Ecology of free-living nematodes from the continental shelf of the central great barrier reef province

Estuarine,

Coastal

and Shelf

Science

(1991) 32,421-438

Ecology of Free-living Nematodes from the Continental Shelf of the Central Great Barrier Reef Province

John H. Tietjen Department Street, New Received

of Biology, York, NY

I6 May

City Gollege of New 10031 U.S.A.

1990 and in revisedform

York,

Convent

25 September

Keywords: nematodes; ecology; diversity; shelf; Great Barrier Reef (Australia)

carbonate

Avenue

at 138th

1990

sediments;

continental

Nematode assemblages from five sites on the continental shelf of the central Great Barrier Reef (GBR) along a transect ranging from inshore muddy quartz to offshore carbonate sands were examined in austral spring (October 1987) and summer (January 1988). Assemblages at all sites were characterized by very even distributions (low dominance) of families, genera and species. Average per cent abundances of the dominant family (Chromadoridae), genus (Theristus) and species (Spilophorella paradoxa), respectively, were 16, 10 and 8”,, of the total number of specimens identified. The diversity of species (H’ = 3~35-408) from the GBR was higher than that normally calculated for shelf nematode assemblages; species richness (SR= 10.64-16.67) and evenness (J’=O82-0.91) values approximate those characteristic of deep-sea nematode assemblages, suggesting equitable exploitation of the interstitial environment on the GBR shelf by many species. This was also indicated by a nodal analysis of the 22 dominant species, which exhibited no strong preference for any particular sediment or site. Nonselective deposit and epistrate feeders were the most abundant trophic types among the nematodes. The abundance of non-selective deposit feeders was significantly greater in the summer than spring assemblages, accompanying differences also observedin the per cent composition of several species. Shortterm fluctuations in species composition and high species diversity of nematodes on the central Great Barrier Reef shelf may be the result of high sediment heterogeneity (caused by cyclones and frequent prawn trawling), a rich bacterial flora, continuous warm temperatures and low macroinfaunal abundance.

Introduction

While much information is available on the ecology of nematodes from temperate continental shelves, comparatively little is known about tropical sublittoral nematodes in general (Salvat & Renaud-Mornant, 1969; Renaud-Mornant et al., 1971; Thomassin et al., 1976; Grelet, 1984; Gourbault & Renaud-Mornant, 1989), and from the Great Barrier Reef (Australia) in particular. A Belgian expedition to the Great Barrier Reef in 1967 resulted in a seriesof largely taxonomic papers on nematodes(Decraemer, 1974u,b, 1975; Decraemer & Coomans, 1978a,b). To date, the only study to focus on the structural and 0272-7:14/91!‘050421+

18 SO3.00/0

@ 1991 Academic

Press Limited

422

J. H. Tiztjw

Hlnchlnbrook Island

i 146’

Figure Barrier

1. Locations of the five sampling Reef Province.

1470

sites on the continental

shelf of the central

Great

functional ecology of nematodes from the Great Barrier Reef is that of Alongi (1986) for Davies Reef; two additional papers by Alongi (1987,199O) have addressedthe ecology of nematodes inhabiting intertidal mangal and sandflat sediments in several estuariesfrom nearby Queensland. The Great Barrier Reef (GBR), especially its inter-reef regions, is the site of a rapidly expanding prawn trawl fishery (Watson & Goeden, 1989). Epibenthic and infaunal communities from several individual reefs in the central GBR area (16-21”s) have been examined (Alongi, 1986; Hansen et al., 1987; Riddle, 1988), and a few studies of trawled macrofauna have been published (Watson & Goeden, 1989), but until recently the only detailed investigation of macroinfauna from the inner shelf region was that of Arnold (1979) for polychaetes. However, in 1989 Alongi reported the results of a comprehensive investigation of several inter-reef stations in the central GBR region that yielded information on abundance and biomassof macro-, meio- and microbenthos, microbial production, sedimentary structures and biogeochemical processes. This paper focuses on the composition, diversity and trophic structure of nematodes inhabiting a gradient of sedimentsacrossthe GBR ranging from inshore terrigenous muds to offshore carbonate sand. The nematodes described in this study were collected from sedimentssampled by Alongi (1989). Methods Sampling

locations

and description

of study area

Five benthic siteswere visited along a transect from Hinchinbrook Island to the inter-reef region between Otter and Britomart Reefs in October 1987 (austral spring) and January 1988 (summer; Figure 1, Table 1). Four of the sites (MS 1, MS 2, OS 3, OS 4) were sampled in both seasons;site IS 5 was sampledonly in January. Site numbers used in this

Ecology of Great Barrier

423

Reejnematodes

1. Location, water depth, number of nematodes identified and mean population densities of nematodes for the five sites sampled on the central Great Barrier Reef continental shelf

TABLE

Site

Latitude i S)

IS5 MS1 MS2 OS3 OS4

18 18 18 18 18

aData from

Alongi

20.2 16.8 13.2 18.2 07.0

Longitude ( E 146 146 146 146 146

19.2 24.4 29.5 34.6 39.5

Depth cm) 15 26 33 42 46

Number of nematodes identified

Mean population density of nematodes ino. 1Ocm ‘:

303 489 553 516 497

310 655 1250 625 500

(1989).

are consistent with those used by Alongi (1989); that publication gives detailed information on sediment composition and other environmental parameters. Sediments along the transect ranged from very fine (OS 4) to medium (MS 1) sands with small amounts of gravel (<6”,,). Mud content was greatest at the inshore site (IS 5; 34”,,). slightly lessat the outermost site (OS 4; 28”,,) and least at the intermediate sites ( < 16”,,). All sediments were poorly to very poorly sorted, and no significant granulometric differencesbetween spring and summer samplesoccurred. Calcium carbonate content was less than30”,, at IS 5,30 to60”,, atMS 1,60to80”,, atMS2andOS 3,andgreater than80”,, at. OS 4 (Alongi, 1989). paper

