Biodiversity Data Journal 8: e53864
doi: 10.3897/BDJ.8.e53864
Taxonomic Paper
New records of amphipod crustaceans along the
Israeli Mediterranean coast, including a rare
Mediterranean endemic species, Maera schieckei
Karaman & Ruffo, 1971
Sabrina Lo Brutto‡, Davide Iaciofano‡
‡ Dept. SteBiCeF, University of Palermo, Palermo, Italy
Corresponding author: Sabrina Lo Brutto (sabrina.lobrutto@unipa.it)
Academic editor: Yasen Mutafchiev
Received: 02 May 2020 | Accepted: 24 Jul 2020 | Published: 31 Jul 2020
Citation: Lo Brutto S, Iaciofano D (2020) New records of amphipod crustaceans along the Israeli Mediterranean
coast, including a rare Mediterranean endemic species, Maera schieckei Karaman & Ruffo, 1971 . Biodiversity
Data Journal 8: e53864. https://doi.org/10.3897/BDJ.8.e53864
Abstract
Background
A survey has been carried out at four Israeli rocky sites to evaluate the diversity of the
amphipod fauna on various hard substrates, still scarcely monitored, as potential pabulum
for amphipod crustacean species.
New information
A survey of shallow rocky reefs along the Mediterranean coast of Israel recovered 28
species and integrated the Amphipoda checklist for the country ofIsrael with 12 newlyrecorded species. Such renewed national list includes Maera schieckei Karaman & Ruffo,
1971, a rare species endemic to the Mediterranean Sea, recorded here for the first time
from the southern Levant Basin. The species, described from specimens collected in the
Tyrrhenian Sea in 1970, has been only recorded eight times within the whole
© Lo Brutto S, Iaciofano D. This is an open access article distributed under the terms of the Creative Commons Attribution License
(CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source
are credited.
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Lo Brutto S, Iaciofano D
Mediterranean Sea. A revision of the bibliography on the distribution and ecology of M.
schieckei showed that, although mentioned only for the western Mediterranean basin by
some authors, it is listed in the checklist of amphipods of the Aegean Sea and
neighbouring seas and has been found in the eastern Mediterranean basin since 1978.
Maera schieckei was rarely found in the Mediterranean, one of the most studied marine
biogeographic region as concerns the amphipod fauna; and the species seems to prefer
bays or gulf areas. The role of updating and monitoring faunal composition should be reevaluated.
Keywords
Crustacean amphipods, first records, endemism, Mediterranean Sea, Levant Sea
Introduction
The link between the variation of biodiversity over time and the change of marine
environment detected nowadays is becoming a challenge for different taxonomists'
communities, which aim to re-evaluate the role of taxonomy in actual and historical
collections, mainly if selectively focused on specific taxa (Coll et al. 2010, Beermann and
Franke 2011, Hawkins et al. 2013, Pyke and Ehrlich 2010, Scipione 2013, De-La-OssaCarretero et al. 2010, Costello et al. 2010, Costello 2020). The updating of checklists
(Sorbe et al. 2002, Christodoulou et al. 2013, Ferrario et al. 2017) is now becoming the
prerequisite for ecological and monitoring studies, also in the light of invasive alien species
monitoring (Cao et al. 2003, Servello et al. 2019).
Many habitats often represent a sink for invasive alien species, unknown species (not yet
described) or rare species. Those can be the artificial (Bonifazi et al. 2018) or biogenic
(Plicanti et al. 2016, Bertocci et al. 2017) hard substrates, which can significantly influence
the faunal composition especially in countries, such as Israel, where sandy and muddy
bottoms show a large extension along the coast. In some cases, such scattered habitats
create the favourable conditions for settlement and successive establishment, facilitating
the dispersal of the species also over long distances. An example was the vermetid
platforms habitat whose shape and structure favoured the settlement and successive
increasing density of the lessepsian mussel Brachidontes pharaonis (P. Fisher, 1870)
(Sirna Terranova et al. 2006, Rilov et al. 2004), now widespread in the eastern and central
Mediterranean (Servello et al. 2019).
