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Coral-associated invertebrates:
Diversity, ecological importance and
vulnerability to disturbance
Jessica S. Stella1,2,3, Morgan S. Pratchett2,
Pat A. Hutchings4 & Geoffrey P. Jones1,2
1School of Marine and Tropical Biology, James Cook University,
Townsville, Queensland 4811, Australia
E-mail: Jessica.Stella@my.jcu.edu.au (corresponding author)
2ARC Centre of Excellence for Coral Reef Studies, James Cook University,
Townsville, Queensland 4811, Australia
3 Climate Adaptation Flagship, CSIRO, Hobart, Tasmania 7001, Australia
4 The Australian Museum, Sydney, New South Wales 2010, Australia
Abstract The biodiversity of coral reefs is dominated by invertebrates. Many of these invertebrates
live in close association with scleractinian corals, relying on corals for food, habitat or settlement
cues. Given their strong dependence on corals, it is of great concern that our knowledge of coralassociated invertebrates is so limited, especially in light of severe and ongoing degradation of coral
reef habitats and the potential for species extinctions. This review examines the taxonomic extent
of coral-associated invertebrates, the levels of dependence on coral hosts, the nature of associations
between invertebrates and corals, and the factors that threaten coral-associated invertebrates now
and in the future. There are at least 860 invertebrate species that have been described as coral associated, of which 310 are decapod crustaceans. Over half of coral-associated invertebrates appear
to have an obligate dependence on live corals. Many exhibit a high degree of preference for one or
two coral species, with species in the genera Pocillopora, Acropora and Stylophora commonly preferred. This level of habitat specialization may place coral-associated invertebrates at a great risk of
extinction, particularly because preferred coral genera are those most susceptible to coral bleaching
and mortality. In turn, many corals are also reliant on the services of particular invertebrates, leading to strong feedbacks between abundance of corals and their associated invertebrates. The loss of
even a few preferred coral taxa could lead to a substantial decline in invertebrate biodiversity and
have far-reaching effects on coral reef ecosystem function. A full appreciation of the consequences
of further coral reef degradation for invertebrate biodiversity awaits a more complete description
of the diversity of coral-associated invertebrates, the roles they play in coral reef ecosystems, their
contribution to reef resilience and their conservation needs.
Introduction
Coral reefs are complex and productive ecosystems that encompass the highest biodiversity of any
marine ecosystem (Sebens 1994, Gray 1997, Hoegh-Guldberg 1999, Veron 2000). Estimates of the
number of species found on coral reefs range from 172,000 to over 9 million (Reaka-Kudla 1997,
43
Ruppert et al. 2004). The uncertainty in species estimates is largely because like most marine ecosystems, coral reef biodiversity is dominated by highly diverse invertebrate taxa that are understudied
and incompletely described (Reaka-Kudla 1997). The literature on coral reef organisms and their
taxonomy has a strong bias towards the most conspicuous reef organisms, such as corals and fishes,
whereas smaller, cryptic organisms remain largely ignored (Gaston 1991, Bouchet et al. 2002). The
estimates of reef fish and coral diversity stand at about 4000 (Choat & Bellwood 1991, Lieske &
Myers 1994, Bellwood et al. 2003) and about 800 species, respectively (Paulay 1997, Veron 2000,
Hughes et al. 2002). However, invertebrates other than corals account for the vast majority of animal species on coral reefs. It is an unfortunate circumstance that, given the documented global
threats to coral reef ecosystems (Sebens 1994, Hoegh-Guldberg 1999, Gardner et al. 2003, Hughes
et al. 2003, Bellwood et al. 2006), the taxa that account for the greatest biodiversity are those that
have received the least attention.
The extraordinary biodiversity of coral reefs is evident at all taxonomic levels (Table 1).
Members of all the 34 extant animal phyla, except the Onycophora and Cycliophora, occur on coral
reefs (Castro 1988, Gray 1997, Williamson 1997, Ponder et al. 2002, Ruppert et al. 2004). The
most recent estimates indicate that there are at least 165,000 described invertebrate species associated with coral reefs (Table1). In terms of described species, the fauna is dominated by molluscs,
arthropods, nematodes, platyhelminthes and cnidarians. The true diversity of coral reef invertebrate
species will not be known until there are many more systematic studies of most groups (but see
Abele 1974, Austin et al. 1980, Edwards & Emberton 1980, Black & Prince 1983). It is estimated
that 1635 new marine species are currently described every year, mostly crustaceans and molluscs
(Bouchet 2006), but sampling effort remains insufficient for most invertebrate groups (Bouchet
et al. 2002). Even without precise species counts, it is clear that invertebrates account for the greatest biodiversity on coral reefs, regardless of the taxonomic level by which it is measured (Ray 1985,
Earle 1991, Ray & Grassle 1991, Williamson 1997, Ruppert et al. 2004). Despite their ubiquity, the
factors affecting biodiversity and abundance of invertebrates on coral reefs are poorly understood.
Consequently, understanding of coral reef processes is drawn from knowledge of a relatively small
proportion and taxonomically biased selection of coral reef species.
The high biodiversity of coral reef organisms is partly attributed to the extraordinary diversity of
habitats and topographic complexity provided by scleractinian corals (Luckhurst & Luckhurst 1978,
Sale 1991, McClanahan 1994, Jennings et al. 1996, hman & Rajasuriya 1998, Lawson et al. 1999,
Lindahl et al. 2001, Gratwicke & Speight 2005, Garpe et al. 2006, Wilson et al. 2007). In addition,
coral reefs have been associated with the evolution of the largest diversity of symbiotic associations
in the marine environment (Castro 1988). Many of these symbioses involve branching corals and
other reef invertebrates (Patton 1966, 1974, Tyler 1971, Bruce 1972b, 1977, Abele & Patton 1976,
Austin et al. 1980, Coles 1980, Chang et al. 1987, Castro 1988, Tsuchiya et al. 1992, Sin 1999, Stewart
et al. 2006). Symbiotic associations with branching corals have many benefits for reef invertebrates;
corals provide them with a large surface area on and in which to live, refuges from predation, food in
the form of coral tissue, mucus and its associated detritus, and a hard skeleton used as a substratum
by specialized burrowers and gall-forming animals (Castro 1988). In utilizing coral in such ways,
many reef invertebrates have become reliant on the coral substratum. Whereas some utilize coral
hosts indiscriminately, a high proportion of them may exhibit a degree of specialization to a living
coral host, and this mode of life can often involve lifelong associations between individuals. The
relationship coral-associated invertebrates have to corals can be either obligate (must live on their
coral host to survive) or facultative (may live on a coral host but does not have to for survival) (Castro
1976). The difference between obligate and facultative symbiosis may have fundamentally different
consequences for the structure and dynamics of these invertebrate assemblages.
An understanding of the degree of dependence of invertebrates on corals has become a particularly important issue in light of the increasing variety of factors contributing to a global decline
in coral cover (Sebens 1994, Hoegh-Guldberg 1999, Jones et al. 2004, Bellwood et al. 2006). A
44
CORAL-ASSOCIATED INVERTEBRATES
Marine
Coral reefs
Freshwater
Terrestrial
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
X
0
1
20
7,800
9,980
80
20,000
1,120
80
50
500
150
20,000
4
2
1,150
100
8,000
150
150
50,000
35,000
800
350
4,000
14
6,000
150
70
75
150
0
3
2,300
168,249
Source: Updated, based on Ray & Grassle 1991 and Ruppert et al. 2004.
decline in coral cover will presumably affect the animals that interact with living coral, and the
nature of these interactions may be used to predict the effects of declining coral cover on coral associates. If particular coral species disappear, facultative associates may persist by switching hosts,
whereas the more specialized, obligate associates will be at greater risk of extinction (McKinney
1997). The co-dependence between obligate associates and corals appears to be so strong that some
species of corals do not seem able to persist without their symbionts (Glynn 1983, Stewart et al.
2006), and obligate associates are only found in association with certain coral hosts (Glynn 1983).
Understanding how specialized species are to a certain habitat is important because these factors
can greatly enhance the risk of extirpation or extinction following declines in the availability of
potential habitats (Lawton 1993, McKinney 1997, Pratchett et al. 2008). Habitat degradation is a
45
Number of species
Number of studies
5
4
3
2
1
0
Invertebrates
Fish (includes
sharks and rays)
Corals
major threat to coral reefs worldwide, so it is imperative that we understand the degree of specialization and codependence of these symbiotic relationships and learn more about how disturbance will
affect their diversity.
Current research on the potential impact of coral bleaching on the biodiversity of reef organisms highlights the disparity in our knowledge of different taxonomic groups. To date, much of the
focus has been on the impact of bleaching on the corals themselves and on the consequences for
reef fishes (Figure1). Despite the disproportionate diversity represented by invertebrates, there are
practically no data on the coral-invertebrate relationship and the potential effects of coral reef degradation via prolonged and frequent bleaching or coral death on their biodiversity (Figure1). Studies
of coral-reef fish associations have documented a high degree of dependence on the coral substratum and the consequent dramatic effects of habitat loss and degradation on reef fish assemblages
(e.g., Reese 1977, Harmelin-Vivien & Bouchon-Navaro 1983, Sano 1989, Hughes 1994, Shears &
Babcock 2002, Bellwood et al. 2003, Duffy 2003, Hughes et al. 2003, Jones et al. 2004, Munday
2004, Garpe et al. 2006, Graham et al. 2006, Pratchett et al. 2006, Wilson et al. 2006). By comparison, the nature of the association between corals and other invertebrates and their response
to human impacts on coral reef habitats are not well known even though their association may be
stronger and the threat to reef biodiversity may be greater than for fishes. To assess the likely effects
on reef biodiversity due to coral reef degradation, it is first necessary to focus clearly on the largest
component of reef biodiversity: the invertebrates.
To date, there has not been a systematic review of all known coral-associated invertebrates and
the coral taxa with which they associate. The aim of this review is to assemble and synthesize the
disparate literature on the diversity and taxonomic composition of coral-associated invertebrates
and their hosts. First, an assessment is made of the roles coral-associated invertebrates play in
reef processes and the nature of their association with scleractinian corals, examining both positive and negative feedbacks in invertebrate-coral host relationships. Second, the patterns of habitat
use and specialization are examined, including the extent of their coral dependence across a range
of invertebrate groups for which information is now available. Finally, both the anthropogenic and
46
CORAL-ASSOCIATED INVERTEBRATES
environmental threats they are currently facing and how habitat specialization may enhance their
risk of extinction are assessed.
500
56%
400
33%
300
200
11%
100
0
Obligate
Unknown
Facultative
ecosystems are likely to experience a large proportional change in biodiversity as coral reef habitats
are continually degraded. Also of concern are the 283 species for which knowledge of coral dependence is unknown. Without further studies, it is impossible to speculate into which category these
species should be classified.
The reason why coral-associated invertebrates use a coral host is an important factor in determining how reliant on a host they are. Coral dwellers are those that utilize coral as habitat, refuge
from predation as well as mating sites within the protection of coral branches (Castro 1988, Munday
et al. 1997). Corallivores consume live coral tissue, mucus or coral skeleton. Corallivorous invertebrates can inflict minor or lethal damage on their coral hosts, which subsequently can have deleterious effects on coral growth and fitness (Rotjan & Lewis 2008). Invertebrate corallivores employ a
wide range of feeding strategies and as such can be obligate or facultative coral feeders (Robertson
1970). The largest proportion of coral-associated invertebrates was found to utilize a coral host for
habitat or food (Appendix, Figure3). Habitat was the primary reason for use for 332 species, and
314 species have been documented to consume coral, with only 26 species using coral as a substratum (such as for grazing) (Figure3). For the remaining portion of coral-associated invertebrates
(197 species), there is no information on the reason for coral use, only a record documenting that
the species is found associated with a coral host (Figure3). It is also unknown whether some of
these species also occur on non-coral hosts. The majority of arthropods utilized coral as habitat
(282 species) and food (239 species) (Figure 3). Molluscs were the second-largest component of
coral-associated invertebrates, with 34 species that utilize coral as habitat and 53 species that consume coral tissue (Figure3). Classifying coral-associated invertebrates by coral use is not always
straightforward. For instance, obligate species, such as trapeziid and tetraliid crabs and alpheid
shrimp, use branching coral for both food and habitat, yet it is unclear which takes precedence.
CORAL-ASSOCIATED INVERTEBRATES
700
Habitat
Number of species
600
Food
Unknown
500
Substratum
400
300
200
100
0
Ar
p
ro
th
od
s
lu
ol
M
ca
od
in
h
Ec
m
er
at
a
lid
e
nn
er
rif
Po
Pl
lm
he
y
at
es
th
in
Si
c
un
ul
ta
da
r
ho
ic
m
e
H
Phyla
Figure 3 Patterns of coral use among coral-associated invertebrates by phyla (based on documented
evidence).
Negative feedback
The most apparent effects of coral-associated invertebrates on corals are direct negative effects
associated with coral feeding. However, coral feeding (by both fishes and invertebrates) is generally
regarded to have negligible effects on corals (reviewed by Cole et al. 2008, Rotjan & Lewis 2008).
The main exception is those species that exhibit population explosions (termed outbreaks) and
thereby cause extensive and widespread coral mortality. Much of the research on invertebrate corallivores has been directed towards those species with the potential to cause rapid and extensive coral
loss, such as the crown-of-thorns starfishes Acanthaster spp., (Glynn 1974, Glynn & Krupp 1986,
Williams 1986, Glynn 1994, Reyes-Bonilla & Calderon-Aguilera 1999, Pratchett 2005) and the gastropod snails Drupella spp. (Boucher 1986, Turner 1994, McClanahan 1997) and Coralliophila spp.
(Brawley & Adey 1982, Baums et al. 2003a,b). There is, however, an exceptional, and ever-growing,
list of invertebrate species known to feed on scleractinian corals. Extensive searches of published
49
sources revealed 314 invertebrate species, from 24 families and 5 phyla, that have been reported
to feed on scleractinian corals (Figure3). This greatly exceeds the number of vertebrate species
(128 species) known to feed on scleractinian corals (Cole et al. 2008) and is much higher than previous estimates of the diversity (51 species) of invertebrate corallivores (Rotjan & Lewis 2008).
Of the 314 corallivorous species revealed during this study, the vast majority (76%, 239 species) were arthropods (Appendix). The remaining species were molluscs (53 species), echinoderms
(12 species), platyhelminthes (9 species) and polychaetes (1 species) (Appendix). The high diversity of arthropods that consume coral included many species of obligate coral-dwelling decapod
crabs (e.g., Cymo, Trapezia and Tetralia), and endoparasitic copepods (Corallovexia, Xarifia and
Corallonoxia). Obligate coral-dwelling crabs are often observed grazing on their host corals, feeding on either live tissue, mucus or fat bodies produced by Pocillopora corals (e.g., Knudsen 1967,
Stimson 1990, Rinkevich et al. 1991, Castro et al. 2004). Given their small size and generally low
densities on each coral colony (typically 2 individuals per colony (e.g., Stella et al. 2010) it is often
assumed that these common and widespread coral crabs do not have any significant negative effects
on their hosts (Rotjan & Lewis 2008). Moreover, some species (e.g., Tetralia) feed predominantly on
mucus rather than live tissue (Stimson 1990), which could have significant beneficial effects (Stewart
et al. 2006), as discussed further in this chapter. Impacts of most corallivorous organisms (including
many polyp-feeding and mucus-feeding fishes) are presumed to be negligible (e.g., Harmelin-Vivien
& Bouchon-Navaro 1983, Hixon 1997) because they cause little apparent damage to prey corals
(Rotjan & Lewis 2008).
