Increasing risk of invasions by organisms on marine debris in the Southeast coast of India

Increasing


Introduction
Marine debris is currently a major global environmental threat that has gained more attention in the last decades from the scientific community, intergovernmental organizations and agencies due to its severe impacts on fisheries, ecosystems and ultimately human health (Beaumont et al., 2019).Marine debris such as plastic, food cover, glass, rubber, tyre, household material, among others, is disposed, discarded or abandoned in coastal and marine environments (Coe and Rogers, 1997; UNEP/PAM/MEDPOL, 2009; Thompson and Gall, 2014;Bergmann et al., 2015) or brought indirectly to the sea by inland waterways and winds (UNEP, 2009;Lima et al., 2014;Jambeck et al., 2015;Aragaw, 2021).
It has been estimated that 4.8-12.7 million tons of marine litter enter into marine habitats annually (Jambeck et al., 2015).Furthermore, nearly 19 to 23 million tons of marine debris produced worldwide in 2016 entered aquatic habitats (Borrelle et al., 2020).Once debris enters the sea, it either floats or sinks, and can be transported to other areas by currents, washing up onto the shoreline and beaches ( Van der Mheen et al., 2020;Mghili et al., 2020;Behera et al., 2021;Bouzekry et al., 2022;Fruergaard et al., 2023), or drifting offshore (Lebreton et al., 2012) and sinking to the deepest ocean trench (Chiba et al., 2018).
The southeast coast of India is one of the richest marine biodiversity regions in India (Venkataraman and Maelkani, 2007) with >380 fish species (Purusothaman et al., 2015;Mogalekar et al., 2018).It also acts as nursery ground for various fish and shell fish larvae, plankton diversity, macrobenthic communities and meiofauna assemblages (Mahesh and Saravanakumar, 2015;Punniyamoorthy et al., 2021;Saravanakumar et al., 2021).Furthermore, the IUCN endangered species, such as olive ridley (Lepidochelys olivacea (Eschscholtz, 1829)) and green turtle (Chelonia mydas (Linnaeus, 1758)), are frequently occurring along this coast (Chandrasekar and Srinivasan, 2013).However, its biodiversity richness is threatened by anthropogenic activities (urbanization and economic development), extreme weather events, habitat loss, pollution and invasion of non-native species (Ravi, 2011;Rameshkumar and Rajaram, 2017;Vidyasakar et al., 2020;Gunasekaran et al., 2021;Sanjai Gandhi et al., 2021;Gunasekaran et al., 2022).In the southeast coast of India, the Tamilnadu region receives the largest amount of litter (Patterson Edward et al., 2020;Vidyasakar et al., 2020;Neelavannan et al., 2022;Pattiaratchi et al., 2022).However, its impact on the marine fauna is unknown because no research has been conducted on the potential of marine litter as a dispersal vector of non-indigenous marine organisms, including invasive species.Assessing the nature of biofouling should be a high priority to detect new species introduction and develop effective plans to prevent and mitigate their spread.This study aims to report, for the first time, biofouling communities attached to marine litter found on eight beaches of Tamilnadu in the southeast coast of India.Speciesspecific substrate preferences are also analyzed.

