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1
Morphological diversity and abundance in the tube-dwelling polychaete
Spirobranchus giganteus (Pallas, 1766) in the Indo-Pacific: adaptations to its
coral host?
S.J. Rowley
School of Biological Sciences, University of Plymouth, Drake Circus, Plymouth, PL4 8AA, UK
ABSTRACT: The tube-dwelling serpulid Spirobranchus giganteus (Pallas 1766) is an obligate associate of
living hermatypic corals, its distribution following that of its host. The distribution and abundance of S.
giganteus was assessed across four sites around the islands in the Wakatobi Marine National Park, SE
Sulawesi, Indonesia, selected relative to their variability in natural and anthropogenic impact and recovery.
Morphological variability between both worm and host were further assessed to elucidate the nature of the
association between such taxa, and which species within the S. giganteus complex are present within the study
area. Results revealed that S. giganteus abundance and distribution is non random and changed in response to
differential environmental parameters. Eight coral species: Montipora danae, M. informis, M. spumosa, M.
venosa, Porites cylindrica, P. lobata, P. lutea and P. nigrescens, were most heavily colonized by S. giganteus,
such host taxa being competitively subordinate and possessing small plocoid corallites. S. giganteus abundance
was six times higher on the pristine low sedimented site than a high sedimented lagoonal site subject to
continual marine resource exploitation. Therefore, the validity of this taxon as an indicator of reef health ought
not be overlooked. Univariate and multivariate analyses further revealed that branching poritids, predominantly
on the reef flats, influenced substrate availability and S. giganteus abundance and morphological variability,
illustrating potential morphological adaptations of both worm and host to environmental conditions. This study
further presents observations on morphological traits with tentative assignment to two most dominant taxa; S.
gardineri complex on branching poritids on the reef flats and S. cf crucigerus (Grube 1862) exhibiting
generality in host and bathymetric distribution. Such patterns may infer intraspecific polymorphism revealing
the potential for phenotypic plasticity or incipient ecological divergence consequential of resource partitioning
and response to natural light. Further systematic and molecular studies may provide insights into the intriguing
nature of the S. giganteus complex within the Indo-Pacific.
KEY WORDS: Spirobranchus giganteus · Coral host · Morphological diversity · Tube-dwelling · Polychaete ·Indo-Pacific
INTRODUCTION
Coral reefs are high in species diversity with a low effective population size for most species and a high
incidence of coevolution among interacting taxa (DeVantier et al. 1986, Marsden 1993). Identifying such
interactions, and subsequent associations between species, helps understand coral reef biodiversity, trophic
structure and biochemical cycling, and whether specific species traits persist in response to dynamic
environmental conditions (Rachello-Dolmen & Cleary 2007). Hermatypic (reef building) corals provide
secondary space to other organisms (Todd pers. comm. 2007) through morphological diversity as a function of
habitat complexity (Edinger & Risk 2000). Coral associates, sessile invertebrates that live on or within the coral
skeleton (Smith 1984a, Risk et al. 2001, Scott 1987), are predominantly suspension or filter-feeding
heterotrophs (Risk et al. 2001, Kleemann 2001). Little is known about such associates, however, the species
composition of associate polychaetes, for example, alters relative to water quality, terrigenous input (Pey-
Clausade et al. 1992, Hutchings & Pey-Clausade 2002, Perry & Smithers 2006, Mallela & Perry 2007),
destructive wave action and bioerosion (Tribollet et al. 2002, Risk et al. 2001), thus suggested indicators of reef
health (Bailey-Brock 1976, Scott 1987, Risk et al. 2001, Low et al. 1995). However, the role of polychaetes in
coral biology is unknown (Work & Rameyer 2005).
2
The tube-dwelling serpulid Spirobranchus giganteus (Pallas 1766) is an obligate associate of living
hermatypic corals found in tropical and subtropical waters (Smith 1984a, Strathmann et al. 1984, DeVantier et
al. 1986, Marsden 1984, 1986, 1987, Marsden & Meeuwig 1990, Marsden et al. 1990, Hunte et al. 1990a, b,
Frank & Hove 1992, Dai & Yang 1995, Nishi & Kikuchi 1996, Martin & Britayev 1998, Qian 1999, Floros et
al. 2005, Lewis 2006), its distribution following that of the host (Bailey-Brock 1976). S. giganteus is a
dioecious filter feeding heterotroph, with a planktonic larval phase of 9-12 days (Smith 1984a, Marsden 1987,
Marsden et al. 1990) and an estimated adult life span of over 30 years (Nishi & Nishihira 1999). The
relationship between S. giganteus and its coral host is, as yet, unclear. The coral-worm association may be
mutualistic, the coral providing the worm with support, nutrition and protection from predation by fish and
Crustacea (Strathmann et al. 1984); and the worm protecting the coral host from predation (DeVantier et al.
1986), and enhancing water circulation to adjacent polyps facilitating coral recovery in algal dominated
colonies (Dai & Yang 1995, Ben-Tzvi et al. 2006). Conversely, Borger (2005) stated that all Dark Spot
Syndrome (DSS) Type III blemishes were caused by irritation of the coral surface from S. giganteus. Such
recent evidence illustrates the importance of associate organisms on coral reefs.
The non-random clustered distribution of Spirobranchus giganteus on specific coral species has been well
documented (Bailey-Brock 1976, Smith 1984a, Scott 1987, Marsden 1987, Hunte et al. 1990a, Pey-Clausade et
al. 1992, Dai & Yang 1995, Nishi 1996, Nishi & Kikuchi 1996, Floros et al. 2005), likely consequential of
differential mortality following settlement or pre-settlement larval preference (Hunte et al. 1990a, Connell
1985) found to respond positively to water-borne exudates of corals commonly colonized by S. giganteus
(Marsden 1987, Marsden et al. 1990, Marsden & Meeuwig 1990). Planktonic larval responses to biological
factors: conspecifics, sympatric species, biofilms, and environmental factors such as water flow, light intensity,
chemical cues and substrate properties may greatly influence larval dispersion and settlement (Pawlik et al.
1991, Rodríguez et al. 1993, Qian 1999, Fox 2004). Interestingly, host corals possessing small plocoid
(corallites with their own walls) corallites have been related to coral associate distribution (Scott 1987, Dai &
Yang 1995, Wielgus et al. 2006, Scaps & Denis 2007), providing a high coencosteum to corallite ratio for
larval settlement. However, larvae settle on exposed coral skeleton and extend their tubes towards the living
tissue (Smith 1984a, Nishi & Kikuchi 1996), which subsequently obscures the tube.
Mean worm density on individual coral species is independent of abundance, distribution and competitive
dominance of available coral in the Caribbean (Hunte et al. 1990a, Marsden & Meeuwig 1990) with
Spirobranchus giganteus larvae demonstrating immunity to nematocyst discharge (Smith 1984a). Conversely,
coral species frequently colonized in Taiwan are competitively subordinate in terms of aggression (Dai 1990,
Dai & Yang 1995). Such disparity between host species in the different regions requires further investigation to
determine any notable trends. However, S. giganteus distribution and abundance in different reef areas is likely
affected by disruptive processes such as wave action, marine resource exploitation, sediment loading and
subsequent availability of colonizable substrate (Dai & Yang 1995). Furthermore, S. giganteus may be
morphologically selective of coral species, typically colonizing stress tolerant slow growing massive species
over foliaceous and branching forms irrespective of relative abundance (Hunte et al. 1990a, Marsden &
Meeuwig 1990, Dai & Yang 1995). Selection for different host species may be adaptive, with larger worms on
coral species most heavily colonized in the field (Hunte et al. 1990b). Yet even in the presence of suitable
substrate, S. giganteus is absent in areas of high turbidity (Scott 1987, Frank & ten Hove 1992, Perry &
Smithers 2006) due to the physical impairment of settlement, feeding, reproduction and growth (Mallela &
Perry 2007).
