Progebiophilus upogebiae ( Hay, 1917 )

Boyko, Christopher B., Williams, Jason D. & Shields, Jeffrey D., 2017, Parasites (Isopoda: Epicaridea and Nematoda) from ghost and mud shrimp (Decapoda: Axiidea and Gebiidea) with descriptions of a new genus and a new species of bopyrid isopod and clarification of Pseudione Kossmann, 1881, Zootaxa 4365 (3), pp. 251-301 : 269-273

Progebiophilus upogebiae ( Hay, 1917)

Figs 5D, E , 6 , 7

Pseudione upogebiae Hay, 1917: 572 –573, pl. 100, figs. 7–12 (type locality: Beaufort, North Carolina, U.S.A., infesting Upogebia affinis (Say, 1818)) .—Nierstrasz & Brender à Brandis, 1923: 72, 76 (list).— Brian & Darteville, 1941: 350 –351 (mention).— Pearse, 1947: 326 (part) (Beaufort, North Carolina, infesting U. affinis ).— Shiino, 1951: 32 (mention).— Catalano & Restivo, 1965: 203 (list).—Lemos de Castro, 1965: 11–14, figs. 1–11 (Ceará, Brazil, infesting Upogebia sp.; identified as U. omissa Gomes Corrêa, 1968 in Lemos de Castro, 1970 ).— Schultz, 1969: 325, fig. 520 (list; key).—Lemos de Castro, 1970: 3, 5, pl. 3,figs. 15–17 (Ceará, Brazil, infesting U. omissa ).— Restivo, 1970: 314 (mention).— Restivo, 1971: 71, table 1 (list).— Wass, 1972: 147 (York River, Virginia, U.S.A., infesting U. affinis ).— Restivo, 1975: 153, table 1 (list).— Markham, 1977: 813, 816 (synonymy of Phyllodurus robustus Pearse, 1953 ).— Kelley, 1978: 169 (list).— Lawler, 1978: 310 (list).— Bourdon, 1981b: 127 (mention), 128 (key to males of the genus).— Williams, 1984: 192 (mention).— Fox & Ruppert, 1985: 53, 196, 289, 301 (South Carolina, infesting U. affinis ).

Pesudione [sic] upogebiae — Hay & Shore, 1918: 408 (Beaufort, North Carolina, infesting U. affinis ).

P. upogebiae — Van Name, 1920: 72 (mention).

P. urogebiae [sic]— Popov, 1929: 13 (mention).

Ps. urogebiae [sic]— Popov, 1929: 14 (mention).

Pseudodione [sic] upogebiae — Pearse, 1945: 305 (Beaufort, North Carolina, infesting U. affinis ).— Williams, 1965: 104 (mention).

Pseudione panopei Pearse, 1947: 326 –328, figs. 1–11 (Beaufort, North Carolina, infesting Panopeus herbstii H. Milne Edwards, 1934 , but see below).— Schultz, 1969: 328, fig. 525 (key).— Danforth, 1970b: 49, 153 (list), fig. 33E, F.— Markham, 1975: 61 (report on type material).— Kelley, 1978: 169 (list).— Markham, 1988: 56 (list) (new synonymy).

Phyllodurus robustus Pearse, 1953: 235 –237, figs. 131–143 (type locality: Alligator Point, Florida, infesting U. affinis ).— Lemos de Castro, 1965: 12 (mention).— Williams, 1965: 104 (mention).— Menzel, 1971: 76 (list).— Markham, 1977: 813, 816 (synonymy with P. upogebiae ).— Williams, 1984: 192 (mention).

Pseudione urogebiae [sic]— Schultz, 1969: fig. 520.

Pseudoione [sic] furcata — Kaestner, 1970: 463 (mention occurrence on “Gulf coast” [Gulf of Mexico], infesting unknown host) (not Orthione furcata (Richardson, 1904)) .