Study area
Tamilnadu coast is located in the southern part of India and is connected to the Bay of Bengal.The Tamilnadu coastline is the third largest coastal region of India with 1076 km of coastal length and an Exclusive Economic Zone (EEZ) of 73,359 mile 2 , contributing 0.72 million tons of fish production.The major geomorphic features of this coastal line comprise raised beaches, sand dunes, mangroves swamp, estuaries and tidal flats.This coastal region supports an enormous variety of important marine species, including molluscs, sea turtles, coral reef fishes and others (Chinnadurai and Fernando, 2007;Babu et al., 2010;Satheeshkumar and Khan, 2012;Chandrasekar and Srinivasan, 2013).
The study area is densely populated by various major and minor chemical-based industries, involved in mineral and metal processing, oil refinement, pharmaceutical, dye and fertilizer production.It also receives a large amount of debris from recreational, fishing and tourism activities (Dowarah and Devipriya, 2019;Jeyasanta et al., 2020;Sanjai Gandhi et al., 2021;Gunasekaran et al., 2022;Kannan et al., 2023a) and from international shipping from Southeast Asian countries (Dharani et al., 2003).Climate in the area is tropical, with temperatures between 20.5 and 37.8 • C and high rainfall from northeast during the monsoon season (November to February, average precipitation over the period 698 mm).The resulting wind and hydrodynamic may influence the dispersal and transport of marine litter (Al Khayat et al., 2021).
To assess biofouling communities on beached marine litter, four urban (Puducherry-S1, Silver beach-S4, Samiyarpettai-S6 and Puthupettai-S7) and four village (Veerampattinam-S2, China Veerampattinam-S3 Periyakuppam-S5 and Parangipettai-S8) beaches were selected (Fig. 1; Supplementary Table S1) along the southeast coast of Tamilnadu to represent most of its shoreline, considering site accessibility, level of exposure and usage/activity.The urban beaches are referred here to frequented beaches with a large amount of activities (e. g. swimming and fishing) and the village beaches to beaches near small populations mainly used during holiday seasons.The Puducherry beach (S1) is a natural urban beach and this site is one of the busiest beaches in the state, attracting 3000 visitors per day and even more during weekends and public holidays.In the Puducherry coast, beaches are generally narrow and suffers from severe erosion along the northern segment, whereas the southern segment is comparatively broader and characterized by a depositional nature.The Silver beach (S4), situated between Parangipetai to the south, Pondicherry to the north, Cuddalore city to the west and the Bay of Bengal to the east, covers an area of 2 km 2 .The study area is composed of fluvio-marine quaternary sediments.Fishing and tourism activities are major sources of plastic litter in S4 (Kannan et al., 2023a).On the other hand, Samiyarpettai (S6) and Puthupettai (S7) small urban beaches are located on the Coromadel coast of the Bay of Bengal.The Veeramapttinam, Chinna veerampattinam, Periyakuppam and Parangipettai are village beaches, which have significant lower population density and fishing activities when compare to S1 and S2.Recently these two beaches became some of the most popular holiday locations of the region.

Litter sampling
The sampling was conducted on the eight sites between March and April 2022 following the methods used on the beaches of Morocco and Peru described in De-la-Torre et al. ( 2021) and Mghili et al. (2022).Along the length of each beach, 100 m transects were randomly selected, maintaining at least 30 m distance between them.The Global Positioning System was used to register the geographic coordinates of each transect on each beach.At each beach, sampling was carried out for nearly 60 min in daylight, prior to the beach cleanup.Marine litters were collected in the tidal zone.Only the fouled litter items were considered for this study.The collected fouled litters were stored in aluminum foil bags, transported to the Faculty of Marine Science at Annamalai University, and classified according to the codes and categories developed by the United Nations Environment Programme (Cheshire et al., 2009).The source of collected marine litter were also categorized into two groups: sea based and land-based origin (Veiga et al., 2016).The seabased origin group includes debris from the fishing industry, commercial and recreational shipping, and offshore platforms (Stelfox et al., 2020;Richardson et al., 2021), while the land-based origin group includes debris from recreation, tourism, shoreline, medical and agricultural activities.It should be acknowledged that, while this classification may help to determine the contribution of various anthropogenic activities, the origin of the litter cannot be determined with absolute certainty.
Each marine litter item collected was scrutinized to carefully record all fouling individuals and photographed following previous studies (Shabani et al., 2019;De-la-Torre et al., 2021;Mghili et al., 2022;Póvoa et al., 2022;Subías-Baratau et al., 2022).Samples were preserved in 70 % ethanol to allow further identification.Fouling species were identified at the lowest taxonomic level using a stereomicroscope and taxonomic guides.As it is standard practice given their fine diagnostic characters, low-vacuum scanning electron microscopy (SEM) was used to identify bryozoan species by means of a Hitachi TM4000plus Tabletop at the Natural History Museum, University of Oslo (Norway).After species identification, the number of individuals/colonies were counted for each taxon.Identified species were classified as invasive and/or cryptogenic based on their distribution and population status on the World Register of Marine Species (WoRMS Editorial Board, 2019) and the Global Invasive Species Database (International Union for Nature Conservation, http://www.iucngisd).
The frequency of occurrence was calculated for each fouled species.Non-parametric tests (Kruskal-Wallis) were employed to check whether the number of individuals/colonies and taxa varied by litter type.Statistical tests were carried out using the SPSS v20 software at the 0.05 level of significance.
A subset of 10 beached litter items were analyzed using a FT-IR spectrometer to identify the polymer composition based on IR absorption bands representing the presence or absence of specific functional groups in the material.The spectra collected were analyzed with Open Specy v0.9.3 software (Cowger et al., 2021) and compared to spectra references in library databases to identify the compounds.The plot in Fig. 2 was constructed using ggplot2 (Wickham, 2016) in R version 4.2.0 (https://www.rproject.org/).

