Invertebrate Biology, Volume 121, No. 1

Contents and Abstracts
© 2002 American Microscopical Society, Inc.

HEADER ILLUSTRATION: Rudimentary ocellus in the brain of the sandhopper Talitrus saltator. This is the first such ocellus known in an amphipod. (See Frelon-Raimond et. al.)


Abstracts for all articles in this issue are presented below.
Individual abstracts can also be accessed directly by clicking on the highlighted titles here:

An aplacophoran postlarva with iterated dorsal groups of spicules and skeletal similarities to Paleozoic fossils
Amélie H. Scheltema and Dmitry L. Ivanov. pp 1-10

Laboratory spawning, larval development, and metamorphosis of the limpets Lottia digitalis and Lottia asmi (Patellogastropoda, Lottiidae)
Matthew C. Kay and Richard B. Emlet. pp 11-24

Life history of Littorina scutulata and L. plena, sibling gastropod species with planktotrophic larvae
Paul A. Hohenlohe. pp 25-37

Survival of heterotopic heart xenografts from Helisoma duryi, Planorbula armigera, and Planorbarius corneus in Biomphalaria glabrata (Pulmonata, Basommatophora, Planorbidae): evidence for phylogenetic relatedness?
John T. Sullivan and Dana A. Farengo. pp 38-46

Methane-based symbiosis in a mussel, Bathymodiolus platifrons, from cold seeps in Sagami Bay, Japan
James P. Barry, Kurt R. Buck, Randall K. Kochevar, Douglas C. Nelson, Yoshihiro Fujiwara, Shana K. Goffredi, and Jun Hashimoto. pp 47-54

Reproduction and simultaneous hermaphroditism in Branchiomma luctuosum (Polychaeta, Sabellidae) from the Mediterranean Sea
Margherita Licciano, Adriana Giangrande, and Maria Cristina Gambi. pp 55-65

Impact of males on variation in the reproductive cycle in an androdioecious desert shrimp
Naida Zucker, Gabriela A. Aguilar, Stephen C. Weeks, and L. Garner McCandless. pp 66-72

Intracerebral ocelli in an amphipod: extraretinal photoreceptors of the sandhopper Talitrus saltator (Crustacea, Amphipoda)
Maryline Frelon-Raimond, V. Benno Meyer-Rochow, Alberto Ugolini, and Gilbert Martin. pp 73-78


Invertebrate Biology 121(1):1-10
© 2002 American Microscopical Society, Inc.

An aplacophoran postlarva with iterated dorsal groups of spicules and skeletal similarities to Paleozoic fossils Abstract. A tiny neomenioid postlarva (Neomeniomorpha, or Solenogastres) collected from the water column 3 to 6 m above the east Pacific seamount Fieberling Guyot has 6 iterated, transverse groups of spicules and 7 regions devoid of spicules between the transverse groups and the anterior- and posteriormost spicules. Three pairs of ventral, longitudinal zones with columns of single spicules, each pair with its own distinctive spicule morphology, lack transverse iteration. The 7 regions bare of spicules are compared to shell fields in developing polyplacophorans, and spicule arrangement is compared to sclerite arrangement on the Cambrian fossils Wiwaxia corrugata and Halkieria evangelista and to the spines and shell plates of the Silurian Acaenoplax hayae. The term iteration is used to denote processes that result in both metameric segments and repeated ectodermal skeletal structures. Iterative morphogenesis was probably present in bilateral animals before the Cambrian. Comparisons of iterated ectodermal skeletal structures among fossil and extant forms are suggested to indicate evolutionary relationship.

Additional key words: Aplacophora, Neomeniomorpha, Mollusca, Halkieria, Wiwaxia, Acaenoplax, Polyplacophora, sclerites, spicules, engrailed, iteration, segmentation, Fieberling Guyot


Invertebrate Biology 121(1):11-24
© 2002 American Microscopical Society, Inc.

Laboratory spawning, larval development, and metamorphosis of the limpets Lottia digitalis and Lottia asmi (Patellogastropoda, Lottiidae) Abstract. This study describes and compares laboratory spawning, larval development, and metamorphosis in the patellogastropod limpets Lottia digitalis and Lottia asmi. Both species were dioecious and freely spawned their gametes, which were fertilized externally. Eggs from L. digitalis and L. asmi averaged 155 and 134 µm in diameter, respectively. Early cleavage patterns were typical of other patellogastropods. Swimming trochophore larvae had developed ~15 hours after fertilization, and ultimately developed into lecithotrophic veliger larvae that reached metamorphic competence at 5.25-5.5 days after fertilization (13°C). Food particles were frequently visible in the gut of newly metamorphosed individuals one day after settlement, and adult shell growth was typically initiated within 2-4 days of settlement. Small egg size in L. asmi, relative to other eastern Pacific lottiids, may be directly related to the need for high fecundity in this small-bodied species; however, developmental information is available for relatively few lottiid species. Because broadcasting lottiids do not secure egg masses in safe microhabitats for development, this reproductive mode may have been conducive to their ecological radiation into novel habitats.

