99 1.22 )0.03 0.89

1 ⁄ 4 0.70 0.09 93.60 2.31 2 1.33 1.18 )0.15 0.98

1 ⁄ 5 0.50 9.77 85.61 4.63 2 0.87 1.52 )0.03 1.13

1 ⁄ 6 0.40 16.03 76.99 6.98 2 0.94 1.96 0.02 1.07

2 ⁄ 1 0.80 11.57 88.36 0.07 1 0.23 1.02 )0.12 1.07

2 ⁄ 2 1.30 14.25 82.76 2.98 1 0.53 1.37 )0.06 0.94

2 ⁄ 3 3.50 1.01 89.06 9.93 4 2.27 1.75 )0.01 1.12

2 ⁄ 4 5.00 0.11 95.18 4.71 3 2.81 0.82 0.03 1.01

2 ⁄ 6 1.50 16.61 82.03 1.36 0 )0.22 0.96 0.22 1.21

2 ⁄ 7 1.50 4.77 94.94 0.30 1 0.71 1.14 0.00 0.90

2 ⁄ 8 1.10 9.23 89.35 1.42 2 1.19 1.38 )0.20 0.98

3 ⁄ 1 0.60 2.40 92.99 4.61 3 1.67 1.33 )0.17 1.12

3 ⁄ 2 1.50 1.54 96.47 2.00 2 1.90 0.97 0.00 1.09

3 ⁄ 4 0.90 7.89 90.85 1.27 1 0.70 1.27 )0.02 1.02

3 ⁄ 5 1.20 8.47 90.75 0.77 1 0.76 1.24 )0.09 1.08

3 ⁄ 6 1.40 7.29 85.43 7.27 1 0.67 1.63 0.19 1.51

Fig. 3. Meiofaunal abundances at each sampling station.



123 nematode genera belonging to 34 families (for a list

of all of the genera identified, see Appendix 1). Desmodo-

ridae and Chromadoridae were the richest families, with

16 and 14 genera present, respectively; the most abundant

families were Desmodoridae (26%), Chromadoridae

(13%), Xyalidae (12%) and Draconematidae (7%).

At South Male, 72 genera and 26 families of nematodes

were found; the most abundant genera were Spirinia, Mic-

rolaimus, Prochromadorella, Eubostrichus, Paradesmodora

and Chromaspirinia (SIMPER, 50%). At North Felidhoo,

93 genera and 27 families of nematodes were recorded;

Spirinia, Dracognomus, Prochromadorella, Viscosia, Stylo-

theristus, Paradesmodora and Eubostrichus were the most

abundant genera (SIMPER, 50%). Finally, at East Felid-

hoo, 98 genera and 30 families were found, which were

mainly represented by Microlaimus, Desmodora, Paradesm-

odora, Eubostrichus and Spirinia (SIMPER, 50%).

Significant differences in the nematode community

were detected between the stations (ANOSIM, R = 0.67;

P = 0.001), but not between the transects (P > 0.05)

(Fig. 5B). However, SIMPER tests revealed that the great-

est assemblage dissimilarity was at North Felidhoo, which

had the highest dissimilarity values whether comparisons

were made between the stations at North Felidhoo or

between the different transects (Table 4). Similarly, b-

diversity only revealed significant differences between sta-

tions (ANOSIM, R = 0.69; P = 0.001), indicating that the

greatest dissimilarity in genus composition was at North

Felidhoo (Table 4; Fig. 7).

Regarding the Shannon and Pielou indices of nema-

todes, no significant differences were identified between

the three transects (ANOVA, P > 0.05), even though the

H¢ index was, on average, lower at North Felidhoo,

whereas significant differences were found between the

stations (ANOVA, F17,53 = 7.30 and 3.78 P < 0.001)

(Fig. 6).

