Pacific Science (1996), vol. 50, no. 1: 84-92 © 1996 by University of Hawai'i Press. All rights reserved Atlantid Heteropods as Living Substrata for Eggs of Halobates sericeus (Heteroptera: Gerridae)1 ROGER R. SEAPy 2 ABSTRACT: 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 cap­ sules 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. Ex­ clusive usage of males by H sericeus is suggested to result from swarming be­ havior by male atlantids at the water surface. Although egg capsules were re­ corded 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 gastro­ Tesch (1949: 51) was the first person to pod molluscs that includes three families: the speculate on the physical appearance and the Atlantidae, Carinariidae, and Pterotracheidae site of spermatophore deposition on female (Lalli and Gilmer 1989). All heteropods are heteropods: "In my material of Atlantidae I holopelagic and show a number of reproduc­ found some females provided with a sausage­ tive adaptations to an oceanic life style. Males like object, glued to the shell, eitheronthe right produce spermatophores, which are thought or left side, and once even on both sides. It to be transferred by the sperm groove of the occurred in Oxygyrus keraudreni, Atlanta in­ penis to the female during copulation (re­ clinata and A. turriculata. I think that this viewed by Lalli and Gilmer [1989]). Copula­ remarkable sausage is a kind of spermato­ tion has been observed only in Pterotrachea phor [sic]." He illustrated two of these ob­ hippocampus Phillipi (Harbison, pers. comm., jects, the first of which was 0.8 mm long and cited in Lalli and Gilmer [1989]), although was attached to the right side of a small 0. transfer of spermatophores was not seen. keraudreni (Lesueur) (1.9 mm diameter, ex­ Fertilized eggs are released by the female in a clusive of the keel [redrawn here in Figure continuous mucoid string that periodically 1a]), and the second was 0.7 mm long and detaches, except in Firoloida desmaresti was attached to the left side of a 2.7-mm A. Lesueur, where a permanent egg filament is inclinata Souleyet. The objects consisted ofan present at the posterior end of the body (re­ outer, clear capsule with dark contents hav­ viewed by Lalli and Gilmer [1989]). ing no particular structure. Tokioka (1955) subsequently described a 1.5-mm specimen of 0. keraudreni 1 Manuscript accepted 10 April 1995. (sex of animal not indicated) 2 Department of Biological Science, California State from Japanese waters that had two "sper­ University, Fullerton, California 92634. matophores" (0.64 and 0.71 mm long) at- 84 Eggs of Halobates on Atlantid Heteropods-SEAPY 85 tozoa escape and then swim to the genital tract. The findings of Thiriot-Quievreux and Martoja raise the question: if the objects at­ tached to the shells are not spermatophores, then what are they? Since the early 1980s I have collected het­ eropods during cruises aboard research ves­ sels 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 occasion­ ally came across atlantids with narrowly ellip­ tical, clear capsules attached to their shells. The capsules were striking because their con­ tents 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 ap­ peared 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 FIGURE 1. Sketches of Oxygyrus keraudreni with (a) a (Table 1). Plankton samples were taken in single Halobates sericeus egg attached to the right side of the epipelagic zone by oblique tows using the shell, and (b) two H. sericeus eggs attached to the left open ring nets (l-m2 and 4-m2 mouth areas) side of the shell (from Tesch [1949] and Tokioka [1955], 2 respectively). Scale bars = 1.0 mm. and paired Bongo nets (0.38-m mouth area each), and by surface neuston tows using manta nets. Atlantids were sorted from fresh tached to the left side of the shell (redrawn plankton samples aboard ship, preserved in here in Figure Ib). Van der Spoel (1972: 552) buffered 5% sea water-formalin solution, noted that all male