Colonial Ascidian Didemnum Psammatodes (Sluiter, 1895) in the Eastern Persian Gulf

BioInvasions Records (2019) Volume 8, Issue 3: 582–589

CORRECTED PROOF

Research Article First record, description and distribution of the colonial ascidian Didemnum psammatodes (Sluiter, 1895) in the Eastern Persian Gulf

Mohammad Mohaddasi1, Mohammad Ali Salari Ali-abadi1,*, Rahim Abdi1, Farzaneh Momtazi2, Mohammad Sharif Ranjbar3 and Rosana Moreira da Rocha4,* 1Department of Marine Biology, Faculty of Marine Science and Oceanography, Khorramshahr University of Marine Science and Technology, Khorramshahr, Iran 2Iranian National Institute for Oceanography and Atmospheric Science, Tehran, Iran 3Department of Marine Biology, University of Hormozgan, Bandar Abbas, Iran 4Zoology Department, Universidad Federal do Paraná, Curitiba, Brazil Author e-mails: [email protected] (MM), [email protected] (MASA), [email protected] (RA), [email protected] (FM), [email protected] (MSR), [email protected] (RMR) *Corresponding author

Citation: Mohaddasi M, Ali-abadi MAS, Abdi R, Momtazi F, Ranjbar MS, da Rocha Abstract RM (2019) First record, description and distribution of the colonial ascidian Non-native ascidians are becoming a global problem and several species have Didemnum psammatodes (Sluiter, 1895) in recently been used as models for studying invasion success in the marine realm. the Eastern Persian Gulf. BioInvasions Despite a limited dispersal due to their short-lived larvae, they are often found in Records 8(3): 582–589, https://doi.org/10. coastal habitats as a result of human activities. As one of the warmest waterways in 3391/bir.2019.8.3.14 the world characterized by heavy marine traffic, the Persian Gulf is particularly Received: 28 August 2018 prone to invasive ascidians. This study is the first to have documented the occurrence Accepted: 4 March 2019 of the colonial ascidian Didemnum psammatodes in natural and man-made Published: 24 May 2019 substrates in intertidal zones at 15 study sites in Qeshm and Hengam Islands in the Handling editor: Thomas Therriault Eastern Persian Gulf. High densities of D. psammatodes were observed at several Thematic editor: Cynthia McKenzie study sites located far from major ports, but close to human residences, which may be explained by the prevalence of hard-surface man-made substrates. Copyright: © Mohaddasi et al. This is an open access article distributed under terms of the Creative Commons Attribution License Key words: Ascidians, the Persian Gulf, non-native species, Didemnidae, intertidal (Attribution 4.0 International - CC BY 4.0). zones, Tunicata OPEN ACCESS. Introduction Ascidians (Ascidiacea, Tunicata) are among the taxa with the highest recorded number of introduced species (Lambert and Lambert 2003; Evans et al. 2017). Some species of ascidians have caused significant ecological and economic damage to the invaded marine ecosystems (Lambert 2007). As one of the most diverse groups of ascidians, Didemnids (Giard, 1872) have a wide geographic range and comprise a major component of filter- feeding communities in tropical marine waters, where their almost two- dimensional growth pattern and rapid rate of replication allow them to occupy much of the existing substrates (Kott 2001). In addition, they adapt to survive in a wide range of environmental conditions and are subject to little or no predation (Bullard et al. 2007; Valentine et al. 2007; Abdul et al. 2016). They produce short-lived, non-feeding, swimming tadpole larvae

Mohaddasi et al. (2019), BioInvasions Records 8(3): 582–589, https://doi.org/10.3391/bir.2019.8.3.14 582 Didemnum psammatodes in the Eastern Persian Gulf

