Environmental gradients structure gorgonian assemblages on coral reefs in SE Sulawesi, Indonesia

Abstract

Indonesian coral reefs are the epicenter of marine biodiversity, yet are under rapid anthropogenically induced decline. Therefore, ecological monitoring of high diversity taxa is paramount to facilitate effective management and conservation. This study presents an initial report from a comprehensive survey of shallow-water (0–15 m) gorgonian assemblage composition and structure across sites with varying habitat quality within the Wakatobi Marine National Park (WMNP), SE Sulawesi, Indonesia. Current estimates of over 90 morphospecies from 38 genera and 12 families within the calcaxonian, holaxonian and scleraxonian groups are reported. This extensive survey confirms high local gorgonian abundance, diversity and species richness in the absence of anthropogenic influence and increasing with depth. Notably, morphological variants of the zooxanthellate species Isis hippuris Linnaeus, 1758, and Briareum Blainville, 1830, drive site and habitat assemblage differences across environmental gradients. Azooxanthellate taxa, particularly within the Plexauridae, drive species richness and diversity with depth. Of the 14 predictor variables measured, benthic characteristics, water flow and natural light explained just 30% of gorgonian assemblage structure. Furthermore, zooxanthellate and azooxanthellate taxa partitioned distinct gorgonian communities into two trophic groups—autotrophs and heterotrophs, respectively—with contrasting diversity and abundance patterns within and between study sites. This study strongly supports the WMNP as an area of high regional gorgonian abundance and diversity. Varying ecological patterns across environmental clines can provide the foundation for future research and conservation management strategies in some of the most biodiverse marine ecosystems in the world.

Full text

REPORT
Environmental gradients structure gorgonian assemblages
on coral reefs in SE Sulawesi, Indonesia
Sonia J. Rowley
1,2
Received: 9 April 2017 / Accepted: 7 April 2018
ÓSpringer-Verlag GmbH Germany, part of Springer Nature 2018
Abstract Indonesian coral reefs are the epicenter of mar-
ine biodiversity, yet are under rapid anthropogenically
induced decline. Therefore, ecological monitoring of high
diversity taxa is paramount to facilitate effective manage-
ment and conservation. This study presents an initial report
from a comprehensive survey of shallow-water (0–15 m)
gorgonian assemblage composition and structure across
sites with varying habitat quality within the Wakatobi
Marine National Park (WMNP), SE Sulawesi, Indonesia.
Current estimates of over 90 morphospecies from 38 gen-
era and 12 families within the calcaxonian, holaxonian and
scleraxonian groups are reported. This extensive survey
confirms high local gorgonian abundance, diversity and
species richness in the absence of anthropogenic influence
and increasing with depth. Notably, morphological variants
of the zooxanthellate species Isis hippuris Linnaeus, 1758,
and Briareum Blainville, 1830, drive site and habitat
assemblage differences across environmental gradients.
Azooxanthellate taxa, particularly within the Plexauridae,
drive species richness and diversity with depth. Of the 14
predictor variables measured, benthic characteristics, water
flow and natural light explained just 30% of gorgonian
assemblage structure. Furthermore, zooxanthellate and
azooxanthellate taxa partitioned distinct gorgonian com-
munities into two trophic groups—autotrophs and hetero-
trophs, respectively—with contrasting diversity and
abundance patterns within and between study sites. This
study strongly supports the WMNP as an area of high
regional gorgonian abundance and diversity. Varying
ecological patterns across environmental clines can provide
the foundation for future research and conservation man-
agement strategies in some of the most biodiverse marine
ecosystems in the world.
Keywords Gorgonian corals Indonesia Ecology Coral
reefs Environmental gradient
Introduction
The Indonesian archipelago is a center of marine biodi-
versity, likely a consequence of geological and oceano-
graphic processes influencing species diversification and
persistence (Carpenter et al. 2011; Sanciangco et al. 2013)
at local and regional scales. Eastern Indonesian reefs are
particularly diverse, with low climatic variability and
strong seasonal upwellings (Gieskes et al. 1988; Baars
et al. 1990), yet ecological assessments are sparse (To-
mascik et al. 2004). Increases in human population growth,
continual marine resource exploitation through coral min-
ing, and cyanide, dynamite and subsistence fisheries mean
that such biodiverse ecosystems are being destroyed before
their components are discovered (McManus 1997).
Therefore, comparative assessment of coral reef commu-
nities relative to their environment, including the increas-
ing assortment of anthropogenic influences, provides a
valuable resource for conservation management.
Topic Editor Dr. Alastair Harborne
Electronic supplementary material The online version of this
article (https://doi.org/10.1007/s00338-018-1685-y) contains supple-
mentary material, which is available to authorized users.
&Sonia J. Rowley
srowley@hawaii.edu
1
Department of Geology & Geophysics, University of Hawai‘i
at Ma¯noa, Honolulu, HI, USA
2
Invertebrate Zoology, Bernice Pauahi Bishop Museum, 1525
Bishop St, Honolulu, HI, USA
123
Coral Reefs
https://doi.org/10.1007/s00338-018-1685-y

Gorgonian corals (Cnidaria: Anthozoa: Octocorallia) are
conspicuous, diverse and often dominant components of
benthic marine environments, notably tropical shallow
reefs, deep-sea habitats and mesophotic habitats (Cerrano
et al. 2010; Rowley 2014b;Sa
´nchez 2016). Numerous
gorgonians are conservation ‘flagship’ species (e.g., Euni-
cella verrucosa Pallas, 1766; Tinsley 2005,Paramuricea
clavata Risso, 1826; Linares et al. 2008a; Cerrano et al.
2010), being ecologically diverse, long-lived engineering
taxa that maintain habitat heterogeneity and provide sec-
ondary space to other organisms (Buhl-Mortensen et al.
2010). Nevertheless, despite their ecological importance
and diversity, there is still little information on gorgonians
within the Indonesian archipelago (Tomascik et al. 2004).
Gorgonian corals are colonial suspension feeders pri-
marily defined by a semirigid scleroproteinaceous (gor-
gonin) axis with varying amounts of calcification deposited
primarily as magnesium calcite (Bayer 1961). The Octo-
corallia are characterized by polyps bearing eight pinnate
tentacles, and eight mesenteries dividing the gastrovascular
cavity (Bayer 1961). Originally classified under the order
Gorgonacea, gorgonians currently comprise the subordinal
groups, Holaxonia and Calcaxonia, and the group scler-
axonians within the order Alcyonacea (Bayer 1981). Even
though taxonomically obsolete, the term gorgonian con-
tinues to be used and indicates a specific structural group
that is differentiated from the ‘true soft corals’ (of the
subordinal group Alcyoniina characterized by lacking a
skeletal axis). Taxonomic identification of Indo-Pacific
gorgonians is, however, confounded by widespread
homoplasy, considerable morphological variability, cryptic
and sibling taxa (Knowlton 1993). Classified as ‘poorly
known’ (van Ofwegen 2004), shallow-water gorgonian
taxonomy within Central Indonesia remains in a state of
flux requiring integrative systematic, molecular and eco-
logical approaches.
Gorgonian ecology reflects, together or in part, repro-
ductive strategies and changes along environmental gradi-
ents relative to individual species tolerances (Fabricius and
Alderslade 2001). Environmental factors such as substrate
type, light, temperature, sedimentation, salinity, current
regime and flow rate (Garrabou et al. 2001) influence
gorgonian demography. Biotic factors, including competi-
tion, predation, symbioses, reproduction, settlement and
developmental properties, further refine local community
structure (Sa
´nchez 2004,2016). Such factors have been
shown to induce intra- and interspecific morphological
variability (West 1997; Linares et al. 2008b; Prada et al.
2008), habitat selection and colony orientation (Sa
´nchez
et al. 2003). Nevertheless, gorgonians are typically asso-
ciated with areas of low sedimentation and high water flow
through strong currents and upwellings (Yoshioka and
Yoshioka 1989); the largest planar arborescent colonies
occur in healthy reef environments (Linares et al. 2008b).
Complex habitats provide more vertical relief, colonizable
area and microhabitat variability than soft benthic substrata
(Etnoyer et al. 2010). Yet even with suitable substratum,
most gorgonians are absent in the areas of high turbidity
and sediment load, likely due to the physical impairment of
settlement, feeding, reproduction and growth (Anthony and
Fabricius 2000). In contrast, high-turbidity reefs in Singa-
pore, for example, support healthy azooxanthellate gor-
gonian communities (Goh and Chou 1994). Reduced
irradiance may therefore provide competitive release
(Rogers 1990) for azooxanthellate taxa, turbid habitats
being marginal for zooxanthellate gorgonians as they tend
to follow similar depth ranges to scleractinian corals with
no evidence of hard coral community replacement (Fabri-
cius and Alderslade 2001). Moreover, there appears to be
no evidence for negative associations with other benthic
space competitors in other areas (e.g., Yoshioka and
Yoshioka 1989).
Gorgonian distribution has been positively associated
with substrate availability and type (Goh and Chou 1994),
localized overlapping of species range sizes (as a function
of temperature) and benthic–pelagic coupling (Matsumoto
et al. 2007). Both azooxanthellate and zooxanthellate
gorgonians show eco-phenotypic interactions that strongly
correlate with depth (West et al. 1993) and size (Sebens
1982). Yet little is known of the ecology, reproductive
strategies and relative range sizes for most gorgonian
species in the Indo-Pacific.
Prominent drivers of gorgonian ecology, therefore,
remain unclear; studies usually describe regional differ-
ences (Singapore: Goh and Chou 1994; Caribbean: Sa
´n-
chez et al. 1997; Guam: Paulay et al. 2003; Hong Kong:
Fabricius and McCorry 2006; Japan: Matsumoto et al.
2007; tropical America: Sa
´nchez 2016). However, eco-
logical factors that regulate species diversity, as well as
consistency in species nomenclature, are of significant
research and conservation importance, especially within
the Indonesian archipelago, which is subject to continual
overexploitation and habitat loss. Published expeditions
within Central Indonesia, such as the ‘Siboga’ (Versluys
1902,1906; Nutting 1910a,b,c,d,e,1911; Stiasny 1937)
and ‘Snellius’ (e.g., Stiasny 1940; Verseveldt 1966) sam-
pled only deepwater and Alcyoniidae taxa, respectively,
which are largely unrepresentative of shallow-water gor-
gonians on Indonesian reefs. Annual rapid assessment
surveys are increasingly conducted by conservation agen-
cies (e.g., World Wildlife Fund, The Nature Conservancy)
throughout the Indonesian archipelago, with a view for
sustainable conservation management. Such surveys are
rudimentary with low taxonomic resolution for gorgonians.
The disparity between gorgonian diversity and ecological
assessment within Indonesia is therefore primarily due to
Coral Reefs
123

