Description of the mature female and epicaridium larva of Cabirops montereyensis Sassaman from southern California (Crustacea: Isopoda: Cabiropidae)

10 Pages·1992·5.3 MB·English

by  Clay Sassaman

PROC. BIOL. SOC. WASH.
105(3), 1992, pp. 575-584
DESCRIPTION OF THE MATURE FEMALE AND
EPICARIDIUM LARVA OF CABIROPS MONTEREYENSIS
SASSAMAN FROM SOUTHERN CALIFORNIA
(CRUSTACEA: ISOPODA: CABIROPIDAE)
Clay Sassaman
Abstract. —The cryptoniscoid isopod Cabirops montereyensis Sassaman, pre-
viously known only from Monterey Bay, California, has been collected at
Malibu, California. Diagnostic characters of the cryptoniscus larva are illus-
trated with scanning electron microscopy and the mature female and epicari-
dium larva are described. The mature female exhibits characteristics typical of
most species in the genus, especially those parasitic on pseudionine bopyrids.
The epicaridium larva differs from other described Cabiropidae in details of
the appendages and in the possession ofa prominent anal tube.
Cabirops Kossmann, 1884 is a genus of fourMacrocystis holdfasts collected at Mal-
hyperparasitic isopod crustaceans that are ibu, California, over the last three years.
brood parasites of bopyrid isopods which Comparisons of cryptoniscus larvae and
are, in turn, branchial parasites ofdecapod immature females between these collections
shrimps and crabs. Cabirops has a complex and those from Monterey Bay indicate that
taxonomy stemming from confusion about the southern California specimens represent
C
the relationship between it and Paracabi- a range extension of montereyensis. The
rops Caroli, 1953, which is now considered diagnosis of the cryptoniscus stage is illus-
ajunior synonym (Restivo 1975), and from trated, and supplemented by descriptions of
the number ofunnamed species which have several new characters, based on scanning
been assigned to this genus. I have reviewed electron microscopy.
the nomenclature of the fifteen described Neither the mature female nor the epi-
species of Cabirops elsewhere (Sassaman caridium stage ofC. montereyensishas been
1985) and follow those conventions here; described. The southern California collec-
the superfamily nomenclature has been re- tions include a mature female brooding ep-
viewed recently by Grygier & Bowman icaridium stage larvae; these stages are de-
(1990, 1991). scribed and compared with similar stages in
Although the genus is widespread in its other species.
occurrence throughout the world, only one
species, Cabirops montereyensis, has been
Superfamily Cryptoniscoidea
described from the entire eastern Pacific
Kossmann, 1880
Ocean. Its known distribution has been lim- &
Family Cabiropidae Giard
ited to Monterey Bay, California; previous
Bonnier, 1887
collections of its definitive host, Aporobo-
Cabirops Kossmann, 1884
pyrus muguensis, parasitizing porcellanid
Cabirops montereyensis Sassaman, 1985
crabs of the genus Pachycheles in central
Figs. 1A-I, 2, 3A-H, 4A-I
and southern California did not yield this
species (Sassaman 1985). Materials examined.—Specimens from
I have found specimens of Cabirops in southern California were extracted from
576 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
Macrocystis holdfasts collected by Rimmon tributions of the coxal plate denticles (Fig.
C. Fay (Pacific Bio-Marine Laboratories) at IB), the setal comb on the dactyl of pe-
Malibu, California, at depths from 8 to 10 raeopod III (Fig. 1C), the bifid dactyls of
m
as follows: 8 Jan 1988, 1 cryptoniscus peraeopods VI (Fig. ID) and VII, and the
larva from branchial cavity of Pachycheles branched setae at the base of the uropodal
holosericus parasitized by an unpaired fe- endopod (Fig. IE). The fused mouthparts
male Aporobopyrus muguensis; 22 May of the oral cone are shown in Figure 1F. I
1989, 1 cryptoniscus larva found free in res- previously characterized the medial setae
idue from holdfast; 2 May 1990, 1 crypton- arising from the pleopodal sympods as sim-
iscus larva and 1 immature female in mar- ple; they actually terminate in a trifid pro-
supium of 1 unpaired A. muguensis and 2 cess, the middle tine being barbed (Fig. 1G)
cryptoniscus larvae and 2 females (1 im- as illustrated by Goudeau (1970) for Hemi-
mature and mature) in marsupium ofsec- oniscus balani and Nielsen & Stromberg
1
ond (paired) A. muguensis, each bopyrid in (1973b) for Parapodascon stebbingi.