Fouling organisms
A total of 3130 specimens/colonies belonging to seven phyla and representing 17 species were recorded on marine debris (Fig. 2 and Table 1).The number of individuals/colonies registered on each litter varied from 1 to 176 (mean = 8.64).Three species of barnacles represented almost half (46.5 %) of all fouling specimens, while three species of bryozoans accounted for the 32.7 % of the recorded specimens (Figs.2-3; Table 1).
Fouling organisms were observed on 20 types of marine litter according to the UNEP code (Supplementary Table S2).The most frequent types were PL24 (plastic fragments) followed by PL01 (bottle caps & lids), PL02 (bottles <2 L), GC02 (bottles & jars), PL07 (plastic bags), PL14 (plastic buoys) and PL06 (food containers).Other items were also reported in lower numbers (ropes, clothing, fishing net, cigarette lighters, bottles >2 L, shoes, tyres, metal body spray, gloves, inner-tubes, cutlery and paint brush).Land-based activities were the major source accounting for the 88.5 % of total litter collected, followed by sea-based activities with 11.5 % (e.g.buoys, fishing net and ropes; Supplementary Table S2).Regarding polymer composition of the plastic items, most of the litter items were composed of polyethylene (40 %) and polyamide (40 %), while polyethylene terephthalate (PET) represented the 20 %.
The three barnacle species were present on all types of litter but they were dominant on plastic and glass bottles, buoys, fishing ropes, bottle caps/corks and foam sponges (Table 2).Foraminifera, Cnidaria and Chlorophyta were exclusively observed on plastic items.
The common occurrence of the barnacles Lepas anserifera and Amphibalanus amphitrite confirms that both species have a welldeveloped ability to attach to artificial materials of different compositions (Katsanevakis and Crocetta, 2014;Shabani et al., 2019;Al Khayat et al., 2021).We also present the first records on stranded litter for the species P. cingulata, U. vestiarium, the foraminiferan Ammonia beccarii and the oyster Magallana bilineata (Table 1).
Remarkably, we found the non-indigenous mussel Mytella strigata attached in high density groups to fishing nets.This species, previously documented in India in 2019 on floating plastic bottles, wooden pilings, hulls of boats and walls of fish cages, is considered invasive (Jayachandran et al., 2019).Marine litter may thus have facilitated its spread in Indian waters.Our findings indicate that the growing presence of plastic litter may increase the probability of introducing non-indigenous and invasive species into Indian waters, potentially generating a negative impact on the ecological characteristics of the invaded habitat as already happened (Rech et al., 2016;Miralles et al., 2018;Lins and Rocha, 2022).The phyla recorded here include several invasive species previously documented on marine litter (Garcia-Vazquez et al., 2018;Miralles et al., 2018;Rech et al., 2018b;Lins and Rocha, 2022).
The stranded litter collected was composed mostly of plastic material, which is also in line with previous results from other Indian beaches (Kaviarasan et al., 2022;Mishra et al., 2023).The dominance of plastic litter is due to the combination of its low decomposition rate and high persistence (Derraik, 2002) with the dramatically increased input from land-and sea-based activities since the mid-XX century (Jambeck et al., 2015;Lau et al., 2020).Furthermore, the low density of most plastics facilitates its spreading throughout different oceans and ecosystems by winds and ocean currents.In particular, the main sources of plastic debris were land-based (88.6 %), while recreational activities followed by fishing activities were the major sources of marine litter, both results consistent with previous studies on other Indian beaches (Sulochanan et al., 2019;Gunasekaran et al., 2022;Kaviarasan et al., 2022;Mishra et al., 2023).
Species diversity was higher on plastic litter compared to other materials, with variations observed across different categories, likely due to their higher abundance, prolonged presence and persistence in the marine environment.Several past studies reported the preference of arthropods, molluscs and annelids for plastic material (Rech et al., 2021;Mghili et al., 2022;Póvoa et al., 2022).Nevertheless, three barnacle species were found on all types of litter as these species are capable to attach to a diverse range of litter, regardless of the litter type.While bryozoans preferentially colonized plastic surfaces and glass bottles, other studies found that they also frequently colonize hard plastic and nylon (Rech et al., 2021;Póvoa et al., 2022).Consistent with our findings, litter with simple, smooth surfaces, such as plastic and glass, are usually highly covered by sessile organisms including bryozoans, polychaetes and hydrozoans (Kiessling et al., 2015;Rech et al., 2018a;Póvoa et al., 2022).Other phyla, such as Foraminifera, Cnidaria and Chlorophyta, were exclusively observed on plastic, confirming previous knowledge regarding cnidarians (Crocetta et al., 2020;Rech et al., 2021;Mghili et al., 2022).