Recent research on effects of corallivorous fishes on prey corals revealed that energetic costs of
chronic predation could be significant (e.g., Cole et al. 2009), and that differential feeding among
coral species could influence the relative abundance of preferred versus non-preferred prey (Bellwood
et al. 2006, Cole et al. 2010). Effects of coral-feeding fishes may be particularly pronounced following extensive depletion of prey (e.g., after mass bleaching) whereby feeding is concentrated on
the few remaining corals and may represent the ultimate cause of coral mortality (Bellwood et al.
2006). Similarly, obligate coral-dwelling crabs have specific associations with a select number of
different corals and, together with diverse assemblages of other coral-feeding organisms or in conjunction with other coral disturbances, may contribute to selective coral mortality. In the Chagos
Archipelago, central Indian Ocean, high densities of the decapod Cymo melanodactylus (up to
47 crabs per colony) were recorded on colonies of Acropora cytherea that exhibited extensive areas
of recent mortality (Pratchett et al. 2010). It is unknown whether these coral-feeding crabs caused,
or contributed to, observed coral mortality, but more research is needed to assess the effects of
chronic predation by small, persistent, coral-associated invertebrates.
The greatest diversity of coral-feeding invertebrates is represented by parasitic copepods. At
least 243 species of copepods are known to associate with live coral, of which 199 species parasitize
their coral host (Appendix). Although their typical body size is about 1 mm, copepods may occur in
high number; up to 668 individual copepods have been recorded within a single (ca. 16-cm diameter) colony of Pocillopora damicornis (Humes 1994), although it is unknown what effect, if any,
they have on the growth, reproduction or survivorship of heavily infested corals (Humes 1985a).
It is assumed that most copepods feed on coral mucus (especially endoparasitic species) rather
than live tissue (Humes 1985a). However, recently Cheng & Dai (2010) analysed the gut contents
of a copepod, Xarifia fissilis, and found an abundance of unicellular algae with characteristics of
Symbiodinium, which they obtained from their coral host, Pocillopora damicornis. Interestingly,
the algal cells remained viable in the gut after 2 weeks of starvation in the laboratory. Some copepods were also retained in either an all-light or an all-dark environment. After 5 days, all copepods
in the dark treatment died, possibly due to starvation because photosynthesis would have stopped.
Because the algal cells remained photosynthetically active for a certain period of time, it was suggested that Xarifia fissilis may temporarily retain the ingested Symbiodinium, possibly for the benefits obtained through the release of photosynthetic products to the hosts (Cheng & Dai 2010). The
50
CORAL-ASSOCIATED INVERTEBRATES
use of obtained Symbiodinium by marine invertebrates has been widely documented (Trench &
Winsor 1987, Trench 1993, Lobban 2002, Barneah et al. 2007), but this situation has yet to be tested
for a comprehensive range of coral-associated species.
Crown-of-thorns starfish (nominally Acanthaster planci, but see Vogler et al. 2008) are among
the best-studied invertebrate corallivores and are renowned for their capacity to devastate local
coral assemblages (see reviews by Potts 1981, Moran 1986, Birkeland & Lucus 1990). Ordinarily,
crown-of-thorns starfish occur at very low densities (typically < 1 starfish ha1) and have little effect
on the abundance of reef corals (e.g., Glynn 1973, Zann et al. 1990). However, each starfish consumes up to 6 m2 of live coral per year (Birkeland 1989), and the cumulative impacts of highdensity populations (up to 20,000 ha1) can result in extensive and widespread coral loss (Carpenter
1997). Consequently, there has been considerable research focused on understanding when and
why outbreaks occur. The explanation that has the greatest traction at present relates to increased
nutrient loads in tropical waters or enhanced phytoplankton levels (Brodie et al. 2005, Houk et al.
2007, Fabricius et al. 2010) because increased abundance of planktonic prey increases survival
rates of larval A. planci (Fabricius et al. 2010), leading to increases in local adult abundance 3 years
thereafter (Birkeland 1982). Conversely, the removal of predatory fishes may increase survival and
abundance of postsettlement starfishes, resulting in increased incidence of outbreaks in areas with
higher fishing pressure (Dulvy et al. 2004, Sweatman 2008). There is, however, little evidence that
postsettlement stages of A. planci are actually prone to predation (Sweatman 1995). Ultimately,
crown-of-thorns starfish are predisposed to major population fluctuations due to inherent properties
of their life history, such as immense fecundity, density-dependent fertilization successes, and short
generation times (Moore 1978, Stump 1992). Furthermore, it is likely that there are multiple causes
for outbreaks (Pratchett 2005), which may also vary regionally.
Outbreak densities of A. planci have been reported throughout the Indo-Pacific (Moran 1986).
However, destructive effects of A. planci have been mostly restricted to the western Pacific, especially southern Japan, Australias Great Barrier Reef, Guam and Fiji (Moran 1986, Birkeland &
Lucas 1990, Bruno &Selig 2007). Differential impacts of A. planci outbreaks in different geographic areas may relate to regional variation in the structure of coral communities (Pratchett 2010),
whereby the greatest coral loss tends occur in areas dominated by Acropora, which is the preferred
coral prey for Acanthaster planci (Death & Moran 1998, Pratchett 2001, 2007). Crown-of-thorns
starfish are well adapted to feeding on a wide range of different corals but often exhibit a striking
preference for a small suite of the available prey species, which causes differential mortality among
coral species, and can exert a major influence on coral community structure (Pratchett 2001). In the
eastern Pacific, Glynn (1974, 1976) found crown-of-thorns starfish fed mostly on rarer coral species,
increasing the dominance of the abundant coral species, Pocillopora damicornis (see also Branham
et al. 1971). Elsewhere, Acanthaster planci tend to feed mostly on relatively abundant coral species
(e.g., Acropora and Montipora) and thereby increase the prevalence of non-preferred corals (e.g.,
Ormond et al. 1976, Colgan 1987, Keesing 1992, Death & Moran 1998).
Aside from feeding on prey corals, invertebrate corallivores have been implicated in transmitting
or increasing vulnerability to coral disease (e.g., Sussman et al. 2003, Nugues & Bak 2009), which
indirectly contributes to coral loss or shifts in community composition. Controlled experimental studies have been done that suggest that the corallivorous fireworm Hermodice carunculata (Sussman
et al. 2003), the gastropod Coralliophila abbreviata (Williams & Miller 2005) and a corallivorous
nudibranch, Phestilla sp. (Dalton & Godwin 2006), are effective vectors for coral disease. There
are further anecdotal observations suggesting that Drupella cornus (Antonius & Riegl 1997a,b) and
Acanthaster planci (Nugues & Bak 2009) may also contribute to spread of coral diseases.
The fireworm Hermodice carunculata plays an important role as a winter reservoir and subsequent vector for the bacterium Vibrio shiloi, which causes bleaching of Oculina patagonica in the
Mediterranean (Sussman et al. 2003). Initial instances of Vibrio shiloi infections at the start of summer correspond with the distribution of Hermodice carunculata, although there is also potential
51
for subsequent localized transmission independent of the fireworm (Sussman et al. 2003). In the
Caribbean, Williams & Miller (2005) showed that the gastropod Coralliophila abbreviata effectively transmits disease (potentially white pox: Rodrguez-Martnez et al. 2001) among colonies of
Acropora cervicornis when sequentially feeding on infected and uninfected colonies. In contrast,
Coralliophila abbreviata snails taken only from uninfected colonies and allowed to feed on control
colonies did not cause any disease infections (Williams & Miller 2005), suggesting that transmission potential may be short lived. In contrast, experimental studies using Phestilla sp. revealed
that that after feeding on infected coral tissue the same individual nudibranch could sequentially
infect five different fragments of Turbinaria mesenterina over 12 days (Dalton & Godwin 2006).
Moreover, corals infected with a tissue-sloughing disease after being consumed by Phestilla sp.
were contagious and could be used to reinfect further coral fragments through direct contact. The
agent of this disease was not confirmed but is suspected to be a Beggiatoa bacterium (Dalton &
Godwin 2006).
In Indonesia, Nugues & Bak (2009) found that several (five of eight) colonies of Acropora
cytherea that had been partially consumed by Acanthaster planci were secondarily affected by
brown-band disease. These results suggest that A. planci may be a vector of coral disease that
transmits primary pathogens during feeding (Nugues & Bak 2009). Alternatively, the starfish may
simply facilitate the spread of the disease, whereby areas of tissue loss provide an entry point for
disease pathogens to infect additional coral colonies (e.g., Page & Willis 2007). Similarly, an outbreak of white syndrome among Acropora corals in the Red Sea was correlated with an outbreak
of Drupella cornus (Antonius & Riegl 1997a). It was unclear, however, whether coral mortality
caused by white syndrome attracted or benefitted D. cornus or whether feeding activities of highdensity populations of the corallivorous snails contributed to the disease epidemic (Antonius &
Riegl 1997a). At least two different coral diseases (brown-band disease, Aeby & Santavy 2006;
skeletal-eroding band, Page & Willis 2007) have been shown to readily and rapidly infect coral
fragments that were subject to experimentally induced injuries, whereas comparable coral fragments with intact coral tissue were almost never infected. In each of these experiments, injuries
were imposed by air blasting or physically scraping the live coral to expose small areas (14 cm2)
of underlying skeleton (Aeby & Santavy 2006, Page & Willis 2007). As such, any corallivores that
remove coral tissue and expose the underlying skeleton, including Acanthaster planci and Drupella
spp., may predispose corals to disease.
Injuries to live corals inflicted by coral-feeding organisms may also facilitate the establishment of epibionts (e.g., Spirobranchus giganteus) and allow boring organisms to access the skeleton of live corals (Hutchings 1986). Many different sessile invertebrates, such as polychaetes and
molluscs, live on or within live corals (Hutchings 1986), although their effects on host corals are
generally unknown. Only a few specific coral-epibiont associations have ever been studied, such
as interactions involving Spirobranchus polychaetes and vermetid gastropods. Although epibionts
clearly occupy space that might otherwise be filled with coral polyps, Strathmann et al. (1984) and
DeVantier et al. (1986) suggested that Spirobranchus spp. generally have beneficial effects for host
corals (as discussed in the next section). Vermetid gastropods, however, feed with extruded mucus
nets that can smother surrounding substrata, including corals (Colgan 1985). In French Polynesia,
Shima et al. (2010) showed that colonization by the vermetid gastropods Dendropoma maximum,
reduced skeletal growth of host corals by up to 81% and reduced survival by up to 52%. Vermetid
gastropods also had a disproportionate effect on Pocillopora corals and may therefore contribute to
increased abundance of other corals (mostly Porites) within local coral assemblages (Shima et al.
2010). Similarly, some other sessile coral-associated invertebrates, such as sponges, may directly
compete with host corals for common resources (Suchanek et al. 1983, Aerts & van Soest 1997,
Rtzler 2002). Sponges are able to damage corals by producing active substances even without
direct contact (Suchanek et al. 1983, Sullivan et al. 1983, Porter & Targett 1988). Thus, competitive
interactions between sponges and corals can often result in the overgrowth or death of the coral
52
CORAL-ASSOCIATED INVERTEBRATES
(Macintyre et al. 2000, Rtzler 2002), although, as discussed in the next section, some sponges are
mutualistic (Goreau & Hartman 1963).
Bioeroding activities of many boring organisms can be highly detrimental for host corals,
undermining their structural integrity, making them more susceptible to being dislodged during
storm events (Hutchings 2011) or potentially leading to structural collapse (Goreau & Hartman
1963). Most commonly, macroboring coral-associated animals are polychaete worms, sipunculans,
bivalve molluscs and sponges (Hutchings 2011). Although a few boring species, such as barnacles,
occur in living coral the majority avoid live coral due to the high predation of settling larvae by
the corals (Hutchings 2011). The majority of larvae of boring organisms, therefore, settle on dead
or damaged parts of the coral colony, typically at the base of the coral head. Boring sponges are
the best studied, and most significant of all boring animals (Hutchings 1986), accounting for up to
94% of skeletal excavation. However, boring sponges are relatively slow colonizers. Rather, it is the
polychaetes that are the initial colonizers of newly available coral substrata, and they may actually
facilitate subsequent colonization of boring sponges and sipunculans (Hutchings & Bamber 1985,
Pari et al. 2002). Once these borers have settled and bored into the substratum they are effectively
entombed for the rest of their life. Each borer produces characteristic burrows that can be identified
(Hutchings 1986, 2008). These burrows, when vacated by the death of the borer, provide favourable
habitat for a wide range of other non-boring species, commonly referred to as nestlers or cryptofauna (Hutchings 1986), including many species that only occur on coral reefs. Bioerosion may
create an extensive three-dimensional structure, which may then be infilled by sediment and lithification, thus strengthening the habitat (Wilkinson 1983). The process of bioerosion is generally most
pronounced in the aftermath of coral death, whereby erect coral colonies may be reduced to rubble
within 46 years (Sheppard et al. 2002, Graham et al. 2006). Internal bioeroders may be abundant,
especially in areas enriched with nutrients (e.g., Fabricius 2005), and thus can greatly compromise
coral growth, if not survival.
Positive feedback
Despite the large number of coral-associated invertebrates that directly feed on live corals, or other
wise contribute to reduced health and mortality of corals, there are certain species (e.g., obligate
coral-dwelling crabs) considered to be fundamental to the persistence and resilience of their host
corals (Glynn 1983). Obligate coral-dwelling crabs from the family Trapeziidae, for example, are
considered highly beneficial for host corals for two reasons: (1) they actively defend their host corals
from larger and potentially devastating coral-feeding organisms, such as Acanthaster planci and
Drupella cornus (Glynn 1982, 1987, Vannini 1985, Pratchett et al. 2000, Pratchett 2001); and (2) in
turbid conditions, they contribute to the removal of excess sediment, which can otherwise smother
corals (Stewart et al. 2006).