Sampling

procedures

Two 0.027-m’ Bouma boxcores were taken on each sampling date for meiofaunal samples (Alongi, 1989). The Bouma boxcorer (Bouma & Marshall, 1964) yields an undisturbed sample and is quite efficient for collecting nematodesand other meiofauna. Three plastic: subcores (6.6 cm2 surface area) were inserted to a depth of 10 cm in each boxcore Sediments were preserved in a 5”,, seawater-formalin-Rose bengal (0.5 g 1-l) mixture. In the laboratory, sedimentswere washed through a nest of two sieves,the larger with a mesh opening of 0.50 mm and the smaller with a mesh opening of 0.045 mm. Nematodes retained on the smaller mesh sieve were identified to lowest possible taxon. No worms were found on the 0.50-mm mesh sieve. Abundances of nematodes at each site are summarized in Table 1 and discussedin more detail by Alongi (1989). In rhe Tables and Figures presented in the Results section reference is made to nematode samples. Each sample consists of all the nematodes identified from the two boxcores taken at eachsite in eachseason.BecauseIS 5 was sampledonly in January 1988, a total of nine samples(one from IS 5, two each from the other sites) is given.

Data analysis Cluster analysis of rhe families, genera and speciesfrom the nine sampleswas done using Bray-Curtis similarity coefficients (Bray & Curtis, 1957) and group-average sorting (Clifford & Stephenson, 1975). A cross-relation between normal and inverse classifications, termed nodal analysis and expressed in nodal diagrams (Boesch, 1977) was done

424

J. H. Tietjru

to describe the collection groups on the basis of their characteristic genera (or species) and the genera (or species) on the basis of their patterns of occurrence over the sites (sediments). The comparisons of coincidence are expressed in terms of constancy and fidelity, the equations for which are given in Tietjen (1984). Speciesdiversity wasmeasuredby the Shannon information function (H’) and evenness by J’ (Pielou, 1975). Speciesrichness was estimated by SR= (S- l)/ln n, where S is the number of speciesand n the number of individuals in a sample (Margalef, 1958). Results Families The systematic schemeof Lorenzen (1981) wasused. Twenty-eight known families were identified from the nine samples(Table 2). In addition, some specimenswere identified only to subclass,order or suborder. These were usually represented by one or two specimens; known families comprised at least 95” (, of the individuals in any given sample.Only four families (Chromadoridae, 15.69;,; Desmodoridae, 12.7”,; Comesomatidae, 11.6”,,; and Xyalidae, 11.5”,) had mean relative abundances greater than lo”,,, and on only three occasionsdid the relative abundance of any family in a single sample exceed 20°, (Table 2). Twenty of the 28 families occurred in five or more samples,and 11 (Oxystominidae, Oncholaimidae, Desmodoridae, Chromadoridae, Cyatholaimidae, Selachinematidae, Comesomatidae, Desmoscolecidae,Siphonolaimidae, Linhomoeidae and Xyalidae) were present in all nine samples.Four families (Leptosomatidae, Haliplectidae, Tarvaiidae and Paramicrolaimidae) were found in only one sample. The total number of families per sampleranged from 17 (IS 5) to 21 (OS 3 in January). Cluster analysis revealed that IS 5 (the inshore site) was different from all other sites, whether all nine samplesor only those from January were compared (Figure 2). Sample IS 5 clustered to the main body of eight samplesat 53O,,; it was characterized by greater than average per cent abundances of the Oxystominidae, Ironidae, Chromadoridae and Xyalidae, and less than average per cent abundances of Desmodoridae and Comesomatidae. Affinities among the remaining samplesranged from 67 to 82O,, with some clustering by site (MS 2, OS 3) and others by month (MS 1 and OS 4 January). Genera One hundred and thirty-five genera were identified, 93 of which were known, Twenty of the unknowns were identified to family, 10 to order and 12 were of unknown affiliation. None of the 42 unknown genera were numerically abundant; most were represented by single or few specimens. Twenty-five genera had mean relative abundances 3 1O0of the total number of worms identified (Table 3); thesedominant genera comprised from 621, (MS 2 October) to 78”,, (MS 1 January) of the individuals present in any particular sample. All 25 genera were present in six or more samples,and nine were present in all samples.However, dominance of the nematode assemblagesby any single genus or group of genera was not especially great; Theristus(9.900), Spilophoda (8.1°0) and Halalaimus (6.5”,) were the only genera whose mean relative abundances exceeded 5”,,. Furthermore, per cent abundance of a single genus in any samplewasnever more than 199;, (Spilophorella at MS 1 October), and Spilophorella, Theristus, Halalaimus and Metacomesomawere the only genera whose abundances ever exceeded loo/” at any time (Table 3). Thus the dominant genera tended to be both widely and evenly distributed in the nine samples.

Leptosomatidae Oxystominidae Ironidae Thoracostomopsidae Oncholaimidae Enchelidiidae Trefusiidae Microlaimidae Desmodoridae Chromadorida I Chromadoridae Ethmolaimidae Cyatholaimidae Selachinematidae Comesomatidae Desmoscolecidae Leptosomatidae Haliplectidae Tarvaiidae Aegialoalaimidae Ceramonematidae Paramicrolaimidae Axonolaimidae Diplopeltidae Siphonolaimidae Sphaerolaimidae Linhomoeidae Xyalidae Monhysteridae Monhysterida Unknown

Family

9 1 3 6

1

8 1 4 1 7 2 7 5 1

2 1

6 15 1 2 2

1.49

8.38 0.49 26.62 0.49 10.82 0.98 9.86 3.92 0.49

1.47 0.49

4.41 10.79 0.49 1.47 0.98

B

8.36 2.46 1.47 5.42

A

Oct.

MS1

1 5 1 4

3 1 6 7

1

1 1 1 1 4 9 1 1

3.26 0.54 22.27 6.52

1.09

0.54 054 0.54 1.09 4.89 14.65 0.54 0.54

1 6 1

1.09 10.32 0.54

2.71 5.42 0.54 15.21

2

B

5.97

A

Jan.