taxonomic uncertainty (Bayer 1981), with concomitant
difficulties in field identification (Fabricius and Alderslade
2001).
Little is known of gorgonian ecology within SE Sula-
wesi, Indonesia, despite their high regional abundance and
diversity. The aims of this study therefore were to (1)
characterize gorgonian assemblage composition and
structure across a gradient of habitat quality within the
Wakatobi Marine National Park (WMNP), (2) assess gor-
gonian diversity and abundance between reef habitats as a
function of depth within each site, (3) describe differences
in the distribution patterns of zooxanthellate (phototrophic)
and azooxanthellate (heterotrophic) gorgonian taxa and (4)
identify potential environmental driver(s) of gorgonian
assemblage structure.
Materials and methods
Study area
The WMNP (Tukang Besi Islands) is a remote island group
of ca. 13,900 km
2
in SE Sulawesi, Indonesia (Fig. 1a).
Established in 1996, the WMNP is the second largest
marine park in Indonesia containing ca. 600 km
2
of the
most biodiverse coral reefs in the world (Scaps and Denis
2007), with a low incidence of coral disease (0.57%;
Haapkyla
¨et al. 2007) and ENSO-induced bleaching events
(Crabbe and Smith 2003; Haapkyla
¨et al. 2007) likely due
to local upwelling (in April–November; Gieskes et al.
1988; Baars et al. 1990; Tomascik et al. 2004). Approxi-
mately 100,000 people live within the Wakatobi Marine
National Park, resulting in extensive subsistence marine
resource dependence and destructive commercial fisheries
in populated areas (Clifton 2013). Four sites were selected
around the islands of Kaledupa (ca. 17,000 people) and
Hoga (\100 people; Fig. 1b) which have different levels
of natural and anthropogenic disturbance (Electronic sup-
plementary material, ESM, Fig. S1), and distance from
shore. Sampela (impacted), an enclosed lagoon with an
outer reef wall ca. 400 m from a Bajo (sea gypsy) village
of ca. 1600 people, is subject to exploitation through coral
mining, fishing and high sediment loading due to natural
re-suspension, bioturbation through gleaning, and man-
grove loss. Furthermore, community wastewater is released
onto the reef (Haapkyla
¨et al. 2007). Buoy 3, ca. 500 m
offshore, is a moderately sheltered fringing reef with a
sheer reef wall containing small cryptic overhang habitats.
This site has an extended reef flat, which is subject to
frequent gleaning of marine invertebrates by local inhabi-
tants, in addition to recovering from coral mining and blast
fishing since 2004. Pak Kasim’s, ca. 500 m offshore, is a
topographically complex fringing reef, also subject to coral
mining and blast fishing on the reef flat and crest until
2004. Ridge 1 (healthy), ca. 1 km offshore, is an exposed
reef ridge with strong water currents (Fig. 1b) and upwel-
ling with a small amount of blast fishing on the reef crest in
2004 (D. J. Smith pers. comm.). The reef slope can also be
sheer with cryptic overhang habitats. All sites have a
pronounced reef flat of\3 m depth (Ridge 1 has a shallow
reef plateau at ca. 3 m depth), reef crest (3–6 m depth) and
slope ([6 m depth) with varying levels of sedimentation
draining from the reef flats during spring tides.
Fig. 1 a Location of the Wakatobi Marine National Park in SE Sulawesi, Indonesia. bStudy sites Sampela, Buoy 3, Pak Kasim’s and Ridge 1 of
the islands of Kaledupa and Hoga, respectively
Coral Reefs
123

Sample collection
Gorgonian distribution and abundance
Surveys were conducted between June and September 2009
using SCUBA, snorkeling and scaled digital photography.
Four 10 94 m belt transects were laid ca. 20 m apart,
running parallel to the reef contour in each reef habitat (flat
B3 m, crest ca. 6 m and slope ca. 12 m depth) within each
site. The 12 transects (four at each depth/habitat: flat, crest
and slope) were run at each study site, covering a total area
surveyed of 1920 m
2
. Individual colonies encountered
along each transect, including beneath canopy structures
(Goatley and Bellwood 2011), were photographed using a
Canon IXUS 900Ti, with WP-DC7 underwater housing and
INON UWL-105 AD 90.51 lens. Considering the
propensity for asexual fragmentation in some octocorals
(Fabricius and Alderslade 2001), an individual colony was
defined as an independent colony unassociated with any
other colony of the same phenotype (e.g., touching, as in
encrusting forms of Briareum spp.). Each image was taken
directly opposite and/or above each colony with a ruler for
scale. Voucher specimens (branch clippings of *2to8cm
in length) were preserved in 95% ethanol for taxonomic
clarification and stored at the Bernice P. Bishop Museum,
Honolulu, USA (Accession number: 2014.005). Sclerites
were dissolved from the surrounding tissue in 5% sodium
hypochlorite solution and visualized using optical micro-
scopy. Gross taxonomic identification followed Bayer
(1981), Fabricius and Alderslade (2001) and references
therein (see ESM taxonomic notes). A thorough taxonomic
account (morphological and molecular) of the gorgonian
corals from this region is currently underway. Taxa were
determined to be zooxanthellate through centrifugation as
described in Rowley (2014a). Many colonies were identi-
fied based on colony and branching morphology, polyp
characteristics and sclerite analysis, and assigned to
‘morphospecies’ within genera since most gorgonian spe-
cies within the Indo-Pacific are undescribed and there are
considerable crossover/intermediates with those that are.
However, individuals were grouped in accordance with
Bayer’s (1981) three-group system (suborders Holaxonia
and Calcaxonia, and scleraxonians group) and the families
and genera therein.
Environmental variables
Sites were characterized through the assessment of 14
environmental variables (Table 1). Benthic characteristics
were determined using transects as described for gorgonian
surveys and categorized according to English et al. (1997)
using point-intercept transects with points every 0.5 m
(Kingsford and Battershill 1998). Values are expressed as
% cover (±SE). Rugosity was measured with a 7.30-m
chain laid over three replicate transects per habitat and
calculated using the ratio of contoured surface distance to
linear distance (McCormick 1994). Rugosity was not
measured for overhangs due to logistical constraints.
Suspended sedimentation rates were assessed using four
standard 1-L sediment traps (English et al. 1997) deployed
in each habitat at all sites for 10 d. Sediment and water
were filtered (0.2 lm pore size), dried at 60 °C and
weighed (g dry weight d
-1
). Sediment grain diameter for
all samples was measured using Retsch Technology test
sieves (aperture size range 2.0, 1, 0.5, 0.125, 0.25, 0.063,
\0.063 mm), logarithmically converted, expressed as phi
(U) and classified under the Wentworth scale (Wentworth
1922). Water flow velocity (cm s
-1
) was measured using a
General Oceanics flow meter with a low-velocity rotor and
custom-made aluminum pipes for reef placement. Chloro-
phyll-a(lgL
-1
), salinity (PSU) and turbidity (NTU) were
measured using RBR XR-420 CTD data loggers. Tem-
perature (°C) and light (measured as lux and presented as
K
d(PAR)
) were measured using HOBO data loggers. The
loggers were placed upright at each transect depth,
recording every minute for up to 24-h cycles for at least the
study period. Latitude and longitude were determined by a
handheld GPS meter (Garmin eTrex). All variables except
latitude and longitude were entered into the statistical
models as raw values. Significant outliers were removed.
Outliers included light measurements during days of per-
sistent cloud cover and sediment traps containing fish and
invertebrates that may have skewed the end results.
Data analyses
Data were analyzed using univariate (SPSS v18.0) and
multivariate routines in the PRIMER-E v6.1.12 statistical
package (Clarke and Gorley 2006), with PERMANOVA?
v1.02 extension (Anderson 2001). Gorgonian assemblage
data were dispersion weighted, a transformation procedure
that accounts for the variance structure of individual spe-
cies (Clarke et al. 2006b). Differences in gorgonian
assemblages were analyzed with a two-factor (site and
habitat) crossed model with pairwise comparisons using
9999 permutations (PERMANOVA; Anderson 2001) based
on a zero-adjusted Bray–Curtis similarity matrix (Clarke
et al. 2006a). Results were visualized using a constrained
canonical analysis of principal coordinates (CAP; Ander-
son and Willis 2003), which reveals real group differences
from the maximum variation between groups. Prominent
taxa contributing to dissimilarities among gorgonian
assemblages were identified using similarity percentages
(SIMPER; Clarke 1993). The influence of dominant spe-
cies was further investigated using Pearson’s product-mo-
ment correlations for each species with each canonical axis
Coral Reefs
123

