Beneath the waves: A multivariate approach on species-specific Crinoid-Crustacean Decapod association in the Lakshadweep archipelago

Nithyanandam Marimuthu^1*Sanjeevi Prakash²

• ¹Zoological Survey of India, Kolkata, India
• ²Centre for Climate Change Studies, Sathyabama Institute of Science and Technology, Chennai, Tamil Nadu, India

Symbiotic associations between marine animals and sessile invertebrates are a remarkable feature of coral reef ecosystems. However, most studies often concentrate on free-living organisms, which are easier to collect and identify. In contrast, symbiotic animals are frequently overlooked or underestimated because of their small size, hidden lifestyles, and the broad distribution of sibling or cryptic species that are specialized to specific host species (Knowlton 1993;Horka et al., 2016). Although the uniqueness of these symbiotic relationships is not fully understood, crustacean decapods associate with other macro invertebrates. In particular, various echinoderms are notably common and exhibit astonishing diversity in their morphology, ecology and sexual biology within the tropical Indo-Pacific region (Bruce 1976;Williams 1984;Ng & Jeng 1999;Hayes 2007;Hayes et al. 2016).Among different classes in the phylum, Echinodermata, Crinoids are a vital component of coral reef ecosystems, exhibiting notable diversity in the coral reef ecosystems of India (Sastry et al., 2019). Earlier studies on crinoids in India have been reported by Clark (1912) and Clark and Rowe (1971). About 25-30 species of crinoids have been hitherto recorded from the Indian waters. There are about 28 species reported in the Andaman and Nicobar Islands (Venkatraman et al., 2011) whereas 12 species in the Lakshadweep archipelago (Sastry et al., 2019). Recently, studies on crinoid-associated crustacean decapods have received further attention in Indian waters with special reference to the Lakshadweep archipelago (Prakash and Marimuthu, 2020, 2022, 2024). The present study aims to establish a baseline dataset spatially to understand the diversity of crustacean decapod communities that are associated with different crinoid species in Lakshadweep by using multivariate analyses.During our regular faunal explorations under Zoological Survey of India In-house activities funded by the Ministry of Environment, Forest and Climate Change, Government of India entitled, "Fauna of protected areas of Lakshadweep: newly declared PAs (2020-24) and Fauna of Lakshadweep: Echinoderms (2017-2020)", these Crinoidea and associated crustacean fauna were collected from 85 locations. These fauna were collected systematically from the sessile coral habitat using the line intercept transect method (English et al., 1997) followed parallel to the shore. The mean abundance data on the Crinoid host and their associated crustacean fauna based on their availability in the Islands were calculated and used as raw data for validation. Six surveys were conducted between February 2018 and February 2023 to assess these species distribution patterns along the Islands and Islet of Lakshadweep Archipelago.The position of the Islands and Islet has been classified into three based on the proximity and geographical locations of the archipelago (Supplementary Figure 1). They were Amindivi Islands (Amini, Kadamat and Kilthan Islands), Laccadive Islands (Agatti, Kavaratti, Bangaram, Androth, Suheli, Kalpeni, Piramulpar Islands and Pitti Islet) and Minicoy Island. The collected crinoid (Sastry et al., 2019) and their associated crustacean fauna (Prakash and Marimuthu, 2020;2022;2024) were identified through standard methods and the taxonomical notes were published. The distribution pattern of the crinoid host was assessed with respect to the Islands and the associated faunal distribution was evaluated with respect to their host fauna. SCUBA diving were was made conducted for collecting these organisms at a depth between 10 and 40m. The spatial analyses such as principal component analysis (distribution variability of crinoid host and associated crustacean fauna), non-metric multidimensional scaling analysis (distance matrix of Islands based on the available crinoid host), Mondrian plot and indicator species analysis (probability of association within the community structure) were assessed through PRIMER 7 version 7.0.5 (Clarke and Gorley 2015) and PAST, version 4.13 (Hammer et al., 2001;Hammer and Harper, 2024). Principal component analysis (Figure 1A) revealed the spatial variability of crinoid distribution along the Lakshadweep archipelago. showed that tThere was a variability (PC1: 26.8% variance) between the Islands and the most influenced crinoid genus observed in this study was Stepanometra spp. (Stephanometra tenuipinna and Stephanometra Indica) followed by Phanogenia distincta. Stepanometra spp. are more contributed towards Minicoy Island followed by Laccadive group of Islands led by Kavaratti Island. In the case of Phanogenia distincta, followed as the second key contributor it is observed towards Laccadive group such as Bangaram and Agatti Islands. A little variability (PC2: 20.2% variance) was also observed due to the influence of Comaster multifidus towards around Kadamat Island of Amindivi group and Lamprometra palmata towards around Agatti Islands.Metric multidimensional scaling analysis (Figure 1B) showed the distance matrix of the Islands based on the intensity of multiple crinoidea species observed. It indicates the complete segregation of all classified Islands such as Minicoy Island, Amindivi and Laccadive group of Islands. Bray-curtis cluster analysis (Figure 1B) showed found four different main clusters:; two complete clusters formed in the Laccadive group with 58.5% and 36.27% similarity, one complete cluster formed in the Amindivi group with 48.58% similarity, one mixed cluster formed between Laccadive and Amindivi group of Islands with 48.58% similarity and one outlier, Minicoy Island. The rationale behind the two complete clusters formed in Laccadive group of Islands due to the contribution in highest intensity of multiple crinoidea species such as Tropiometra carinata and Cenometra bella followed by Himerometra robustipinna and Phanogenia gracilis. These species are also clustered together with 37.17% similarity based on their occurrence in higher intensity