REPORT

Diversity and abundance of invertebrate epifaunal assemblagesassociated with gorgonians are driven by colony attributes

Joao Curdia1,2,3• Susana Carvalho1,3

• Fabio Pereira1• Jose Manuel Guerra-Garcıa4

•

Miguel N. Santos1• Marina R. Cunha2

Received: 15 August 2013 / Accepted: 12 March 2015 / Published online: 20 March 2015

� Springer-Verlag Berlin Heidelberg 2015

Abstract The present study aimed to explicitly quantify

the link between the attributes of shallow-water gorgonian

colonies (Octocorallia: Alcyonacea) and the ecological

patterns of associated non-colonial epifaunal invertebrates.

Based on multiple regression analysis, we tested the con-

tribution of several attributes (colony height, width, and

area, fractal dimension as a measure of colony complexity,

lacunarity as a measure of the heterogeneity, and ‘‘colo-

nial’’ epibiont cover) to abundance and taxonomic richness

of associated assemblages. The results highlight the var-

iation in the response of epifaunal assemblages to the

gorgonian colony characteristics. The nature and intensity

of the relationships were gorgonian species-dependent and

varied from one taxonomic group to another. For both

gorgonian species analyzed, the strongest predictor of

species richness and abundance of the epifaunal assem-

blages was ‘‘colonial’’ epibiont cover, possibly due to a

trophic effect (direct or indirect enhancement of food

availability) combined with the surface available for

colonization (species–area effect). Although structural

complexity is usually indicated as the main driver for rich

and abundant coral-associated assemblages, no significant

relationship was observed between fractal dimension and

the community descriptors; lacunarity, which reflects the

sizes of the inter-branch spaces, was only linked to taxo-

nomic richness in the assemblages associated with Lepto-

gorgia lusitanica. The validity of the paradigm that

structural complexity enhances biodiversity may be scale-

dependent. In the case of gorgonians, the effect of com-

plexity at the ‘‘garden’’ level may be more relevant than at

the individual colony level. This reinforces the need for the

conservation of gorgonian aggregation areas as a whole in

order to preserve host diversity and size structure.

Keywords Gorgonians � Invertebrate biodiversity �Structural complexity � Fractal dimension � Lacunarity �Multiple regressions

Introduction

A likely mechanism by which marine habitats might influ-

ence associated animal assemblages is through provision of

complex habitats; in general, structurally complex marine

habitats (e.g., sponge and octocoral aggregations, coral

reefs) support a greater number of species than simple ones

(e.g., Gratwicke and Speight 2005a). A previous study car-

ried out to characterize the biodiversity patterns of epifaunal

assemblages associated with gorgonians in southern Portu-

gal. Carvalho et al. (2014) showed high diversity values

compared to those reported for some scleractinian corals

around Lizard Island (Great Barrier Reef, Australia) (Stella

et al. 2010) and much larger than those reported by Goh et al.

(1999) and Kumagai and Aoki (2003) in shallow-water

gorgonians from Singapore and Japan. Potential

Communicated by Biology Editor Dr. Stephen Swearer

& Susana Carvalho

susana.carvalho@kaust.edu.sa

1 IPMA, Instituto Portugues do Mar e da Atmosfera, Av. 5 de

Outubro, s/n, 8700-305 Olhao, Portugal

2 Departamento de Biologia and CESAM, Universidade de

Aveiro, Campus de Santiago, 3810-193 Aveiro, Portugal

3 Red Sea Research Center, KAUST- King Abdullah

University of Science and Technology, Thuwal 23955-6900,

Saudi Arabia

4 Departamento de Zoologıa, Facultad de Biologıa,

Universidad de Sevilla, Avda Reina Mercedes 6,

41012 Seville, Spain

123

Coral Reefs (2015) 34:611–624

DOI 10.1007/s00338-015-1283-1

explanations for the high diversity of complex systems in-

clude a wider range of niche availability (Attrill et al. 1996;

Kovalenko et al. 2012), refuge against predators (Jordan

et al. 1996; Vytopil and Willis 2001; Gratwicke and Speight

2005b; Lingo and Szedlmayer 2006), and increased

availability of the colonizable surface translated into a

species–area relationship (Dean and Connell 1987; Attrill

et al. 2000; but see Matias et al. 2010). Rigorously testing the

role of habitat complexity is difficult because of the lack of

widely accepted and objective measures of habitat com-

plexity (Parker et al. 2001). Nevertheless, several proxies

have been applied to coral reef areas: surface topography of

the bottom (Ohman and Rajasuriya 1998), visual estimation

of habitat topography (encompassing reef topography, reef

height, rugosity, and number of refuge cavities; Wilson et al.

2007), cover of branching coral colonies (Chabanet et al.

1997), acoustic roughness (Bejarano et al. 2011), habitat

assessment score (integrating rugosity, variety of growth

forms, height, refuge size categories, percentage live cover,

and percentage hard substratum; Gratwicke and Speight

2005a), and fractal dimension (Bradbury and Reichelt 1983;

Knudby and LeDrew 2007; Zawada et al. 2010). At the scale

of the individual colony, fractal dimension has also been

applied to quantify coral shape (Martin-Garin et al. 2007),

morphological variability (Kruszynski et al. 2007), or even

for modeling coral growth (Merks et al. 2003). Measurement

of fractal dimension (D) allows a formal estimate of a

habitat’s physical complexity to be obtained, regardless of

the specific structural components (Beck 2000).

Invertebrates that rely on corals for food, shelter, or

settlement cues dominate the biodiversity of coral habitats

(reviewed by Stella et al. 2011). Small invertebrates are

expected to have stronger relationships with habitat char-

acteristics (shape, niche availability, complexity) compared

to fish because of their reduced mobility and predominantly

sedentary behavior. Consequently, small invertebrates are

potentially more susceptible to alterations in habitat (Stella

et al. 2010). The role of coral host attributes in structuring

the assemblages of associated invertebrates has been

assessed for the hexacorals Pocillopora and Acropora

(Vytopil and Willis 2001; Stella et al. 2010 and references

therein) but not for octocoral species, such as gorgonians.

