The coral-killing red sponge Clathria (Microciona) aceratoobtusa (Porifera: Demosponigiae) invades various coral communities of Gulf of Mannar Marine National Park, southeast India

Abstract

Accounts of the encrusting, coral-killing sponges are increasing at an alarming rate. The present paper details about a thinly encrusting red sponge Clathria (Microciona) aceratoobtusa (Carter, 1887) which is invasive or locally spreading species and create deleterious outbreaks on Gulf of Mannar coral reefs. Earlier it has also been recorded from Yemen, but not taxonomically identified. This sponge is regarded as an aggressive space-competitor locally overgrowing and killing corals, mostly belonging to the coral genera such as Porites, Acropora, Montipora, Favia and Turbinaria. We observed that Turbinaria colonies were the substrate more preferred by the sponge than other coral colonies in the entire study site. The present observation analyses detail the taxonomical and ecological data of Clathria (M.) aceratoobtusa with a comprehensive review of its ecological preference.

Keywords:

• Sponge overgrowth
• coral mortality
• Porifera
• coral reefs
• Vilanguchalli Island

Introduction

The boundless competition for space, and cooperation processes, exhibited by reef communities favour physical and biological structuring and functioning of reef ecosystems (Wang et al. 2012). Sponges are one among the major actors of coral reef communities (Benayahu & Loya 1981; Acker & Risk 1985) and are considered as the main habitat-forming organisms (Chornesky 1989; Rützler 2002). There are various interactions happening between the sponges and the corals; the outcome of these interactions potentially may lead to large-scale destruction of coral reef communities (González-Rivero et al. 2011). The density and bottom cover of coral excavating sponges are proven similar to or higher than hard corals (Zea 1993); excavating sponges play a key role in balancing reef growth and erosion (Wilkinson 1983; Glynn 1997) and if their action intensifies and speeds up, overcoming reef growth, they may destroy the reef framework (Hutchings 1986; Schönberg et al. 2017). Sponges also intensely interact with scleractinian corals, competing for the substrate; they may overgrow and smother corals, often producing allelopathic molecules able to kill coral tissues (Coles & Bolick 2007; Pawlik et al. 2007; Benzoni et al. 2008; de Voogd et al. 2013).

Temperature increase (Rose & Risk 1985; Holmes 1997; Holmes et al. 2000; Rützler 2002), coral tissue die-off, coral disease and bleaching (Cortés et al. 1984; Glynn 1997; Williams et al. 1999; Rützler 2002; Schönberg et al. 2017), aggravated by climate change, may strongly affect sponge/coral interaction promoting the shift of some coral reefs towards sponge dominated reefs (Bell et al. 2013).

Though coral reefs have been widely studied around the words, the interaction between corals and sponges is not well understood (Peyrot-Clausade et al. 1995; Carreiro-Silva & McClanahan 2001; Zahir et al. 2002; Ashok et al. 2019). There are several reports on the sponges of the family Clionaidae (Marulanda-Gómez et al. 2017; Ashok et al. 2018), Suberitidae (Rützler 1971; Raj et al. 2018; Fromont et al. 2019), Chalinidae (Rossi et al. 2015) and Poeciloscleridae (Coles & Bolick 2007; Benzoni et al. 2008) (Table I) which can excavate or smother corals. Poecilosclerida is the largest order in the phylum Porifera with vast diversity (Bergquist & Formont 1988; Hajdu et al. 1994). They are variedly studied for the possession of various secondary metabolites (Melawaty & Pasau 2015) but their ecological aspects have not drawn enough attention in the Indian Ocean. To date, 26 Poecilosclerids have been described and documented from the Indian Ocean (Pattanayak 1999). Many of the reported species from the Indian Ocean are currently subjected to taxonomic revisions on account of a poor description, lack of stock specimens or want of confirmation for some of the identifications (Schönberg et al. 2017).