Progebiophilus upogebiae — Markham, 1988: 4, 9–12, 17, 56, fig. 3 (syntype and other material, Beaufort, North Carolina, U.S.A., infesting U. affinis ).— Salazar-Vallejo & Leija-Tristán, 1990: 423, 428 (mention), 429 (key), table 1.— Williams, 1993: 37 (mention), 44 (Barra del Tordo, Mexico, infesting Upogebia felderi Williams, 1993 ).— Kazmi & Bourdon, 1997: 62 (mention).—Brasil-Lima, 1998: 636 (list).—Campos & de Campos, 1998: 288, 293 (mention).— Markham, 2001: 198, 200 (list).— Markham, 2005: 86 (Indian River Lagoon, Florida, infesting U. affinis ).— Heard et al., 2007: 26 (mention).— Román-Contreras, 2008b: 103 (mention).—An et al., 2009: 234 (list).— Schotte et al., 2009: 980 (list).

Progebiophilus urogebiae [sic]— Salazar-Vallejo & Leija-Tristán, 1990: 428 (mention).

“bopyrid” Williams, 1993: 44 (Barra del Tordo, Mexico, infesting U. felderi ).

not Pseudione upogebiae — Pearse, 1947: 326 (in part, Beaufort, North Carolina, U.S.A., infesting Upogebia affinis ) (= Orthione furcata ).

Material examined. United States: Two ovigerous female paratypes of Pseudione upogebiae (9.8 – 11.1 mm), mature male paratype (3.1 mm), ex branchial chambers of Upogebia affinis (sizes and sexes unknown), Beaufort, North Carolina, coll. W. P. Hay, 17 Aug 1915, (USNM 48370); mature holotype female of Pseudione panopei (12.1 mm), ex branchial chamber of “ Panopeus herbstii ” [erroneous identification; see Remarks; size and sex of host unknown], Beaufort, North Carolina, coll. A. S. Pearse, 22 Aug. 1946 (USNM 82669; body excepting most of abdomen in EtOH, abdomen mounted on slide); mature allotype male of P. panopei , same data as holotype (USNM 82670; mounted on slide); paratype female of P. panopei , same data as holotype (USNM 82671; mounted on slide); mature female (likely ovigerous but no eggs currently present in vial) (9.9 mm), ex branchial chamber of “ Uca pugilator ” (Bosc, 1801) [incorrect host identification; see below], Beaufort, North Carolina, coll. A. S. Pearse, 20 Jul 1946 (USNM 84047; also present in vial was a mature male Probopyrus pandalicola (Packard, 1879) (3.0 mm); mature male (4.5 mm, USNM 1424905) and single first oostegite), ex branchial chamber of “ Panopeus herbstii ” [incorrect host identification; see below], Beaufort, North Carolina, coll. A. S. Pearse, 22 Aug 1946 (USNM 84049; also present in vial was an ovigerous female (11.8 mm) of Orthione furcata , now USNM 1424906); unidentifiable fragments, ex U. affinis (as per label; host not in vial), Beaufort, North Carolina, coll. A. S. Pearse, 13 Jun 1946 (USNM 84050); mature female (likely ovigerous but no eggs currently present in vial) (8.3 mm), mature male (3.2 mm), ex branchial chamber of U. affinis (as per label; host not in vial), Beaufort, North Carolina, coll. A. S. Pearse, 17 Jun 1946 (USNM 84051); ovigerous female (10.0 mm), mature male (3.3 mm), ex right branchial chamber of U. affinis, Goose Cove sand spit, Cedar Key, Levy County, Florida, 29.133° –83.037°, 0–1 m depth, coll. G. F. Paulay & UF Invertebrate Zoology class (UF 044634).

Mexico: Ovigerous female (9.0 mm, part sacrificed for molecular work), mature male (2.7 mm), ex right branchial chamber of female paratype of Upogebia felderi (8.0 mm CL), Stn 6, Barra del Tordo, mouth of Rio Carrizal , Tamaulipas, inshore of grass beds, yabbby pump, coll. D. L. Felder & R. Tinnin, 24 May 1982 ( ULLZ 3019 ) ; mature female (7.0 mm, ½ sacrificed for molecular work), ex left branchial chamber of female U. felderi (8.0 mm CL), Stn 6, Rio Carrizal , Barro del Tordo, Tamaulipas, coll. D. L. Felder & R. Tinnin, 24 May 1982 ( ULLZ 10200 ) ; ovigerous female (7.8 mm), mature male (2.5 mm), ex branchial chamber of U. felderi (sex and CL unknown), Barra del Tordo, mouth of Rio Carrizal , Tamaulipas, oyster covered beaches near grass beds, shallow and intertidal, coll. D. L. Felder, Rabalais et al., 14 Jun 1978 ( USNM 1084297 ex ULLZ 3071 ) .