atlantids he examined had and transferred subsequently to 70% ethanol. "one and sometimes two spermatophores in Most egg capsules (92 on 45 atlantids) were development in the accessory sexual glands" collected during a cruise in February 1991. adjacent to the penis, and that "the sperma­ Five replicate oblique tows to a depth of tophores found attached to the shell as de­ about 100 m were taken with a 4_m2 ring net scribed by Tesch (1949) are identical to those at each of six locations, separated by ca. 1° found in the sexual organs." latitudinal increments and extending north­ Detailed histological studies of the female ward to 27° N from the island of Kaua'i (at reproductive system in atlantids by Thiriot­ 22° 25' N). Quievreux and Martoja (1974) showed that Shell diameters of specimens belonging males deposit spermatophores directly in the to the three species of atlantids having the female's mantle cavity. After deposition, the greatest numbers of attached egg cases were spermatophore sac ruptures and the sperma- compared using two-sample Student's t-tests 86 PACIFIC SCIENCE, Volume 50, January 1996 TABLE 1 COLLECllON DATA FOR ATLANTID HETEROPODS WITH ATTACHED H. sericeus EGG CAPSULES FROM OCEANIC WATERS OFF HAWAI'I NET DEPTH NO. NO. DATE LOCATION TYPE (m) ATLANTIDS CAPSULES 4 Apr. 1984 Leeward O'ahu Bongo 0-40 1 1 12 Apr. 1984 Leeward O'ahu 1 m2 0-150 1 1 4 Aug. 1984 Leeward O'ahu Bongo 0-140 1 2 22 Aug. 1985 Leeward O'ahu 1 m2 0-150 1 2 10 Sept. 1985 Leeward O'ahu Manta surface 1 1 24 Mar. 1986 Leeward O'ahu 4m2 0-300 1 2 7 Aug. 1986 Leeward O'ahu 4m2 0-230 1 2 1/3 Nov. 1989 Leeward O'ahu 1 m2 0-150 7 13 6-10 Feb. 1991 North of Kaua'i 4 m2 0-100 45 92 10-16 Jan. 1992 Off Mo1oka'i, Liina'i, Maui 1 m2 0-75 13 22 Total 72 139 with the shell diameters of series of in­ surface of the developing embryo. The ven­ dividuals of each species from representative tral side of the egg is always oriented toward plankton samples collected offleeward O'ahu the viewer because the egg is cemented to the in April 1984. Differences were considered substratum on its dorsal side (Herring 1961; significant if P < 0.05. cited in Andersen and Polhemus [1976]). The parallel lines on the ventral surface of the embryo demarcate the developing rostrum, antennae, and front legs of the nymph. Also, RESULTS the faint red rudiments of the paired com­ Seven egg capsules, at various stages of pound eyes become evident at this stage. In development, attached to four specimens of the late stage, the yellow color of the embryo Atlanta turriculata d'Orbigny, were examined fades, and the developing nymph becomes by L. Cheng, along with three male and three brown. As the appendages become more de­ female Halobates collected off O'ahu with a fined, the brown color darkens and the eyes manta net. She confirmed that the brown, become bright red (plate Ib, middle capsule). late developmental stages were preemergent Mter the nymph emerges, the clear capsule nymphs and identified the nymphs and adults can remain attached to the atlantid shell as Halobates sericeus Eschscholtz, the Pacific (Plate Ib, lower left capsule). pelagic seaskater or ocean strider. Because All 139 H. sericeus egg capsules were at­ H. sericeus is the only species of Halobates tached to the shells of adult male atlantids. recorded from oceanic waters in the vicinity When these atlantids were sorted from fresh and to the north of the Hawaiian Islands plankton samples aboard ship, they always (Cheng 1989), all egg capsules on atlantid appeared to be healthy and not weakened by shells collected in this study are assumed to the presence of the capsules. Aside from the have been deposited by this species of Halo­ atlantids the only other living animals ob­ bates. served with attached H. sericeus capsules were Egg capsule contents were subjectively two small Janthina sp. (2.40 and 2.42 mm shell categorized at early, intermediate, or late width) collected in neuston tows; the first had stages of development.