Research Article |
Corresponding author: Sabrina Lo Brutto ( sabrina.lobrutto@unipa.it ) Academic editor: Charles Oliver Coleman
© 2018 Sabrina Lo Brutto, Davide Iaciofano.
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.
Citation:
Lo Brutto S, Iaciofano D (2018) A taxonomic revision helps to clarify differences between the Atlantic invasive Ptilohyale littoralis and the Mediterranean endemic Parhyale plumicornis (Crustacea, Amphipoda). ZooKeys 754: 47-62. https://doi.org/10.3897/zookeys.754.22884
|
Ptilohyale explorator (formerly Parhyale explorator), described by
An assessment of the nominal valid species belonging to the genus Ptilohyale was carried out and a comparison between the Atlantic Ptilohyale littoralis and the very similar Mediterranean hyalid species, Parhyale plumicornis, is presented based on morphological features and distribution. Due to the invasive ability of Ptilohyale littoralis, a comparison between the two species is necessary.
Atlantic, Hyalidae , Invasive species , Mediterranean Sea, Parhyale plumicornis , Ptilohyale littoralis
Ptilohyale explorator (formerly Parhyale explorator) was described by
List of Parhyale and Ptilohyale species excluded by Barnard’s taxonomy key (
Ptilohyale littoralis (Stimpson, 1853) – formerly Allorchestes littoralis |
Ptilohyale plumulosus (Stimpson, 1857) – formerly Allorchestes plumulosus |
Ptilohyale crassicornis (Haswell, 1879) – formerly Allorchestes crassicornis |
Parhyale inyacka KH Barnard, 1916 |
Ptilohyale barnardi (Chevreux, 1926) nomen dubium – formerly Hyale barnardi |
Ptilohyale ptilocerus (Derzhavin, 1937) – formerly Allorchestes ptilocerus |
Ptilohyale tristanensis (Macnae, 1953) nomen dubium – formerly Allorchestes tristanensis |
Ptilohyale iole (JL Barnard, 1970) – formerly Hyale iole |
Ptilohyale barbicornis (Hiwatari & Kajihara, 1981) – formerly Hyale barbicornis |
As a consequence, Arresti described a new hyalid species under the name Parhyale explorator, and deposited eight males and two females in the laboratory of the University of the Basque Country (Spain; holotype; allotype; six males and one female paratypes), one male paratype in the Carcinology Laboratory of Natural History Museum of Paris (France), and one male and one female paratypes in the Laboratory of Dr. S. Ruffo in the Museum of Natural History of Verona (Italy).
In 2008, Ptilohyale explorator (
Ptilohyale explorator is currently considered a valid species even if some authors have already highlighted the need of further investigations, in light of its high similarity with Ptilohyale littoralis (
To clarify the position of Ptilohyale explorator, here considered species inquirenda, the paratypes deposited at the Natural History Museum of Verona and at the Natural History Museum of Paris were examined, together with some topotypic specimens collected in the type locality of the species, Bay of Arcachon, France. Descriptions and illustrations of current species belonging to the genus Ptilohyale were also consulted, and it was observed that some of them were not ascribable to this genus.
The paratypes of Parhyale explorator (voucher number 330/P) deposited in Sandro Ruffo’s collection of the Museum of Natural History of Verona, Verona (Italy) and the Ptilohyale explorator paratype (voucher number
Additionally, a total of 126 specimens of Ptilohyale sp. (84 females and 42 males) was collected in the intertidal zone associated with mussel beds (Mytilus edulis), from Bay of Arcachon, France (the type locality of Ptilohyale explorator), 43°34’N, 1°14’W (DDM), in October 2015, and fixed in 95% ethanol. Their body lengths, from tip of rostrum to apex of telson, were measured using ImageJ software after placement on graph-paper and photography (FINEPIX S1800, FUJIFILM); pencil drawings were scanned and ‘inked’ using the software Adobe Illustrator CS5. The specimens were identified as Ptilohyale littoralis and deposited at the Museum of Zoology of the University of Palermo (MZPA), Palermo (Italy), Voucher Number MZPA-AMPH-0024.
Descriptions of the 12 world species of the genus Ptilohyale, according to the World Amphipoda Database (
The paratypes of Ptilohyale explorator preserved in the Museum of Natural History of Verona were entire and in good condition for observations (Fig.
Comparison with the description of Ptilohyale explorator (
Diagnostic character states observed in the Ptilohyale explorator (species inquirenda) paratypes stored at the Museum of Natural History of Verona (Italy) and the Natural History Museum of Paris (France), and in the Ptilohyale littoralis sampled in the Bay of Arcachon (France); compared with Arresti’s description of Ptilohyale explorator and Bousfield and Hendricks’s Ptilohyale littoralis description. The table shows the incongruences (*) between the description of Ptilohyale explorator by Arresti and the deposited paratypes.