Table I. Sponge species able to overgrowth on hard coral species with visible negative effects; the geographic area refers to the area where interaction activity was observed; also excavating species are considered when they couple an erosion activity with a lateral growth

Sponge species	Geographical area	References
Agelas clathrodes (Schmidt, 1870)	Caribbean (Colombia)	Aerts & van Soest 1997
Agelas conifera (Schmidt, 1870)	Caribbean (Colombia)	Aerts & van Soest 1997
Aplysina cauliformis (Carter, 1882)	Caribbean (Colombia)	Aerts & van Soest 1997
Aplysina fistularis (Pallas, 1766)	Caribbean (Colombia)	Aerts & van Soest 1997
Callyspongia (Cladochalina) armigera (Duchassaing & Michelotti, 1864)	Caribbean (Colombia)	Aerts & van Soest 1997
Chalinula nematifera (De Laubenfels, 1954)	Marshall Islands, Tropical Eastern Pacific, tropical Indo-Pacific region, Indonesia,	De Laubenfels 1954; Ávila & Carballo 2009; Rossi et al. 2015
Cliona albimarginata Calcinai, Bavestrello & Cerrano, 2005	Indonesia	Calcinai pers. obs.
Cliona aprica Pang, 1973	Caribbean	López-Victoria & Zea 2004
Cliona caribbaea Carter, 1882	Caribbean	Rützler 2002; López-Victoria & Zea 2004
Cliona delitrix Pang, 1973	Caribbean	Rützler 2002; López-Victoria et al. 2006
Cliona tenuis Zea & Weil, 2003	Caribbean	Márquez et al. 2006
Cliona orientalis Thiele, 1900	Australia, Pacifc	Schönberg & Wilkinson 2001; Schönberg 2003
Cliona varians (Duchassaing & Michelotti, 1864)	Caribbean	Rützler 2002
Clathria (Microciona) sp.	Yemen, Maldives, Gulf of Mannar	Benzoni et al. 2008; present paper
Clathria (Thalysias) venosa (Alcolado, 1984)	Caribbean (Colombia)	Aerts & van Soest 1997
Desmapsamma anchorata (Carter, 1882)	Caribbean (Colombia)	Aerts & van Soest 1997
Dysidea etheria Laubenfels, 1936	Caribbean (Colombia)	Aerts & van Soest 1997
Ircinia felix (Duchassaing & Michelotti, 1864)	Caribbean (Colombia)	Aerts & van Soest 1997
Ircinia strobilina (Lamarck, 1816)	Caribbean (Colombia)	Aerts & van Soest 1997
Mycale (Mycale) grandis Gray, 1867	Hawaii	Coles & Bolick 2007
Mycale (Mycale) laevis (Carter, 1882)	Caribbean (Colombia)	Aerts & van Soest 1997
Niphates erecta Duchassaing & Michelotti, 1864	Caribbean (Colombia)	Aerts & van Soest 1997
Pione lampa (de Laubenfels, 1950)	Caribbean	Aerts & van Soest 1997; Rützler 2002
Scopalina ruetzleri (Wiedenmayer, 1977)	Caribbean (Colombia)	Aerts & van Soest 1997
Siphonodictyon coralliphagum Rützler, 1971	Caribbean	Sullivan & Faulkner 1985
Terpios hoshinota (Rützler & Muzik, 1993)	Guam, Gulf of Mannar Palk Bay, Indonesia, Central Pacific, Japan, China, Australia	Plucer-Rosario 1987; Rützler & Muzik 1993; Reimer et al. 2011; Shi et al. 2012; de Voogd et al. 2013; Montano et al. 2015; Thinesh et al. 2015; Raj et al. 2018; Yang et al. 2018; Ashok et al. 2019; Fromont et al. 2019

Corals (Pillai 1972, 1977, 1986, 1994) and sponges (Thomas 1968a, 1968b, 1968c, 1968d, 1968e, 1969, 1972, 1979, 1985, 1989) have been well documented in the Indian reefs although the interaction between them has not been given importance. The Gulf of Mannar (GoM) is one of the major reef regions of India with a significant amount of corals (Edward et al. 2007, 2012, 2018). The dearth of correctly identified sponges with colour images and lack of regional taxonomists makes sponges of the Gulf of Mannar as enigmatic creatures to the recent researchers. The recognition of the importance of sponges in these reef ecosystems reflects sponges are not anymore that neglected species (CARICOMP 1997).