branchial cavity of P. holosericus, 1 1 ad- To the previous description ofthis stage
ditionalA. muguensis unparasitized; 4 Feb- (Sassaman 1985) I add that the dorsal cu-
ruary 1991,9 cryptoniscus larvae on 1 paired ticle of the head has scattered circular de-
A. muguensis in branchial cavity of P. ho- pressions containing a single, central, short
losericus, 6 additional A. muguensis unpar- cilium (Fig. 1H) reminiscent of structures
&
asitized. mentioned by Nielsen Stromberg (1973a)
All material was fixed in 70% ethanol ex- and recently described by Bocquet-Vedrine
cept the cryptoniscus collected in May 1989 (1985) in Crinoniscus equitans. In addition,
and six cryptoniscus larvae collectedin Feb- the dorsal surface of the cephalon and the
ruary 1991, which were fixed in 3% glutar- pre-antennal ventral surface contain rows
aldehyde in sea water. The May 1989 spec- of circular button-like structures (Fig. 1H,
imen was subsequently prepared for 1) which are easily observed as dark circles
scanning electron microscopy (SEM) with under highly polarized bright light. Al-
&
theprotocol ofNielsen Stromberg(1973a), though initially identified as glandular se-
gold-palladium coated, and examined with cretions in Cironiscus dahli on the basis of
a Philips 5 1 5 microscope. Epicaridium lar- azocarmine-positive histological staining
vae were dissected from the marsupium of (Nielsen & Stromberg 1965), these struc-
SEM
the mature female and prepared for tures clearly have a morphological basis in
by the same procedure. Cabirops montereyensis (Fig. 1H, I) and are
The 3 females collected on 2 May 1990, evident in SEMs of several other crypton-
&
their accompanying males, bopyrid hosts, iscoid species (Nielsen Stromberg 1973b).
and decapod hosts have been deposited with Their function and their taxonomic useful-
the Los Angeles County Museum ofNatural ness have yet to be determined.
LACM
History under catalog number 90- Mature female.—The 2 immature fe-
90. males collected 2 May 1990 correspond in
Cryptoniscus larva.—Comparison of the morphology with the Stage A and Stage B
cryptoniscus larvae from Malibu with ma- females previously illustrated (Sassaman
terial from Monterey Bay indicates that the 1985). This similarity further supports the
southern California specimens are Cabirops identification of the southern California
montereyensis. Diagnostic characteristics of specimens as Cabirops montereyensis which,
C. montereyensis that are also present in the in the immature female stages, differs from
new material include the configuration of other described species of the genus (Sas-
the lateral dentition ofthe 2nd article ofthe saman 1985). Only the mature female (Fig.
1st antenna (Fig. 1A), the shapes and dis- 2) is described here.
VOLUME NUMBER
105, 3 577
Fig. 1. Cabirops montereyensis, cryptoniscus larva. A, Second article ofthe first antenna; B, Coxal plates of
peraeonal segments I-VII; C, Dactyl ofperaeopod III; D, Distal tip ofdactyl ofperaeopod VI; E, Lateral margin
ofthe uropodalendopodat itsbase; F, Oral cone; G, Distal tip ofmedial seta ofpleopodal sympod 1; H, Sensory
pit on dorsal surface ofthe cephalon at anterior margin; I, Detail ofcephalic birefringent button. Scale bar in
B = 50 /urn; scale bars in A, C, E, F, G, and H = 5 yum; scale bars in D and I = 1 yum.