Characters | Samples of Ptilohyale littoralis (this paper) | Bousfield and Hendricks’s description of Ptilohyale littoralis | Paratypes of Ptilohyale explorator (deposited by Arresti at Museum of Verona) | Paratype of Ptilohyale explorator (deposited by Arresti at Museum of Paris) | Arresti’s description of Ptilohyale explorator |
Antenna II, flagellar articles ventrally setose * | 4–9 | NA | 8 | NA | 10–11 |
Coxal plate I | subquadrate | subquadrate | subquadrate | NA | subquadrate |
Gnathopod I, basis distinct anterodistal lobe | absent | absent | absent | NA | absent |
Peraeopod VII basis* | without strong depression on posterior margin | without strong depression on posterior margin | without strong depression on posterior margin | without strong depression on posterior margin | with strong depression on posterior margin |
Uropod I rami spines* | 3–4 outer; 1–2 inner | 2–3 outer | 3 outer; 2 inner | NA | 6 outer; 2 inner |
Uropod II rami | subequal | subequal | subequal | subequal | subequal |
Uropod III apical spines* | 5–9 | 5–6 | 5–6 | NA | 8–10 |
Following the detailed description updated by
Allorchestes
littoralis
Stimpson, 1853: 49, t 3, fig. 36;
Hyale
littoralis
(Stimpson, 1853)
Hyale prevosti (part) Della Valle, 1893: 519.
Hyale
plumulosa
(Stimpson, 1853)
Plumulohyale
plumulosa
(Stimpson, 1853)
Ptilohyale
littoralis
(Stimpson, 1853)
Parhyale explorator Arresti, 1989: 101–115.
Ptilohyale
explorator
(Arresti, 1989)
Neotype deposited in Canadian Museum of Nature Collection; voucher number CMNC 2002-0071 (
Grand Manan Island (Canada), northern eastern Atlantic coast.
One hundred and twenty-six specimens were collected at the Bay of Arcachon France (43°34’N, 1°14’W), 13October 2015; intertidally, 0 m, on the heavy substrate of the semi-closed beach (MZPA-AMPH-0024).
Male. 11.4 mm length specimen. Antenna II ventral margins of the 5th peduncular article and first 4–9 flagellar articles (other one or two articles with sparse plumose setae) densely covered with plumose setae (brush setae). Palp of maxilla I with median constriction. Coxal plate I sub-quadrate with distinctive cups; Gnathopod I, basis lacking distinct anterodistal lobe (hydrodynamic lobe). Gnathopod II, carpus lobe present in juvenile male and absent on adult male. Coxal plate V posterior lobe smaller than anterior lobe; Peraeopod V, basis rounded. Peraeopod VII slender, basis rounded. Uropod I, peduncle with one distomedial robust seta; rami subequal with 3–4 robust setae on outer ramous and 1–2 robust setae on inner ramus. Uropod II, rami sub-equal in length. Uropod III, outer ramus with 5–9 apical robust setae. Telson acute. Female. Description based on a 10.6 mm length specimen. Gnathopod I, basis with anterodistal lobe.
Northern, western, and eastern Atlantic coasts; north eastern Pacific coast.
The genus Ptilohyale includes 12 species: P. barbicornis (Hiwatari & Kajihara, 1981); P. barnardi (Chevreux, 1925); P. bisaeta (Kim & Kim, 1991); P. brevicrus
Ptilohyale (formerly Parhyale) explorator was described by
Characters used by
Parhyale explorator | Parhyale eburnea Krapp-Schickel, 1974 |
Uropod I with robust seta on peduncle; Rami of uropods I and II with strong dorsal setae. | Uropod I without robust seta on peduncle; Rami of uropods I and II without strong dorsal setae. |
Parhyale explorator | Parhyale plumicornis (Heller, 1866) |
Uropod III with only apical setae; Inner ramous of uropod III poorly defined and fused to the peduncle; Carpus of gnathopod II male with stout process. | Uropod III with apical and dorsal setae; Inner ramous of uropod III well defined and not fused to the peduncle; Carpus of gnathopod II male with evident process. |
Parhyale explorator | Parhyale aquilina (Costa, 1857) |
Uropod I with robust seta on peduncle. | Uropod I without robust seta on peduncle; |
Parhyale explorator | Parhyale ? zibellina (Derzhavin, 1937) |
Uropod III with only apical setae; Inner ramous of uropod III poorly defined and fused to the peduncle; Uropod I with robust seta on peduncle. | Uropod III with apical and dorsal setae; Inner ramous of uropod III well defined and not fused to the peduncle; Uropod I without robust seta on peduncle. |
Parhyale explorator | Parhyale ? iwasai (Shoemaker, 1956) |
Uropod III with only apical setae; Propodus of peraeopod VII without setae on posterior margin. | Uropod III with apical and dorsal setae; Propodus of peraeopod VII with setae on posterior margin. |
Parhyale explorator | Parhyale hawaiiensis (Dana, 1853) |
Inner ramous of uropod III poorly defined and fused to the peduncle; Propodus of peraeopod VII without setae on posterior margin. | Inner ramous of uropod III well defined and not fused to the peduncle; Propodus of peraeopod VII with setae on posterior margin. |
