﻿Diversity and distribution of the Isopoda (Crustacea, Peracarida) of Kuwait, with an updated checklist

﻿Abstract Thirty-eight species of Isopoda, belonging to 13 families and 29 genera, are listed from Kuwait based on previous literature records (of 17 species) and collections carried out along Kuwait’s coastal and subtidal zones during the present study. The majority of species belongs to the suborder Cymothoida (23), followed by Sphaeromatidea (9), Oniscidea (3), Valvifera (2), and Asellota (1). In total, 25 species were collected and identified from 12 families and 22 genera from Kuwaiti coastal and subtidal areas. These include eight families, 15 genera, and 21 species recorded for the first time from Kuwait. Isopod diversity was highest in the sandy rock areas, including southern Kuwait, particularly in Al-Khiran and Al-Nuwaiseeb, and in mixed habitat (muddy, rocky, and sandy) intertidal transects such as in Failaka Island. The species number increased from the subtidal and lowest zones into the high tidal zone. Isopods were found in sandy substrata, among shells, cobbles, rocks, dead corals, and algae.


Introduction
lose and resting on the surface and others being part of the bedrock. All sandy beaches, rocky beaches, underneath stones, rubble, algal turf, and/or seagrass beds were sampled at each transect. Samples were left in seawater for a day before the fauna was collected from the bottom of the containers. Additionally, fauna living within porous rocks was collected by breaking the rocks with a hammer, placing the resulting debris in isotonic magnesium chloride solution, and collecting the fauna after their relaxation. For soft substrates, a 25 × 25-cm square metal box corer, 15 cm deep, was placed randomly, and sediment was collected by spade from inside the corer. These samples were sieved with seawater using 0.3-mm mesh sieves 45-and 75-cm in diameter, and all sediment and organisms remaining were preserved with 5% buffered formalin for subsequent picking and identification. Isopod specimens were also collected qualitatively from under rocks and among intertidal vegetation. Sand was sieved further samples were collected from rocks broken by a hammer, washing algae, sponges and seagrass, turning over stones, as well as collecting directly in the habitat. Material was rinsed under seawater, and all the washings passed through a 0.3-mm mesh sieve to collect any isopod specimens. The collected isopods were fixed in a 75-95% ethanol solution for subsequent morphological and molecular analyses. All specimens were deposited in the Kuwait Institute for Scientific Research (KISR) reference collection.

Species identification
For identification, morphological studies were conducted using a Leica DFC450 camera mounted on a Leica M125 Stereomicroscope equipped with an imaging system that was employed to obtain colour images of the specimens. For greater depth of field, we merged 10-20 source images of a single specimen taken at different focus distances into one final image with the software LAS V4.5. The final image was edited using Adobe Photoshop. Isopods were identified to the lowest possible taxonomic level.

Results
In total, 25 species representing 12 families and 22 genera were identified from specimens collected in the present study. These species were collected from 31 intertidal transects, including 17 mainland and 14 island transects, and two subtidal sites (Table 2). Sphaeromatidae Latreille, 1825 was the best-represented family with five genera and eight species, followed by the family Cirolanidae comprising five genera and five species. Two species were recorded in each of the families Gnathiidae and Arcturidae. The remaining seven families were represented by single species (  Stebbing, 1904, was collected from ten transects. Interestingly, some species occurred in their 100s from single qualitative samples. Such high numbers for S. sarii and C. delvarii were obtained from randomly collected Sargassum at Al-Nuwaiseeb and Failaka Island. Similarly, high numbers of S. sarii occurred on algal turfs from Kubbar Island. Other species found in high numbers were found from rocks, dead coral, or dead shells and included Gnathia sp., H. mccaini, and Sphaeroma walkeri Stebbing, 1905. Thirty-eight isopod species under five sub-orders, 13 families, and 29 genera are listed in taxonomic order, including Kuwait's previous records (17 species), type localities, and geographical distributions.  (Negoescu, 1980) is the only species of this genus recorded from the nearest locality (Gulf of Aden). The specimens examined here differ from A. motasi in the shape of the pleon with different lengths of pleonites 1-5 (vs. pleonites 1-5 similar to each other in A. motasi), the setation of pereopods, uropods and pleotelson; antenna and antennular articles are narrower than in A. motasi.