7 8 1 2

0.54 2.28

1

1 1 3

1 4 2 2 3 13 1 7 2 8 4 8 1 1

1 6

B

8.16 9.24

1.09

0.54 0.54 2.72

1.09 9.28 2.73 1.08 3.81 20.09 1.09 11.36 1.08 9.15 2.16 5.97 0.54 0.54

0.54 4.34

A

Oct.

MS2

1.69

6-33 11.19 0.53

0.52 1.06 0.53

1.06

2.14 6.34 20.15 1.60 12.75 1.06 4.81 1.60 9.61 1.53 0.53

0.53 8.54

5.33

A

Jan.

3

7 11 1

1 2 1

2

1 1 11 1 5 2 3 1 5 3 1

1 6

6

B

1.14 l-71

12.60 10.12

3.43 1.14

1.14 12.31 0.57 12.31 0.57 10.31 0.57 8.02 2.71 2.85 0.57 0.57 0.57 2.28

0.57 5.15

7.99

A

Oct.

1 2

8 12

4 1

2 8 1 6 1 7 1 5 3 3 1 1 1 2

1 4

11

B

OS3

2.80 8.96 0.56 0.56 1.68

4 13 1 1 3

1 3 2

1 2

0.56 1.12 0.56 2.26 1.12

2 2 8 1 2 1 5 2 5 6 3

I 6

10

B

1.12 2.24 14.58 1.12 11.23 0.56 7.86 1.12 15.16 5.05 1.68

l-68 7.29

8.96

A

Jan.

1.35

8.22 6.32

0.90 0.90 1.81

2

6 8

1 2 2

1 1

6 1 5 1 8 2 3

14.75 2.26 5.87 2.71 10.39 2.26 3.16

0.45 1.36

2 1 14

1 2

8

2.71 3.62 19.70

0.45 2.71

7.77

ABAB

Oct.

OS4

9.87 12.22 1.88

0.47 1.41 0.47

0.94

4.22 2.35 17.38 1.41 1.41

I.41 6.52 0.47 1.88 5.16 10.80 0.94 13.62

5.17

Jan.

8 10 3

1 1 1

2

4 2 9 3 2

2 6 1 2 2 7 1 5

8

5.19

1.56 0.52 6.21 19.66

1.55

0.52

2.59 0.52 5.70 1.66 052

22.23

5.16 3.11

4.66 0.52

15.94 6.84

A

Oct.

IS5

4

2 1 5 8

1

1

2 1 5 3 1

4

2 3

1 1

5 3

B 0.06 7.75 1.03 0.92 6.65 0.47 1.15 2.78 12.73 0.70 15.56 0.67 6.54 1.39 11.59 2.85 l-24 0.06 0.06 0.17 0.99 0.06 0.81 1.23 0.97 0.18 7.05 11.46 0.44 0.47 1.65

Average

Great

2 21 4 6 13 2 4 4 20 1 11 2 11 6 17 12 5 1 1 2 6 1 4 6 3 2 21 37 5 6 12

Total number of species

TABLE 2. Relative abundance (Ai and number of species (Bi for families of nematodes collected in October 1987 and January 1988 in the central Barrier Reef Province shelf samples. Also given are average per cent abundance and total number of species for each family

426

J. H. Tietjen

October

and

January

January

Genera

Figure 2. Cluster nematode families, region. Shown are 1988 (B) as well as

only

Sample

Sample

0 t

analyses (Bray-Curtis similarity coefficient) of the abundances of genera and species in the central Great Barrier Reef continental shelf analyses using nematodes sampled in October 1987 (A) and January analyses using nematodes sampled only in January 1988.

Eighty per cent (107/135) of all genera were monotypic; 34 of these were represented by single specimens.Twenty-three monotypic genera could not be identified below the rank of family. The number of monotypic generaper sampleranged from 2 1 at IS 5 to 40 at MS 2 (October); per cent contribution of monotypic genera averaged 59”,,, and ranged from 51”/, at MS 1 (January) to 68”/b (OS 4 January). Filipjeva, Onyx, Eubostrichus, ? Catanema, Spilophorella, Chromadora, Paralongicyatholaimus, Paracanthonchus, Paracomesoma and Metacomesoma were dominant monotypic genera. The monotypic genera were numerically important, comprising up to 45O’ ,0 of the individuals present in any particular sample (MS 1 October).

11.41 2.72 2.18 2.72 1.63 IO.31 45 23

8.69 1.63 4.35 1.09

0.98 1.47 1.47 0.49 1.47 10.30 56 32

1.62 1.63

5.97 4.35 2.71 2.71 2.17

Jan.

4.89 5.43

0.98

Spirinia

MS1

2.72 1.18 652 63 40

0.54

3.80 4.91 3.28 3.81 1.09 6.01 1.09 4.36 4.37 1.64 4.37 1.64 1.63 0.54 3.82 1.08 1.08 2.18 0.54

Ocr.

MS2

0.53 1.06 1.07 2.13 9.59 52 27

2.67 1.60 3.20 2.67

3.73 6.41 0.53 5.34 3.74 2.14 2.67 3.73 0.53 2.67 1.07 5.88 0.53 2.14

Jan.

1.71 1.14 2.87 5.75 0.57 0.57 518 1.14 1.14 2.87 I,72 0.57 1.72 1.14 0.57 6.89 1.14 8.41 59 35

1.14 2.30 4.59

6.85 4.01

Oct.

6.72 3.37 1.12 1.12

Jan.

1.68 2.81 0.56 1.68 6.72 57 34

2.25 2.25 1.68 4.49 5.05 5.06

1.12 3.93 5.05 3.36 0.56 10.11 1.12

OS3

2.26 2.26 o-45 6.32 55 32

5.41 1.81 0.90 3.62 0.90 3.62 2.71 1.35 4.96 7.24 8.60 0.45 0.90 0.90 0.90 2.26 7.24 1.35 0.45 0.45

Oct.

OS4

7.04 0.47 3.76 0.94 1.88 0.94 8.45 5.17 2.35 0.94 0.47 0.47 4.70 2.82 12.22 41 28

4.69 3.76 0.47

4.20 1.88 2.82 5.16 0.94

Jan.