Parhyale explorator | Parhyale penicillata Shoemaker, 1956 |
Inner ramous of uropod III poorly defined and fused to the peduncle; Rami of uropods I and II with strong dorsal setae. | Inner ramous of uropod III well defined and not fused to the peduncle; Rami of uropods I and II without strong dorsal setae. |
Parhyale explorator | Parhyale fascigera Stebbing, 1897 |
Inner ramous of uropod III poorly defined and fused to the peduncle; Rami of uropods I and II with strong dorsal setae. | Inner ramous of uropod III well defined and not fused to the peduncle; Rami of uropods I and II without strong dorsal setae. |
Parhyale explorator | Parhyale of Bulycheva |
Inner ramous of uropod III poorly defined and fused to the peduncle; Basipodite of peraeopod VII with rounded posteroventral lobe. | Inner ramous of uropod III well defined and not fused to the peduncle; Basipodite of peraeopod VII without rounded posteroventral lobe. |
Parhyale explorator | Parhyale basrensis Salman, 1986 |
Inner ramous of uropod III poorly defined and fused to the peduncle; Uropod I with robust seta on peduncle; Propodus of peraeopod VII without setae on posterior margin. | Inner ramous of uropod III well defined and not fused to the peduncle; Uropod I without robust seta on peduncle; Propodus of peraeopod VII with setae on posterior margin. |
Parhyale explorator | Parhyale multispinosa Stock, 1987 |
Inner ramous of uropod III poorly defined and fused to the peduncle; Propodus of peraeopod VII without setae on posterior margin. | Inner ramous of uropod III well defined and not fused to the peduncle; Propodus of peraeopod VII with setae on posterior margin. |
The following character states are considered diagnostic of Ptilohyale explorator: the arrangement of setae on the uropods and the presence of a strong depression on the posterior margin of the basis of peraeopod VII (Table
Recently, Ptilohyale littoralis was declared as a recent alien species spreading along the eastern Atlantic coast since 2009 (
Moreover, Ptilohyale littoralis was recently recorded along the eastern Pacific coast of North America (Campbell River, Vancouver,
The genus Ptilohyale has been diagnosed with plumose setae on ventral margins of antenna II that start at the 5th peduncular segment and distomedial robust seta on peduncle of uropod I. Behaviourally, it is described as saltatory and occurring in brackish and estuarine waters (
Ptilohyale is distributed along both the Atlantic and Pacific coasts (
List of Ptilohyale species exhibiting diagnostic generic characters, and their distribution.
Ptilohyale species | Distribution | Reference |
Ptilohyale barbicornis (Hiwatari and Kajihara, 1981) | Japan Sea, Korea and Japan |
|
Ptilohyale bisaeta (Kim and Kim, 1991) | Japan Sea, Korea |
|
Ptilohyale
brevicrus
|
Japan Sea, Korea |
|
Ptilohyale crassicornis (Haswell, 1879)* | Tasman Sea, Australia; Yellows and Japan Seas, China and Korea |
|
Ptilohyale iole (JL Barnard, 1970) | Pacific Ocean, Hawaii |
|
Ptilohyale littoralis (Stimpson, 1853) | Atlantic Ocean, France, Netherlands, United States and Canada; Pacific Ocean, Canada |
|
Ptilohyale plumulosus ( |
Pacific Ocean, Alaska, Canada and United States |
|
Ptilohyale ptilocerus (Derzhavin, 1937) | Japan Sea, Russia |
|
Due the high connectivity between eastern Atlantic and Mediterranean area, which has already caused a high similarity in the Portuguese and Mediterranean amphipod fauna (
Parhyale plumicornis belongs to the Mediterranean fauna and it is the most similar hyalid species to Ptilohyale littoralis due to the overlapping morphological and ecological characters such as the brush setae along ventral margin of antennae II (
Some morphological character states are presented in Fig.
These two species show a different and non-overlapping distributions: Ptilohyale littoralis was recorded along European Atlantic coast (Fig.
Comparison between Ptilohyale littoralis and Parhyale plumicornis diagnostic characters and distributions. Ptilohyale littoralis: A illustration of male (
The authors are grateful to Dr. Leonardo Latella and Dr. Roberta Salmaso who provided laboratory facilities and access to the Sandro Ruffo’s collection at the Museum of Natural History of Verona; to Dr. Laure Corbari who provided laboratory facilities and access to the collection of the Muséum national d’Histoire naturelle, Departement Systematique et Evolution (Paris, France); to Dr. Benoit Gouillieux of French National Centre for Scientific Research (Paris, France) for providing the authors of this paper with specimens of Ptilohyale littoralis from Arcachon bay. The authors are grateful to reviewers who provided valuable suggestions and comments during revision of the manuscript.
This work was supported by the University of Palermo (Grant FFR 2012/2013).