A review of the genus Zonophryxus Richardson, 1903 (Crustacea: Isopoda: Dajidae) with recognition of Colypurus agassizi Richardson, 1905 (Crustacea: Isopoda: Colypuridae) as a synonym of Zonophryxus similis Searle, 1914 and the requisite sinking of Colypuridae

Most isopods belonging to Dajidae G. O. Sars, 1883 (59 species) are ectoparasitic on euphausids, mysids, and shrimp as definitive hosts, although some are known from isopods, anomurans, and brachyurans with a number of species described without known hosts (Boyko et al. 2008 onwards). As with other epicarideans, dajid life cycles also include copepods as intermediate hosts (Coyle & Mueller 1981). Typically, adult females attach to the dorsal carapace (euphausids and shrimp) or within the marsupia (mysids) of hosts; however, in some cases they attach to the eyestalks, antennules or pereopods of definitive hosts (Williams & Boyko 2021). Regardless of position on the hosts, all dajid females pierce the cuticle with styliform mandibles and feed on hemolymph of hosts and some have been shown to reduce reproduction and impact secondary sexual characters (e.g., Field 1969, Shields & Gómez-Gutierrez 1996, Nagler et al. 2020).

The genus ZonophryxusRichardson, 1903 is currently comprised of six species (Boyko et al. 2008 onwards), most known parasitizing caridean hosts primarily in Pandalidae and rarely in Nematocarcinidae in relatively deep water (210–1401 m) in the Atlantic, Pacific, and Antarctic (Southern) Oceans. The bodies of females are ovate and dorsally swollen, often showing little to no dorsal segmentation, with no visible appendages in dorsal view, and with a row of triangularly-shaped processes along the posterior border of the body, giving the posterior end a “notched” appearance (Kensley 1979). Females of Zonophryxus are oriented with their head toward the posterior end of the host and with mouthparts positioned toward the posterior end of the dorsal surface of the host carapace (see Fig. 4), corresponding to the region of the heart of the host into which they insert their mouthparts. They possess five or six pairs of pereopods for attachment to the host cuticle. The first five pairs of pereopods are clustered around the head and used to clutch onto the host carapace with their dactyli, possibly aided by the ventral surface being closely applied to the carapace and acting as a “suction-cup” (Brandt & Janssen 1994, Nagler et al. 2020). When present, the sixth pair of pereopods is positioned at the base of the sixth oostegite; it is not known if these posterior pereopods also aid in attachment.

Males of Zonophryxus species are of two types, probably part of a developmental series: one similar to those seen in other dajid genera (e.g., HolophryxusRichardson 1905a) and another that is quite different, with larger pereomeres, a head bearing dorsal lobes, and a ventrally displaced pleon with all pleomeres fused into a single segment. The unusual morphology of this second type of male led Richardson (1905b) to remark that the holotype of Colypurus agassizi Richardson, 1905 did “not seem to belong to any of the known families of the order,” although she did not specify what characters she considered distinctive. Because of the novel morphology of this specimen, Richardson (1905b) used it as the basis for her description of a new species, genus, and family of uncertain relationships with other isopods. Richardson (1905b) did not make note of the sex of the specimen and thought that the specimen was a parasite; this is not strictly correct as only epicaridean females directly parasitize their hosts (i.e., pierce the host and feed on hemolymph).

In the present paper, we show that Colypurus agassizi Richardson, 1905 is the male of Zonophryxus similisSearle, 1914, and that Colypurus Richardson, 1905 and Colypuridae Richardson, 1905 are junior synonyms of Zonophryxus and Dajidae, respectively. Additionally, we describe a new species based on a pair of specimens collected in Peruvian waters. We also review all the species in the genus and provide morphological details about species that were incompletely described and/or illustrated in earlier publications. Finally, we discuss the variable number of pereopods found in females, a feature previously considered a species-specific character but shown herein to represent phenotypic plasticity. A key to species is provided based on female characters because mature and immature males are not known for all species.

Line drawings were made with a camera lucida drawing tube attached to Olympus compound or dissecting microscopes. Final images were created by tracing a scanned copy of the original sketch with a Wacom tablet or Wacom Cintiq pen display using Adobe Illustrator. In addition to conventional light micrographs, the holotype of Zonophryxus similisSearle, 1914 (USNM 46432) was imaged with a Macropod Pro kit (MacroscopicSolutions), and resulting pictures were aligned and stacked with the focus stacking software Zerene Stacker (10 images from bottom to top of specimen).

Note that when Harriet Richardson married William Searle in 1913, she took his name as Harriet Richardson Searle but published only three papers using the latter name (Damkaer 2000). The 1914 paper in which Z. similis was described is often cited as “Richardson 1914,” but the header on alternating pages reads “Searle: Isopoda” and so we attribute authorship of the species to Searle, rather than Richardson or Richardson Searle.

Specimens were borrowed from and deposited in the National Museum of Natural History, Smithsonian Institution, Washington, D.C. (USNM). References are provided for taxonomic authorities of isopod taxa but not for those of decapod hosts. This work is registered in ZooBank with the registration number urn:lsid:zoobank.org:pub:E208CA4D-D822-4B14-828A-73EED7A8FE38.

Isopoda Latreille, 1817 Epicaridea Latreille, 1825 Cryptoniscoidea Kossmann, 1880 Dajidae G. O. Sars, 1883 

• Dajidae G. O. Sars, 1883:19.

• Colypuridae Richardson, 1905b:105 (n. syn.).