In the light of that, a survey has been carried out at four Israeli rocky sites to evaluate the
diversity of the amphipod fauna on variegate hard substrates (e.g. rocks, bryozoans,
sponges, seaweeds, coralligenous, plastic objects etc.) as potential pabulum for an
establishment of amphipod crustacean species, still scarcely monitored in scattered areas
of the eastern Mediterranean Sea (Lo Brutto et al. 2016, Lubinevsky et al. 2019, Sorbe et
al. 2002). In European aquatic ecosystems, including the coastal Mediterranean ones,
where biodiversity is changing due to climate change and the invasion of alien species,
New records of amphipod crustaceans along the Israeli Mediterranean coast, ...
3
such a ubiquitous animal group, as amphipods, plays a crucial role in detecting such
changes and deserves relevant attention as fundamental tool in monitoring biodiversity
(Borja et al. 2003, Lo Brutto et al. 2013).
Materials and methods
Four shallow rocky reefs (intertidal - 25 m depth) off the Israeli Mediterranean coast were
sampled by SCUBA diving in 2009: (Rosh Hanikra (RH) (33°04'20.35''N; 35°05'42.10''E);
Haifa (HF) (32°48'47.42''N; 34°57'16.15''E); Caesarea (CS) (32°29'07.34''N;
34°53'19.93''E) and Mikhmoret (MM) (32°24'28.52''N; 34°52'02.38''E) (Fig. 1).
Crustaceans, hydroids, bryozoans, sponges, macrophytes and coraligenous matrices were
collected and preserved in EtOH 70%. Amphipods were examined under a
stereomicroscope and dissected. Body length, from tip of rostrum to apex of telson, was
measured using by ImageJ software after placement on graph paper and photographed
(FINEPIX S1800, FUJIFILM); drawings were scanned and ‘inked’ using Adobe Illustrator
CS5. The specimens of Maera schieckei are deposited at the Museum of Zoology “P.
Doderlein” of the University of Palermo (MZPA), Italy and the Steinhardt Museum of
Natural History (SMNH), Tel Aviv University, Israel.
Figure 1.
Sample sites.
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Lo Brutto S, Iaciofano D
Museum collections
Natural History Museum of Verona (NHMV), Italy: 1216-1218 Maera schieckei one
holotypus, a male dissected into microslides and one male and two females, from Ischia
Island, central Tyrrhenian basin. Museum of the Faculty of Fisheries of Ege University
(ESFM), Turkey: ESFM-MAL/2003-2 Maera schieckei two individuals, but one heavily
damaged from the Aegean coast of Turkey and ESFM-MAL/2005-1839 Maera schieckei
one individual from the Levantine coast of Turkey (Bakir and Katağan 2014). Museum of
Zoology "P. Doderlein" of the University of Palermo (MZPA), Italy: MZPA-AMPH-0027
Maera schieckei seven females from the coast of Israel (this paper).
Data resources
Results
A total of 3106 amphipod specimens were collected. Most specimens (88.6%) were
identified to species (Table 1), the remainder to the genus level (Ampelisca sp., N = 27;
Caprella sp., N = 5; Corophium sp., N = 10; Melita sp., N = 1; Microdeutopus sp., N = 187;
Quadrimaera sp. N = 24) or remained unclassified (N = 27) being immature or damaged.
The most abundant species were tube-dwelling: Leptocheirus guttatus (N = 1227),
Ericthonius brasiliensis (N = 285), Ampithoe ramondi (N = 260), Photis longicaudata (N =
153).
Table 1.
List of species recorded per site, with their abundance, biogeographical distribution1 and record
along the Levantine coast of Turkey (Bakir et al. 2014) and Cyprus (Kocataş et al. 2001).
