The diaptomid fauna of Israel (Copepoda, Calanoida, Diaptomidae), with notes on the systematics of Arctodiaptomus similis (Baird, 1859) and Arctodiaptomus irregularis Dimentman & Por, 1985 stat. rev
© Marrone et al.; licensee Springer. 2014
Received: 25 June 2014
Accepted: 14 November 2014
Published: 12 December 2014
To date, only scarce information is available about the diaptomid copepods of the Middle East despite the ecological and biogeographical importance of the family Diaptomidae in the inland waters of the Holarctic region. Moreover, the taxonomic status of some of the taxa occurring in the area is in need of revision. We studied crustaceans collected from temporary and permanent lentic water bodies in Israel with the aim of providing an updated census of the diaptomid copepods occurring in the country. Furthermore, we morphologically and genetically analysed samples of Arctodiaptomus similis s.l. to shed light on its taxonomy.
Five diaptomid taxa were collected during this survey. Among these, Phyllodiaptomus blanci is new for the country and the whole circum-Mediterranean area and might be an allochthonous species of eastern origin. Within the collected samples, we singled out two parapatric groups of populations within A. similis s.l.; these consistently differ both based on morphology (chaetotaxy of the left male antennule) and molecular data (divergence over 17% at the mitochondrial gene for the cytochrome b). We thus attribute the full species rank to Arctodiaptomus irregularis Dimentman & Por, 1985 stat. rev., originally described as a subspecies of the widespread species Arctodiaptomus similis (Baird, 1859).
We critically evaluated all species hitherto reported for Israeli inland waters. Considering both the confirmed literature data and the new findings, Israeli diaptomid fauna is composed of at least seven species. However, the need for further surveys in the Middle East and for detailed systematic revisions of some controversial taxa is stressed. Our results on the systematics of A. similis s.l. illustrate the importance of implementing molecular analyses when investigating diversity patterns of groups which are difficult to resolve based on morphology alone.
Representatives of the copepod family Diaptomidae often dominate the lentic inland water bodies of the Holarctic, Oriental, and Afrotropical biogeographical regions, being a key taxon in many lacustrine and pond ecosystems (Dussart and Defaye , ). Species of this family are as a rule characterised by limited distributional ranges, which are significantly constrained by the legacies of historical biogeographical events (Leibold et al. ). However, an ever-increasing corpus of molecular evidence suggests that our knowledge on diaptomid species distributions and biogeography is currently hampered by a gross underestimation of the actual diversity of the group (e.g., Marrone et al. , and references therein). In the inland waters of the Mediterranean area, about 100 diaptomid species belonging to 14 genera are currently reported to occur (Dussart and Defaye ), but the information available for certain regions is far from being satisfactory (cf. Marrone ).
To date, uneven information is available on the inland water calanoid copepod fauna of the Middle East. While the diaptomid faunas of Turkey (e.g., Gündüz ; Ustaoğlu ; Ustaoğlu et al. ) and Iran (e.g., Brehm ; Löffler , ) are relatively well-known, only scarce and anecdotal records are currently available for other countries of this region (e.g., Gurney ; Spandl ; Kiefer [1978b]; Dumont , ; Khalaf ; Mohamed and Salman ). The Israeli diaptomid fauna is quite a peculiar case: although several papers and reviews are available (e.g., Baird ; Richard ; Kiefer ; Yaron ; Dimentman and Por , Azoulay , and references therein), only five diaptomid taxa are currently listed for the country; this seems quite a species-poor fauna when compared to other circum-Mediterranean regions of comparable area, where usually about 9 to 14 diaptomid species are present (e.g., Ruffo and Stoch ; Marrone et al. ; Marrone ; Turki and Turki ; Alfonso and Belmonte ). Furthermore, the taxonomical validity of some ‘forms’ or ‘subspecies’ described in the past decades based on Israeli specimens is rather controversial, and the presence itself of some taxa in the country is in need of confirmation, thus casting further uncertainty on the actual composition of the Israeli diaptomid fauna.