0.52 1.04 0.52 3.10 3.11 16-59 34 21

3.62 1.04

5.18 2.07

8.88

0.52 2 07

0.52

14.50

Oct.

IS 5

of dominant nematode genera occurring in the Great Barrier Reef samples (genera with average abundances as well as abundance in each sample in October 1987 and January 1988 are given. Total number of genera and sample are also given

1.96 2.46 2.46 18.22 2.46 3.94 1.97 2.95 0.49 2.95 2.46

7.38 2.46 0.98

Halalaimus Mononcholaimus Filipjeva Microlaimus onyx

Eubostrirhus Desmodora Molgolaimus ? Catanema Spilophorella Chromadora Dichromadora Paralongicyatholaimus Paracanthonchus Pomponema Cervonema Sabatieria Paracomesoma Metacomesoma Tricoma Quadricoma Terschellingia Paralinhomoeus Theristus Number of genera Monotypic genera

Oct.

Genus

TABLE 3. Per cent abundance Average per cent abundance, monotypic genera in each

6.50 3.24 1.37 2.54 1.29 2.05 I.73 2.84 2.10 1.94 8.08 I.58 1.74 1.64 1.43 1.14 4.12 3.07 I ,29 1.78 1.06 1.25 2.72 1.84 9.89 135 107

Average

2 l.O”,,). number of

428

J. H. Tietjen

Total number of genera per 100individuals wasused asan index of generic diversity in the samples. The number ranged between 24 (MS 1 January) and 34 (MS 2 and OS 3 October) except for IS 5 (January), which had only 18. Sample IS 5 wasalsodistinguished by its low affinity (34”,,) with the other samples(Figure 2). This low affinity was due mainly to higher than average relative abundances of Halalaimus, Dichromadora and Theristus, and the absenceof Mononcholaimus, Spirinia, Molgolaimus, Chromadora, Pomponema, Filipjeva and Paracanthonchus at IS 5. In addition, several non-dominant genera (Syringolaimus,Pseudopelagonema, Innocuonemaand Neochromadora) weremoreabundant at IS 5 than elsewhere. Some evidence of differences in generic composition between spring (October) and summer (January) sampleswere seen.Among the samplesthat clustered separately from IS 5, two subgroups were present. One was comprised of all January samplesand one October sample (MS 1). Dominant genera tending to be more abundant in October than January included Spirinia, Molgolaimus, ? Catanema and Paracanthonchus; those less abundant in October were Eubostrichus, Sabatieria, Paracomesoma and Metacomesoma. Among non-dominant genera, Marilynia, Cyatholaimus, Metacyatholaimus and Metalinhomoeus were more abundant, and Oncholaimus and Actinonema lessabundant, in October than in January samples. For the nodal analysis, data on frequency of occurrence of dominant genera from those sites for which there were October and January sampleswere pooled, becauserelationships among the five sites were the same, whether all nine samplesor only the January sampleswere compared (Figure 2). Four genera (Halalaimus, Spilophorella, Cervonema and Theristus) had a high constancy at all sites; the first three of these formed an especially tight cluster (78”,,) to which Cervonema was joined at 50”,, (Figure 3). Each remaining genus chained to this group of four. Although highly constant at all sites, the above four genera were not unusually faithful to any one site (all had average fidelity values at each site), In fact, with but few exceptions, fidelity of all the dominant genera tended to be average at all sites (Figure 3). Species

Two hundred and forty-eight specieswere identified; 104 of these occurred in only one sample, and an additional 53 in only two samples. Sixty-one specieshad mean relative abundances 2 0.5O,, of the total number identified (Table 4); these dominant species accounted for 60”,, (OS 3 October) to 810,, (MS 1 January) of the individuals present in any sample. Four species(Desmodora sp. 2, Spilophorella paradoxa, Paralongicyatholaimussp. and Terschellingia sp. 2) were found in all samples,while one (Syringolaimus sp. 1) occurred in only one sample (IS 5). Forty-two speciesoccurred in a majority (at least five) of the samples.IS 5 had the smallestnumber of dominant species(29) and MS 2 (October) the largest (46); numbers in the remaining samplesranged between 34 and 44. Per cent abundancesof the dominant specieswere not very high (Table 4); the top three specieswere Spilophorellaparadora (mean abundance, 8.0S00), Cervonema sp. 1 (3.18O,,) and Microlaimus sp. 1 (2.3”;)). Only three species(S. paradoxa at MS 1 and OS 3 in October; Metacomesoma sp. at MS 1 in January; and Theristus sp. 17 at IS 5) had abundances that ever exceeded 10YO.As was the case for dominant genera, the dominant speciestended to be widely and evenly distributed among the five sites. Cluster analysesrevealed that IS 5 was distinct from all remaining samples,whether all or only January sampleswere compared (Figure 2). Certain dominant specieswere more abundant at IS 5 than elsewhere(Halalaimus sp. 5, Syringolaimus sp. 1, Pseudopelagonema

Ecology

of Great

Barrier

Reef

nematodes

429

Per cent similarity 0

IO

20

30

40

60

80

100

-I

Figure 3. Inverse classification the five central Great Barrier

of dominant nematode genera and their nodal statistics Reef sites. Key to genera: 1, Halalaimus; 2, Mononcholaz-

mus; 3, Filipjeva; 4, Microlaimus; 5, Onyx; 6, Spirinia; 7, Eubostrichus; 8, Desmodora; Molgolaimus; 10, ? Catanema; 11, Spilophorella; 12, Chromadora; 13, Dichromadora; 14, Parafongicyatholaimus; 15, Paracanthonchus; 16, Pomponemu; 17, Cervomma; Sabatieria; 19, Paracomesoma; 20, Metacomesoma; 71, Tricoma; 22, Quadricoma: Terschellingia; 24, Paralinhomoeus; 25, Thrrisrus.