Evidence to date, therefore, suggests that the non-random distribution of Spirobranchus giganteus on corals
results primarily from active habitat selection by planktonic larvae, and that habitat selection displayed by the
larvae is probably adaptive (Hunte et al. 1990b). Furthermore, morphological variability and habitat selection
may be indicative of ecological divergence leading to reproductive isolation as seen in Spirobranchus polycerus
(Schmarda 1861) in Barbados (Marsden 1992).
Spirobranchus giganteus has four recognized full species complexes (ten Hove 1994). In the Indo-Pacific
Spirobranchus corniculatus complex and Spirobranchus gardineri complex are currently recognized having
five and two subspecies respectively (ten Hove 1994, Appendix 1), primarily distinguished by their opercular
and tube morphology (for detailed account see ten Hove 1994, Fiege & ten Hove 1999, Fiege & Sun 1999).
However, further elucidation on the taxonomic status of, and within, such complexes are required including
systematic, molecular and ecological analysis. From here on in, S. giganteus will remain assigned thus, unless
otherwise specified.
3
Little is known of the distribution and association between Spirobranchus giganteus and its coral host
relative to environmental parameters in the Indo-Pacific, an area comprising ca. 400 recognized scleractinian
taxa (Porter 1976, Veron 2000, Haapkylä et al. 2007). Therefore, the aims of this study were to assess the
distribution and abundance of S. giganteus; (1) across sites of varying natural and anthropogenic exposure and
recovery; (2) between reef habitats as a function of depth within each site; (3) on host species most commonly
colonized; (4) their subsequent morphological characteristics; (5) to potentially determine, through preliminary
field observations, which species within the S. giganteus complex are present within the Wakatobi National
Marine Park; and if morphotypes exist within them.
MATERIALS AND METHODS
Study area
The Wakatobi Marine National Park (formerly Tukang Besi Islands) is a remote island group of ca. 2000
km2 in S.E. Sulawesi, Indonesia (Fig. 1a). Established in 1996, the Wakatobi MNP contains ca. 500 km2 of the
most biodiverse coral reefs in the world (Scaps & Denis 2007), with 396 scleractinian coral species, a low
incidence of disease (0.57% see Haapkylä et al. 2007) and relatively free of recent ENSO-induced bleaching
events (Crabbe & Smith, 2003) likely due to local upwelling (Geiskes et al. 1988). Approximately 90,000
people live within the Wakatobi, resulting in extensive subsistence marine resource dependence and destructive
commercial fisheries in populated areas.
Four sites were selected around the islands Kaledupa (ca. 17,000 people) and Hoga (<100 people, Fig. 1b)
relative to their variability in natural and anthropogenic impact, and recovery. Sampela, an enclosed lagoon
with an outer reef wall ca. 400 m from a Bajau (sea gypsy) village of ca. 1300 people, is subject to continuous
exploitation through coral mining, fishing activities, and high sediment loading due to natural re-suspension,
bioturbation through gleaning, and mangrove loss (Smith pers. comm. 2006). Kaledupa, ca 500 m offshore, is a
moderately exposed fringing reef with a patchy, soft coral dominated reef flat due to extensive blast fishing
(Fox et al. 2003) until 2005. Pak Kasim’s, ca. 500 m offshore, is an intermediate topographically complex
fringing reef, subject to coral mining and blast fishing on the reef flat and crest until 2004. Ridge 1, ca. 1 km
offshore, is an exposed reef ridge with strong water currents (Fig. 1b) and upwelling with nominal blast fishing
on the reef crest in 2004. All sites have a pronounced reef flat (< 3 m), reef crest (3 - 6 m) and slope (> 6 m)
with varying levels of sedimentation draining from the reef flats during spring tides (Smith pers. comm. 2006).
Fig. 1. (a) Location map of the Wakatobi Marine National Park in S.E. Sulawesi, Indonesia. (b) Areas of study; Sampela, Kaledupa, Pak Kasim’s
and Ridge 1 off the islands K aledupa and Hoga respectively.
Pak Kasim’s →
Ridge 1 →
Sampela →
← Kaledupa
(b)
(a)
HOGA
Waves
Prevailing
current
4
Sample collection
Observations were conducted from 7th July to 29th August 2006 by SCUBA or snorkeling. Four 30 m belt (1
m either side) transects laid 20 m apart, ran parallel to the reef contour at each reef habitat (flat ≤ 3 m, crest ca.
6 m and slope ca. 12 m depth), within each site with a total area surveyed of 2880 m2. All Spirobranchus
giganteus encountered within this area were recorded, and host coral identified to species level, with the longest
and perpendicular axes measured (to the nearest centimeter). Preliminary surveys revealed conspicuous
variations in S. giganteus morphology, namely tube aperture (Fig. 2a & b) and operculum types (Fig. 2c-f, Fig.
3a-f). Such observations were subsequently included in the data collection procedure. Opercula obscured by
filamentous algae, sedimentation or encrusting invertebrates (e.g. Bryozoa, Porifera and Didemnid ascidians)
were also recorded (Fig. 2c-f). Digital image photography (Canon IXUS 900Ti) was employed to clarify
uncertainties in coral species identification (following Veron 2000).
Benthic characteristics were determined using transects as described for Spirobranchus giganteus surveys,
and categorized according to English et al. (1997) utilizing the point (every 0.5 m) intercept transect method
(Kingsford & Battershill 1998). Rugosity (quantification of habitat complexity) was measured with a 7.30 m
length chain laid over three replicate transects per habitat and calculated using the ratio of contoured surface
distance to linear distance method (McCormick 1994). Sediment rates were assessed using four standard
sediment traps (English et al. 1997) at each habitat per site over 10 days. Sediment and water were filtered,
dried with rates expressed as g dry weight day-1. Turbidity estimates were taken in situ prior to each survey dive
using a Secchi disk. Temperature was taken throughout the sampling period using in situ data loggers
(HOBOware® Pro). Salinity was measured using a hand-held salinometer. Latitude and longitude were
determined by a hand-held GPS meter.
Data analysis
Data were analyzed utilizing univariate (SPSS vs. 15.0) and multivariate (PRIMER-E, Clarke & Gorley
2006) statistical packages. Analysis of variance (ANOVA) was performed with the following factors, all of
which fixed and orthogonal: turbidity across all sites, coral characteristics on all or selected colonized corals by
Spirobranchus giganteus as appropriate (ANOVA one-way); rugosity and sedimentation across all sites and
habitats (ANOVA two-way); S. giganteus abundance and aperture type between sites, habitats, coral species
and morphology (ANOVA three-way). Mean difference significance level was set at P < 0.05 with all
interactions tested. All data were log10 transformed where appropriate subject to Kolmogorov-Smironov
normality testing and Levene’s test for heterogeneity of variances. Post-hoc pairwise comparisons using Tukey
(HSD) tests were performed where differences were significant. S. giganteus abundance data did not meet the
assumptions of normality and homoscedasticity required for parametric analysis, post transformation (log10).