AO= Atlantic Ocean; Med= Mediterranean Sea; BS= Black Sea; RS= Red Sea; IO= Indian Ocean;
PO= Pacific Ocean; IPO=Indo-Pacific Ocean; *First record in Israeli waters herein presented; 1
References from which distribution has been inferred: Ruffo 1982, Ruffo 1989, Ruffo 1993, Ruffo
1998, Bakir et al. 2014 and Christodoulou et al. 2013.
Species
Rosh
Hanikra
Haifa Mikhmoret Caesarea Distribution1
Apolochus neapolitanus (Della Valle,
1893)*
Ampithoe ramondi Audouin, 1826
1
2
3
AO-Med- IPO
Yes
No
213
46
AO-Med-BSRS-IO
Yes
Yes
18
Med
Yes
Yes
1052
43
AO-Med
Yes
Yes
21
18
Med-IO
No
No
12
Cosmopolitan
No
Yes
Ampithoe riedli Krapp-Schickel,
1968*
Leptocheirus guttatus (Grube, 1864)* 72
60
Bemlos leptocheirus (Walker, 1909)*
Caprella equilibra Say, 1818
Turkey Cyprus
Phtisica marina Slabber, 1769
3
AO- Med-PO
Yes
Yes
Colomastix pusilla Grube, 1861
1
Cosmopolitan
Yes
Yes
New records of amphipod crustaceans along the Israeli Mediterranean coast, ...
5
Species
Rosh
Hanikra
Haifa Mikhmoret Caesarea Distribution1
Turkey Cyprus
Dexamine spinosa (Montagu, 1813)
4
22
AO- Med
Yes
Yes
Tritaeta gibbosa (Spence Bate,
1862)
34
AO- Med
No
Yes
67
AO-Med-RS
Yes
Yes
131
AO-Med-IO
No
Yes
2
Med
Yes
No
2
Cosmopolitan
Yes
Yes
26
Med
Yes
Yes
Elasmopus pectenicrus (Spence
Bate, 1862)
34
AO-Med -RSIO-PO
Yes
No
Elasmopus pocillimanus (Spence
Bate, 1862)
4
AO-RS-IO-Med
No
Yes
Protohyale (Boreohyale) camptonyx
(Heller, 1866)*
7
Ericthonius brasiliensis (Dana,
1853)*
154
Coxischyrocerus inexpectatus
(Ruffo, 1959)
Leucothoe cf. spinicarpa
(Abildgaard, 1789)
2
Lysianassa caesarea Ruffo, 1987
3
23
Maera grossimana (Montagu, 1808)*
39
23
Maera schieckei Karaman & Ruffo,
1971*
5
2
Quadrimaera inaequipes (A. Costa,
1851)*
68
47
AO-Med-BS
Yes
Yes
Med
Yes
No
154
Cosmopolitan
Yes
Yes
10
AO-RS-IO-Med
Yes
Yes
Med
No
No
4
Med
No
No
118
34
AO- Med-IO
Yes
No
10
15
AO- Med
Yes
No
1
21
AO- Med
Yes
Yes
7
AO- Med
Yes
Yes
AO- Med
No
Yes
32
Perioculodes longimanus (Bate &
Westwood, 1868)
Synchelidium longidigitatum Ruffo,
1947*
12
32
18
Megamphopus brevidactylus Myers,
1976
Photis longicaudata (Spence Bate &
Westwood, 1862)
1
Metaphoxus simplex (Spence Bate,
1857)
1
Podocerus variegatus Leach, 1814
Stenothoe tergestina (Nebeski,
1880)*
Stenothoe dollfusi Chevreux, 1887*
5
8
The list of the 28 species (Table 1) integrates with the last checklist published for the whole
Israeli coast by Sorbe et al. (2002) and adds 12 species not recorded yet up to now. Six
are exclusively from the Mediterranean Sea, eight have been already recorded from the
Mediterranean and the Atlantic Ocean and 14 have a wider distribution, including the Red
Sea, the Indian and Pacific Oceans. Two amongst them are considered to have entered
the Mediterranean Sea through the Suez Canal: Elasmopus pectenicrus and Bemlos
leptocheirus (Marchini and Cardeccia 2017) (see Table 1 for details). Specimens of Maera
6
Lo Brutto S, Iaciofano D
schieckei collected at Rosh Hanikra and Haifa constitute the first recorded in the southern
Levant Sea.
