1 Introduction

Coral reefs in the global oceans are impacted by multiple stressors such as climate change, ocean acidification [1], global warming [2], bleaching events [3], coral diseases [4], sedimentation [5], algal invasion [6], coral-killing sponge infestation [7], coral-eating gastropods and echinoderms [8], coral mining [9], dredging [10], destructive fishing [11], anchoring activities [12], reef damaging diving/snorkeling activities [13], and several other anthropogenic activities [14, 15]. Depending on the type and intensity of natural or stressful conditions, corals are known to display varied colors, which indicate the healthy and distressed conditions of corals [16,17,18,19]. Among various known coral colors, pink pigmentation has been known for a long time due to its common appearance in healthy and diseased corals. A red fluorescent protein is known to be responsible for pink pigmentation under stress conditions [20]. Hazraty-Kari et al. reported the prevalence of pink spots on Porites from six islands of Persian Gulf and highlighted the research gaps in etiology of this disease [21]. Das et al. observed pink line syndrome on Acropora ocellata, Porites solida, and mushroom corals as well as trematodiasis/pink spots on P. solida from Atolls of Lakshadweep islands [22]. However, the fundamental mechanisms of pink pigmentation in massive corals under varied conditions are less understood from Indo-Pacific coral reefs.

The Gulf of Mannar Marine Biosphere Reserve (GoMMBR), India, is one of the biodiversity-rich hotspots in Southeast Asia. However, the biodiversity (traditional and molecular taxonomy) of vermitid gastropods [23, 24] and crustose coralline algae [25] from coral reefs of GoMMBR is least studied. Although vermitid gastropods and crustose coralline algae are prevalent in coral reefs of the GoMMBR, documentation of their interactions and impact on corals is very limited in Indian waters. Therefore, the present study investigated the interactions of Porites sp. with infesting agents from coral reefs of the GoMMBR, southeast coast of Tamil Nadu, India, to understand pink pigment response of Porites as a sign of stress and defense against vermitids and calcareous red algae settled coral surface interfaces.

2 Materials and methods

An extensive shallow reef monitoring was undertaken between August 2018 to August 2019 around the 21 Islands distributed along the GoMMBR, Southeast coast of Tamil Nadu, India (Fig. 1). The 21 islands distributed under four regions of GOMMBR are as follows: (I) Mandapam group: Shingle Island (1), Krusadai Island (2), Pullivasal Island (3), Poomarichan Island (4), Manoliputti Island (5), Manoli Island (6), and Hare Island (7); (II). Keezhakkarai group: Mulli Island (8), Valai Island (9), Thalaiyari Island (10), Appa Island (11), Poovarasanpatti Island (submerged island) (12), Vallimunai Island (13), and Anaipar Island (14); (III) Vembar group: Nallathanni Island (15), Puluvinichalli Island (16), and Upputhanni Island (17); (IV) Tuticorin group: Kariyachalli Island (18), Vilanguchalli Island (submerged island) (19), Koswari Island (20), and Vaan Island (21).

Fig. 1
figure 1

Map showing 21 islands distributed under the GoMMBR, Tamil Nadu, India

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Reef sites found around the 21 islands were surveyed during low tide at a depth range between 1 to 6 m. The coral video transect method [26], was conducted by snorkeling at each dive site for a maximum duration of one hour. Vermitids and calcareous red algae (infesting agents) spreading over massive coral colonies of Porites sp. were examined and recorded along the 20 m line transects by the visual census and photographic documentation. Underwater images of Porites colonies infected with vermitids, and rhodoliths were obtained using Nikon W300 Waterproof 30 m depth and 16.05 Megapixel Digital Camera. The percentage of Porites sp. colonies infected by infesting agents was calculated by: The number of Porites colonies infected by individual infesting agent/Total number of Porites colonies investigated × 100.

3 Results and discussion

Massive coral, Porites sp. producing pink pigmentation around vermitids were 12% (n = 49) of 517 colonies investigated. Investigations revealed that Porites sp. corallites initially produce conspicuous pink pigmentation around the vermetid snails as encapsulation (Fig. 2a–d). Then Porites sp. forms new corallites over encapsulated vermitids, thereby restricting the further spread of vermitids. These observations are consistent with earlier reports from Porites sp. [27] and other coral species [28]. Upon encapsulation of vermitids, pink pigmentation became pale and gradually disappeared (Fig. 2e). Vermitid gastropods were reported to alter the physical and chemical conditions at the coral-algal interaction interface and resulted in deleterious effects on both corals and algae [29]. Observations of this study suggest two possible assumptions that pink pigmentation may help Porites sp. to avoid: (1) inhibition of coral polyps by arresting the spread (space competition) of infesting agents, and (2) chemical damage by infesting agents that causes boring and enhances overwhelming growth over coral surface. However, our underwater evidences need to be confirmed through experimental studies to support these assumptions. While, it is unknown about the actual internal damage made by the vermitids by boring on Porites.