Litter items with high buoyancy, such as bottles, buoys and plastic bags (mostly made of polyethylene or expanded polystyrene), supported abundant macroinvertebrate assemblages.These materials can be more suitable for macroinvertebrate colonization and transportation, as they can persist on the sea surface for longer periods of time (Goldstein et al., 2014;Rech et al., 2021).However, their capacity to transport fouling organisms is also influenced by other factors, such as size, texture, persistence, polymer type, material color and roughness (Rech et al., 2018a(Rech et al., , 2021;;Shabani et al., 2019;Póvoa et al., 2021;Mghili et al., 2022;Póvoa et al., 2022).In particular, biofouling of floating debris may also decrease its buoyancy causing it to sink (Kaiser et al., 2017;Kooi et al., 2017).A recent study provided evidence of this phenomenon as the most abundant fouled benthic plastics had lower densities than seawater, and all bryozoan species were characteristic of shallower depths than those sampled (Subías-Baratau et al., 2022).Benthic plastic debris substrates may thus change biodiversity of benthic communities.Furthermore, litter with low buoyancy, such as fishing nets and ropes made of polyamide, may have been deposited in the seafloor before being colonized.
Litter distribution was uneven among the studied beaches, with urban beaches displaying the highest abundances of fouled litter.This finding is consistent with previous studies conducted along the Indian coast, which also identified urban areas as the main contributors to marine litter accumulation (Sulochanan et al., 2019;Gunasekaran et al., 2022;Kaviarasan et al., 2022;Mishra et al., 2023).The greater quantity of marine litter is probably the result of higher population density and significant coastal tourism in urban beaches.In contrast, village beaches showed lower litter abundances, probably because they are less frequented by human activity.Once litter reaches the beaches, it can eventually enter the coastal waters.The introduction of large quantities of litter makes it more probable for marine organisms to settle on these substrates in urban areas compared to villages.Furthermore, factors like winds, currents and waves may also contribute to the variation in fouled litter abundance on the studied beaches (e.g.Rech et al., 2018a).
In comparison to open sea areas, urban coastal environments are also more prone to the introduction of invasive species, through different pathways, including marine litter (González-Ortegón and Moreno-Andrés, 2021; Wang et al., 2021).Alien species can probably benefit more from, or can at least be less affected by, urbanization compared to indigenous species owing to their adaptive behavioral traits and strategies that allow them to cope better with changing conditions (González-Ortegón and Moreno-Andrés, 2021; Wang et al., 2021).Therefore, the monitoring of biological invasions should prioritize coastal waters near urban areas due to the high number of pressures they experience, including intense vessel traffic and abundant marine litter introduction.Implementing monitoring programs becomes crucial to understand the extent of the interaction between marine litter and fouling organisms, as well as to assess the role of marine litter in introducing non-indigenous and invasive species.
Based on the inscriptions present on the fouled litter, we found that four items might potentially come from Indonesia (PL06, with bryozoans and polychaetes, approximate distance from our sampling station 5607 km), six from Myanmar (PL02, with L. anserifera, 2252 km), and two from Sri Lanka (PL02, with bryozoans, 274 Km).In line with this observation, these specific items were plastic bottles with high buoyancy, suggesting the potential for long distance transport.However, further in-depth studies in this region are necessary to substantiate this hypothesis.Marine debris has been previously considered a primary vector for carrying marine species to remote areas (García-Gomez et al., 2021).
This study demonstrates that Indian beaches are littered by recreational, fishing and tourism activities as well as domestic use, and this littering may facilitate biological invasions.A reduction of marine littering would help reducing the risk of introduction of non-indigenous species.To control its input, it is important to focus on its sources (Lau et al., 2020).Efforts should also be made to mitigate the leakage of debris from fishing activities.Education has to be focused on changing the human behavior regarding the use of plastics (Bouzekry et al., 2022), encouraging the reuse, recycling (e.g. the program Container Deposit Legislation (CDL) that encourages public participation in recycling plastic waste bottles by offering small cash incentives to individuals who return beverage containers; Al Khayat et al., 2021;Schuyler et al., 2018) and recovery of new and innovative resources.This could be supported by the establishment of innovative solutions in the context of the circular economy.While beach clean-ups may also help reduce the risk of introducing non-indigenous species via plastic litter, it is essential to acknowledge that they do not provide a comprehensive solution to the plastic problem.Conversely, awareness campaigns serve as one of the potential tools to mitigate the amount of litter arising from recreational beach use (Grelaud and Ziveri, 2020).Given that plastic pollution is a global issue, international cooperation is required to coordinate efforts and make informed decisions that can effectively reduce the amount of floating plastics, thus mitigating the risk of invasive species transportation between oceans.At the local scale, there is a need for more extensive research on floating litter in Indian waters to comprehensively understand and address this issue.We also highlight the need for further collaborative research involving taxonomists with expertise on different groups and molecular biologists to monitor the occurrence of non-native species on marine debris.