However, differences in S. giganteus abundance were tested using a General Linear Model (three-factor GLM),
robust to large sample sizes and variations to normality (Underwood 1997). Coral colony surface area estimates
were calculated according to morphological classification (English et al. 1997, Veron 2000): massive 2πr2;
encrusting and foliaceous 2πr; branching and sub-massive 2πr2 with a conversion factor of three (Dahl 1973).
Analysis of benthic characteristics and operculum types followed multivariate routines within the PRIMER
software package. Data were loge(x + 1) transformed and a triangular matrices of similarity constructed
between sites and habitat samples using Bray-Curtis similarity coefficient. Differences in variables between
sites and habitats were tested using the permutation based Analysis of Similarity (ANOSIM, Clarke & Green
1988). Similarity percentages (SIMPER) further revealed prominent variables contributing to dissimilarities as
visualized in multidimensional scaling (MDS) ordination analysis. Relationships between environmental
variables and S. giganteus and its associate morphological characteristics (aperture and operculum type) were
investigated using the BIO-ENV routine (Clarke & Ainsworth 1993). Results expressed as a rank correlation
coefficient (r [max. 1]), indicate the proportion of variation in biological data “best explained” by
environmental variable(s) (Clarke & Ainsworth 1993, Clarke & Gorley 2006).
5
Fig. 2. (a). Spirobranchus cf. corniculatus spine bearing ap erture on Porites lobata (Dana 1846). (b). Spirobranchus cf. gardin eri complex round
aperture on Porites cf. nigrescens (Dana 1846). (c) Spirobranchus cf. crucigerus on Porites sp. with algae obscured operculum . (d) Spirobranchus
sp. with filam ent and sediment obscu red operculum on Acropora cf palifera (Lamarck 1816). (e) Spirobranchus cf. crucigerus with sponge obscured
operculum (ten Hove pers comm. 2008) on Porites sp. (f) Spirobranchus sp. with branchiae 1.5 turns on Porites nigrescens (Dana 1846). [Images (a-
d) Rowley (2006); (e) Flavell (2006); (f) Trebilco (2006)].
(f)
(c)
(d)
(e)
(a)
(b)
•
•
6
Fig. 3. (a) Spirobranchus crucigerus (Grube 1862). (b & c) Spirobranchus gardineri (Pixell 1913) complex. (d) Spirobranchus gardineri sensu
stricto (Grube 1862). (e) Infrequently observed in the present study, however, may be observed in numerous Spirobranchus spp. (ten Hove 1970). (f)
Spirobranchus corniculatus sensu stricto (Grube 1862). [Illustrations (a-c, e) Smith (1985), ten Hove & Fiege pers comm. (2008); (d) as
representation of field observation not of species discussed by P ixell (1913)].
(b)
(f)
(e)
•
k
(a)
(d)
•
•
•
•
•
•
•
•
(c)
•
•
•
7
RESULTS
Environmental parameters
Environmental parameters (Table 1) were largely concordant with previous studies (Crabbe & Smith 2002,
2003, 2005, Bell & Smith 2004, Haapkylä et al. 2007, Hennige et al. in press) undertaken in this area. Minimal
variation in pH, salinity and temperature occurred between study reefs (Table 1). Turbidity as a measure of
light-limitation differed significantly (ANOVA, F3,70 = 11.79, p < 0.01) between sites with Sampela (Tukey
test, p < 0.001 in all cases) as the determining factor. High turbidity at Sampela was in accordance with high
Table 1. Environmental and biotic characteristics of the four study sites in the Wakatobi Marine National Park, Indonesia.
Parameter Recorded
Mean value ± SE (where appropriate)
Site
Sampela
Pak Kasim's
Kaledupa
Ridge 1
Latitude (S)
5˚ 29'01"
5˚ 27'569"
5˚ 28'22"
5˚ 26'565"
Longitude (E)
123˚45'08"
123˚45'179"
123˚43'47"
123˚45'38"
Temperature (˚C)
27.38 ± 0.01
27.48 ± 0.01
27.26 ± 0.02
27.0 ± 0.01
Salinity (‰)
32
34
34
34
Turbidity (m)
6.83 ± 0.80
8.5 ± 1.07
10.95 ± 1.20
10.13 ± 0.77
Sedimentation (g d-1)
3.05 ± 0.48
0.98 ± 0.09
0.97 ± 0.09
2.73 ± 1.03
Rugosity Index
0.82 ± 0.04
0.71 ± 0.03
0.70 ± 0.04
0.61 ± 0.03
Hard Coral Cover (%)
14.62
29.8
17.9
30.87
Dead Coral Cover (%)
2.867
7.24
5.6
3.83
Soft Coral Cover (%)
20.77
26.09
44.67
33.47
Biotic (%)
2.87
5.6
9.43
12.43
Abiotic (%)
58.88
31.28
22.4
19.4
sedimentation rates (Table 1) having fine slow settling particles, compared with coarse fast settling particles at
the other sites. No habitat effect or interaction (Table 2) was shown, however, pairwise comparisons revealed
no difference between Sampela and Ridge 1 ([Fig. 4a] largely due to sediment traps at Ridge 1 laid over high
springs through logistical constraints), likely an artifact of overall insufficient replication.
Table 2. ANOVA-two-way table showing the effects of site and habitat on rugosity
and sedimentation rates *p < 0.05; ** p < 0.01; *** p < 0.001; ns, not Significant
(ANOVA with post hoc testing – Fig. 4a & b).
Rugosity
Sedimentation
Source
df
MS
F
p
df
MS
F
p
Site
3
0.025
8.384
***
3
0.663
14.689
***
Habitat
2
0.012
4.039
*
2
0.050
1.114
ns
Site x Habitat
6
0.007
2.463
ns
6
0.058
1.290
ns
Error
24
0.003
35
0.045
8
0
0.2
0.4
0.6
0.8
1
1.2
Sampela Pak Kasims Kaledupa 1 Ridge 1
Rugosity Index
Flat
Crest*
Slope*
***
0
1
2
3
4
5
6
7
8
Sampela Pak Kasims Kaledupa 1 Ridge1
Mean Sedimentation (g d-1)
Flat
Crest
Slope
***
***
**
**
Fig. 4. Mean (± SE) (a) rugosity index for each site across all habitats, and (b) sedimentation rates for each site across all habitats. Lin es indicate
pairwise significance (Tukey test: *p < 0.05; ** p < 0.01; *** p < 0.001).
Differences in rugosity, as a measure of habitat complexity, were significant between sites and habitats with
no interaction effect (Table 2). Post hoc tests indicated differences were between Sampela and Ridge 1 (Fig. 4b)
and the crest and slope (Tukey p < 0.05). Multivariate analysis revealed differences in benthic composition
(Table 3) between sites (ANOSIM, global R = 0.355, p < 0.001) and habitats (ANOSIM, global R = 0.322, p <
0.001), primarily due to Sampela and the reef slope respectively as illustrated by MDS ordination (Fig. 5a & b).
Table 3. ANOSIM-two-way out put with pair wise comparisons from the benthic survey
across all sites and habitats (*p < 0.05; ** p < 0.01; *** p < 0.001; ns, not Significant).
