Phylogeny and taxonomy of the enigmatic genus Petalidium (Decapoda, Sergestidae), with biological remarks

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1 bs_bs_banner Zoological Journal of the Linnean Society, 015, 174, With 8 figures Phylogeny and taxonomy of the enigmatic genus Petalidium (Decapoda, Sergestidae), with biological remarks ALEXANDER L. VERESHCHAKA* and ANASTASIA A. LUNINA Institute of Oceanology, Russian Academy of Sciences, Moscow, Russia Received 17 September 014; revised 9 December 014; accepted for publication 13 January 015 Petalidium (Decapoda: Dendrobranchiata: Sergestidae) is one of the least known genera of pelagic decapods. On the basis of collections taken during Dana Expedition 190 and , we revise the morphology of the genus. To understand the taxonomic status and position of Petalidium within other sergestid genera, we used 150 morphological characters (17 binary, 3 multistate). Three recognized species of Petalidium and eighteen type species representing all other genera of Sergestidae were included as terminals. Characters were polarized using Lucifer typus (Luciferidae: Sergestoidea) and Aristeomorpha foliacea (Aristeidae: Penaeoidea) as the outgroups. Phylogenetic analysis revealed monophyly of Petalidium comprising three species: Petalidium foliaceum Bate, 1881; Petalidium obesum (Krøyer, 1859); and Petalidium suspiriosum Burkenroad, Phylogenetic analyses also revealed possible monophyly of the clade including 15 new genera of the former Sergia and Sergestes and the position of Lucifer (family Luciferidae) within the clade Sergestidae. These results highlight necessity of future phylogenetic analyses of the remaining genera Lucifer, Acetes, Peisos, and Sicyonella involving all species of these genera and promise interesting changes for the classification of Sergestoidea. Morphological trends within Sergestoidea are discussed, and an emended diagnosis of Petalidium and diagnoses of the species it includes are given. All species are illustrated and biology of the genus is discussed. Keys to species of Petalidium based upon new information are presented.. doi: /zoj.143 ADDITIONAL KEYWORDS: cladistic analysis morphological characters pelagic decapods. INTRODUCTION Sergestid shrimps are pelagic crustaceans that represent an important food resource for other marine animals, such as fish, whales, and other crustaceans (Omori, Kawamura & Aizawa, 197). Some species of the genera Eusergestes, Lucensosergia, and Acetes may reach such high abundance and biomass that they are subject to commercial exploration (Omori, 1974; Mutoh & Omori, 1978). Despite their panoceanic distribution and importance in both marine and human economies, Sergestidae is one of the least understood groups of Decapoda. The family comprises: (1) seventy-one *Corresponding author. alv@ocean.ru species of the former genus Sergestes sensu H.J.H. Hansen (1896, 1903), now split into fifteen genera (Vereshchaka, Olesen & Lunina, 014); () fourteen species of Acetes (Omori, 1975); (3) three species of Petalidium (Hansen, 1919, 19; Burkenroad, 1937); (4) three species of Sicyonella (Hansen, 1919; Fukuoka, Tamaki & Kikuchi, 005); and (5) one species of Peisos (Burkenroad, 1945). The taxonomy of Sergestidae had become entangled until recently, for historical and other reasons (Vereshchaka, 1994, 000, 009) but has now been more or less disentangled in a series of revisions that include diagnoses and redescriptions of most genera and species. In chronological order, these revisions are: Acetes (Omori, 1975), Sergia (Vereshchaka, 000; Vereshchaka et al., 014), Sicyonella (Fukuoka et al., 005), and Sergestes 459

2 460 A. L. VERESHCHAKA AND A. A. LUNINA (Vereshchaka, 009; Vereshchaka et al., 014). Only the deep-sea genus Petalidium remains unrevised. The genus Petalidium (Fig. 1A) was established by Bate (1881) for a species from the Southern Ocean, which he called Petalidium foliaceum. Later, Hansen (1896, 1903) found that two previously described species, Sergestes obesus Krøyer, 1859 from the Central Atlantic and Sergestes sanguineus (Chun, 1889), were synonymous and should also be placed in the genus Petalidium and be named Petalidium obesum (Krøyer, 1859) (the gender of the genus Petalidium Spence Bate, 1881 was treated as masculine by Perez-Farfante & Kensley, 1997; sensu De Grave & Fransen, 011, we treat it as neuter, in recognition of the name of the type species P. foliaceum and of the other species assigned to this genus). Almost half century later Burkenroad (1937) described the third species, Petalidium suspiriosum, based upon two female specimens taken in the eastern