Conclusions
India ranks among the top producers and consumers of plastic globally (Shahab and Anjum, 2022).Like many other countries, India suffers the challenge of managing the escalating amounts of plastic waste (Kannan et al., 2023b).Sadly, inadequately managed plastic litter finds its way into the marine environment, exacerbating the situation.The Covid-19 pandemic has further contributed to this issue with increased demand for single-use plastic (e.g.face masks and gloves) (Gunasekaran et al., 2022;Kannan et al., 2023b).It is clear that inadequately managed litter in the region has significant adverse effects on coastal biodiversity.While many previous studies have quantified the impact of plastic litter on marine wildlife in Indian waters mainly associated with ingestion and entanglement (e.g., Nisanth and Kumar, 2019;Harikrishnan et al., 2023;Kannan et al., 2023b), this is the first documentation of marine litter acting as a vector for species dispersal in Indian waters.Our results indicate that floating plastic litter represents a habitat for a diverse array of marine biota, including invasive species.Moreover, our study shows the potential of marine litter to transport marine organisms by over significant distances.As the volume of plastic litter entering the Pacific Ocean grows, it will increasingly become a substrate for marine species, heightening the risk of introducing nonnative species into Indian waters.These non-native marine species can turn invasive and profoundly impact habitats and diminish the essential services they provide.More extensive research and monitoring surveys targeting fouling litter thus play a crucial role in detecting alien species in Indian waters.However, it is raising awareness and promoting education that are vital components in fostering sustainable solutions to combat plastic pollution in the country and globally.

Fig. 1 .
Fig. 1.Sampling sites of stranded marine litter along the southeast coast of India.

Fig. 2 .
Fig. 2. Percentages of the seven different phyla recorded fouling the marine litter sampled and examples of stranded marine litter with fouling organisms sampled on the beaches studied.A) individuals of the anemone Anthopleura sp.; B) encrusting bryozoan colonies of Jellyella tuberculata; C) individuals of the oyster Magallana bilineata; D) goose barnacles of the species Lepas anserifera; E) acorn barnacles of the species Amphibalanus amphitrite; F) encrusting bryozoan colonies of Biflustra savartii.

Table 1
List of fouling species and their frequency of occurrence on all stranded litter items.Abbreviations for Status: C = cryptogenic; I = invasive; N = native.

Table 2
Abundance of individuals/colonies of each phylum on the different types of marine litter.