Differences in the structure of the nematode assem-

blages relating to sediment type were detected (ANOSIM,

R = 0.47; P = 0.001) (Table 3), and the main nematode

genera responsible for the majority of the average similar-

ity within each sediment type are set out in Table 5. The

assemblages were found to be significantly different in all

of the sediment type pair-wise comparisons. In particular,

the greatest differences were detected between the assem-

blages found in the very coarse versus the fine sands,

while the least differences found were between coarse ver-

sus medium sands [Group (Gr.) CS versus Gr. MS]

(Table 5). The differences between the coarse versus the

medium sands were mainly due to the greater abundance

of the genus Dracognomus in the former and the Desmo-

doridae genera in the latter.

The H¢ and J indices differed according to sediment

type (ANOVA, F3,53 = 5.63 P < 0.01; F3,53 = 10.48

P < 0.001) and had significantly lower values in fine

sands (Tukey’s test P < 0.01). This confirms the results of

the k-dominance curve, whereby a visual trend of nema-

tode diversity can be observed: the greatest dominance of

nematode genera was detected in the fine sands followed

Table 2. Presence (X) ⁄ absence (–) of the different meiofaunal taxa found at each station.

taxa

South Male North Felidhoo East Felidhoo

1 ⁄ 1 1 ⁄ 2 1 ⁄ 3 1 ⁄ 4 1 ⁄ 5 1 ⁄ 6 2 ⁄ 1 2 ⁄ 2 2 ⁄ 3 2 ⁄ 4 2 ⁄ 6 2 ⁄ 7 2 ⁄ 8 3 ⁄ 1 3 ⁄ 2 3 ⁄ 4 3 ⁄ 5 3 ⁄ 6

Cnidaria X – – – – – X – – – X – – – – X X –

Turbellaria X X X – X X X X X X X X X X X X X X

Nemertea X X X X X X X X X X X – X – X X X X

Nematoda X X X X X X X X X X X X X X X X X X

Gastrotricha X X X X X X X X X X X X X X X X X X

Kinorhyncha – – – – – – – – X – – X – – – – X X

Opistobranchia – – – – – – – – – – – – – X X – X –

Polychaeta X X X X X X X X X X X X X X X X X X

Oligochaeta X X X X – X – – X X X X X X X X X X

Copepoda X X X X X X X X X X X X X X X X X X

Ostracoda X X X X X X X X X X X X X X X X X X

Isopoda – – – – – – – X – – – – X – – – – –

Tanaidacea X X – – – – – – – – X – – – – – – –

Amphipoda – X – – – – – – – – X – – – – – – X

Cumacea X – – – – – – – – – – – – – X – – X

Halacarida X X X – X – X X X – – X X X X X X X

Tardigrada X X X X X X X X X X – X X X X X X X

Chironomida larvae X – – – – – – – X – X X

Sipunculida – – – – – – – – X – – – – – – – X –

Chaetognatha – – – – – – – – – – – – – – – – X –



by the very coarse sands, while coarse and medium sands

had very similar k-dominance curves (Fig. 8). The Spear-

man rank correlations for the nematode genera and the

main sedimentological parameters are set out in Table 6.

The overall nematode assemblage was predominantly

made up of epistrate feeders (56% of total assemblage),

followed by non-selective and selective deposit feeders

(17% and 16%, respectively) and predators ⁄ omnivores

(12%) (Fig. 9). The nematode trophic groups were also

found to be differentially distributed between the different

sediment types. In particular, 1B (non-selective deposit

feeders) showed the greatest differences (ANOVA,

F3,53 = 29.09; P < 0.001) and were the most abundant in

fine sands (Tukey’s test P < 0.001). A significant differ-

ence was also detected for 2B (predators ⁄ omnivores)

(ANOVA, F3,53 = 4.99; P < 0.01), which was the most

abundant in medium sands (Tukey’s test P < 0.01). Selec-

tive deposit feeders (1A) were significantly abundant in

coarse sands (ANOVA, F3,53 = 3.21 P < 0.05; Tukey’s test

P < 0.05), whereas no significant differences were

detected for 2A (epistratum feeders).