Distribution. Virginia, U.S. A to Brazil, and northern Gulf of Mexico west to Tamaulipas, Mexico.

Hosts. Upogebia affinis (Say, 1818) (type host), and U. felderi Williams, 1993 . The record of Panopeus herbstii H. Milne Edwards, 1834 , as host of the type specimens of Pseudione panopei is in error; see below.

Remarks. Pseudione panopei has always been a puzzle because it is the only species in Pseudioninae , outside those of Gigantione Kossmann, 1881 , that has been reported from a brachyuran host. Markham (1975) examined Pearse's type material of Pseudione panopei and stated that “this species is definitely assignable to Pseudione , but there is some reason to believe that the host was incorrectly recorded.” Markham (1975) did not, however, indicate why he thought the host was not Panopeus herbstii as given by Pearse (1947). We have examined all of the type material of Pseudione panopei ( Fig. 7 ) and concur with Markham’s (1975) conclusion that the host was recorded in error. The morphological characters of the holotype female of Pseudione panopei are identical with those of Progebiophilus upogebiae (compare Fig. 6 herein with Fig. 3 in Markham 1988). The allotype male (USNM 82670) and the immature paratype female (USNM 82671) are both mounted on slides and in poor condition; both are highly distorted and their length cannot be measured accurately. The pleotelson of the male has lateral lobes that were folded somewhat when the specimen was mounted on a slide and Pearse (1947) inaccurately drew them as if they were segmented uropods.

Now that the identity of Pseudione panopei has been clarified and it is actually a species that is only known from gebiidean hosts, this leaves the following explanations for its occurrence on a brachyuran: 1) Progebiophilus upogebiae does, in fact, occur on Panopeus herbstii in Beaufort , North Carolina (and perhaps elsewhere in the host’s range) and this is an unique case of a bopyrid species found on both gebiidean and brachyuran hosts or 2) the host identity was recorded in error and the types of Pseudione panopei were actually obtained from a Upogebia host. If the former is true, then it is hard to explain why no one has subsequently found this parasite on Panopeus herbstii , which is a common and well-studied crab. Given the clear evidence of Pearse mixing multiple bopyrid species within lots (see Material Examined above), the most parsimonious explanation is that Pearse mixed up his lots with respect to host identity as well. All of Pearse’s samples except USNM 84047 (see below) include a label hand-written by Pearse (confirmed based on comparison with Pearse journals); labels include locality, date and host identification data. It is unclear why he described Pseudione panopei as a new species, but he may have been influenced by the now-discredited theory of Giard & Bonnier (1890b) that each parasite discovered on a novel host must be specifically distinct from all other previously described species.

USNM 84047 contains a female Progebiophilus upogebiae and a male Probopyrus pandalicola (Packard, 1879) (now USNM 1424905, Fig. 5C ), a species also mentioned by Pearse (1947) and providing another example of Pearse’s co-mingling of taxa and poor labeling of specimens. The host recorded on another label as “ Uca pugilator ” (now Leptuca pugilator (Bosc, 1801)) is also clearly in error. The original Pearse identification label for USNM 84047 is missing and the two labels in the vial indicate identification of the parasites as Pseudione upogebiae by Roland Bourdon. However, given that USNM 84046 and 84048 are both lots of Leidya distorta (Leidy, 1855) found parasitizing L. pugilator , we suspect that the original Pearse identification label for USNM 84047 also read L. distorta and this was changed when Bourdon examined the specimens. Both USNM 84046 and 84048 were cited in Bourdon & Bowman’s (1970) paper on Leidya but 84047, conspicuously, was not. Apparently, Bourdon did not look at the male in 84047 closely as he did not notice it belonged to Probopyrus pandalicola , but this is perhaps not surprising as he was likely focusing on the fact that the lot did not contain any Leidya specimens.

The fragmentary specimen (USNM 84050) was identified on the label as “ Pseudodione [sic] upogebia [sic].” Based on the poor condition of the specimen and Pearse’s confusion between Progebiophilus upogebiae and Orthione furcata ( Richardson, 1904) (see also Markham 1988); this vial may or may not contain fragments of P. upogebiae .