Additional key words: egg size, fecundity, protoconch, trochophore, veliger


Invertebrate Biology 121(1):25-37
© 2002 American Microscopical Society, Inc.

Life history of Littorina scutulata and L. plena, sibling gastropod species with planktotrophic larvae Abstract. The intertidal, sibling species Littorina scutulata and L. plena (Gastropoda, Prosobranchia) are sympatric throughout most of their ranges along the Pacific coast of North America. Both species release disc-shaped, planktonic egg capsules from which planktotrophic veliger larvae hatch. Here I review existing data and present new observations on these species' life history, including age at first reproduction, spawning season, maximum fecundity rates, capsule morphology, egg size and number, pre-hatching development, larval growth at three food concentrations, potential settlement cues, planktonic period, and protoconch size. Previous classification of egg capsule morphologies used to distinguish the species is inaccurate; instead, capsules can be categorized into three types of which each species may produce two. Females of L. scutulata produced capsules with either two rims of unequal diameter or one rim, while females of L. plena produced capsules with one rim or two rims of nearly equal diameter. Females of each species spawned sporadically from early spring to early fall in Puget Sound. Larvae of L. plena hatched one day earlier than those of L. scutulata, and both species grew fastest in the laboratory at intermediate food concentrations. Larvae metamorphosed in the presence of a variety of materials collected from their adult habitat, including conspecific adults, algae, rocks, and barnacle tests. This is the first report of planktotrophic larvae in this genus metamorphosing in the laboratory. The total planktonic period of 8 larvae of L. scutulata raised in the laboratory was 37-70 days, and a single larva of L. plena metamorphosed after 62 days. Protoconch diameter of shells collected from the field was 256-436 µm and did not differ significantly between the species. Previous allozyme and mitochondrial DNA work has suggested high levels of genetic variability in both species and greater genetic population structure in L. plena, despite the long spawning season and long-lived larvae in both species. The interspecific life history differences described here appear insufficient to produce consistent differences in gene flow patterns.

Additional key words: development, dispersal, gene flow, metamorphosis, larval settlement


Invertebrate Biology 121(1):38-46
© 2002 American Microscopical Society, Inc.

Survival of heterotopic heart xenografts from Helisoma duryi, Planorbula armigera, and Planorbarius corneus in Biomphalaria glabrata (Pulmonata, Basommatophora, Planorbidae): evidence for phylogenetic relatedness? Abstract. Heart xenografts from the pulmonate snail Helisoma trivolvis survive in Biomphalaria glabrata, whereas xenografts from most other pulmonate snail genera are rejected within 3 to 15 days. To test whether xenografts from snails closely related to H. trivolvis were also accepted, specimens of an albino strain of B. glabrata were implanted with hearts from H. duryi, Planorbula armigera, and Planorbarius corneus. The fate of implants was monitored for 180 days by measuring heartbeat and by histological analysis. All 3 types of implants survived beyond the 3 to 15 days required for the complete destruction of incompatible xenografts, suggesting a degree of physiological and immunological compatibility between B. glabrata and these donors. Among the 3 types of xenografts, all from H. duryi survived for the entire 180 days. Fewer grafts from P. armigera and P. corneus survived for prolonged periods, although some still were beating at 60 and 180 days post implantation (DPI) respectively, suggesting that a range of histocompatibility, and perhaps phylogenetic relatedness, with B. glabrata occurs within this group. Paradoxically, the initial hemocytic response by the recipient was strongest against grafts from H. duryi, the most compatible donor, while responses to grafts from P. armigera and P. corneus were mild or did not occur during the first 7 DPI. We used 2 albino strains of B. glabrata in these studies, and the data suggest slight differences in recipient strain compatibility.

Additional key words: tissue transplantation, histocompatibility, snails, immunity, phylogeny


Invertebrate Biology 121(1):47-54
© 2002 American Microscopical Society, Inc.