Pacific Ocean off Mexico. The species was redescribed with figures of the petasma and other details by Wasmer (1974). Studies of Petalidium and understanding its place within the family Sergestidae face three problems: 1. Information concerning the genus Petalidium is scattered, having been published over a period of more than a century. Information on many characters was absent (e.g. the petasma) or incomplete and fragmentary (particularly the cervical sulcus and the presence or absence of supraorbital and hepatic spines and of a second tubercle on the ocular peduncle). To highlight the problem, Burkenroad (1937) drew together information on P. foliaceum from descriptions of the species by Bate (1888), Hansen (1903), Illig (1914, 197), and Stebbing (1914) and concluded that with regard to the other named species of the genus... the available information is... so contradictory as perhaps even to indicate the existence of still another species of Petalidium.. All specimens are very fragile and deep-living; they are much mutilated during retrieval by trawls; most thoracic appendages, from the third maxillipeds to the last pereopods, antennae, and even apical parts of the uropods and scaphocerites, are missing. The usual state of specimens is illustrated by the preserved syntype of P. suspiriosum (Fig. 1B). Deepsea samples with Petalidium are quite rare and the discovery of any specimen with thoracic appendage present is fortunate. The detailed morphology of the genus was originally reconstructed from available material. The morphology of P. obesum was detailed by Hansen (19), whose material fortunately included one well preserved immature male, and that of P. suspiriosum by Wasmer (1974) who based his description on extensive collections taken off Oregon (all the individuals used were imperfect but it was possible to assemble undamaged parts from among them). 3. The presence of three different types of characters that demonstrate nonparallel phylogeny (Vereshchaka et al., 014): (i) traditional external body characters used in carcinology (spines, setae, etc.); (ii) a male clasping organ (modified part of Antenna I); and (iii) a petasma (male copulatory organ), which may differ in similar species and be similar in distant species. The present study attempts to overcome the problems outlined above by examining the available information on the morphology and species composition of Petalidium, as well as by analyzing the position of this genus within Sergestidae on the basis of a phylogenetic analysis, and then summarizes the available information about the biology of the species. MATERIAL AND METHODS MATERIAL The results were based upon studies of the Danish collections taken during the Dana I (190 ) and Dana II (198 30) Expeditions (1409 samples from temperate and tropical waters of the Atlantic, Indian, and Pacific Oceans were examined). The specimens of Petalidium were sorted and identified; individuals were selected for further examination and illustration using a dissection microscope and photographed. In addition to Dana material, we have examined specimens sent on request from the British Museum (Natural History), Museum National d Histoire Naturelle, Paris, Naturhistoriska Riksmuseet, Sweden, US National Museum, and Yale Peabody Museum, USA. TERMINAL TAXA Three recognized species of Petalidium and eighteen type species representing all other genera of Sergestidae were included as terminals. Character state scoring for each species was derived from examination of specimens (see Supporting information, Appendix Sl). Characters were polarized using Lucifer typus H. Milne Edwards, 1837 (the type species for Lucifer Thompson, 189, family Luciferidae De Haan, 1849, superfamily Sergestoidea Dana, 185) and Aristeomorpha foliacea (Risso, 187) (the type species for Aristeomorpha Wood-Mason, 1891, family Aristeidae Wood-Mason, 1891, superfamily Penaeoidea Rafinesque-Schmaltz, 1815), as the outgroups. MORPHOLOGICAL CHARACTERS One hundred and fifty morphological characters (3 multistate) used in the analysis are listed in the Supporting information (Appendix S), along with character states, brief descriptions, and references to

3 PHYLOGENY AND TAXONOMY OF PETALIDIUM 461 1A 1B mm 5mm 1C mm LI LT 1D PV LC LAc LA PU 1mm LA LAc PV LC LT 1E LI Figure 1. A, Petalidium obesum, male, ZMUC-CRU B, Petalidium suspiriosum, YPM IZ , female, syntype. C, P. obesum, male clasping organ. D, Petalidium foliaceum, petasma. E, P. obesum, petasma. LI, lobus inermis; LT, lobus terminalis; PV, processus ventralis; LC, lobus connectens; Lac, lobus accessorius; LA, lobus armatus; PU, processus uncifer.