Site Groups
Global R
p
Habitat Groups
Global R
p
Sampela, Pak Kasim’s
0.368
**
Slope, Crest
0.299
*
Sampela, Kaledupa
0.569
***
Slope, Flat
0.583
***
Sampela, Ridge 1
0.705
***
Crest, Flat
0.083
ns
Pak Kasim’s, Kaledupa
0.104
ns
Pak Kasim’s, Ridge 1
0.208
ns
Kaledupa, Ridge 1
0.257
**
SIMPER analysis depicted that abiotic forms (e.g. rubble, sand and rock, Table 1) and branching coral
contributed most towards dissimilarities between Sampela and all sites with the latter being least abundant at
Sampela (data not shown). Ridge 1 had the greatest abundance of branching and encrusting coral compared to
the heavily bombed site Kaledupa (average dissimilarity 20.53). Dissimilarities between reef habitats were
largely due to other sessile organisms (e.g. sponges, ascidians and algae), encrusting and branching coral
(average dissimilarity 23.37 between slope and flat) and dead coral (average dissimilarity 19.56 between slope
and crest), the latter greatest on the reef crest.
(a)
(b)
9
Trans for m: Log(X+1)
Resemblanc e: S17 Bray Curtis similarity
Sa
Sa
Sa
Sa
Sa
Sa
Sa
Sa
Sa
Sa Sa
Sa
PK
PK
PK
PKPK
PK PK PK
PK
PK
PK
PK
K
KK
K
K
K
K
K
K
K
K
K
R
R
R
R
R
R
R
RR
R
R
R
2D Stress : 0.18
Trans for m: Log(X+1)
Resemblanc e: S17 Bray Curtis similarity
S
S
S
S
C
C
C
C
F
FF
F
S
S
S
SC
CC
C
F
F
F
F
S
S
S
S
C
C
C
C
F
F
F
F
S
S
S
S
C
C
C
CF
F
F
F
2D Stress : 0.18
Fig. 5. MDS ordination of the benthic survey across (a) sites: Sa = Sampela; PK = Pak Kasim’s; K = Kaledupa, and R = Ridge 1, and (b) habitats: F
= reef flat; C = crest, and S = slope.
Spirobranchus giganteus abundance
A total of 13,240 Spirobranchus giganteus on 52 coral species (of 15 genera) were encountered: 42 found on
colonies exhibiting partial mortality, eight on substrata other than hermatypic coral (Appendix II), and 1126,
3426, 2426 and 6262 recorded at Sampela, Pak Kasim’s, Kaledupa and Ridge 1 respectively. Coral species
previously recorded across study sites (253 to date, Trebilco et al. unpublished data) were not all colonized by
S. giganteus. Degree of colonization varied between coral species (Appendix II), with those most frequently
colonized (Montipora danae, M. informis, M. spumosa, M. venosa, Porites cylindrica, P. lobata, P. lutea and P.
nigrescens) selected for further analyses (Total 11,504 worms). 77% of S. giganteus recorded, colonized
poritids (60% branching, 17% massive) and 23% on encrusting Montipora species.
Differences in Spirobranchus giganteus abundance across all sites, habitats and coral species were
significant with no interactions (Table 4). Post hoc comparisons revealed prominent significance between
Sampela, Ridge 1, and all habitats (Fig. 6a & b). P. cylindrica and P. nigrescens were consistently different
from all coral species, with no difference between Montipora encrusting and Porites massive species (Fig. 6c).
A similar pattern was observed regarding coral morphological type (Table 4); branching coral being the
significant factor (Fig. 6d). BIO-ENV also revealed that coral morphological types were the best exposition for
S. giganteus abundance (r = 0.596).
Table 4. Spirobranchus giganteus. ANOVA (three-way) of the effects of site, habitat, host coral species and morphological type on S. giganteus
abundance (*p < 0.05; ** p < 0.01; *** p < 0.001; ns, not significant; see Fig. 6a-d for pairwise significance)
Coral Species
Coral Morphology
Source
df
MS
F
p
Source
df
MS
F
p
Site
3
1.113
7.747
***
Site
3
0.998
6.852
***
Habitat
2
0.429
2.986
*
Habitat
2
1.016
6.976
***
Coral
7
1.610
11.205
***
Morph
2
8.047
55.251
***
Site x Habitat
6
0.216
1.502
ns
Site x Habitat
6
0.307
2.106
ns
Site x Coral
21
0.117
0.815
ns
Site x Morph
6
0.176
1.208
ns
Habitat x Coral
14
0.153
1.063
ns
Habitat x Morph
4
0.021
0.143
ns
Site x Habitat x Coral
35
0.185
1.288
ns
Site x Habitat x Morph
11
0.239
1.644
ns
Error
1493
0.144
Error
1547
0.146
(a)
(b)
10
0
2
4
6
8
10
12
Sampela Pak Kasims Kaledupa Ridge 1
Mean S. giganteus
***
***
**
***
0
2
4
6
8
10
12
Flat Crest Slope
Mean S. giganteus
***
***
***
0
2
4
6
8
10
12
14
M.danae M.informis M.spu mos a M.venos a P.cylindric a P.lobata P.lutea P.nigres c ens
Mean S. giganteus
*
ººº
**
*
**
ººº
0
2
4
6
8
10
12
14
Branching Encrusting Massive
Mean S. giganteus
***
***
Fig. 6. Spirobranchus giganteus mean (± SE) abundance across all (a) sites; (b) habitats; (c) host coral species (Tukey test: ºººp < 0.001 across all
coral species), and (d) morphology. Lines indicate pairwise significance (Tukey test: *p < 0.05; ** p < 0.01; *** p < 0.001).
Colonizable area among selected coral species (Table 5) differed significantly between Montipora and
Porites spp. in all cases (Fig. 7a) and thus morphology; however only the branching corals P. cylindrical and P.
nigrescens were significantly different from all other species (Fig. 7a). Morphological characteristics within
coral species most colonized further suggested selection for particular host morphologies (Table 5, Fig. 7b-d).
S. giganteus significantly colonized less aggressive coral species (as classified by Dai 1990, Sheppard 1979
[total and selected coral species, Table 5, Fig. 7b]) possessing small, 0.5 – 2 mm diameter (Fig. 7c), plocoid
corallites (Fig. 7d). All selected coral species had small plocoid corallites (Table 5), however, insufficient
evidence regarding coral aggression in the Indo-Pacific (Dai 1990), suggests such data should be treated with
caution.
Table 5. ANOVA (one-way) for colonizable coral host characteristics
(*** p < 0.001; see Fig. 7a-d for pairwise significance).
Source
df
MS
F
p
Coral Area†
7
118.46
545.10
***
Error
1395
0.22
Coral Aggression‡
5
8.245
48.27
***
Error
1826
0.171
Coral Aggression†
2
13.988
75.80
***
Error
1400
0.185
Corallite Size (mm) ‡
2
0.949
7.63
***
Error
1829
0.124
Corallite Morphology‡
2
4.27
22.65
***
Error
1829
0.188
† = Selected host corals, ‡ = all corals colonized by Spirobranchus giganteus.
(d)
(c)
(b)
(a)
11
1
1000
1000000
M. danae M. informis M. spu mos a M. venos a P. cylindrica P. lobata P. lutea P. nigre scen s
Mean Coral Area (cm 2)
ns
ººº
ººº
ººº
ººº
0
2
4
6
8
10
12
A I MA MS S U
Mean S. giganteus
All
Selected
ººº
***
***
ººº
0
1
2
3
4
5
6
7
8
9
0.5-2 mm 3-6 mm 8-12 mm
Mean S. giganteus
***
***
0
1
2
3
4
5
6
7
8
9
Ploccoid Ceroid Other
Mean S. giganteus
***
Fig. 7. Spirobranchus giganteus mean (± SE) abundance associated with specific host coral characteristics: (a) mean (± SE) colonizable area per host
species (Tukey test: ºººp < 0.001 across all coral species); (b) coral aggression for selected and all colonized corals (Tukey test: ºººp < 0.001 for both
selected and all coral sp ecies colonized); (c) g rouped corallite size, and (d) corallite morphology. Lines indicate pairwise significance (Tukey test:
*p < 0.05; ** p < 0.01; *** p < 0.001; ns, not significant).