at the Laccadive group of Islands (Figure 1C). Similarly, Himerometra robustipinna and Phanogenia gracilis played a vital role in single complete cluster formed in Amindivi group. Minicoy Island was an outlier due to higher intensity of multiple crinoidea species from the Mariametridae family (Figure 1C).Principal component analysis (Figure 2A) of crinoid associated crustacean faunal distribution along the Lakshadweep archipelago showed that there was a strong variability (PC1: 52.1% variance) between the associated crustacean fauna specific to thewith the cCrinoid hosts. and tThe most influenced crustacean species observed were palaemonid shrimps (Periclimenes pitti, Periclimenes affinis and Cuapetes seychellensis), brachyuran (Permanotus purpureus) and porcelain crabs (Aliaporcellana pygmaea) followed by alpheid shrimps (Synalpheus carinatus and Synalpheus stimpsonii) which were totally dependent on Phanogenia gracilis. A little variability (PC2: 14.6% variance) was also observed between the crustacean fauna in choosing the Crinoid host. Similarly, Phanogenia gracilis acts as a host for Synalpheus comaturalum.Phanogenia gracilis dependent crustacean fauna got clustered together (Figure 2B) with a similarity of 49.92% in connection with their selection of this crinoid fauna as a host.Among the crustacean fauna, Periclimenes affinis, Synalpheus carinatus and Periclimenes pitti were observed as dominant taxa in selecting Phanogenia gracilis as host (Figure 2B).Moreover, aAlpheid shrimps preferred to associate only with the Comatulidae family of crinoids (Phanogenia gracilis, Phanogenia multibrachiata and Comaster multifidus) with a lower similarity of 25.51% (Figure 2B). Metric multidimensional scaling analysis (Figure 2C) and Indicator species analysis (Supplementary Figure 31) showed that the highest diversity of crustacean fauna associated with Phanogenia gracilis with the high Shannon-Weiner diversity index of 1.993, while. sSquat lobsters preferred Mariametridae family of Crinoids (Stephanometra indica, Stephanometra tenuipinna) as host (Figures 2B and2C).The distribution pattern of faunal resources spatially by using statistical methods helps to understand the relationship of species richness along the study sites/regions. It would also be helpful to express the variability in the temporal assessment when the present assessment will be compared in the future. The present status of both the crinoid host and their associated crustacean fauna along the Islands of Lakshadweep archipelago was presented by using multivariate approach. The live specimens documentation of host crinoids (Supplementary Figure 2) and their associtated decapod crustaceans (Prakash and Marimuthu, 2020;2022;2024) were presented based on the systematic identification on the duplicate specimens in the laboratory (Sastry et al., 2019;Prakash and Marimuthu, 2020;2022;2024).The principal component analysis helps to observe the influencing fauna crinoid species and their variability crustacean association between the study sites/cluster of study sites/regions recorded during the study period. In the present study, Steaphanometra spp., Phanogenia distincta, Comaster multifidus and Lamprometra palmata acted as principal components of crinoid hosts with 20.2 to 26.8% variability. Based on the proximity of Islands in the archipelago, the crinoid species diversity gradually decreased from the north (Amindivi group) and central (Laccadive group) Islands to southern Minicoy Island based on the contribution of most influenced (PC1) species; Stephanometra spp. (Stephanometra tenuipinna and Stephanometra iIndica). In Among the case of crustacean associates, palaemonid shrimps, brachyuran and porcelain crabs followed by alpheid shrimps acted as principal components associated exclusively with the crinoid, Phanogenia gracilis with 52.1% variability. Such kind of expression was made for the taxa (coral and fish communities) based on proximity of pollution/non-pollution and on/offshore as factors in the Red Sea ecosystem (Sawall et al., 2014). In India, the variability of bio-physical parameters (Jha et al., 2013;Manikandan et al., 2014aManikandan et al., , 2014b;;Riyas et al., 2020) pertaining to coral community structure, Drupella cornus on coral colonies (Marimuthu et al., 2022), Holothuroidea (Gole et al., 2022) and phytoplankton diversity (Sachithanandam et al., 2022) based on the proximity of Island/mainland were practiced by using different multivariate analyses. But, the influencing fauna of the host and their associated crustaceans were expressed here individually to understand both the proximity of the Islands as well as speciesspecific association. Further, few species of crustacean decapods were associated with more Formatted: Font: (Default) Times New Roman, 12 pt, Not Bold than one crinoid species. Horká et al. (2016) reported such multiple host switching phenomenon particularly on palaemonid shrimps. Similarly, such associations in particularly, squat lobsters (Allogalathea elegans) and alphaeid shrimps (Synalpheus stimpsonii, Synalpheus carinatus, and Synalpheus comaturalum) were found associated with multiple hosts in the present study. Interestingly, certain crinoid species attract specific crustacean associates due to differences in crinoid morphology, habitat complexity, and chemical cues, which provide suitable microhabitats and protection for particular decapods (Prakash and Marimuthu 2020;Korzhavina et al., 2024). Further, the decline in crinoid diversity from northern Amindivi Islands to southern Minicoy Island may stem from environmental gradients similar to Red Sea coral-reef fish dynamics (Ellis et al., 2017;Lucia, G.M. 2024).In the Red Sea, coral diversity and symbiotic relationships weaken near polluted or nearshore areas due to factors like nutrient runoff, sedimentation, and human activity (Hoegh-Guldberg et al., 2017;Lucia, G.M. 2024). Similarly, the Lakshadweep archipelago's northern and central islands (Amindivi and Laccadive) likely offer more stable habitats for healthier crinoid populations, supporting diverse decapods like Synalpheus shrimps and Allogalathea squat lobsters (Prakash and Marimuthu, 2020). Hence, the monitoring of such environmental variables is need of the hour to interpret the diversity of crinoids and their associates.