Taxonomy
Distribution. New record for Kuwait.

Family Cymothoidae Leach, 1814
Of the cymothoid isopods (parasites of fishes), the following species have been reported by Bowman and Tareen (1983).

Distribution.
A widespread species, recorded in the Indian Ocean from Hong Kong to South Africa (Bowman and Tareen 1983).
Distribution. India (Bowman and Tareen 1983) Family Gnathiidae Leach, 1814 Genus Gnathia Leach, 1814 Gnathia sp. Figure 3A Material examined. Remarks. The specimen is closely related to Gnathia luxata Kensley, Schotte & Poore, 2009 from Khawr Musharraba, Saudi Arabia, Persian Gulf. However, it differs from G. luxata by having a larger and conical mediofrontal process and bifid superior frontolateral process instead of a conical process. Also, the supraocular lobe is blunt and oblique rather than simply rounded.
Distribution. New record for Kuwait.

Discussion
Bowmen and Tareen (1983) were the first to study Kuwait's isopod fauna, recording nine species of Cymothoidae, all ectoparasitic on marine fishes (Table 6). Jones (1986) included six isopod species in his 'Field Guide to the Seashores of Kuwait': Apanthura sandalensis, Ligia exotica, and Cymodoce richardsoniae are reidentified as Amakusanthura sp., L. persica, and C. delvarii, respectively. Moreover, Cymodoce sp. of Jones (1986) is reidentified as Cymodoce fuscina and Tylos sp. is identified as Tylos maindroni. The widespread supratidal isopod Tylos maindroni was previously reported from Kuwait by Taiti and Ferrara (1991). However, Sphaeroma annandalei Stebbing, 1911 was not found in the current study: the known distribution of S. annandalei is from the West Bengal estuaries in India to the Arvandroud (Shatt-Al-Arab) riverbanks between Iran and Iraq (Khalaji-Pirbalouty and Wägele 2010). Two additional species, Arcturinoides angulata and Astacilla mccaini, were collected from Kuwait Bay by Kensley et al. (2007). In monitoring the fauna of recently dredged canals in the Al-Khiran area of Kuwait, Jones and Nithyanandan (2012) discovered and described two new isopod species from Kuwait and mentioned the occurrence of a third, increasing the valid species of Isopoda recorded from Kuwait to 17. With the present survey, we now count 38 species of Isopoda, more than doubling Kuwait's known isopod fauna. Twenty-one of the 25 species collected for this study represent first records for Kuwait (Table 2). Only four of these 25 species were reported previously: Eurydice peraticis, Tylos maindroni, Arcturinoides angulata, and Astacilla mccaini.
The geographical distribution of isopod species in Kuwait waters show very different patterns. The burrowing isopod Sphaeroma walkeri was found living in soft rocks in the high intertidal area of the Al-Zour coast. The type locality of this species is Sri Lanka, and it has been considered restricted to the northern Indian Ocean. This thermophilic species is also tolerant to a range of salinities, and its distribution is worldwide in the tropics (Ríos-Touma et al. 2017). The ranges of other species are also limited to the Indian Ocean. For example, Lanocira gardineri, is widely distributed from western Australia Sidabalok 2011) andthe Maldives, Kenya, andMadagascar (Delaney 1989). Delaney (1989) recorded it from the Khor Abdullah estuary, Iraq, in the northwestern Gulf. Tolerance of salinity fluctuations is believed to be a primary reason for the wide distribution of this species throughout the Indian Ocean. Other species, such as Dynamenella granulata, and Atarbolana exoconta, are widely distributed along the northeastern coast of the Gulf and along the Pakistani coast. Their distribution pattern is similar to some brachyuran decapods as suggested by Apel and Türkay (1999) and Naderloo et al. (2011). According to this distribution pattern, the fiddler crab fauna of the southern and western Gulf is similar in East Africa, the Gulf of Aden, and the Red Sea. At the same time, the fauna of the northeastern parts of the Persian Gulf is also somewhat similar to that of the northeastern Arabian Sea coasts of Pakistan and India. Finally, some of the known species of isopoda (e.g., Heterodina mccaini ; Sphaeroma khalijfarsi, and Sphaeromopsis sarii) are indigenous to the Gulf.