As shown below, the male holotype of Colypurus agassizi belongs to the same species as the female holotype of Zonophryxus similisSearle, 1914 and, consequently, Colypuridae is a junior synonym of Dajidae.

ZonophryxusRichardson, 1903 

• ZonophryxusRichardson, 1903 

• ColypurusRichardson, 1905b:105–106 (n. syn.).

Colypurus agassizi Richardson, 1905 by monotypy; Zonophryxus retrodensRichardson, 1903 by original designation.

Female. Body symmetrical, ovate, longer than broad, dorsally convex; body regions indistinct in dorsal view; appendages not visible in dorsal view; head, pereon, and pleon fused. Well-developed anterior margin (frontal lamina) and thin lateral margins on ventral surface. Antennules as recurved flat lobes, posteriorly tapering and surrounding buccal cone. Antennae small, digitiform. Sternal plate distinct. Six pairs of oostegites but sixth pair variously fused to posterior margin of fifth. Adults with five or six pairs of isomorphic pereopods; sixth pair (if present) near posterior margin of body at bases of oostegite 6 pair. Pleon lacking appendages or uropods. Posterior margin of body with row of triangularly-shaped processes (margin appears “notched”).

Male body flattened. Head ovate, fused with first segment of pereon. Antennules minute, rounded; antennae elongate, blade-like. Pereon with 6 free segments. Seven pairs of isomorphic pereopods. Pleomeres fused with pleotelson into single ovate pleon, without segmentation or appendages. Type 1 male (“Zonophryxus-type”) head ovate, sloping from posterior to anterior, more or less smooth. Pereomere 7 smaller than pereomere 2. Pleon extending posteriorly from pereomere 7. Type 2 male (“Colypurus-type”) head with distinct medial and lateral lobes. Pereomere 7 larger than pereomere 2. Pleon ventrally displaced under pereomere 7.

As shown below, the male holotype of Colypurus agassizi belongs to the same species as the female holotype of Zonophryxus similis and, consequently, Colypurus is a junior synonym of Zonophryxus. The only clear synapomorphy for Zonophryxus is the presence of the triangularly-shaped processes on the posterior of the body in females; it is possible that the type 2 male morphology, not known to occur in males of other dajid genera, is also a synapomorphy for the genus, but this male form has not been found in all species to date. However, this is perhaps not surprising as the number of specimens known for any of the species in the genus is small.

Richardson (1903) incorrectly interpreted the sixth oostegites of the female as a pair of pleopods; examination of specimens bearing six pairs of pereopods clearly shows that these are oostegites. She also identified the row of triangularly-shaped processes at the posterior end of the body as “coalesced abdominal segments” but they represent the remnants of only the lateral margins of the pleon (see Kensley 1979: Fig. 2).

Prior to the present study, no females of any species of Zonophryxus have been reported as ovigerous. We are not aware of any other documented cases of dajids with two morphological types of males such as the presumed immature type 1 males and mature type 2 males found in species of Zonophryxus. Developmental studies are needed to determine whether molt(s) are involved and verify the sexual immaturity/maturity of the morphotypes. We know of one species that possesses two male morphotypes in Bopyridae (see Parathelges aniculi (Whitelegge, 1897) in Williams & Boyko 2016), but this may represent a case of cryptic species rather than development.

Zonophryxus agassizi (Richardson, 1905), new combination Figs. 1, 2

• Colypurus agassiziRichardson, 1905b:106, Figs. 1, 2 (06°36′N, 81°44′W, off Mariato Point, south of Coiba Island, Panama (Pacific).—Searle, 1914:370–371 (description after Richardson 1905b).—Nierstrasz & Brender à Brandis, 1923:112 (list).—Brusca, 1987:273 (mention).—Markham, 2020:150 (list).

• Zonophryxus similisSearle, 1914:369–370, Fig. 16 (06°36′N, 81°44′W, off Mariato Point, south of Coiba Island, Panama (Pacific).—Holthuis, 1949:212 (mention).—Danforth, 1970c:31 (mention), 52 (list), 155 (key), Fig. 44f, g (after Searle, 1914).—Lopretto, 1983:96 (key).—Brandt & Janssen, 1994:343, 350 (mention).—Shimomura et al., 2010:9, 10 (list).—Markham, 2020:151 (list).—Nagler et al., 2020:342 (list).

• Zonophryxus similes [sic] Raupach & Thatje, 2006:439 (mention).

Mature holotype male (5.0 mm TL) of Colypurus agassizi, “Albatross” Sta. 4621, 06°36′N, 81°44′W, off Mariato Point, south of Coiba Island, south coast of Panama (Pacific), 581 fms (=1063 m), 21 Oct 1904 (USNM 46433). Mature holotype female (17.4 mm TL) of Zonophryxus similis, “Albatross” Sta. 4621, 06°36′N, 81°44′W, off Mariato Point, south of Coiba Island, Panama (Pacific), 581 fms (=1063 m), 21 Oct 1904 (USNM 46432).

06°36′N, 81°44′W, off Mariato Point, south of Coiba Island, Panama (Pacific).

Known only from the type locality.

1063 m.

Female 17.4 mm TL; male 5.0 mm TL.

Unknown (no shrimp species from “Albatross” Station 4621 in the USNM online catalog).