Spirobranchus giganteus morphology
Preliminary observations revealed morphological differences in Spirobranchus giganteus (Fig. 2a-e, 3a-f).
1885 recorded S. giganteus possessed spine bearing apertures (Fig. 2a), 5-6 branchial whorls (Fig. 2c & e), and
were observed to colonize massive poritids and encrusting Montipora spp. over branching corals (1021, 732
and 132 S. giganteus respectively). 9620 S. giganteus possessed round apertures (Fig. 2b), 1.5-4 branchial
whorls (Fig. 2f), and observed to favour branching poritids (6784 on branching; 1927 on encrusting; 907 on
massive corals).
There was no difference in mean spine aperture abundance between coral species, morphology or sites
(Table 6). A weak habitat effect between the reef crest and flat (Fig. 8b) was further confounded by a three
factor interaction for both coral species and morphological type (Table 6). Conversely, mean round aperture
abundance differed across all sites for Sampela and Kaledupa (Fig. 8e), all habitats, and the branching corals
Porites cylindrica and P. nigrescens (Fig. 8g & h). However, a replicate ANOVA model incorporating coral
morphology showed no main site effect, yet both models revealed a significant first order interaction: site x
coral (Table 6), i.e. differences in mean abundance of round apertures between the four study sites are not
independent of the factors ‘coral species’ or ‘morphology’. BIO-ENV analysis further demonstrates that
variation in coral morphology (r = 0.373) “best explains” aperture abundance, with branching corals being the
main explanatory variable (r = 0.436).
(a)
(c)
(b)
(d)
12
0
1
2
3
4
5
6
7
Sampela Pak Kasims Kaledupa Ridge 1
Mean S. giganteus
0
1
2
3
4
5
6
7
Flat Crest Slope
Mean S. giganteus
*
0
1
2
3
4
5
6
7
M. danae M. informis M. spumosa M. venosa P. cylindrica P. lobata P. lutea P. nigrescens
Mean S. giganteus
0
1
2
3
4
5
6
7
Branching Encrusting Massive
Mean S. giganteus
0
2
4
6
8
10
12
Sampela Pak Kas ims Kaledupa Ridge 1
Mean S. giganteus
*
***
ººº
0
2
4
6
8
10
12
14
Flat Crest Slope
Mean S. giganteus
***
***
***
0
2
4
6
8
10
12
14
16
M. danae M. informis M. spumosa M. venosa P. cylindrica P. lob ata P. lutea P. nigrescens
Mean S. giganteus
*
*
*
ººº
ººº
0
2
4
6
8
10
12
14
Branch ing Encrust ing Mas s ive
Mean S. giganteus
***
***
Fig. 8. Spirobranchus giganteus mean (± SE) spine ap erture abundance across all (a) sites; (b) habitats; (c) host coral species, and (d) morphology.
(e) Spirob ranchus giganteus mean (± SE) round aperture abundance across all sites; (f) habitats; (g) host coral species (Tukey test: ºººp < 0.001
across all coral species), and (h) mo rphology. Lines indicate pairwise significance (Tukey test: *p < 0 .05; ** p < 0.01; *** p < 0.001).
(a)
(b)
(c)
(d)
(e)
(f)
(h)
(g)
13
Table 6. Spirobranchus giganteus. ANOVA (three-way) of the effects of site, habitat, host coral species and morphological type on S. giganteus
spine and round aperture abundance resp ectiv ely (*p < 0.05; ** p < 0.01; *** p < 0.001; ns, not significant; see Fig. 8a-d, and Fig. 9a-d for pairwise
significance).
Spine Aperture
Source
df
MS
F
P
Source
df
MS
F
p
Site
3
0.034
0.233
ns
Site
3
0.019
0.129
ns
Habitat
2
0.477
3.259
*
Habitat
2
0.401
2.691
ns
Coral
7
0.219
1.494
ns
Morph
2
0.160
1.076
ns
Site x Habitat
6
0.048
0.331
ns
Site x Habitat
6
0.235
1.575
ns
Site x Coral
18
0.191
1.307
ns
Site x Morph
6
0.315
2.114
ns
Habitat x Coral
13
0.120
0.821
ns
Habitat x Morph
4
0.066
0.441
ns
Site x Habitat x Coral
15
0.266
1.815
*
Site x Habitat x Morph
6
0.420
2.816
**
Error
321
0.147
Error
356
0.149
Round Aperture
Source
df
MS
F
P
Source
df
MS
F
p
Site
3
0.586
4.229
**
Site
3
0.119
0.853
ns
Habitat
2
0.427
3.084
*
Habitat
2
0.887
6.359
**
Coral
7
1.918
13.850
***
Morph
2
8.844
63.365
***
Site x Habitat
6
0.123
0.886
ns
Site x Habitat
6
0.213
1.527
ns
Site x Coral
21
0.222
1.604
*
Site x Morph
6
0.308
2.207
*
Habitat x Coral
14
0.157
1.135
ns
Habitat x Morph
4
0.053
0.381
ns
Site x Habitat x Coral
30
0.120
0.864
ns
Site x Habitat x Morph
10
0.237
1.696
ns
Error
1112
0.138
Error
1162
0.140
ANOSIM results (Table 7) show a weak difference in operculum types across sites (R = 0.276, p < 0.01) and
habitats (R = 0.134, p < 0.05) consistent with MDS ordination (Fig. 9a & b). Operculum types assigned to:
Spirobranchus cf. crucigerus, Spirobranchus gardineri complex and sedimented account for dissimilarity
between Ridge 1 and all other sites, notably Sampela (average dissimilarity = 42.25) with sedimented
operculum prevalent on the latter. Operculum types Spirobranchus cf. crucigerus and Spirobranchus gardineri
complex further account for differences between reef slope and flat (average dissimilarity = 33.64),
Spirobranchus gardineri complex predominantly on the latter. BIO-ENV analysis revealed variation in
operculum types was, again, “best explained” by coral morphology (branching, encrusting and massive, r =
0.302).
Table 7. Spirobranchus giganteus operculum abundance across all sites and habitats (ANOSIM-two-way,
with pair wise comparisons *p < 0.05; ** p < 0.01; *** p < 0.001; ns, not Significant).
Site Groups
Global R
p
Habitat Groups
Global R
p
Sampela, Pak Kasim’s
0.119
ns
Slope, Crest
-0.027
ns
Sampela, Kaledupa
0.104
ns
Slope, Flat
0.338
**
Sampela, Ridge 1
0.681
***
Crest, Flat
0.078
ns
Pak Kasim’s, Kaledupa
0.014
ns
Pak Kasim’s, Ridge 1
0.24
**
Kaledupa, Ridge 1
0.434
***
14
Trans for m: Log(X+1)
Resemblanc e: S1 7 Bray Curtis similarity
Sa
Sa
Sa
Sa
Sa
Sa
Sa
Sa
Sa
Sa Sa
Sa
R
R
R
R
R
R
R
R
R
R
R
R
PK
PK
PK
PK
PK
PK
PK
PK PK
PK
PK
K
K
K
K
K
K
K
K
K
K
K
K
2D Stre ss: 0.18
Trans for m: Log(X+1)
Resemblanc e: S1 7 Bray Curtis similarity
S
S
S
S
F
F
F
F
C
CC
C
S
S
S
S
F
F
F
F
C
C
C
C
S
S
S
F
F
F
F
CC
C
C
S
S
S
S
F
F
F
F
C
C
C
C
2D Stre ss: 0.18
Fig. 9. Spirobranchus giganteus MDS ordination of operculum abundance across (a) sites: Sa = Sampela; PK = Pak Kasim’s; K = Kaledupa, and R =
Ridge 1, and (b) habitats: F = reef flat; C = crest, and S = slope.