Although most studies indicate a relationship between

epifaunal abundance and species richness with the habitat

structure of coral colonies (Abele and Patton 1976; Coles

1980; Caley et al. 2001; Vytopil and Willis 2001; Stella

et al. 2010), results were not consistent. A few studies

focusing on invertebrate fauna associated with gorgonians

(Octocorallia: Alcyonacea) have already been undertaken;

however, limited information is available, especially in

shallow temperate Atlantic waters, on the effect and extent

that the attributes of gorgonians have on the levels of local

biodiversity. Along with other corals, gorgonians have

been pointed out as foundational species in the sense that at

both individual colony and aggregation levels, high bio-

diversity values of the associated assemblages are main-

tained. This is achieved by providing a great variety of

niches ranging from sheltered cavities to high water-flow

areas with little sedimentation (Buhl-Mortensen and Mor-

tensen 2005).

Gorgonian aggregations are frequent in the Northeast

Atlantic and Mediterranean Sea (Gori et al. 2011; Curdia

2012) and were recently proposed for the OSPAR (Con-

vention for the Protection of the marine Environment of the

Northeast Atlantic) list of protected habitats (Anonymous

2011), because of their vulnerability and high conservation

value. In a previous study, we demonstrated the high bio-

diversity associated with shallow gorgonian gardens on the

south coast of Portugal (Curdia 2012). Herein, we provide

the first quantitative data on the relationship and consis-

tency between the abundance and biodiversity of the as-

sociated epifaunal assemblages and a set of gorgonian

colony attributes. The colony attributes are intended to

represent the effects of the surface available for coloniza-

tion, the structural complexity and heterogeneity, and the

functional (trophic) intricacy. In previous studies, namely

on epifaunal assemblages associated with seagrasses and

macroalgae, epiphytes were found to have a relevant role in

structuring associated mobile epifaunal assemblages (Ca-

cabelos et al. 2010). On the other hand, among octocorals,

aggregations of epibionts (mainly hydrozoans and bry-

ozoans) are known to develop on branches showing signs

of tissue damage (Bavestrello et al. 1997). Therefore, they

were also considered in the present study. Specifically, we

assessed the following hypotheses: (1) higher surface area

will result in increasing diversity and abundance of asso-

ciated epifaunal organisms (i.e., solitary organisms able to

be quantified in terms of abundance); (2) higher structural

complexity of gorgonians will result in increasing diversity

and abundance of associated epifaunal organisms; (3)

‘‘colonial’’ epibiont cover (i.e., sessile organisms unable to

be quantified in terms of abundance; e.g., bryozoans, hy-

drozoans, sponges, and macroalgae) of gorgonians has a

relevant role in structuring associated epifaunal assem-

blages; and (4) different taxonomic and/or functional

groups will respond differently to gorgonian attributes as

they have different habitat requisites.

Materials and methods

Gorgonian species selected and their attributes

The genera Eunicella and Leptogorgia have a worldwide

distribution. For the purposes of the present study, we se-

lected Eunicella gazella and Leptogorgia lusitanica, which

612 Coral Reefs (2015) 34:611–624

123

are widely distributed and among the most abundant gor-

gonians on the southern Portuguese coast (Curdia et al.

2013). Although both species belong to the family Gor-

goniidae, morphologically they are different: L. lusitanica

colonies are generally larger in width than in height, while

E. gazella colonies are more evenly shaped (i.e., display

similar width and height). Leptogorgia lusitanica colonies

may reach up to 80 cm in width, while E. gazella is a small

species reaching a maximum of 30 cm in height. Branches

of L. lusitanica may have different colors, while E. gazella

branches are generally white and thicker (Table 1).

In order to assess the effect of surface available for

colonization, we measured the height and maximum width

of each colony and estimated the total surface area. Both,

maximum height and width were measured in the labora-

tory. Using a tripod to keep a fixed linear distance to the

gorgonian (and thus maintaining scale), each colony was

photographed with a digital camera at right angles (90�).Analysis of the photographs, using the IMAGE J software,

gave an estimation of the total surface area of the colony.

Due to the relative bi-dimensional structure of the gor-

gonians, the estimation of the total surface area was de-

termined instead of the volume. Structural complexity was

inferred by measuring fractal dimension (D), while lacu-

narity was calculated as a proxy for heterogeneity based on

the analysis of the photographs with the IMAGE J software

(Table 1). Specifically, for fractal analysis, the box-

counting method was used, which involves laying a square

mesh grid of various sizes (r), over the gorgonian image

(fractal) to count how many boxes (N) are required to cover

it completely. To implement the box-counting Method, the

plugin FracLac for Image J (Karperien 1999) was used.

The sizes of the square boxes forming the grid varied from

2 to 200 pixels using the following custom sizes (2, 4, 8,

10, 20, 50, 100, and 200 pixels). The number of boxes (N)

that contain any part of the fractal object (gorgonian) was

automatically counted for each iteration with different box

sizes. The fractal dimension, which is characteristic of the

morphology (i.e., the overall structure of the gorgonian

colony), is defined as the structural fractal dimension (D)

D ¼ logN

log r

and it was calculated by the software as the mean fractal

dimension over 50 scans of differing grid positions. This

fractal dimension is meaningful for objects with complex

outlines such as gorgonians (Martin-Garin et al. 2007).

Lacunarity describes the texture of a fractal, using the

size distribution of holes of that fractal. If a fractal has

large gaps or holes, it has high lacunarity (Karperien 1999).

Lacunarity was calculated as:

Ekr ¼ 1 þ rrlr

� �2

where r is the standard deviation of the number of pixels

and l is the average number of pixels in squares of size

r. During the calculation of Ek, the pixels of the image

background were considered together with the object pix-

els. The mean lacunarity value was calculated for 50 grids

of different origin.