Obligate coral crabs occupy virtually all branching species of both Acropora and pocilloporids,
including Pocillopora, Stylophora and Seriatopora (Abele & Patton 1976, Stella et al. 2010), but the
associates of pocilloporid corals are the most effective in repelling Acanthaster planci from feeding
on host corals (Pratchett 2001). Differences in the symbiont assemblages of Acropora and pocilloporids are consistent across a wide range of coral species (Knudsen 1967, Tsuchiya & Yonaha
1992). Most notably, Acropora species always contain Tetralia crabs, whereas pocilloporids always
contain Trapezia species (Abele &Patton 1976, Patton 1994). The larger size (of both the carapace
and chelipeds) of Trapezia species, compared with Tetralia crabs, may account for their increased
efficacy in repelling Acanthaster planci (Glynn 1987). Moreover, behavioural observations have
revealed that Trapezia crabs often attack the thorns of the starfish, breaking them off at the pedicel,
whereas Tetralia pinch mainly at the tube feet and, unlike Trapezia, do not cause any lasting damage to the starfish (Glynn 1982, Pratchett et al. 2000). Glynn (1983) observed that these coral associates could detect approaching Acanthaster planci from a distance and began to exhibit a variety of
53
aggressive responses. Defence of host corals from A. planci may also be aided by shrimps (Alpheus
and Coralliocaris) or coral gobies (Gobiodon and Paragobiodon), which alert crabs to any potential
intruders or corallivores (see also Vannini 1985). Pratchett (2001) demonstrated that the occurrence
of coral-associated crustaceans (especially Trapezia and Alpheus) significantly influenced the feeding preferences of Acanthaster planci. When given a choice of acroporid and pocilloporid corals
with associates present, A. planci consistently selected acroporid corals. However, when all associates were removed the corals were consumed without selectivity. As such, widely reported feeding
preferences of A. planci for Acropora over pocilloporid corals (Brauer et al. 1970, Collins 1975,
Ormond et al. 1976, Death & Moran 1998) may relate to effectiveness of respective coral associates in defending their coral hosts. The scallop Pedum spondyloideum also repels Acanthaster
planci from its coral host, massive Porites, using expellent water jets (DeVantier & Endean 1988).
Similarly, the rapid retraction of tube-forming polychaetes (e.g., Spirobranchus giganteus) tends to
deter Acanthaster planci, but rather than preventing A. planci from eating their host colony, these
organisms enhance the survival of only a few adjacent coral polyps, which may enable subsequent
regeneration of the colony (DeVantier et al. 1986, DeVantier & Endean 1988).
Obligate coral-dwelling crabs further contribute to the health of host corals by actively removing sediment deposits from coral surfaces that would otherwise be detrimental to the health of
the coral (Stewart et al. 2006). When sediments were experimentally added to host corals, crabs
contained within colonies of both Acropora and Pocillopora became highly active and began
removing particles by kicking with back appendages and shoveling and throwing them off
with their chelae (Stewart et al. 2006), which may contribute to increased survival of these corals in habitats with high-sediment regimes. To test this suggestion, Stewart et al. (2006) removed
the obligate coral associates from healthy Acropora and Pocillopora corals located inside the
lagoon in Moorea, French Polynesia. After 24 days, mortality rates for acroporid and pocilloporid colonies divested of associates were 45% and 80%, respectively. Whole-colony mortality resulted from excessive sedimentation and subsequent bleaching (Stewart et al. 2006). In
contrast, nearby corals that retained intact assemblages of associates were healthy throughout.
In the eastern Pacific, Glynn (1983) also showed that pocilloporid corals occupied by Trapezia
crabs, as well as Alpheus shrimps, had a higher survival compared with corals divested of their
crustacean associates. After 3 months, 31% of colonies without crustaceans experienced massive
tissue loss. In contrast, corals occupied by crustaceans experienced no mortality and produced
19% more mucus than those without crustacean associates. Glynn (1983) argued that additional
mucus production, stimulated by the presence of crabs, may protect the coral tissue from settling
microorganisms, bacterial infections, sediment and invading larvae. The Pocillopora colonies
harbouring crabs and shrimp demonstrated higher survival and growth rates than those deprived
of crustaceans.
On temperate reefs in North Carolina, Stachowicz & Hay (1999) observed a unique mutualistic
association between an Oculina coral and the decapod crustacean, Mithraculus forceps. The crab
relies on the coral for habitat and food in the form of lipid-rich mucus. In return, the crab defends its
host from being overgrown by chemically noxious seaweeds like Dictyota and Sargassum that are
avoided by most local herbivores. Corals from which crabs were experimentally removed developed
a dense cover of epibionts and exhibited reduced growth and increased mortality relative to corals
with crabs, which remained free of all epibionts. This association acts to promote the persistence of
both species in habitats from which they might otherwise be excluded by competition and predation
(Stachowicz & Hay 1999).
Many obligate associates, such as trapeziid crabs, are trophically reliant on their coral host,
using the coral tissue, mucus and associated detritus as their primary food source (Knudsen 1967,
Glynn 1983). Trapezia live in symbiosis with their coral host, using it as both a food source and a
refuge from predation. Although living within the branches of a coral host offers protection, these
crabs are potential prey for other reef organisms. Trapeziid crabs are consumed by a number of reef
54
CORAL-ASSOCIATED INVERTEBRATES
fishes, including squirrel fishes, flounders, wrasse, moray eels, hawkfishes and sweepers (Hiatt &
Strasburg 1960). Trapeziid crabs move amongst coral colonies at night (Castro 1978), and there is
some opportunistic generalized predation on these crabs, but most fishes are not able to prey on the
crabs while the crabs are within the protection of their coral host. However, the wrasse Gomphosus
varius specializes in foraging between coral branches, using a slender, protruding snout as forceps to extract crustaceans from between coral branches (Hiatt & Strasburg 1960, Hobson 1974,
Sano et al. 1984). Hobson (1974) found that coral-associated crustaceans formed up to 70% of the
wrasses diet in Hawaii. Coral associates, such as Trapezia, are therefore part of a multilevel trophic
system-energy flow through both horizontal and vertical pathways stemming from their coral host
and extending to the wider-ranging food web (Rinkevich et al. 1991).
Importantly, obligate coral associates may actively participate in nutrient recycling, whereby
their excretion and excrement may enrich nutrient availability within the local vicinity of coral
polyps (Patton 1976). Confirmation of nutrient enrichment was shown in the interaction between
the shrimp Periclimenes yucatanicus and its anemone host Condylactis gigantea (Spotte 1996).
The shrimp excretes ammonia, which consequently enriches the nitrogen concentration of water
surrounding the tentacles of the anemone. Spotte (1996) found that anemones associated with the
shrimp had a greater ability to take up external ammonia and contained a greater concentration of
zooxanthellae within their tissue than those without the symbiont. Similarly, the mytilid bivalve
Lithophaga simplex, which commonly inhabits Astreopora myriophthalma in the Red Sea, has
been shown to enhance ammonium contributions, which benefit the host coral (Mokady et al. 1998).
Lithophaga simplex, which bores into the skeletons of living coral colonies, is usually considered to
be parasitic in association with corals. This view of the bivalves is based on the obvious damage
associated with bioerosion of the coral skeleton. However, the benefit provided through nutrient
enrichment may significantly outweigh the cost of localized structural damage (Mokady et al.
1998), so caution must be exercised in ascribing the nature of interactions (parasitic or mutualistic)
between corals and their resident associates. In contrast to the damage boring sponges can cause
to corals, some sponges can actually prevent coral heads from being dislodged, due to the added
flexibility of the basal part of the coral colony, which allows the colony to bend with the water currents (Goreau & Hartman 1963). Filter-feeders, such as sponges, have been found to play a crucial
role in nutrient and carbon cycling on the reef, and those that live in association with coral may be
particularly important in improving water quality and transporting nutrients into the vicinity of the
coral colony (Richter et al. 2001, Ribes et al. 2005).
The ability of some associates to protect corals from predators, alleviate detrimental effects
of sedimentation, inhibit algal overgrowth and enrich nutrient concentration has important implications for the persistence of coral reef ecosystems. These abilities suggest that some associates
increase coral vitality and may play a key role in coral resiliency by providing services beneficial to
coral host health. For sessile corals, with limited innate defences, their symbiotic relationships with
other invertebrates may be vital to the persistence and population dynamics of the coral.
1%
10%
1 taxon
2 taxa
3 taxa
4 taxa
>4 taxa
84%
Figure 4 The number of coral taxa used by coral-associated invertebrates based on all published records
of occurrence.
available resources (i.e., ecological specialists) are expected to be less able to cope with fluctuations
in resource availability and thus, more susceptible to extinction during major disturbances (the
specialization-disturbance hypothesis, Vazquez & Simberloff 2002). In support of this theory, specialist species tend to predominate in less-disturbed (more stable) areas, whereas generalist species
are more common in highly disturbed environments (Kitahara et al. 2000, Kassen 2002). Moreover,
the responses of coral-dependent fishes to coral depletion are strongly dependent on their degree of
resource specialization (Munday 2004, Pratchett et al. 2008). Among both coral-dwelling gobies
(Gobiodon) and coral-feeding butterflyfishes (Chaetodon), local declines in the abundance of species after extensive coral loss were directly proportional to the number of different corals that the
fishes used for food or shelter (Munday 2004, Pratchett et al. 2008). The most specialized species,
which tended to use only one or a few different corals, were extremely vulnerable to coral depletion
and may be at risk of extinction given ongoing coral loss (Munday 2004).
Establishing resource specialization for coral-associated invertebrates is often limited by significant data deficiencies. Based on published records of occurrence on an identified coral host, 84% of
coral-associated invertebrates have been recorded from only one coral host taxon (Figure4). Given
the limited records of species occurrence (in some cases only one), it is not possible to assess whether
these coral-associated invertebrates only utilize a single coral type or have yet to be recorded from
other corals. Therefore, we can only speculate on the potential proportion of coral-associated invertebrates that are extreme specialists. If these 662 species of invertebrates are true specialists, they
may face an increased risk of local and global extinction, although this also depends on the inherent
vulnerability and abundance of the specific corals used for food or shelter.
Dietary specialization
Coral-feeding organisms (both fishes and invertebrates) often exhibit strong selectivity for specific coral prey, typically consuming only a small set of available coral species (reviewed by Cole
et al. 2008, Rotjan & Lewis 2008). Moreover, most corallivores consume corals in significantly
different proportions to which they are available (e.g., Cox 1994, Graham 2007, Pratchett 2007).
In the northern Great Barrier Reef, Australia, Pratchett (2005) showed that virtually all species
of coral-feeding butterflyfishes (11/14 species) fed mainly on Acropora hyacinthus or Pocillopora
damicornis. There was, however, marked variation in levels of specialization exhibited by different
56
CORAL-ASSOCIATED INVERTEBRATES
coral-feeding butterflyfishes (Pratchett 2005). Hence, there are two important ecological questions
pertaining to dietary specialization among coral-feeding organisms: (1) why are certain corals (e.g.,
Acropora) consistently and strongly preferred? and (2) why are some corallivores highly specialized, whereas others are comparative generalists?
Optimal foraging theory would predict that coral-feeding organisms would choose prey that
maximize energetic return (Ormond et al. 1976) and thereby selectively consume coral with the
highest calorific content (Keesing 1990), carbon-to-nitrogen ratio (Graham 2007) or high carbohydrate, protein or lipid content. Keesing (1990) explored the relationship between the nutritional
value of corals and prey preferences of Acanthaster planci, and although the most highly preferred
corals (e.g., Acropora spp.) were among the corals with the highest calorific content, other nonpreferred corals from the family Faviidae also had similar nutritional value. Similar problems have
hindered understanding of prey preferences among coral-feeding fishes (Graham 2007), whereby
prey preferences do not consistently relate to patterns of nutritional quality. In reviewing feeding habits of Acanthaster planci, Potts (1981) suggested that coral prey consumed by A. planci
may represent the least-avoided species, rather than those that are actually preferred. For example,
nematocysts, mesenterial filaments, secondary metabolites, and the antagonistic behaviour of coral
symbionts may all deter corallivores from feeding on certain corals (Potts 1981). A further complication in relating feeding preferences to prey quality is that the nutritional value of corals, as
measured using standard analytical techniques, may poorly reflect the nutritional quality of coral to
corallivores (e.g., Glynn & Krupp 1986). Glynn & Krupp (1986) conducted pairwise choice experiments to assess prey preferences of the starfish Culcita novaeguineae and showed that Pocillopora
meandrina was strongly preferred to Porites compressa, Montipora verrucosa and Fungia scutaria.
Although the organic content of Pocillopora meandrina was the lowest of the four corals, the percent loss of organic matter after feeding by Culcita novaeguineae was the highest. This suggested
that Pocillopora meandrina provides the highest energetic return for Culcita novaeguineae (Glynn
& Krupp 1986), probably due to the superficial location of tissue layers and the ease with which
tissues can be removed. Strong prey preferences for Acropora have also been observed for Drupella
rugosa (Morton et al. 2002) and Coralliophila abbreviata (Hayes 1990) irrespective of coral community composition. Corallivorous invertebrates that are capable of feeding on a diverse range of
different corals generally prefer Acroporidae (Acropora and Montipora) corals (e.g., Acanthaster
planci, Pratchett 2007; Drupella cornus, Morton et al. 2002), although this may be due to conditioning, whereby species simply prefer the most abundant coral or the coral last consumed (e.g.,
Coralliophila abbreviata, Hayes 1990).
Dietary specialization is expected to confer considerable benefits, such as increased capture
and assimilation efficiency (Schoener 1971), whereby specialists are expected to outperform generalist species when preferred prey are readily accessible (e.g., Dearing et al. 2000). There was not,
however, any evidence for this trade-off in the one study that specifically compared performance
of specialist and generalist corallivores, based on sympatric butterflyfishes in the northern Great
Barrier Reef (Berumen & Pratchett 2008). Moreover, a number of seemingly specialist corallivores
appear to be able to exploit a wide range of different corals as prey becomes scarce.
Habitat specialization
Coral-associated invertebrates generally exhibit strong selectivity for different coral hosts, although
the range of different corals used can vary enormously. The most selective species, such as Tetralia,
are known only from only one genus, Acropora (Abele & Patton 1976, Patton 1994, Sin 1999), and
some tetraliids use only one or two species of Acropora, irrespective of coral abundance (Sin 1999).
It would be expected that animals would select habitats that would optimize their survival and
reproductive success (Orians & Wittenberger 1991, Pulliam & Danielson 1991). Patterns of coral
use can potentially arise from active habitat selection and differential predation risks associated
57
with living in different coral morphologies (Lee & Sin 2009). With regard to coral morphology,
tightly branching corals potentially offer greater protection from predators (Vytopil & Willis 2001).
Shirayama & Horikoshi (1982) recorded a greater number of free-living associates on corals with
relatively fine branches and narrow interbranch space. Yet even among branching corals, there is
a large discrepancy in the abundance and diversity of coral associates (Stella et al. 2010). The
complexity of branch growth patterns appears to be a determinant in host selection; coral with a
more complex branching pattern harbours a higher diversity of associates (Stella et al. 2010). This
preference for certain microhabitat characteristics results in a few coral taxa being used by a high
proportion of species.
Many coral associates utilize their coral host as mating sites as well, protected within coral
branches (Castro 1988, Munday et al. 1997). Species of Trapezia and Tetralia crabs and Alpheus
shrimps are usually found in strict mating pairs on their coral host (Castro 1978, Patton 1994, Sin
1999). Copulation in decapods usually only takes place after the female has moulted (Cheung 1968),
when her soft body makes her more vulnerable to predation. Male crabs are known to guard females
from predators after moulting while the females exoskeleton is still soft (Ryer et al. 1990, Shirley
et al. 1990). Once she has laid her eggs, she broods them in her abdomen until they hatch. This is
a crucial time for the crabs because hatching time can range from days to weeks. Therefore, the
shelter offered by coral branches can be a vital component for reproductive success and can differ
in effectiveness among coral hosts.