(Anderson and Willis 2003) and displayed as a vector
overlay on CAP ordinations. Morphospecies diversity
indices were used to quantitatively assess gorgonian
assemblage structure among the study sites and habitats;
indices were species richness as the total number of mor-
phospecies (S) present, and the Hill numbers N1, N2 and
modified ratio N21’ (Peet 1974) to assess the influence
(defined as the effect of certain morphospecies on the
assemblage sampled) of rare and dominant species and
taxonomic spread (equitability), respectively (Clarke and
Gorley 2006). For example, the higher the mean value for
each metric, the higher the influence of rare (N1) or
dominant (N2) morphospecies sampled in an assemblage.
Similarly, higher taxonomic spread (N21’) or evenness in a
sample indicates a similar number of individuals per
morphospecies and, therefore, low dominance of any one
morphospecies. Conversely, a low level of evenness
reveals that one or more morphospecies are represented by
a higher number of individuals and are thus dominating the
assemblage sampled. It is noteworthy that the diversity
indices presented here each assess a specific objective, e.g.,
the effect that rare or dominant morphospecies have/has on
the section of the assemblage sampled. Therefore, in this
study four indices were selected to describe the assem-
blages sampled, which have varying species richness and
diversity across sites and habitats. Species accumulation
curves with eight estimates of morphospecies richness
extrapolated to 48 samples (transects) were also assembled
in PRIMER-E v6.1.12 (ESM Fig. S2). Replicates were
permuted randomly 999 times. Zooxanthellate and azoox-
anthellate gorgonian distributions were tested for inde-
pendence using the Wald–Wolfowitz (runs) test (SPSS
v18.0; Wald and Wolfowitz 1943).
Predictor environmental variable(s) thought to influence
the ecological structure of gorgonian assemblages were
investigated using distance-based forward selection analy-
sis of linear models (DISTLM forward; McArdle and
Anderson 2001) based on a Euclidean distance matrix.
Variables were normalized and conditionally tested using
9999 permutations of the residuals under a reduced model
(Anderson 2001). This model was then replicated using
only the primary environmental variables as identified by
the initial ‘all variable’ DISTLM forward model. Results
were visualized using the distance-based redundancy
analysis ordination (dbRDA; McArdle and Anderson
2001).
Results
Study site characteristics
Environmental variables characterizing each study site
reveal a gradient of habitat quality from the impacted site
Table 1 Environmental
characteristics of the four study
sites in the Wakatobi Marine
National Park, Indonesia
Parameter recorded Mean value ±SE (where appropriate)
Site Sampela Buoy 3 Pak Kasim’s Ridge 1
Latitude (S) 005°2900100 005°2803800 005°2705700 005°2605700
Longitude (E) 123°4500800 123°4504700 123°4501800 123°4503800
Temperature (°C min–max) 25.61–29.36 24.69–29.25 26.59–30.457 24.06–28.07
Light (K
d(PAR)
min–max) 0.31–3.14 0.27–1.96 0.16–2.55 0.1–1.56
Salinity (PSU) 32.5 ±0.45 33 ±0.08 32.8 ±0.52 32.6 ±0.26
Flow (cm s
-1
) 5.02 ±2.18 4.17 ±1.35 11.22 ±2.55 30.54 ±2.61
Chlorophyll-a(lgL
1
) 0.3 ±0.01 0.27 ±0.03 0.14 ±0.01 0.35 ±0.03
Turbidity (NTU) 4.38 ±1.80 1.04 ±0.53 0.54. ±0.72 0.17 ±0.33
Sedimentation (g d
-1
,n= 12) 3.28 ±0.26 1.52 ±0.2 1.23 ±0.13 1.16 ±0.07
Sediment grain size (Un= 12) 5 [31.25–62.5 lm] 1 [0.5–1 mm] 1 [0.5–1 mm] 1 [0.5–1 mm]
Rugosity index (n= 12) 0.82 ±0.04 0.79 ±0.7 0.71 ±0.03 0.61 ±0.03
Hard coral (%, n= 12) 5.33 ±2.04 57.23 ±4.6 36.72 ±5.11 40.12 ±3.1
Dead coral/rubble (%, n= 12) 38.34 ±7.1 10.81 ±3.61 12.21 ±3.2 6.96 ±1.27
Soft coral (%, n= 12) 3.88 ±1.42 9.84 ±2.91 30.14 ±4.85 38.98 ±3.83
Biotic (%, n= 12) 4.31 ±1.21 13.12 ±4.43 4.26 ±1.65 6.99 ±1.44
Abiotic (%, n= 12) 48.14 ±6.3 9.0 ±3.13 16.67 ±4.26 6.95 ±1.9
All values expressed as mean (±SE) with discrete sample variables specific to each transect as n= 12 (four
transects at each of three habitat types consistent at each site), and the exception of diurnal temperature
range (°C), light (K
d(PAR)
) and sediment grain size (U)
Abiotic rock, rubble and sand; biotic sponges, ascidians and algae (English et al. 1997)
Coral Reefs
123