Besides these morphological attributes, the abundance of

macroscopic algae, cnidarians, bryozoans, sponges, and hy-

drozoans was scored by a semiquantitative index ranging

from 0 to 4 (0—absent, 1—rare, 2—common, 3—abundant,

and 4—very abundant). In order to minimize bias, scoring was

always carried out by the same observer. For simplicity, this

relative index will be hereafter designated as CEC, ‘‘colonial’’

epibiont cover, where the term colonial is used loosely to

represent modular organisms (Carvalho et al. 2014). CEC will

be used to infer the enhancement of functional intricacy of the

gorgonian colonies derived from the presence of sessile or-

ganisms, which may provide additional ecological niches and/

or a greater variety of food resources for the associated in-

vertebrate assemblages. For each colony, CEC will be the sum

of the scores of each epibiont observed (Table 2).

Study areas and sampling design

Sampling was undertaken in two consecutive summers (July

2010 and August 2011), at Pedra da Greta (PG), the main

rocky subtidal area in the central part of the Algarve coast.

The area is located at a depth of approximately 15 m and is

roughly 3.6 km in length and ranges from 20 to 90 m in

width. It presents high heterogeneity with a wide range of

features that encompass flat surfaces with high sedimenta-

tion and large blocks that can reach a height of 4 m. How-

ever, the area is characterized by numerous, small canyon-

like ridges that cut large, solidified, ancient belts of sand

dunes creating a ‘‘giant’s causeway’’ like scenery. These

channels can be up to 2 m wide, but they are more com-

monly 1–1.5 m wide. Gorgonians are present all over the

Table 1 Minimum (min) and maximum (max) values for the gor-

gonian attributes considered in the analyses: area (mm2); width (mm);

height (mm); D, fractal dimension; L, lacunarity; CEC, ‘‘colonial’’

epibiont cover

Attributes Eunicella gazella Leptogorgia lusitanica

Min Max Min Max

Area 507.28 12,851.13 496.85 24,316.12

Width 29.91 236.35 70.03 441

Height 53.51 223.64 51.27 445

D 1.52 1.81 1.58 1.79

L 0.93 2.99 0.81 4.84

CEC 0 28 0 30

See text for further details

Coral Reefs (2015) 34:611–624 613

123

area, but their density varies considerably, with an average

number of 5.83 colonies m-2 (maximum of 31 colonies

m-2; unpublished data). In the shallow continental shelf of

the Algarve, the most common gorgonian species are E.

gazella, L. lusitanica, E. labiata, E. verrucosa, and Lepto-

gorgia sarmentosa (Curdia 2012), although low abundances

of some other rare species are observed. This study focuses

on the two most common species, E. gazella (average 2.65

colonies m-2, max 18 colonies m-2) and L. lusitanica (av-

erage 1.81 colonies m-2, maximum 18 colonies m-2). It is

very common that in shallow continental shelf areas (down

to 30 m) these two species coexist. This is especially true

either in sloped areas or in the ridges that cut the large

blocks, which are present in the upper parts of the rocky

formations. However, L. lusitanica is less common in areas

with high sedimentation, such as the bottom parts of the

ridges where another Leptogorgia species, L. sarmentosa,

becomes more frequent and abundant (Curdia et al. 2013).

The size distribution of E. gazella ranges from 1 to

22 cm in height (mean: 9 cm) and is skewed toward small

sizes, but with a broad range of sizes that are well repre-

sented (Curdia 2012). Leptogorgia lusitanica also presents

a skewed distribution toward small colony sizes (2–40 cm

height, mean: 7.9 cm), but with a clear dominance of small

sizes (Curdia 2012). In the study area, a large percentage of

gorgonian colonies were damaged ([90 %, unpublished

data), especially Eunicella species (40 % of E. gazella

colonies had more than 25 % of their colony damaged).

Underwater observations indicated that algae, barnacles,

bryozoans, and zoanthids mostly colonized the damaged

areas. For the purpose of this study, the colonies that were

highly damaged were not collected.

The summer period was chosen because it generally

corresponds to the peak of invertebrates’ diversity and

abundance in this region. In each sampling period, 18

colonies of each species were collected with different

lengths totaling 72 colonies. Each colony was enclosed in a

plastic bag to prevent faunal loss and to assure only or-

ganisms on the colony were being collected and then

carefully detached from the hard substrate. Extra care was

taken to prevent the collection of any extra material, such

as sediment, surrounding the base of the colony. All gor-

gonians were transported to the laboratory for processing.

Biodiversity of associated epifaunal assemblages

In the laboratory, the colonies were preserved in 96 %

ethanol. All samples were washed through a 100-lm mesh

sieve, and colonies were observed under a magnifying

glass to ensure that all fauna and flora had been removed.

All specimens associated with each colony were preserved

Table 2 Taxonomic list of the epibionts found on the 72 colonies

surveyed and accounted for in the ‘‘colonial’’ epibiont cover

Group FO (%)