at 9, 18, 23,

sp., Innocuonema sp., Theristus sp. 17), while others were absent (Microlaimus sp. 1, Chromadora sp., Fitipjeva sp., Spirinia parasitzfera, Pomponemu sp. 1, Cervonema sp. 1; Table4). In addition, 25”,, of the speciesidentified from sampleIS 5 were not found in any other samples.The per cent of endemic speciesat IS 5 was 1.5 times greater than that found in any other sample. As wasthe casefor genera, someevidence of differences in speciescomposition between the October and January samplesoccurred. A cluster consisting primarily of October samples(sites MS 2, OS 3 and OS 4) was characterized by greater per cent abundancesof Spirinia parasitifera, Paracanthonchus sp. and ? Catanema sp., and lesserabundances of Microlaimus sp. 1, Paracomesoma sp. and Halalaimus sp. 2, in October than January. However, at MS 1 there were few differences in per cent abundances of speciesbetween the October and January samples;these samplesformed a single cluster weakly linked to the MS 2 and OS 4 January samples(Figure 2). Twenty-two specieshad mean relative abundances 3 1(Ia; the two most abundant species(Spilophorella paradoxa and Cervonema sp. 1) formed one cluster (61 O,,), but no other obvious groups of specieswere evident (Figure 4). Constancy of both speciesat the sites was moderate to high, except for the absenceof Cervonema sp. 1 at IS 5; neither specieswas unusually faithful to any particular site. In addition to Cervonema sp. 1, 10 other dominant specieswere absent at site IS 5, which was further characterized by two

430

3. H.

Tietjen

TABLE 4. Per cent abundance of dominant nematode species (those with average abundances >05”,,) in each central Great Barrier Reef sample, October 1987 and January 1988 MS1

MS2

OS3

OS4

IS 5

Species

Oct.

Jan.

Oct.

Jan.

Oct.

Jan.

Oct.

Jan.

Halalaimus sp. 1 H. sp. 2 H. sp. 5 H. sp. 7 H. sp. 9 Syringolaimus sp. 1 Trileptinae a Mononcholaimus sp. 2 M. bandaensis M. papillatus Pseudopelagonema sp. Filipjeva sp. Trefusia sp. 1 Microlaimus sp. 1 Onyx sp. Spirinia parasitifera s. sp. 2 Eubostrichus sp. Desmodora sp. 2 D. sp. 3 Metonyx sp. Molgolaimus sp. 1 M. sp. 3 ? Catanema sp. Chromadorida I Spilophorella paradoxa Actinonema sp. Chromadora sp. Dichromadora sp. 1 D. sp. 2 Innocuonema sp.

0.98 1.48

2.71 3.26

1.64 0.54 0.54

1.07 1.69

0.57 1.14 0.57 0.57 0.57

1.68

0.90 0.45 1.81

2.82

1.48 1.97

0.54

1.12 1.13

Jan. 0.52 1.04 7.77 1.55

0.45 5.70

0.49 1.48

1.09 3.26 1.09

0.49 0.98 1.49

0.98

2.46 2.46 1.48

0.53 1.07 3.74

2.18 1.63 2.71 2.71 2.17

0.49 0.98 0.49 1.48 0.98 2.49 0.49 18.22

1.09 2.73

0.54 0.54 1.63

0.54 8.69 0.54 1.63 4.35

3.28 0.54 2.73 1.09 4.37 1.64 1.09 1.54 1.09 1.64 1.64 1.64 1.09 4.37 1.09 1.64 0.54 1.09 1.09

0.57

1.68 0.56 0.56

1.14 0.53 0.53 2.14 5.34 3.74 1.07 1.07 2.67 0.53 1.07 4.81

1.81 4.66

0.57 2.30 3.45 1.14 1.14

1.12 0.56 1.12 1.12 3.93 4.49 0.56 1.69

0.53 2.67 1.60 1.07 0.53 5.88

0.94 0.47 1.41

0.57 2.87 0.57 5.75 0.57 0.57

0.56 1.12 10.11 1.12

0.90 1.81 3.62 0.90 1.36 2.26 2.71 0.45 0.90

2.82 1.40 4.69 0.94

0.90 2.26 7.24

0.47

8.60 0.45 0.45 0.90

0.53 1.14

0.45

4.69 1.88 1.41

0.94 7.04 1.88 0.47 3.76

0.52

0.52 2.07

8.80

5.18 5.23 (Continued)

species (Halalaimus sp. 5, Theristus sp. 17) that attained high dominance only at this site (Table 4). At least 16 of the 22 specieswere present at each of the other four sites, where most of them displayed average constancy and fidelity (Figure 4). Species diversity

Speciesdiversity ranged from 3.35 (IS 5) to 4.08 (OS 3 October), with no great differences between the October and January samples (Table 5). Although lowest diversity was associatedwith lowest speciesrichness (IS 5) and high diversity with highest species richness (OS 3 October), speciesrichness was a significant function of evenness(H’= - 0.04 + 4.39 J’, ? = 0.76, P < 0.05) rather than species richness (H’ = 2.88 + 0.06 SR r2= 0.22, P> 0.05). As might be expected in samplesso dominated by monotypic genera, the relationship between generic richness and speciesrichness was quite close(Kendall’s tau=0.86, PCO.05). Trophic

composition

The feeding classification of Wieser (1953) was used. Nematodes were divided into four feeding categories based on their buccal morphology: selective deposit feeders

Ecology

of Great

Barrier

Reef nematodes

431

TABLE 4. (Continued) MS1 Species

Oct.

Neotonchus sp. Paralongicyatholaimrus Metacyatholaimus sp. l’aracanthonchus sp. Pomponema sp. 1 Chrlronchus sp. 1 Cer7~onema spy 1 c. sp. 2 Sabatieria sp. 1 s. sp. 2 s. sp. 4 Paraconresoma sp. Metacomrsoma sp. Lainrellu sp. Quadricoma sp. 1 Camacalaimus sp. Parodontophora sp. Siphonolaimus sp. 1 Terschellittgia sp. 3 7‘. Lmgicaudata ParJinhontoeus sp. 1 Metalinhomoeus sp. 1 Linhonrmidae 8 Paramotzhvstera sp. Thwimts sp. 2 T. sp. 4 7‘. sp. 5 T. rip. 8 I-. !;p. 17 ScL~ptrcUa sp.