Female body ovate, head, pereon, and pleon fused, widest in middle, dorsally convex (Fig. 1A, B); small notches visible on lateral margins indicating some pereon segments; eleven closely approximated triangularly shaped processes on posterior margin of body short, not visible in dorsal view (Fig. 1A, F). Ventral side of body concave, with five pairs of isomorphic pereopods closely approximated from head to midpoint of body (Fig. 1A, D, E). Antennules as recurved flat lobes, posteriorly tapering and surrounding buccal cone (Fig. 1A, C). Antennae small, digitiform, situated behind and extending anterolaterally from antennules (Fig. 1C). Maxilliped not dissected out. Sternal plate distinct below oral cone, triangular in shape at anterior end and continuing as ridge between oostegites (Fig. 1A). Oostegite 1 large with subquadrate anterior lobe and rounded posterior lobe (Fig. 1D); oostegite 5 large, subquadrate, basally fused to small, subquadrate oostegite 6 (Fig. 1A, F), both with some minute setae on margins.

Type 2 male dorsoventrally flattened (Fig. 2A, B). Head with lateral rounded extensions, narrower than pereomere 1, dorsal surface with two large lobes (Fig. 2A). Antennule a small indistinct lobe bearing few setae, merged with frontal margin (not visible in figures). Antennae of two segments, tapering blade-like distal segment more than four times as long as rounded basal segment (Fig. 2C, D). First pereomere fused with head, followed by six free pereomeres, slightly wider posteriorly; all pereomeres laterally directed (Fig. 2A). Seven isomorphic pereopods present (Fig. 2B, E, F). Pleomeres fused with pleotelson, forming single ovate, elongate pleon (Fig. 2A, B). Pleon ventrally displaced, affixed near anteroventral margin of pereomere 7 and extending posteriorly, slightly visible in dorsal view, lacking pleopods or uropods (Fig. 2A, B).

The male holotype of C. agassizi is a type 2 male and is very similar to one of the male morphotypes found in Z. quinquedens (see Lopretto 1983, Brandt & Janssen 1994) and, as such, is easily recognizable as a male belonging to Zonophryxus; Colypurus and Zonophryxus are therefore synonymous. The male of C. agassizi was likely paired with the female holotype of Z. similis in life; this is inferred based on the fact that they were collected from the same station on the same day. Given the rarity of Zonophryxus species in samples, the likelihood of a second species in the genus occurring in the same sample is small, and we consider the two species synonymous as well. Although Colypurus is a junior synonym of Zonophryxus, the specific name C. agassizi is the senior synonym of Z. similis and so the correct name for the species is Zonophryxus agassizi.

Richardson (1905b) stated that the holotype of C. agassizi was in the Museum of Comparative Zoölogy (Harvard University), but for reasons unknown, it was deposited in the USNM; Searle (1914) cited the catalog of the specimen as USNM 46433. Intriguingly, the USNM catalog numbers of the two holotypes are sequential, despite their being described nine years apart. Was this merely a coincidence or did Searle (née Richardson) recognize the relationship between the two specimens but never publish on it?

Searle (1914) stated of the female of Z. similis that “the antennae are widely separated and seem to be composed of three articles. The antennulae are concealed by the maxillipeds.” It appears that Searle (1914) interpreted the antenna and antennule as one structure, hence the supposed three segments. The antennule is not obscured by the maxilliped in any species of Zonophryxus. Only the type 2 male is known from this species.

Zonophryxus retrodensRichardson, 1903 Fig. 3A–L

• Zonophryxus retrodensRichardson, 1903:52, Figs. 4, 5 (Oahu, Hawaii), 1904:678, 679, Figs 32, 33 (after Richardson, 1903), 1910:41 (mention).—Koehler, 1911:18, 21, 22, 33 (mention).—Searle, 1914:370 (mention).—Holthuis, 1949:212 (mention).—Danforth, 1970a:27 (mention), 1970b:462 (mention), 1970c:31, 32, 52 (mention), 128 (description after Richardson, 1903), 155 (key), Fig. 44C–E (figures after Richardson, 1903), 1976:79 (mention).—Brandt & Janssen, 1994:350 (mention).—Moore, 2004:82 (list).—McLaughlin et al., 2005:189 (list).—Raupach & Thatje, 2006:439 (mention).—Shimomura et al., 2010:9–17, Figs. 1–7 (32°09.015′N, 129°30.259′E–32°09.034′N, 129°31.725′E, 499–496 m, ex Plesionika semilaevis Spence Bate, 1888).—Shimomura, 2017:110 (mention).—Markham, 2020:151 (list).

Mature syntype female (12.4 mm TL), mature syntype male (3.4 mm TL), “Albatross” Sta. 3815, south coast, southeast of Diamond Head, Oahu Island, Hawaii, 228–312 fms (=417–571 m), 28 Mar 1902 (USNM 28970).

Off Oahu Island, Hawaii, 417–571 m.

Hawaii and Japan.

417–571 m.

Female to 12.4 mm TL; male to 3.4 mm TL.

Type host unknown (but see Remarks); also found on Plesionika semilaevis Spence Bate, 1888.

Female body ovate, head, pereon and pleon fused, widest in middle, dorsally convex; small notches visible on lateral margins indicating some pereon segments; nine triangularly-shaped processes on posterior margin of body short, scarcely visible in dorsal view, broadly separated laterally (Fig. 3I); small notches visible on lateral margins indicating some pereonal segments. Ventral side of body concave with five pairs of isomorphic pereopods closely approximated from head to midpoint of body (Fig. 3G, H). Antennules as recurved flat lobes, posteriorly tapering and surrounding buccal cone (Fig. 3G). Antennae small, digitiform, situated behind and extending anterolaterally from antennules (Fig. 3G). Maxilliped of two ovate lobes, anterior margin irregular, posterior margin rounded; appendix digitiform, slightly curved, attached to side of posterior lobe (Fig. 3J), hooked around oostegite 1 when in situ. Sternal plate distinct below oral cone, triangular in shape at anterior end and continuing as ridge between oostegites (Fig. 3G). Oostegite 1 large with subquadrate anterior lobe and recurved, tapering posterior lobe (Fig. 3K), internal ridge smooth; oostegite 5 large, subquadrate, basally fused to small, ovate oostegite 6 (Fig. 5L), both with setose margins.