EG LL

Macroalgae

sp. 1 41.7 52.8

sp. 2 55.6 47.2

sp. 3 22.2 30.6

sp. 4 13.9 5.6

sp. 5 13.9 2.8

sp. 6 0.0 2.8

sp. 7 13.9 11.1

Porifera

Porifera sp. 1 2.8 8.3

Porifera sp. 2 11.1 16.7

Cnidaria, Hydrozoa

Halecium sp. 41.7 8.3

Laomedea sp. 50.0 36.1

Gymnangium montagui 0.0 5.6

Sertularella sp. 16.7 5.6

Aglaophenia sp. 0.0 2.8

Sertularia sp. 13.9 2.8

Hydrozoa sp. 1 41.7 52.8

Hydrozoa sp. 2 5.6 8.3

Hydrozoa sp. 3 0.0 2.8

Bryozoa

Celleporina sp. 11.1 13.9

Fenestrulina sp. 0.0 2.8

Cf. Microporella sp. 8.3 11.1

Schizobrachiella sp. 2.8 2.8

Schizoporellidae sp. 1 13.9 5.6

Pentapora fascialis 2.8 2.8

Beania sp. 5.6 0.0

Bugula sp. 7.0 10.0

Scrupocellaria sp. 15.0 12.0

Cellaria sp. 16.7 11.1

Chartella sp. 13.9 8.3

Electra pilosa 11.1 16.7

Cf. Vesicularia sp. 41.7 38.9

Crisia sp. 22.2 11.1

Tubulipora sp. 19.4 19.4

Gymnolaemata sp. 1 0.0 5.6

Gymnolaemata sp. 2 2.8 2.8

Gymnolaemata sp. 3 11.1 19.4

Gymnolaemata sp. 4 2.8 2.8

Arthropoda

Cirripedia 69.4 61.1

FO, frequency of occurrence; EG, Eunicella gazella; LL, Leptogorgia

lusitanica

614 Coral Reefs (2015) 34:611–624

123

in 96 % ethanol and afterward identified to the lowest

practical taxonomic level. To estimate species richness

(i.e., the number of species per colony), unidentifiable or-

ganisms were, whenever possible, differentiated into dif-

ferent operational taxonomic units (OTUs). If animals were

juveniles and/or were extremely damaged and it was not

possible to recognize whether they were different entities

or belong to any of the already identified species, they were

not used in the analyses. The number of taxa and indi-

viduals per colony, as well as the Hurlbert (1971) expected

number of species [ES(n)], was calculated both for the

whole assemblage and for the main taxonomic groups

separately (Arthropoda, Mollusca, Polychaeta). Feeding

habits were also ascribed for all OTUs with more than ten

individuals, based on the literature available.

Data analysis

In order to assess the relationship between gorgonian at-

tributes and the biodiversity and abundance of the associated

epifaunal assemblages, Spearman rank correlations were

performed. The best combination of gorgonian attributes

explaining the diversity and abundance patterns of the as-

sociated epifaunal assemblages was determined using a

backwards stepwise multiple generalized linear regression.

This approach, recommended whenever colinearity between

independent variables is suspected (Haedrich et al. 2008),

begins with a full model, including all independent variables.

Then, based on standard criteria, the variables failing at

contributing to the explanation of the dependent variable

(number of species or abundance) are systematically

eliminated (Younger 1979). The relationship between epi-

faunal feeding habits and CEC was investigated using re-

gression analysis. Differences in epifaunal assemblage

structure between gorgonian species, as well as the rela-

tionship between assemblage structure and the CEC, were

analyzed by a distance-based redundancy analysis (dbRDA;

McArdle and Anderson 2001). In the present study, dbRDA

was performed to order biological samples from each colony

as a function of the attendant epifaunal composition and

structure, using the CEC value for the most common colonial

taxa as explanatory variables. For the present analysis, the

modified Gower dissimilarity measure (Anderson et al.

2006) was used after removing singletons (i.e., taxon rep-

resented by a single organism or found on a single colony)

from the community data matrix.

Results

Associated epifaunal assemblages were numerically

dominated by arthropods, accounting for 48 and 65 % of

total abundance in E. gazella and L. lusitanica, respectively

(Fig. 1a). Mollusks were also abundant in both gorgonians

(18 % in E. gazella and 22 % in L. lusitanica). Platy-

helminthes, which were exclusive of E. gazella epifaunal

assemblages, were the second most abundant group. In terms

of species richness (i.e., the number of different OTUs),

polychaetes were highly diverse, accounting for more than

30 % of total number of species on both gorgonians

(Fig. 1b). Indeed, in E. gazella assemblages, polychaetes

were the richest group (34 %), followed by arthropods

(31 %) and mollusks (29 %). In L. lusitanica colonies,

arthropods were dominant not only in abundance but also in

number of species (35 % of total number of species), fol-

lowed by annelids (33 %) and mollusks (27 %; Fig. 1b).

Regarding the feeding guilds of the associated epifaunal

assemblages, in E. gazella colonies, carnivores/omnivores

and suspension-feeders/deposit-feeders were the dominant

feeding modes (Fig. 1c). Epifaunal assemblages associated

with L. lusitanica colonies presented a more even distri-

bution of the main feeding guilds. Besides the trophic

guilds above mentioned, the contribution of deposit-feed-

ers, deposit-feeders/herbivores, and suspension-feeders was

also relevant.

Hurlbert’s expected number of species can be rarefied to

the same number of individuals (equal or lower than the

maximal common number of individuals). This allows

comparisons of the assemblages sampled from colonies

with different sizes, different surfaces available for

colonization, or different gorgonian species. Most of the

rarefaction curves showed relatively steep slopes and were

far from reaching the asymptotic values (species saturation;

Fig. 2). By comparing the patterns of the rarefaction curves

constructed for the three main taxonomic groups, it is ap-

parent that polychaeta contributed the most to biodiversity

for both gorgonians, while arthropods were the most

abundant (Fig. 2).

Correlations between gorgonian attributes and the

number of taxa and abundance were performed for the

whole epifaunal assemblage and the main taxonomic

groups separately. Consistently highly significant correla-

tions were obtained for the relationships between both

abundance and species richness of the associated assem-

blages and functional intricacy (CEC index) in both gor-

gonian species. The correlation between species richness

and indicators of colonizable surface also showed sig-

nificant values in most cases, with the highest values for

height in L. lusitanica and for area in E. gazella. Abun-

dance showed consistently lower correlation with the

indicators of colonizable area, and most values were not

significant in L. lusitanica (Tables 3, 4). Except for the

relationship between species richness and lacunarity in L.

lusitanica, measures of complexity and heterogeneity

showed no significant correlations with the associated

assemblages (Tables 3, 4).

Coral Reefs (2015) 34:611–624 615

123

These trends were incorporated into multiple linear re-

gression models to analyze the relationships between the

associated assemblage variables and gorgonian attributes

(Tables 5, 6). Again, CEC was always the variable that

contributed the most to the total variability. It is also

noteworthy that more variables were generally kept in the

final model concerning L. lusitanica assemblages, com-

pared with those of E. gazella, for which the best fits were

obtained for CEC alone or combinations of CEC and area

(Tables 5, 6). Also, the significant contribution of com-

plexity measures (D and lacunarity) was only detected for

L. lusitanica assemblages.

Organisms considered for the CEC analysis (Table 2)

were present in 67 of the analyzed colonies. Thus, only

6.9 % of the colonies were completely devoid of those

epibionts (8.3 % in E. gazella and 5.6 % in L. lusitanica).