Habitat specialization has also been documented for other coral-associated invertebrates. Dai
& Yang (1995) documented a non-random distribution of the tube-dwelling serpulid Spirobranchus
giganteus on coral reefs in southern Tawain. Four coral species, Porites lutea, P. lobata, P. lichen
and Montipora informis, considered competitively subordinate were frequently colonized by the
worm, whereas most coral species were not colonized. Evidence of host selection is also apparent
in molluscs. Chen et al. (2004) examined the distribution, size and reproductive characteristics
of the gastropod Coralliophila violacea on two different host morphologies: branching and massive Porites. Coralliophila violacea living on branching Porites were significantly smaller than on
massive hosts (Chen et al. 2004). Chen et al. (2004) also found that reproductive success differed
because females on branching Porites had significantly lower fecundity than those on the massive
Porites, and male-female sex changes occurred at smaller sizes on branching forms. Mokady et al.
(1991) discovered that the bivalve Lithophaga lessepsiana is host specific to Stylophora pistillata,
actively choosing it over all other available corals. Stylophora pistillata was also found to trigger
metamorphosis of settling larvae significantly more than other corals (Mokady et al. 1991). We have
yet to understand the full mechanisms behind host selectivity. Further research may lead to a better
understanding of how these species associations evolved.
When the 869 coral-associated invertebrates in this review are grouped by the coral hosts they
use, it is clear that a narrow range of coral taxa is preferred (Figure 5). Of 44 coral taxa used,
Pocillipora was the most preferred, with nearly 30% of species associated with this genus (Figure5).
Although this preference could be due to a bias in research on Pocillopora, resulting in more records
of occurrence of the species, Pocillopora has been shown to harbour an immense diversity and
abundance of associates compared with Acropora (Stella et al. 2010). The apparent high dependence
of coral-associated invertebrates on certain corals could have dire consequences, depending on how
those corals cope with the suite of environmental threats currently challenging coral reefs.
CORAL-ASSOCIATED INVERTEBRATES
Pocillopora
300
Acropora
250
Porites
Faviidae
Seriatopora
Fungiidae
Montipora
Gonipora
50
Agariciidae
100
Pavona
150
Stylophora
200
Montastrea
350
0
Coral taxa
Figure 5 Pattern of coral taxa use among coral-associated invertebrates including only those coral taxa
known to be used by more than 20 species.
Huston 1985, Karlson & Hurd 1993, Jones & Syms 1998, Nystrm et al. 2000). Components of
coral reef natural disturbance regimes include tropical cyclones, flood plumes, crown-of-thorns
starfish outbreaks (Pearson & Endean 1969) and the various grazing and boring activities of reef
inhabitants (Hutchings 1986). Apart from the natural disturbances that reefs experience, over the
past century reefs have also been subject to many anthropogenic disturbances, which are increasing in frequency and intensity. These disturbances include coastal development and sedimentation,
destructive fishing practices and pollution, as well as impacts associated with climate change, such
as elevated sea-surface temperatures, salinity and ocean current changes, and ocean acidification
(Goreau 1992, Sebens 1994, Wilkinson & Buddemeier 1994, Bryant et al. 1998, Wilkinson 1999,
Jackson et al. 2001, Pandolfi et al. 2003, Jones et al. 2004). These impacts have and will cause a
dramatic reduction in coral cover and consequently alter the structure of populations and communities of species. Coral cover is in decline in many parts of the world, with 50% to 70% under direct
threat from human activities (Goreau 1992, Hughes 1994, Sebens 1994, Wilkinson & Buddemeier
1994, Bryant et al. 1998, Wilkinson 1999, Gardner et al. 2003, Bellwood et al. 2004), and management priorities aim to identify and remedy these threats.
The impacts of reef degradation due to anthropogenic activities can be swift and devastating.
Land-based pollution and destructive fishing practices have caused a sharp decline of 3060% in
coral species diversity in Indonesia (Edinger et al. 1998). The loss or reduction of coral equates to
a loss of vital resources to coral-associated invertebrates and other reef organisms. The subsequent
effects of coral reef habitat degradation on reef organisms have been shown to be substantial. For
example, Jones et al. (2004) documented serious declines in the diversity of fish assemblages due
to reef degradation, with species most reliant on living coral displaying the greatest decline in
abundance. As other studies have also observed the same decline of corallivorous (e.g., chaetodontids, Pratchett et al. 2006) and coral-dwelling fishes (e.g., gobies, Munday 2004), it is imperative to
understand what proportion of coral-associated invertebrates rely on live corals for their long-term
persistence to assess their likely sensitivity to reef degradation. The range of associations previously discussed highlights that some invertebrates associate with coral only intermittently (facultative users), while others depend on live coral for food and habitat (obligate users). Of those
59
that have an obligate dependence on live coral, a proportion is specialized to certain coral hosts.
Specialist species, which selectively utilize only one or two species of coral for food or habitat, will
be particularly susceptible to reef degradation, potentially suffering greater population declines
and extinction risks should their host coral decline in abundance (McKinney 1997, Pratchett et al.
2008). Therefore, the level of dependence on a coral host and how specialized an organism is to a
particular coral taxon are major factors in determining the fate of coral-associated invertebrates as
coral reef degradation continues.
Continued coral reef degradation and the ultimate reduction in coral will probably lead to changes
in the coral community composition or phase shifts, from coral-dominated to algal-dominated reefs
(Hughes 1994, Hughes et al. 2007). How these changes will affect coral-associated invertebrates is
not known and has only been superficially explored. Invertebrates are fairly restricted in their ability to avoid disturbance physically because most are sedentary or have limited mobility. The longterm persistence of coral-associated invertebrates will largely depend on the response diversity of
different species to disturbance as well as their adaptability to a changing coral community, which
may involve utilizing alternate coral hosts that are more resistant to disturbance. As biological data
for the majority of coral-associated invertebrates is essentially non-existent, we have little insight
regarding what the observed effects of habitat degradation might be. From the limited research into
these effects, results can be conflicting. For example, Glynn et al. (1985) documented lower densities
of the obligate associates Trapezia spp. on partially bleached colonies of Pocillopora damicornis,
whereas Tsuchiya et al. (1992) reported an increase of the same associates after bleaching. The
impact of disturbance on reef biodiversity will depend on factors such as physiology and response
diversity of different species, yet ecological and biological data for most coral reef invertebrates
are lacking, hampering our ability to assess which species will be most susceptible. Characteristics
that some invertebrates may possess that enhance vulnerability include restricted geographic distribution or having a few small, highly fragmented populations, direct development, low fecundity,
rarity and a close association with threatened taxa or threatened habitat. However, most of these
factors have received little attention. Because a close association with threatened taxa (i.e., coral)
increases the extinction risk of species, we can make some predictions about the fate of coralassociated invertebrates with increasing reef degradation.
The close association many invertebrates have with corals often relates to a certain degree of
habitat specialization, which has been deemed a major factor determining the vulnerability of a species (McKinney 1997). This vulnerability is evidenced by linking four apparent recent extinctions
of marine gastropods to a vulnerable habitat (Carlton 1993). Importantly, the habitat requirements
of a species may differ significantly at various points in its life cycle; one or more life phases may be
specialized for a particular habitat with limited availability. There are many examples (Pawlik 1992,
Gerlach et al. 2006) of larvae that exhibit requirements for specific types of habitat or chemical
stimuli for successful settlement and even metamorphosis, such as the mussel Lithophaga lessepsiana (Mokady et al. 1991). Without specific corals to render these cues, recruitment will probably
be affected. Such influences on recruitment will potentially affect population size, structure and
persistence even if there are no obvious factors affecting the adults.
It is predicted that climate change, through prolonged and intense bleaching events and subsequent habitat degradation, will cause extensive population declines and the extinction of many
species, ultimately reducing biodiversity and consequently threatening the stability and resilience
of coral reefs worldwide (Naeem & Li 1997, Walther et al. 2002, Bellwood et al. 2003, Julliard et al.
2003, Bellwood et al. 2006, Przeslawski et al. 2008), but the mechanisms, whether lethal or sublethal effects, are not fully understood. Sea temperatures in many tropical regions have increased by
almost 1C over the past 100 years and are currently increasing at about 1.2C per century (HoeghGuldberg 1999). Coral bleaching is predicted to increase in both frequency and magnitude in the
years to come (Hoegh-Guldberg 1999), and rapid changes are already being seen in the community
structure of coral reefs (Hughes et al. 2003). Bleaching and subsequent death of corals would in
60
CORAL-ASSOCIATED INVERTEBRATES
turn result in habitat degradation and loss for many reef species, especially those considered coral
specialists (Williams 1986, Kokita & Nakazono 2001, Munday 2004, Pratchett et al. 2004).
Glynn et al. (1985) observed that obligate crab associates (Trapezia spp.) exhibited sublethal
effects to warming that induced coral bleaching. Reproductive activity apparently declined, emigration increased, and there was a noticeable reduction in defensive behaviours. Within 2 weeks,
lipid content declined by 50% in coral hosts and 78% in symbiotic crabs. Bleached corals with
unfit crab associates may be more susceptible to disturbance and predation because these crabs
have been shown to be vital to coral health through grooming and defence from predators (Glynn
1983, Stewart et al. 2006). Documented studies of coral decline have shown consequent declines in
coral-associated fish assemblages and even local extinctions of coral specialists (Jones et al. 2004,
Munday 2004). If fish biodiversity is affected by coral decline, and the most negative impacts are on
those species deemed coral specialists, then it can be assumed that coral decline would also affect
invertebrates, many of which show some degree of specialization.
All coral species are not equally susceptible to coral bleaching (Coles & Brown 2003). Coral
colonies vary in shape and size, and these differences affect the physiological ecology of corals
(Sebens 1987, Anthony et al. 2002). Branching corals in particular provide a high surface area,
and energy allocation to growth is disproportionately assigned to tissue growth rather than skeletal
growth (Anthony et al. 2002). Fast-growing branching species (e.g., Acropora and Pocillopora)
continually suffer higher bleaching mortality than slow-growing massive species (e.g., Porites and
Astreopora) (Brown & Suharsano 1990, Gleason 1993, Marshall & Baird 2000, Loya et al. 2001,
Floros et al. 2004, McClanahan et al. 2004). In fact, three taxa of corals are particularly susceptible:
Acropora, Pocillopora and Stylophora (Loya et al. 2001, Hughes et al. 2003, McClanahan et al.
2004). Therefore, a potential outcome of increased sea-surface temperatures is a change in the relative abundance of corals. Susceptible coral taxa are often more abundant, and their loss will lead to
large losses in total coral cover (Goreau et al. 2000, McClanahan et al. 2004).
The apparent preference for Pocillopora may have important consequences for the many associated invertebrates. Pocillopora is known to be one of the most susceptible coral taxa to bleaching
and subsequent colony mortality (Brown & Suharsano 1990, Gleason 1993, Marshall & Baird 2000,
Loya et al. 2001, Floros et al. 2004, McClanahan et al. 2004). McClanahan et al. (2004) compared
bleaching susceptibility among coral taxa on Australian and Kenyan reefs using an index to indicate differences in bleaching susceptibility (score of 0100, 0 being most resistant to bleaching and
100 being most susceptible). When this bleaching index was compared with the preferences exhibited by the coral-associated invertebrates in this review, it was clear Pocillopora is the coral taxon
used by the highest proportion of coral associates and is one of the most susceptible coral taxa to
bleaching (Figure6). Moreover, it was found that invertebrates exhibit a heavy reliance on other
susceptible coral taxa as well. Of all the coral-associated invertebrates found in this review, 53%
(462 species) utilize three branching coral species considered to be the most susceptible coral taxa:
Acropora, Pocillopora, and Stylophora (Figure6). Therefore, the decline of even three genera of
coral, with prolonged and frequent bleaching, could potentially result in an immense loss of reef
biodiversity. The widely predicted scenario in which coral reefs become dominated by algae will
result in systems that are unlikely to host the highly specialized invertebrate associates intimately
associated with corals.
250
225
200
175
150
Acropora
125
100
75
Fungiidae Porites
Goniopora
Porites
Pavona
Montipora
Astreopora
Goniastrea
Galaxea
25
0
Stylophora
Faviidae
50
10
20
30
40
50
60
70
80
90
100
and Resource Economics [ABARE] 1998). Bait harvests typically include worms, intertidal molluscs, crustaceans and ascidians. Species collected for jewellery include shelled molluscs, such as
trochus, cowry and cone shells, as well as coral, some echinoderms and crustaceans. Although this
trade is strictly controlled in parts of the world, such as Australia, many developing countries have
few, if any, controls. Moreover, many other species are collected live for the aquarium trade. Direct
exploitation of marine invertebrates for human consumption is a valuable industry, worth more than
A$1.3 billion in Australia alone (ABARE 1998) and in many developing countries would be much
higher as part of subsistence fishing. Due to the small size of most coral associates, they are not
as highly valued as food items but are still collected as bait, ornamentation and the live aquarium
trade. However, overexploitation is not considered an immediate threat (Hutchings et al. 2007).
Marine invertebrate biodiversity also represents a vast resource of novel bioactive compounds, such
as the anticancer agent developed from the Caribbean sponge Cryptotheca crypta (McConnell et al.
1994) and the potential use of the toxin of the cone snail to treat neuropsychiatric disorders such as
Alzheimers and Parkinsons diseases (Olivera et al. 1990). However, as the progress of drug discovery in the marine environment is slow, overharvesting for medicinal purposes is not a threat, and
many would argue that the potential benefits could far outweigh the risks.
Climate change will subject coral reefs to a suite of environmental changes, including changes
in ocean currents, a rise in the sea-surface temperature, changes in ocean chemistry, increased
rainfall and freshwater plumes, a rising sea level and increased irradiance (Hoegh-Guldberg 1999,
Hughes et al. 2003, West & Salm 2003, Munday et al. 2007). The impacts of climate change on
coral reef invertebrates are almost entirely unknown (but see Przeslawski et al. 2008). Rising sea
level has the potential to affect the distribution of intertidal invertebrates, allowing them to expand
landwards, providing that suitable habitat is available. Changes in ocean currents may have serious
implications for marine invertebrate populations. Many marine invertebrates have a pelagic larvae
stage that may extend from a few hours to many weeks (Levin 2006). The strength and direction
62
CORAL-ASSOCIATED INVERTEBRATES
of ocean currents is critical for larvae to return to either their natal reef or a nearby suitable reef.
Changing the direction and strength of ocean currents may carry larvae to unsuitable habitats where
survival will be unlikely. Increases in storm activity and associated changes in salinity will affect
both larval survival and the invertebrates living in shallow waters, including lagoonal reefs.
Temperature is considered to be the most influential factor in the physiological processes of
marine animals and thus greatly shapes their biogeographic distributions (Clarke 2003, Mueter
& Litzow 2008, Richardson 2008, Tewksbury et al. 2008). Temperature is a critical factor for
invertebrates and determines growth and reproduction rates and survival. The developmental and
growth rates of marine invertebrates show a strong positive correlation with temperature (Fujisawa
& Shigei 1990, Palmer 1994, Reitzel et al. 2004, OConnor et al. 2007, Sheppard Brennand et al.