Type 1 male dorsoventrally flattened (Fig. 3A, B). Head ovate, fused with pereomere 1. Antennule small, rounded, bearing few terminal setae, superficially appearing to be composed of two articles (Fig. 6C; see Remarks); antennae with two articles, large basal article with anterior notch and small digitiform terminal article with setae (Fig. 3D). Pereomeres 2–6 free, maximal width at pereomere 4; pereomeres 2 and 3 anterolaterally curved, 4 and 5 laterally directed, 6 and 7 posterolaterally directed (Fig. 3A, B). Seven isomorphic pereopods present (Fig. 3E, F). Pleomeres fused with pleotelson, forming single ovate, elongate pleon, lacking pleopods or uropods (Fig. 3A, B).

The type host is unknown, but two potential species, cataloged in the USNM with the same collection and station data as the syntypes, are Heterocarpus ensifer A. Milne-Edwards, 1881 and Aristeus semidentatus Spence Bate, 1881.

Only the type 1 male is known from this species. The largest female reported by Shimomura et al. (2010) was the same size as the female syntype and the types match in most respects the redescription by these authors, although there is a large geographical distance separating the two collection localities. Shimomura et al. (2010) also used SEM to examine fine morphological details, including setules on the antennae and other structures of females, observed herein for this species and the others studied (as well as for Z. quinquedens by Brandt & Janssen 1994). Shimomura et al. (2010: Fig. 2C) incorrectly drew the antennule and antenna of the female, showing the anterior portion of the antennule as contiguous with the antenna rather than the posterior portion of the antennule (see Fig. 3G herein); however, their description and SEM image of these structures were accurate. The antennules are similar to those in species of the genus Holophryxus, and Rustad (1935) suggested they “probably serve as stuffing during sucking, thus increasing the sucktive power” while feeding on host hemolymph. This conclusion has recently been supported by Nagler et al. (2020) who also suggested that additional mouthparts function in sealing the wound to enhance sucking during feeding. In addition, the maxilliped and appendix are similar between species of Zonophryxus and those of other dajid genera; the appendix hooks around oostegite 1 and the presumed function is to regulate water flow and prevent the escape of ova and larvae (Rustad 1935, Williams & Boyko 2021).

The antennules of the male (Fig. 3C) each appear to have two segments, but this may represent a crease in the cuticle; both specimens examined by Shimomura et al. (2010; Fig. 7B, C) have a single rounded lobe, as does the male of the new species of Zonophryxus (Fig. 6D) described herein.

Zonophryxus trilobusRichardson, 1910 Fig. 3M–O

• Zonophryxus trilobusRichardson, 1910:41, Fig. 39 (off Caluya Island, Philippines, 571 m).—Searle, 1914:370 (mention).—Holthuis, 1949:212 (mention).—Danforth, 1976:79 (mention).—Kensley, 1979:665–670, Figs. 1–3 (Makyan Islands, Indonesia, 503 m, ex Heterocarpus gibbosus Spence Bate, 1888).—Lopretto, 1983:96 (key).—Brusca & Wilson, 1991:160 (mention).—Brandt & Janssen, 1994:350 (mention).—Trilles, 1999:284, 298, Figs. 8.4C, 8.18 (figured after Kensley 1979).—Raupach & Thatje, 2006:439 (mention).—Shimomura et al., 2010:9, 10, 17 (mention).—Sidabalok, 2013:61 (list).—Suharsono, 2014:156 (list).

Mature holotype female (13 mm TL), “Albatross” Sta. 5259, off Caluya Island, Philippines, 11°57′30″N, 121°42′15″E, 312 fms (=571 m), 3 June 1908 (USNM 40927).—3 immature females (3.0–5.0 mm TL), 2 mature males (1.4 mm TL each), 1 cryptoniscus larva (1.0 mm TL), “Albatross” Sta. 5622, west of Halmahera, Makyan Islands, Indonesia, 0°19′20″N, 127°28′30″E, 503 m, 29 Nov 1909 (USNM 189065).

Off Caluya Island, Philippines, 11°57′30″N, 121°42′15″E, 571 m.

Philippines and Indonesia; possibly from Western Samoa (see Remarks).

503–571 m.

Type host unknown; Heterocarpus gibbosus Spence Bate, 1888.

Females to 13 mm TL; males to 1.4 mm TL.

See Kensley (1979).

The host of the holotype is unknown; however, Chace (1985) identified the potential hosts from Sta. 5259, the station at which the holotype was collected, as Plesionika bifurca Alcock & Anderson, 1894, Plesionika semilaevis Spence Bate, 1888, and Plesionika spinidorsalis (Rathbun, 1906).

No specimens of Heterocarpus gibbosus Spence Bate, 1888, the host of Kensley's (1979) specimens, were cited from this station. The hosts for Kensley's (1979) non-type specimens are not in the vial with the parasites, but two of three of the immature females were said to each be attached to a H. gibbosus (Kensley 1979; size and sex of host unknown). Chace (1985) cited nine male (13.1–33 mm CL) and 12 female (27.2–32.2 mm CL) H. gibbosus from the same station as the parasites from this station of which at least two probably the same host specimens cited by Kensley (1979).