A

B

C

Fig. 4. Composition of meiofauna at each sampling station (Ne,

nematodes; Co, copepods; Po, polychaetes; Tu, turbellarians; Os,

ostracods; Oth, Others).

A

B

Fig. 5. nMDS plot of the meiofaunal (A) and nematode (B) assem-

blages (square root-transformed) (stress coefficient: 0.13). The

sampling grouping was based on Bray–Curtis clustering.

Table 3. Results of one-way ANOSIM (global R) on the meiofaunal and

nematode assemblages for the different sediment type comparisons.

meiofauna nematodes

R P R P

global 0.34 0.001 0.47 0.001

coarse sand versus very coarse sand 0.56 0.006 0.59 0.009

coarse sand versus medium sand 0.13 0.028 0.19 0.007

coarse sand versus fine sand 0.55 0.001 0.73 0.001

medium sand versus very coarse sand 0.73 0.005 0.99 0.001

medium sand versus fine sand 0.35 0.004 0.78 0.001

fine sand versus very coarse sand 0.98 0.012 1.00 0.012



Discussion

A high number of meiofauna taxa, some of them rare,

were found in this study, demonstrating the great diver-

sity of the interstitial fauna in the Maldives. The finding

of a chaetognath species at Fotteyo Finolhu was particu-

larly interesting, as only two meiobenthic species of this

phylum have been identified to date (Kapp & Giere

2005). A great richness in nematode genera was also

found, and the presence of a remarkable 96 of 123 genera

set ‘new records’ for the archipelago. A notable overlap in

generic composition can be observed between the Maldi-

vian nematode assemblage found in this study and those

reported for other tropical and even temperate areas

(Heip et al. 1985; Alongi 1986; Gourbault & Renaud-

Mornant 1990; Gourbault et al. 1995; Boucher 1997;

Ndaro & Olafsson 1999; Raes et al. 2007). The distribu-

tion of some genera across a broad range of different

habitats, and even geographically distant areas, not only

proves the wide distribution of these taxa, but also the

existence of iso-communities that mainly associate with

specific sediment grain sizes (Raes et al. 2007). Indeed, all

of the families that appeared to be dominant in this study

are found in coarse sands, confirming the independence

of the community structure with respect to latitude, and

its main relationship with the granulometry or microhab-

itat type (Heip et al. 1985; Raes et al. 2007, 2008).

The Maldivian sea floor has a continuous supply of

originally biogenic sediments of different sizes. Due to the

inadequate distances and transport times involved, waves

and currents are not able to rework and select these sedi-

ments to any significant degree. Consequently, the granu-

lometric statistical parameters (i.e. mean grain size,

sorting, skewness and kurtosis) are less indicative of the

hydrodynamic conditions than those of the terrigenous

sediments. Nevertheless, some considerations can be taken

into account to explain the distribution of the assem-

blages.

Our study suggests that the Maldivian back reef plat-

forms are all relatively similar in terms of meiofaunal

assemblage structure, even when spatially separated (i.e.

located on opposite sides of the same atoll, or even on

different atolls), and geomorphologically different. This

was especially evident for the nematode assemblage,

which had greater b-diversity within individual platforms

(i.e. on a ‘small-scale’) than between platforms (i.e. on a

‘large-scale’). In general, the occurrence of species extinc-

tion or migration does not necessarily have to result in

Fig. 6. Shannon–Wiener (H¢) and Pielou (J)

index values for the nematode assemblages

at each sampling station. *Significant

difference, where P < 0.05 (Tukey’s test).



the overall loss of that species from the surrounding area;

i.e. the same species could continue to be present in other

patches within the same area. Accordingly, an overall

higher level of species similarity, and consequent lower

b-diversity, should be observed on the larger spatial scale.