Epibiont coverage was, however, low (always \20 %). A

high similarity in taxonomical composition was observed

in both gorgonians in terms of both taxonomic richness

and abundance (Table 2). Bryozoans, hydrozoans, and

macroalgae dominated in terms of diversity, while cirripeds

showed the highest frequency of occurrence in both gor-

gonians (69.4 and 61.1 %, in E. gazella and L. lusitanica,

respectively). These organisms could be found attached to

the branches of the gorgonians or on their base.

Considering the relevance of the CEC explaining the

composition and structure of associated fauna, the rela-

tionship between the frequency of occurrence and richness

of ‘‘colonial’’ epizoans was also analyzed. No correlation

between colony size and the frequency of occurrence (E.

gazella: r2 = 0.0001, p = 0.988; L. lusitanica: r2 =

0.0271, p = 0.376) or richness of CEC (E. gazella:

Num

ber

of ta

xa0

10

20

30

40

50

Annelida Arthropoda Echinodermata Mollusca Platyhelminthes OtherN

umbe

r of

indi

vidu

als

500

1000

1500

2000

2500

3000

Annelida Arthropoda Echinodermata Mollusca Platyhelminthes Other

Num

ber

of in

divi

dual

s

0

200

400

600

800

1000

C/O H DF DF/H SF SF/DF

EG LL

a

b

c

Fig. 1 a Number of taxa,

b individuals, and c feeding

guilds of the dominant phyla

observed in both gorgonian

species. ‘‘Other’’ includes data

from Chordata, Cnidaria,

Nematoda, Phoronida, Porifera,

and Sipuncula. C/O, carnivores/

omnivores; H, herbivores; DF,

deposit-feeders; DF/H, deposit-

feeders/herbivores; SF,

suspension-feeders; SF/DF,

suspension-feeders/deposit-

feeders; EG, Eunicella gazella,

LL, Leptogorgia lusitanica

616 Coral Reefs (2015) 34:611–624

123

0 1000 2000 3000 40000

20

40

60

80

100

120

140

0 1000 2000 3000 40000

20

40

60

80

100

120

140

Mollusca Polychaeta Arthropoda Total

Exp

ecte

d N

umbe

r of

Spe

cies

(E

S)

Number of individuals

Eunicella gazella Leptogorgia lusitanicaFig. 2 Comparison of

rarefaction curves (Hurlbert’s

expected number of species) for

the whole assemblage (total)

and the main taxonomic groups

(Arthropoda, Mollusca and

Polychaeta) in Eunicella gazella

and Leptogorgia lusitanica

Table 3 Eunicella gazella.

Relationships between

gorgonian attributes and species

richness (number of taxa per

colony) and abundance (number

of individuals per colony) for all

of the taxa and the main

taxonomic groups separately

Area Width Height D L CEC

Number of taxa

All assemblage 0.51** 0.47** 0.40* 0.26ns -0.15ns 0.79***

Polychaeta 0.43** 0.37* 0.31ns 0.12ns -0.05ns 0.67***

Arthropoda 0.55*** 0.47** 0.44** 0.26ns -0.12ns 0.77***

Mollusca 0.39* 0.38* 0.28ns 0.32ns -0.22ns 0.64***

Number of individuals

All assemblage 0.41* 0.40* 0.32ns 0.28ns -0.19ns 0.75***

Polychaeta 0.47** 0.38* 0.31ns 0.13ns -0.05ns 0.62***

Arthropoda 0.18ns 0.15ns 0.16ns 0.17ns -0.12ns 0.59***

Mollusca 0.44** 0.43** 0.28ns 0.29ns -0.20ns 0.65***

D fractal dimension, L lacunarity, CEC ‘‘colonial’’ epibiont cover, ns not significant

* p\ 0.05; ** p\ 0.01; *** p\ 0.001

Bold values indicate significant values

Table 4 Leptogorgia

lusitanica. Relationships

between gorgonian attributes

and species richness (number of

taxa per colony) and abundance

(number of individuals per

colony) for all taxa and the main

taxonomic groups separately

Area Width Height D L CEC

Number of taxa

All assemblage 0.47** 0.45** 0.56*** -0.23ns 0.47** 0.76***

Polychaeta 0.29ns 0.27ns 0.37* -0.11ns 0.37* 0.69***

Arthropoda 0.51** 0.52** 0.62*** -0.31ns 0.43** 0.65***

Mollusca 0.48** 0.37* 0.50* -0.15ns 0.38* 0.63***

Number of individuals

All assemblage 0.35* 0.32ns 0.40* -0.12ns 0.27ns 0.77***

Polychaeta 0.25ns 0.23ns 0.32ns -0.06ns 0.31ns 0.69***

Arthropoda 0.34* 0.34* 0.36* -0.11ns 0.21ns 0.50**

Mollusca 0.28ns 0.23ns 0.32ns -0.04ns 0.19ns 0.55***

D fractal dimension, L lacunarity, CEC ‘‘colonial’’ epibiont cover, ns not significant

* p\ 0.05; ** p\ 0.01; *** p\ 0.001

Bold values indicate significant values

Coral Reefs (2015) 34:611–624 617

123

r2 = 0.0027, p = 0.762; L. lusitanica: r2 = 0.0483,

p = 0.235) was observed. However, when the macrofauna

patterns are related to the CEC data (most frequent taxa)

through the dbRDA, it is clear that some colonial taxa are

important to explain the differences in the macrofauna in

both gorgonian species (Fig. 3). Some bryozoans (cf.

Vesicularia sp. and Crisia sp.), hydrozoans (Halecium sp.,

Laomedea sp.), and barnacles (Cirripedia) seemed to be

more associated with E. gazella than with L. lusitanica. No

clear pattern regarding colony size was perceptible though.