We studied plankton samples collected in Israeli inland waters between 2003 and 2011 in order to update the available information on the composition and distribution of diaptomid copepods in the country. Furthermore, we genetically analysed several populations of Arctodiaptomus similis s.l. to test the hypothesis that two parapatric groups of populations differing in morphology, observed in our dataset, actually represent distinct evolutionary lineages of species rank.
Samples are stored in the crustacean collection of Federico Marrone and are available for loan on request. Voucher specimens from the type localities of Arctodiaptomus similis (Baird, ) and Arctodiaptomus irregularis Dimentman & Por,  stat. rev. have been deposited in the collection of the Smithsonian Institution (National Museum of Natural History) in Washington DC, USA, with the catalogue numbers USNM #1226919 and USNM #1226920.
Thirteen specimens of A. similis s.l. from various regions of Israel and two congeneric species to be used as out-groups (Arctodiaptomus cf. stephanidesi (Pesta, 1935) and Arctodiaptomus alpinus (Imhof, 1885), both collected in Italy) were analysed genetically by amplifying and sequencing a 329-bp long fragment of the mitochondrial gene for the cytochrome b (Cyt-b), a molecular marker which is known to be informative on the phylogeography and the molecular systematics of closely related diaptomid taxa (e.g., Staton et al. ; Thum and Derry ; Thum and Harrison ; Marrone et al. , ). Genetic analyses were performed following the protocols and procedures described in Marrone et al. (, ), with the aim of investigating the molecular structuring of the taxon and to compare it with the observed patterns of morphological variation. Chromatograms were imported and edited with Chromas Lite 2.01 (Technelysium Pty. Ltd., South Brisbane, Australia) and aligned with BioEdit (Ibis Biosciences, Carlsbad, CA, USA) (Hall ). The quality of the obtained sequences was checked with Sequence Scanner v1.0. Only sequences with continuous reads of high quality bases were used; when the sequences were not of sufficient quality, the reverse complement sequences were also obtained. MEGA 5 (Tamura et al. ) was used to translate the Cyt-b sequences to amino acids in order to check for the possible presence of frameshifts or stop codons, which would indicate the presence of sequencing errors or pseudogenes. The sequences were deposited in GenBank under Accession Numbers KM488608 to KM488622.
Bayesian inference (BI) of phylogeny and maximum likelihood (ML) analyses were performed on the Cyt-b dataset as implemented by MrBayes 3.2.1 (Ronquist et al. ) and PhyMl v.3 (Guindon and Gascuel ), respectively. Both analyses were performed using a Hasegawa, Kishino, and Yano model of sequence evolution for molecular data with a proportion of invariable sites (HKY + I), as selected by the Akaike information criterion in MrModeltest 2.2 (Nylander ). Node supports were evaluated by their posterior probabilities in the BI tree and with 1,000 bootstrap replicates in the ML analysis. The BI analysis was performed with two independent runs of 2,000,000 generations and four Markov chains using default heating values. Trees and parameter values were sampled every 100 generations resulting in 20,000 saved trees per analysis. An initial fraction of 5,000 trees (20%) was conservatively discarded as ‘burn-in’. For all analyses, standard deviation of split frequencies reached values lower than 0.0065, and values of the potential scale reduction factor (PSRF) were between 1.0 and 1.004 for all parameters, indicating convergence of the runs.
In order to compare the observed molecular distances with those available in literature for other diaptomid taxa, uncorrected molecular distances among specimens and between groups were calculated in PAUP 4.0b10 (Swofford ).
