Larval Development of Caribeopsyllus Amphiodiae (Thaumatopsyllidae: Copepoda), an Enterozoic Parasite of the Brittle Star Amphiodia Urtica

Abstract

A B S T R A C TAlthough most parasitic copepods produce free-living larvae, Caribeopsyllus amphiodiae and other thaumatopsyllid copepods have a parasitic larval stage (metanauplius) that inhabits an ophiuroid stomach. Metanauplii of C. amphiodiae collected from its burrowing host, Amphiodia urtica, and reared in the laboratory gave rise to ovigerous females that released free-swimming first nauplii (NI). We provide the first full descriptions for a thaumatopsyllid of the NI, parasitic metanauplii, and free-living copepodid I to copepodid VI of the female and male based on developmental stages obtained. Extraordinary features of C. amphiodiae NI are the presence of one pair of setae on the labrum, a character unique among Copepoda, and the presence of a maxillule represented by one seta, making the larva a metanauplius by definition. In most other copepods, the one-seta or one-spine maxillule appears no earlier than NII. The mandible of the metanauplius becomes massive, and a spiniform process from the first endopodal segment forms a chelate complex with the distinctly curved, clawlike second endopodal segment. Transient vestiges of the antenna and mandible remain in the CI, but maxillule, maxilla, and maxilliped are absent during the copepodid phase. Other body structures appear earlier than reported for other copepods: pediger 5 and the bud of swimming leg 4 are present at CI, and pediger 6 and the buds of legs 5 and 6 are present at CII. During leg development setal development is accelerated, but ramal segmentation is delayed. In addition, the major body articulation of the copepodid and adult stages occurs between the third and fourth pedigers, unlike the tagmosis of most gymnoplean and podoplean copepods. Such shifts in the timing of ontogenesis, atypical naupliar morphology, and unique adult body set apart the thaumatopsyllids from other copepods.

Early Post-Embryonic Development of Marine Chelicerates and Crustaceans with a Nauplius

“…[Sources: Sanders, 1963;Sanders & Hessler, 1964;Addis et al, 2007; present study.] Copepods: B. some parasitic copepods lack a naupliar arthrite (e.g., Ivanenko et al, 2001;Dojiri et al, 2008); some free-living copepods lack a naupliar arthrite on the first, non-feeding stage although the arthrite is added on later feeding stages (Ferrari & Dahms, 2007); C. bud of caudal ramus present on all copepods, bud of maxilla 1 present on thaumatopsylloids; F. gymnopleans with five, podopleans with four; G. new limb buds appear after the first molt of podopleans, and after the second molt of gymnopleans. [Sources: Ferrari & Dahms, 2007;Dojiri et al, 2008.]…”

“…Copepods: B. some parasitic copepods lack a naupliar arthrite (e.g., Ivanenko et al, 2001;Dojiri et al, 2008); some free-living copepods lack a naupliar arthrite on the first, non-feeding stage although the arthrite is added on later feeding stages (Ferrari & Dahms, 2007); C. bud of caudal ramus present on all copepods, bud of maxilla 1 present on thaumatopsylloids; F. gymnopleans with five, podopleans with four; G. new limb buds appear after the first molt of podopleans, and after the second molt of gymnopleans. [Sources: Ferrari & Dahms, 2007;Dojiri et al, 2008.] Dendrobranchiates: C. ventral setae on rami of antenna 1, antenna 2 and mandible suggest that each ramus is a segment complex and so these are transformed limbs; F. buds of maxilla 1-2 and maxilliped 1-2 are present early in development, and later in development those limbs are reorganized and buds of five pereiopods are added, finally five pereiopods are reorganized and buds of five pleopods are added.…”

The contrariwise life of a parasitic, pedomorphic copepod with a non‐feeding adult: ontogenesis, ecology, and evolution

“…The Thaumatopsyllidae, unlike other endoparasitic copepods of ophiuroids, have a protelean life cycle (i.e., one with a parasitic larva) and a free‐living, non‐feeding adult stage. Little has been published on the biology of the five known thaumatopsyllid species, and their phylogenetic relationships within the Copepoda are uncertain (Ho et al 2003; Boxshall & Halsey 2004; Dojiri et al 2008).…”

“…For only two species, Caribeopsyllus amphiodiae H o , D ojiri , H endler & D eets 2003 and Thaumatopsyllus paradoxus S ars 1913, have both sexes been described, the ophiuroid host species identified, and adults reared from parasitic metanauplii (Dojiri et al 2008). Copepodid stages of both species and of Caribeopsyllus chawayi S uárez‐morales & C astellanos 1998 have been observed (Sars 1913, 1921; Bresciani & Lützen 1962; Fosshagen 1970; Suárez‐Morales & Tovar 2004), but Orientopsyllus investigatoris S ewell 1949 and Australopsyllus fallax M c K innon 1994 are known from just a few preserved adults.…”

“…Herein, we describe aspects of the behavior and ecology of C. amphiodiae and its ophiuroid host Amphiodia urtica (L yman 1860) that are key to understanding the species' life history and phylogeny, and we compare the biology of C. amphiodiae with C. chawayi and T. paradoxus . External morphology of the developmental stages of C. amphiodiae previously has been depicted (Ho et al 2003; Dojiri et al 2008). Here, we describe the ontogenesis of its elaborate nauplius eye, its larval gonads, and the pronounced sexual dimorphism of the metanauplius stage, which are exceptional attributes among Crustacea.…”