Urothoe grimaldii Chevreux, 1895

Urothoe grimaldii Chevreux, 1895 View in CoL

This urotoid is reported in Atlantic Ocean, Indian Ocean, and Mediterranean Sea ( Sorbe et al., 2002) and in particular for the European waters and Mediterranean Basin is observed in France, England, Germany, Spain, Portugal, Italy, Israel, Tunisia and Turkey ( Gottlieb, 1960; Toulmond, 1964; Ladle, 1975: Kingston and Rachor, 1982; Grémare et al., 1998; Martínez and Adarraga, 2001; Sorbe et al., 2002; Marín-Guirao et al., 2005; Covazzi Harriague et al., 2008; Moreira et al., 2008; Bakalem et al., 2009; Zakhama-Sraieb et al., 2009; Bakir and Katağan, 2014; Sampaio et al., 2016).

Urothoe grimaldii View in CoL is considered a characteristic species of the well sorted fine sand sensu Pérès & Picard (1964) ( Dauvin et al., 2017) and is closely associated with surface and intertidal soft substrates ( Grémare et al.,1998; Momtazi and Maghsoudlou, 2022). This species has been reported on different types of seabeds and intertidal zone of sandy beach ( Dahl, 1952; Daief et al., 2014), sandflats ( Wynberg and Branch, 1997; Siebert and Branch, 2007), coarse sands ( Penas and Gonzalez, 1983; Moreira et al., 2008) fine sands ( Bakalem et al., 2009), Tellina fabula View in CoL sand communities ( Kingston and Rachor, 1982), Spisula subtruncata View in CoL sand community ( Grémare et al.,1998), Ampelisca brevicornis View in CoL fine sand community ( Toulmond, 1964), Amphioxus View in CoL sands ( Chen et al., 2013), mud, mud and sand mixture ( Bakir and Katağan, 2014). Moreover, it was observed in lagoon environments ( Wynberg and Branch, 1997; du Plessis and Pillay, 2022), in soft substrates vegetates by Fucus spp. and Caulerpa cylindracea ( Toulmond, 1964; Lorenti et al., 2011) and as epibiont of loggerhead sea turtle Caretta caretta ( Zakhama-Sraieb et al., 2009) View in CoL . Urothoe grimaldii View in CoL is also adapted to live in polluted coastal areas ( Ibanez et al., 1993) and can survive near urban discharges ( Avramidi et al., 2022).

This species lives exclusively in shallow coastal waters between 0.5 and 20 m ( Penas and Gonzalez, 1983; Moreira et al., 2008; Bakir and Katağan, 2014) and performs seasonal depth migrations. Indeed, it descends to greater depths in summer until it reaches a maximum depth of around 20-30 m ( Amouroux, 1974).

Like all species of the genus Urothoe , U. grimaldii is considered a predator carnivorous species that preys on benthic meiofauna ( Macdonald et al., 2010). Females of this species generally live for two years, while the less long-lived males mature within a year ( Ladle, 1975). This urothoid can also exploit the burrows of some benthic fossorial species as a source of protection and prey seeking, in fact Goulliart (1952) observed that U. grimaldii can live in the tunnels burrowed by the polychaete Arenicola marina (Linnaeus, 1758) . This amphipod is preyed by coastal fish species such as gobies ( Villiers, 1982) and is part of the diet of the flamingo Phoenicopterus roseus Pallas, 1811 ( du Plessis and Pillay, 2022).

In this work, 1593 individuals of this species were sampled and identified. Urothoe grimaldii was observed only on mobile substrates distributed between 8.41 and 12.81 m. Urothoe grimaldii has been consistently observed along the entire coast of Israel, with occasional records in Haifa Bay, but never in the anthropised sites (HM2.1 and HM27).

Spatiotemporal variation

The temporal variation in the richness of all the taxa, i.e. species and genus taxa, and their total abundance was shown for each station during the consecutive years ( Figure 4 View Figure 4 ). In general, the highest abundances were not linked to the highest richness, probably due to the low number of species and the features of sandy amphipod assemblages where local explosions of a few species often occur. An example is the occurrence of 1805 Cheiriphotis mediterranea individuals in station HM2.1 in the year 2014, not comparable to a proportional increase in species richness ( Figure 4 View Figure 4 ).

The absence of correlation between the abundance and the species richness was caused by a differential contribution of different species. The fluctuations in abundance were due to an increase in the dominant species not the rare and sporadic species; in contrast, the richness was determined by the total number of species and taxa, and influenced by the occasional taxa ( Figure 4 View Figure 4 ).

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The nMDS did not reveal any temporal variation which could have been associated with changes over the eight years ( Figure 5 View Figure 5 ). The contribution of the most abundant species to the taxocenosis profile (SIMPER analysis in Supplement) supported such result, as Perioculodes longimanus and Urothoe grimaldii were the species with the maximum weight in similarity analyses, showing a stable presence. To explore the spatial variability, the long-term monitoring supported the division into two principal zones. The nMDS analysis ( Figure 5 View Figure 5 ) showed a discrepancy in amphipod assemblage between the area corresponding to Haifa Bay (HB) and the zone corresponding to the Southern Israel Coast (SIC).