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5 PHYLOGENY AND TAXONOMY OF PETALIDIUM 463 A B LAc LA RESULTS Analysis 1 with L. typus as the outgroup retrieved five minimal length trees of length 8 (Fig. 6). The most basal sergestid clades are Peisos and Acetes followed by Sicyonella; Peisos is sister to Acetes. This clade, however, is not statistically robust. The clade Acetes + Peisos is followed by the clade Sicyinella + Petalidium, which also has not received significant bootstrap or Bremer support. The crowngroup Sergia sensu Vereshchaka (000) + Sergestes sensu Vereshchaka (009), which is now split into 15 genera (Judkins & Kensley, 008; Vereshchaka et al., 014), is robust (bootstrap and Bremer supports are 91 and 5, respectively) and sister to Sicyinella + Petalidium. Within the crown group, the former genus Sergia sensu Vereshchaka (009) has a terminal position and is also supported (Bremer support 3). C PV LI LC LT D Figure 4. Petalidium obesum, male ZMUC-CRU A, lateral view of anterior part of carapace. B, male clasping organ. C, petasma. la, lobus armatus; lc, lobus connectens; li, lobus inermis; lt, lobus terminalis; pv, processus ventralis. D, uropodal exopod. E, scaphocerite. Scale bar = mm. LI, lobus inermis; LT, lobus terminalis; PV, processus ventralis; LC, lobus connectens; Lac, lobus accessorius; LA, lobus armatus; PU, processus uncifer. E Analysis 1 shows that the clade Petalidium is sister to Sicyonella and received 98 bootstrap support and 6 Bremer support, suggesting a monophyletic origin for this genus. Analysis with Aristeomorpha foliacea as the outgroup retrieved five minimal length trees of length 45. The most basal sergestoid clades are Sicyonella followed by Petalidium and Lucifer + Peisos + Acetes. The clades Petalidium and Lucifer + Peisos + Acetes are statistically robust, both receiving Bremer support 5. The crown-group is again Sergia sensu Vereshchaka (000) + Sergestes sensu Vereshchaka (009), which is robust (Bremer supports 3) and sister to Lucifer + Peisos + Acetes. Analysis resulted in 94 bootstrap support and 5 Bremer support of the clade Petalidium, also suggesting a monophyletic origin for this genus.

6 464 A. L. VERESHCHAKA AND A. A. LUNINA Figure 5. Petalidium suspiriosum. A, lateral view of anterior part of carapace (YPM IZ , female, syntype). B, male clasping organ. C, petasma. a, pars externa; e, pars astrigens; la, lobus armatus; lc, lobus connectens; li, lobus inermis; lt, lobus terminalis; m, pars media; pb, processus basalis; pv, processus ventralis. D, uropod. Scale bar: (A) = mm, (B) = 4 mm, (C) = 1 mm. (A C, Wasmer, 1974; D, Burkenroad, 1937). LI, lobus inermis; LT, lobus terminalis; PV, processus ventralis; LC, lobus connectens; Lac, lobus accessorius; LA, lobus armatus; PU, processus uncifer. DISCUSSION THE MONOPHYLY OF THE GENUS Analysis 1 with the outgroup within Sergestoidea showed that Sicyonella is sister to Petalidium. Analysis with the outgroup outside Sergestoidea corrected the position of Petalidium and showed that the genus is a sister group of the clade including all Sergestoidea except Sicyonella. Both share reduced fewer dorsal teeth behind the orbital margin (character ), absence of the pterygostomial teeth (5), lamellar posterior arthrobranch on the somites IX (13), X (17), XI (1), fewer movable lateral spines on telson (34), fewer number of segments on fourth (71, 73) and fifth pereopods (77, 79), and presence of hooks on the pars externa of petasma (96). Both analyses revealed very high support of the clade Petalidium, thus suggesting a monophyletic origin for all species of the genus. Analyses 1 and showed the following identical synapomorphies: membraneous in-

7 PHYLOGENY AND TAXONOMY OF PETALIDIUM 465 A Lucifer typus Peisos petrunkevitchi Acetes indicus Sicyonella maldivensis Petalidium suspiriosum Petalidium foliaceum Petalidium obesum Neosergestes edwardsi Parasergestes armatus Cornutosergestes cornutus Sergestes atlanticus Eusergestes arcticus Allosergestes sargassi Deosergestes corniculum Sergia tenuiremis Lucensosergia lucens Challengerosergia challengeri Scintillosergia scintillans Prehensilosergia prehensilis Gardinerosergia gardneri Robustosergia robusta Phorcosergia phorca tegument (0), absence of the supraorbital tooth (4), reduced anterior arthrobranch on the somite XII (3), subequal basal and terminal segments of the antennular peduncle (39), three endites in the maxillula (47), presence of an additional row of serrated bristles adjacent to the tubercle in the male clasping organ (9), and rudimentary LC of petasma (105). Within Petalidium, the phylogenetic position of three species is not resolved. Petalidium foliaceum is characterized by the absence of the posterior arthrobranch on the somite XIII, whereas P. obesum is lacking the hepatic spine and has the posterior arthrobranch on the somite XIII lamellar. MORPHOLOGICAL TRENDS