0.49 1.97 1.97 2.95 0.49 0.49 2.95

sp. 1

1.97

MS2 Jan.

1.09 163

3.80 1.09 3.26 2.17

Jan.

Oct.

Jan.

Oct.

0.53 0.54 0.54 3.82 0.54 0.54 0.54 0.54

0.53 2.14

0.53

0.57 5.18 0.57 1.14 1.14

1.60

2.87

0.56 2.25 1.12 2.25 1.68 0.56 4.49

2.26 0.90 0.45 0.90 2 26 2-71 6.79

1.60

11.41 1.09

0.49 0.49

0.49 0.98 1.48 0.98

1.60 2.67

0.54 1.09 1.63 1.09

3.80 2.71 3.80 1.09

0.54

0.54 1.64 1.09 2.18 0.54

2.14 0.53 0.53 0.53 0.53 1.07

0.56 I.72 0.57 1.72 1.14 1.14 1.14 4.02 2.87

4.49 5.06 O-56 2.25 0.56 0.56 0.56 O-56

0.53 1.07 0.53 0.54

1.14 0.57 I.14

0.54

0.54 2.18

0.53 0.53

0.57

1.07

0.57

IS 5

OS4

Oct.

0.54 0.54 0.98 0.49

OS3

0.56

0.56 0.56 O-56 0.56

0.45 0.90 0.45 0.45 o-45 1.36 1.81 0.90 1.36 2.26

2.71 0.90 0.45 1.36

Jan.

Jan.

0.94

2.07 o-52

1.88 0.94 1.41 5.63 1.88 1.88 2.82 2.35 0.94

0.47 0.47 2.35 1.41 1.88 0.94 0.94 0.47 0.47 3.29 1.88

0.52 3.62

0.52

0.52 1.55 0.52 1.55 1 55 O-52

l-55 (1.52 1 04 I1 92

(individuals with unarmed buccal cavities, 1-3 urn in diameter); non-selective deposit feeders (with unarmed, but larger buccal cavities); epistrate feeders (provided with small teeth for rasping or puncturing); and predators/omnivores (provided with large teeth and capable of ingesting other animals). Non-selective deposit feeders (41”,, of all nematodes identified) and epistrate feeders (37(),) were the most abundant feeding types at all five sites; selective deposit feeders and predators/omnivores each comprised 11 0o (Figure 5). At IS 5, the relative abundance of selective deposit feeders (mainly Halalaimus species) was nearly twice as great (210,) as the average. Except for non-selective deposit feeders, which were significantly more abundant in January than October samples (Student’s ttest, t = 3.25, 7 dof, P
Discussion Fauna1

composition

The results of this and other studies suggest that, despite widespread geographic separation, nematode assemblagesfrom shallow carbonate sedimentsare especially dominated

J. H. Tietjen

432

Constancy Percent

Fldehty

simflarlty

Figure 4. Inverse classification of dominant nematode species (those with average relative abundances 2 l.O”,,) and their nodal statistics at the five central Great Barrier Reef sites. Key to species: 1, Halalaimus sp. 1; 2, Halalaimus sp. 2; 3, Halalaimus sp. 5; 4, Filipjeva sp.; 5, Mononcholaimus sp.2; 6, Micmlaimus sp.1; 7, Onyx sp.; 8, Eubostrichus sp.; 9, Desmodota sp.2; 10, Spilophorella paradoxa; 11, Chromadora sp.; 12, Dichromudora sp. 1; 13, Paralongicyatholaimus sp. I; 14, Paracanthonchussp.; 15, Cervonema sp. 1; 16, Sabatieria sp.4; 17, Paracomesoma sp.; 18, Metacomesama sp.; 19, Terschelkugia sp. 2; 20, Theristus sp. 4; 21, Theristus sp. 17; 22, ? Catanema sp.

5. Species diversity, species richness, individuals of nematodes in the central Great

TABLE

Sample MS 1 (Oct.) MS 1 (Jan.) MS 2 (Oct.) MS 2 (Jan.) OS 3 (Oct.) OS 3 (Jan.) OS 4 (Oct.) OS 4 (Jan.) IS 5 (Jan.)

evenness and number Barrier Reef samples

of genera

per 100

Species diversity (H’)

Species richness (SR)

Evenness (33

Number of genera per 100 individuals

3.79 3.65 3.47 3.39 4.08 3.95 3.97 3.97 3.35

15.99 11.12 1635 14.72 16.67 16.40 14.45 14.36 10.64

0.85 0.90 0.84 082 0.91 0.89 0.91 0.91 0.82

26 24 34 28 34 32 25 29 18

by speciesbelonging to the samefamilies and genera. For example, Grelet (1984) found the nematode assemblagesin carbonate sandsfrom the Red Sea to be dominated by the Desmodoridae (19.89/,), Chromadoridae (14+8°z,)and Xyahdae (13+j0s,).Relative abundancesof these three families in the present study were 156, 12.7 and 11.5O<, , respectively

Ecology of Great Barrier

Reef nematodes

433

Figure 5. Distribution of nematode feeding types in each central Great Barrier Reef continental shelf sample, October 1987 (A) and January 1988 (B). W, selective deposit feeders; 1, non-selective deposit feeders; CZ, epistrate feeders; W, predator/omnivore.