Fig. 2
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Pink pigment production by Porites sp. corallites. Note: pd = pigment deposition; op = operculum; ab-air bubbles; ms = mucus secretion from vermitids; rh = rhodoliths; pg = overgrowing vermetid gastropod Ceraesignum sp. on Porites; eh = empty hole of vermetid snail after mortality. a Commensalism between Porites and vermetid snail; b air bubbles released from operculum of vermetid snails; c pink pigment deposition around vermetid snail opening and mucus secretion (mucus net) from opening; d Porites sp. polyps depositing pink pigment over snails; e Porites sp. corallites encapsulating vermitid snails (right), and pigment deposition as ammensalism and defense against rhodolith Hydrolithon sp. (left)

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On the other hand, pink pigmentation was observed as a defensive strategy to limit the interaction and further spread of a nongeniculate calcareous red algae (family Hydrolithaceae), Hydrolithon sp. (5%; n = 21) (Fig. 2e). Pink pigment production at the interacting zone of rhodoliths with P. lutea was previously reported [20]. Unlike pink pigment encapsulation around vermitids, no evidences of encapsulation around rhodoliths were found during this study. But it was observed that rhodoliths were found to harbor and support the development of filamentous microalgae within the radius of rhodolith infested area. Colonies with both the infesting agents observed was 2% (n = 7). The remaining colonies (n = 440) were healthy (82%) without any vermitids and rhodoliths infestation. Pink pigment depositions by Porites corals were sighted more in Mandapam and Keelakarai regions than in other regions of the GoMMBR (Table 1). Das et al. observed the combined incidence of pink line syndrome and pink spots on Porites corals ranged from 5.5% to 23.4% in Lakshadweep archipelago [22]. Hazraty-Kari et al. reported seasonal variations in Porites pink spots (PPS) from Persian Gulf Islands, where PPS was high (4.96 ± 2.91%; n = 659) in the year 2014 and was observed low (0.62 ± 0.39%; n = 405) in the subsequent year 2015. Seasonal prevalence of on pink pigmentation on Porites colonies from GoMMBR further needs to be investigated for better understanding with respect to environmental factors.

Table 1 Pink pigment deposits observed on Porites corals from the GoMMBR during this study
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Pink pigmentation in the form of spots and lines on corals is often referred as diseases. In fact corals display pink pigmentation under various conditions and indicate various functions and signs: (1) helps in recovering the damaged part of coral fragments [28], (2) act as a defensive mechanism against algal growth, other corals and animals when they interact each other [30], or indicates (3) the newly growing tissue areas or recovering areas of injured coral fragments [28], (4) interaction stress, or an immune response to tolerate bleaching events [31], (5) pink line/pink spot disease [32, 33], (6) indicate invertebrate inflammatory response (e.g., trematodiasis-compromised tissues having pink pigmentation with red fluorescent protein) [33, 34], and (7) biological, environmental, mechanical or chemical disturbance [20, 27, 35]. In the present study, Porites sp. produced pink pigmentation as an antagonistic substance to arrest the spread of vermetid snails and rhodoliths. Compromised tissues of corals under distressed conditions deposit visible or no apparent swollen pink pigmentation lines or spots at damaged, diseased, and epibionts colonized interfaces for protection and healing purposes [20, 27, 33, 35,36,37,38,39]. The pigmentation represents coral's response to stress generated by the growth of coralline algae development on coral tissue [20]. The present study observations are in accordance with previous studies and confirm that pink pigmentation is a stress indicator of corals. However, its biological property has not been demonstrated to explore its possible application in treating overgrowing vermetid snails and rhodoliths on massive corals.

The present study observations confirm that pink spots or pink lines on Porites would not always indicate disease or other mechanical stress; hence, pink pigmentation shall not be concluded as a generalized response. They may indicate defensive mechanisms against organisms showing commensalism or ammensalism with corals like Porites. The distinguishing features between different types of pink spots and pink lines can only be made after meticulous underwater investigations but not merely using photographs. Further, microscopic observations, and microbiological analysis would help to understand the possible occurrence and role of parasites and pathogens associated with such pigment depositions. Therefore, underwater assessments on corals with pink pigmentation must be done meticulously to avoid misidentification and discrimination of pink pigmentation-associated diseases or functions. This study infers that Porites sp. in the case of vermetid snails and rhodoliths infestation, produces pink pigmentation as an active strategy to fight epibionts and limit their expansion on the coral surface. This strategy enables Porites colonies to defend themselves and minimize further surface tissue damage caused by infesting agents. Furthermore, a time-series study is needed to understand the seasonal prevalence of infesting agents on Porites colonies as well as pink pigmentation production levels by corals in correlation to infesting agents. Further, in vitro experiments are required to demonstrate the inhibitory activity of purified pigment against vermitid gastropods and rhodoliths.