Methane-based symbiosis in a mussel, Bathymodiolus platifrons, from cold seeps in Sagami Bay, Japan Abstract. Bathymodiolus platifrons, a chemosynthetic mussel from cold seeps off Japan, relies for its nutrition on the productivity of methylotrophic or methanotrophic endosymbionts. High densities of bacterial symbionts appearing to be type I methanotrophs were observed in transmission electron micrographs of gill tissues. Methanol dehydrogenase activity in gill tissue from a single individual was positive compared to non-methanotrophic control samples, indicating a high potential for methanotrophy. Stable isotopic ratios of carbon in symbiont-containing gill tissue, as well as host tissues, were extremely depleted in 13C, and similar to values reported for other methanotrophic species. TEMs of gill tissue showing symbionts in various stages of digestion support the hypothesis that carbon transfer from symbionts to B. platifrons occurs through intracellular digestion of the symbionts. Discovery of methane- or methanol-based symbioses in B. platifrons from cold seeps in Sagami Bay extends the range of such symbioses to include cold seeps and hydrothermal vents, and supports the idea that environmental methane levels control the distribution of these symbioses.

Additional key words: chemosynthesis, methanotrophy, methylotrophy, bivalve, biogeography


Invertebrate Biology 121(1):55-65
© 2002 American Microscopical Society, Inc.

Reproduction and simultaneous hermaphroditism in Branchiomma luctuosum (Polychaeta, Sabellidae) from the Mediterranean Sea Abstract. Previous observations on the reproductive biology and gametogenesis of Branchiomma luctuosum (Polychaeta: Sabellidae) were extended in this study, with a description of larval development and of reproduction at the population level, comparing populations from the Tyrrhenian Sea (Ischia, Naples) and Ionian Sea (Gulf of Taranto). Although B. luctuosum is a simultaneous hermaphrodite, producing both male and female gametes in each fertile segment, present observations seem to preclude self-fertilization. Both gametes were spawned under laboratory conditions, and broadcasting was confirmed by sperm structure, which appears adapted for external fertilization. Larval development revealed the shortest pelagic period known for sabellids of similar size and life history. Oogenesis was prolonged and extraovarian. The Ionian population seemed to have a resting period during which eggs, having already begun vitellogenesis, remained at a diameter of about 30 µm. After this period, rapid growth was observed: the oocytes reached maximum diameter (140 µm) in about 2 months. The spawning period began earlier and lasted longer in the Ionian population, compared to the Tyrrhenian population. This pattern seems to be due to asynchronous vitellogenesis within individuals. Documenting the reproductive features of this species will help us to understand its role as a primary colonizer, since hermaphroditism and a short pelagic phase may produce high population densities starting from only a few individuals.

Additional key words: life cycle, gamete structure, gametogenesis


Invertebrate Biology 121(1):66-72
© 2002 American Microscopical Society, Inc.

Impact of males on variation in the reproductive cycle in an androdioecious desert shrimp Abstract. In the clam shrimp Eulimnadia texana and some other species of desert ephemeral pool-dwelling branchiopod crustaceans, males coexist with hermaphrodites. The hermaphrodites can mate with males or can fertilize their own eggs but cannot mate with other hermaphrodites. Understanding the evolutionary dynamics of this mixed mating system, known as androdioecy, requires a basic knowledge of the reproductive behavior of this species. Here we describe the reproductive cycle of hermaphrodites when isolated and when in the presence of a male. Videos were analyzed to provide a description of egg movement from the ovotestes to the brood chamber. Through time-lapse photography, we determined that paired hermaphrodites carried their brood longer and swam fast for a greater duration than did isolated hermaphrodites. Isolated hermaphrodites dug more preliminary burrows before burying their clutch and had longer inter-clutch intervals than did paired hermaphrodites. These observations suggest that hermaphrodites may behave in ways that maximize the likelihood of mating, and that males may interfere with hermaphrodites during egg laying.

Additional key words: androdioecy, mating behavior, clam shrimp, Eulimnadia texana, Branchiopoda, Conchostraca, Crustacea


Invertebrate Biology 121(1):73-78
© 2002 American Microscopical Society, Inc.

Intracerebral ocelli in an amphipod: extraretinal photoreceptors of the sandhopper Talitrus saltator (Crustacea, Amphipoda) Abstract. No morphological clues on the amphipod head indicate the existence of ocelli. However, as in several isopod species studied so far, two rudimentary photoreceptors are integrated into the medio-dorsal part of the brain. This electron microscopical study of the photoreceptors is the first report on the presence of ocelli in amphipods. Each ocellus is made up of 3 receptor cells which contribute to the formation of a photoreceptive surface (the rhabdom) formed by tightly packed microvilli. The rhabdoms are twisted and irregular in outline. Membrane turnover is suggested by the presence of different kinds of lysosomes. Lacking dioptric lenses, these photoreceptors are not likely to be involved in image formation but may function as appraisers of ambient light intensity. Physiological and behavioral studies will, henceforth, have to take into account these unexpected ocelli, which may represent remnants of the naupliar eye.

Additional key words: eye, vision, rhabdom, membrane turnover, brain, Talitridae