Sampela to the healthy reefs of Ridge 1 (Tables 1and 2).
Live benthic variable abundance, particularly soft coral
cover, increased toward Ridge 1, while abiotic variables
and dead coral decreased toward Ridge 1(Table 1). Hard
coral cover also increased toward Ridge 1, but peaked at
Buoy 3 due to a dominance of encrusting Montipora
colonies on the reef slope (Haapkyla
¨et al. 2007). Rugosity
also increased from low (0.82 ±0.04) at Sampela to
complex (0.61 ±0.03) at Ridge 1 (Table 1). Daily sedi-
mentation rate, turbidity, light attenuation and water flow
also followed the same trend, with sediment grain size
markedly smaller at Sampela than at the other sites. Sedi-
ment was of limestone origin except at Sampela, which had
smaller, darker and slightly oily sediment particles (S
Rowley pers. obs.). The annual range of both salinity and
temperature at each site was small, with the lowest tem-
perature at Ridge 1 (Table 1). Chlorophyll-avaried across
sites, the greatest variance being at the far ends of the
gradient.
Gorgonian distribution and abundance
A total of 3483 gorgonian colonies were documented in
this study; 126, 441, 1171 and 1745 recorded at Sampela,
Buoy 3, Pak Kasim’s and Ridge 1, respectively (Fig. 2;
Table 2). To date, over 90 gorgonian morphospecies from
38 genera and 12 families within the suborders/group
Calcaxonia, Holaxonia and Scleraxonia have been identi-
fied (Table 2). Species richness and diversity followed a
typical pattern of increase from the impacted site Sampela
to the healthy site Ridge 1 (Fig. 2; Table 2). This pattern of
increased species richness and diversity was similarly
replicated with depth except at Sampela, where most
colonies and species were found on the reef crest and flat
(Fig. 2). The contrast between the relatively constant
evenness values (N21’) with increases in both rare (N1)
and dominant (N2) morphospecies as depth increases and
disturbance decreases (Fig. 2) suggests that zooxanthellate
and azooxanthellate gorgonians have different distributions
in the WMNP. Diversity indices highlight the differences
between the two trophic groups (Fig. 3; azooxanthellate
diversity increases with depth as evenness decreases due to
differential distribution between taxa). Buoy 3 is an
exception; here, individuals were distributed relatively
evenly among morphospecies. In contrast, zooxanthellate
morphospecies diversity decreased with depth, with even-
ness relatively constant. This pattern was very weak at
Sampela and Buoy 3 due to the small number of zooxan-
thellate taxa present at depth at these sites (Fig. 5a, g;
Table 2).
Colony density (colonies 20 m
-2
) followed a very
similar pattern to species richness across all sites and
habitats (ESM Fig. S2a–c). The highest density of
gorgonian colonies was on the reef slope at Ridge 1
(171 ±120m
-2
; ESM Fig. S2a) largely composed of
azooxanthellate taxa (101 ±0.8 20 m
-2
; ESM Fig. S2c).
Pak Kasim’s had the greatest density on the reef crest
(101 ±1.7 20 m
-2
) dominated by zooxanthellate taxa
(76 ±1.4 20 m
-2
; ESM Fig. S2b). Overall colony density
at the degraded site Sampela was greatest on the reef crest
and completely attributed to zooxanthellate colonies
(13.25 ±1.7 20 m
-2
; ESM Fig. S2a, b), which was also
the case on the reef flat at Buoy 3 (29.75 ±2.4 20 m
-2
;
ESM Fig. S2a, b).
Gorgonian community structure
There were clear differences in gorgonian community
structure among sites and habitats within the WMNP
(Figs. 2,3,4,5and 6). Seven families from the Calcaxonia
(Ellisellidae, Isididae), Holaxonia (Acanthogorgiidae,
Plexauridae) and Scleraxonia (Briareidae, Subergorgiidae
and Melithaeidae) characterized reef habitats from low
diversity and abundance at the impacted site Sampela to
high diversity and abundance at Ridge 1 (Fig. 3). Fur-
thermore, morphospecies accumulation indices confirm
that richness was predominantly represented by azooxan-
thellate taxa, particularly a high number of rare taxa
observed in just one or two samples (ESM Fig. S3a, b;
Table S1).
The Isididae at Sampela were dominant across the flats
and crest (11.5 ±1 and 11.5 ±1.4 20 m
-2
, respectively),
with occasional Briareidae on the slope (2 ±120m
-2
). At
Buoy 3, Isididae were dominant on the reef flat (30 ±2
20 m
-2
), Acanthogorgiidae characterized overhangs on the
reef crest (20 ±1.5 20 m
-2
), and Plexauridae on the reef
slope (18 ±120m
-2
). Pak Kasim’s was dominated by
high numbers of the Isididae on the reef flat and crest
(68 ±3 20 and 58 ±220m
-2
, respectively), with Plex-
auridae and Briareidae on the reef slope (56 ±2 20,
27 ±120m
-2
, respectively). Isididae and Briareidae had
the greatest relative abundance on the ridge top at Ridge 1
(48 ±2 20, 30 ±320m
-2
, respectively), Plexauridae,
Isididae, Briareidae and Melithaeidae on the reef crest
(49 ±2, 36 ±3, 28 ±1 and 27 ±120m
-2
, respec-
tively), and Plexauridae and Briareidae on the reef slope
(63 ±0.1 20, 67 ±120m
-2
). In sum, pho-
totrophic/zooxanthellate taxa were low in species diversity
(Fig. 5; ESM Fig. S3c), but had the greatest relative
abundance on the reef flats and crest for Isididae and reef
slope for Briareidae (Fig. 3). Heterotrophic/azooxanthel-
late taxa, especially within the family Plexauridae, con-
tributed greatest to the increased biodiversity with depth
(Fig. 3).
Colony size is not reported in this study (it was recor-
ded; these data will be reported in a future study), but
Coral Reefs
123

Table 2 Gorgonian species inventory and abundance recorded in this study across sites in the WMNP
Taxon Z/AZ NT Sampela Buoy 3 Pak Kasim’s Ridge 1
[GROUP: Scleraxonians]
FAMILY: Anthothelidae Broch, 1916
Iciligorgia cf. brunnea (Nutting 1911)AZNT––––
Iciligorgia sp. AZ NT – – – –
Solenocaulon akalyx Germanos, 1896 AZ NT – – – –
Solenocaulon cf. tortuosum Gray, 1862 AZ NT – – – –
FAMILY: Briareidae Gray, 1859
Briareum sp. B
c
Z – 10 54 168 159
Briareum sp. E
d
Z – 3 19 35 325
Briareum violaceum (Quoy & Gaimard, 1833) Z – 4 1 – 15
FAMILY: Melithaeidae Gray, 1870
Melithaea ochracea (Linnaeus, 1758) AZ – 1 – 7 26
Melithaea squamata (Nutting 1911)AZ––2–5
Melithaea cf. spinosa (Ku
¨kenthal, 1878) AZ – – 2 1 1
Melithaea variabilis (Hickson, 1905) AZ – – – 2 3
Melithaea sp.1 AZ – – 2 – 48
Melithaea sp.2 AZ – – 10 – 72
Melithaea spp. AZ – – 11 11 59
Melithaea spp. AZ NT – – – –
FAMILY: Parisididae Aurivillius, 1931
Parisis fruticosa Verrill, 1864 AZ NT – – – –
FAMILY: Subergorgiidae Gray, 1859
Annella mollis (Nutting 1910a,b,c,d,e)AZ––9–20
Annella reticulata Ellis & Solander, 1736 AZ – – 2 14 19
Subergorgia rubra Gray, 1857 AZ NT – – – –
Subergorgia suberosa Pallas, 1766 AZ NT – – – –
[SUBORDER: Holaxonians]
FAMILY: Keroeididae Kinshita, 1910
Keroeides cf. gracilis Whitelegge, 1897 AZ – – 1 – –
FAMILY: Gorgoniidae Lamouroux, 1812
Guaiagorgia sp. AZ NT – – – –
Hicksonella princeps (Nutting 1910a,b,c,d,e)Z–– –– 1
Pinnigorgia flava (Nutting 1910a,b,c,d,e)Z–––2 1
Pseudopterogorgia sp. AZ – – – – 1
Rumphella aggregata (Nutting 1910a,b,c,d,e)Z–3 – 1 5
Rumphella antipathes Linnaeus, 1758 Z – – – 2 1
FAMILY: Acanthogorgiidae Gray, 1859
Acanthogorgia spinosa Hiles, 1899 AZ – – 2 9 32
Acanthogorgia sp.1 AZ – – 2 21 15
Acanthogorgia sp.2 AZ – – 83 17 12
Acanthogorgia sp.3 AZ – – 2 – 6
Anthogorgia spp. AZ NT – – – –
Muricella sp.1 AZ – – 2 2 –
Muricella sp.2 AZ NT – – – –
FAMILY: Plexauridae Gray, 1859
Astrogorgia bayeri Ofwegen & Hoeksema, 2001 AZ NT – – – –
Astrogorgia sp.1 AZ – – 22 205 160
Astrogorgia sp.2 AZ – – 20 23 62
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123

Table 2 continued
Taxon Z/AZ NT Sampela Buoy 3 Pak Kasim’s Ridge 1
Astrogorgia sp.3 [= Acanthomuricea]AZ––11–
Astrogorgia spp. AZ – 1 7 24 80
Astrogorgia spp. AZ NT – – – –
Bebryce cf. indica Thomson, 1905 AZ – – 1 10 52
Bebryce cf. nuttingi Stiasny, 1942 AZ – – 3 2 3
Bebryce spp. AZ NT – 5 6 10
Bebryce sp.1 AZ NT – – – –
Echinogorgia sp.1 AZ – – – – 2
Echinogorgia sp.2 AZ – – – 2 6
Echinogorgia spp. AZ – – 1 5 8
Echinogorgia spp. AZ NT – – – –
Echinomuricea cf. indomalaccensis Ridley, 1884 AZ – – 2 8 7
Echinomuricea sp.1 AZ – – – 2 2
Echinomuricea sp.2 AZ – – – 5 1
Echinomuricea spp. AZ – – 2 6 15
Echinomuricea sp. AZ NT – – – –
Euplexaura rhipidalis Studer, 1895 AZ – – 1 – 4
Euplexaura spp. AZ – – 4 7 6
Euplexaura sp.1 AZ NT – – – –
Menella sp.1 AZ – – 2 9 24
Menella spp. AZ – – 4 5 8
Paracis sp.1 AZ – – – – 1
Paracis sp.2 AZ – – – 4 2
Paracis spp. AZ NT – – – –
Paraplexaura sp.1 AZ – – 1 6 19
Paraplexaura spp. AZ – – 5 8 2
Trimuricea sp.1 AZ – – – 1 –
Trimuricea sp.2 AZ NT – – – –
Villogorgia sp.1 AZ – – – 1 2
Villogorgia sp.2 AZ – – 1 – 7
Villogorgia spp. AZ NT – 2 2 15
[SUBORDER: Calcaxonians] – –
FAMILY: Ellisellidae Gray, 1859
Ctenocella pectinata (Pallas, 1766) AZ NT – – – –
Ellisella ceratophyta Linnaeus, 1758 AZ – – 2 2 24
Ellisella plexauroides (Toeplitz, 1919) AZ – – – – 8
Ellisella sp. AZ – – 2 1 5
Dichotella gemmacea Milne Edwards & Haime, 1857 AZ – – – 6 3
Heliania cf. spinescens Gray, 1859 AZ NT – – – –
Junceella fragilis Ridley, 1884 AZ – – 2 – 16
Junceella juncea Pallas, 1766 AZ – – – – 1
Nicella sp. AZ NT – – – –
Verrucella cf. rubra (Nutting 1910a,b,c,d,e)AZ–– 21 5
Verrucella sp.1 AZ – – 4 3 3
Verrucella sp.2 AZ NT – – – –
Viminella sp. AZ – – – – 1
FAMILY: Ifalukellidae Bayer, 1955
Ifalukella yanii Bayer, 1955 Z NT – – – –
Coral Reefs
123