IN SERGESTOIDEA Analysis shows that all genera of Sergestoidea differ most obviously from basal Sicyonella in reduction of external teeth on body (rostrum, carapace, telson) and in the degenerate arthrobranch on somites IX XI. This trend may be associated with the planktonic mode of life in all sergestids except the benthic/benthopelagic Sicyonella. A smoother body reduces energy wastes when swimming; water flows in the branchial chamber may accelerate oxygen exchange, thus allowing reduction of the branchial surface. The polarization of characters 71, 73, 77, and 79 indicates that a general shortening of the swimming pereopods IV V has occurred in Sergestoidea. Synchronously, these pereopods are flattened and act as oars thus demonstrating swimming mechanisms different from that of other planktonic malacostracans: euphausiids and carid shrimps of the families Oplophoridae and Pasiphaeidae move by means of pereopodal exopods. Further reduction of external teeth and branchs may be observed in the Petalidium clade. Membranous integument may be related to a deep-sea mode of life B Aristaeomorpha foliacea Sicyonella maldivensis Petalidium suspiriosum Petalidium foliaceum Petalidium obesum Lucifer typus Peisos petrunkevitchi Acetes indicus Neosergestes edwardsi Parasergestes armatus Cornutosergestes cornutus Sergestes atlanticus Eusergestes arcticus Allosergestes sargassi Deosergestes corniculum Sergia tenuiremis Lucensosergia lucens Challengerosergia challengeri Scintillosergia scintillans Prehensilosergia prehensilis Gardinerosergia gardneri Robustosergia robusta Phorcosergia phorca Figure 6. The strict consensus trees, principal clades and their bootstrap support (numbers above the clade) and Bremer support (numbers below the clade in circles). A, analysis 1 with Lucifer typus as the outgroup. B, analysis with Aristeomorpha foliacea as the outgroup. of this genus, whereas synapomorphies in the male antennula, in the clasping organ, and in the petasma may be related to a mating behaviour characteristic for his genus. Within Petalidium, the main trend is related to the development of branchs. They are least developed in P. foliaceum occurring in the Southern Ocean, where the oxygen concentration is high. Conversely, the arthrobranch is most developed in P. suspiriosum, which lives within lower part of the oxygen-depleted zone of the North Pacific. ADDITIONAL RESULTS Analyses 1 and showed statistically significant support of the crown group Sergestes + Sergia including 15 new genera sharing synapomorphies concerning arthrobranch development on somite VIII (8), clasping organ (89), luminous organs (14), and metamorphosis (148). These synapomorhies may illustrate further adaptations to pelagic life related to metabolism, mating procedures, communication, and development. The clade including eight new genera of the former Sergia (with the root Sergia left in the generic name) may also represent a monophyletic terminal clade: both bootstrap and Bremer supports are high, although not statistically significant. Analysis with the use of the outgroup outside Sergestoidea revealed a position of Lucifer (Luciferidae) within (not outside!) the clade Sergestidae. Lucifer was considered as the only genus of the family Luciferidae, which, along with Sergestidae, represents the superfamily Sergestoidea. Future studies on the morphology and phylogeny of Acetes, Lucifer, Sicyonella, and Peisos are required for a deeper understanding of the phylogenetic relationships within Sergestoidea. Petalidium Sergia S ergia + Sergestes

8 466 A. L. VERESHCHAKA AND A. A. LUNINA KEY TO SPECIES OF THE GENUS PETALIDIUM (FOR THE KEYS TO GENERA OF SERGESTIDAE, SEE VERESHCHAKA ET AL., 014) 1. Arthrobranchs on somite XIII absent (Fig. A). LA of petasma more slender that LAc, armed with 1 hooks. Occurs South of 30 S...Petalidium foliaceum Bate, 1881 Arthrobranchs on somite XIII present, lamellar or dendritic. LA of petasma subequal or more robust that LAc, armed with > 5 hooks. Occurs north of 35 S.... Hepatic spine absent. Arthrobranchs on somite XIII lamellar (Fig. B). LA of petasma more robust that LAc, armed with 1 hooks. Atlantic species...petalidium obesum (Krøyer, 1859) Hepatic spine present. Arthrobranchs on somite XIII dendritic (Fig. C). LA of petasma subequal to LAc, armed with > 5 hooks. North Pacific species...petalidium suspiriosum Burkenroad, 1937 TAXONOMY OF PETALIDIUM The character dataset indicates the need of an emended diagnosis of the genus. For a deeper insight into the taxonomy of Petalidium, we analyzed the data in the available literature, which included a total of 10 variable characters (see Supporting informartion, Appendix S4). Having summarized these data, we concluded that only four of these 10 characters are of taxonomic value: character 3 (hepatic spines), character 5 (arthrobranchs on somite XIII), character 7 (LA of petasma