Recently the encrusting sponge Clathria (Microciona) aceratoobtusa (Carter 1887), showy for its brilliant orange-red colour, has become abundant on the reefs of the Gulf of Mannar, and turned out to be really detrimental to various species of live corals. In the present paper, we dealt with taxonomical and ecological data of Clathria (M.) aceratoobtusa with a detailed review of its ecological preference. The data may assist in future monitoring efforts of the GoM reefs, considering the negative, long-term consequence of the proliferation of this species on dynamics and community structure of the reefs.

Materials and methods

The Gulf of Mannar in southeast India is known for its coral reefs and associated biodiversity. There are 21 uninhabited coral islands in the Gulf of Mannar that come under the Gulf of Mannar Marine National Park (GoMMNP). The National Park area is a “no go” and “no take” zone. Tuticorin region of the Gulf of Mannar encompasses four islands, namely, Vaan, Koswari, Kariyachalli and Vilanguchalli (Edward et al. 2012). Vilanguchalli Island (Figure 1) is a submerged Island that occurs 6 km from the mainland. Submergence of this Island has been reported to be caused by decades of rampant coral mining coupled with sea-level rise (Raj et al. 2015). Parts of this Island expose during low tides. Reef type in this Island is fringing that occurs at depths between 0.5 and 5.4 m and the dominant coral genera are Acropora, Montipora, Porites and Turbinaria (Edward et al. 2007). Climate-driven coral mortality has caused serious damage to the reefs of the Gulf of Mannar including Vilanguchalli Island (Edward et al. 2018).

Figure 1. Map of the study site at the Vilanguchalli Island, Gulf of Mannar, southern coast of India

After noticing the unusual occurrence of a red patch on various coral colonies, an underwater assessment was carried out involving scuba diving. The sponge incrustations were first misinterpreted as coral disease and further analysis confirmed the sponge identity. To estimate the ecological context of the sponge colonies, ten 20 × 2 m belt transects were haphazardly laid on island reef, parallel to the shore and to each other, separated by a distance of 5 m, resulting in an area of 400 m². The depth ranged between 2 and 4.5 m along all transects. Data were collected on the total number of coral colonies, listed by genus, and the number of corals invaded by the sponge within the belt transects. Small volumes of sponge-infested colonies were collected for the identification of the sponge species. The samples were immediately stored in 80% ethanol, and subsequent laboratory analyses, for spicule preparations, were made following Rützler (1974). Spicule range was evaluated by measuring 15 spicules per type. Size is given as maximal (average sizes ± standard error) minimal, for length and width. For SEM analyses, carried out with a Philips XL 20, dissociated spicules, and coral fragments covered by sponge, were transferred onto stubs, sputtered with gold and observed.

Chi-square test was done to compare the observed proportions of infestation of C. (M.) aceratoobtusa, towards several genera of corals, to expected ones, predicted by the coral proportion observed in the transects.

Results

In Vilanguchalli patch reef we observed the occurrence of an orange-reddish, encrusting sponge overgrowing on live tissues of massive and branching corals of several genera (Figure 2); it extended as a thin red sheet over the corals, leaving a red stain throughout its proliferation. A thin, white band was visible near the coral and sponge boundary (Figure 2(a,d)).