In contrast, on the small-scale level, species extinctions or

migrations might equate to the total loss thereof from an

area, resulting in the local disappearance of the species

when too few patches of a habitat remain (high b-diver-

sity). This might be due to predation or competition, or

other effects of patch dynamics that are related to spatial

heterogeneity, which on a small-scale can have a major

impact (Raes et al. 2007). However, it is interesting to

note that, even though significant differences were not

detected, North Felidhoo was the area with the greatest

degree of assemblage dissimilarity. This is most probably

due to the fact that the transects of South Male and East

Felidhoo were located on the sandy parts of the reef flats,

whereas the North Felidhoo transect was on a filling-up

karst Pleistocene depression (Fig. 2). Here, two deposi-

tional features were visible: (i) the presence of fine depos-

its at the bottom of the depression, and (ii) the presence

of advancing inclined layers of coarse sands, due to a

continuum of sediment supply from storm events. These

features would have contributed to the increased hetero-

geneity of the platform’s habitat in line with the structure

and composition of the studied assemblages. It is worth

noting that the greatest dissimilarities calculated were

always found when more weight was given to the abun-

dance of nematode genera and the common taxa (�transformed). This highlights that the dissimilarities were

mainly caused by the different contributions of the genera

to the whole community, rather than by the presence of

unique and very specific taxa restricted to a particular

atoll, platform or station (Table 4).

The influence of sediment grain size on the meiofauna

assemblages was further investigated by ordering the sam-

ples according to sediment type. When sediment types are

ordered irrespective of the station or transect of origin, a

strong relationship exists between nematodes and grain

size, in confirmation of the findings by Vincx (1989). This

is also evident when specimens are identified on the genus

level, in contrast with the observations of Vanaverbeke

et al. (2002) (Table 3). When it comes to explaining even

minor differences in the assemblage structure (see Raes

et al. 2007), the importance of small sedimentological

variations was confirmed: when only the mean grain size

(Mz) was considered, few statistically significant correla-

tions were found in relation to genus; however, when the

granulometric classes were considered, a larger and more

significant number of correlations were identified (Table 6).

Although the assemblages were found to be signifi-

cantly different in all of the pair-wise comparisons, it is

Table 4. Average dissimilarities (Av. Diss.) calculated on nematode

assemblages (SIMPER tests with 50% cut-off). Genera abundances

were square root- and presence ⁄ absence-transformed. Comparisons

were performed between assemblages inhabiting different transects

and between assemblages within the same transect.

groups

square root

Av. Diss.

presence ⁄ absence

Av. Diss.