On the other hand, L. lusitanica samples show a gradient

separating small size colonies from medium and large

colonies. Macroalgae (sp. 3 and sp. 7), a bryozoan (Gym-

nolaemata sp. 1), and a hydrozoan (Hydrozoa sp. 1) relate

well to that pattern, as they tend to show higher occurrence

and abundance at medium and large gorgonian colonies.

Significant relationships between the abundance of in-

dividuals of the main trophic groups and CEC were found

in the epifaunal assemblages associated with both gor-

gonians, except for the deposit-feeders in L. lusitanica

(Fig. 4).

Discussion

The use of different measures of habitat complexity to-

gether with different sampling methods hampers direct

comparisons of results gathered on the relationships be-

tween habitat complexity and associated animal assem-

blages. Besides, measures of structural complexity can

change unpredictably across spatial scales, and typical

coral habitats are too complex for any single measure of

Table 5 Eunicella gazella.

Subset of gorgonian attributes

that explain the most variability

in the number of species and in

the number of individuals

(backwards stepwise regression)

Adj. R2 Variables

Number of taxa

All groups 0.649*** CEC (0.0323), area (0.2035)

Polychaeta 0.453*** CEC (0.000), area (0.161)

Arthropoda 0.683*** CEC (0.000), area (0.004), -width (0.047)

Mollusca 0.397*** CEC (0.000)

Number of individuals

All groups 0.555*** CEC (0.000)

Polychaeta 0.473*** CEC (0.000), area (0.006), -D (0.1191), -height (0.1277), -width (0.1573)

Arthropoda 0.335*** CEC (0.000)

Mollusca 0.422*** CEC (0.000), area (0.126)

Models for all faunal assemblages and those for the main taxonomic groups have been derived separately.

The variables comprising the best model are listed in order of decreasing significance (p values in

parentheses). (-) indicates a negative relationship for a variable in the model

D fractal dimension, L lacunarity, CEC ‘‘colonial’’ epibiont cover

* p\ 0.05; ** p\ 0.01; *** p\ 0.001

Table 6 Leptogorgia

lusitanica. Subset of gorgonian

attributes that explain the most

variability in the number of

species and in the number of

individuals (backwards stepwise

regression)

Adj. R2 Variables

Number of taxa

All assemblage 0.652*** CEC (0.000), area (0.022), -L (0.0482), -width (0.0549), D (0.1084)

Polychaeta 0.589*** CEC (0.000), L (0.004), D (0.007), width (0.0612), area (0.1254)

Arthropoda 0.518*** CEC (0.002), height (0.004)

Mollusca 0.594*** CEC (0.000), area (0.001), -width (0.003), L (0.042), D (0.1116)

Number of individuals

All assemblage 0.333*** CEC (0.000)

Polychaeta 0.531*** CEC (0.000), D (0.011), L (0.030)

Arthropoda 0.228** CEC (0.002)

Mollusca 0.374*** CEC (0.000), area (0.056), -width (0.062)

Models for all faunal assemblages and those for the main taxonomic groups have been derived separately.

The variables comprising the best model are listed in order of decreasing significance (p values in

parentheses). (-) indicates a negative relationship for a variable in the model

D fractal dimension, L lacunarity, CEC ‘‘colonial’’ epibiont cover

* p\ 0.05; ** p\ 0.01; *** p\ 0.001

618 Coral Reefs (2015) 34:611–624

123

complexity (Knudby and LeDrew 2007). In coral reef

systems, species diversity of fish (Nagelkerken et al. 2000;

Gratwicke and Speight 2005b; Lingo and Szedlmayer

2006; Wilson et al. 2007) and epifaunal invertebrate

assemblages (Vytopil and Willis 2001; Idjadi and Edmunds

2006) has been positively correlated with habitat com-

plexity. In some studies, results differed with the nature of

the reef (Ohman and Rajasuriya 1998) or were inconsistent

in studied areas (Luckhurst and Luckhurst 1978; Bejarano

et al. 2011). Other studies also reported no relationship

between species diversity and habitat complexity (Ca-

ballero and Schmitter-Soto 2001). This inconsistency may

be related to the use of different measures of complexity or

the scales at which complexity was assessed. These scales

should preferably match the typical body size of the or-

ganisms whose habitat is being investigated (e.g., Knudby

and LeDrew 2007).

A positive relationship between habitat complexity and

the enhancement of the biodiversity of its associated

assemblages was not unequivocal in the present study, even

though habitat complexity, as assessed by fractals, was

measured at the scale of the gorgonian colony. The fractal

nature of the analyzed gorgonians, similarly to other self-

similar organisms (e.g., trees, algae), may be related to

physical and metabolical limitations (West et al. 1999),

suggesting that the architecture of the organisms is defined

by a set of branching rules (Bentley et al. 2013). This

explains why fractal dimension does not vary significantly

between species and sizes, generally indicating that even

small-sized colonies present the characteristic structure of a

gorgonian. In cases where a fractal analysis does not show

simple scaling properties, the observed complexity can be

due to fundamentally different processes operating on

different scales (Lam and Quattrochi 1992; Sievanen et al.

2000). The processes determining the abundance and di-

versity patterns of the associated fauna may occur at a

smaller scale (i.e., at the same scale as CEC) than the one

that can be analyzed with the methodology adopted in the

present paper. A differential response of different taxo-

nomic groups to gorgonian attributes, most likely as a re-

sult of their different environmental and/or biological

requisites, was also observed. Structural complexity and

heterogeneity measures in the multiple regression analyses

were, in general, not relevant for the ecological patterns.

Fig. 3 Distance-based

redundancy analysis (dbRDA)

ordination biplot for epifaunal

assemblages associated with

Eunicella gazella, EG (circles;

different shades represent

colony size) and Leptogorgia

lusitanica, LL (squares;

different shades represent

colony size). Samples are

plotted as points using weighted

averages of species scores in

each constrained axis. The

vector lines reflect the

relationship of colonial

epibionts (most common; 18

taxa) to the ordination axes;

their length is proportional to

their relative significance.