Figure 2. Clathria (Microciona) aceratoobtusa at Vilanguchalli Island, Gulf of Mannar. (a) A prominent and profound dermal canal pattern was radiating all over the body upon close observation underwater; (b) Sponge infestation on live tissues of Acropora muricata; (c) Infestation on Favia sp.; (d) The sponge penetrates in a downward direction, inside the coral; (e) Intact corallites, smothered by the sponge cover, still detectable. Scale bars: a, b, c = 2 cm; d, e = 1 cm

The morphological study led to identify it as Clathria (Microciona) aceratoobtusa (Carter 1887). The sponge was characterized by a rough surface and tough consistency. Samples turned pale upon alcohol preservation. The oscules were contractile and poorly visible and distributed. A prominent and profound dermal canal pattern was radiating all over the body upon close observation underwater (Figure 2(a,e)). Intact corallites, smothered by the sponge cover, were still detectable (Figure 2(a,d,e)). The sponge could not be separated with moderate ease from the underlying substrate, because it penetrates in a downward direction, inside the corals (Figure 2(d)).

Skeleton by SEM appears typical of Clathria (Microciona), i.e. hymedesmoid-like (Figure3(a,b)). Macroscleres consist of principal long, and thick subtylostyles (Figure 3(c)) with smooth tylo (Figure 3(d)); very few have micro-spiny tylo; thinner, smooth (Figure 3(e)) or microspined styles/subtylostyles (Figure 3(f)); smooth echinating styles (Figure 3(g,h)), some microspined; microscleres are palmate isochelae and toxas (Figure 3(i,j)). The abundantly distributed toxas were small and delicate and also oxhorn toxas (Figure 3(i)). Chelae often displayed contort shafts (Figure 3(c,f,i,j)). Measurements of the spicules in Table II.

Table II. Spicule dimensions of Clathria (Microciona) aceratoobtusa from Vilanguchalli Island Tuticorin group, Gulf of Mannar Marine National Park, and from Yemen (N = 15 Min. – minimum, max. – maximum, S.E. – standard error)

	Long tylostyles	Echinating styles	Thinner styles	Chelae	Toxas
Present material	268-(320 ± 1.2)-294 × 5 µm	146-(175 ± 1.5)-160.5 × 4 µm	143-(234 ± 1)-188.5 × 1.8 µm	9.2-(9.9 ± 1.2)- 10.8 µm	30.5-(47.25 ± 1)-64 µm
Benzoni et al. 2008	97.5-(160.4 ± 14.6)-308.6 × 5 µm	42.5-(57.4 ± 11)-87.5 × 2.5-(3 ± 0.8)-3.7 µm	137.5-(172.2 ± 40)-242.5 × 2 µm	9-(9.5 ± 3)-10.6 µm	20-(48 ± 10.5)-75 µm

Figure 3. Clathria (Microciona) aceratoobtusa. (a, b) Typical hymedesmoid-like skeleton by SEM; (c) Principal long, and thick subtylostyle; (d) Smooth tylo of the thick subtylostyle; (e) Smooth tylo of the thin subtylostyle; (f) Thin auxiliary subtylostyle; (g) Smooth echinating style; (h) Smooth tylo of the echinating style; (i) Oxhorn toxa and palmate isochelae; (j) Palmate isochelae

In the surveyed area, numerous coral genera are present: the most common genus, in healthy state, is Acropora with 0.64 ± 0.35 colonies/m², followed by Turbinaria (0.22 ± 0.13 colonies/m²) and by Favia (0.07 ± 0.04 colonies/m²). Many other genera e. g Acanthastrea, Pavonia or Cyphastrea are very rare, with few, scattered colonies only (respectively, 2, 3 and 7 colonies in all the examined transects). Turbinaria colonies were the substrate more preferred by the sponge than other coral colonies in the entire study site (χ² = 29.911, df = 4, p-value = 5.1 10⁻⁶). Sponge prevalence followed in the order Turbinaria (29.6%, n = 37) > Porites (21.43%, n = 6) > Favia (12.5%, n = 4) > Acropora (11.07%, n = 32) > Montipora (9.73%, n = 18), that was the least preferred substrate by the sponge (Figure 4).

