Probopyrus cf. pandalicola (Packardı 1879)

Horch, Felipe Bezerra Ribeiro ı Amanda Porciuncula & Williams, Jason D., 2019, New occurrences and host records for two species of parasitic isopods (Isopodaı Cymothoidaı Bopyridae) associated with caridean shrimps (Decapodaı Caridea) from Brazil, Journal of Natural History 53 (39), pp. 2437-2447 : 2440-2444

Probopyrus cf. pandalicola (Packardı 1879)

Figures 2 ı 3

Abbreviated synonymy (see Markham 1985; the synonymy list below includes only taxonomic resources since 1985ı see discussion for taxonomic notes and non-taxonomic references).

Bopyrus pandalicola Packardı 1879: 308 – 310 ı fig. 262 [type locality: unspecifiedı east coast of the United States].

Probopyrus pandalicola – Markham 1985: 26 – 35 ı 127 – 128 (Table 2; in part)ı 134ı figs. 7 – 8; Verdi and Schuldt 1988: 22 – 24; Kensley and Schotte 1989: 112 ı 266 (lists; in part); Jiménez and Vargas 1990: 457 – 462 ı figs. 1 – 11; Román-Contreras 1993: 689 ı 690ı 694ı 695; Brasil-Lima 1998: 209; Alvarez-León et al. 1999: 17 – 21 ı 19 (Table 1; in part)ı fig. 1; Rocha and Bueno 2000: 134 ı 137ı 138; Román-Contreras and Bourdon 2001: 918 ı 920 (Table 1)ı 922 (Table 2); Román-Contreras 2004: 153 ı 154 (Table 1)ı 156ı 157 (Table 2)ı 161ı figs. 1ı 2; Román- Contreras and Martinez-Mayén 2011: 1145 ı 1149ı 1150; Pralon et al. 2018: 6 ı 7; Saito et al. 2010: 173 (Table 1; in part)ı 179. not Probopyrus pandalicola: Campos and de Campos 1989: 29 – 34 ı 33 (Table 1); Alvarez- León 1993: 307 – 308; Alvarez-León et al. 1999: 17 – 21 ı 19 (Table 1; in part); Bunkley- Williams and Williams 1998: 149 ı 150 (Table 1; in part).

Material examined

Brazil: mature female (4.4 mm TL)ı Olivençaı Ilhéusı Bahia (14°56 ʹ 28.4 ” Sı 39°00 ʹ 39.3 ” W)ı 06/ V / 2015ı Coll. J. T. Lisboaı infesting left branchial chamber of male Palaemon northropi (Rankinı 1898) (9.8 mm CL) ( UFRGS 6630 ); Mature male (1.09 mm TL)ı same data; mature female (3.45 mm TL) and mature male (0.9 mm TL)ı infesting right branchial chamber of male P . northropi (4.5 mm CL)ı same data; mature female (2.6 mm TL)ı infesting left branchial chamber of female P . northropi (3.0 mm CL)ı same data; mature female (1.9 mm TL)ı infesting left branchial chamber of female P . northropi (3.0 mm CL)ı same data; mature female (1.5 mm TL)ı infesting left branchial chamber of female P . northropi (3.4 mm CL)ı same data; mature female (1.2 mm TL)ı infesting left branchial chamber of female P . northropi (3.5 mm CL)ı same data; mature female (2.7 mm TL) and mature male (0.9 mm TL)ı infesting right branchial chamber of female P . northropi (3.9 mm CL)ı same data .