Description: Body strongly flexed ven- Cephalon indicated by paired cephalic plates
trally into U-shape. Maximum dimension and cup-shaped cephalic appendages pro-
in flexed state 1.8 mm; total length (if un- jecting forward. Peraeon indicated dorsally
flexed) approximately 2.8 mm. Entire body by 7 regions each delimited by chitinous
filled with hatched epicaridium larvae. transverse ribs and cuticular creases. Perae-
PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
578
Fig. 2. Cabirops montereyensis, mature female, cp, cephalic plate; ca, cephalic appendage; blp, basal lateral
plate; dip, distal lateral plate; tr, transverse rib; lr, longitudinal rib; m, marsupium; p, papilla. Scale bar = 0.5
mm.
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onal segments also indicated by 6 lateral- lobiformis (Lemos de Castro 1970), and
plate complexes composed of 2 elements, C. reverberii (Restivo 1971). Five features
basal plate attached laterally anddistal plate that are common to C. montereyensis and
projecting postero-dorsally and partially all but two ofthese species are: the body is
free. Two large, laterally expanded, ventral ventrally flexed and has a characteristic
lobes (marsupium)attachedto peraeonal re- U-shape in lateral view; laterally paired
gion. Small papilla extending ventrally on ventral swellings of the peraeonal region
each side from last peraeonal segment. Pleon form a marsupium; six lateral plate-like
with 3 regions demarcated by transverse processes are associated with the peraeon;
chitinous ribs, dorsal and ventral pleonal traces ofperaeonal segmentation are marked
regions separated by prominent longitudi- by transverse chitinous ribbing; and trans-
nal chitinous rib. Ventral border with sev- verse segmentation ofthe pleonal region is
eral irregular swellings. Pleon approximate- indicated by dorsal and ventral regions sep-
ly 1:3 total body length. arated by longitudinal ribbing.
Remarks: Adult females have been de- One species, C. perezei, lacks obvious lat-
scribed previously for eight other species of eral plates and a marsupium. It is possible
C
Cabirops: perezei (Carayon 1942a), C. that the most advanced female described by
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marsupialis (Caroli 1953, Reverberi Ca- Carayon (1942a), although brooding eggs,
talano 1963, Restivo 1975), Cabirops sp. is not fully mature and therefore does not
(Romano 1953, Attardo 1955), C. codrea- completely express the adult characters; the
nui (Bourdon 1966), C. ibizae (Bourdon female he described subsequently (Carayon
1966), C. pseudione(Lemos de Castro 1970), 1942b) is clearly not fully mature. Alter-
VOLUME 105, NUMBER 3 579
natively, C. perezei may represent a some- Cabirops-Mke genus recentlydescribed from
what derived form; it is, for example, the Bopyroides hippolytes.
only Cabirops in which eyes are lacking in Among those species parasitic on pseu-
the cryptoniscus stage. The second excep- dionine bopyrids, and showing the typical
tion to the general pattern of adult female suite of Cabirops characters, there is, nev-
C
characters is lobiformis, which shows ertheless, subtle variation in morphological
none ofthe typical characteristics ofmature features. Not all descriptions have indicated
female Cabirops. Females oftwo additional the presence ofcephalic plates and cephalic
species have been described: C. lernaeodis- appendages, and the relative size and the
coides (Kossmann 1872) lacks the marsu- degree of segmentation of the pleon varies
pium and C. tuberculatus (Shiino 1942) re- considerably (e.g., Bourdon 1966; Restivo
sembles C. lobiformis in lacking most ofthe 1971, 1975). The small papilla on the ven-
typical characteristics of mature females. tral surface ofthe peraeon of C. monterey-
Both of these descriptions probably are of ensis appears to be unique.
immature females. Epicaridium larva.—General body form:
I have suggested, based on cryptoniscus in dorsal aspect of slightly flattened speci-
morphology, that Cabirops may include two mens, body drop shaped, widest at pe-
groupings of species, one associated with raeonal segment V. Length measured from
pseudionine and orbionine hosts and the anterior edge ofcephalon to posterior bor-
other associated with bopyrine and ionine der oftelson about 200 nm. Second anten-
hosts (Sassaman 1985). Mature females of nae (excluding terminal spines) extendingto
all species known from pseudionine hosts pleonal segment 1.