The new results reveal a low species richness of Isopoda in Kuwait waters compared to the adjacent regions of the Indian Ocean. Based on Kensley's (2001) isopod checklist, the Indian Ocean exhibits a high species diversity of more than 1000 species. Of these, 268 species inhabit the Indian coastal region, and fewer than half that number, 121 species, has been recorded from Pakistan's coast by Kazmi et al. (2002). The apparently low species richness of Isopoda in the Kuwait region compared to that of other areas of the Indian Ocean is due to Kuwait's limited coastline, less than 200 km, but also to the Gulf 's young age, less than 6,000 years BP (Sheppard et al. 2010), and the harsh environmental conditions. The age of the environment is an essential factor for the evolution of diversity (Gaston and Chown 1999). The seabed regions of the Gulf presently at depths of 4-6 m have only been submerged for 3,000-4,000 years (Sheppard et al. 2010). Therefore, the current coastal habitat development is comparatively young.
The harsh environmental conditions in Kuwait coastal zone arise from high temperatures and high salinity. Salinities exceed 40 PSU, and summer temperatures often exceed 35 °C. For instance, from 2000 to 2013, the mean seawater temperature in Kuwait Bay was 23.6 °C with a range of 9.7-36.0 °C, and salinity ranged from 30-46 PSU (Al-Yamani et al. 2004). Furthermore, extreme air temperatures with highs up to 55°C in the summer months and winter lows around freezing are known from Kuwait (Jones 1986).
However, a comparison between this study and restricted localities of similar size suggested no lower diversity in Kuwait. Brusca (1987) reported 36 species of marine isopods from the Galapagos. Seventeen species of these were shallow-water species from the littoral to a depth of 100 m. Furthermore, Kensley (1984) identified only 24 species of isopods from the Belizean reef crest. The low species composition of these studies may arise from limited sampling. This study focuses on the Kuwaiti shoreline; therefore, many species living in sub-tidal depths were not collected.
Some isopod species appear to be introduced into Kuwait Bay from outside of the Gulf. For example, Cymodoce fuscina and C. waegelei were found in the subtidal zone of the Iranian and Arabian coasts of the Gulf, but were also recently reported from the Mediterranean basin, Greece (Ulman et al. 2017) and Egypt (pers. obs.). This distribution supports the hypothesis of a human-assisted introduction, such as through ballast water discharge. According to the Public Relations Department of Hormozgan Ports, Iran, ca. 53,000 tanker and cargo ships enter the Gulf annually and ca. 40% of the world's total oil transportation passes through the Strait of Hormuz (Al-Yamani et al. 2015). In this context, ships transport a billion tonnes of ballast water annually, so although this intertidal study was comprehensive, it was only limited to sampling in the intertidal zone. Repeated sampling during different seasons as well as subtidal investigations would certainly increase Kuwait's known isopod fauna.
The present study provides a baseline account of Kuwait's coastal zone isopod fauna. The next step will be evaluating their ecology and conservation status. As Kuwait is one of the major oil exporters, invasive species are a significant issue, mainly due to the discharge of ballast water from oil tankers and cargo ships. Therefore, prevention is crucial for decision-making and implementation of invasion control and detection of new exotics. The results of this study highlight the need for further morphological as well as molecular studies to clarify the taxonomic status of some specimens, and a larger sampling effort in deeper waters of this area. entry, and Miss Muneera Aljeri for preparing the GIS map. We thank especially Dr. James Bishop for his helpful suggestions on the first draft of the manuscript. Dr. Wolfgang Wägele (Zoological Research Museum Alexander Koenig, Bonn), Dr. Gary Poore (Museums Victoria), Dr. Niel Bruce (Queensland Museum), Dr. Lena Hartebrodt (University of Auckland), Dr. Brenda Doti (Universidad de Buenos Aires, Argentina), and Dr. Rachael Peart (National Institute of Water and Atmospheric Research, New Zealand) are thanked for their constructive suggestions and comments that improved the manuscript. Extended thanks to all KISR staff in project FM075C for helping in macrofauna sampling in the field and sample processing in the laboratory.