Although Hay & Shore (1918) misspelled the genus name and Markham (1988) correctly noted this fact, Markham’s citation erroneously showed the genus name as spelled correctly. The first author to report Progebiophilus upogebiae from Upogebia felderi was Williams (1993). An additional paratype lot of U. felderi (ULLZ 3017) was cited by Williams (1993) as containing a host parasitized by Progebiophilus upogebiae and there is a note to that effect in the vial, but no parasitized specimen is present; the parasite is actually deposited as USNM 1084297 (see material examined). Both the female and male from the Florida Gulf coast show no differences from the material described and figured by Markham (1988) from North Carolina ( Figs. 5D, E ) except that the present male has broad midventral tubercles on pereomeres 5–7, however, these structures are rather low and can only be seen in lateral view. The specimens examined from Cedar Key, Florida ( Fig. 6 ) are only the second record of Progebiophilus upogebiae under that name from the northeastern Gulf of Mexico; the first was that of Pearse (1953, as the type locality of the synonym Phyllodurus robustus ). However, Kaestner’s (1970) record of “ Pseudoione ” [sic] furcata Richardson, 1904 , from the “Gulf coast” is almost certainly based on misidentified Progebiophilus upogebiae .

Protozoans similar in morphology to members of the genus Cothurnia (Vaginicolidae) were attached to the pereopods of Progebiophilus upogebiae from the Gulf of Mexico ( Fig. 6C, D ). In addition, these bopyrid specimens had mesomycetozoeans (Class Mesomycetozoea, Order Eccrinales) attached to the cuticle ( Fig. 6C ). Such ectosymbionts have previously been reported from other bopyrids (Williams & An 2009) and their hosts ( Shields et al. 2015).

Figures

FIGURE 3. Acrobelione halimedae n. sp., mature holotype female (ZRC 1990.4330), ex Austinogebia spinfrons (Haswell, 1881). A, dorsal overview of female; B, ventral overview of female; C, right antennule and antenna; D, left barbula; E, right maxilliped, outer view; F, right oostegite 1, internal view; G, right oostegite 1, outer view; H, right pereopod 1; I, left pereopod 7; J, right pereomere 7 (Per7) and right lateral plate 1 (Lp1); K, left lateral plate 1; L, ventral view of fifth pleopods (Ple5) and uropods (Uro).Scale bars:A, B, E, F = 1 mm; C = 125 µm; D, = 250 µm; G–L = 500 µm.

FIGURE 7. Pseudione panopei Pearse, 1947 (= Progebiophilus upogebiae (Hay, 1917)), mature female holotype (USNM 82669). A, dorsal overview of female; B, right maxilliped, outer view; C, right barbula; D, right pereopod 1; E, right pereopod 7;F, pleon,dorsal view ofright side showing pereomere 7 (Per7) and pleomeres 1–3 (Ple1, 2 and 3); G,pleopod 2, ventral view of endopod and exopod. Scale bars:A, B, F = 1 mm; C–E, G = 500 µm.

FIGURE5. Orthionefurcata (Richardson, 1904), Probopyrus pandicola (Packard,1879), and Progebiophilus upogebiae (Hay, 1917). A, female dorsal view of O. furcata (USNM 1424906 ex USNM 84049); B, male dorsal view of O. furcata (USNM 84052); C, male dorsal view of P.pandicola (USNM 1424905 ex USNM 84047); D, male dorsal view of P. upogebiae (USNM 48370); E, left oostegite 1 of P.upogebiae, internal view (USNM 84049).Scale bars: A–E = 1.0 mm.

FIGURE6. Progebiophilus upogebiae (Hay, 1917) (UF 044634).A, female, dorsal view; B,female,ventral view with male in situ; C, seventh pereopod from left side; note the Cothurnia-like ciliate (Vaginicolidae) and Eccrinales attached directly to the pereopod (shown only on right side) as well as on the protozoans; D, close-up of single Cothurnia-like sp. with attached Eccrinales(asterisk indicatesonly specimen ofEccrinales with septa drawn).Scale bars:A, B = 1mm; C = 250µm; D = 25 µm. A, B courtesy of Gustav Paulay.