Table 2 continued
Taxon Z/AZ NT Sampela Buoy 3 Pak Kasim’s Ridge 1
Plumigorgia hydroides (Nutting 1910a,b,c,d,e)ZNT– 1 – –
FAMILY: Isididae Lamouroux, 1812
Isis hippuris[N]
a
Linnaeus, 1758 Z – 45 123 439 293
Isis hippuris[LT]
b
Linnaeus, 1758 Z – 59 7 71 49
Zignisis sp. AZ – – 1 – –
Unidentified Plexauridae
e
AZ – – 9 14 13
Total # colonies 126 441 1171 1745
Z and AZ, zooxanthellate and azooxanthellate taxa as classified for statistical analyses. Where morphological characters were highly variable
and/or not clearly distinguishable, these species were numbered or pooled and designated spp.
NT not present in transects but specimen collected
a
N—denotes normal branching, i.e., planar, short, tightly packed branched colonies
b
LT—denotes bushy long thick branched colonies
c
B—denotes branching morphology
d
E—denotes encrusting morphology
e
—denotes colonies where no specimens were sampled and thus indeterminate below the level of Plexauridae from images taken in the field
Fig. 2 a Gorgonian species richness. b–dHill’s diversity indices across sites and habitats (mean ±SE): N1, for the influence of rare species (b);
N2 for the influence of dominant species (c); and modified ratio for evenness N21’ (d). Sa, Sampela; B3, Buoy 3; PK, Pak Kasim’s; R1, Ridge 1
Coral Reefs
123

Fig. 3 Site-specific gorgonian family abundance (mean ±SE)
across sites and habitats within the Wakatobi Marine National Park.
aSampela, bBuoy 3, cPak Kasim’s, and dRidge 1. E, Ellisellidae; I,
Isididae; A, Acanthogorgiidae; P, Plexauridae; B, Briareidae; M,
Melithaeidae; S, Subergorgiidae
Fig. 4 Constrained CAP ordinations of gorgonian assemblages based on dispersion-weighted pretreated data and zero-adjusted Bray–Curtis
distance matrices, between asites and bhabitats. Vector overlays show species contributing the most difference among the a priori groups tested
Coral Reefs
123

Fig. 5 Mean zooxanthellate (a,c,e,g) and azooxanthellate (b,d,f,
h) gorgonian species richness (a,b), Hill’s diversity indices N1 for
the influence of rare species (c,d), N2 for the influence of dominant
species (e,f) and modified ratio for evenness N21’ (g,h) across sites
and habitats. Errors are standard errors Sa, Sampela; B3, Buoy 3; PK,
Pak Kasim’s; R1, Ridge 1
Coral Reefs
123

numerous azooxanthellate species were small (\10 cm
high) and located within sheltered crevices, overhangs, or
at the base or under other coral colonies (e.g., the soft coral
Sarcophyton Lesson, 1834, and tabulate scleractinian
Acropora Oken, 1815). Observations at depths greater than
those reported here suggest a continual increase in gor-
gonian diversity, abundance and size, plus a remarkable
frequency of new recruits (\5 cm tall, generalized esti-
mate across taxa from a combination of repeated annual
surveys [Rowley unpublished data] and published gor-
gonian studies e.g., Bramanti et al. 2005; Linares et al.
2008b). Additional gorgonian species present within the
WMNP not encountered during the surveys are
documented in Table 2. Additional observations to note
include colony asexual fragmentation by Junceella fragilis
(also noted by Fabricius and Alderslade 2001) and the
morphotypes of Isis hippuris and Briareum spp. Ad hoc
measurements and tagging of fragments of Isis morpho-
types at each study site revealed upward growth irrespec-
tive of site or depth (SJ Rowley unpublished data). Finally,
small colonies of Acanthogorgia and Bebryce were fre-
quently encountered at the base of large ([50 cm in
height) Annella reticulata Ellis and Solander 1736, A.
mollis Nutting 1910, and Melithaea spp. colonies. This
contrasted with occasional observations of the same
Fig. 6 Constrained CAP ordinations based on dispersion-weighted
pretreated data and zero-adjusted Bray–Curtis distance matrices, of
(a,c) zooxanthellate and (b,d) azooxanthellate gorgonian
assemblages between sites (a,b) and habitats (c,d). Vector overlays
show species contributing the most difference among the a priori
groups tested
Coral Reefs
123

species on the open reef, where it would invariably be
heavily infested with fouling organisms (ESM Fig. S4).
Gorgonian abundance varied significantly among all
sites and habitats with no interaction effects (PERMA-
NOVA: pseudo-F= 7.938, P\0.0001; pseudo-
F= 6.714, P\0.0001). Pairwise comparisons revealed
significant differences were between all sites and habitats,
most notably Sampela and Ridge 1, and the reef flat and
slope, respectively (Fig. 4). CAP analyses were consistent
with these results, where strong allocation success (number
of correct allocations to each factor level) clearly defined
distinct assemblage variability between sites and habitats
(Fig. 4; Table 2). SIMPER further revealed that particular
morphotypes within the zooxanthellate taxa Isis hippuris
Linnaeus, 1758, and Briareum Blainville, 1834, accounted
most for the differences in gorgonian assemblages among
sites and habitats (Table 3). Specifically, I. hippuris colo-
nies with long thick branches (hereafter I. hippuris[LT])
were prevalent on the reef flat at Sampela (Fig. 4a, b),
whereas low-lying branching Briareum species (hereafter
Briareum sp.B) were more abundant toward the reef slope,
particularly at Ridge 1 (Fig. 6a, c). In contrast, I. hippuris
colonies that were planar or multiplanar with short bran-
ches (hereafter I. hippuris[N]) were more abundant on the
reef crest (Fig. 4b). Encrusting Briareum colonies (denoted
Briareum sp.E) were more abundant on the reef flat, par-
ticularly at Ridge 1 (Fig. 4a, b). In addition, the azooxan-
thellate Acanthogorgia sp.2 contributed considerably to the
difference between the reef crest and flat (Fig. 4b). This
was due to its exclusive and abundant presence on the
ceilings of caves and overhangs, characteristic of Buoy 3.
Zooxanthellate versus azooxanthellate gorgonians
The dominance of the zooxanthellate gorgonians I. hip-
puris (1094 colonies) and Briareum spp. (792 colonies)
obscured distribution patterns of azooxanthellate taxa
(Fig. 4). A total of 1896 zooxanthellate and 1587 azoox-
anthellate gorgonian colonies were surveyed. Calcaxoni-
ans, holaxonians and scleraxonians were represented by
both zooxanthellate and azooxanthellate taxa with six
genera belonging to four families and 31 genera belonging
to 10 families, respectively. Taxonomic richness and
diversity of azooxanthellate species largely replicated that
of Fig. 2(and ESM Fig. S2a), increasing toward Ridge 1
and with depth (Fig. 5). Zooxanthellate taxonomic richness
and diversity also increased with site, but showed an
inverse relationship with depth, being greatest at the reef
crest and flat (Fig. 5).
The distributions of zooxanthellate and azooxanthellate
taxa were non-random [Wald–Wolfowitz (runs) test,
P\0.001]. The relative abundance of both zooxanthellate
and azooxanthellate taxa differed significantly across sites
(PERMANOVA, pseudo-F= 9.476, P\0.0001 and
pseudo-F= 3.997, P\0.0001, respectively) and habitats
(PERMANOVA, pseudo-F= 7.716, P\0.0001 and
pseudo-F= 4.687, P\0.0001, respectively). Yet an
interaction effect (pseudo-F= 1.925; P= 0.012) between
sites and habitats for azooxanthellate taxa revealed that
significance levels were principally driven by zooxanthel-
late gorgonians. Results were further supported by CAP
analyses; allocation success was weaker for azooxanthel-
late taxa at Pak Kasim’s, Buoy 3 and the reef crest
(Table 3). CAP and SIMPER analyses confirmed previous
results of I. hippuris[LT] on the reef flats at Sampela, and I.
hippuris[N] toward the reef crest (Fig. 6a, c; Table 3).
Briareum spp. followed a typical pattern of encrusting on
Table 3 CAP analyses results
assessing gorgonian species
assemblages for all (All spp.),
zooxanthellate (Z) and
azooxanthellate (AZ) taxa
between sites and habitats
within the WMNP, Indonesia
Factor m%var. Allocation success (%) d
2
P
Site Sampela Buoy 3 Pak Kasim’s Ridge 1 Total
All spp. 27 97.86 83.33 83.33 83.33 91.67 85.42 0.979 0.0001
Z 10 93.97 83.33 75 83.33 91.67 83.33 0.883 0.0001
AZ 28 99.53 100 66.67 50 100 79.17 0.991 0.0001
Factor m%var. Allocation success (%) d
2
P
Habitat Flat Crest Slope Ridge 1 Total
All spp. 17 89.55 87.5 68.75 81.25 – 79.17 0.946 0.0001
Z 5 82.24 87.5 56.25 68.75 – 70.83 0.676 0.0001
AZ 8 71.86 100 43.75 62.5 – 68.75 0.516 0.0009
mis the maximum number of principle coordinate (PCO) axes with minimal misclassification; % var.
quantifies total variance explained by the first mPCO axes; allocation success denotes the proportion of
correct allocations to each group; d
2
is the first squared canonical correlation size
Coral Reefs
123