(Table 2). Boucher and Gourbault (1990) have observed that nematode assemblages from the shallow carbonate sediments near Guadaloupe are highly dominated by the Desmodoridae (33”,,) and Xyalidae (21.5”,), with species from the Chromadoridae, Cyatholaimidae, Ethmolaimidae, Linhomoeidae, Oncholaimidae, Comesomatidae, Selachinematidae and Microlaimidae comprising another 38.5”,, of the total. These 10 families comprised 92.5”,, of the individuals in the Guadaloupe study and 76.4”,, of the individuals in the present GBR study. Tietjen (1976) reported that the shallow (50 m) carbonate sands off North Carolina were also dominated by species belonging to the Desmodoridae, Microlaimidae, Chromadoridae, Cyatholaimidae and Xyalidae. Closer to the sites of the current study Alongi (1986) indicated that 34 of the 50 speciesidentified from several zones of Davies Reef belonged to families that were dominant in the present study (Chromadoridae, Cyatholaimidae, Desmodoridae, Oncholaimidae, Xyalidae, Comesomatidae, Linhomoeidae). Similarities among the regions discussedabove alsoexisted for nematodesat the generic level of organization. Of the 25 dominant genera cited by Boucher and Gourbault (1990) from Guadaloupe, 13 were found at the GBR sites (although not all were dominant). Spirinia, Molgolaimus, Eubostrichus, Microlaimus, Tershcellingia and Theristus each comprised greater than 1 OC,of the individuals present in both regions. While the most abundant chromadorids at GBR (Spilophorella, Chromadora and Dichromadora) were not dominant at Guadaloupe, others were (Ptycholaimellus, Innocuonema, the latter also occurring at GBR). The dominant genusat Guadaloupe wasNeonyx; although this genus was not present at the GBR sites, a closely related one (Onyx) was (Table 3). Grelet (1984) reported that the Red Seanematode assemblageswere dominated by Microlaimus, Spirinia and Spilophorella (as were the GBR assemblages),and in the carbonate sandsoff North Carolina genera that were identical or closely related to those from the GBR were

434

J. H. Tirtjcn

also dominant (Desmodora, Microlaimus, Monoposthia, Theristus and Xyala). Finally, 27 of 40 genera reported by Alongi (1986) from Davies Reef were also present at the GBR sites. While it appears that nematode assemblagesfrom shallow carbonate sediments in different areasof the world are dominated by identical or closely related genera, more information is needed to seehow widespread the genera truly are or to identify possible reasonsfor the successof certain genera in carbonate sediments. Dominant nematodesat the GBR and other carbonate sediment sites tend to have highly ornamented cuticles, and speculation on possible links between cuticular ornamentation and locomotion of nematodes in shallow marine sandshas been proffered (Ward, 1975). To date, however, no clear cause-and-effect relationship between cuticle type and distribution of marine nematodeshas been established. Among the GBR sitesthemselves, cluster analysesof the species,genera and families of nematodes all helped to distinguish IS 5 from the others (Figure 2). In addition, population densities at IS 5 were significantly lower than those at the remaining sites (Alongi, 1989). Sediments at IS 5 were comprised primarily of terrigenous muds and quartz sands; per cent CaCO, was lessthan IO”,, (Alongi, 1989). In contrast, CaCO, in the middle and outer shelf sedimentsranged from 32O,, (MS 1) to 81”,, (OS 4), and there was no evidence of extensive terrigenous input. Bacterial abundance and production, aswell aschlorophyll a and phaeopigment concentrations, showed no consistent significant differences among sites (Alongi, 1989). Thus the uniqueness of the nematodes at IS 5 (shown not only by differences in fauna1composition and dominance but alsoby the lower numbers of species, genera and families at IS 5) was probably a function of different sediment types and the proximity of IS 5 to terrestrial influences. Recently, Watson and Goeden (1989) reported differences in the speciescomposition of the demersaltrawl fauna between stations close to IS 5 and stations farther offshore. In considering the effects of depth and sediment composition on the benthic fauna of the central GBR region, they stated that ‘ sediment may be the more important in determining the distribution of demersal and benthic organisms ‘. Site IS 5 lies within 10 km of Hinchinbrook Island and one of the intertidal sitesstudied by Alongi (1987). Despite the proximity of these two sites, however, their nematode assemblageswere quite different. None of the 10 dominant genera at IS 5 was among the dominant genera at Hinchinbrook Island and vice versa. Differences in fauna1 composition between site IS 5 and the intertidal sites at Hinchinbrook Island were not unexpected, given the report by Alongi (1987) that the nematode assemblageshe observed were eachhighly faithful to one of five separateestuariesin north-eastern Queensland. Of the environmental factors cited by Alongi (1987) that might contribute to inter-estuary variation in intertidal nematode speciescomposition, differences in sediment type and food resourcesare the most likely causesof the differences in speciescomposition between the nearby intertidal and subtidal Hinchinbrook Island sites. In contrast to the high fidelity for particular estuariesexhibited by intertidal nematodes, the subtidal nematodes from the present study generally lacked high fidelity to any particular site. While only 11of the 25 dominant genera occurred in samplesfrom all five sites, with the exception of IS 5 (which lacked nine of the genera), no site lacked more than four genera (MS l), and the outer reef siteslacked only one or two (Figure 3). The moderate to high constancy of these generain the middle and outer shelf samples,coupled with the fact that very few of them showed a strong preference for any particular site(s), suggeststhat each of these genera is able to exploit the carbonate sedimentary environment more or

Ecologv

of Great

Barrier

Reef nematodes

435

less equally well. Results from the Red Sea (Grelet, 1984) and Guadaloupe (Boucher & Gourbault, 1990) also bear this out. Most of the species contributing at least lo, to the total number of individuals were present at all sites (except for IS 5, which lacked 11 of the 22 species; Figure 4). The only species to cluster together were Spilophorella paradoxa and Cervonema sp. 1 (the two most abundant speciesin the study), and Hululaimus sp. 5 and Theristus sp. 17, a weakly linked pair of speciesthat were especially abundant only at IS 5. Becausefidelity values for the dominant speciesat each of the four other sitestended to be about average (Figure 4), the high evennessindices (J’) calculated for the entire speciesassemblagesin each sample were not unexpected (Table 5). Species diversity