DISCUSSION
Spirobranchus giganteus abundance
Results from this study demonstrate that the abundance and distribution of Spirobranchus giganteus is non
random following that of its host (Bailey-Brock 1976), and changes in response to differential environmental
parameters. Therefore, the validity of this taxon as an indicator of reef health should not be overlooked (Bailey-
Brock 1976, Scott 1987, Frank & ten Hove 1992, Low et al. 1995, Floros et al. 2005).
In the Wakatobi Marine National Park, Indonesia, 52 coral species (27 of which previously undocumented,
Appendix II) were colonized by Spirobranchus giganteus, with eight coral species: Montipora danae, M.
informis, M. spumosa, M. venosa, Porites cylindrica, P. lobata, P. lutea and P. nigrescens, representing three
morphological types: branching, encrusting and massive, most heavily colonized. Such a non-random
distribution of S. giganteus on specific coral taxa has been well documented (Bailey-Brock 1976, Smith 1984a,
Scott 1987, Marsden 1987, Hunte et al. 1990a, Pey-Clausade et al. 1992, Dai & Yang 1995, Nishi 1996, Nishi
& Kikuchi 1996, Marsden & Meeuwig 1990, Floros et al. 2005), likely consequential of pre-settlement larval
preferences, differential mortality following settlement (Connell 1985, Hunte et al. 1990a) and subspecies level
differences (Nishi & Kikuchi 1996). However, larval settlement and recruitment varies in accordance to biotic
and abiotic parameters (Pawlik et al. 1991, Rodríguez et al. 1993, Day & Yang 1995, Qian 1999, Fox 2004).
The distribution and abundance of Spirobranchus giganteus was in concordance with profound differences in
composition and environmental conditions, both natural and anthropogenic, across the four study sites.
Differences in S. giganteus abundance were, however, most notable between Ridge 1 and Sampela, the former
being six times that of the latter. Such a marked difference in worm abundance is a reflection of larval
behaviour and/or substrate availability (Hunte et al. 1990b), thus environmental conditions. Univariate and
multivariate analysis revealed habitat complexity and live coral cover were highest at Ridge 1 and depauperate
at Sampela, coral morphology being the best explanatory variable for differences in both benthic cover and S.
giganteus abundance across sites and habitats. Coral morphology followed a typical bathymetric distribution of
branching on the reef flats to encrusting on the slope (Porter 1976), with stress tolerant massive species less
defined. However, the impoverished branching community at Sampela is characteristic of low wave action,
high turbidity and sedimentation rates, favouring massive and encrusting species due to morphological and
behavioural pre-adaptations such as phenotypic and photoacclimatory plasticity, colony polyp size,
reproductive strategy and recruitment survival (Stafford-Smith 1993, Anthony 2000, Edinger & Risk 2000,
Kelmo & Attrill 2001, Crabbe & Smith 2002, 2003, 2005, Kelmo et al. 2003, Fox 2004, Hennige et al. in
press). Such patterns may be attributed to intermediate disturbance levels, maintaining relative species diversity
within a reef community (Ostrander et al. 2000, Connell 1978), influenced by high wave exposure and water
currents at Ridge 1, and continuous resource exploitation and sediment re-suspension at Sampela. Furthermore,
comparatively high soft coral cover at Sampela and Kaledupa (Table 1) is characteristic of heavily disturbed or
overfished sites (Fox et al. 2003). Greater abundance of both overall live coral cover and S. giganteus at
Kaledupa, however, is probably an artifact of elevated wave activity, low turbidity and reduced human impact
(a)
(b)
15
at this site.
High water motion and localized upwelling at Ridge 1 (Smith pers. comm. 2006, Fig. 1b) provides elevated
nutrients for primary productivity, thus enhanced substrate and food availability (Jokiel 1978, Floros et al.
2005). Spirobranchus giganteus typically colonizes prominently positioned corals (Strathmann et al. 1984,
Hunte et al. 1990b, Martindale 1992, Dai & Yang 1995) in moderate-high wave exposure (Martindale 1992,
Nishi & Nishihira 1999, Mallela & Perry 2007), thus maximizing feeding efficiency for both worm
(Strathmann et al. 1984, Frank & ten Hove 1992) and host (Jokiel 1978). However, little is known of the
physiological effects of sedimentation on S. giganteus. Frank & ten Hove (1992) suggested differences in
branchial morphologies of S. giganteus (spiraled branchiae: reliant on ambient water currents preventing
excurrent refiltration) and S. teteraceros (paired circles: reduced filtration device) were an expression of
alternate filtering strategies at turbid sites. Yet both species were equally tolerant of varying sedimentation
regimes in vitro, thus the distribution and abundance of S. giganteus may be attributed to larval and substrate
availability in terms of host tolerance to environmental conditions.
Comparatively greater abundance of Spirobranchus giganteus on the branching corals Porites cylindrica and
P. nigrescens on the reef flats (≤ 3 m depth), of Ridge 1 and Pak Kasim’s (data not shown), was concordant
with previous observations (Frank & ten Hove 1992, Nishi & Kikuchi 1996), yet in contrast to other work
where abundance was highest between 6-18 m depth on massive and tabulate coral taxa (Hunte et al. 1990a,
Dai & Yang 1995, Floros et al. 2005) which may represent regional variation (Nishi & Kikuchi 1999). Habitat
structural complexity, thus colonizable area, profoundly influences the abundance and diversity of associate
communities (Gee & Warwick 1994, Attrill et al. 2000) with coral species richness peaks at intermediate depths
(reviewed by Cornell & Karlson 2000) in alignment with habitat complexity in the present study. Yet
colonizable area by S. giganteus was predominately branching Porites spp., K-strategists (competition adapted)
typical of Indonesian reef flats (Edinger & Risk 2000). Selection for such host taxa, apparently unoccupied by
superior competitor(s) (Rowley pers. obs. 2006), would decrease interspecific competition with other associate
organisms such as Dendropoma maxima and Lithophaga spp. (Peyrot-Clausade et al. 1992), further
maximizing reproductive success due to close proximity to conspecifics (Dai & Yang 1995, Rodríguez et al.
1993, Pawlik 1991). The apparent inverse bathymetric distribution of S. giganteus (Fig. 6b) may also be due to
planktonic larval displacement by water currents (Hunte et al. 1990a) or predation by predominantly
heterotrophic coral taxa (Anthony 2000). However, timing of spawning events during neap tides (see Beaver et
al. 2004, Hickson 2007) and a preference by young S. giganteus larvae for coral (Marsden 1987, Marsden et al.
1990, Marsden & Meeuwig 1990) and/or conspecific exudates, acting together with a known positive
phototaxis (Smith 1984a, b, Marsden 1984, 1986) may be adaptive helping to maintain larvae in surface waters
over the reef in the vicinity of a specific coral until competency (Marsden 1987).