A few details of the description by Kensley (1979) require clarification. He noted that the female holotype had an antenna with “a simple digitiform process attached to outer region of antennular lamella.” However, the antenna is not fused (unless very basally, see Fig. 3M), it is clearly separated from the antennule (unlike in his Fig. 3A which shows the antennules and antennae as one large plate). Kensley (1979) drew the antennule of the cryptoniscus larva accurately (compare his Fig. 1A with Fig. 3O herein); however, he described the second segment of the antennule as “tripartite” (cited by Brusca & Wilson (1991) as a “trilobed second article”) but which is not of three parts as this segment bears a small, slender articulated ramus on the distomedial margin that is not, strictly speaking, part of the segment. Additionally, Kensley (1979) drew the antenna of the cryptoniscus larva with four basal and two flagellar segments and described them as “of 4 relatively elongate proximal segments, and few distal articles (some possibly missing),” but the right antenna (Fig. 3N) shows the characteristic 4+5 basal and flagellar segment count of dajids (Boyko & Williams 2015). Only the type 1 male is known from this species.

There is a female specimen, probably of this species, in the Naturalis Biodiversity Center (formerly Rijksmuseum van Natuurlijke Historie; RMNH.CRUS.I.6430; not examined) with an erroneous spelling of the species name as “tribbus” on the label; it was collected from Western Samoa ex Heterocarpus sibogae de Man, 1917. Given that Kensley's (1979) specimens were obtained from H. gibbosus, the occurrence of the species on H. sibogae is not surprising. The specimen should be examined, but we were unable to borrow it during the COVID 19 pandemic (Pennisi 2020).

Brandt & Janssen (1994) stated that “Zonophryxus dodecapus and Z. trilobus are characterized by six pereopods” but as far as is known only the immature females of Z. trilobus have six pairs of pereopods whereas the mature females have five pairs; this is in contrast to the mature females of Z. dodecapus which can have five or six pairs when mature (see Remarks under that species below).

Zonophryxus grimaldiiKoehler, 1911 

• Zonophryxus grimaldiiKoehler, 1911:16–22, 31, Figs. 13, 14 (36°14′N, 08°06′W, 1401 m).—Searle, 1914:370 (mention).—Holthuis, 1949:212, 213 (mention).—Danforth, 1976:78, 79 (mention).—Brandt & Janssen, 1994:350 (mention).—Junoy & Castillo, 2003:304 (list).—Raupach & Thatje, 2006:439 (mention).—Shimomura et al., 2010:9, 10 (mention).—Diego, 2012:133 (mention).—Nagler et al., 2020:342 (mention).

Mature holotype female (16 mm TL) (most likely deposited in the Oceanographic Museum of Monaco but this has not been verified).

36°14′N, 08°06′W, 1401 m.

Known only from the type locality.

1401 m.

Female, 16 mm TL.

Heterocarpus grimaldii A. Milne-Edwards & Bouvier, 1900 (probable; see Remarks).

See Koehler (1911).

This species is only known from the female holotype, and this is the only species in the genus to have been described from, and remain known only from, a single specimen. Koehler (1911) provided a lengthy description of the female but only provided ventral and lateral whole body illustrations. The type host was not known for certain by Koehler (1911), but he thought H. grimaldii was likely, based on the number of specimens of that species collected with the holotype of Z. grimaldii.

Zonophryxus quinquedensBarnard, 1914 

• Zonophryxus quinquedensBarnard, 1914:228–230, pl. 22 (Cape Point, South Africa, 470–700 fms (=860–1280 m), ex Nematocarcinus sp. (see Remarks).—Stebbing, 1914:48 (mention).—Barnard, 1940:495 (list).—Holthuis, 1949:210, 212 (mention).—Barnard, 1950:674 (mention).—Taberly, 1954:9, 10 (mention).—Danforth, 1976:79 (mention).—Lopretto, 1983:87–97, Figs. 1–45 (off South Orkney Island, 62°48′W).—Brandt & Janssen, 1994:343–350, Figs. 1–5 (Weddell Sea, 69°58.9′S, 05°08.5′E, 665 m).—Raupach & Thatje, 2006:439–442, Fig. 1 (Weddell Sea, 71°18′S, 13°56′W–71°18′S, 13°58′W, 900–1040 m, ex Nematocarcinus lanceopes Spence Bate, 1888).—Wilson, 2009:179–183, 186–189, 191 (phylogenetic placement).—Shimomura et al., 2010:9, 10 (mention).—Boyko et al., 2013:499, Figs. 1, 2 (placement in phylogenetic tree).—Vogt, 2016:1409, Fig. 7B (mention, figure reproduced from Raupach & Thatje 2006).—Gómez-Gutierrez et al., 2017:164 (mention).—Zhang et al., 2019:1806 (phylogenetic placement).—Nagler et al., 2020:340, 342, 348.

4 mature females, 1 juvenile female, 1 male, 3 cryptoniscus larvae (all syntypes) (SAM A270-1, A2276 fide Barnard, 1914; now SAM 16641, 16782, 17101 fideBrandt & Janssen 1994).

“Cape Point NE. by E. distant 36 miles, 650–700 fathoms”/“Cape Point ENE., distant 36 miles, 66 fathoms”/“Cape Point NE. ¾ E., distant 29 miles, 470 fathoms.”

South Africa, Weddell Sea.

860–1280 m.