T1 versus T2 72.0 66.2

T2 versus T3 73.4 68.2

T1 versus T3 65.8 59.1

11 versus 12 59.0 41.7

11 versus 13 54.2 45.4

12 versus 13 59.7 56.5

11 versus 14 65.1 59.3

12 versus 14 64.4 48.0

13 versus 14 60.4 57.1

11 versus 15 45.5 41.8

12 versus 15 65.8 56.5

13 versus 15 57.6 53.9

14 versus 15 59.2 53.6

11 versus 16 62.0 49.3

12 versus 16 55.4 48.2

13 versus 16 56.8 53.1

14 versus 16 58.0 41.2

15 versus 16 59.3 50.0

21 versus 22 61.9 46.9

21 versus 23 90.8 84.0

22 versus 23 77.8 70.5

21 versus 24 91.6 85.4

22 versus 24 85.3 73.1

23 versus 24 48.9 54.7

21 versus 26 69.0 55.5

22 versus 26 73.4 70.2

23 versus 26 91.5 87.5

24 versus 26 87.1 79.5

21 versus 27 76.5 64.0

22 versus 27 48.7 44.3

23 versus 27 80.6 71.0

24 versus 27 86.5 77.4

26 versus 27 73.0 66.7

21 versus 28 81.3 78.0

22 versus 28 51.7 48.4

23 versus 28 70.0 68.1

24 versus 28 78.8 71.8

26 versus 28 77.0 70.0

27 versus 28 55.3 44.7

31 versus 32 55.3 52.3

31 versus 34 46.1 40.9

32 versus 34 48.0 41.1

31 versus 35 58.4 44.1

32 versus 35 54.8 45.7

34 versus 35 49.8 47.8

31 versus 36 62.8 67.2

32 versus 36 55.1 53.9

34 versus 36 56.7 56.0

35 versus 36 61.4 54.9



interesting that the lowest differences were found between

assemblages in coarse versus medium sands (Gr. CS versus

Gr. MS) (Table 3). This is probably due to the fact that

these sediments were mainly occupied by interstitial fauna

(Table 3). In this dimensional range, e.g. in the nematode

assemblage, a greater degree of genera overlap was pres-

ent, highlighting the similar effects of these two sediment

types upon both fauna composition and the relative

contributions of the different taxa.

The nematode genera listed in Table 5 could be

regarded as indicators of the four sediment types found

in this Maldivian study area, which, in turn, provide use-

ful information about the relationship of some taxa with

granulometry. Genera that are known to be typical of

coarse sediment fractions and habitats exposed to high

energy hydrodynamics (Heip et al. 1985; Somerfield et al.

1995; Schratzberger & Warwick 1998; Nicholas & Hodda

1999; Raes & Vanreusel 2006; Raes et al. 2007) were here

identified as being taxa that are indicators of the very

coarse and the coarse sands. On the other hand, the num-

ber of different Desmodoridae genera present increased as

the size of the sediment interstitial spaces decreased (i.e.

Desmodoridae were more prevalent in medium than in

coarse sands). Of the Desmodoridae genera identified,

Table 5. Main nematode genera responsible for most of the average similarity within each sediment type; detected using the SIMPER test (50%

cut-off).

very coarse sand (Gr. VCS) coarse sand (Gr. CS) medium sand (Gr. MS) fine sand (Gr. FS)

Genera Contrib. % Genera Contrib. % Genera Contrib. % Genera Contrib. %

Theristus 1B 8.91 Dracognomus 2A 9.53 Eubostrichus 1A 10 Stylotheristus 1B 30.3

Dracognomus 2A 8.91 Microlaimus 2A 8.41 Microlaimus 2A 8.89 Spirinia 2A 20.11

Chromadora 2A 7.72 Prochromadorella 2A 7.35 Chromaspirinia 2B 8.88

Paracyatholaimus 2A 7.72 Spirinia 2A 7.24 Paradesmodora 2A 7.86

Halalaimus 1A 7.72 Paradesmodora 2A 6.33 Spirinia 2A 7.68

Prochromadorella 2A 6.3 Epacanthion 2B 5.6 Odontophora 1B 4.62

Viscosia 2B 6.3 Eubostrichus 1A 5.46 Desmodora 2A 3.89

Perepsilonema 1A 3.91

Fig. 7. nMDS plot of the nematode

assemblages (presence ⁄ absence-transformed)

(stress coefficient: 0.16). The sampling

grouping was based on Bray–Curtis

clustering.

Fig. 8. k-dominance curves of nematode assemblage for each sedi-

ment type.



Eubostrichus (Stilbonematinae), Eubostrichus cf. parasitifer

and Eubostrichus cf. exilis were the most dominant, and

were primarily correlated with medium sands and

secondly with coarse, poorly sorted sands (Table 6).

Species of Eubostrichus are sediment-dwellers which tend

to penetrate into deeper, anoxic sediments, where they

are able to exploit the high concentrations of sulfide

present around the chemocline by means of their ecto-

symbiotic bacteria (Hentschel et al. 1999; Ott et al. 2005).

Curiously, high abundances of Stilbonematinae have been

frequently reported in subtropical and tropical sediments,

and especially coralline sands (Gerlach 1963a,b; Boucher

1997; Riemann et al. 2003; Raes et al. 2007). The great

abundance of these species in carbonate sediments may

be related to the presence of large grains in generally

sheltered habitats, a condition which represents an unu-

sual combination of wide interstitial spaces and sulfide

conditions with an associated rich thiobios (Riemann

et al. 2003; Giere 2009).