2010) until the thermal threshold is reached. Therefore, temperature increases associated with climate change may at first accelerate the growth rates of many species living in the middle of their
temperature tolerance range, whereas those living closer to their thermal maxima may become
extinct (Precht & Aronson 2004, Greenstein & Pandolfi 2008). For many species, it is the climate
extremes that are critical, and as Lough & Barnes (1990) indicated, it is the extremes that are projected to increase significantly. Tropical species typically have a lower tolerance to temperature
variation than temperate species (Compton et al. 2007) because they may already live near their
thermal optima (Tewksbury et al. 2008). Furthermore, symbioses in tropical species may be less
stable during thermal fluctuations than those in temperate species (Muller-Parker & Simon 2001).
Invertebrates, particularly crustaceans, are sensitive to salinity and thermal changes. Abele (1976,
1979) found that the crustacean associates of Pocillopora were generally more sensitive to environmental extremes, particularly salinity changes, than their coral hosts. Increased temperatures
associated with El Nio were found to have significant negative effects on crustacean associates,
causing a massive decline in abundance (Glynn & DCroz 1990). Upwellings and oxygen depletion
can kill crab and shrimp associates but may only cause partial mortality to the corals (Abele 1976,
1979, Glynn et al. 1985). Echinoderms are also sensitive to temperature increases. Complete developmental failure was observed among sea urchins in manipulated high temperatures (46C above
normal) (Byrne et al. 2009). An increase in ocean temperature therefore would have deleterious
effects on the development, growth and reproduction of marine invertebrates.
Ocean acidification is also a direct threat to marine invertebrates, particularly species with
calcareous shells (i.e., molluscs, echinoderms, crustaceans, bryozoans, serpulid polychaetes, foraminiferans, and sponges as well as corals) especially if ocean pH falls below 7.5 (Raven et al. 2005,
Kleypas et al. 2006, Gazeau et al. 2007, but see Wood et al. 2008). Vulnerability to ocean acidification on larval development and calcification is highly variable among crustaceans and molluscs
(as reviewed by Byrne 2011). Crustaceans may be more resilient to ocean acidification due to the
high organic content of chitin in their shells (Derry & Arnott 2007), as opposed to the more susceptible aragonite skeleton of molluscs (Byrne 2011). Bivalve molluscs appear to be particularly
susceptible to decreases in ocean pH. High levels of atmospheric carbon dioxide have detrimental
effects on the shell synthesis of larval bivalves (Kurihara et al. 2008). Adults have also been shown
to suffer deleterious effects. Carbon dioxide levels equivalent to 740 ppm caused the calcification
rate in the mussel Mytilus edulis to decrease by 25% (Gazeau et al. 2007). Echinoderms are also
under direct threat of ocean acidification. Sea urchins have exhibited a marked decrease in fertilization success, developmental rates, and larval size with increasing carbon dioxide concentrations
(Kurihara & Shirayama 2004, Sheppard Brennand et al. 2010). The direct threats climate change
poses to marine invertebrates may be severe, and it is important to consider that many threats will
be acting synergistically and with apparent selectivity on certain invertebrate groups (reviewed by
Byrne 2011). The onslaught of temperature increases, reduced salinity and ocean acidification as
well as the consequences of habitat degradation will be trying, at best, on the persistence of coralassociated invertebrate populations.
63
Acknowledgements
We thank the Australian government, Department of Climate Change, the Australian Institute of
Marine Science, the Linnean Society of New South Wales, the School of Marine and Tropical
Biology at James Cook University and the ARC Centre of Excellence for Coral Reef Studies for
their support of this study. Thanks to R. Gibson for comments on the manuscript.
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CORAL-ASSOCIATED INVERTEBRATES
Appendix
List of invertebrate species known to utilize coral based on published studies*
Higher Taxa
Species
Coral taxa
Type Use
Reference
Gammaropsis sp.
Gammaropsis sp.
Monp
Monp
O
O
H
H
Bergsma 2009
Bergsma 2009
Parapilumnus sp.
Poc
Alpheus bicostatus
Alpheus bidens
Alpheus bucephaloides
Alpheus clypeatus
Alpheus collumianus
Alpheus diadema
Alpheus frontalis
Alpheus gracilis
Alpheus leviusculus
Alpheus lottini
Alpheus malleodigitus
Alpheus obesomanus
Alpheus pachychirus
Alpheus panamensis
Alpheus parvirostris
Alpheus strenuus
Alpheus sublucanus
Alpheus sulcatus
Alpheus ventrosus
Athanas areteformis
Athanas dimorphus
Athanas granti
Athanas sibogae
Pomagnathus corallinus
Racilius compressus
Synalpheus biungulculatus
Synalpheus brevispinus
Synalpheus charon
Synalpheus digueti
Synalpheus mexicanus
Synalpheus nobilii
Poc
Poc
Sty
Poc
Poc
Poc, Sty
Poc
Sty, Poc
Poc, Ser, Acr
Poc
Ser
Scl
Poc
Poc
Sty
Poc
Sty
Poc
Poc
Poc
Poc
Poc
Poc
Poc
Gal
Poc
Scl
Poc, Sty
Poc
Poc
Poc
U
F
U
U
U
U
U
U
U
O
U
U
U
U
U
U
U
U
U
U
U
U
U
O
O
U
U
O
U
U
U
U
H
H
H
U
H
H
H
U
F
U
H
U
H
H
U
H
H
H
U
U
U
U
H
H
H
H
H
H
H
H
Phylum Arthropoda
Class: Malacostraca
Order: Amphipoda
Family: Photidae
Order: Decapoda
Family:
Acidopsidae
Family : Alpheidae
continued
*
83
Higher Taxa
Family:
Cryptochiridae
Species
Coral taxa
Synalpheus sanjosei
Synalpheus sanlucasei
Synalpheus tumidomanus
Cecidocarcinus brychius
Cecidocarcinus zibrowii
Cryptochirus coralliodytes
Cryptochirus planus
Cryptochirus rubrilineatus
Dacryomaia edmonsoni
Dacryomaia japonica
Dacryomaia sp. A
Dacryomaia sp. B
Detocarcinus balssi
Poc
Poc
Poc
Den
Den
Fav, Ocu
Fav, Ocu
Fav, Ocu
Tham, Sid, Fav
Tham, Sid, Fav
Sid
Sid
Rhi, Ocu, Cary,
Den
Mus
Mus
Mus
Mus
Mus
Fung
Fung
Poc, Acr, Ser,
Sty, Por br.
Fav, Mer
Fav, Mer
Fav, Mer
Fav, Mer
Fav, Mer
Fav, Mer
Fav, Mer
Fav, Mer
Fav, Mer
Pav
Den, Tub
Den, Tub
U
U
U
O
O
O
O
O
O
O
O
O
O
H
H
U
H
H
H
H
H
H
H
H
H
H
O
O
O
O
O
O
O
O
H
H
H
H
H
H
H
H
Kropp 1990
Takeda & Tamura 1980
Kropp 1994
Fize & Serne 1956
Kropp 1994
Fize & Serne 1956
Kropp 1990
Fize & Serne 1957
O
O
O
O
O
O
O
O
O
O
O
O
H
H
H
H
H
H
H
H
H
H
H
H
Aga, Pav
Aga, Pav
Aga, Pav
Aga, Sid
Aga, Pav
Aga, Pav
O
O
O
O
O
O
H
H
H
H
H
H
Kropp 1989
Kropp 1989
Kropp 1989
Fize & Serne 1957
Kropp 1989
Kropp 1989
Aga, Pav
Aga, Pav
Fav
Den, Tub
Aga, Sid
O
O
O
O
O
H
H
H
H
H
Kropp 1989
Kropp 1989
Edmondson 1933
Fize & Serne 1957
Fize & Serne 1957
Fizesereneia heimi
Fizesereneia ishikawai
Fizesereneia latisella
Fizesereneia stimpsoni
Fizesereneia tholia
Fungicola fagei
Fungicola utinomi
Haplocarcinus marsupialis
Hiroia krempfi
Lithoscaptus grandis
Lithoscaptus helleri
Lithoscaptus nami
Lithoscaptus pacificus
Lithoscaptus paradoxus
Lithoscaptus pardalotus
Lithoscaptus prionotus
Lithoscaptus tri
Luciades agana
Neotroglocarcinus dawydoffi
Neotroglocarcinus
hongkongensis
Opecarcinus aurantius
Opecarcinus crescentus
Opecarcinus granulatus
Opecarcinus hypostegus
Opecarcinus lobifrons
Opecarcinus peliops
Opecarcinus pholeter
Opecarcinus sierra
Pelycomaia minuta
Pseudocryptochirus viridis
Pseudohapalocarcinus
ransoni
84
Type Use
Reference
CORAL-ASSOCIATED INVERTEBRATES
Higher Taxa
Family: Diogenidae
Family:
Domeciidae
Family: Dromiidae
Family: Epialtidae
Family: Galatheidae
Family:
Gnathophyllidae
Family:
Hippolytidae
Species
Coral taxa
Sphenomaia pyriforma
Troglocarcinus corallicola
Fav
Ast, Sid, Fav,
Ocu, Mea,
Mus, Cary
Poc
Fav, Mer, Pec
Fav, Mer, Pec
Fav, Mer, Pec
Phyl
Poc
Scl
Poc
Poc
Poc
Acr, Por br.,
Poc, Sty, Ser
Poc
Scl
Sty
Scl
Sty, Acr
Poc
Scl
Sty
Scl
Scl
Scl
Poc
Acr
Acr
Acr, Poc
Poc, Sty
Fav, Pav, Por
Scl
Sty
Poc
Poc
Poc
Sty
Sty, Acr, Poc
Sty
Sty
Poc
Poc
Poc
Poc
Utinomiella dimorpha
Xynomaia boissini
Xynomaia sheni
Xynomaia verrilli
Zibrovia galea
Aniculus elegans
Calcinus albengai
Calcinus californiensis
Calcinus explorator
Calcinus gouti
Calcinus guamensis
Calcinus haigae
Calcinus inconspicuus
Calcinus latens
Calcinus lineapropodus
Calcinus minutus
Calcinus obscurus
Calcinus pulcher
Calcinus rosaceus
Calcinus spicatus
Ciliopagurus strigatus
Diogenes serenei
Trizopagurus magnificus
Domecia acanthophora
Domecia africana
Domecia glabra
Domecia hispida
Jonesius triunguiculatus
Palmyria palmyrensis
Cryptodromia granulata
Herbstia tumida
Menaethius monoceros
Pelia pacifica
Perinea tumida
Tylocarcinus styx
Galathea affinis
Galathea humilis
Gnathophyllum panamense
Hymenocera picta
Hippolysmata vittata
Hippolyte varians
Type Use
Reference
O
O
H
H
Edmondson 1933
Kropp & Manning 1987
O
O
O
O
O
F
U
U
U
F
U
H
H
H
H
H
F
U
U
U
U
U
F
U
U
U
U
U
U
U
F
F
U
F
F
F
F
F
F
O
U
U
U
U
U
U
U
U
U
O
F
F
U
U
U
U
U
U
U
U
U
U
U
F
H
H
H
H
H
H
U
U
U
U
U
U
U
U
U
H
U
U
85
Higher Taxa
Family:
Hymenosomatidae
Family:
Leucosiidae
Family:
Mithracidae
Family: Paguridae
Family:
Palaemonidae
Species
Coral taxa
Hippolyte ventricosus
Latreutes mucronatus
Lysmata californica
Phycocaris simulans
Saron marmoratus
Thor algicola
Thor amboinensis
Thor cordelli
Thor maldivensis
Thor paschalis
Elamena abrolhosensis
Halicarcinus ovatus
Uhlias ellipticus
Poc
Poc
Poc
Poc
Poc, Sty
Poc
Poc
Poc
Poc
Poc
Poc
Poc
Poc
F
F
U
F
F
U
F
U
F
F
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
Mithraculus forceps
Mithrax pygmaeus
Teleophrys cristulipes
Paguritta sp.
Paguritta corallicola
Paguritta gracilipes
Paguritta harmsi
Paguritta kroppi
Paguritta morgani
Paguritta scottae
Pagurixis amsa
Pagurus lepidus
Brachycarpus biunguiculatus
Coralliocaris brevirostris
Coralliocaris graminea
Coralliocaris labyrintha
Coralliocaris macrophthalma
Coralliocaris nudirostris
Coralliocaris pavoni
Coralliocaris sandyi
Coralliocaris superba
Coralliocaris taiwanensis
Coralliocaris venusta
Coralliocaris viridis
Fennera chacei
Harpiliopsis beaupresii
Harpiliopsis depressa
Harpiliopsis spinigera
Harpilius bayeri
Harpilius consobrinus
Harpilius lutescens
Ischnopontonia lophos
Jacoste japonica
Jacoste lucina
Ocu
Poc
Poc
Monp
Acr
Scl
Scl
Scl
Monp
Por
Poc
Poc
Poc
Acr
Acr
Acr
Acr
Acr
Pav
Acr
Acr
Pav
Acr
Acr
Poc
Poc, Sty
Poc, Sty
Poc, Sty
Poc
Poc
Acr, Poc
Gal
Acr
Acr
F
U
U
F
O
U
U
U
U
U
U
U
U
U
O
U
U
O
U
U
O
O
O
O
O
U
O
U
O
O
O
O
U
U
H
U
U
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
86
Type Use
Reference
CORAL-ASSOCIATED INVERTEBRATES
Higher Taxa
Species
Coral taxa
Kemponia amymone
Kemponia kororensis
Metapontonia fungiacola
Palaemonella assymetrica
Palaemonella holmesi
Palaemonella rotumana
Palaemonella spinulata
Palaemonella tenuipes
Paratypton siebenrocki
Periclimenaeus arabicus
Periclimenaeus hectat
Periclimenes andamanensis
Periclimenes calmani
Periclimenes consobrinus
Periclimenes difficilus
Periclimenes diversipes
Family: Pandalidae
Periclimenes elegans
Periclimenes grandis
Periclimenes holthuisi
Periclimenes longirostris
Periclimenes madreporae
Periclimenes magnificus
Periclimenes mahei
Periclimenes pettihouarsi
Periclimenes seychellensis
Periclimenes sibogae
Periclimenes speciosus
Periclimenes spiniferus
Periclimenes suvadivensis
Periclimenes toloensis
Philarius gerlachi
Philarius imperialis
Philocheras sp.