the reef flats at Ridge 1, with low-lying branching colonies
characterizing the reef crest and slope, a pattern particu-
larly replicated at Pak Kasim’s (Fig. 6a, c). It is
notable that both Briareum spp. and I. hippuris colonies
had different coloration at depth and areas of high turbid-
ity; Briareum colonies were typically magenta on the reef
flat and crest and brown or gray on the reef slope and at
Sampela. Similarly, I. hippuris colonies were mustard
yellow on the reef flat and crest, but beige on the reef slope,
particularly at Sampela.
Azooxanthellate species within five families principally
defined the reef slope (Fig. 6d) except at Sampela. How-
ever, only two azooxanthellate colonies (Melithaea
ochracea Linnaeus, 1758, and an Astrogorgia sp.) were
encountered during the survey at Sampela (Table 2). Spe-
cies richness and diversity were similar to the first model
(Fig. 2) for the crest and slope except at Sampela (Fig. 5b,
d, f, h). The pattern of Acanthogorgia sp.2 on the reef crest
at Buoy 3 (Fig. 6b, d) was replicated by Melithaea sp.2 at
Ridge 1, which also inhabited the ceilings of caves, over-
hangs and crevices. Both species are undescribed. Meli-
thaea sp.1 showed distinct assemblages on the ridge top at
Ridge 1 (Fig. 6d). However, most azooxanthellate taxa
inhabited the reef slope with similar assemblage compo-
sition and distribution patterns across Buoy 3 and Pak
Kasim’s as evident by the reduced allocation success (an
indicator of reduced site and habitat distinction; Table 3)
and site x habitat interaction.
Environmental variables
Biotic variables (sponges, algae, ascidians, mollusks),
sediment grain size, light and rugosity explained 34.04% of
the variability in gorgonian assemblage structure (pseudo-
F= 3.864, P\0.001; Fig. 7a, c). Benthic covariates of
gorgonian assemblages and low influential variables
(temperature, salinity) were omitted from a repeated anal-
ysis revealing light, sediment grain size, rugosity and water
flow explained 41.65% of gorgonian assemblage variability
(pseudo-F= 3.645, P\0.001; Fig. 7b, d). The same
model was applied separately to zooxanthellate and
azooxanthellate species. Biotic variables, water flow and
light explained 33.7% of the variability in zooxanthellate
communities (pseudo-F= 4.732, P= 0.001), whereas
rugosity, biotic variables and sediment grain size explained
28.24% of the variability in azooxanthellate communities
(pseudo-F= 2.221, P\0.001). Results from the abated
model suggested that water flow, light and chlorophyll-
a(40.15%; pseudo-F= 4.232, P= 0.001), rugosity, sedi-
ment grain size and light (45.50%; pseudo-F= 2.222,
P= 0.001) had a significant influence on zooxanthellate
and azooxanthellate distributions, respectively.
Discussion
Current estimates of over 90 gorgonian species and distinct
morphotypes from 38 genera and 12 families were docu-
mented across shallow (0–15 m) coral reefs within the
WMNP, Indonesia. This study strongly supports the
WMNP as an area of high regional gorgonian abundance
and diversity comparable with previously described shal-
low-water gorgonians across the Indo-Pacific comprising
*50 genera within 14 families (Grasshoff 1999; Fabricius
and Alderslade 2001; Samimi-Namin et al. 2011; Reijnen
et al. 2014). Distinct community types across sites and
habitats along an environmental gradient are characterized
by contrasting distributions between zooxanthellate and
azooxanthellate gorgonians. This pattern results in part
from variations in habitat complexity, water flow and
natural light.
Gorgonian assemblage structure
Gorgonian distribution within the WMNP followed a gra-
dient of low diversity and abundance at the impacted site
Sampela to high diversity and abundance at Ridge 1.
Species richness and diversity increased with depth, a
pattern consistent with previous research on azooxanthel-
late benthic invertebrates within the area (e.g., Porifera:
Bell and Smith 2004), yet the inverse was true for zoox-
anthellate gorgonians, also seen for Scleractinia (Haapkyla
¨
et al. 2007). Similarly, gorgonian diversity is greater at
depth in other areas (Singapore: Goh and Chou 1994;
Caribbean: Sa
´nchez et al. 1997; Marianas: Paulay et al.
2003; Hong Kong: Fabricius and McCorry 2006; Japan:
Matsumoto et al. 2007; Palau: Fabricius et al. 2007;
Philippines: Rowley 2014b) with concomitant zooxan-
thellate octocoral abundance in the shallows (Great Barrier
Reef: Fabricius and Klumpp 1995; Thailand: Chan-
methakul et al. 2010).
Gorgonian populations within the WMNP reached a
mean density of up to 9 colonies m
-2
on the reef slope at
Ridge 1. They were dominated primarily by plexaurids and
branching Briareum. Similarly, densities of I. hippuris
colonies on the reef flat and crest of Sampela, even though
greater than other benthic taxa at this site, were still
comparatively lower (1.7 m
-2
) than at the other study sites
(up to 9 m
-2
at Pak Kasim’s). Densities were nevertheless
greater than the anthropogenically impacted gorgonian
populations reported at other geographic locations (Bra-
manti et al. 2014; Etnoyer et al. 2016). Similar densities to
those seen at Ridge 1, particularly for taxa in the Plexau-
ridae, have also been found at shallow depths (\10 m) in
the Caribbean (Etnoyer et al. 2010; Lenz et al. 2015), as
well as for the endemic and azooxanthellate precious coral
Coral Reefs
123

Corallium rubrum Linnaeus, 1758, in the Mediterranean
(Bramanti et al. 2014). However, the Plexaurids of the
WMNP were azooxanthellate and increased in colony
density and species diversity with depth, unlike those of the
Caribbean and tropical Atlantic, which are zooxanthellate.
Nonetheless, increased octocoral ecological assessments
particularly at greater depths may lead to the discovery of
new species (e.g., Etnoyer et al. 2010) in the WMNP. This
pattern is also seen in other Indo-Pacific locations (e.g.,
Philippines: Rowley 2014b), providing opportunities for
phylogeographic comparisons.
Differences in gorgonian assemblage structure between
sites and habitats were driven by morphotypes of the
zooxanthellate isidid I. hippuris and morphotypes of the
genus Briareum. The dominance of I. hippuris on shallow
reef flats may be due, in part, to differential disturbance
levels among study sites. As posited by the intermediate
disturbance hypothesis, continual disturbance maintains
species diversity, stability and biodiversity within a reef
community (Connell 1978; Aronson and Precht 1995;
Bohn et al. 2014). For example, strong upwelling and water
currents at Ridge 1 are frequent yet not necessarily dev-
astating disturbances. Frequent colonization of patches of
Fig. 7 Distance-based redundancy ordinations of the best predictor
variables for differences in gorgonian assemblages among sites (afull
variables; babated variables) and habitats (cfull variables; dabated
variables) within the Wakatobi Marine National Park. Vector overlays
depict both direction and strength of the most influential variables on
the dbRDA axes
Coral Reefs
123