List of the sampled localities with diaptomid presence
Site name - district
Lake Ram - Golan Heights
14 March 2011
Pool at El Rom - Golan Heights
9 March 2010
Bab El Hawa pool - Golan Heights
9 March 2010
Orvim reservoir - Golan Heights
7 March 2010; 14 March 2011
Khusniya pool - Golan Heights
8 March 2010
Vernal pools close to Daliyot Reservoir, Golan Heights
8 February 2003
Lehavot Habashan - Northern District
15 March 2011
Mashkena pool - Northern District
6 March 2010; 17 March 2011
Ditch at Atlit - Haifa District
30 January 2003
Dora pool - Haifa District
7 March 2011
Ga'ash pool - Haifa District
7 March 2011
Pond in Yarkon park - Tel Aviv District
29 January 2003
Pond in Holon - Tel Aviv District
26 January 2004
Moshav Ishrash - Center District
Rainwater-flooded field near Tel Ashdod - Southern District
22 January 2004
Mamilla pool - Jerusalem District
4 March 2011
Small pools in Sde Boker, Vadi Zin - Southern District
9 March 2011
Pool in Makhtesh Ramon crater - Southern District
12 March 2010; 17 March 2011
Checklist of Israeli Diaptomidae (Copepoda, Calanoida)
Sites of occurrence (present study)
Hemidiaptomus (Hemidiaptomus) gurneyi canaanita Dimentman & Por, 
ISR02, ISR05, ISR06, ISR11, ISR14
2, 6, 8, 9, 11, 13
a Eudiaptomus drieschi (Poppe & Mrázek 1895)
Arctodiaptomus (Arctodiaptomus) similis (Baird, )
ISR07, ISR08, ISR09, ISR10, ISR11, ISR13, ISR15, ISR16
1, 2, 3, 4, 5, 6, 7, 8, 9, 10, 13
Arctodiaptomus (Arctodiaptomus) irregularis Dimentman & Por, 
ISR02, ISR03, ISR04, ISR05, ISR06
a Arctodiaptomus (Rhabdodiaptomus) salinus (Daday, 1885)
b Phyllodiaptomus blanci (Guerne & Richard, 1896)
Neolovenula alluaudi (Guerne & Richard, 1890)
ISR01, ISR03, ISR17, ISR18
8, 9, 12, 13
A. similis s.l. populations based on setae number on 13th, 15th, and 17th segments of left male antennule
ISR01 - Golan Heights
ISR02 - Golan Heights
ISR03 - Golan Heightsa
ISR04 - Golan Heights
ISR05 - Golan Heights
ISR06 - Golan Heights
ISR07 - Northern District
ISR08 - Northern District
ISR11 - Haifa District
ISR13 - Tel Aviv District
ISR15 - Southern District
ISR16 - Jerusalem Districtb
The mean intra-clade uncorrected molecular distance was 1.6% (ranging from 0.9% to 3%) within the Israeli clade and 0.7% (ranging from 0% to 0.9%) within the Golan clade. The average uncorrected molecular distance between the two clades was 17.3%.
Checklist and distribution
Five diaptomid taxa were collected in the present survey; in addition to these, Eudiaptomus drieschi and Arctodiaptomus (Rhabdodiaptomus) salinus have to be considered parts of the Israeli diaptomid checklist based on bibliographical evidence. The reports of Arctodiaptomus (Arctodiaptomus) wierzejskii and Eudiaptomus gracilis in the country are in need of being substantiated and are possibly erroneous (see comments below). At the present state of knowledge, the checklist of Israeli diaptomid copepods is thus composed of seven taxa (Table 2).
The paradiaptomid N. alluaudi, which was previously known in the country only from the Sinai and Negev deserts (Dimentman and Por ), was collected in our survey both in the Negev desert and on the Golan Heights, thus widening to the north the distribution of this species in the country. This finding was recently anticipated by Alfonso and Belmonte () in a review on N. alluaudi distribution.