Results from this study suggest selection by Spirobranchus giganteus larvae for host specific morphological
and behavioural characteristics may be adaptive and/or consequential of post-settlement mortality. Corals
commonly colonized by S. giganteus were competitively subordinate in terms of aggression suggesting
planktonic larvae of S. giganteus may be susceptible to the nematocysts of aggressive corals (Dai & Yang
1995). However, Smith (1984a) observed that searching larvae (from the Great Barrier Reef) appeared immune
from the polyps’ nematocyst discharge. The Spirobranchus genus does confer a degree of immunity to
nematocyst discharge (as observed by Smith 1984a) often inhabiting the aggressive hydrocoral Millepora spp.
(Hunte et al. 1990a, Dai & Yang 1995, Lewis 2006, Ben-Tzvi et al. 2006, this study). Furthermore, coral mucus
associated bacteria show host specificity (Bourne et al. 2007) with considerable antagonistic activity to other
organisms (Ritchie 2006). Such potential influences may be of significance.
In this study, all selected host taxa possessed small (1 – 1.5 mm diameter) plocoid corallites (Appendix II).
Whether this provides an increased surface area for larval settlement remains to be seen (see Floros et al. 2005
cf. Smith 1984a, Nishi & Kikuchi 1996), however, such host morphological traits increase photosynthetically
active tissue surface area, thus selective for optimal light capture (Porter 1976). This, combined with branching
morphology, providing a surface area three times that of the substratum (Dahl 1973), and multidirectional light
distribution due to scatter and reflection between particles in the water column, maintains photosynthetically
active tissue, enhancing overall coral accretion (Porter 1976). Calcification, therefore, is strongly influenced by
light intensity (Dark & Barnes 1993, Mass et al. 2007, Hennige et al. in press) with branching corals,
predominantly on the reef flats (Edinger & Risk 2000, this study), having fast growth rates (Latypov 2006)
compared to massive or encrusting taxa (Nishi & Kikuchi 1996). Moreover, S. giganteus tube length and body
size were shown to be larger on branching compared to massive poritids (Nishi & Nikuchi 1996 cf. Hunte et al.
16
1990b), suggesting S. giganteus may be morphologically selective for coral taxa in terms of overall worm
fitness. However, previous studies demonstrate selection for robust, slow growing massive hosts, inferring
longevity and stability (Hunte et al. 1990a, b, Martindale 1992, Dai & Yang 1995) compared to short lived
rapidly growing branching taxa (Hunte et al. 1990b).
Tube thickness follows host growth rate (Nishi & Kikuchi 1996, Nishi & Nishihira 1999), preventing
overgrowth of the aperture by host tissue (Scott 1987). Spirobranchus giganteus precipitates CaCO3 from
glands adjacent to the coral surface, therefore, it is possible that Ca2+ present in coral mucus is taken up and
used by the worm. Coral mucus is an important carrier of energy and nutrients with high concentrations of Ca2+
(Marshall & Wright 1998, Clode & Marshall 2002). Coral mucus maintains a Donnan equilibrium (medium
which separates an unequal distribution of diffusible ions between two ionic solutions) at the oral-sea-water
interface facilitating Ca2+ uptake by the coral (Clode & Marshall 2002). Coral mucus uptake (as illustrated by
Strathmann et al. 1984) and utilization by S. giganteus, resulting in nitrogen secretion (Rotjan & Lewis 2006,
reviewed by Rowley 2008), subsequent use by the host coral and zooxanthellae with a possible increase in
mucus Ca2+ concentration further utilized by the worm may be occurring. To test this hypothesis, the use of
45Ca and 14C (as used by Marshall & Wright 1998) and 15N (as used by Gresty & Quarmby 1991) may ascertain
any trophic recycling and/or niche partitioning (Tapanila 2004) occurring between S. giganteus, host coral and
its zooxanthellae. Furthermore, juvenile tube construction, via rapid carbonate (calcite or aragonite, Smith
1985, Rouse & Pleijel 2001) deposition, only proceeds in the presence of live coral (Smith 1984a). Selection
for photosynthetically active tissue, especially in a high energy environment, such as that seen in branching
corals, may therefore maintain survival, higher growth rate and reproductive potential. Interestingly, tubes of
the S. giganteus complex (Indo-Pacific, Appendix I) contain up to 100% aragonite (Smith 1985), at least 50%
more soluble than calcite (Mucci 1983). Marine organisms forming aragonite structures are particularly
susceptible to increased PCO2 (Feely et al. 2004, Hoegh-Guldberg et al. 2007, Hall-Spencer et al. in review).
Such taxa, therefore, harbour significance to marine systems in terms of global climate change.
Spirobranchus giganteus morphology
Many sessile marine invertebrates’ demonstrate marked morphological adaptations (Foster 1983) or
phenotypic plasticity (Spitze & Sadler 1996, Kelmo et al. 2003) between habitats. In the Wakatobi MNP
differences in worm morphology relative to host taxa were observed with Spirobranchus giganteus round
aperture abundance, predominantly on branching poritids, over five times that of spine aperture abundance.
Results, however, show differences in mean spine aperture abundance were dependent on a combination of site,
habitat and coral/morphology, further revealing the inconsistency of an already weak habitat main effect
between the reef flat and crest. Such variability in spine aperture abundance may, in part, be attributed to a finer
taxonomic resolution. Spine aperture, most likely assigned to Spirobranchus cf crucigerus and/or S.
corniculatus s.s. (Fig. 2c & a, S. spec. ‘type C & A’ of Smith 1985 respectively, see Fiege & ten Hove 1999;
ten Hove pers. comm. 2008. Note: S. cf crucigerus, possessing the most prominent aperture spine was more
frequently observed, however, operculum spines obscured by algae, invertebrates or sediment prevented further
delineation between the two taxa in the field) were observed by Smith (1985) to have a relatively wide host taxa
distribution, on massive and occasionally branching taxa. Furthermore, Smith (ten Hove pers. comm. 2008*)
noted statistical trends in the morphological distribution and variability of the S. giganteus complex on the
Great Barrier Reef. Such ecological and morphological variability, therefore, likely contributes to the
inconsistencies observed in the data.
Mean round aperture abundance across sites, habitats, coral species and morphology followed a similar
pattern to the overall Spirobranchus giganteus mean abundance (Fig. 8e-h cf. Fig. 6a-d respectively). However,
there was a significant interaction for site x coral species, and site x coral morphology (the latter showing no
main site effect) which was amplitudinal in origin (i.e. not due to “crossing-over”). Such interactions revealed
mean round aperture abundance on branching poritids to be consistently higher than for other coral species and
subsequent morphology at Ridge 1 and Pak Kasim’s; yet proportionality of abundance associated with the
different coral taxa between sites changed markedly. Out of such variability, univariate and multivariate
analysis revealed two main patterns; first, mean round aperture abundance was greatest on the reef flats, the
overall distribution consistently bathymetric in nature. Second, that such abundance is attributed to branching
corals (BIO-ENV r = 0.436). These patterns follow the preferred host taxa of branching poritids, in
comparatively greater abundance on the reef flats of Ridge 1 and Pak Kasim’s than Sampela and Kaledupa,
17
consequential of differences in influential magnitude exerted by local factors, such as hydrodynamic regime,
anthropogenic impact and state of reef recovery, influencing larval dispersal, settlement and post-settlement
mortality of both worm (Hunte et al. 1990a) and host (Connell 1985).