The spatial variation of the most abundant taxa, i.e. the taxa with more than 150 individuals in the period 2010-2017, was observed to understand how the species were distributed among the stations ( Figure 6 View Figure 6 ). Figure 6 View Figure 6 shows the total number of individuals detected per site. Two different assemblages between the two areas (stations “HM” in Haifa Bay vs. stations “H” in Southern Israeli Coast) are evidenced. Ampelisca spp. was present along the coast of Israel and occasionally close to the Haifa promontory (sites HM27 and H3). Bathyporeia guilliamsoniana was found along the southern coast of Israel and only sporadically in Haifa Bay in 2014 and 2016-2017; it was very abundant in the southern coastal area, in the region between the Haifa promontory and Tel Aviv (H3-H13), with lower abundances southernmost close to the Israeli desalination plants (sites H19-H24 and H28). Cheiriphotis mediterranea was found abundant in Haifa Bay and only occasionally along the southern coast of Israel, with a localised discrete amount in the southern coast close to the Israeli desalination plants (sites H19- H24 and H28). Grandidierella bonnieroides , a species recorded for the first time in 2014 in Haifa Bay, showed sporadic occurrence in other sites. Megaluropus massiliensis showed a homogeneous distribution along the coast, and higher abundances around the Haifa port sites (HM10 and HM23.1), Tel Aviv (H13), and Ashkelon (H28). Perioculodes longimanus was consistently present in high abundance along the entire coast of Israel, confirming its tolerance to different conditions. Photis longicaudata was collected only in the Bay of Haifa, close to the ports, (H2.1 and HM27), and sporadically close to the desalination plants, particularly starting from 2015 (sites H19-H24 and H28). Urothoe grimaldii was a dominant species along the southern Israeli coast and occasionally in Haifa Bay.

The spatial distribution of the most abundant taxa and granulometry dataset was analysed through a principal component analysis (PCA). A substantial diversity was scored between Haifa Bay Port (HM27) and Haifa Bay harbour (HM2.1) sites and the other stations ( Figure 7 View Figure 7 ). The PCA plot indicates significant site discrepancy ( Figure 7 View Figure 7 ). The first two PCA axes explained respectively the 83.1 and 9.6 % of the total variation. The first principal component separated the sites based on the relevant presence of Cheiriphotis mediterranea + Photis longicaudata species in Haifa Bay (HM2.1 and HM27) (see also Figure 6 View Figure 6 ) and the gravel/coarse sediment. The second principal component distinguished the sites due to the presence of Bathyporeia guilliamsoniana + Perioculodes longimanus + Urothoe grimaldii assemblage (see also Figure 6 View Figure 6 ) and the fine sand sediment.

Discussion

Marine biodiversity changes across spatial and temporal scales and the extent of such changes can depend on the context and the taxon investigated ( Steger et al. 2024). In this paper, a monitoring survey along the Israeli coast provided an example of what a multiscale approach can reveal.

A study of the Israeli amphipod fauna – a dominant taxon of the marine ecosystems – was conducted along the coast on the soft littoral bottom area for eight years. This was the first temporal quantitative study performed on the benthic amphipod fauna in the country. Twenty-five taxa (species or genera) were recorded from a sampling effort in the same stations, located in the northernmost Haifa Bay and along the southern coast, at the same depth range.

The dataset showed an overall stable assemblage of the most common species, with sporadic records of occasional species usually associated with macroalgae or seagrasses reaching very low abundances, generally, less than 150 individuals or detected once over the eight years.

Seven species showed the highest abundances and a temporally constant presence: the Levantine endemic Cheiriphotis mediterranea ; the Mediterranean endemic Megaluropus massiliensis ; the NE Atlantic–Mediterranean Bathyporeia guilliamsoniana and Perioculodes longimanus ; and Photis longicaudata and Urothoe grimaldii presumably widely distributed in the Atlantic Ocean, the Mediterranean Sea and the Indian Ocean. The most significant change was the detection of an alien species in 2014, the circumtropical aorid Grandidierella bonnieroides which resulted naturalized ( Lo Brutto et al. 2016).

This is not the only Non-Indigenous (NIS) amphipod species detected in Israeli waters; Bemblos leptocheirus, and Paracaprella pusilla were documented in the region at different sites not included in the present paper ( Lo Brutto et al., 2019; Lo Brutto and Iaciofano, 2020).

The abundance of these seven species was observed to be unstable at the local level, as fluctuations occurred in the different stations. The range of abundance fluctuations was considerable, encompassing peaks of high numbers of individuals concentrated in specific years which differed among the species; for instance, Cheriphotis mediterranea reached 1805 individuals in station HM2.1 in 2014. No correlation was observed between the total abundance per site and year and the species richness, as the fluctuating abundances were attributable to the few dominant species and the assemblages showed a low α- diversity.