Hemidiaptomus (Hemidiaptomus) gurneyi canaanita is an endemic taxon whose distinct status was confirmed by molecular analyses, in spite of the morphological identity of Israeli populations with those collected in the central Mediterranean, including the type locality of the species (Marrone et al. ). Hemidiaptomus gurneyi s.l. is characterised by a sharply disjointed distribution, with the populations belonging to Hemidiaptomus gurneyi gurneyi occurring in the central Mediterranean area (from eastern Algeria to the Balkan Peninsula), and those belonging to the subspecies Hemidiaptomus gurneyi canaanita occurring in Israel (Marrone et al. ). The report of the presence of the species in Hungary (Dussart and Defaye ) is not supported by any reference or sample (cf. Kiefer [1978a]; Petkovski ; Stella ; Dussart ; Borutzky et al. ; Marrone et al. ); it has thus to be considered a lapsus calami of the authors. In our survey, H. gurneyi canaanita was collected in water bodies of central and northern areas of Israel, which is in good accordance with the distribution pattern described for the species by Dimentman and Por (). Based on the available drawing, the report of the occurrence of a female Hemidiaptomus specimen in ‘Birket de Banias’ (Richard ), originally attributed to Hemidiaptomus amblyodon (Marenzeller, 1873) by the author, can in fact be unequivocally ascribed to H. gurneyi canaanita.
Two species belonging to the genus Eudiaptomus are to date reported for the country: Eudiaptomus gracilis (G.O. Sars, 1863) and Eudiaptomus drieschi (Poppe & Mrázek, 1895), both of them for Lake Kinneret (see Azoulay , and references therein). As it has already been stressed (e.g., Dimentman and Por ; Azoulay ), it is possible that the early reports of E. gracilis for Lake Kinneret should be in fact ascribed to a misidentification of E. drieschi, and that E. gracilis should thus be excluded from Israeli diaptomid fauna. However, conclusive evidence is not available, and the report of occurrence of this euryecious diaptomid species in the lake cannot be excluded. Eudiaptomus species were observed in Lake Kinneret only since the 1960s onwards, although the Lake Kinneret zooplankton was investigated by frequent sampling since the early 20th century. This suggests a relatively recent colonization of the lake from an unknown source area, possibly corresponding with various anthropogenic changes of the Lake Kinneret system which took place since the 1950s, including intensive stocking of fish exotic to the lake (e.g., Gophen ). No Eudiaptomus species were collected during our survey; however, we did not sample this large freshwater lake.
Richard () reported the occurrence of Arctodiaptomus (Rhabdodiaptomus) salinus from ‘Birket Abo-Zeineh’, a brackish marsh close to the northern coast of Lake Kinneret. The species is considered part of the Israeli fauna by Ranga-Reddy () and Dussart and Defaye (). Dimentman and Por () considered that this finding needed to be substantiated; however the presence of A. salinus in Israel is rather likely as this halophilous taxon is characterised by a broad circum-Mediterranean and Palaearctic distribution, including several countries in the Middle East (Dussart and Defaye ; Dumont ). Inland endorheic water bodies and salty coastal marshes and lagoons are the habitats to be sampled in order to find new evidence for the presence of this taxon in Israel.
Arctodiaptomus (Arctodiaptomus) wierzejskii was xerroneously cited to be present in Israel by Yaron (), who misidentified A. similis s.l. for this species (this erroneous datum was then unfortunately perpetuated by Dussart and Defaye ). The mistake was possibly due to the use of the trinomen Diaptomus wierzejskii palaestinensis by Kiefer () for the diaptomid population inhabiting ‘Birket Mamilla’ and by Fischer () for the populations inhabiting some fish ponds throughout the country. D. wierzejskii palaestinensis is in fact a synonym of Arctodiaptomus similis (Kiefer , ).