Patterns in round aperture abundance were largely concordant with operculum types attributed to S. gardineri
complex (Fig. 3b & c); multivariate analysis revealing greater abundance at Ridge 1 and on the reef flats. S.
gardineri complex possess a round aperture (Fig. 2b) with “none or only a small spine” (Fiege & Sun 1999)
and circular operculum plate with a long common process (Pixell 1913, ten Hove 1994, Fiege & Sun 1999; Fig.
3b & c, former most prevalent in the present study, Rowley pers. obs. 2006). In contrast, S. cf crucigerus (Fig.
3a) has a prominent aperture spine, conspicuous processes from a circular to egg-shaped operculum plate (S.
spec. ‘type C’ of Smith 1985; see Fiege & ten Hove 1999; ten Hove pers. comm. 2008), and were largely
present on massive poritids (Rowley pers. obs. 2006). In addition, morphological traits assigned to S. gardineri
sensu stricto (Fig. 3d), S. gardineri complex (Fig. 3d), and S. corniculatus sensu stricto (Fig. 3f), in terms of
operculum and aperture types were also observed in this study, however, operculum spines obscured by algae,
invertebrates or sediment, likely an artifact of host worm longevity or ambient conditions favouring such
organism proliferation, prevented further preliminary delineation between taxa, with a likelihood of
Spirobranchus spp. also noted in this area to be present (ten Hove pers. comm. 2008, see ten Hove 1970, 1994,
Fosså et al. 1996, Nishi 1996, Fiege & ten Hove 1999, Fiege & Sun 1999). However, operculum morphology is
notoriously variable (ten Hove 1970, 2008) and morphological characters traditionally used in Spirobranchus
taxonomy is potentially misleading (Kupriyanova et al. 2006). Therefore, this study presents observations on
morphological traits, tentative assignment to two most dominant taxa; S. gardineri complex and S. cf
crucigerus; with acknowledgement for further taxonomic revision through systematic and molecular analyses.
Morphological differences of associates to host morphology is not unknown (Hunte et al. 1990b, Dai & Yang
1995, Nishi & Kikuchi 1996, Chen et al. 2004) and maybe adaptive in terms of phenotypic plasticity or
divergence. A sharp aperture spine, prominent operculum processes, and diverse branchial colouration (Smith
1985), characteristic of Spirobranchus cf crucigerus, may act in predator defense when colonizing prominently
positioned corals. Interestingly, Acanthaster planci (crown of thorns starfish) are least selective for massive
poritids (De’ath & Moran 1998), being actively deterred by the operculum processes and branchial crown of the
worm suggesting predator-induced selection by the host (DeVantier et al. 1986). Moreover, retraction and
conspicuous branchial colouration, significantly reduces scarid predation risk regardless of worm palatability
(Kicklighter and Hay 2006). In contrast, individuals colonizing branching poritids typically possessed a round
aperture, relatively small branchial apparatus, with operculum morphology characteristic of Spirobranchus
gardineri complex. Such traits may be indicative of phenotypic responses to reduced predation pressure in such
cryptic habitats further protected by certain territorial Pomacentridae (Wilson et al. 2008). Furthermore,
reduced branchial apparatus may be due to spatial constraints between host branches and /or decreased reliance
on ambient currents by creating “separation between ingoing and outgoing currents” (Frank & ten Hove 1992)
compared to larger individuals on massive host corals. It could be argued that individuals within the
Spirobranchus giganteus complex are simply one species, habitat generalists (Spitze & Sadler 1996) exhibiting
phenotypic plasticity in the face of environmental change and host availability. However, the overwhelming
abundance of individuals with traits characteristic of Spirobranchus gardineri complex on branching corals,
thus habitat specialists (Spitze & Sadler 1996), cannot be ignored.
Alternatively, variability and habitat selection may be indicative of ecological divergence leading to
reproductive isolation as seen in Spirobranchus polycerus (Schmarda 1861) in Barbados (Marsden 1992). Such
taxa show distinct operculum types relative to habitat in Barbados, yet intermediate operculum types occur
elsewhere, and may represent hybridization. A similar scenario may also be occurring within the Spirobranchus
giganteus complex in the Wakatobi MNP, with incipient divergence-with-gene-flow (Rice & Hostert 1993,
Carlon & Budd 2002) between neighbouring populations, and hybridization accounting for the considerable
crossover between morphological characteristics or recognized taxa in this study. Intriguingly, morphological
traits can be altered by a few amino acid substitutions through mutation (Nei 2007). Elevated mutation rates
from ionizing energy of high temperatures and/or UV (‘evolutionary rate hypothesis’; Rohde 1992)
characteristic of high energy environments such as those on the reef flats, drives metabolic rates in small bodied
organisms, increasing growth rate, fecundity, reduced generation times with a concomitant increase in
speciation rate (Rohde 1992) and possibly elevated population size (Evans et al. 2005). Therefore, high
abundance of individuals on branching corals, may be indicative of incipient ecological divergence
consequential of resource partitioning (Slatkin 1980) between both worm and host. Cross-fertilization (Marsden
18
1992) and gamete recognition protein (see Biermann 1998) experiments coupled with allozyme (see Carlton &
Budd 2002) and /or mitochondrial cytochrome oxidase C subunit I analyses (see Chen et al. 2004) may provide
insights into the patterns of morphological variability demonstrated by S. giganteus species within the
Wakatobi MNP.
CONCLUSION
Results from this study demonstrate that the abundance and distribution of Spirobranchus giganteus is non
random following that of its host (Bailey-Brock 1976), and changes in response to differential environmental
parameters. Environmental disturbances such as wave action, marine resource exploitation, and sediment
loading influence morphology, growth form and availability of benthic organisms (Dai & Yang 1995), thus
differences in S. giganteus abundance between sites and habitats in the Wakatobi MNP are a reflection of
substrate availability consequential of environmental parameters. Thus, the significantly reduced abundance of
S. giganteus in areas of high turbidity and marine resource exploitation is noteworthy as an indicator of reef
health. Furthermore, selection for branching poritids may represent a trade off between substrate availability
and host stability of massive corals, in non turbid environments. Biological factors such as coral aggression,
predation, surface area availability or aperture overgrowth define coral associate survival or fitness (Scott
1987). Results from this study suggest S. giganteus is well adapted to symbiotic existence with its coral host,
favouring competitively subordinate species with small plocoid corallites. Furthermore, observations on
morphological traits present tentative assignment to the two most dominant taxa; S. gardineri complex on
branching poritids on the reef flats and S. cf crucigerus exhibiting generality in host and bathymetric
distribution. Such, adaptive selection may extend to intraspecific polymorphism revealing the potential for
phenotypic plasticity or incipient ecological divergence consequential of resource partitioning and response to
natural light. Further systematic and molecular studies may reveal possible genetic distance (Knowlton 1992,
Palumbi 1994) within the S. giganteus complex. Such evidence may provide insights into the intriguing nature
of the S. giganteus complex within the Indo-Pacific if, that is, one exists at all.
Acknowledgements. Special thanks would like to be extend ed to M. J. Attrill for continuous constructive guidance and supervision, J.
Trebilco and D. J. Smith for field supervision, Operation Wallacea for logistical support during field sampling, J. Summerton and C.
D. Todd for stimulating discussion, H. A. ten Hove and D. Fiege for enthusiastic taxonomic guidance.
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