Remarks

We have provisionally identified these specimens as Probopyrus cf. pandalicola which has been reported from P. northropi in Mexicoı Venezuelaı and Brazil ( Markham 1985). The new record from Ilhéusı Bahiaı Brazil is approximately 1200 km south of previous collections of P. pandalicola from Vila Velhaı Pernambuco. The adult female specimens of P. cf. pandalicola analysed here ( Figure 2 ) are characterised by a pyriform bodyı subtriangular cephalon with anterior margin slightly extending beyond pereionı subrectangular maxilliped with palp on anterior lobe bearing five setae and prominent spurı oostegite 1 internal ridge with five digitiform projectionsı dactyli of pereopods 1 and 7 deeply inset in propodiı and pleomeres separated laterally and pleotelson deeply bilobed. This combination of charactersı as well as those of the male ( Figure 3 )ı are closest morphologically to P. pandalicola (versus P. fl oridensis Richardsonı 1904) but without larval morphology or molecular data it is presently not possible to be more definitive in identification (see below). Howeverı the present female specimens differ from Markham ’ s (1985) material in having a broad frontal lamina ( Figure 2 (a)) (lacking frontal lamina in Markham ’ s specimens)ı antenna 2 with two articles ( Figure 2 (c)) (antenna 2 with three articles in Markham ’ s specimens) and maxilliped palp large and not inset in the distal margin of the anterior maxilliped article ( Figure 2 (eıf)) (maxilliped palp small and inset in the distal margin of the anterior maxilliped article in Markham ’ s specimens). Probopyrus pandalicola has a complex taxonomic history with multiple species being synonymised by Markham (1985) and purportedly recorded from over 15 species of freshwater and marine palaemonid shrimp ( Kensley and Schotte 1989). Howeverı Román-Contreras (1993) concluded that three species synonymised by Markham (1985) are distinct from P. pandalicola : P. bithynis Richardsonı 1904 [Louisianaı USA infesting Macrobrachium ohione (Smithı 1874) and M. olfersii (Wiegmannı 1836) ]ı P. fl oridensis [Floridaı USA infesting Palaemon paludosus (Gibbesı 1850) ]ı and P. panamensis Richardsonı 1912 [Paraisoı Panama infesting M. acanthurus (Wiegmannı 1836) ]. A fourth species P. palaemoneticola (Packardı 1881) [Atlantic coastı USA from Palaemon Weberı 1795 ] was later synonymised with P. pandalicola by Román-Contreras and Martinez-Mayén (2011) ı in agreement with Markham ’ s (1985) assessment. Adult female specimens of P. bithynis can be distinguished from P. pandalicola by horn-shaped anterolateral processes on the head and the presence of a largeı subtriangular high carina on the seventh pereopodı both of which are lacking in the material examined from Brazil. In additionı the epicaridium and cryptoniscus larvae of P. bithynis are distinct from P. fl oridensis and P. pandalicola ( Dale and Anderson 1982) . Unfortunatelyı adult specimens of P. fl oridensis and P. pandalicola are difficult to distinguish based on morphology (see Table 1 in Román-Contreras and Bourdon 2001); howeverı the larvae can be distinguished by morphometric analysis ( Dale and Anderson 1982). Jiménez and Vargas (1990) were in error when stating ‘ it is impossible to separate the larvae of P. pandalicola and P. fl oridensis’; these authors presumably were only considering epicaridium larvae and did not take into consideration the morphometric data of Dale and Anderson (1982) that showed significant differences between both the epicaridium and cryptoniscus larval stages of P. fl oridensis and P. pandalicola (as well as differences in swimming speed and pigmentation of the cryptoniscus larvae). Thusı although almost morphologically indistinguishable as adultsı P. fl oridensis and P. pandalicola appear to represent reproductively isolated species and we accept the conclusion of others that they are valid species ( Román-Contreras 1993; Rocha and Bueno 2000; Saito et al. 2010). Presently there are four species of Probopyrus recognised in Brazil: P. bithynisı P. fl oridensisı P. palaemoni Lemos de Castro and Brasil-Limaı 1974 [from Palaemon pandaliformis (Stimpsonı 1871) ]ı and P. pandalicola .

It is important to note that much work remains to be done in testing species boundaries in this group. Although P. pandalicola has been considered by some to be on both sides of the isthmus of Panama ( Kensley and Schotte 1989; Vargas-Ceballos et al. 2016)ı the presence of the species in the eastern Pacific has been questioned ( Román-Contreras 2004). These debates are amenable to testing with new collections and molecular data to determine if the species truly has such a wide geographic and host use pattern (known in some other bopyrids; see Athelges Gerstaeckerı 1862 in McDermott et al. 2010 ; Argeia Danaı 1853 in An et al. 2015 ) or represents an even more diverse cryptic species complex than currently recognised. Specimens of P. pandalicola collected from the Rhode Riverı Chesapeake Bayı MD have been sequenced for cytochrome oxidase subunit 1 (COI) and vouchered (USNM 1463140)ı thus can serve as a starting point for such work. Members of the genus Probopyrus are some of the best studied bopyrids in terms of morphology and development (e.g. Dale and Anderson 1982)ı ecology (e.g. Beck 1979 ı 1980; Chaplin- Ebanks and Curran 2007; Conner and Bauer 2010)ı and impacts on host physiology and/ or behaviour (reviewed in Brinton and Curran 2015aı 2015b). We urge researchers to appropriately preserve and voucher the parasites during future studies in order to allow for accurate identificationı particularly because some of the results on their interactions with hosts are potentially confounded by lack of taxonomic knowledge ( Conner and Bauer 2010).

Figures

Figure 2. Probopyrus cf. pandalicola (Packard, 1879), females (UFRGS 6630): (a), habitus dorsal view (4.4 mm TL); (b), habitus ventral view (4.4 mm TL); (c), antennule (left) and antenna (right) (3.45 mm TL); (d), barbula (2.6 mm TL); (e), maxilliped (2.6 mm TL); (f), maxilliped palp (2.6 mm TL); (g), maxilliped spur (2.6 mm TL); (h), oostegite 1, outer view (3.45 mm TL); (i), oostegite 1, inner view (3.45 mm TL); (j), right pereopod 1 (3.45 mm TL); (k), right pereopod 7 (3.45 mm TL). Scale bars: (a) and (b) = 1.0 mm; (c) = 0.1 mm; (d) = 0.37 mm; (e) = 0.2 mm; (f) and (g) = 0.1 mm; (h) and (i) = 0.25 mm; (j) and (k) = 0.1 mm.

Figure 3. Probopyrus cf. pandalicola (Packard, 1879), male (1.09 mm TL) (UFRGS 6630): (a), habitus ventral view; (b), habitus dorsal view; (c), antennule; (d), antenna; (e), left pereopod 1; (f), left pereopod 7. Scale bars: (a) and (b) = 0.25 mm; (c–f) = 0.05 mm.