Occurrence of opportunistic invasive macroalgal genus Caulerpa and Halimeda opuntia in coral reefs of Gulf of Mannar

: Investigations on indigenous and non-indigenous invasive flora and fauna of a certain geographical area are always important to assess their impact on native biodiversity and control their spread by making conservation strategies to protect biodiversity. In this study, we have encountered overwhelming growth of six seaweed species, Caulerpa racemosa , C . serrulata , C . sertularioides , C . taxifolia , C . peltata


MATERIAL AND METHODS
Reef monitoring surveys were carried out during August to November 2018, from Manoli Putti and Hare Islands under the Gulf of Mannar region, southeastern coast of Tamil Nadu, India. Several underwater dives on fringing reefs of these two islands revealed moderate bloom forming and overwhelming growth of four green seaweeds Caulerpa serrulata, C. racemosa, C. sertularioides, and C. peltata on live and dead corals. Underwater photographs of these bloom-forming species were documented using Nikon Coolpix underwater camera. Species identification was made using standard identification keys and AlgaeBase (Guiry & Guiry 2018).

RESULTS AND DISCUSSION
Caulerpa racemosa, C. serrulata, C. sertularioides, C. taxifolia, C. peltata, and Halimeda opuntia are usually seen in smaller size on corals and rubbles. Their usual occurrence on reefs or rubbles used to be within the size range <5->30 cm. However, their bloom forming nature identified by recording their overwhelming spread on corals ranged >30 cm->1 m. Blooms of these species overwhelming on the coral reefs of Mandapam group of Islands were recorded during our study (Image 1a-h; Image 2a-f). The favourable physicochemical conditions that promote their spread in the reef area are poorly understood. These algal species have displayed a distinct distribution in the reef environment, where C. sertularioides and C. racemosa grew on rubbles, rocky substratum, and Porites sp.; C. serrulata on dead Acropora corals and live Porites species; and C. peltata on live Acropora corals. C. taxifolia has formed small patches on rubbles and near reef slopes, and is also found to grow mostly on Montipora digitata and Porites solida rather than on Acropora. Interestingly, C. racemosa was observed to grow on multiple species of corals such as Porites, Acropora, and Montipora. C. racemosa, H. opuntia, and C. taxifolia grew together with no inhibition activity against each other. H. opuntia was found to cover a few massive Porites coral colonies in Manoliputti Island. While its spread in seagrass beds was also observed (Image 2a-f), its actual impact on seagrass beds is yet to be studied.
We did not observe any grazers that preferred to feed on these Caulerpa species. Although C. taxifolia was found in the reef flats but were not seen to occur profusely. These algal blooms appear to be unsuitable for the development of corals due to their proliferation, smothering the corals. Also, overwhelming algal growth inhibits light penetration required for zooxanthellae to generate energy for polyps. These reasons appear to inhibit the growth of coral polyps and restrict juvenile corals' settlement on the dead reefs or rubble in the Gulf of Mannar reefs.

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Previous reports indicated that C. racemosa and C. taxifolia could inhabit the entire reef area, which would ultimately undermine the resilience of corals (Hoey et al. 2011). The impact of these Caulerpa species on Gulf of Mannar's reef environment is yet to be studied in detail. However, the present study observations are

Image 2. a-Caulerpa taxifolia invasion on M. digitata | b-around a newly recruited P. solida | c-C. racemosa invading on M. digitata | d-its interaction with Halimeda opuntia and C. sertularioides (top left) | e-profuse growth of H. opuntia on P. luteus | f-its propagation in seagrass bed. © Ramesh Ch.
challenging the issues related to the algal destruction and conservation of corals and coral reef biodiversity from invasive algae.
A recent study revealed that a feeding deterrent activity assay on green algae C. peltata, C. sertularioides, and C. taxifolia species display highest deterrent J TT activity of >80% (Rajan & Padmakumar 2017). While C. cupressoides and C. fergusonii showed moderate deterrent activity, C. scalpelliformis and C. microphysa exhibited negligible deterrent activity (Rajan & Padmakumar 2017). Experimental studies also show that grazing on C. taxifolia resulted in the loss of spines and less gonosomatic ratios in sea urchin Paracentrotus lividus (Boudouresque et al. 1996). Later it was observed that high production of toxic and repellent chemical metabolite 'caulerpenyne' in summer causes sea urchins to avoid C. taxifolia (Lemee et al. 1996). The deterrent activity exhibited by C. taxifolia might be the reason that restricts grazers not to feed on it.
Whereas the same compound produced by C. racemosa had not displayed any deterrent activity towards herbivorous surgeon fish Zebrasoma flavescens (Wylie & Paul 1988), and it was highly preferred by both juvenile and adult rabbitfish Siganus argenteus (Paul et al. 1990). In this study, we have not found any grazers feeding on these Caulerpa species during our underwater observations. A recent study also indicated that C. racemosa distribution could drastically change over time by spreading from deep water to the shallow waters, as observed in the Columbretes Islands, Mediterranean Sea (Kersting et al. 2014). A study also suggested that overgrowth of C. racemosa via chemotropism results in smothering or even death of sponge Sarcotragus spinosulus (Žuljevic et al. 2011).
Caulerpa species are well known as edible seaweeds in eastern Asian countries such as China, Japan, Korea, Philippines; southeastern Asian countries like Indonesia, Vietnam; and Indo-Pacific regions (Kaliaperumal & Chennubhotla 2017). In India, C. lentillifera is cultured on the Gulf of Mannar coast (Mary et al. 2009). But utilization of these six species in India has not been implemented so far. Hence, they remain an untapped and unutilized food resource from the Indian Coast. Thus, Caulerpa species can be considered a potential natural edible seafood to the increasing population in India.
Crustose coralline algae are well known as they support the settlement of coral polyps (Tebben et al. 2015). Although we have found very few coralline algae in our surveys at Hare Island and Manoli Island, the coral recruitment was appreciable on the dead corals free from these algae. However, there is high competition for substrata between algae and corals, similar to previous reports (McCook et al. 2001). Therefore, monitoring the bloom-forming invasive seaweeds in terms of their reproductive strategies and favourable conditions that promote their propagation is essential for developing remedies. Reports evidenced that ease dispersion and spread of Caulerpa species is mostly due to fishing nets, anchors, boats, and aquaria (Otero et al. 2013). Studies from the Mediterranean Sea have shown the rapid spread of invasive C. taxifolia by fragment mechanism (Ceccherelli & Cinelli 1999;Smith & Walters 1999). Therefore, further investigations are important to understand the temporal and spatial expansion of C. racemosa, C. serrulata, C. sertularioides, C. taxifolia, and C. peltata in these Islands. Also, multidisciplinary approaches are essential to address issues related to invasive species distribution dynamics, impacts, management, and utilization in the Gulf of Mannar. Also, the impact of environmental factors such as light, temperature, and water quality in different seasons should be analysed in future studies to understand bloom dynamics.

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