Atlantid Heteropods as Living Substrata for Eggs of Halobates sericeus (Heteroptera: Gerridae)

Atlantid heteropods are collected occasionally in Hawaiian waters with yellow, narrowly elliptical objects attached to their shells. Examination of 139 of these objects from 72 atlantids showed that they consisted of an outer, clear capsule whose contents were usually yellow, although 16 were empty and four contained brown insects at an advanced stage of development. The latter were identified as preemergent nymphs of the Pacific pelagic seaskater or ocean strider, Halobates sericeus Eschscholtz. The maximal number of attached capsules was four, although most shells (79%) had one or two. Capsules averaged 0.93 mm long and 0.36 mm wide and were deposited on either the right, left, or both sides of the shell. All 72 atlantids with egg capsules were adult males. Exclusive usage of males by H sericeus is suggested to result from swarming behavior by male atlantids at the water surface. Although egg capsules were recorded from eight species of atlantids, most (86%) were on Atlanta turriculata d'Orbigny and A. fusca Souleyet, two of the most strongly pigmented species. Hypothetically, these two species would be the most visually conspicuous to H sericeus at the ocean surface. THE HETEROPODA IS a superfamily of gastropod molluscs that includes three families: the Atlantidae, Carinariidae, and Pterotracheidae (Lalli and Gilmer 1989). All heteropods are holopelagic and show a number of reproductive adaptations to an oceanic life style. Males produce spermatophores, which are thought to be transferred by the sperm groove of the penis to the female during copulation (reviewed by Lalli and Gilmer [1989]). Copulation has been observed only in Pterotrachea hippocampus Phillipi (Harbison, pers. comm., cited in Lalli and Gilmer [1989]), although transfer of spermatophores was not seen. Fertilized eggs are released by the female in a continuous mucoid string that periodically detaches, except in Firoloida desmaresti Lesueur, where a permanent egg filament is present at the posterior end of the body (reviewed by Lalli and Gilmer [1989]). 1 Manuscript accepted 10 April 1995. 2 Department of Biological Science, California State University, Fullerton, California 92634. 84 Tesch (1949: 51) was the first person to speculate on the physical appearance and the site of spermatophore deposition on female heteropods: "In my material of Atlantidae I found some females provided with a sausagelike object, glued to the shell, either on the right or left side, and once even on both sides. It occurred in Oxygyrus keraudreni, Atlanta inclinata and A. turriculata. I think that this remarkable sausage is a kind of spermatophor [sic]." He illustrated two of these objects, the first of which was 0.8 mm long and was attached to the right side of a small 0. keraudreni (Lesueur) (1.9 mm diameter, exclusive of the keel [redrawn here in Figure 1a]), and the second was 0.7 mm long and was attached to the left side of a 2.7-mm A. inclinata Souleyet. The objects consisted of an outer, clear capsule with dark contents having no particular structure. Tokioka (1955) subsequently described a 1.5-mm specimen of 0. keraudreni (sex of animal not indicated) from Japanese waters that had two "spermatophores" (0.64 and 0.71 mm long) atEggs of Halobates on Atlantid Heteropods-SEAPY FIGURE 1. Sketches of Oxygyrus keraudreni with (a) a single Halobates sericeus egg attached to the right side of the shell, and (b) two H. sericeus eggs attached to the left side of the shell (from Tesch [1949] and Tokioka [1955], respectively). Scale bars = 1.0 mm. tached to the left side of the shell (redrawn here in Figure Ib). Van der Spoel (1972: 552) noted that all male atlantids he examined had "one and sometimes two spermatophores in development in the accessory sexual glands" adjacent to the penis, and that "the spermatophores found attached to the shell as described by Tesch (1949) are identical to those found in the sexual organs." Detailed histological studies of the female reproductive system in atlantids by ThiriotQuievreux and Martoja (1974) showed that males deposit spermatophores directly in the female's mantle cavity. After deposition, the spermatophore sac ruptures and the sperma85 tozoa escape and then swim to the genital tract. The findings of Thiriot-Quievreux and Martoja raise the question: if the objects attached to the shells are not spermatophores, then what are they? Since the early 1980s I have collected heteropods during cruises aboard research vessels in Hawaiian waters. The most abundant heteropods in the epipelagic zone off Hawai'i are the atlantids (Seapy 1990a). While sorting through the live plankton samples I occasionally came across atlantids with narrowly elliptical, clear capsules attached to their shells. The capsules were striking because their contents were bright yellow. During a cruise in 1991 when an extensive series of shallow plankton tows was taken, I sorted out a large number of atlantids that had these attached capsules. Their correct identity was finally solved when I encountered an atlantid with a capsule containing a brown insect that appeared to be a nymphal stage of a sea skater, Halobates sp. MATERIALS AND METHODS Specimens of atlantid heteropods with attached egg capsules were collected from Hawaiian waters during a number of cruises (Table 1). Plankton samples were taken in the epipelagic zone by oblique tows using open ring nets (l-m2 and 4-m2 mouth areas) and paired Bongo nets (0.38-m2 mouth area each), and by surface neuston tows using manta nets. Atlantids were sorted from fresh plankton samples aboard ship, preserved in buffered 5% sea water-formalin solution, and transferred subsequently to 70% ethanol. Most egg capsules (92 on 45 atlantids) were collected during a cruise in February 1991. Five replicate oblique tows to a depth of about 100 m were taken with a 4_m2 ring net at each of six locations, separated by ca. 1° latitudinal increments and extending northward to 27° N from the island of Kaua'i (at 22° 25' N). Shell diameters of specimens belonging to the three species of atlantids having the greatest numbers of attached egg cases were compared using two-sample Student's t-tests 86 PACIFIC SCIENCE, Volume 50, January 1996