S small (\9 cm for EG;\10 cm

for LL), M medium (9–17 cm

for EG; 10–30 cm for LL),

L large ([17 cm for EG;

[30 cm for LL), following

Carvalho et al. (2014)

Coral Reefs (2015) 34:611–624 619

123

Only lacunarity, used here as a measure of the colony

heterogeneity, was found to have a positive correlation

with the number of taxa of the assemblages inhabiting L.

lusitanica colonies. The higher values of lacunarity found

in those colonies reflect the differences in morphology of

the colonies of both gorgonian species: L. lusitanica

colonies have more inter-branch spaces and higher vari-

ability and consequently will have higher number and di-

versity of niches compared with E. gazella. The

combination of both will promote the colonization of

species with a wider range of body sizes, enhancing taxo-

nomic richness (Tokeshi and Arakaki 2012). Pierre and

Fig. 4 Relationship between the abundance of individuals (square

root-transformed) belonging to the main trophic groups and the

‘‘colonial’’ epibiont cover (CEC). The regressions are presented in

black for Eunicella gazella (solid line) and gray for Leptogorgia

lusitanica (dashed line). ns not significant. *p\ 0.05; **p\ 0.01;

***p\ 0.001

620 Coral Reefs (2015) 34:611–624

123

Kovalenko (2014) also found that species richness in

macrophyte-associated assemblages in freshwater systems

was more influenced by space-size heterogeneity than

overall complexity. As pointed out by the authors, this

heterogeneity of sizes may also reflect heterogeneity of

niches available to be colonized by species with a wider

size range. Also, as observed before, fractal measures do

not always provide a comprehensive characterization of

habitat complexity (Tokeshi and Arakaki 2012). These

authors even hypothesized that the highest levels of bio-

diversity will be most likely linked to intermediate levels

of fractal dimension when an entire range of values is

considered.

Epifaunal abundance and diversity were, however,

strongly related to gorgonian attributes representing the

surface available for colonization, although not consis-

tently between gorgonian species or across faunal groups.

This relationship varied for each host, as well as on the

faunal group analyzed. In the present study, regardless of

the measure used, the correlations between animal abun-

dance and habitat attributes were always weaker than those

found for diversity, which corroborates the findings of

earlier studies (Ohman and Rajasuriya 1998; Idjadi and

Edmunds 2006).

Taking into consideration the studies highlighting the

relationship between structural complexity and diversity in

marine environments both for fish and invertebrates, the

nonsignificant correlations found between the fractal mea-

sure of complexity, and both the number of species and

abundance of invertebrate assemblages could be surprising.

Although this is the first attempt to apply fractal dimensions

in estimating habitat complexity in coral colonies and then to

assess its relationship with associated epifaunal assem-

blages, it is a common approach in studies of plants and

algae (Morse et al. 1985; Gee and Warwick 1994; Davenport

et al. 1999; Attrill et al. 2000). Attrill et al. (2000), while

assessing the relationship between seagrass structural com-

plexity and the associated macroinvertebrate community,

found that seagrass biomass, rather than complexity, was the

crucial factor for the enhancement of the number of indi-

viduals and species. As no significant positive relationship

was detected between biomass and complexity, the authors

linked the increase in species diversity with increasing

seagrass biomass to a species–area relationship effect (larger

surface area available for colonization). These authors pro-

posed that the relationship between seagrass biomass and

macroinvertebrate diversity was a sampling artifact result-

ing from the probability of collecting more of the rare spe-

cies as the area sampled increases.

The most striking pattern emerging from the results is

that, from the parameters analyzed, the ‘‘colonial’’ epibiont

cover of gorgonians was the most relevant attribute of the

gorgonian habitat driving biodiversity and abundance

patterns of their associated assemblages. Although multiple

factors are expected to influence epifaunal assemblage

patterns associated with gorgonians, the abundance of

‘‘colonial’’ epibionts in each colony consistently enhanced

diversity and abundance of all non-colonial species,

although size measures (area, width, and/or height) were

also relevant. Despite the generally low level of ‘‘colonial’’

epibiont coverage (\20 %), the biological, structural

component of the habitat was always the most relevant.

This suggests that the enhancement of local diversity pro-

moted by gorgonians may be also indirectly supported by

‘‘colonial’’ epibionts that settle and grow up on the external

surface of their skeletons. Furthermore, the lack of sig-

nificance between the fractal dimension and the biodiver-

sity patterns may be related to the lack of resolution at the

scale of these epibionts.

Associations between marine invertebrates and colonial

animals, such as hydrozoans and bryozoans (Lindberg and

Stanton 1988; Conradi et al. 2000; Bradshaw et al. 2003),

or even algae (Hall and Bell 1988; Bologna and Heck

1999; Cacabelos et al. 2010), have been frequently re-

ported. In the past few years, the importance of interactions

between organisms for structuring communities has been

reemphasized, suggesting that the coexistence of species is

of primary importance for the biodiversity of ecosystems

(e.g., Chesson 2000; Bruno et al. 2003; HilleRisLambers

et al. 2012). Therefore, it is suggested that gorgonians can

function as facilitators for several species using different

processes (e.g., niche availability and trophic cascades) to

increase the abundance and diversity of local macrofaunal

communities. Previous studies on the relationships between

macroalgae/seagrasses and associated epifaunal assem-

blages reported that epiphytes (mainly algae) play an im-

portant role in structuring the patterns of distribution and

abundance of mobile organisms (Schneider and Mann

1991; Martin-Smith 1993; Attrill et al. 2000; Cacabelos

et al. 2010). These organisms can increase structural

complexity (Hall and Bell 1988; Schneider and Mann

1991; Martin-Smith 1993) and/or provide additional food

resources (Kitting et al. 1984; Orth and Van Montfrans

1984; Bologna and Heck 1999; Jones and Thornber 2010),

which will probably contribute to the maintenance of more

diverse and abundant epifaunal assemblages. However,

some epibionts can also compete with suspension-feeders

for food, leading to growth and reproductive costs, espe-

cially when the distribution of trophic resources is deter-

mined by flow (Kim and Lasker 1997). Indeed, some

epibionts can invade a gorgonian colony extensively, ulti-

mately resulting in partial or complete colony death due to

either feeding constraints or its collapse to the ground. For

example, hydrozoans are known as pioneer epibiont spe-

cies that take advantage of minor injuries but in the case of

extensive and/or repeated injuries, tissues are colonized by

Coral Reefs (2015) 34:611–624 621

123

stronger competitors, like bryozoans, which are the starting

point for a permanent and varied epibiont community

(Riegl and Riegl 1996; Bavestrello et al. 1997; Cerrano

et al. 2005). Both bryozoans and hydrozoans were ran-

domly found on the gorgonian colony branches or base,

which is in agreement with their opportunistic behavior of

preferentially colonizing areas that have been damaged.

