Short-Lived Aggregations of Filograna/Salmacina Tube Worms in the Gulf of Oman

Abstract

Dense aggregations of serpulid worms were encountered in the Daymaniyat Islands (Gulf of Oman) from 10 to 20 m depth, over the period January–March, 2021. The species responsible for these aggregations belongs to the Filograna/Salmacina-complex (Annelida: Serpulidae). This species has been present in the area and observed along the Oman coastline, but high-density aggregates like this have not been reported before. The most probable cause of the aggregations, supported by field observations and Aqua-MODIS satellite data, was natural eutrophication with a subsequent algal bloom linked to the local winter monsoon. This observation emphasises the importance of documenting biodiversity and dynamics of reef communities along the Oman coastline.

As sedentary filter-feeders in coastal waters, tube-dwelling polychaetes of the families Sabellidae and Serpulidae are often considered bioindicators owing to potential increases in their abundance in relation to eutrophication [1,2,3]. Some serpulids occur in clusters and are considered habitat formers, especially as fouling organisms on manmade substrates [4,5]. Furthermore, serpulid worms account for 15% of the alien polychaetes species recognized worldwide [6,7,8].

Dense aggregations and outbreaks of Serpulidae can be opportunistic responses to changes in environmental conditions [9], especially to nutrient pollution [10]. These worms may thrive in conditions that are unfavourable to many other marine fauna [11,12]. The aggregations often develop in sheltered areas, sometimes at salinity levels outside the normal oceanic range [9,13], and with limited water movement facilitating larval settlement [14].

In January–March, 2021, dense aggregations of serpulid worms were observed in reef communities of Jabal Al Kabir Island (also known as D3 Island) in the Daymaniyat Islands Nature Reserve, north of Oman (Figure 1). The worms were mainly overgrowing hard substrates in the sheltered bays and seaward cliffs, forming fragile, branching clusters up to 20 cm in diameter from 10 to 20 m depth (Figure 2). The aggregations occurred during a phytoplankton bloom and were relatively short-lived. By the end of April, the density of the worms had decreased, and only remnants of the tube clusters remained. They were no longer evident in February 2022 when we revisited the area.

These serpulids, although uncommon, have been present in the area and observed along the Oman coastline as individuals or in small clusters. However, high density aggregates and outbreaks of these worms have not been reported until now and we do not have field observations to confirm the formation of high-density aggregations in other locations.

The observed species can be attributed to the Filograna/Salmacina-complex. While nearly 800 polychaete species, including 48 serpulids, have been recorded from the waters around the Arabian Peninsula, only two nominal species have been reported in this complex: Filograna implexa Berkeley, 1835, and Salmacina dysteri Huxley, 1855 [16]. Filograna implexa is the only valid species in that genus [17], characterised by two spoon-shaped opercula. The genus Salmacina, which comes closest to our specimens, includes nine species and one uncertain attribution, all non-operculate, some with inflated radiole tips (Figure 2c). Poor descriptions of most species in this group, and lack of assessment of intra-specific variability, make it currently impossible to confidently identify the specimens.

Molecular studies have shown that some of the previously reported serpulids with wide, almost circumtropical distributions are actually a mix of several taxa, each with restricted regional distributions [18,19,20]. For example, the widespread taxa Spirobranchus kraussii and S. tetraceros (both recorded from Arabian Seas), appear each to consist of more than six species, all with geographically limited distributions [18,19]. The same is likely true for the taxa Filograna implexa and Salmacina dysteri, both originally described from the temperate coasts of south-eastern Great Britain and later reported from around the globe, including the Arabian Seas [16,17,21]. Although it is likely that the worms encountered in Oman represent a new species, any further identification requires genetic studies and a taxonomic revision to establish diversity and relationship within the Filograna/Salmacina complex [21,22].