In the fine sands, 50% of the total community was

made up of just two genera (Stylotheristus and Spirinia),

which include species known to be associated with fine

and silty sediments (Heip et al. 1985; Buchholz & Lamp-

adariou 2002). It is also worth noting that the genus

Spirinia, discovered by Gerlach (1963a,b) in the Maldives,

was common in all of the sediment types, except for very

coarse sands. Ndaro & Olafsson (1999) also reported a

widespread presence of Spirinia in all of the sediment

typologies of the Zanzibar lagoons, demonstrating the

general importance of this genus in carbonate sediments,

although in this study a closer relationship with sediment

grain sizes lower than 125 lm was found.

In accordance with the literature, the Shannon (H¢)and evenness (J) indices for the nematode assemblages

were highest in medium-coarse sands and lowest in fine

sands (see also: Heip et al. 1985; Steyaert et al. 1999;

Vanaverbeke et al. 2002). This is confirmed by the

k-dominance curves, which reveal a very similar pattern

for nematode genera dominance in medium-coarse sands

in accordance with the observations on the structure of

the nematode assemblage (Fig. 9). Medium and coarse

sediments are, in fact, richer in micro-niches (see Giere

2009 for an overview) and have relatively large interstitial

spaces. These provide areas for feeding and sheltering, as

well as biofilms and microalgae that grow on the grain

surfaces and are an abundant food source for the meiofa-

una. The uniform diversity pattern of this grain size

dimensional range also proves that the majority of

Table 6. Spearman correlations between the main nematode genera and sediment parameters (including all of the grain size classes).

2000 lm 1000 lm 500 lm 250 lm 125 lm 62 lm <62 lm Mz (mm) d % gravel % sand % pelite

Chromaspirinia )0.12 )0.02 0.00 0.62 0.20 )0.07 )0.05 )0.10 0.21 )0.11 0.24 )0.01

Daptonema )0.55 )0.48 )0.49 )0.07 0.43 0.56 0.26 )0.48 )0.26 )0.54 0.42 0.23

Desmodora )0.16 )0.04 0.02 0.42 0.10 0.06 )0.14 )0.02 )0.04 )0.14 0.27 )0.19

Dracognomus 0.28 0.52 0.52 0.33 )0.45 )0.56 )0.47 0.54 )0.12 0.28 0.00 )0.44

Paradesmodora )0.04 )0.04 )0.05 0.48 0.12 0.00 0.14 )0.03 0.34 )0.02 0.01 0.14

Prochromadorella 0.58 0.46 0.46 0.10 )0.45 )0.65 )0.50 0.56 )0.21 0.59 )0.26 )0.47

Spirinia )0.40 )0.51 )0.42 0.03 0.48 0.53 0.32 )0.55 0.18 )0.41 0.22 0.35

Stylotheristus )0.47 )0.59 )0.58 )0.38 0.49 0.64 0.51 )0.62 0.01 )0.49 0.17 0.51

Trefusia )0.26 0.02 0.12 0.10 )0.01 0.13 0.24 )0.11 0.35 )0.29 0.09 0.25

Zalonema )0.11 )0.28 )0.28 0.27 0.26 0.20 0.04 )0.17 )0.18 )0.10 0.12 )0.10

Eubostrichus )0.17 )0.19 )0.14 0.27 0.20 0.21 0.21 )0.22 0.32 )0.18 0.03 0.21

For values in bold, P < 0.05; for values in bold ⁄ italics, P < 0.01.

Fig. 9. Trophic structure of nematode

assemblages at each sampling station. 1A

(selective deposit feeders); 1B (non selective

deposit feeders); 2A (epigrowth feeders); 2B

(predators ⁄ omnivores).



nematodes are better adapted to an interstitial life strat-

egy. This was particularly evident in the comparison with

the fine sands, which were strongly dominated by few

and tolerant genera (Table 5). An intermediate condition

was present in very coarse sands, and despite this

sediment type represents a selective micro-habitat with

few genera, its indicator genera are all well adapted to the

present conditions, and overall are more equally

represented than in the fine sediments (Raes & Vanreusel

2006).