Low dominance (high evenness) of species in nematode and other meiobenthic assemblageshas been associated with heterogeneous sediments that permit maximum exploitation of the interstitial environment (Warwick & Buchanan, 1970; Heip & Decraemer, 1974; Tietjen, 1977, 1980, 1984; Willems et al., 1982; Boucher, 1990). Sediments at the central GBR sites were all poorly to very poorly sorted, and all were comprised of particles ranging in size from gravels to muds (Alongi, 1989); such high microhabitat diversity would help to relax competition and permit coexistence of many species.X-radiographs of the sediments revealed low levels of bioturbation by macroinfauna compared with other shelf environments; macroinfaunal biomasswas also quite low (Alongi, 1989). Reduced pressurefrom competingmacroinfauna, coupled with physical reworking of sedimentsby frequent prawn trawling (Watson & Goeden, 1989), probably permit a higher speciesdiversity of nematodes to exist in central GBR sediments relative to that seenin similar shelf environments where macroinfauna are more abundant (e.g. Long Island Sound, Tietjen, 1977; North Sea, Warwick & Buchanan, 1970; Spanish shelf, Tenore et al., 1984). In contrast, the speciesdiversity of intertidal nematodes in nearby northern Queensland is low, probably asa result of great physical stressplaced on them by salinity changes experienced during monsoonal rains, influx of soluble tannins from decomposing mangrove litter and great temperature fluctuations (Alongi, 1987). While species diversity was primarily a function of evenness, the species richness observed in the GBR sedimentswas much higher than that normally occurring in temperate continental shelf sediments of similar depth (Boucher, 1990). In fact, speciesrichness values were equal to those normally associated with deep-sea nematode assemblages (Tietjen, 1984,1989; Jensen, 1988). However, monotypic generacomprised about 80”,, of the total genera (107/135) in the GBR assemblages,much lessthan has been observed for deep-seanematodes(Tietjen, 1989). In addition, monotypic generacomprised about 38”,, of the individuals present in the GBR samplescompared with about 16”,, in somerecently reported deep-seasamples(Tietjen, 1989). The species/genus(S/G) ratio (mean f 1 SE) for nematodes from the GBR sites was 1.48 k 0.11, which was significantly less(MannWhitney test, P < 0.05) than that calculated for nematodes from several deep-seasites in the Atlantic Ocean (1.78 k 0.19). Thus the high nematode speciesrichness observed in the central GBR sediments is at least partially due to a relatively high generic richness. The high generic richness of nematodes in the GBR region may be sustained by the complexity of the sedimentary environment, an environment that not only provides a large number of spatial microhabitats via sediment heterogeneity but also one that contains a variety of different food resources for the nematodes (high bacterial biomass, Alongi, 1989; mangrove litter, Robertson et al., 1988; settling phytodetritus, Furnas &

436

J. H. Tietjen

Mitchell, 1986). However, the lower S/G ratio observed for the GBR assemblages(relative to deep-seanematode assemblages)alsosuggeststhat competition among congeneric speciesmight be higher than among deep-seanematodes, where higher S/G ratios imply mutual accommodation among speciesbelonging to a smaller number of genera extremely well adapted for life in the deep sea.For a discussionof S/G ratios aspotential indicators of competition, seeSimberloff (1978). The S/G ratios calculated for nematodes from several shallow temperate shelves are significantly less than those from the GBR region (Long Island Sound, 1.29+ 0.12, Tietjen, 1977; New York Bight, 1.31+ 0.09, Tietjen, 1980; Louisiana shelf, 1.34 f 0.08, Tietjen, unpubl.). Such low S/G ratios suggest that competition among congeneric speciesof nematodes may be higher in temperate shelf sediments than in those from the GBR. Trophic

composition

In shallow, temperate shelf environments the predominant nematode feeding types are usually non-selective deposit feeders and epistrate feeders (see Heip et al., 1985, for a discussion); a similar distribution prevailed in the current study (Figure 5). Co-equal dominance by thesetwo trophic types reflected the availability of the two major sourcesof food generally utilized by shallow subtidal nematodes: detritus and bacteria for deposit feeders, and microalgae (both benthic and recently settled planktonic forms) for epistrate feeders. Both sources of food are available to nematodes in the central GBR Province (Furnas & Mitchell, 1986, 1987; Alongi, 1989), although bacterial abundance is much higher than abundance of microalgae (Alongi, 1989). An additional food resource for epistrate feeders in the region may be the organic coatings that can surround calcium carbonate particles (Suess, 1968). These organic coatings may be scraped off by the rasping action of epistrate feeders. In the deep sea,Tietjen (1970, 1984, 1989) has found epistrate feeders well represented in such carbonate sediments. The relatively high percentage of selective deposit feeders at IS 5 (mainly speciesbelonging to the oxystominid genera Halalaimus and Oxystomatina) may somehow have been associatedwith the site’s proximity to land-derived organic matter, although such speciesare thought to largely ingest bacteria (Wieser, 1953), and bacterial abundance and production at IS 5 were no higher there than at other stations (Alongi, 1989). The relative abundance of non-selective deposit feeders was significantly greater in January than in October samples(Figure 5), but no other differences in trophic composition occurred. Although studies of nematodes from temperate subtidal sedimentshave failed to reveal consistent seasonalvariations in speciesand trophic compositions (see Heip et al., 1985), irregular short-term (2-3 months) fluctuations in abundance of species may sometimes occur (Juario, 1975; Boucher, 1980). Similarly, Alongi (1990) found evidence of such fluctuations among nematodes inhabiting intertidal sites in northern Queensland, which he attributed mostly to changesin sediment temperature. Since the difference in temperature between the October and January samples was only 3 ‘C (Alongi, 1989), temperature can be safely discarded as a factor explaining the trophic differences noted above. Because of their rapid generation time (generally less than 2 months; Heip et al., 1985), nematodes are capable of responding rapidly to changing environmental conditions. The benthic habitat of the central GBR Province is characterized by intermittent (albeit low) inputs of outwelled mangrove litter and settling phytodetritus, physical disturbances from cyclones and frequent prawn trawling, and continuous warm temperatures. Coupled with very high bacterial production rates

Ecology

of Great

Barrier

Reef nematodes

437

(Alongi, 1989), these environmental factors may lead to an assemblage of nematodes characterized by rapid fluctuations in species composition and having a high species diversity.

Acknowledgements The author thanks Dr D. M. Alongi of the Australian Institute of Marine Science for help in providing nematodes used in this study. This research was supported by WC-CUNY Grant 667181, National Science Foundation Grant INT-8611445 and the City College Fund.

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