The diaptomin taxon Arctodiaptomus (Arctodiaptomus) similis s.l. (Baird, ) inhabits both permanent and temporary water bodies of central and northern parts of the country, proving to be the commonest calanoid copepod occurring in Israeli inland waters. In spite of its abundance, the taxonomy of A. similis s.l. is to date controversial. Currently, two taxa of subspecific rank are ascribed to A. similis s.l., but the taxonomical arrangement of the species is in need of revision (cf. Ranga-Reddy ; Dussart and Defaye ). The species was described from Israel by Baird () and later reported to occur throughout Southwestern Asia and Eastern Europe (e.g., Richard ; Petkovski ; Kiefer , , ; Dimentman and Por , Azoulay , Dussart and Defaye ). Some authors reported the presence of the species in Sardinia (Kiefer [1978a]; Dussart and Defaye, ) without providing any drawing or precise locality data; furthermore, extensive limnological surveys carried out in the island (e.g., Stella ; Stella et al. ; Stella and Margaritora [1975/1976]; Fadda et al. ; Marrone and Stoch, unpublished data) only recorded the presence of the congeneric species A. salinus and A. wierzejskii, and no evidence of the presence of A. similis s.l. was ever collected. Thus, the report of the presence of the species in Sardinia is almost certainly erroneous, and the species is currently not considered part of the Italian copepod fauna (Stella ; Ruffo and Stoch ). The Israeli populations of A. similis s.l. studied by us could be split into two parapatric groups (Table 3), differing in the chaetotaxy of the left male antennule (Figure 2C,G) and in the mtDNA Cyt-b sequences (Figure 3).
Taxonomical notes on Arctodiaptomus(Arctodiaptomus) similis(Baird, ) and Arctodiaptomus(Arctodiaptomus) irregularis Dimentman & Por,  stat. rev
A. similis was described by Baird () based on specimens raised from dried mud collected in the pool of Gihon in Jerusalem (now Birket Mamilla pond). Later on, Kiefer () described D. wierzejskii palaestinensis based on specimens collected in Birket Mamilla, but this taxon was later synonymised, by the author himself, with A. similis (see Kiefer  for an annotated list of the synonyms of the species). In the same work, Kiefer () stressed the variability of the ornamentation and chaetotaxy of the male antennule and established two infrasubspecific formae based on the presence of two versus one setae on the 13th, 15th, and 17th segments of the left male antennule (forma saetosior) and on the presence of a rod-like instead of claw-like process of the antepenultimate segment of the right male antennule (forma irregularis). Based on this last character, and on the presence versus absence of a tooth on the 14th segment of the right male second antenna, Dimentman and Por () established the subspecies Arctodiaptomus similis irregularis, whose type locality lies in Birket Bab el Hawa, on the Golan Heights. However, it has to be stressed that several authors (Richard ; Petkovski ; Kiefer , [1978a]) reported the presence of a pronounced intra-populational morphological variability for the morphological characters which, according to Dimentman and Por (), should allow unequivocal assignment of each population to one or the other subspecies.
In good accordance with Richard () and Petkovski (), the A. similis s.l. populations studied by us showed a noteworthy variability in the morphology of the right male antennule; although the populations from the Golan Heights show, as a rule, a smaller tooth on the 14th segment (Figure 2D) and a blunter process on the antepenultimate segment of the antennule (Figure 2B), exceptions and intermediate forms were observed. Conversely, the number of setae on the 15th and 17th segments of the left male antennule allowed us to soundly distinguish the specimens collected throughout the country in two groups (Table 3). This observation is in sharp contrast with Kiefer (, [1978a]), who stressed a significant variability for the chaetotaxy of the segments 13th, 15th, and 17th both at intra- and inter-population level.
The two groups of populations singled out based on the number of setae present on the 15th and 17th segments of the left male antennule (Figure 2C,G) are parapatric and in good accordance with the observed molecular clustering in two clades of the studied populations (Figure 3). The molecular distance observed between the two groups is of the same order of magnitude of those observed among different lineages deserving the status of cryptic species within other diaptomid species, like Skistodiaptomus pallidus (14.3% to 17.2%, Thum and Harrison ), Hemidiaptomus ingens (18%, Marrone et al. ), and Onychodiaptomus sanguineus (22%, Thum and Derry ); furthermore, a high sequence similarity was observed within each of the two clades.