compared to Lac of petasma), and character 8 (LA of petasma; number of hooks). These four characters, along with others that we have defined, are used by us as diagnostic characters for species of Petalidium, and for phylogenetic reconstructions. PETALIDIUM BATE, 1881 Diagnosis: Carapace and abdomen smooth, rostrum as a small protrusion of carapace, acute; supraorbital spine absent; cornea well pigmented; stylocerite fixed; mandible with three-segmented palp; maxillipeds I II each with well-developed endopod; maxilliped I with threesegmented endopod; maxilliped III seven-segmented, dactylus not subdivided; pereopods IV V progressively decreasing in length, flat, six-segmented, lacking dactyli, two distal segments setose only on one margin; uropodal exopod setose for distal 0% of outer margin, with small tooth. Male clasping organ: well-developed, bearing numerous spatulate ordered spines on both inner margins, tubercle absent, replaced by long stout spine. Petasma: LA, Lac and LI developed, entire; LC rudimentary, without hooks; LT divided, PU short, bearing hook; PV elongate, armed with hooks. Photophores: dermal organs and organ of Pesta absent. Branchiae: pleurobranchs on somites VIII XII, lamellar posterior arthrobranch on somite XII. Type species: By monotypy, P. foliaceum Bate, 1881 (Perez-Farfante & Kensley, 1997: 191). Type locality: off Marion Island, S, E, depth 516 m. South of Australia, 47 5 S, 130 E, depth 3935 m. Species: Petalidium foliaceum Bate, 1881; P. obesum (Krøyer, 1859); P. suspiriosum Burkenroad, PETALIDIUM FOLIACEUM BATE, 1881 (FIGS A, 3A C) Petalidium foliaceum Bate, 1881: 194; 1888: 349, plate 60. Hansen, 1896: 936; 1903: 54, plate II, figure I. Illig, 1914: 37, figures Stebbing, 1914: 84, plate 8. Burkenroad, 1937: 36. Hale & Johnston (1941): 61, figures 1,. Material examined: Dana stations (1 f 11 mm, catalogue number YPM IZ 04046), 364- ( ff mm; 1 juv 6 mm, catalogue number YPM IZ ), ( ff 9 10 mm, catalogue number YPM IZ 04047), (1 f 6 mm, catalogue number YPM IZ 04048), (1 f mm, catalogue number YPM IZ 04045), (1 f 15 mm, catalogue number YPM IZ 04049), (1 m 8½mm), (6 juv 5 mm). Challenger Expedition, Station 159, South Australia (syntype, Natural History Museum, catalogue number 1888.), Station 146, Marion Island (five syntypes, Natural History Museum, catalogue number (four syntypes) and (1 syntype). Type material: Six syntypes of Petalidium foliaceum, Natural History Museum (see above). Type locality: Off Marion Island, S, E, depth 516 m. South of Australia, 47 5 S, 130 E, depth 3935 m. Diagnosis: Hepatic spine present; petasma with LAc (3 4 hooks) stronger than LA (1 hooks), LT bearing 4 5 and 1 hooks on branches; no arthrobranchs on somite XIII. Remarks: Both males and females of this species may be distinguished from the other species of the genus by the absence of any arthrobranchs above pereopod IV. In addition, in males, the Lac on the petasma is significantly more robust than the LA. According to our data, any specimens found south of 35 S belong

9 PHYLOGENY AND TAXONOMY OF PETALIDIUM 467 to this species. Petalidium foliaceum and P. obesum cooccur in the South Atlantic between 30 S and 35 S; if taken from in this area, P. obesum is easily distinguished by the absence of an hepatic spine and by its much more slenderer Lac. Ethymology: from the Greek foliaceum, meaning foliaceous, leaf-like. Geographical distribution (Fig. 7): Most of the southern seas between 35 S and 66 S: South Atlantic, South of Africa (Illig, 1914; Kensley, 1971, 1981; Dana material), southern Indian Ocean, (Bate, 1888; Stebbing, 1914; Hale & Johnston, 1941), south of Australia (Bate, 1888; Iwasaki & Nemoto, 1987), Antarctic Polar Frontal Zone of the Indian Ocean (Pakhomov & Froneman, 000). The species was recorded south of the Polar Front, in Western Antarctica (Tiefenbacher, 1991), Prydz Bay ( S, E; Ikeda, 013), and the Scotia and Weddell Seas (Lancraft, Torres & Hopkins, 1989; Arntz & Gorny, 1991). Vertical distribution: Recorded from the Dana stations m wire corresponding to approximately m of actual depth (Vereshchaka, 000). Hale & Johnston (1941) reported the species from similar depths ( m). PETALIDIUM OBESUM (KRØYER, 1859) (FIGS B, 4A E) Sergestes obesus Krøyer, 1859: 57, 79, plate 4 (figure 10a f) Sergestes sanguineus Chun, 1889: 538 (mastigopus stage) Petalidium obesum Hansen, 1896: 968; 1903: 56; 19: 190, plate 11 (figures 3, 4). Burkenroad, 1937: 34. Wasmer, 1974: 165 Petalidium foliaceum non Bate, Illig, 197: 8, figures 1 5 Material examined: Dana stations (3 mm mm; 5 ff mm); (1 m 6 mm; 6 ff mm); (4 m mm; 10 ff mm); (1 f 7.5 mm); (1 m 8 mm; 3 ff 8 10 mm); (6 mm mm; 7 ff 8 10 mm); (3 mm 6 9 mm; 3 ff 6 mm); ( mm 6 mm; 1f9mm) Type material: holotype of Sergestes obesum (Krøyer, 1859), Zoological Museum, Copenhagen University, catalogue number CRU Type locality: Central Atlantic, 4.5 N, 1.5 W. Diagnosis: Hepatic spine absent in adults; petasma with LAc (1 3 hooks) more slender than LA (6 10 hooks), LT bearing 0 3 and 1 3 hooks on branches; arthrobranchs on somite XIII lamellar. Remarks: Both males and females of this species may be distinguished from the other species of the genus (1) by the absence of an hepatic spine in adults and () by the arthrobranchs above pereopod IV being lamellar. In addition, in males, the Lac of the petasma is much more robust than the LA. According to our data, any specimens found in the Atlantic Ocean North of 30 S belong to this species. Geographical distribution (Fig. 7): Atlantic Ocean between 45 N and 35 S: of Cape Verde, Canary Islands, Azores Islands (Hansen, 19; Dana Stations), Northwest Atlantic (Yale Peabody Museum material, Dana material) Central Atlantic (Krøyer, 1859), and South of Africa (Kensley, 1981; Dana material). Vertical distribution: Recorded from the Dana stations m wire corresponding to approximately m of actual depth. PETALIDIUM SUSPIRIOSUM BURKENROAD, 1937 (FIGS C, 5A D) Petalidium suspiriosum Burkenroad, 1937: 35, figures 8 1. Pearcy & Forss, 1966: , Wasmer, 1974:160, figures 1 8. Material examined: Templeton Crocker Expedition, Zaca Station 165, T-3 (syntype, two appendages, YPM IZ and syntype, 1 f 7 mm,iz ). Type material: Two syntypes of Petalidium suspiriosum, Yale Peabody Museum (see above). Type locality: Gulf of California, 0.60 N, W. Diagnosis: Hepatic spine present; petasma with LAc (5 6 hooks) subequal to LA (9 11 hooks), LT bearing 0 and hooks on branches; arthrobranchs on somite XIII dendritic. Remarks: Both males and females of this species may be distinguished from the other species of the genus by the arthrobranchs above pereopod IV being dendritic. In addition, in males, the Lac is subequal to the LA (it is much more slender in R. obesum and significantly more robust in P. foliaceum). Also, the LA of P. suspiriosum bears many more hooks (> 8) than in other species. According to recent knowledge, any specimens found in the Pacific Ocean North of 0 N belong to this species.

10 468 A. L. VERESHCHAKA AND A. A. LUNINA Figure 7. Macroscale geographical distribution: Petalidium foliaceum (pink), Petalidium obesum (green), and Petalidium foliaceum (crimpson). Type localities (black circles) and Dana stations (yellow circles) are indicated; filled areas are supported by literature data. Geographical distribution (Fig. 7): Only found in the North Pacific between 0 N and 5 N: off Oregon (Pearcy & Forss, 1966; Krygier & Pearcy, 1981), off Hawaii (Walters, 1977), and off Japan (Kikuchi & Omori, 1985). Specimens in the Oregon State University, Department of Oceanography collections have been taken as far north as N W and as far south as 34 3 N W (Wasmer, 1974). The most southerly capture record is that of the type locality, 0 36 N W (Burkenroad, 1937), where specimens were evidently brought from the north by the cold California Current. Vertical distribution: m (off Hawaii, Walters, 1977), m (Kikuchi & Omori, 1985). BIOLOGICAL REMARKS On the global scale, the genus Petalidium shows allopatric speciation, whereas, for P. obesum and P. foliaceum, speciation is almost parapatric. Both species co-occur in the Southern Atlantic between approximately 30 S and 35 S, with P. foliaceum being restricted to Antarctic and Subantarctic waters. Mesoscale data on geographical distribution are available only for P. foliaceum. Iwasaki & Nemoto (1987) included this species in a group of species distributed from the Subtropical Zone to the Antarctic Zone south of Australia. Figure 8 shows the distribution of P. foliaceum based on 115 specimens from 1 Eltanin stations (Wasmer, 1993). The species was collected from the Subtropical Zone near 40 S in the Tasman Sea to 74 S in the Ross Sea, between 174 W and 117 E. The occurrence of P. foliaceum was not limited to certain water masses and the range of this species was not restricted by hydrological barriers. The absence of Petalidium in the South-western Atlantic region may be a result of the poor sampling efforts in this area (no stations during the Dana and other great pelagic expeditions). However, the absence of Petalidium in Tropical/Subtropical areas of the Indian and Pacific Oceans is intriguing. Specimens of Petalidium were absent in the Dana samples from these regions, whereas other planktonic sergestid species were well represented (approximately specimens in total: Vereshchaka, (000, 009). This absence of Petalidium in Dana material along with the lack of any reports of its presence in the literature indicate that it is very unlikely for Petalidium to occur in Tropical/Subtropical areas of the Indian and Pacific Oceans. Vertical distribution was studied in detail for two species, P. suspiriosum and P. obesum. Information about P. suspiriosum is available from a series of eight cruises by the R/V Yaquina and R/V Wecoma from 197 to 1976, off Oregon. The species was found between 150 and 1750 m, with its population maximum between 600 and