Type host probably Nematocarcinus longirostris Spence Bate, 1888 (see Remarks); Nematocarcinus lanceopes Spence Bate, 1888.

Females to 27 mm, males to 7 mm (fide Lopretto, 1983).

See Lopretto (1983) and Brandt & Janssen (1994).

The identity of the type host is not known, but Barnard (1914) stated that several potential host species were in the same bottles as the syntypes but that one bottle with a single female Z. quinquedens contained only an unidentified species of Nematocarcinus A. Milne-Edwards, 1881 (later identified as N. longirostris Spence Bate, 1888; see Barnard 1950); this led Barnard (1914) to conclude that N. longirostris was the likely host. The finding of Z. quinquedens on a specimen of N. longirostris by Brandt & Janssen (1994) supports Barnard's (1914) conclusion; however, Brandt & Janssen (1994) apparently were unaware of Barnard's (1950) paper in which he identified his earlier (1914) record of Nematocarcinus sp. as N. longirostris. This species is the only one in the genus known to parasitize hosts outside of Pandalidae.

Lopretto (1983) provided a thorough redescription of the species but did not state at what depth or from what hosts his specimens were collected. Both the type 1 and type 2 males are known from this species (Lopretto 1983).

Raupach & Thatje (2006) reported their specimens from Nematocarcinus lanceopes, a host they stated was previously known for Z. quinquedens from Brandt & Janssen's (1994) paper, but the species cited as host in the latter paper was actually N. longirostris. The notation in Boyko et al. (2013) that the 18s rDNA sequence for this species was novel was incorrect as it originated from the data of Raupach & Thatje (2006).

Zonophryxus dodecapusHolthuis, 1949 Fig. 4

• Zonophryxus dodecapusHolthuis, 1949:3–8, Figs. 1, 2, pl. 1 (Los Cristianos, Tenerife, Canary Islands, 210 m, ex Parapandalus narval (J. C. Fabricius, 1787) (= Plesionika narval (J. C. Fabricius, 1787)).—Danforth, 1970c:33 (mention).—Kensley, 1979:670 (mention).—Lopretto, 1983:93, 95, 96, 97 (mention).—Brandt & Janssen, 1994:343, 347 (mention).—González Pérez, 1995:100 (mention), Fig. 52 (color photograph in situ on Plesionika narval (J. C. Fabricius, 1787).—González & Santana, 1996:179 (record from off La Gomera, Canary Islands, ex P. narval).—Trilles, 1999:287, 299, 300, Figs. 8.5B, C, 8.19A, B, 8.21C (figured after Holthuis 1949).—Raupach & Thatje, 2006:439 (mention).—Castello & Junoy, 2007:26 (list).—Shimomura et al., 2010:9, 10, 17 (mention).—Boyko & Williams, 2012:401 (mention).—Diego, 2012:132, 133, Fig. 1 (Cantabrian Sea, ex Plesionika heterocarpus (A. Costa, 1871)).—Boyko et al., 2013:499, Figs. 1, 2 (placement in phylogenetic tree).—González, 2015:6 (mention).—Zhang et al., 2019:1806, Fig. 5 (placement in phylogenetic tree).

• Zonophryxus dodecarpus [sic] Brandt & Janssen, 1994:350 (mention).

• Not Zonophryxus dodecapus: Danforth, 1976:78, 79 (Guam, 274 m, ex Heterocarpus ensifer A. Milne-Edwards, 1881).—Ross, 1983:167 (list) (? = Zonophryxus retrodensRichardson, 1903).

1 ovigerous female with 6 pairs of pereopods (12.0 mm TL), 1 mature male (2.8 mm TL), ex Plesionika narval (J. C. Fabricius, 1787), 12.0 mm CL (excluding rostrum; head only, cannot sex), Candelaria, Tenerife, Canary Islands, ca. 150 m depth, coll. L. M. Abad, 10 Jan 2010 (USNM 1659606). 1 ovigerous female with 5 pairs of pereopods (11.0 mm TL), 1 mature male (2.7 mm TL), ex P. narval, 13.5 mm CL (excluding rostrum; head only, cannot sex), Candelaria, Tenerife, Canary Islands, ca. 150 m depth, coll. L. Moro Abad, 10 Jan 2010 (USNM 1659607).

5 females and 2 males (1 syntype is RMNH.CRUS.I.1712; see Remarks) (not examined).

Los Cristianos, Tenerife, Canary Islands, 210 m depth.

Canary Islands and Cantabrian Sea.

150–210 m.

Plesionika narval (J. C. Fabricius, 1787) (type host); Plesionika heterocarpus (A. Costa, 1871).

Females to 12 mm TL; males to 3 mm.

See Holthuis (1949).

Examination of the two pairs of specimens cited above shows that characters of both the males and females are in agreement with the description of the species by Holthuis (1949) with the notable exception that one female has only five pairs of pereopods, not the six pairs that are the basis of the species name. This variability in pereopod number is similar to that seen in females of species in the genus Holophryxus, although in that case, the sixth pereopods are said to be lost during development (Rustad 1935, Butler 1964, Coyle & Mueller 1981, Wasmer 1988). In Z. dodecapus, the presence/absence of the sixth pereopods may represent phenotypic plasticity, not a developmental loss, as both females examined here were ovigerous. Identification of specimens of Zonophryxus should therefore not rely on presence of six pairs of pereopods as a species-level character. The specimen with five pairs of pereopods (Fig. 4) was preserved in 100% ethanol and was the source of the 18s rDNA molecular data (GenBank number KF765768) for the species given in Boyko et al. (2013); the specimen with six pairs of pleopods was formalin-fixed. Only the type 1 male is known from this species.