Our morphological and genetic data thus support a classification of Israeli A. similis s.l. into two main lineages of species rank. Accordingly, two species are present in Israel: A. similis (Baird, ) (Figure 2E,F,G,H), inhabiting the whole country with the exception of the Golan Heights, and A. irregularis Dimentman & Por,  stat. rev. (Figure 2A,B,C,D), apparently confined to the Golan Heights.
Arctodiaptomus similis (Baird, )
Type locality: Mamilla pool (Jerusalem District; ISR16)
syn.: Diaptomus wierzejskii palaestinensis Kiefer, 
Arctodiaptomus similis similis Dimentman & Por, 
A. irregularis Dimentman & Por,  stat. rev.
Type locality: Bab el Hawa pool (Golan Heights; ISR03)
syn.: Arctodiaptomus similis forma irregularis Kiefer, 
Arctodiaptomus similis irregularis Dimentman & Por, 
The two taxa Arctodiaptomus similis var. smirnovi Brehm, 1938 and Arctodiaptomus spectabilis Mann, 1940 are junior synonyms of A. similis s.l. (cf. Kiefer, ), but at the current state of knowledge, it is impossible to soundly ascribe them to, or differentiate from, either A. similis s.s. or A. irregularis. The distribution of these two taxa in the Middle East and Eastern Europe is in fact to date unknown. Interestingly, a parapatric distribution of two distinct lineages similar to that within A. similis has also been observed in Israeli populations of the cladoceran Daphnia (Ctenodaphnia) chevreuxi Richard, 1896: one lineage was only detected in lowland pools in the Mediterranean coastal plain, while a genetically distinct lineage was widespread in the Golan Heights but not found elsewhere (A. Petrusek, unpublished data).
In the light of a critical review of the existing and new data, the calanoid family Diaptomidae proved to be better represented in Israel than previous literature data suggested, with seven species certainly occurring in the country. This value is close to that observed in other circum-Mediterranean countries of comparable size (e.g., Marrone ). Furthermore, it also needs to be stressed that representatives of the genus Metadiaptomus, known to occur throughout the arid regions of the Mediterranean and Black Sea (e.g., Kiefer [1978b]; Jaume ; Rayner ; Marrone and Naselli-Flores : Samchyshyna , and references therein), although never recorded to date in Israel, are likely to also occur in the country; for instance, Metadiaptomus chevreuxi (de Guerne & Richard, 1894) is known from Jordan, and Metadiaptomus mauretanicus Kiefer & Roy, 1942 from Egypt (Dumont , ).
Based on the updated checklist of Israeli diaptomids (Table 2), counts of endemic (i.e., H. gurneyi canaanita, A. irregularis) and eastern taxa (A. similis, E. drieschi, P. blanci) in this country are comparable to counts of taxa with wider distribution areas (i.e., Arctodiaptomus salinus and Neolovenula alluaudi). Unfortunately, due to a lack of sound checklists for most of the other Middle East countries, it is currently difficult to understand the biogeographic affinities of the Israeli calanoid copepod fauna.
The possible presence of an allochthonous species in the country is in accordance with the ever-growing number of successful biological invasions affecting the freshwater zooplankton in the last decades. Such phenomenon is becoming increasingly important in the Western Palaearctic region, where the records of allochthonous calanoid copepods are increasing at a fast pace (e.g., Ferrari et al.; Rossetti et al. ; Alfonso and Belmonte ; Brandorff ; Alfonso et al. ).
Nicolas Rabet (National Museum of Natural History, Paris, and University Pierre and Marie Curie, Paris) kindly provided the diaptomid sample from Moshav Ishrash (Center District). Tereza Petrusková helped during the sampling campaigns. T. Chad Walter (National Museum of Natural History, Washington DC) kindly provided the catalogue numbers of the copepod specimens deposited in the collection of the Smithsonian Institution. We thank Fabio Stoch (University of L'Aquila, L'Aquila) for his help in the correct application of the International Code of Zoological Nomenclature and Jessica Richardson for language corrections.
The research was partially supported by the ‘Fondi di Ateneo’ (60%) of the University of Palermo.
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