have been described and only C. perezei de- Cephalon: Broadly rounded, dorsal cuti-
viates from the general pattern of charac- cle smooth. No trace of eyes. Antenna 1
teristics enumerated above. In contrast, with 3 articles (Fig. 3A). Basal article in-
adult females ofspecies parasitic on ionine completely resolved, but bearing at least 1
and bopyrine hosts are less well known, but branched seta at antero-lateral corner. Sec-
it is within this group that the most notable ond article simple, with 3 branched setae at
exceptions in female morphology occur, e.g., distal edge. Third article biramous, dorsal
C C
lobiformis and perhaps tuberculatus. branch simple with 2 terminal spines, ven-
Further descriptions ofCabirops from these tral branch with 1 articulation, distal part
lattertwo host subfamilies are much needed bearing 3 terminal spines. Two aesthetascs
to clarify this hypothesis ofintrageneric het- originate at base of 3rd article. Antenna 2
erogeneity. The Cabirops sp. parasitic on of 5 articles (Fig. 3B): 2 peduncular, 3 fla-
Bopyrina ocellata is a case in point. This gellar. Distal peduncular article (Fig. 4B)
C
species has been confused with marsu- with 4 setae: 3 dorsomedial (2 branched), 1
pialis, a parasite of Gyge branchialis, and terminal. Two stout spines at distal ends of
mature females have been differently de- first 2 flagellar articles. Distal flagellar ar-
scribed by Romano (1953) and Attardo ticle with 4 short, smooth, terminal spines,
(1955). Although Romano's illustration of and 2 longer ones with regular rows ofshort
the mature female (reproduced also by At- spinules along most of distal part, spinules
tardo [1955]) does not show the chitinous more developed on shorter (outermost) of
ribbing and lateral plates, they are never- these spines (Fig. 4C) than on innerone (Fig.
theless evident in Attardo's (1955, fig. 11) 4D). Mandibles terminating in row of bi-
photograph of the spent female. Clarifica- cuspid teeth forming grinding surface
tion ofthe status ofthese bopyrine parasites flanked laterally by cylindrical processes
may also have bearing on the affinities of bearing terminal pores (Fig. 4E).
Cabirops to Bourdonia Rybakov, 1990, a Peraeon: 6 segments with appendages.
PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
580
Fig. 3. Cabirops montereyensis, epicaridium larva. A, Antenna 1; B, Antenna 2, ventral view; C, Peraeopod
I; D, Peraeopod V; E, Peraeopod VI; F, Pleopod 1; G, Pleopod 5; H, Uropod. Scale bars = 10 nm. (A-G are
to the scale shown at the lower left ofthe figure.)
Each peraeopod with 6 articles, but carpus carpal complex (Fig. 3C), peraeopods III-V
broadly fused to propodus on all peraeo- with more elongate complex, ending almost
pods forming propodocarpal complex. Pe- squarely (Fig. 3D), peraeopod VI with lon-
raeopods I and II with bulbous propodo- gest complex, tapering distally (Fig. 3E).
VOLUME 105, NUMBER 3 581
Fig. 4. Cabirops montereyensis, epicaridium larva. A, Lateral view, intact larva; B, Dorsal view ofthe distal
penduncular article ofAntenna 2; C, Outer terminal spine ofantenna 2; D, Inner terminal spine ofantenna 2;
E, Mandibles; F, Distal tip of peraeopod V; G, Pleon with insertion of anal tube; H, Anal tube; I, Detail of
terminal hairs ofanal tube. Scale bar in A = 50 nm; scale bars in B, C, D, F, G, H, and 1 = 5 ftm; scale bar in
E = nm.