Taxon treatment
Maera schieckei Karaman and Ruffo, 1971
Encyclopedia of Life https://eol.org/pages/46530501
Catalogue of Life http://www.catalogueoflife.org/annual-checklist/2019/details/species/id/
ea87d3953b995921e521c66e0eac83a6
World Amphipoda Database http://www.marinespecies.org/amphipoda/aphia.php?
p=taxdetails&id=102825
•
•
•
Nomenclature
Maera schieckei described in Karaman and Ruffo 1971: p. 132, fig. 11-13
Materials
a.
b.
scientificName: Maera schieckei Karaman and Ruffo, 1971; order: Amphipoda; family:
Maeridae; subgenus: Maera; specificEpithet: schieckei; scientificNameAuthorship:
Karaman and Ruffo, 1971; locationID: Rosh Hanikra; waterBody: Mediterranean Sea;
country: Israel; verbatimCoordinateSystem: 33°04'20.35''N, 35°05'42.10''E; eventDate:
2009 June; sex: 5 females; lifeStage: adult; catalogNumber: MZPA-AMPH-0027;
recordedBy: S. Piraino; basisOfRecord: PreservedSpecimen
scientificName: Maera schieckei Karaman and Ruffo, 1971; order: Amphipoda; family:
Maeridae; subgenus: Maera; specificEpithet: schieckei; scientificNameAuthorship:
Karaman and Ruffo, 1971; locationID: Haifa; waterBody: Mediterranean Sea; country:
Israel; verbatimCoordinateSystem: 32°48'47.42''N, 34°57'16.15''E; eventDate: 2009 June;
sex: 2 females; lifeStage: adult; catalogNumber: MZPA-AMPH-0027; recordedBy: S.
Piraino; basisOfRecord: PreservedSpecimen
Description
Body: Body slender, up to 6 mm long (Fig. 2A). Head: Lateral cephalic lobes rounded,
antennal sinus shallow; eyes subrounded. Antenna 1 length about 1/2 body, peduncle
articles 1-2 subequal, article 3 shorter; flagellum with 9 articles, shorter than peduncle;
accessory flagellum with 5 articles. Antenna 2, article 3 of peduncle 2× as long as
broad, article 4 longer than 5, flagellum with 5-6 articles; antennal gland cone reaching
tip of peduncle article 3. Mandibular palp article 1 with distal tooth, article 2 longer than
3. Pereon: Coxae 1-4 short, coxa 1 with anterodistal corner acutely produced.
Gnathopod 1 carpus longer than propodus, propodus ovate; palm oblique, convex;
dactylus with 1 anterior seta. Gnathopod 2 carpus short, propodus large,
subtrapezoidal, twice as long as broad; palm with a median excavation (in male, palm
slightly oblique, with deep medial excavation flanked by 2 strong teeth, defined by 2
spines and a small tooth; dactylus stout, with row of setae on anterior margin (Fig. 2B,
D). Peraeopods 3-4 slender. Peraeopods 5-7 relatively slender, basis almost 2× as
New records of amphipod crustaceans along the Israeli Mediterranean coast, ...
7
long as broad, posterodistal lobe present; dactylus half-length of propodus, nail short,
anterior margin with 1-3 minute teeth. Pleon: Epimeral plates 1-2 with small
posterodistal tooth. Epimeral plate 3 postero-distal corner produced with several teeth
(Fig. 2C). Uropod 1 peduncle with 1 ventro-facial spine, rami subequal. Uropod 2
shorter than uropod 1, rami subequal. Uropod 3 stout, not exceeding tip of uropod 1,
peduncle as long as rami; rami subequal, 1-articulate with distal spines as long as rami.