11 PHYLOGENY AND TAXONOMY OF PETALIDIUM 469 Figure 8. Distribution of Petalidium foliaceum south of Australia (sensu Wasmer, 1993). PF, Polar Front; STF, Subtropical Front m. Petalidium suspiriosum apparently exhibited no diel migration, although slight seasonal changes in depth distribution have been noted, with peaks in abundance that are shallower in winter than in summer (Pearcy et al., 1977). Walters (1977) reported a bathymetric range from 750 to 1500 m for this species off Hawaii. Population maxima both day and night were found within the layer m (Walters, 1975). Information of vertical distribution for P. obesum is scarcer. At 18 N, both day- and night-time distributions lay below 1000 m, whereas, at 30 N, their vertical range extended upward to 700 m; there was no evidence of a night-time migration (Fasham & Foxton, 1979). Thus, scattered information on the vertical distribution of Petalidium shows that the vertical ranges of both species are similar; all three Petalidium species have population maxima in the lower meso- and upperbathypelagic zones. By contrast to most other crustaceans of these layers, they do not migrate diurnally and migrate only slightly seasonally (Pearcy et al., 1977). Females of Petalidium are larger, more abundant, and generally live deeper than males. In addition to data from the Dana Expeditions, statistically significant information was collected for P. suspiriosum by Krygier & Pearcy (1981) in which the sex ratio was 1.5 females to 1.0 males (N = 471). In upper water layers of m, the sex ratio was almost even but, in deep water greater than 1000 m, females predominated in the catches. Males normally did not exceed 10 mm (postorbital carapace length), whereas most females were between 9 13 mm, suggesting that females may either grow more rapidly or live longer than males. Similar to many other deep-living and high-latitude crustaceans, specimens of Petalidium have high lipid content (6.7 3.% in P. foliaceum) (Clarke & Holmes, 1986). There was no relationship between size and lipid content. The same species exhibited high C : N ratios ( ) suggesting significant permanent deposition of lipids in the body (Ikeda, 013). Petalidium may be significant in midwater plankton assemblages. For example, P. suspiriosum was the fourth most abundant shrimp species, accounting for 0.6% of the total Isaacs Kidd Midwater Trawl pelagic decapods in the North Pacific (Walters, 1975). Petalidium foliaceum is even more important in the Southern Ocean, accounting for 11.4% of shrimp abundance (Pakhomov & Froneman, 000). The absolute abundance of Petalidium in the water column is exemplified by P. foliaceum in the Southern Ocean at individuals m (Walters, 1975). The same species showed abundances of individuals m 3 during autumn and individuals m 3 during winter (Parker, Donnelly & Torres, 011). The available data for P. suspiriusum are similar, with approximately 1.0 individuals m 3 recorded by Kikuchi & Omori, (1985). Parker et al. (011) found that the biomass of Petalidium ranges from mg m 3 during autumn to mg m 3 during winter.

12 470 A. L. VERESHCHAKA AND A. A. LUNINA Information available in the literature indicates that the genus Petalidium is a visible component in midwater communities. Petalidium shrimps are food for mesopelagic fish and squids. In turn, the Petalidium species feed intensively and thus plays a significant role in mesopelagic communities; for example, Pakhomov, Perissinotto, & Froneman (1999) measured the daily food ration of P. foliaceum at 1.7% of dry weight. Accurate identification of Petalidium species is thus important for both zoological and fishery research. CONCLUSIONS Phylogenetic analysis with the use of two different outgroups resulted in statistically significant bootstrap and Bremer supports of the clade Petalidium, thus showing the monophyly of the genus. Observed morphological trends are related to adaptation to the planktonic life and concern external body teeth, branchs, swimming appendages, and mating organs. Additional results of these analyses were (1) possible monophyly of the crown-group including 15 new genera of the former Sergia and Sergestes and () the position of Lucifer (family Luciferidae) within the clade Sergestidae. The results highlight the need for future phylogenetic analyses of the remaining genera Lucifer, Acetes, Peisos, and Sicyonella involving all species of these genera and promise interesting changes in the classification of Sergestoidea, the sister family of Penaeoidea. ACKNOWLEDGEMENTS The authors are grateful to Rick Webber (Te Papa, New Zealand) and two very constructive unknown reviewers for their help and valuable comments. The authors also thank Dr. Jorgen Olesen, the Natural History Museum of Denmark, for the opportunity