that help the species disperse over short distances. Therefore, the occurrence of a species hundreds or even thousands of kilometers from its previously documented habitat likely indicates that it has been transported through anthropogenic vectors such as ballast water or hull fouling (Lambert 2007). Didemnum vexillum, first recorded in the 1980s along the coasts of North America, established large populations at numerous sites, where it overgrew sessile invertebrates and macroalgae (Valentine et al. 2007), resulting in significant ecological and economic damage (Carman et al. 2010; Adams et al. 2011). The presence of Didemnum psammatodes (Sluiter, 1895), another colonial ascidian with a global distribution in warm waters, has been documented in numerous localities of the Indo-Pacific region (Kott 2001; Lee et al. 2016; Supplementary material Table S1). The universal distribution of D. psammatodes is often explained by its high dispersal potential, facilitated larval transport, budding, and colony fragmentation (Yund and Stires 2002; Tamilselvi et al. 2011). This colonial ascidian has a strong potential to colonize areas with a suitable hard substrate, whether natural (embedded rocks, seaweed, mussel bed, coral pieces, etc.) or artificial (cement blocks, boat hulls, oyster cages, etc.), the presence of which may facilitate its settlement (Abdul et al. 2016). The globalization of maritime trade has facilitated the invasion of non- native species against coastal and marine ecosystems, accelerating the transportation of species to other biogeographic zones (Hulme 2009). Several lines of evidence indicating potentials of rapid invasion require additional studies on the management and conservation of ascidians. The Persian Gulf is a very important body of water in the world because of its rich gas and oil resources (Reynolds 1993; Pak and Farajzadeh 2007). This strategic body of water is connected to the Gulf of Oman and, then, to the Indian Ocean through the Strait of Hormuz (Azizpour et al. 2014; Bayani 2016). Furthermore, the Persian Gulf is part of the Western Indo- Pacific realm, comprising the tropical waters of the Indian Ocean (Spalding et al. 2007) successfully invaded by numerous invader species (Lambert 2007). Approximately 60% of the world’s marine oil transportation passes through this Gulf. In peak periods, one ship passes the Strait of Hormuz each six minutes (Al-Hajri 1990, quoted in Reynolds 1993). Researchers have reported the occurrence of Didemnum psammatodes as an invasive species in south India (Abdul et al. 2016). Noting the geographical proximity between the Persian Gulf and the location reported in Abdul et al.’s study and considering the heavy marine traffic between these two locations, we have investigated the occurrence of D. psammatodes as an invasive colonial ascidian in Qeshm and Hengam Islands as the representatives of the Eastern Persian Gulf. Such data are highly important in terms of the estimated rate of invasion and its possible effects on the fauna native to the natural environment as well as for potential monitoring and management purposes, including eradication and control.

Mohaddasi et al. (2019), BioInvasions Records 8(3): 582–589, https://doi.org/10.3391/bir.2019.8.3.14 583 Didemnum psammatodes in the Eastern Persian Gulf

Figure 1. Map of the study areas (for details see Supplementary material Table S2).

It is necessary to point out that the occurrence of Didemnum psammatodes had not been previously reported in the Persian Gulf, which makes the current study the first to have reported the presence of this colonial ascidian in the Persian Gulf with a detailed taxonomic description of the collected specimens.

Materials and methods A field study was conducted in February 2015 at 15 intertidal sites along the southern coastlines of Qeshm Island and the northwestern and western coastlines of Hengam Island in the Persian Gulf, Iran (Figure 1, Supplementary material Table S2). Attempts were made to select both natural and artificial substrates in areas close to and far from human presence. The study sites do not lie in close proximity to major ports and are located relatively away from international marine traffic. The distances from major ports are laid out in Figure 1. All surveys were timed to coincide with low tides to optimize the search area in intertidal zones and man-made structures. To this end, the researchers were set in the study sites two hours before the high tide. The coordinates of sample-collection sites are listed in Table S2. The survey was carried out on foot and the specimens were collected manually. Observations were made on site in intertidal zones for both natural and artificial substrates – calcareous stones, embedded rocks, boat hulls, cement blocks, etc. The substrates were simultaneously surveyed and when appropriate, small boulders and calcareous stones were overturned and examined. Samples were collected in order to confirm species identification and labelled on site with their location in the harbor and the substrate.

Mohaddasi et al. (2019), BioInvasions Records 8(3): 582–589, https://doi.org/10.3391/bir.2019.8.3.14 584 Didemnum psammatodes in the Eastern Persian Gulf

Figure 2. A. Didemnum psammatodes colonies overgrowing Green Zoanthids (Z. natalensis) in intertidal zones. B. D. psammatodes colonies growing on a cement block. Photo by Mohammad Mohaddasi.