Telson nearly as long as broad, deeply cleft. Telson lobes bifurcate with 2 long distal
spines (of unequal length) and 3 plumose setae.
Figure 2.
Maera schieckei Karaman & Ruffo, 1971; A. Lateral habitus; B. Second gnathopod female; C.
Illustration of the third epimeral plate, with focus on the postero-distal corner teeth; D.
Illustration of the second gnathopod male (Gn2 male) and female (Gn2 female).
8
Lo Brutto S, Iaciofano D
Distribution
Mediterranean. Italy: Tyrrhenian Sea, Gulf of Naples (Karaman and Ruffo 1971). Spain:
Menorca Channel (Junoy and Viéitez 2008). Algeria: Bay of Oran (Bakalem et al.
2014). Italy: Gulf of Castellammare (Lo Brutto 1991); Turkey: Bay of Izmir (Kocataş and
Katağan 1978, Çinar et al. 2006); Anamur Bay (Bakir and Katağan 2014); Israel: Haifa
Bay (Fig. 3). General: Mediterranean endemic.
Figure 3.
Records of Maera schieckei in the Mediterranean Sea pointed out in the map below.
Details of the records in the Table above, from the following references: Bakalem et al. 2014,
Bakir and Katağan 2014, Çinar et al. 2006, Junoy and Viéitez 2008, Karaman and Ruffo 1971,
Kocataş and Katağan 1978, Lo Brutto 1991.
New records of amphipod crustaceans along the Israeli Mediterranean coast, ...
9
Notes
Five species of Maera have been recorded in the Mediterranean Sea: M. grossimana
(Montagu, 1808), M. hirondellei Chevreux, 1900, M. pachytelson Karaman & Ruffo,
1971, M. schieckei and M. sodalis Karaman & Ruffo, 1971 (accessed at http://
www.marinespecies.org/amphipoda on 05-04-2020). Maera schieckei is distinguished
from congeneric Mediterranean species by the presence of a median U-shaped
excavation in the palm of the second gnathopods and several teeth on the
posterodistal corner of third epimeral plate (character not always appreciable) (Fig. 2B,
C, D). The genus Maera, erected by Leach (1814), is one of the oldest amphipod
genera, which has undergone extensive revision, throughout which Maera schieckei
has maintained its original name and taxonomic position.
The specimens described in this study corresponds to the morphology of Maera
schieckei as described by Karaman and Ruffo 1971 and available also in Ruffo (1982).
Discussion
In spite of their important ecological role within benthic ecosystems, hard bottom
amphipods were rarely investigated on the Mediterranean coast of Israel compared with
the soft-bottom ones (Lubinevsky et al. 2019, Lo Brutto et al. 2016, Sorbe et al. 2002).
Of the 28 amphipod species identified from the rocky reefs, 16 had been previously
recorded (Sorbe et al. 2002) and 12 are new records for Israel (see Table 1), whereas 19
and 20 had been recorded off Cyprus and the Levantine coast of Turkey, respectively
(Bakir et al. 2014, Kocataş et al. 2001 and references herein). Bemlos leptocheirus
(Walker, 1909), occasionally recorded as Mediterranean alien species and Synchelidium
longidigitatum (Ruffo, 1947), an endemic Mediterranean species, are the first records for
the whole Levantine Sea.
Currently, the Mediterranean Sea suffers a high anthropogenic impact due to warming
water, internal and external boat traffic and pollution (Galil 2000, Occhipinti-Ambrogi 2007).
The effects of these activities can be assessed by the spread of some species, for which
the hard substratum can be a point of the pathway. Several studies focused on the spread
of alien species (Marchini and Cardeccia 2017, Servello et al. 2019, Ulman et al. 2017) and
do not often consider the spread of the autochthonous species as an additional significant
signal of changing.