Figure 4. Prevalence of Clathria (Microciona) aceratoobtusa invasion on coral colonies

Discussion

Clathria (M.) aceratoobtusa was recorded by Carter (1887) from Mergui Archipelago and later it has been variedly reported by Hentschel (1911) from Shark Bay, by Thomas (1985) from the Gulf of Mannar, and by Hooper (1996) from Thailand and Indonesia. The sponge from Mannar fits with the species C. (M.) aceratoobtusa in its general appearance, colour, and spicule size and shape. In particular, virtually smooth spicules, as well as the oxhorn toxas and contort chelae, characterize C. (M.) aceratoobtusa (Hooper et al. 2000). Our specimens are very close to those described by Thomas (1985) and Hentschel (1911), and slightly different in respect with the neotype, illustrated by Hooper (1996), characterized by macroscleres with, in general, prominent swollen heads. Anyway, Hooper (1996) pointed out how the neotype slightly differed from the sponges described by Carter and Hentschel, suggesting a certain morphological variability in spicule features and size.C. (M.) aceratoobtusa was described as thinly encrusting on bivalves, rock, coral substrate, shell detritus or worm tubes (Carter 1887; Hentschel 1911; Hooper 1996); in 2008, Benzoni et al. reported in South Yemen a very thin encrusting Clathria (Microciona); the sponge was not determined at species level and was described as an orange-reddish band “disease” able to grow over the coral at a rate of about 1 cm/month. It was observed spreading over about 50% of the Porites lutea colonies, killing the coral. Later the same sponge was recorded also in the Maldives (Benzoni & Calcinai pers. obs.). The comparison of the old material with this new one, from Mannar, revealed that they are the same species, identified as C. (M.) aceratoobtusa. The mechanism of sponge–coral interaction appears the same described by Benzoni et al. (2008) (Figure 1(a,b)). The sponge covers corals by peripheral contact (Aerts & van Soest 1997), and the thin, dead and white line of coral along the boundary can be explained by chemical interaction as suggested for similar cases (Porter & Targett 1988; Rossi et al. 2015). Moreover, C. (M.) aceratoobtusa seems able to cover also living portions of coral (see Figure 2(c)).

Turbinaria was the coral genus more covered by the sponge, but it was not the only; in 2008, on the contrary, Benzoni et al. found C. (M.) aceratoobtusa to be highly selective for Porites lutea in Yemen; in Mannar, the plate-like life form of this coral might have favoured the sponge overgrowth over it, even if a clear specificity is not demonstrable, considering that infected and not infected colonies may have the same pattern of growth (Table III) and C. (M.) aceratoobtusa in Yemen covered massive colonies of Porites lutea.

Table III. Clathria (Microciona) aceratoobtusa infestations on various coral growth forms from Vilanguchalli Island Tuticorin group, Gulf of Mannar Marine National Park

Coral	Growth form	Total	Infected
Acropora	ACB	289	32
Montipora	ACB, ACE	185	18
Favia	CE	32	4
Favites	CE	27	0
Goniastrea	CM, CS	18	0
Porites	CM	28	6
Platygyra	CM, CE	19	0
Symphyllia	CM, CS	17	0
Turbinaria	CF	125	37
Hydnophora	CM	12	0
Pavona	CE	3	0
Acanthastrea	CM	2	0
Plesiastrea	CM	9	0
Leptoria	CS, CM	7	0
Goniopora	CS	8	0
Pocillopora	CB	22	0
Leptastrea	CM, CS	6	0
Cyphastrea	CS	7	0

ACB = Acropora branching; ACE = Acropora encrusting; CE = coral encrusting; CM = coral massive; CS = coral submassive; CF = coral foliose.

In the recent period, records about sponges threating coral reefs are numerous (Table I). Since 1973 when Bryan has documented Terpios hoshinota (as Terpios sp.) in Guam, other sponge species were observed competing with corals and killing them (Coles & Bolick 2007; Benzoni et al. 2008) and to spread out across Indo-Pacific Ocean, enlarging their area of distribution (Ávila & Carballo 2009; Shi et al. 2012; de Voogd et al. 2013; Rossi et al. 2015); in particular, in the most recent period, there is an increasing number of records of T. hoshinota spreading throughout the Indo Pacific negatively affecting coral reefs (Ashok et al. 2018; Raj et al. 2018; Yang et al. 2018; Fromont et al. 2019).