However, in the study area, heavily colonized gorgonians

are not very abundant. According to Rotjan and Lewis

(2008), concerning scleractinian fauna, the 51 invertebrate

corallivore species are in fact a small proportion of the total

number of invertebrate fauna described as being associated

with coral species (Stella et al. 2011). For octocorals,

namely gorgonians, it is also known that some gastropods

feed on their hosts’ living tissue (Patton 1972; Burkepile

and Hay 2007; Garcıa-Matucheski and Muniain 2010), but

most of the other invertebrate-associated fauna does not

(Patton 1972; Kumagai 2008). Also, several amphipods,

which were numerically dominant here, have been reported

to feed on algae, bryozoans, and hydrozoans (Duffy and

Hay 2000; Dauby et al. 2001). During a manipulative ex-

periment testing the relative importance of trophic and

structural characteristics of seagrass epiphytes on macro-

faunal associated organisms, Bologna and Heck (1999)

found that mobile seagrass fauna responded positively to

the presence of new trophic resources, rather than the in-

creases in secondary structure. Only caprellids (Crustacea:

Amphipoda) appeared to be associated with both the

structure and trophic resources of epiphytes. Other authors,

however, observed that both epiphyte cover and substratum

shape were relevant in determining the distribution of

epifaunal invertebrates in seagrass beds, but responses

were species-dependent (Schneider and Mann 1991). In the

present study, significant, yet sometimes weak, linear re-

lationships between the abundance of the main trophic

groups and the colonial epibiont cover were detected in

both gorgonians. These results may indicate either their

role as direct food resources, or their contribution to the

enhancement of food resources (e.g., animals for carni-

vores or organically rich particles for suspension/deposit-

feeders). Regardless of the role epibionts play in structur-

ing the epifaunal assemblages associated with gorgonians

(i.e., food resource or additional habitat), the current results

support the hypothesis that gorgonians’ epibiont cover

(both flora and fauna) affects the patterns of abundance and

diversity of their associated assemblages.

In summary, the results of the present, quantitative,

statistically based study suggest that the patterns of diver-

sity and abundance of epifaunal assemblages are better

explained by the presence of other colonial animals and

algae and thus a greater surface area for colonization and

increased ecological niches and food resources, than the

complexity of the colony itself (measured as fractal di-

mension). The lack of significance between fractal di-

mension and biodiversity may be biased by the scale at

which the study was conducted as well as the measure

itself. Indeed, relevant aspects of the habitat structure that

are determinant for the colonizing organisms are not

adequately covered by the fractal concept (Tokeshi and

Arakaki 2012). The paradigm that structural complexity

enhances species diversity may still be valid if tested at a

broader range of habitat complexity (e.g., by comparison

with more complex coral species like scleractinians) or at a

broader spatial scale (e.g., by comparison with the reef

environment or gorgonian aggregation to other less com-

plex habitats), as suggested for seagrass beds (Attrill et al.

2000). That is to say that this paradigm may be scale-

dependent. This is supported by some studies that analyzed

coral reefs as a whole, instead of focusing on the colonies

themselves (Luckhurst and Luckhurst 1978; Chabanet et al.

1997; Gratwicke and Speight 2005a; Wilson et al. 2007).

Manipulative experiments on structural complexity using

artificial reef blocks to create habitats with different levels

of complexity also provided evidence, supporting the hy-

pothesis that habitat complexity increased the diversity of

reef-fish species (Lingo and Szedlmayer 2006). In the case

of gorgonians, apparently their importance relies in part on

the overall environment at the aggregation scale instead of

the scale of individual colonies, which reinforces the need

for the conservation of gorgonian aggregation areas as a

whole, including their size structure and taxonomical di-

versity. Benthic communities in areas where gorgonians

are common seem to be affected by cascade effects that are

related to gorgonians directly (scale/area in both gorgonian

species and increased heterogeneity in medium and large

colonies in L. lusitanica) and indirectly (facilitation due to

colonial epibionts). What is more, the indirect effects seem

to be more important for explaining the patterns in a patchy

environment where multiple factors shape the community.

The apparent random distribution of facilitators (colonial

epibionts) further emphasizes the complex and unpre-

dictable nature of the biotic relationships typical of a

metapopulation. Furthermore, possible interactions that

could not be addressed in the present study, such as pos-

sible cascade effects in fish species (Bozec et al. 2013), can

lead to ecological shifts related to the loss of gorgonians as

recently suggested by Ponti et al. (2014) for the coral-

ligenous assemblages in the Mediterranean. Nevertheless,

future research should attempt to compare corals of con-

trasting structural complexities (e.g., gorgonians vs.

scleractinian) and to separate the effects of habitat com-

plexity, food availability, and shelter in order to better

assess the relationship between host attributes and associ-

ated epifaunal assemblages.

622 Coral Reefs (2015) 34:611–624

123

Acknowledgments J. Curdia (SFRH/BD/29491/2006) and S. Car-

valho (SFRH/BPD/26986/2006) benefit from Ph.D. and postdoctoral

grants, respectively, awarded by ‘‘Fundacao para a Ciencia e a Tec-

nologia’’ (FCT). The authors would like to acknowledge John Pear-

man for proofreading the manuscript and two anonymous reviewers

for the invaluable comments that helped improving a previous version

of the manuscript. This work was partially supported by European

Funds through COMPETE and by National Funds through the Por-

tuguese Science Foundation (FCT) within project PEst-C/MAR/

LA0017/2013.

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