The value of the Mediterranean basin in relation to its role as a hotspot of endemisms can
be enhanced also by the capture of rare species. Maera schieckei is here identified for the
first time along the Israeli coast and it is the most south-eastern record of the species in the
Mediterranean Sea (Fig. 2). This rare Mediterranean endemic species has only been
collected from a few locations, with a low number of specimens found only four times in the
western basin and three times in the eastern basin (Fig. 3). The zoogeography of M.
schieckei is scarcely known and, in some cases, inaccurate. Though Christodoulou et al.
(2013) recently reported the species only present in the western Mediterranean basin and
10
Lo Brutto S, Iaciofano D
it was not listed in the check-list of the north Aegean Sea (Stefanidou and VoultsiadouKoukoura 1995) and Israel (Sorbe et al. 2002), this species has been identified in the
eastern Mediterranean basin since 1978.
Even if this species occurred within a wide geographical range (approximatively all over the
Mediterranean basin), in a wide habitat specificity (different types of substrate), it was
recorded only in bay or gulf areas, often polluted and degraded areas due to the presence
of commercial harbours (see references in Fig. 3); and it remains uncertain if a small-sized
crustacean can spread for hundreds of kilometres along the Mediterranean basin and be
recorded only few times. Studies on its life history needs to better understand dispersal
and establishment. Data suggest it to be an opportunistic species. It is noteworthy to
mention Ferrario et al. (2017) who evaluated the role of harbours in spreading non-native
species; they can be probably significant in driving the range expansion of autochthonous
species as well.
Its small populations make the species being attributed to a rarity with wide geographical
range and low frequency of occurrence (Rabinowitz 1981) and the data deficiency
collocating it as species Not Evaluated (NE), according to International Union for
Conservation of Nature (IUCN) 2001; in this case, the IUCN recommends to give it the
same degree of attention as threatened taxa, at least until the status can be assessed.
A recent estimate fixes the number of benthic amphipod species in the Mediterranean
basin at 449 (Coll et al. 2010). Yet, there is no doubt that this number is an underestimate
and that we lack information for wide swathes of the region as research efforts vary greatly
along the coasts of the Mediterranean and even amongst particular habitats within wellstudied areas (Lo Brutto et al. 2019, Curatolo et al. 2013). A cursory examination of recent
publications reveals the magnitude of the gaps. The number of species and genera new to
science, some described from material collected in well-studied areas, confirm that the
actual number of Mediterranean amphipods is a function of search effort and taxonomic
expertise (Coleman 2015). For instance, a study along the Algerian coast listed 33 new
records (Bakalem et al. 2014) and, even along the Spanish coast, a study of the shallow
soft bottom fauna listed five new records and 14 second records (De-La-Ossa-Carretero et
al. 2010). Records of native ‘rare’ species, whose role in the ecosystem and importance in
bioassessment is still debated (Cao et al. 2003), accrue as well (Scipione 2013). The
Marine Science Framework Directive, with its descriptors for 'good environmental status'
(Review of the Commission Decision 2010/477/EU concerning MSFD criteria), opens new
perspectives to monitor, manage and protect the marine environment. The three criteria for
the assessment of any species are distribution, population size and population condition
and special attention is called to the “integrated understanding of the distribution, extent
and condition of their habitats … to make sure that there is a sufficiently large habitat to
maintain its population, taking into consideration any threat of deterioration or loss of such
habitats.” During an era of intensification of anthropogenic activities which drive complex
and fundamental changes in the Mediterranean Sea (European Environment Agency, EEA
2015), it is important to strengthen and augment the study of the faunal diversity of the
Mediterranean Sea – a sea notable for its endemisms.
New records of amphipod crustaceans along the Israeli Mediterranean coast, ...
11
Acknowledgements
The authors are grateful to Stefano Piraino for collecting samples, to Ahmet Kerem Bakır
for information on Turkish samples; to Traudl Krapp-Schickel and Bella Galil who
commented on the text before submission and to an anonymous reviewer, for helpful
comments.
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