Platycaris latirostris
Pontonides maldivensis
Pontonides sibogae
Pontonides unciger
Tectopontonia maziwiae
Thaumatocaris streptopus
Vir longidactylus
Vir orientalis
Vir philippinensis
Yemenicaris trullicauda
Chlorocurtis jactans
Chlorotocella gracilis
Type Use
Reference
Patton 1966
O
U
U
U
F
F
U
O
U
F
F
U
U
U
U
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
Bruce 1977
Bruce 1974b
Abele & Patton 1976
Hernndez et al. 2009
Bruce 1972b
Preston & Doherty 1990
Bruce 1972b
Bruce 1978
Bruce 1974c
Austin et al. 1980
Preston & Doherty 1990
Edwards & Emberton 1980
Bruce 1974d
Bruce 1977
Bruce 1976
F
F
F
F
O
U
U
U
F
U
U
U
F
F
U
U
F
U
O
O
O
U
F
O
U
O
U
F
F
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
U
U
87
Higher Taxa
Species
Coral taxa
Family: Pilumnidae
Tanaocheles stenochilus
Tanaocheles bidentata
Pilumnus reticulatus
Pilumnus stimpsonii
Megalobrachium erosum
Megalobrachium smithii
Megalobrachium
tuberculipes
Pachycheles biocellatus
Pachycheles granti
Pachycheles pisiodes
Pachycheles sculptus
Pachycheles vicarius
Petrolisthes agassizii
Petrolisthes carinipes
Petrolisthes edwardsii
Petrolisthes galanthinus
Petrolisthes glasselli
Petrolisthes haigae
Petrolisthes hirtispinosus
Petrolisthes polymitus
Petrolisthes sp.
Pisidia inaequalis
Pisidia magdalenensis
Ulloaia perpusillia
Thalamitoides tridens
Thalamita sp.
Processa australiensis
Sicyonia sp.
Stenopus hispidus
Poc
Poc
Poc
Poc
Poc
Poc
Poc
U
U
U
U
U
U
U
H
H
H
H
U
U
U
Kropp 1984
Ng & Clark 2000
Abele & Patton 1976
Abele & Patton 1976
Abele & Patton 1976
Abele & Patton 1976
Abele & Patton 1976
Poc
Poc
Poc
Poc
Poc
Poc
Sty
Poc
Poc
Poc
Poc
Poc
Poc
Poc
Sty
Poc
Poc
Sty
Poc
Poc
Poc
Scl
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
F
F
F
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
H
Neaxius vivesi
Poc
Tetralia aurantistellata
Tetralia brengelae
Tetralia brunalineata
Tetralia cavimana
Tetralia cinctipes
Tetralia glaberrima
Tetralia muta
Tetralia nigrolineata
Tetralia ocucaerulea
Acr
Acr
Acr
Acr
Acr
Acr
Acr
Acr
Acr
O
O
O
O
O
O
O
O
O
F
F
F
F
F
F
F
F
F
Trautwein 2007
Trautwein 2007
Trautwein 2007
Trautwein 2007
Vytopil & Willis 2001
Vytopil & Willis 2001
Galil & Clark 1988
Vytopil & Willis 2001
Trautwein 2007
Tetralia rubridactyla
Tetraloides heterodactyla
Tetraloides nigrifrons
Quadrella boopsis
Trapezia areolata
Trapezia bella
Acr, Poc
Acr
Acr
Den
Poc
Poc
O
O
O
O
O
O
F
F
F
H
F
F
Family:
Porcellanidae
Family: Portunidae
Family: Processidae
Family: Sicyoniidae
Family:
Stenopodidae
Family:
Strahlaxiidae
Family: Tetraliidae
Family: Trapeziidae
88
Type Use
Reference
CORAL-ASSOCIATED INVERTEBRATES
Higher Taxa
Family:
Upogebiidae
Family: Xanthidae
Species
Coral taxa
Trapezia bidentata
Trapezia cheni
Trapezia corallina
Trapezia cymodoce
Trapezia digitalis
Trapezia flavopunctata
Trapezia ferruginea
Trapezia formosa
Trapezia garthi
Trapezia globosa
Trapezia guttata
Trapezia intermedia
Trapezia lutea
Trapezia plana
Trapezia neglecta
Trapezia punctimanus
Trapezia richtersi
Trapezia rufopunctata
Trapezia septata
Trapezia serenei
Trapezia speciosa
Trapezia tigrina
Upogebia operculata
Pomatogebia rugosa
Chlorodiella laevissima
Chlorodiella nigra
Chlorodiella spinipes
Cyclodius nitidus
Cyclodius ungulatus
Cycloxanthus bocki
Cycloxanthus vittatus
Cymo andreossyi
Cymo barunae
Cymo cerasma
Cymo deplanatus
Cymo lanatopodus
Cymo melanodactylus
Cymo quadrilobatus
Cymo tuberculatus
Etisus anaglyptus
Etisus electra
Heteractaea lunata
Liocarpilodes integerrimus
Liomera rugata
Lophoxanthus lamellipes
Macromedaeus nudipes
Paractaea retusa
Poc
Poc
Poc
Poc, Sty
Poc, Sty
Poc
Poc, Sty
Poc
Poc
Poc
Poc, Sty
Poc, Sty
Poc
Poc
Poc
Poc
Poc
Poc
Poc
Poc
Poc
Poc
Por ma.
Por ma.
Poc, Ser, Acr
Poc, Sty
Sty
Sty
Poc
Poc
Poc
Poc
Acr
Poc
Acr
Poc
Acr
Poc
Poc
Poc
Sty
Poc
Sty
Sty
Poc
Ser
Sty
Type Use
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
U
U
U
U
U
U
U
U
U
U
O
U
O
O
O
O
U
U
U
U
U
U
U
U
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
H
H
U
H
H
H
H
H
H
H
H
H
H
H
F
H
H
U
H
H
H
H
H
U
H
Reference
Castro et al. 2004
Chang et al. 1987
Castro et al. 2004
Chang et al. 1987
Chang et al. 1987
Castro et al. 2004
Edwards & Emberton 1980
Chang et al. 1987
Chang et al. 1987
Castro et al. 2004
Castro et al. 2004
Castro et al. 2004
Castro et al. 2004
Castro et al. 2004
Castro et al. 2004
Castro et al. 2004
Castro et al. 2004
Chang et al. 1987
Chang et al. 1987
Castro et al. 2004
Castro et al. 2004
Castro et al. 2004
Scott 1987
Fonseca & Corts 1998
Stella et al. 2010
Austin et al. 1980
Edwards & Emberton 1980
Edwards & Emberton 1980
Patton 1974
Abele & Patton 1976
Abele & Patton 1976
Patton 1974
Ho & Ng 2005
Morgan 1990
Patton 1994
Galil & Vannini 1990
Patton 1994
Galil & Vannini 1990
Serne 1984
Black & Prince 1983
Edwards & Emberton 1980
Abele & Patton 1976
Edwards & Emberton 1980
Edwards & Emberton 1980
Abele & Patton 1976
Stella et al. 2010
Edwards & Emberton 1980
continued
89
Higher Taxa
Order: Stomatopoda
Family:
Gonodactylidae
Species
Coral taxa
Type Use
Reference
Paractaea rufopunctata
Paraxanthis elegans
Psaumis cavipes
Pseudoliomera granosimana
Pseudoliomera remota
Pseudoliomera speciosa
Stenorynchus debilis
Poc
Poc
Poc
Sty
Sty
Sty
Poc
U
U
U
U
U
U
U
U
H
U
H
H
H
H
Gonodactylus falcatus
Gonodactylus sp.
Sty
Poc
F
U
H
H
Armatobalanus allium
Ahoekia chuangi
Ahoekia microtrema
Ahoekia tanabensis
Arossella lynnae
Australhoekia cardenae
Cantellius acutum
Cantellius albus
Cantellius alphonsei
Cantellius arcuatum
Cantellius brevitergum
Cantellius cardenae
Cantellius euspinulosa
Cantellius gregarius
Cantellius hiroi
Cantellius hoegi
Cantellius iwayama
Cantellius iwayama
Cantellius madreporae
Cantellius octavus
Cantellius pallidus
Cantellius preobrazhenskyi
Cantellius pseudopallidum
Cantellius quintus
Cantellius secundus
Cantellius septimus
Cantellius sextus
Cantellius sinensis
Cantellius sumbawae
Cantellius transversalis
Cantellius tredecimus
Ceratoconcha domingensis
Ceratoconcha floridana
Ceratoconcha paucicostata
Mont
Scl
Scl
Scl
Scl
Scl
Acr
Scl
Monp
Scl
Scl
Acr
Ast
Scl
Scl
Pach
Ast
Ast
Scl
Scl
Ast
Scl
Scl
Scl
Acr
Monp
Scl
Scl
Scl
Scl
Ast
Scl
Scl
Scl
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
Class : Maxillopoda
Sub Class : Cirripedia
Order: Sesslilia
Family: Balanidae
Family:
Pyrgomatidae
90
CORAL-ASSOCIATED INVERTEBRATES
Higher Taxa
Species
Coral taxa
Ceratoconcha quarta
Cionophorus guillaumae
Cionophorus soongi
Creusia spinulosa
Darwiniella conjugatum
Eohoekia chaos
Eohoekia nyx
Galkinia angustiradiata
Galkinia decima
Galkinia indica
Galkinia supraspinulosa
Hiroa stubbingsi
Hoekia fornix
Hoekia monticulariae
Hoekia mortenseni
Hoekia philippensis
Megatrema anglicum
Megatrema madreporarium
Megatrema oulastreae
Neopyrgoma lobata
Neotravatha elongatum
Nobia conjugatum
Nobia grandis
Nobia halomitrae
Nobia orbicellae
Parahoekia aster
Pyrgoma cancellatum
Pyrgoma japonica
Pyrgoma kuri
Pyrgoma monticulariae
Pyrgoma projectyum
Pyrgoma sinica
Pyrgopsella annandalei
Pyrgopsella stellula
Savignium crenatum
Savignium elongatum
Trevathana dentata
Trevathana jensi
Trevathana margaretae
Trevathana mizrachae
Trevathana niuea
Trevathana orientale
Trevathana paulayi
Trevathana sarae
Wanella andersonorum
Wanella snelliusi
Por
Ast
Ast
Scl
Scl
Scl
Scl
Scl
Scl
Scl
Scl
Ast
Scl
Scl
Scl
Scl
Scl
Aga
Scl
Tub
Fav, Goni
Scl
Scl
Scl
Scl
Scl
Den
Loph
Cary
Scl
Cary
Den
Scl
Scl
Goni
Scl
Goni, Lep
Fav
Fav
Plat
Gon
Fav
Acan
Cyph
Scl
Scl
Type Use
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
U
U
O
O
O
O
O
O
O
O
O
O
O
O
U
O
O
O
O
O
O
O
O
O
O
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
H
Reference
Scott 1987
Achituv & Newman 2002
Ross & Newman 2000
Ross & Newman 2000
Ross & Newman 2000
Ross & Newman 2000
Ross & Newman 2000
Ross & Newman 2000
Ogawa et al. 1998
Ogawa et al. 1998
Ross & Newman 2002
Achituv & Newman 2002
Ross & Newman 2000
Ross & Newman 2000
Ross & Newman 2000
Ross & Newman 2000
Ross & Newman 2000
Scott 1987
Ross & Newman 2000
Ross & Newman 2002
Ross & Newman 2002
Ogawa et al. 1998
Ogawa et al. 1998
Ross & Newman 2000
Ross & Newman 2000
Ross & Newman 2000
Ogawa et al. 1998
Ross & Newman 2002
Ross & Newman 2002
Ross & Newman 1969
Ross & Newman 2002
Ross & Newman 2002
Ross & Newman 2002
Ross & Newman 2002
Ross & Newman 1973
Ogawa et al. 1998
Ogawa et al. 1998
Brickner et al. 2010
Brickner et al. 2010
Brickner et al. 2010
Ogawa et al. 1998
Ogawa et al. 1998
Ogawa et al. 1998
Brickner et al. 2010
Ross & Newman 2000
Ross & Newman 2000
continued
91
Higher Taxa
Species
Coral taxa
Type Use
Reference
Corallonoxia baki
Corallonoxia longicauda
Corallonoxia mixtibrachium
Corallonoxia similis
Corallonoxia ventrospinosa
Corallovexia brevibrachium
Corallovexia dorospina
Corallovexia kristenseni
Corallovexia longibrachium
Corallovexia mediobrachium
Pterinopsyllus stirpipes
Mea
Mea
Fav
Acr
Mont
Dip
Mont
Fav
Fav
Dip
Gal
O
O
O
O
O
O
O
O
O
O
O
F
F
F
F
F
F
F
F
F
F
H
Stock 1975
Stock 1975
Stock 1975
Stock 1975
Stock 1975
Stock 1975
Stock 1975
Stock 1975
Stock 1975
Stock 1975
Humes 1997a
Alteuthellopsis corallina
Humes 1981
O
O
H
H
Humes 1981
Humes 1981
Monp
Ocu
Aga
Gon, Gal
Gal
Gon, Gal
Gal
Gon, Fung
Gon
Aga
Ech
Aga
Gon
Pav
Fung
Fung
Fung
Fung
Gon
Gal
Alv
Gal
Fung
Ser
Fung
Fung
Hydn
O
O
O
O
O
O
O
O
O
O
O
O
O
O
U
U
U
U
O
O
O
O
O
U
U
O
U
H
F
F
F
F
F
F
F
F
F
F
F
F
F
U
U
U
U
F
F
F
F
F
U
U
F
U
Humes 1994
Humes 1991a
Kim 2006
Humes 1995a
Humes 1996a
Humes 1995a
Humes 1979b
Humes & Ho 1968
Humes & Ho 1968
Humes & Stock 1972
Humes 1991a
Humes 1992
Humes 1995a
Kim 2007
Humes 1996a
Kim 2007
Humes 1978a
Kim 2003
Humes 1995a
Humes 1996a
Kim 2003
Humes 1996b
Humes 1978a
Kim 2003
Humes 1978a
Humes 1978a
Kim 2007
Family:
Pterinopsyllidae
Order: Harpacticoida
Family: Peltidiidae
Family: Tegastidae
Tegastes acroporanus
Tegastes georgei
Order: Poecilostomatoida
Family:
Allopodion mirum
Anchimolgidae
Anchimolgus abbreviatus
Anchimolgus angustus
Anchimolgus brevarius
Anchimolgus compressus
Anchimolgus conformatus
Anchimolgus contractus
Anchimolgus convexus
Anchimolgus digitatus
Anchimolgus eparmatoides
Anchimolgus exsertus
Anchimolgus gibberulus
Anchimolgus gigas
Anchimolgus gracilipes
Anchimolgus gratus
Anchimolgus hastatus
Anchimolgus latens
Anchimolgus maximus
Anchimolgus mimeticus
Anchimolgus moluccanus
Anchimolgus multidentatus
Anchimolgus nasutus
Anchimolgus notatus
Anchimolgus noumensis
Anchimolgus orectus
Anchimolgus pandus
Anchimolgus paragensis
92
CORAL-ASSOCIATED INVERTEBRATES
Higher Taxa
Species
Coral taxa
Anchimolgus partenuipes
Anchimolgus prolixipes
Anchimolgus punctilis
Anchimolgus setellus
Anchimolgus tanaus
Anchimolgus tenuipes
Anchimolgus tridentatus
Andrianellus exsertidens
Andrianellus papillipes
Amarda compta
Amarda cultrata
Amarda curvus
Amarda goniastreae
Amardopsis merulinae
Dumbeana undulatipes
Ecphysarion ampullulum
Ecphysarion lobophorum
Ecphysarion spinulatum
Cerioxynus alatus
Cerioxynus bandensis
Cerioxynus favitocolis
Cerioxynus moluccensis
Cerioxynus montastreae
Cerioxynus oulophylliae
Ecphysarion lobophorum
Haplomolgus incolumis
Haplomolgus montiporae
Haplomolgus subdeficiens
Humesiella corallicola
Kawanolus parangensis
Lipochaetes extrusus
Odontomolgus actinophorus
Odontomolgus bulbalis
Odontomolgus campulus
Odontomolgus decens
Odontomolgus exilipes
Odontomolgus flammeus
Odontomolgus forhani
Odontomolgus fultus
Odontomolgus geminus
Odontomolgus mucosus
Odontomolgus mundulus
Odontomolgus parvus
Odontomolgus pavonus
Odontomolgus pumilis
Odontomolgus rhadinus
Odontomolgus scitulus
Poc
Por
Fung
Aga
Ocu
Ser
Ech
Fav
Plat
Fav
Fav
Goni
Goni
Mer
Psa
Acr
Acr
Acr
Fav
Fav
Fav
Fav
Fav
Fav
Acr
Monp
Monp
Monp
Hydn
Monp
Psa
Pav
Mer
Alv
Fung
Psa
Fung
Monp
Fung
Psa
Aga
Alv
Goni
Pav
Aga
Psa
Fung
Type Use
U
U
U
O
O
U
U
O
U
O
O
O
O
O
O
O
U
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
U
O
O
U
U
O
O
U
O
O
U
U
O
O
O
U
U
U
F
F
U
U
F
U
F
F
F
F
F
F
F
U
F
F
F
F
F
F
F
H
F
H
F
H
H
F
F
U
F
F
U
U
F
F
U
F
F
U
U
F
F
F
Reference
Kim 2007
Humes & Ho 1968
Humes 1978a
Humes 1992
Humes 1991a
Kim 2003
Kim 2003
Humes & Stock 1973
Kim 2007
Humes & Stock 1972
Humes & Stock 1972
Kim 2007
Humes 1985b
Humes 1974a
Humes 1996b
Humes 1993
Humes & Ho 1968
Humes 1993
Humes 1974a
Humes 1979c
Humes 1974a
Humes 1974a
Humes 1986
Humes 1986
Humes 1994
Humes 1991b
Humes 1994
Humes 1978b
Sebastian & Pillai 1973
Humes 1994
Humes 1996b
Humes & Frost 1964
Humes 1991a
Humes & Ho 1968
Humes 1978a
Kim 2003
Kim 2007
Humes 1978b
Humes 1978a
Kim 2003
Kim 2006
Humes 1974b
Kim 2007
Kim 2007
Humes 1992
Humes & Ho 1967
Humes 1973
continued
93
Higher Taxa
Family:
Clausidiidae
Family:
Rhynchomolgidae
Species
Coral taxa
Odontomolgus unioviger
Panjakus bidentis
Panjakus directus
Panjakus eumeces
Panjakus fastigatus
Panjakus hydnophorae
Panjakus iratus
Panjakus necopinus
Panjakus parvipes
Panjakus platygyrae
Panjakus saccipes
Paraclamocus hiulcus
Prionomolgus lanceolatus
Rakotoa ceramensis
Rakotoa proteus
Schedomolgus arcuatipes
Schedomolgus dumbensis
Schedomolgus exiliculus
Schedomolgus idanus
Schedomolgus insignellus
Schedomolgus majusculus
Schedomolgus tener
Schedomolgus tenuicaudatus
Schedomolgus walteri
Scyphuliger aristoides
Scyphuliger concavipes
Scyphuliger eumorphus
Scyphuliger humesi
Scyphuliger karangmiensis
Scyphuliger latus
Scyphuliger longicaudatus
Scyphuliger manifestus
Scyphuliger paucisurculus
Scyphuliger pennauts
Scyphuliger pilosis
Scyphuliger placidus
Scyphuliger tenuatus
Scyphuliger vicinus
Stockia indica
Unicispina latigenitalis
Hemicyclops columnaris
Aga
Poc
Fav
Hydn
Plat
Hydn
Hydn
Fav
Plat
Plat
Hydn
Psa
Aga
Fav
Fav
Acr
Fung
Acr
Acr
Acr
Acr
Fung
Acr
Lob
Acr
Acr
Acr
Acr
Acr
Acr
Acr
Acr
Acr
Acr
Acr
Acr
Acr
Acr
Fav
Acr
Por ma.