1
Dentate shields on propodus and on distal gressively decreasing in length from pleo-
tip of carpus on all peraeopods (Fig. 4F). pod 1 (Fig. 3F) to pleopod 5 (Fig. 3G). Ex-
Basis elongate on peraeopod VI. opods and endopods ofsimilar length on all
Pleon: 5 pairs of biramous pleopods. pleopods. All exopodswith 3 terminal spines
Sympods lacking medial processes and pro- and all endopods with 2 terminal spines
582 PROCEEDINGS OF THE BIOLOGICAL SOCIETY OF WASHINGTON
bearing fine setae. Uropods (Figs. 3H, 4G) in the configuration ofthe uropods, slender
robust. Protopod bearing lateral plumose and elongate in C. equitans and robust in
spine, exopod with 3 spines (2 plumose) and C. montereyensis.
endopod with 5 spines (2 plumose). Medial Uropodal morphology ofepicaridia likely
margins of uropodal endopod and exopod represents a familial character distinguish-
with fine hairs (Figs. 3H, 4H). Prominent ing Cryptoniscidae (Bocquet-Vedrine 1987)
anal tube originating at base ofuropods (Fig. from other families ofCryptoniscoidea. To
4G), often projecting ventrally or anteriorly what extent otherdifferences in epicaridium
(Fig. 4H), terminal opening ringed with fine morphology might represent characters of
hairs (Fig. 41). systematic value presently isunknown. This
Remarks: Previous descriptions of Ca- stage may be useful in future work in pro-
birops epicaridium larvae (Romano 1953, viding an additional suite of specific char-
&
Attardo 1955, Reverberi Catalano 1963) acters (as has been indicated for the bopyrid
are too fragmentaryand imprecise to permit genus Probopyrus—Dale & Anderson 1982)
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validcomparison with the larvae of mon- and also, perhaps, in providing higher level
tereyensis. Larvae of two other genera of characters which may aid in more firmly
Cabiropidae have been described in suffi- resolving the systematics ofthis superfam-
cient detail to permit general comparison: ily.
Ancyroniscus bonnieri (Holdich 1975) and
&
Clypeoniscus meinerti (Giard Bonnier Acknowledgments
1895). These species differ from C. mon-
I thank C. Williams for preparing the il-
tereyensis in details of antennal, peraeopo-
lustrations and for photographic assistance,
dal, and pleonal structures and both are
M. Kooda for assistance with the electron
characterized by very short anal processes.
microscopy, and G. C. Steyskal for aid in
Similargeneric level differences occurin the
the construction of the family name Cabi-
degrees of development of the anal tube
ropidae. This work was partially supported
within the Cryptoniscidae; it is prominent
by funds from the Committee on Research
in Liriopsis (Caullery 1908), Crinoniscus
of the Academic Senate of the University
(Perez 1900, Boquet-Vedrine 1987), andthe
of California, Riverside.
enigmatic Enthylacus (Perez 1920), but is
lacking in Danalia (Caullery 1908, Fize
Literature Cited
1955). The anal tube is well developed in
Hemioniscus balani, the single species of Attardo, C. 1955. Contribuzioni al problema
Hemioniscidae in which the epicaridium dell'iperparassitismo: annotazioni sulla biolo-
stage has been described (Caullery & Mesnil gia, la determinazione del sesso, l'involuzione
di Cabiropsmarsupialis(Caroli)iperparassitadi
1901). —
Hippolyte viridis. Rivista di biologia 47:109-
The only cryptoniscoid epicaridium that 138 + pi. 1.
has been described in sufficient detail for Bocquet-Vedrine, J. 1985. Redescriptionde la forme
precise comparison with C. montereyensis cryptoniscienne du Crustace Isopode Crinonis-
is Crinoniscus equitans, illustrated exten- cus equitans Perez.—Bulletin du Museum Na-
sively by Bocquet-Vedrine (1987). The two tional d'Histoire Naturelle, Serie 4, 7:819-837.
. 1987. Fertilite et redescription de la larve
species are remarkably similar in the overall epicaridienne du Crustace Isopode Cryptonis-
shapes of appendages and in the distribu- cien Crinoniscus equitans Perez.—Bulletin du
tion and form of various spines and setae. Museum National d'Histoire Naturelle, Serie 4,
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Bourdon, R. 1966 [1967]. Sur quelques nouvelles
the second antennae, peraeopods, and pleo-
especes de Cabiropsidae (Isopoda Epicari-
pods, these differencesare rathersubtle. The dea).—Bulletindu Museum National d'Histoire
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VOLUME NUMBER
105, 3 583
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