Filograna/Salmacina species construct calcareous tubes attached to hard substrates. The individual adults are small, usually less than 350 µm in diameter, and a length of only a few millimetres [11,23]. They reproduce sexually, and asexually by scissiparity. Even if sexual reproduction can contribute to the growth of aggregates [23], the branching tube pattern is a consequence of asexual reproduction [24]. Although the worms and aggregates observed in the Daymaniyat Islands show signs of both sexual and asexual reproduction, the asexual reproduction is likely the main mode of “pseudo-colony” formation [23,24], followed by settlement of larvae on conspecific tubes [9,25]. The tube accretion rate depends on environmental parameters, such as water temperature, salinity, food availability, and can reach up to several millimetres per day in S. dysteri [23]. As a result, pseudo-colonies are formed from numerous joined branching tubes, protruding from the seabed [21,26]. Similar aggregations of tubes (Figure 2a,b) were illustrated by Dalyell [27] (for Salmacina dysteri, as Filipora filograna most probably from subtidal Scotland, North Sea), by Pernet [24] (for Salmacina amphidentata from intertidal and shallow subtidal zones of the Indian River Lagoon), by Bianchi [28] (for Filograna sp., Italy, probably Ligurian Sea), and by Enrichetti et al. [29] (for Filograna/Salmacina complex, at 30–160 m depth on a muddy–sandy seafloor of the Ligurian Sea). The fragile structures of this group often do not accrete to form reefs and are sensitive to physical disturbances [30,31], unlike some other serpulid species that can make aggregates larger than 1 m in diameter and make extensive bioherms [26,32,33,34,35]. All the aggregates encountered in our study site were also fragile and did not accrete to form reefs, but grew on the rocky surfaces (Figure 2, Figure 3 and Figure 4).

Nutrient levels in coastal waters of Oman are mostly linked to monsoonal cycles. A strong, moist, summer southwest monsoon, and a weaker, dry, winter northeast monsoon, both result in upwelling and advection of nutrients to the surface in coastal water [36,37]. These are reflected in the algal bloom patterns, with two annual peaks in January–April and August–September along the northern Oman coastline [38].

Increase in nutrient concentrations create a cascade of effects: shifts in phytoplankton composition and biomass, increase in the abundance of phytoplankton grazers, followed by phytoplankton die-off, decomposition, and oxygen depletion [39,40] particularly below the thermocline, occasionally accompanied by mass mortalities of other organisms [41,42,43,44]. These natural cycles in productivity contribute to ocean acidification and specialized shallow-water communities [45].

Our field observations together with Chlorophyll–a data obtained from Aqua–MODIS satellite, confirmed an algal bloom during February–March, 2021, in the Daymaniyat Islands, with monthly averages of 11.17 mg/m³ and 4.65 mg/m³ [46] (23.8° N, 58.1° E; 0.1°–pixel), presumably driven by elevated nutrient levels in the water column. The temporal correlation between the high abundance of Filograna/Salmacina and the phytoplankton bloom, the rapid growth rate of these animals, and the tendency of serpulids to respond to elevated food levels, all suggest that the bloom could be partly responsible for the outbreak.

During field work in the Arabian Sea coast of Oman around Mirbat (Figure 1) in January 2022, we encountered smaller aggregations of what appeared to be the same species (Figure 4, vouchers deposited at Florida Museum of Natural History, UF Annelida 10242, 10255, 10456). This coast undergoes much more intense upwelling than the Gulf of Oman, and therefore these worms might regularly bloom in that area, lending support to phytoplankton productivity driving these population increases.

Although serpulid outbreaks could be a sign of environmental degradation, it seems that they responded indirectly here to a natural increase in planktonic productivity driven by upwelling-enhanced nutrient levels. It is unknown how these serpulids affected the benthic communities in the Daymaniyat Islands, but they could potentially increase water clarity through their suspension feeding [47] and affect their habitat by providing shelter, food, and substrate for epibiont organisms [9,48,49,50]. We did not observe any sign of smothering or overgrowth on corals, unlike serpulid infestations in the Persian Gulf [51] and the Gulf of Oman following the 2008–2009 Cochlodinium polykrikoides bloom [42], and high densities of Spirobranchus in the Caribbean [50].

These observations illustrate the need for a better taxonomic coverage of invertebrate biodiversity in the region and the importance of long-term monitoring of benthic communities.