The random fluctuations mirrored the ecological traits of the species ( Navarro-Barranco et al., 2017). The taxa identified in the present study can be classified as hyperbenthos, representing the predominant benthic boundary layer faunal component. The inhabitants of the water layer adjacent to the seabed feed on organic particles on the bottom and, at the same time, are capable of vertical migrations, playing a significant trophic role in the benthic communities and within water column food webs ( Buhl-Jensen and Fosså, 1991; Koulouri et al., 2013). These features made the species influenceable by anthropogenic drivers impacting the littoral communities such as nutrient enrichment.

The taxocenosis observed was characterised by deposit feeders on the surface of the bottom, such as ampeliscids, Bathyporeia and Urothoe genus, and species able to perform vertical migrations, such as B. guilliamsoniana , M. massiliensis and P. longimanus . However, a long-temporal variation in the faunal structure which was expected due to the increase of anthropogenic and environmental stressors was not observed.

The analyses detected only a significant spatial variation that discriminated Haifa Bay from the Southern Israeli Coast .

The physical features of the sediment frequently play a crucial role in shaping amphipod assemblage structure ( Buhl-Jensen & Fosså, 1991; Fanelli et al., 2011; de-la-Ossa-Carretero et al., 2012; Scipione, 2013). Along Israeli coast, the bottom, in terms of sediment grain size and chemical composition ( Lubinevsky et al., 2019), displayed two areas of different substratum, with which amphipods were associated. Haifa Bay area was more polluted and eutrophic and with a higher portion of gravel, and coarse and medium sand than the Southern Israeli Coast ( Lubinevsky et al., 2019). As a consequence, the seven most abundant species were spatially distributed according to the type of sediment that favoured their feeding habit. The different species compositions between the two areas reflected the local environmental features.

The information about the sensitivity of the dominant species to disturbances is worthy of remarks. According to de-la-Ossa-Carretero et al. (2012) shallow soft-bottom amphipods can show different sensitivity levels due to their burrowing behaviour; fossorial can show higher sensitivity than domicolous species. This prediction is confirmed in the present paper. Fossorial species, such as Bathyporeia guilliamsoniana , Perioculodes longimanus , and particularly Urothoe grimaldii ( Scipione, 2013) , showed a negative response to polluted stations, where they reduced their abundance; other fossorial species showed an unclear pattern or, indeed, a certain tolerance such as Megaluropus massiliensis , previously indicated as sensitive to polluted areas ( Çinar et al., 2015) and present here with the high abundances around the Haifa harbour localities. The domicolous filter feeders Cheiriphotis mediterranea and Photis longicaudata ( Scipione, 2013) characterized the gravel/coarse sediment stations in Haifa Bay, an area which receives pollutants from rivers effluent of chemical and petrochemical industries, urban and agricultural runoff, and from the Haifa municipality domestic sewage treatment plants.

The dataset also provided biogeographical information on certain species that, to date, appear to exhibit a wide geographic distribution, including U. grimaldii and P. longimanus , the latter of which was unexpectedly documented from the Barents Sea to New Zealand. These geographical ranges must be subjected to rigorous examination and verification, as it is highly improbable that some of these species can be found in areas that are geographically distant or in habitats with markedly dissimilar environmental characteristics. Urothoe grimaldii , a species typically found in sandy habitats, was documented as an epibiont of loggerhead sea turtles ( Zakhama-Sraieb et al., 2009). Similarly, P. longimanus was reported in the literature as both an infralittoral and bathyal species ( Cartes et al., 2007). The present paper shows that the benthic fauna in Israeli coastal marine environments has not changed over time, showing a pattern congruent with long-term analyses of other taxa (molluscs in Steger et al., 2024). Considering the low species richness, changes in amphipod assemblages are expected to be particularly evident if they occur in the future. In this respect, this comprehensive dataset contributes to our knowledge of the Levantine area and its fauna. Data extrapolated from a long time series provide an accurate baseline for detecting putative changes in biodiversity, and a precise understanding of species distributions is essential for monitoring the impact of climate change on marine ecosystems.

Acknowledgments

Financial support was provided by the Department DiSTeM of the University of Palermo and by the National Recovery and Resilience Plan (NRRP), Mission 4 Component 2 Investment 1.4 - Call for tender No. 3138 of 16 December 2021, rectified by Decree n.3175 of 18 December 2021 of Italian Ministry of University and Research funded by the European Union – Next Generation EU. Project code CN_00000033, Concession Decree No. 1034 of 17 June 2022 adopted by the Italian Ministry of University and Research, CUP D33C22000960007, Project title “National Biodiversity Future Center - NBFC”. The authors are grateful to Bella Galil for providing some samples included in the study and Beatrice Scipione for the interesting discussion aimed at improving the manuscript.

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Supplementary material

SIMPER analyses

Data type: pdf

Link: https://www.biotaxa.org/em/article/view/86645/81352