In life, mature female specimens of Z. dodecapus exhibit a bright yellow coloration corresponding to the eggs and ovary in the main portion of the body (Fig. 4), with the anterior end and periphery a pale white/translucent coloration; this is similar to the freshly caught but probably not live individual of Z. dodecapus photographed by González Pérez (1995: Fig. 52). There are also four dark brown/black spots deeply embedded in the body and obscured by eggs in the posterior region of the photographed specimen; these spots are reminiscent of those described by Field (1969) for the dajid Notophryxus lateralis G. O. Sars, 1885. These spots are still visible in the preserved photographed specimen, but no such spots can be seen in the other preserved specimen. Live coloration of females has been described in a few related dajid species, including Z. retrodens that exhibits a pale yellow central region (likely corresponding to the developing eggs) and with marginal region of translucent white (Shimomura et al. 2010, Fig. 1). Rustad (1935) and Greve & Johannsessen (1981) reported that females of Holophryxus richardiKoehler, 1911 varied in color with specimens having light yellow, orange, or red coloration, possibly corresponding with maturation; Rustad (1935) indicated that the red coloration matched that of the liver of the host. Huang et al. (2018: Fig. 5A, B) found females of Holophryxus fusiformisShiino, 1937 varied in color with the pereon being white, pale yellow, beige, or orange, whereas the pleon ranged from white to pale green. In fact, they reported that fishermen collecting host shrimp from Taiwan “call these objects ‘corn kernels' because of the similarities in color and size” (Huang et al. 2018). Similarly, Butler (1964) described the color of Holophryxus alaskensisRichardson, 1905a as “maize.”

Danforth (1976) reported on six females and two males from Heterocarpus ensifer, collected from 900 ft (=274 m) depth off Guam; he did not figure the specimens but did indicate that the females had six pairs of pereopods and used this as the defining character to place an identification on his specimens. Given that it is unlikely that Z. dodecapus occurs in both the Canary Islands and Guam, it is more likely that Danforth (1976) actually had another species. It is possible that the Guam specimens were Z. retrodens, although each female had six pairs of pereopods instead of the five found on the holotype and the Japanese specimens of Shimomura et al. (2010) (such plasticity is now documented in females of the genus). This conclusion is supported by the fact that H. ensifer was one of the shrimps collected from the same station as the holotype of Z. retrodens. Unfortunately, the Guam specimens appear to be lost (Don Cadien, pers. comm.) and recollection is required. The listing of Z. dodecapus in Ross (1983) was based only on Danforth's (1976) Guam record.

There is one female in RMNH labeled “paratype,” but as Holthuis (1949) did not designate a holotype, it is a syntype; the repository of the other syntypes is not known.

Zonophryxus cf. dodecapusHolthuis, 1949 

• Zonophryxus dodecapusHolthuis, 1949.—Thoma & Heard, n.d.:3, 5 (list).

1 mature female (14.9 mm TL), host unknown, “Pelican” Sta P-11, off Cape Canaveral, FL, 27°54′N, 79°45′W, 235 fms (430 m), 11 Mar 1956 (USNM 99555).

According to the specimen label, this female was found “loose in jar” containing Hymenopenaeus robustus Smith, 1885 (= Pleoticus robustus (Smith, 1885)), Plesionika acanthonotus (Smith, 1902), Plesionika ensis (A. Milne-Edwards, 1881), and Glyphocrangon longleyi Schmitt, 1931. Based on the host choices of other species of Zonophryxus, the most likely host was one of the species of Plesionika. Thoma & Heard (n.d.) listed Z. dodecapus among the fauna of the South Atlantic Bight but did not cite the source of their record and only reproduced the drawings of Holthuis (1949). The female examined has six pairs of pereopods, as also found in the syntype females of Z. dodecapus as well as one of the two females examined during the present study. We are unable to find any obvious morphological differences between the Florida female and those from the Canary Islands; however, due to there being only a single Floridian female lacking a male, as well as the uncertainty of the host, we are noncommittal about the identity of this species at the present time.

Zonophryxus sp.

• Zonophryxus [sp. or spp.] Montagne & Cadien, 2001:203, 205 (Southern California Bight, ex Pantomus affinis Chace, 1937 and Plesionika trispinus Squires & Barragan, 1976).

Both hosts cited above occurred at multiple stations, but the precise localities of those found with parasites was not given by Montagne & Cadien (2001). The identity of these purported specimens of a Zonophryxus species, and whether more than one species is present, awaits examination of material from the Southern California Bight.

Zonophryxus probisowa, new species Figs. 5, 6

urn:lsid:zoobank.org:pub:E208CA4D-D822-4B14-828A-73EED7A8FE38.

Mature female holotype (8.0 mm TL), mature male allotype (2.5 mm TL), Peru, 03°48′S, 81°22′W, 615 m depth, coll. E. del Solar, 15 Mar 1971, ex Heterocarpus hostilis Faxon, 1893, female, 14.3 mm CL (excluding rostrum) (USNM 235230).

Peru, 03°48′S, 81°22′W, 615 m depth.

Known only from the type locality.

615 m.

Heterocarpus hostilis Faxon, 1893.

Female 8.0 mm TL; male 2.5 mm TL.

The species name is an arbitrary combination of letters used as a word, formed as an acronym of the journal name, Proceedings of the Biological Society of Washington (1880–2021); it is indeclinable.