When it comes to the trophic composition of the nema-

tode assemblage, unlike the other trophic groups, the dis-

tribution of epistrate feeders (2A) was not significantly

different between the sediment types. In fact, epistrate

feeders were a broadly dominant trophic group in all of

the studied areas. They are commonly found in medium-

coarse sands with a very poor fine fraction (Alongi 1986),

and in tropical habitats they can find a high degree of ben-

thic primary production, a great abundance of diatoms,

and wide surfaces suitable for scraping off the algal and

bacterial biofilms (Boucher 1997; Raes et al. 2007). In this

study, predators ⁄ omnivores (e.g. Chromaspirinia, Epacan-

thion, Viscosia and Oncholaimus) were more abundant in

the medium than in the coarser and exposed sands. This is

probably because these species feed on organisms (other

meiofauna or small macrofauna) which take advantage of

the high organic matter content, which generally increases

as grain size decreases (Netto et al. 1999a,b). Furthermore,

some of these genera (e.g. Oncholaimidae genera) are

facultative predators and are able to exploit a wide range

of food resources (e.g. detrital material). In fact, as oppor-

tunistic feeders, predation is merely an additional mecha-

nism to obtain extra food (Moens & Vincx 1997).

The high abundances of selective deposit feeders (1A)

found in coarse sands in this study contrast with data

from other research (Heip et al. 1985; Alongi 1986; Ndaro

& Olafsson 1999). The presence of this trophic group,

typically dominant in the fine sediment fraction, was

probably high in coarse sands due to the presence of

Epsilonematidae (Perepsilonema, Epsilonema, Leptepsilo-

nema) – a family that is particularly well adapted to

high-energy habitat and larger Mz. As expected, non-

selective deposit feeders (1B) were mostly prevalent in

mud fractions that are generally rich in bacteria and par-

ticulate detritus (Alongi 1986). Indeed, the greatest 1B

abundances were detected at the station situated in the

North Felidhoo depression, characterized by high

amounts of pelite and low hydrodynamic conditions.

Acknowledgements

We are grateful to the referees who made constructive

comments and suggestions to improve the manuscript.

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Appendix 1

List of all nematode genera found in the Maldives Archi-

pelago. The genera marked with an asterisk indicate those

recorded for the first time in the Maldives.