In addition, some samples were collected for detailed morphological inspections and macroscopic imaging. These samples were anesthetized with menthol dissolved in seawater in the field. After two hours, the samples were fixed in formaldehyde 5%, buffered with marble chips. The specimens were dissected under a stereoscopic microscope and the internal structures were stained with hematoxylin dye. Then, the samples were stored in the marine animal collection of Khorramshahr University of Marine Science and Technology (KMSU).

Results In total, 158 colonies of D. psammatodes were observed at the study sites along the coastlines of Qeshm and Hengam Islands in the Persian Gulf (Figure 1). The number of found colonies, the area covered and the duration of search for each survey attempt are reported in Table S2. According to our study, the maximum frequency of D. psammatodes occurs at stations very close to residence areas (the main village). Station 3 is located in the intertidal zone of Hengam Village and Station 2 is not far from the main village. However, the number of colonies encountered during the surveys is almost zero for Station 1 (Table S2), which is located further from the small coastal village of Hengam Island. At Stations 2 and 3 in Hengam Island, we found an abundance of hard-surface litter items – including polyethylene and metal objects, tiers, cement blocks, wooden boards and pillars, pieces of fiberglass and building debris – discarded apparently a long time ago and covered with calcareous sediments, algae and living and dead shells. Moreover, these stations experience low wave action, facilitating D. psammatodes encrustation on the substrata nearby. Colonies are more common in the lower intertidal zone, where exposure time is minimal, although they may be present in the mid intertidal zone as well. D. psammatodes was found overgrowing the Zoanthus species, which constitutes a secondary biofouling layer in the intertidal zone (Figure 2) and,

Mohaddasi et al. (2019), BioInvasions Records 8(3): 582–589, https://doi.org/10.3391/bir.2019.8.3.14 585 Didemnum psammatodes in the Eastern Persian Gulf

thus, should not be mistaken for a substrate. This indicates that the establishment of D. psammatodes may even lead to a reduction in the local species richness, as has been reported in the case of the invasive Didemnum vexillum in North America (Bullard et al. 2007; Valentine et al. 2007). However, the interplay between native and non-native species is a complex issue and may vary across space and time (Rodriguez 2006; Thomsen et al. 2011). Therefore, hypothesizing about the impact of D. psammatodes on local organisms requires more studies. In Qeshm Island, the two stations located in Ramchah (13 and 14) are rich in large coastal-bound stones, where the wave force is salient and oil pollution is clearly visible. These stations are the only sites with no D. psammatodes presence, where barnacles (Amphibalanus amphitrite) and black tunicate (Phallusia nigra) are the dominant fouling organisms on exposed surfaces and on substrates with water depths of more than one meter, respectively.

Discussion The colonial ascidian Didemnum psammatodes is characterized by a brownish color, fecal pellets and calcium carbonate spicules in the tunic (Monniot 2016) (Figure 2). The spicules are often limited to the area around the oral siphons. The zooids are 0.5 to 0.8 mm in length with a single testis surrounded by six to eight coils of the sperm duct. The larvae have three adhesive papillae and four pairs of ampullae, and they are 0.4 to 0.5 mm in trunk length. The diagnostic features of D. psammatodes are presented in detail in Figure 3. Given the limited natural dispersal capabilities of ascidian larvae, the introduction of D. psammatodes could be anthropogenic – as a result of increased marine traffic, temperature and eutrophication (Lambert 2007). Ships have regularly used water as ballast since the 1880s, drawing ambient water into ballast tanks and floodable holds for balance and stability (Hallegraeff and Bolch 1991). This water is discharged while under way and also at ports-of-call as cargo is loaded. Water taken aboard may include any planktonic organisms in the water column. Therefore, rich plankton assemblages may be entrained by ships and then released within days or weeks on a continent or island thousands of kilometers away (Carlton and Geller 1993). As an economically and strategically significant body of water in the Indo-Pacific region, the Persian Gulf is host to heavy marine traffic on a daily basis (Reynolds 1993). In this sense, the Persian Gulf is significantly prone to a wide range of invasive marine species from around the world. Moreover, this gulf has been identified as an area characterized by high temperature conditions (Bayani 2016). Being a final destination for urban runoff and sewage systems has subjected the Gulf to nutrient enrichment (Abuzinada et al. 2007).