Female body ovate (Fig. 5A, B), head, pereon, and pleon fused, widest in middle, dorsally convex with faint traces of segmentation; ventral body surrounded by marginal extension, broad anteriorly and posteriorly, thin laterally; small notches visible on lateral margins indicating some pereonal segments; posterior margin with closely approximated row of nine large triangularly-shaped processes (Fig. 5A, B). Ventral side of body concave with six pairs of isomorphic pereopods, five pairs closely approximated from head to midpoint of body, sixth pair near posterior margin of body at the base of sixth oostegites (Fig 5B). Antennules as recurved flat lobes, posteriorly tapering and surrounding buccal cone (Fig. 5C). Antennae small, digitiform, situated behind and extending anterolaterally from antennules (Fig. 5C). Maxilliped of two ovate lobes (Fig. 5F), with digitiform, slightly curved appendix (not shown in figure, compare to Fig. 3J). Sternal plate distinct below oral cone, triangular in shape at anterior end and continuing as ridge between oostegites. Oostegite 1 large with subquadrate anterior lobe and recurved, tapering posterior lobe (Fig. 5D, E), internal ridge smooth; oostegites 2 and 3 small, distally tapering (Fig. 5G); oostegite 4 small, subquadrate (Fig. 5H); oostegite 5 large, subquadrate, basally fused to small, ovate oostegite 6 (Fig. 5I).

Type 1 male dorsoventrally flattened (Fig. 6A, B). Head ovate, fused with pereomere 1, dorsal surface slightly concave medially and upturned at distal margin (Fig. 6A). Antennule as small indistinct lobe bearing few setae, merged with frontal margin (Fig. 6D). Antennae non-symmetrical: left antenna of six(?) segments, basal segment as large as others combined; right antenna of two(?) segments, blade-like distal segment more than two times as long as basal triangular segment (Fig. 6F). Pereomeres 2–6 free, gradually increasing in width posteriorly; pereomeres 2 and 3 anterolaterally curved, 4 and 5 laterally directed, 6 and 7 posterolaterally directed (Fig. 6A). Seven isomorphic pereopods present (Fig. 6B, G, H). Spherical cells of indeterminant identity dispersed within pereomeres and pleomeres; 82 ± 9 μm (n = 8) in maximal diameter. Pleomeres fused with pleotelson, forming single ovate, elongate pleon (Fig. 6A, B). Pleon affixed near ventrodistal margin of pereomere 7 and extending posteriorly, lacking pleopods or uropods (Fig. 6A, B).

Although the male is somewhat similar in morphology to that of Z. retrodens, the strongly developed, closely approximated, posterior triangularly-shaped processes on the pleon of the female indicates that the two species are distinct, as those processes are short and more widely separated in Z. retrodens. The allotype male of Z. probisowa n. sp. appears to be going through a molt, as evidenced by the asymmetrical nature of the antennae, the cuticle lifting off posteriorly from pereomere 6, and the “shrunken” appearance of the posterior pereomeres and pleon (Fig. 6A, B). Only the type 1 male is known from this species.

The morphology of the posterior margin of the pleon of the female is unique in the genus and separates Zonophryxus probisowa n. sp. from all others previously described. Although the holotype of Z. probisowa n. sp. bears six pairs of pereopods, a character state previously reported only in Z. dodecapus, the variability in pereopod number in that species reported on herein indicates that this character should not be used to distinguish species.

Key to species of ZonophryxusRichardson, 1903 based on females
The only other key to species was given by Lopretto (1983), but most characters in that key, such as antennal segment count and number of pereopods, were either incorrectly interpreted or are variable within at least some species.
• 1a.

  Ventrolateral lobes of mature female converging posteriorly, forming v-shape 2

• 1b.

  Ventrolateral lobes of mature female not tapering 3

• 2a.

  Oostegite 6 of mature female separated from oostegite 5 along most of lateral margin Z. grimaldiiKoehler, 1911 

• 2b.

  Oostegite 6 of mature female fused with oostegite 5 along most of lateral margin Z. trilobusRichardson, 1910 

• 3a.

  Oostegite 6 of mature female separated from oostegite 5 along most of lateral margin 4

• 3b.

  Oostegite 6 of mature female fused with oostegite 5 along most of lateral margin 6

• 4a.

  Triangularly-shaped processes on posterior margin of pleon tightly bunched together, overlapping Z. agassizi (Richardson, 1905)

• 4b.

  Triangularly-shaped processes on posterior margin of pleon not bunched together, not overlapping 5

• 5a.

  Triangularly-shaped processes on posterior margin of pleon short, scarcely visible in dorsal view Z. retrodensRichardson, 1903 

• 5b.

  Triangularly-shaped processes on posterior margin of pleon long, distinctly visible in dorsal view Z. probisowa n. sp.

• 6a.

  Sternal plate with posterior knob (see Lopretto, 1983: fig. 23) Z. quinquedensBarnard, 1914 

• 6b.

  Sternal plate without posterior knob (see Holthuis, 1949: Fig. 1i) Z. dodecapusHolthuis, 1949 

Thanks to L. Moro Abad, whose inquiry for assistance in identifying the Canary Island specimens back in 2010 led to the present study; the color photos were also kindly provided by him. Thanks also to Cheryl Bright and Frank Ferrari for facilitating the loan of USNM material and to Don Cadien for information about Guam specimens. We thank the recent editors (Stephen Gardiner and Rick Hochberg) of the Proceedings of the Biological Society of Washington for their work on this manuscript and the others that they have worked on for us and many colleagues over the years. The comments of two anonymous reviewers greatly improved the manuscript.