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
U
U
O
O
O
O
U
U
U
O
U
U
U
O
O
O
O
O
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
H
U
U
F
F
F
F
U
U
U
F
U
U
U
F
F
F
F
F
H
Kim 2006
Kim 2004
Humes 1995b
Humes 1991a
Kim 2005
Humes & Stock 1973
Kim 2005
Humes 1995b
Kim 2005
Humes & Stock 1973
Kim 2005
Humes 1997b
Humes & Ho 1968
Humes 1979c
Humes & Stock 1973
Humes & Ho 1968
Kim 2003
Humes 1993
Humes 1993
Humes 1993
Humes 1993
Humes 1973
Kim 2003
Kim 2003
Humes 1993
Humes 1991a
Humes 1993
Kim 2004
Kim 2007
Kim 2003
Kim 2003
Humes 1991a
Kim 2003
Kim 2003
Kim 2003
Kim 2004
Humes 1994
Kim 2004
Humes 1994
Humes 1993
Humes 1984a
Diallagomolgus productus
Diallagomolgus vicinus
Isomolgus desmotes
Kombia angulata
Kombia avitus
Kombia curvata
Cyph
Cyph
Ser
Psa
Por
Por ma.
O
O
O
O
U
O
F
F
F
F
U
F
Humes 1979d
Humes 1979d
Dojiri 1988
Humes 1962b
Kim 2007
Nair & Pillai 1986
94
Type Use
Reference
CORAL-ASSOCIATED INVERTEBRATES
Higher Taxa
Family: Xarifiidae
Species
Coral taxa
Kombia imminens
Kombia incrassata
Mandobius regalis
Monomolgus baculigeres
Monomolgus psammocorae
Monomolgus torulus
Monomolgus unihastatus
Numboa porosa
Pennatulicola corallophilus
Ravahina tumida
Spaniomolgus compositus
Spaniomolgus crassus
Spaniomolgus geminus
Wedanus inconstans
Xenomolgus varius
Hastatus faviae
Lipochrus acroporinus
Orstomella faviae
Orstomella lobophylliae
Orstomella yaliuensis
Xarifia ablusa
Xarifia acicularis
Xarifia anomala
Xarifia anopla
Xarifia apertipes
Xarifia basilica
Xarifia brevicauda
Xarifia breviramea
Xarifia bullifera
Xarifia clavellata
Xarifia comptula
Xarifia comata
Xarifia curtata
Xarifia decorata
Xarifia diminuta
Xarifia dispar
Xarifia dissona
Xarifia echinoporae
Xarifia eminula
Xarifia exigua
Xarifia exserens
Xarifia extensa
Xarifia exuta
Xarifia fastiga
Xarifia filata
Xarifia fimbriata
Xarifia finitima
Por ma.
Por ma.
Pec
Por br.
Psa
Por ma.
Por br.
Psa
Por ma.
Por br.
Ser
Sty
Sty
Gon
Por ma.
Fav
Acr
Fav
Lob
Por ma.
Acr
Aga
Acr
Monp
Cary
Acr
Alv
Acr
Acr
Aga
Hydn
Poc
Hydn
Sty
Psa
Ech
Sty
Ech
Ser
Aga
Gal
Monp
Acr
Acr
Aga
Poc
Pav
Type Use
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
Reference
Humes 1979a
Humes 1984b
Humes 1991c
Humes 1979a
Humes & Ho 1967
Humes 1984b
Humes & Stock 1973
Humes 1997b
Nair & Pillai 1986
Humes & Ho 1968
Humes & Frost 1964
Humes & Ho 1968
Humes & Ho 1968
Humes 1978c
Humes & Stock 1973
Ho et al. 2010
Humes & Dojiri 1982
Humes & Ho 1968
Humes & Ho 1968
Cheng et al. 2009
Humes & Dojiri 1982
Humes 1985c
Humes & Ho 1968
Humes & Dojiri 1982
Humes & Dojiri 1983
Humes 1985c
Humes & Ho 1968
Humes 1994
Humes 1985c
Humes 1985c
Humes & Dojiri 1983
Humes 1962a
Humes & Dojiri 1983
Humes & Ho 1968
Humes & Ho 1967
Humes 1962a
Humes 1985c
Humes & Dojiri 1982
Humes 1985c
Humes & Ho 1968
Humes 1985c
Humes & Dojiri 1982
Humes & Dojiri 1982
Humes & Dojiri 1982
Humes 1985c
Humes 1985a
Humes 1985c
continued
95
Higher Taxa
Species
Coral taxa
Xarifia fissilis
Xarifia formosa
Xarifia gerlachi
Xarifia gibberula
Xarifia gracilipes
Xarifia gradata
Xarifia guttulifera
Xarifia hadra
Xarifia hamata
Xarifia heteromeles
Xarifia imitans
Xarifia imparilis
Xarifia indica
Xarifia infrequens
Xarifia insolita
Xarifia jugalis
Xarifia laccadivensis
Xarifia lacerans
Xarifia lamellispinosa
Xarifia levis
Xarifia linearis
Xarifia lissa
Xarifia longa
Xarifia longicauda
Xarifia longipes
Xarifia maldivensis
Xarifia mediolobata
Xarifia minax
Xarifia mucronata
Xarifia obesa
Xarifia pectinea
Xarifia plectrata
Xarifia quinaria
Xarifia radians
Xarifia rasilis
Xarifia reducta
Xarifia resex
Xarifia robusta
Xarifia rosariae
Xarifia sabiuraensis
Xarifia scutipes
Xarifia sectilis
Xarifia serrata
Xarifia simplex
Xarifia syntoma
Xarifia temnura
Xarifia tenta
Xarifia tenuis
Poc
Psa
Acr
Poc
Cary
Cary
Acr
Gon
Tur
Monp
Psa
Poc
Acr
Acr
Tub
Poc
Acr
Tur
Aga
Ser
Acr
Sty
Por br.
Acr
Pav
Poc
Alv
Cary
Acr
Poc
Acr
Ocu
Poc
Alv
Acr
Ser
Gon
Acr
Acr
Acr
Acr
Poc
Poc
Mer
Monp
Monp
Poc
Acr
96
Type Use
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
O
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
F
Reference
Humes 1985c
Humes 1985c
Humes 1994
Humes 1985c
Humes & Dojiri 1983
Humes & Dojiri 1983
Humes & Dojiri 1982
Humes & Dojiri 1983
Humes & Ho 1968
Humes 1994
Humes 1985c
Humes 1985c
Nair 1983
Humes 1962a
Cheng et al. 2007
Humes 1985c
Nair 1983
Humes 1985c
Humes & Ho 1968
Humes 1985c
Nair 1983
Humes & Ho 1968
Cheng et al. 2007
Nair 1983
Humes 1962a
Humes 1960
Humes & Dojiri 1982
Humes & Dojiri 1983
Humes & Dojiri 1982
Humes & Ho 1968
Humes & Dojiri 1982
Humes 1985c
Humes 1985c
Humes & Dojiri 1982
Humes 1985c
Humes 1962a
Humes & Dojiri 1983
Nair 1983
Humes & Dojiri 1982
Humes 1994
Humes & Dojiri 1983
Humes 1985c
Humes 1962a
Humes 1985c
Humes 1994
Humes 1994
Humes 1985c
Humes 1962a
CORAL-ASSOCIATED INVERTEBRATES
Higher Taxa
Species
Coral taxa
Xarifia torigera
Xarifia trituberata
Xarifia tumorisa
Xarifia uncinata
Xarifia umbonata
Xarifia varilabrata
Xarifia villosa
Zazaranus fungicolis
Fav
Acr
Acr
Tur
Ser
Ser
Cyph
Fung
O
O
O
O
O
O
O
O
F
F
F
F
F
F
F
F
Humes 1985c
Humes 1994
Humes 1994
Humes 1985c
Humes 1985c
Humes 1985c
Humes & Dojiri 1982
Humes & Dojiri 1983
Fung
Fung
Monp
Gal
Gal
O
O
O
O
O
H
H
H
H
H
Humes 1997a
Humes 1997a
Humes 1994
Humes 1997a
Humes 1997a
Barbatia foliata
Barbatia fusca
Barbatia setigera
Por
Acr
Anac, Monp
U
U
U
H
H
H
Brachidontes variabilis
Fungiacava eilatensis
Lithophaga antillarum
U
O
O
H
H
H
O
O
O
O
O
O
O
H
H
H
H
H
H
H
Scott 1986
Scott 1988
Soliman 1969
Scott 1986
Otter 1937
Wilson 1979
Wilson 1979
Lithophaga lessepsiana
Lithophaga lima
Lithophaga malaccana
Lithophaga nasuta
Lithophaga nigra
Lithophaga obesa
Lithophaga parapurpurea
Sty
Fung
Cyph, Monp,
Goni, Sty,
Mont, Dip
Ste
Sty
Mad
Por ma.
Poc, Acr, Sty
Por ma., Ast,
Monp, Gon,
Cyph
Sty
Cyph
Por, Poc, Fav
Goni, Por
Goni, Fav
Cyph
Cyph, Monp
O
O
F
O
F
O
O
H
H
H
H
H
H
H
Lithophaga simplex
Lithophaga teres
Modiolus auriculatus
Musculista glaberrima
Septifer bilocularis
O
O
U
U
U
H
H
H
U
U
Wilson 1979
Gohar & Soliman 1963
Mohammed & Yassien 2008
Black & Prince 1983
Black & Prince 1983
Order: Siphonostomatoida
Family:
Temanus halmaherensis
Artotrogidae
Tondua tholincola
Family:
Hetairosyna sororia
Asterocheridae
Hetairosynopsis bucculentus
Madacheres serrulatus
Type Use
Reference
Phylum Mollusca
Class: Bivalvia
Order: Arcoida
Family: Arcidae
Order: Mytiloida
Family: Mytilidae
Lithophaga aristata
Lithophaga bisulcata
Lithophaga cumingiana
Lithophaga dixonae
Lithophaga hanleyana
Lithophaga kuehnelta
Lithophaga laevigata
continued
97
Higher Taxa
Order: Ostreoida
Family: Ostreidae
Family: Pectinidae
Family:
Spondylidae
Order: Pterioda
Family: Pteriidae
Order: Veneroida
Family: Veneridae
Family: Cardiidae
Species
Coral taxa
Type Use
Reference
Alectryonella plicatula
Ostraea sp.
Pedum spondyloideum
Chlamys madreporarum
Chlamys sp. A
Chlamys sp. B
Mimachlamys lentiginosa
Spondylus nicobaricus
Spondylus spinosus
Por ma.
Por ma.
Por, Acr
Acr
Ser
Acr
Poc
Sty
Sty
F
F
O
U
U
U
U
U
U
H
H
H
U
U
U
U
H
H
Coleman 2003
Coleman 2003
Yonge 1967
Stella et al. 2010
Stella et al. 2010
Stella et al. 2010
Stella et al. 2010
Mohammed & Yassien 2008
Mohammed & Yassien 2008
Electroma alacorvi
Pinctada radiata
Acr, Poc
Acr, Sty, Monp
U
U
H
H
Gefrarium pectinatum
Tridacna crocea
Tridacna maxima
Sty
Por ma.