disturbed reef would permit higher species diversity while
preventing competitive dominance, a pattern seen at Ridge
1. Extreme disturbances at the degraded site Sampela
include resource exploitation, high sedimentation rates and
benthic grazing by the echinoderm Diadema spp. (Hodgson
2008), which is reflected in the impoverished gorgonian
communities.
Habitat structural complexity, measured as colonizable
area, substratum type and light intensity, can determine
settlement choices and profoundly influence benthic com-
munity structure on coral reefs (Sa
´nchez et al. 1997;
Linares et al. 2008b). Yet the combination of predictor
biotic variables, sediment grain size, rugosity and light
explained only 23% of gorgonian assemblage structure
across clear environmental clines. Evidently, two inher-
ently related patterns are occurring. First, benthic variables
such as sponges, algae, hard and soft coral, and all mem-
bers of coral reef benthic communities co-vary with gor-
gonian distribution. Remodeling without these covariates
revealed that sediment grain size, light, rugosity and
chlorophyll-astill only explained 25% of gorgonian
assemblage structure. Second, this suggests that zooxan-
thellate and azooxanthellate gorgonian distributions con-
trast with each other, essentially reflecting two different
trophic groups, heterotrophs and phototrophs. This is more
likely due to differential resource use relative to natural
light as a function of bathymetry, than to interspecific
competitive forces among shallow-water gorgonians.
Zooxanthellate versus azooxanthellate gorgonians
The dominance of zooxanthellate taxa driving separation
between reef areas and location obscured azooxanthellate
distribution patterns. Trophic group separation (zooxan-
thellate = phototrophy; azooxanthellate = heterotrophy)
revealed a clear environmental gradient interaction with
depth. Thus, the groups displayed contrasting patterns, with
azooxanthellate species richness and diversity increasing
with depth, consistent with other areas (Goldberg 1973;
Goh and Chou 1994;Sa
´nchez et al. 1997; Paulay et al.
2003; Fabricius and McCorry 2006; Matsumoto et al. 2007;
this study), and the opposite pattern for zooxanthellate
taxa.
Zooxanthellate gorgonian assemblages
Zooxanthellate species are primarily responsible for dif-
ferences between site and habitat. Distinct I. hippuris
morphologies showed patterns of variability both within
and among sites, most notably bushy colonies with long
thick branches (I. hippuris[LT]) on the reef flat at Sampela
and planar short tightly packed branched colonies (I. hip-
puris[N]) at Ridge 1. Colony form can depend on feeding
strategy, and the same genotype can show different
resource allocation patterns in different environments
(Weiner 2004; Rowley 2014a). Alternatively, morpholog-
ical variants in sympatry are common in Cnidaria
(Knowlton 1993; Prada et al. 2008) and may be indicative
of phenotypic plasticity or incipient ecological divergence
in response to natural light and water flow. Variation
through increased branching surface area enhancing pho-
tosynthetic efficiency in shallow-water branching taxa
(Hennige et al. 2008; Rowley 2014a), coupled with a dual
mode of reproduction (external brooding and asexual
fragmentation; Rowley 2014a), may likely explain the
biological success of I. hippuris across environmental cli-
nes within the WMNP.
The zooxanthellate gorgonian I. hippuris is a gonocho-
ristic (Simpson 1906) external brooder (Rowley 2014a),
yet also displays considerable fragmentation. Asexual
propagation through fragmentation is not uncommon in
gorgonians. Because of being exposed to various levels of
disturbance, clones within a species can vary in their sen-
sitivity to various types of disturbances either across sites
or habitats within sites (Coffroth and Lasker 1998). How-
ever, vegetative fragments of I. hippuris were present on
the reef flats across all study sites, suggesting that mor-
photypes were not disturbance sensitive. Asexual propa-
gation through fragmentation facilitates rapid post-
disturbance recovery (Dauget 1992), which can result in
high local population abundance as evident by I. hippuris
on the reef flats in the WMNP.
The asexual fragmentation observed in Isis may enable
colonization of a disturbed area, particularly in the absence
of other taxa or suitable substratum for settlement. How-
ever, densities of I. hippuris[LT] colonies at Sampela were
low compared to the other sites. Therefore, even though I.
hippuris[LT] was the dominant taxon on the reef flats at
Sampela it was still not immune to the frequency of high
disturbances. In contrast to Sampela, Buoy 3 and Pak
Kasim’s, which are both subject to past destructive fishing
practices and bleaching on the former reef flats (ending in
2004; D. J. Smith pers. comm.), have higher gorgonian
abundance, diversity and colony density. However, con-
siderable loose rubble and anthropogenic gleaning on the
shallow (*1–3 m) reef flats of Buoy 3 likely impede set-
tlement success even at low levels of turbulence (Goh and
Chou 1994), thus resulting in minimal recovery and gor-
gonian presence. Yet high I. hippuris abundance on the
deeper (*3–5 m) reef flats at Pak Kasim’s may indicate a
combination of the lack of gleaning at this depth, an
absence of displacement of vegetative propagules by dis-
turbance, and the fact that this species is an r-selected
strategist. Therefore, the response of I. hippuris colonies at
Pak Kasim’s to reef recovery is apparently unencumbered
by inhibitors to settlement and growth. Hence, it thrives in
Coral Reefs
123

elevated current flow, low turbidity and minimal loose
substratum. This pattern may also be true for Briareum
sp.B on the reef slopes of Pak Kasim’s and Ridge 1. A
combination of reduced disturbance (no gleaning, reduced
hydrodynamics, low sedimentation), an increase in com-
petitor release from other benthic zooxanthellate taxa (e.g.,
scleractinians) with increased depth, and an ability to bud
asexually may, in part, explain the abundance of Briareum
sp.B at these sites.
Colony density can be a function of various aspects of
disturbance: type, frequency, intensity and type of sub-
stratum for species capable of asexual/vegetative propa-
gation (Coffroth and Lasker 1998). Clonal propagation of
tolerant clones may eventually lead to phenotypic and
physiological adaptation. Colonies of I. hippuris[LT] at
Sampela had a distinct morphology of long-branched bushy
colonies which may well have become adapted to a turbid
reef environment, whereas short branched planar colonies
(I. hippuris[N]) are found on healthy reefs (Rowley 2014a;
Rowley et al. 2015). Similarly, in the Caribbean, closely
related species within the zooxanthellate genus Antillo-
gorgia Bayer, 1951, also partitioned between two con-
trasting environments, with colony densities at a lagoonal
site still lower than that I. hippuris at Sampela (Sa
´nchez
et al. 1997). Densities were nevertheless greater for the
anthropogenically impacted gorgonian populations repor-
ted in other geographic locations (Bramanti et al. 2014;
Etnoyer et al. 2016). Therefore, gorgonian assemblages
within the WMNP show high regional abundance and
diversity compared to other geographic locations, as well
as the monospecific patches of I. hippuris morphotypes at
Sampela, a pattern also as seen in other gorgonian taxa
(e.g., Bramanti et al. 2014).
The zooxanthellate genus Briareum also influenced
separation between the factors site and habitat. Whereas I.
hippuris and scleractinian corals were most abundant on
the shallow reef flats and crest, low-lying branched Bri-
areum sp.B were more abundant on the reef slope, partic-
ularly at Pak Kasim’s and Ridge 1. Furthermore, numerous
asexual fragments and juvenile colonies were encountered.
This pattern mirrored its Atlantic congener, Briareum
asbestinum Pallas, 1766, which reproduces through asexual
fragmentation and external brooding producing low-dis-
persal philopatric larvae (Brazeau and Harvell 1994).
The dual reproductive strategy (external brooding and
asexual budding) observed in Briareum spp. may likely
explain, in part, the relative success of this species at
depths where few zooxanthellate taxa are encountered and
azooxanthellate diversity is high. Briareum morphotypes
also displayed habitat specificity with branching taxa at
depth and encrusting types on the high flow reef flat/ridge
top. Encrusting morphologies reduce drag in such high
flow environments (Bell and Smith 2004). However,
habitats characterized by low wave action, high turbidity
and sedimentation rates have also been shown to favor
encrusting Briareum spp. (Fabricius and Alderslade 2001;
Fabricius and De’ath 2004), likely due to morphological
and behavioral preadaptations such as phenotypic and
photoacclimatory plasticity, colony and polyp size, repro-
ductive strategy and recruitment survival (Anthony 2000).
Yet such patterns are in direct contrast with those in this
study. Furthermore, Briareum spp. abundance was con-
siderably lower compared to I. hippuris at Sampela; three
of the seventeen colonies encountered were encrusting.
Thus, branching and lobe-like, upward-projecting Bri-
areum morphologies may well be selected for in low light
and water flow, high turbidity and sedimented environ-
ments, reducing sediment smothering with increased sur-
face area-to-volume ratio for photosynthetic efficiency akin
to I. hippuris.
Azooxanthellate gorgonian assemblages
Azooxanthellate gorgonian assemblage structure showed a
relatively consistent pattern across sites and habitats except
at Sampela. However, an amplitudinal/additive interaction
(i.e., not due to ‘crossing-over’) revealed that proportion-
ality of abundance between sites and habitats changed
markedly for some taxa. Nevertheless, azooxanthellate
gorgonians showed assemblage patterns consistent with an
environmental decline from the healthy, high-energy Ridge
1 to the depauperate reef communities at Sampela. Com-
munity structure of azooxanthellate taxa varied little within
the deeper depths with only Plexauridae and Melithaeidae
present across all sites. Species within the most diverse
family, Plexauridae, drove diversity with depth, a pattern
generally observed in other azooxanthellate families (Goh
and Chou 1994; Fabricius and McCorry 2006; Matsumoto
et al. 2007; this study). Increased diversity and a high
frequency of recruits with depth suggest a deeper refugium
and competitor release from zooxanthellate corals. This
pattern is similarly replicated by sponge taxa (Bell and
Smith 2004) inferring no or positive interactions between
these two benthic groups (McLean and Yoshioka 2007),
both of which typically have powerful secondary metabo-
lites. Moreover, increased azooxanthellate diversity with
depth may represent a consistent biological source pool.
Such taxa are invaluable given past sea level variance in
addition to current and future natural and anthropogenic
disturbance, particularly with regards to the insidious
effects of destructive fishing practices and global climate
change.
Acanthogorgia sp.2 was the only azooxanthellate spe-
cies driving differences between and within factor levels in
the full statistical model. This is because of its exclusive
abundance on the ceilings of caves and overhangs on the
Coral Reefs
123