As Elliot et al. (1995) put in evidence, the causes of these sponge outbreaks are not clear. In some cases, it may be due to human-induced factors (Ávila & Carballo 2009) or due to detrimental environmental conditions; for example, high levels of nutrient pollution have been considered the main cause of rapid and catastrophic outbreaks of the sponge T. hoshinota, (Plucer-Rosario 1987; Rützler & Muzik 1993), and also sponge dispersal possibility supported by local currents may play a crucial role (Shi et al. 2012). Further studies are needed to elucidate the environmental factors affecting and promoting Clathria (M.) aceratoobtusa’s spread in the Gulf of Mannar. It is known that coral bleaching, driven by climate change, has become more common in the past few decades causing widespread coral mortality (Wake 2016; Hughes et al. 2018); sponges take advantage of the compromised health of corals due to environmental parameters (Rose & Risk 1985; Holmes 1997; Holmes et al. 2000; Rützler 2002; Carballo 2009). Corals in the Gulf of Mannar were affected significantly by coral bleaching in 2016 and are under significant stress (Edward et al. 2018). Hence, we may interpret the widespread occurrence of overgrowth of the coral excavating sponges as a consequence of the most recent bleaching event occurring in the Gulf of Mannar as evident from recent studies (Ashok et al. 2018; Edward et al. 2018; Raj et al. 2018). Sponges have been reported to be comparatively more capable of thriving in changing climatic conditions and have better regeneration capacity (Miller et al. 2010; Runzel 2016). This alarming increase of Clathria (M.) aceratoobtusa in the Gulf of Mannar deserves to be monitored, and further researches are needed to evaluate the rate and the proportion of this sponge spreading; this sponge could represent another threat to this already damaged reef, causing massive coral mortality and sponge-coral phase shift (Rützler 1970; Suchanek & Green 1981).

Conclusion

The present study provides a first account on the widespread occurrence of a coral-killing sponge in Vilanguchalli Island, Tuticorin region in Gulf of Mannar. Though climate crisis has been portrayed as a key influencer for this sponge outbreak, other important factors such as pollution and nutrient enrichment cannot be ruled out. Tuticorin is an urban area with a huge population and the domestic waste generated every day is directly routed to the sea without any treatment. This condition further upsets the ecosystem balance in favour of the sponges where they outcompete the corals and damage the reefs for long term (González-Rivero et al. 2011). The recently observed coral mortality due to several factors is expected to further enhance the abundances of these sponges in the near future. Coral reefs of Gulf of Mannar act as a hub for reef dependant fishery and provide livelihood to thousands of local fishermen directly.

The coral-killing sponge, Terpios hoshinota has been reported to die after the death of covered coral colonies and if no other live coral substrate is available (see Elliott et al. 2015). In Yemen, Benzoni et al. (2008) noted that C. (M.) aceratoobtusa grows progressively over the coral, but it faded, leaving the dead coral behind. Hence, further focused studies are needed to ascertain the exact interaction between the reported sponge and its host corals. Considering the global concern for declining reef quality, the sponge assemblages on various coral communities of the ecologically sensitive coral reef system such as GoM should be regularly monitored to determine the potential of sponges to become more abundant in response to changing environmental conditions. The present study also aims to draw the attention of the reef managers to the need for focusing more research on the coral threating sponges.

Availability of data and materials

All data generated or analysed during this study are included in this published article.

Consent for publication

Being the corresponding author to this manuscript, I state that all authors agree to its submission and the Corresponding author has been authorized by the co-authors.

Ethics approval consent to participate

This article does not contain any studies with animals performed by any of the authors.

Acknowledgements

Thanks to Ministry of Environment, Forest and Climate Change, Government of India for funding support. Thanks also to Chief Wildlife Warden, Government of Tamil Nadu, India and Wildlife Warden, Gulf of Mannar Marine National Park, for research permissions (Ref.No. WL(A)/11867/2017- Permit No. 43/2017).

Disclosure statement

No potential conflict of interest was reported by the authors.