Por, Sty
U
U
U
H
H
H
Poc
Poc
U
U
U
U
Ser
Poc
Poc
Cary
Por ma.
U
U
F
F
U
U
U
F
F
H
Por
Robertson 1970
Poc, Ser
Poc
Poc
Poc
Acr
Den
Tub
Den
Den
Fung
Fung
Fung
Fung
Fung
Fung
Fung
U
U
U
U
U
O
O
O
O
O
O
O
O
O
O
O
U
U
U
U
U
F
F
F
F
F
F
F
F
F
F
F
Class: Gastropoda
Order: Caenogastropoda
Family: Cerithiidae
Cacozeliana granarium
Cerithium nesioticum
Order: Littorinimorpha
Family: Cypraeidae
Family: Littorinidae
Family:
Pediculariidae
Family: Vermetidae
Cypraea asellus
Austrolittorina unifasciata
Jenneria pustulata
Pedicularia decussata
Dendropoma maximum
Order: Neogastropoda
Family:
Philippia radiata
Architectonicidae
Family: Buccinidae
Pisania fasiculata
Pisania ignea
Family:
Pyrene bidentata
Collumbellidae
Pyrene testudinaria
Family: Epitoniidae
Cirsotrema sp. A
Epidendrium aureum
Epidendrium billeeanum
Epidendrium dendrophylliae
Epidendrium sordidum
Epifungium adgranulosa
Epifungium adgravis
Epifungium adscabra
Epifungium hartogi
Epifungium hoeksemai
Epifungium lochi
Epifungium marki
98
CORAL-ASSOCIATED INVERTEBRATES
Higher Taxa
Family:
Fasciolariidae
Family: Mitridae
Family: Muricidae
Species
Coral taxa
Epifungium nielsi
Epifungium pseudolochi
Epifungium pseudotwilae
Epifungium twilae
Epifungium ulu
Epitonium crassicostatum
Epitonium graviarmatum
Epitonium hartogi
Surrepifungium costulatum
Surrepifungium ingridae
Surrepifungium oliverioi
Surrepifungium
patamakanthini
Microcolus dunkeri
Fung
Fung
Fung
Fung
Fung
Fung
Fung
Pler
Fung
Fung
Fung
Fung
O
O
O
O
O
O
O
O
O
O
O
O
F
F
F
F
F
F
F
F
F
F
F
F
Poc
Mitra ferruginea
Mitra sp. A
Mitra sp. B
Coralliophila abreviata
Coralliophila australis
Coralliophila caribaea
Coralliophila costularis
Coralliophila erosa
Coralliophila fimbriata
Coralliophila latilirata
Coralliophila neritoidea
Coralliophila pyriformis
Coralliophila violacea
Cronia avellana
Dicathais textilosa
Drupella cornus
Poc
Poc, Ser, Acr
Poc, Ser
Acr
Scl
Acr, Por
Acr
Acr, Monp
Aga
Scl
Por
Tur
Por ma.
Poc
Poc
Acr, Monp,
Poc, Ser
Gal, Monp,
Acr
Gal, Monp,
Acr
Acr, Monp
Plat
Scl
Poc
Scl
Scl
Acr
Acr
Poc
Poc, Acr
U
U
U
O
U
O
O
O
U
U
O
O
O
U
U
O
U
U
U
F
F
F
F
F
F
F
F
F
F
U
U
F
Boucher 1986
O
F
U
O
O
O
U
U
O
O
F
F
F
F
F
F
U
U
F
F
Drupella fragum
Drupella minuta
Drupella rugosa
Ergalatax margariticola
Habromorula spinosa
Latiaxis hindsii
Magilus antiquus
Magilus lamarkii
Morula sp. A
Morula sp. B
Muricopsis zeteki
Quoyula madreporarum
Type Use
Reference
continued
99
Higher Taxa
Family:
Phasianellidae
Family: Strombidae
Family: Triviidae
Species
Coral taxa
Quoyula monodonta
Rapa incurvus
Phasianella sp. A
O
U
U
F
F
U
Robertson 1970
Oliverio 2009
Stella et al. 2010
Strombus mutabilis
Strombus sp. A
Strombus sp. B
Strombus sp. C
Trivia merces
Trivia oryza
Ser
Poc, Ser
Acr
Acr
Poc
Poc, Ser, Acr
U
U
U
U
U
U
U
U
U
U
U
U
Poc
Poc
Poc
Poc
Poc
Poc
Poc
Poc
Ser
Poc, Acr
Acr
Acr
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
Phestilla melanobranchia
Phestilla sibogae
Phestilla lugubris
Phestilla minor
Den, Tub
Por, Gon, Tub
Por, Gon, Tub
Por, Gon, Tub
O
O
O
O
F
F
F
F
Harris 1975
Harris 1975
Rudman 1981
Rudman 1981
Cryptoplax sp.
Coscinasterias calamaria
Poc
Acanthaster planci
F
F
F
F
Thomassin 1976
Thomassin 1976
Order: Vetigastropoda
Family:
Scutus antipodes
Fissurellidae
Family: Haliotidae
Haliotis varia
Family: Trochidae
Clanculus denticulatus
Clanculus personatus
Clanculus plebejus
Herpetopoma aspersa
Family: Turbinidae
Australium tentorium
Turbo argyrostomus
Turbo brunneus
Turbo sp. A
Turbo sp. B
Turbo sp. C
Type Use
Reference
Class: Nudibranchia
Order: Aeolidina
Family:
Tergipedidae
Class: Polyplacophora
Order: Chitonida
Family:
Cryptoplacidae
Phylum Echinodermata
Class: Asteroidea
Order: Forcipulatida
Family: Asteriidae
Order: Spinulosida
Family:
Acanthasteridae
Family:
Echinasteridae
Echinaster luzonicus
Echinaster purpureus
100
CORAL-ASSOCIATED INVERTEBRATES
Higher Taxa
Order: Valvatida
Family: Asterinidae
Family:
Ophidiasteridae
Family:
Oreasteridae
Species
Coral taxa
Type Use
Reference
Asterina anomala
Asterina atyphoida
Asterina sp.
Linckia laevigata
Nardoa variolata
Pharia pyramidata
Culcita novaeguineae
Culcita schmideliana
Nidorellia armata
Pentaceraster cumingi
Acr
Poc
Acr
Por ma.
Por ma.
Poc
Poc
Gal, Gon
Pav
Psa
F
U
F
F
F
F
F
F
F
F
F
U
F
F
F
F
F
F
F
F
Yamaguchi 1975
Black & Prince 1983
Yamaguchi 1975
Thomassin 1976
Thomassin 1976
Dana & Wolfson 1970
Glynn & Krupps 1986
Thomassin 1976
Glynn et al. 1983
Glynn 2004
Eucidaris metularia
Eucidaris thouarsii
Ser
Pav, Poc
U
F
U
S
Colobocentrotus atratus
Echinometra lucunter
Echinometra mathaei
Echinometra viridis
Ser, Acr
Scl
Scl
Scl
U
F
F
F
U
S
S
S
F
F
S
S
Herring 1972
Glynn 1988
Diadema mexicanum
Diadema savignyi
Diadema setosum
Echinothrix calamaris
Echinothrix diadema
Scl
Acr, Aga, Mad,
Mont, Por
Scl
Scl
Scl
Scl
Scl
F
F
F
F
F
S
S
S
S
S
Glynn 1988
Bak 1990
Herring 1972
Herring 1972
Bak 1990
Echinoneus cyclostomus
Scl
Herring 1972
Scl
Herring 1972
Poc
Scl
Scl
F
F
S
S
Herring 1972
Herring 1972
Class: Echinoidea
Order: Cidaroida
Family: Cidaridae
Order: Echinoida
Family:
Echinometridae
Order: Echinothuroida
Family:
Astropyga radiata
Diadematidae
Diadema antillarum
Order: Holectypoida
Family:
Echinoneidae
Order: Phymosomatoida
Family:
Stomopneustes variolaris
Stomopneustidae
Order: Temnopleuroida
Family:
Temnopleurus michaelseni
Temnopleuridae
Family:
Microcyphus rousseaui
Toxopneustidae
Tripneustes gratilla
continued
101
Higher Taxa
Species
Coral taxa
Type Use
Reference
Amphipholis squamata
Amphiura luetkeni
Ophiactis savignyi
Ophiactis sp. A
Clarkcoma canaliculata
Ophiocoma dentata
Ophiocoma erinaceus
Ophiocoma sp. A
Ophiocoma sp. B
Ophiocoma sp. C
Ophiocoma sp. D
Ophiocoma sp. E
Ophiocoma occidentalis
Ophiocomella sexradia
Macrophiothrix sp.
Ophiomastix sp.
Ophiothrix acestra
Ophiothrix sp. A
Ophiothrix sp. B
Poc
Poc
Poc
Acr
Poc
Poc
Poc, Ser, Acr
Poc, Ser, Acr
Poc, Ser, Acr
Poc, Ser
Ser, Acr
Poc
Poc
Poc
Ser, Acr
Poc, Ser
Poc
Poc, Ser, Acr
Poc, Ser, Acr
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
U
Chloeia flava
Chloeia fusca
Eurythoe complanata
Hermodice carunculata
Notopygos crinita
Scl
Scl
Mont
Por
Mont
F
F
F
F
F
U
U
U
F
U
Pseudovermilia madracicola
Spirobranchus corniculatus
Poc
Por ma., Por
br., Acr, Aga,
Poc, Mont
Por ma., Pav
Por ma.
Por ma.
Por ma.
Por ma.
Por ma.
Por ma.
O
O
U
H
O
U
O
U
O
U
O
H
H
H
H
H
H
H
Class: Ophiuroidea
Order: Ophiurida
Family:
Amphiuridae
Family:
Ophiactidae
Family:
Ophiocomidae
Family:
Ophiotrichidae
Phylum Annelida
Class: Polychaeta
Order: Amphinomida
Family:
Amphinomidae
Order: Canalipalpata
Family: Serpulidae
Spirobranchus gardineri
Spirobranchus gaymardi
Spirobranchus giganteus
Spirobranchus incrassatus
Spirobranchus nigranucha
Spirobranchus paumotanus
Spirobranchus polycerus
102
CORAL-ASSOCIATED INVERTEBRATES
Higher Taxa
Order: Eunicida
Family: Eunicidae
Family:
Lumbrineridae
Family: Oenonidae
Order: Phyllodocida
Family:
Aphroditidae
Family: Polynoidae
Order: Spionida
Family:
Chaetopteridae
Family: Spionidae
Species
Coral taxa
Type Use
Reference
Spirobranchus spinosus
Spirobranchus tetraceros
Por ma.
Por ma. Pav
U
O
H
H
Eunice floridana
Eunice mutilata
Eunice pennata
Eunice schemacephala
Lumbrineris flabellicola
Ocu
Mont
Mad
Mont
Den, Cary, Fla
F
F
F
F
O
U
H
U
H
U
Britayev 1981
Ebbs 1966
Fauchald 1992
Ebbs 1966
Zibrowius et al. 1975
Oenone fulgida
Mont
Ebbs 1966
Pontogenia sericoma
Mont
Ebbs 1966
Harmothoe aculeata
Hermenia verruculosa
Hololepidella nigropunctata
Lepidonotus variabilis
Mont
Mont
Fung
Mont
F
F
O
F
U
U
U
U
Ebbs 1966
Ebbs 1966
Pettibone 1993
Ebbs 1966
Spiochaetopterus sp.
Monp
Bergsma 2009
Dipolydora armata
Lep
Okuda 1937
Cliona laticavicola
Cliona mucronata
Cliona pocillopora
Acr
Poc
Poc
O
O
O
S
S
S
Pang 1973
Bautista-Guerrero et al. 2006
Bautista-Guerrero et al. 2006
Callyspongia californica
Haliclona caerulea
Chalinula nematifera
Amphimedon texotli
Aka cryptica
Poc
Poc
Poc
Poc
Poc
F
F
O
F
U
S
S
S
S
S
Poc
Mont, Aga, Por
ma., Mus
Poc
F
F
S
S
Phylum Porifera
Class: Demospongiae
Order: Hadromerida
Family: Clionaidae
Order: Haplosclerida
Family:
Callyspongiidae
Family: Chalinidae
Family: Niphatidae
Family:
Phloeodictyidae
Order: Poecilosclerida
Family: Mycalidae
Mycale cecilia
Mycale laevis
Mycale magnirhaphidifera
continued
103
Higher Taxa
Species
Coral taxa
Type Use
Reference
Phylum Platyhelminthes
Class: Turbellaria
Order: Acoela
Family:
Convolutidae
Family:
Sagittiferidae
Order: Polycladida
Family:
Prosthiostomidae
Waminoa brickneri
Waminoa litus
Convolutriloba hastifera
Convolutriloba longifissura
Convolutriloba macropyga
Convolutriloba retrogemma
Haplodiscus sp.
Notoplana tremellaris
Fav
Por ma
Goni, Plat, Ple
Ple
Scl
Ple
Por
Ple
U
U
U
U
U
U
U
U
F
F
F
F
F
F
F
F
Prosthiostomum sp.
Monp
Por ma.
Cary, Den
U
F
H
H
Loph
Phylum Sipuncula
Class: Phascolosomatidea
Order: Aspidosiphonida
Family:
Aspidosiphon elegans
Aspidosiphonidae
Aspidosiphon muelleri
Phylum Hemichordata
Class: Pterobranchia
Order: Rhabdopleuroidea
Family:
Rhabdopleura normani
Rhabdopleuridae
Key to abbreviations
Type:O = Obligate symbiont, F = Facultative symbiont, U = Unknown.
Use: F = Food, H = Habitat, S = Substratum, U = Unknown
Coral taxa: Acan = Acanthastraea, Acr = Acropora, Aga = Agariciidae, Anac = Anacropora, Ast = Astreopora, Cary =
Caryophyllidae, Cyph = Cyphastrea, Den = Dendrophyllidae, Dip = Diplora, Ech = Echinopora, Eup = Euphyllia,
Fav = Favia + Favites, Fla = Flabellidae, Fung = Fungiidae, Gal = Galaxea, Gon = Goniopora, Goni = Goniastrea,
Hydn = Hydnophora, Lep = Leptastrea, Lob = Lobophyllia, Loph = Lophelia, Mad = Madracis, Mea = Meandrina,
Mer = Merulina, Monp = Montipora, Mont = Montastrea, Mus = Mussidae, Ocu = Oculina, Pach = Pachyseris, Pav =
Pavona, Pec = Pectiniidae, Pla t = Platygyra, Pler = Plerogyra, Ple = Plesiastrea, Psa = Psammocora, Por = Porites
(ma, massive, br, branching), Poc = Pocillopora, Rhi = Rhizangiidae, Ser = Seriatopora, Sid = Siderastrea, Ste =
Stephanocoenia, Sty = Stylophora, Scl = Unknown scleractinian coral, Tham = Thamnastrea, Tub = Tubastrea,
Tur = Turbinaria
104