reef crest at Buoy 3. This specialized distribution may be
due to within-overhang microhabitats, pre-settlement larval
preferences such as negative phototaxis (Sa
´nchez et al.
1997), geotaxis or differential mortality following settle-
ment in other areas. Interestingly, species of Acanthogor-
gia and Bebryce were frequently encountered at the base of
large, chemically well-defended gorgonians such as An-
nella reticulata, A. mollis (Puglisi et al. 2002), Melithaea
spp. and the soft coral Sarcophyton (Fleury et al. 2006).
Such taxa may affect recruitment (Yoshioka and Yoshioka
1989) through waterborne exudates facilitating spatial
refugia from predation, competition (Hay 1986) or fouling.
Nonetheless, individual colonies of Acanthogorgia and
Bebryce, which were encountered on the open reef, not
close to other taxa, were heavily infested with fouling
organisms. Preferential settlement is, at present, unknown
for such taxa and would certainly warrant further study.
Furthermore, azooxanthellate Caribbean gorgonian larvae
prefer to settle on consolidated topographically complex
reefs and have longer pelagic larval duration (PLD; Sa
´n-
chez et al. 1997) than zooxanthellate taxa. Yet both fitness
enhancement through substratum selection and PLD are
unknown for Indonesian gorgonians. In this study, diversity
and abundance increased markedly with habitat complexity
toward Ridge 1 and with depth. This bioenvironmental
cline suggests selection and post-settlement success for
sites with high topographic complexity and consolidated
substratum. In contrast, low relief, unconsolidated fine-
grained substratum coupled with low water flow, high
sediment rate, continuous anthropogenic disturbance and
high grazing activity from Diadema spp. at Sampela
(Hodgson 2008) likely act in concert with reduced larval
availability, settlement and survival to result in low bio-
diversity at the Sampela end of the gradient.
Predictor variables highlight water flow, light and
chlorophyll-a for zooxanthellate species, and rugosity, sed-
iment grain size and light for azooxanthellate species. High
water motion and localized upwelling further enhanced by
strong water currents at Ridge 1 fertilize the reef with deep
nutrients for primary productivity and enhanced food
availability (Sebens 1984), maximizing species biodiversity
and abundance. Therefore, increased azooxanthellate spe-
cies richness and diversity on the ridge top at Ridge 1, cou-
pled with slightly reduced zooxanthellate species abundance
compared to Pak Kasim’s, are indicative of a natural reef
environment on Ridge 1 with overall reduced species dom-
inance. Taken together, sedimentation, rugosity, light and
water flow have been shown to be major factors controlling
local gorgonian populations (Sa
´nchez et al. 1997; Linares
et al. 2008b). This pattern seems true, in part, across envi-
ronmental gradients within the WMNP. However, differ-
ences between zooxanthellate and azooxanthellate
gorgonians and coral reef benthic variables may account for
the large amount of variation in gorgonian assemblage
structure unexplained by the predictor variable model.
Conservation implications
Ongoing quantitative ecological and concomitant taxonomic
analyses (combining morphological and molecular tech-
niques, e.g., McFadden et al. 2014) are necessary for the
conservation of tropical marine biodiversity. However, the
social and economic situation in the WMNP appears com-
plex, with an increasing shift from subsistence to income
fisheries through economic development (Pilgrim et al.
2007; Clifton 2013). This discard of folklore and marked
decrease in coral reef fish abundance within the region
(Exton 2010) inevitably leads to alternative adaptations and
ecological shifts. Here, morphotypes of taxa such as I. hip-
puris or Briareum can assist in reef health assessments,
particularly as such patterns are of increasing conservation
management importance, with I. hippuris now under a 5-yr
moratorium from exploitation (Ministry of Marine and
Fisheries Ministerial Decree No. 46/KEPMEN-KP/2014;
Nagib Edrus and Suman 2013). Furthermore, the ubiquitous
and diverse forms of gorgonians over wide geographic ran-
ges suggest that separate species exist at each location with
almost ‘one for each reef’ (Grasshoff 2001; Rowley et al.
2015). Therefore, biodiversity assessments cannot rely on
the bulk sampling methods of the past, which provide a
narrow biodiversity estimate unable to capture rare taxa
(e.g., CoBabe and Allmon 1994; Buzas et al. 2002).
Henceforth, ongoing ecological monitoring and thorough
taxonomic analyses within and among locations are of vital
importance.
Government agencies and local communities acknowl-
edge the disturbing reality of human encroachment on reefs
within the WMNP. Enforcement is often favored over
community education (Clifton 2003), yet neither is suffi-
ciently implemented due to budgetary and organizational
constraints and lack of political willingness (von Heland
et al. 2014). Well-meaning remedial fisheries management
strategies such as no-take zone (Unsworth et al. 2007) and
payoff strategies have been implemented, but withdrawn
instilling false hope and a lack of trust in cross-cultural
cooperation. Interestingly, Barnes-Mauthe et al. (2013)
demonstrated that regular temporary octopus fishery clo-
sures and local community involvement in both fisheries
monitoring and education led to significant increases in
catch and local income, fostering trust and cooperation
with local communities in Madagascar. However,
increased illegal fishing and overfishing on ‘open days’
thwarted conservation efforts over time (Benbow et al.
2014; Oliver et al. 2015). One can only hope that ongoing
education and financial support may be of some benefit to
local WMNP communities, yet in the face of human
Coral Reefs
123

necessity and dogmatic perception it is hard to predict and
sadly out of the scope of this research.
In summary, gorgonian distribution patterns within the
WMNP followed a gradient from low diversity and abun-
dance at the impacted site at Sampela to high diversity and
abundance at Ridge 1. Moreover, this environmental gradi-
ent response interacted with habitat, primarily as a function
of depth (thus light) structuring zooxanthellate and azoox-
anthellate taxa on shallow and slope reef habitats, respec-
tively. In this initial study in the WMNP, light availability
and benthic competitors appear to define the distribution and
abundance of most gorgonian taxa. Most notable are mor-
phological variants of the zooxanthellate species I. hippuris
and morphotypes of the genus Briareum, such biological
success likely being a consequence of dual reproductive
strategies (sexual and asexual reproduction) and morpho-
logical responses to different environments. Tests of physi-
ological resilience of respective morphotypes would be
informative for management plans and coral reef biodiver-
sity assessments. By determining species delineation and/or
potential ‘eco-morphotype’ environmental specificity,
monitoring of gorgonian taxa, in particular I. hippuris, could
therefore greatly assist environmental impact assessments
and identify areas of habitat degradation.
Acknowledgements This study was made possible by the generous
support of the Wakatobi Government, the Indonesian staff at ALAM
of the Wakatobi Marine National Park, and the Wallacea Foundation,
particularly Pak Iwan, Arif and Azrul. The State Ministry of Research
and Technology (RISTEK) granted research permits to Prof. D. J.
Smith, under whose auspices this work was conducted. This manu-
script benefited from spirited discussion and guidance from Profs.
S. M. Stanley, S. K. Davy, J. Gardner, C. Birkeland, C. Todd, L.
Watling, Drs. J. J. Bell, A. Rowden, R. L. Pyle and G. Williams, as
well as insightful comments from two anonymous reviewers. S. J. R
was supported by a Victoria University Wellington Doctoral Research
Scholarship and the Coral Reef Research Unit, with sponsorship from
P Duxfield at Cameras Underwater for camera equipment.
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