Nematode genera

*Actinonema Cobb, 1920

*Aegialoalaimus de Man, 1907

*Alaimella Cobb, 1920

*Ammotheristus Lorenzen, 1977

*Amphimonhystera Allgen, 1929

Anticoma Bastian, 1865

*Ascolaimus Ditlevsen, 1919

*Astomonema Ott, Rieger and Enderes, 1982

*Atrochromadora Wieser, 1959

Axonolaimus de Man, 1889

Bolbonema Cobb, 1920

*Calomicrolaimus Lorenzen, 1976

Camacolaimus de Man, 1889

*Campylaimus Cobb, 1920

*Ceramonema Cobb, 1920

*Chitwoodia Gerlach, 1956

*Chromadora Bastian, 1865

*Chromadorella Filipjev, 1918

*Chromadorina Filipjev, 1918

*Chromadorita Filipjev, 1922

*Chromaspirina Filipjev, 1918

*Cobbia de Man, 1907

*Comesa Gerlach, 1956

Comesomatidae gen. 1

*Coninckia Gerlach, 1956

*Cricolaimus Southern, 1914

Croconema Cobb, 1920

*Cyartonema Cobb, 1920

Cyatholaimidae gen. 1

*Cyatholaimus Bastian, 1865

*Daptonema Cobb, 1920

Dasynemoides Chitwood, 1936

*Demonema Cobb, 1894

Desmodora de Man, 1889

*Desmoscolex Claparede, 1863

*Dichromadora Kreis, 1929

*Didelta Cobb, 1920

*Disconema Filipjev, 1918

*Dracognomus Allen and Noffsinger, 1978

*Dracograllus Allen and Noffsinger, 1978

*Draconema Cobb, 1913

*Epacanthion Wieser 1953

*Epsilonema Steiner, 1927

Eubostrichus Greeff, 1869

*Eurystomina Filipjev, 1921

*Gammanema Cobb, 1920

*Gomphionema Wieser and Hopper, 1966

*Graphonema Cobb, 1898

Halalaimus de Man, 1888

*Halichoanolaimus de Man, 1886

*Innocuonema Inglis, 1969

Appendix 1. (Continued)

*Latronema Wieser, 1954

*Leptepsilonema Clasing, 1983

*Leptolaimus de Man, 1876

Leptonemella Cobb, 1920

*Linhomoeus Bastian, 1865

*Linhystera Juario, 1974

Litinium Cobb, 1920

Longicyatholaimus Micoletzky, 1924

*Marylynnia Hopper, 1977

*Megadesmolaimus Wieser, 1954

*Mesacanthion Filipjev, 1927

Metachromadora Filipjev, 1918

Metacyatholaimus Stekhoven, 1942

*Metalinhomoeus de Man, 1907

*Metepsilonema Steiner, 1927

*Metoncholaimus Filipjev, 1918

*Microlaimus de Man, 1980

*Molgolaimus Ditlevsen, 1921

Monoposthia de Man, 1889

*Monoposthioides Hopper, 1963

*Neochromadora Micoletzky, 1924

*Odontanticoma Platonova, 1976

Odontophora Butschli, 1874

Onchium Cobb, 1920

*Oncholaimellus de Man, 1890

*Oncholaimus Dujardin, 1845

Oxystomina Filipjev, 1921

*Paracanthonchus Micoletzky, 1924

*Paracomesoma Hope and Murphy, 1972

*Paracyatholaimoides Gerlach, 1953

Paracyatholaimus Micoletzky, 1922

Paradesmodora Stekhoven, 1950

*Paralinhomoeus de Man, 1907

*Paralongicyatholaimus Stekhoven, 1942

*Paramonohystera Steiner, 1916

*Parapinnanema Inglis, 1969

*Parodontophora Timm, 1963

*Paroxystomina Micoletzky, 1924

*Perepsilonema Lorenzen, 1973

*Perspiria Wieser and Hopper, 1967

*Polygastrophora de Man, 1922

*Polysigma Cobb, 1920

*Pomponema Cobb, 1917

*Praeacanthonchus Micoletzky, 1924

*Prochromadorella Micoletzky, 1924

*Pselionema Cobb, 1933

*Pseudocella Filipjev, 1927

*Ptycholaimellus Cobb, 1920

*Rhynchonema Cobb, 1920

Robbea Gerlach, 1956

*Sabatieria Rouville, 1903

*Sigmophoranema Hope and Murphy, 1972

*Siphonolaimus de Man, 1893

*Spilophorella Filipjev, 1917

Spirinia Gerlach, 1963

Stilbonema Cobb, 1920

*Stylotheristus Lorenzen, 1977



Appendix 1. (Continued)

*Subsphaerolaimus Lorenzen, 1978

*Symplocostoma Bastian, 1865

*Synonema Cobb, 1920

Tarvaia Allgen, 1934

*Terschellingia de Man, 1888

*Thalassironus de Man, 1889

*Thalassomonhystera Jacobs, 1987

*Theristus Bastian, 1865

*Trefusia de Man, 1893

*Tricoma Cobb, 1893

*Trissonchulus Cobb, 1920

*Tubolaimoides Gerlach, 1963

*Viscosia de Man, 1890

*Xennella Cobb, 1920

Zalonema Cobb, 1920



The distribution of meiofauna on back‐reef sandy platforms in the Maldives (Indian Ocean)

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Transcript of The distribution of meiofauna on back‐reef sandy platforms in the Maldives (Indian Ocean)