Mohaddasi et al. (2019), BioInvasions Records 8(3): 582–589, https://doi.org/10.3391/bir.2019.8.3.14 586 Didemnum psammatodes in the Eastern Persian Gulf

Figure 3. Didemnum psammatodes characteristics. A. surface under magnification. The roundish bodies are fecal pellets in the tunic, absent around the zooids’ oral siphons. Spicules are scarce in tunic and often present around zooids’ oral siphons. B. D. psammatodes larvae in four phases from undeveloped to fully developed. The developed specimen has diagnostic features of D. psammatodes including: four lateral ampullae and three adhesive papillae. C. Abdominal parts of zooids with a single testis surrounded by six to eight coils of sperm duct and one big ovary. D. Zooids with large oral siphons and a wide atrial aperture. Scale bars: A. 2.00 mm, B. 0.33 mm, C. 0.17 mm, D. 0.50 mm. Photo by Mohammad Mohaddasi.

In coastal regions located far from commercial ports, where fishing boats and small ships go back and forth constantly, discarded hard-surface litter items in intertidal zones will provide suitable substrates for D. psammatodes to colonize. In addition, if urban runoff is released into the waters, the resulting condition will likely lead to increased nan-native ascidian growth rates (Carman et al. 2007). On the other hand, the higher rate of occurrence of D. psammatodes in the regions located in close proximity to villages, compared with those located far from human residences, highlights the role of human presence and discarded hard-surface litter items. They provide a suitable substrate for D. psammatodes in marine coastal zones located far from major ports and fishing harbors in southern Iran. Since worldwide shipping facilitates the invasion of exotic species to the ports of various countries (Carlton and Geller 1993; Monniot and Monniot 1994; Hewitt et al. 2004; Abdul et al. 2016), the invasiveness of this species

Mohaddasi et al. (2019), BioInvasions Records 8(3): 582–589, https://doi.org/10.3391/bir.2019.8.3.14 587 Didemnum psammatodes in the Eastern Persian Gulf

into the Persian Gulf could also be substantiated. Because of the uncertainty concerning the origin of D. psammatodes, its status as a nonindigenous species still remains unclear. Besides, genetic fingerprinting approaches to specify its points of origin (Lambert 2007) in the samples collected from the Persian Gulf could provide fundamental perspectives into the patterns of introduction of D. psammatodes. Furthermore, the long- term as well as large-scale monitoring of coastal waters for D. psammatodes and other non-indigenous ascidian species in the Persian Gulf could be an effective method to detect these species in their early phases of invasion. Overall, the results of this study suggest that major ports are not the only areas invaded by nonindigenous marine organisms but regions with no heavy marine traffic or regions located far from major ports may also be exposed to and affected by invasive species.

Acknowledgements

The research for this paper was funded by Khorramshahr University of Marine Science and Technology (KMSU) under grant no. 47764807. Special thanks go to the Iranian National Institute for Oceanography and Atmospheric Science (INIO) for logistically supporting our fieldwork. We are also grateful to Dr. Abdolvahab Maghsoudlou for sharing with us his pearls of wisdom throughout the course of this project. This study is dedicated to Pegah Jalilian for her infinite kindness and spiritual support. The authors would like to thank anonymous reviewers for their useful suggestions for submitted manuscript. The publication of this article is supported by the Open Access Publishing Fund of the International Association for Open Knowledge on Invasive Alien Species (INVASIVESNET).

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Supplementary material The following supplementary material is available for this article: Table S1. Distribution of Didemnum psammatodes (Sluiter, 1895) around the world, based on OBIS database. Table S2. Location, name, and coordinates of Didemnum psammatodes surveys and the number of colonies encountered during surveys per area (m2) conducted in Qeshm and Hengam Islands in the Persian Gulf, Iran. This material is available as part of online article from: http://www.reabic.net/journals/bir/2019/Supplements/BIR_2019_Mohaddasi_etal_SupplementaryTables.xlsx

Mohaddasi et al. (2019), BioInvasions Records 8(3): 582–589, https://doi.org/10.3391/bir.2019.8.3.14 589