to work in this wonderful place. The studies were supported by the Russian Foundation for Basic Research (grant number ) and the Program for a Basic Research of the Presidium of the Russian Academy of Sciences. Financial support for the project was provided by the Danish Carlsberg Foundation. REFERENCES Ahyong ST The polychelidan lobsters: phylogeny and systematics (Polychelida: Polychelidae). In: Martin JW, ed. Decapod crustacean phylogenetics. Los Angeles, CA: Natural History Museum of L. A. County, Arntz WE, Gorny M Shrimp (Decapoda, Natantia) occurrence and distribution in the eastern Weddell Sea, Antarctica. Polar Biology 11: Bate CS On the Penaeidea. Annals and Magazine of Natural History 5: Bate CS Report on the Crustacea Macrura collected by H.M.S. Challenger during the years Report on the scientific results of the voyage of H.M.S. Challenger during the years Zoology, 4: Burkenroad M The Templeton Crocker Expedition. XII. Sergestidae (Crustacea Decapoda) from the Lower Californian region, with descriptions of two new species and some remarks on the organs of Pesta in Sergestes. Zoologica : Burkenroad M A new sergestid shrimp (Peisos petrunkevitchi n. gen. n. sp.), with remarks on its relationship. Transactions of the Connecticut Academy of Arts and Sciences 36: Chun C Bericht über eine nach den Canarischen Inseln im Winter ausgefiihrte Reise. Sitzungsberichte der Konigliche Preussischen Akademie der Wissenschaften zu Berlin 1889: Clarke A, Holmes LJ Lipid content and composition of some midwater crustaceans from the Southern Ocean. Journal of Experimental Marine Biology and Ecology 104: Dana JD Conspectus Crustaceorum, etc. conspectus of the crustacea of the exploring expedition under Capt. C. Wilkes, U.S.A. Proceedings of the Academy of Natural Sciences, Philadelphia 6: 6 8. De Grave S, Fransen CHJM Carideorum catalogus: the recent species of the dendrobranchiate, stenopodidean, procarididean and caridean shrimps (Crustacea: Decapoda). Leiden: NCB Naturalis. Fasham MJR, Foxton P Zonal distribution of pelagic Decapoda (Crustacea) in the eastern North Atlantic and its relation to the physical oceanography. Journal of Experimental Marine Biology and Ecology 37: Fukuoka K, Tamaki M, Kikuchi T The redescription of three species of Sicyonella (Crustacea: Decapoda: Dendrobranchiata: Sergestidae). Zootaxa 833: Goloboff P, Farris S, Nixon K TNT: tree analysis using new technology. Available at: tnt/ de Haan W Crustacea. In: von Siebold PF, ed. Fauna Japonica sive description animalium, quae in itenere per Japoniam, jussu et auspiciis superiorum, qui summum in India Batava Imperium tenent, suscepto, annis collegit, notis, observationibus et adumbrationibus illustravit. Leiden. Hale HM, Johnston TH Decapod Crustacea. Adelaide: BANZAR Expedition Committee, Hansen HJ The Sergestidae of the Siboga expedition. Siboga-Expeditie 38: Hansen HJ. 19. Crustaces Decapodes (Sergestides) provenant des campagnes des Yachts Hirondelle et Princesse-Alice ( ). Résultats des Campagnes scientifiques accomplies par le Prince Albert I de Monaco 64: 1 3. Hansen HJH On the development and the species of the Crustaceans of the genus Sergestes. Proceedings of the Zoological Society of London 1:

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14 47 A. L. VERESHCHAKA AND A. A. LUNINA Vereshchaka AL North Atlantic and Caribbean species of Sergia (Crustacea, Decapoda, Serdestidae) and their horizontal and vertical distribution. Steenstrupia 0: Walters J Ecology of Hawaiian sergestid shrimps (Penaeidea: Sergestidae). University of Hawaii, PhD Thesis. Walters JF Ecology of Hawaiian sergestid shrimps (Penaeidea: Sergestidae). Fishery Bulletin 7 4: Wasmer RA A description of Petalidium suspiriosum Burkenroad, 1937 (Decapoda, Natantia). Crustaceana 7: SUPPORTING INFORMATION Wasmer RA Pelagic shrimps (Crustacea: Decapoda) from six USNS Eltanin cruises in the southeastern Indian Ocean, Tasman Sea, and southwestern Pacific Ocean to the Ross Sea. Antarctic Research Series 58: Wood-Mason J Phylum Appendiculata. Branch Arthropoda. Class Crustacea. In: Wood-Mason J. and A. Alcock. Natural History notes from H.M. Indian Marine Survey Steamer Investigator, Commander R. F. Hoskyn, R.N., commanding. Series II., No. 1. On the results of deepsea dredging during the season Annals and Magazine of Natural History, Series 6 8: Additional Supporting Information may be found in the online version of this article at the publisher s web-site: Appendix S1. Terminal taxa and sources of character scoring. Appendix S. List of characters used. New characters are marked with asterisks (*). Appendix S3. Data matrix. Appendix S4. Observation of characters and their use in taxonomy of Petalidium as known from the literature (Krøyer, 1859; Bate, 1888; Chun, 1889; Hansen, 1903, b, 19; Illig, 1914; Stebbing, 1914; Burkenroad, 1937; Hale & Johnston, 1941; Kensley, 1971; Wasmer, 1974).