Invertebrate Biology, Volume 123, No. 1

Contents and Abstracts
© 2004 American Microscopical Society, Inc.


©Richard Lord, Guernsey

HEADER ILLUSTRATION: Stauromedusans, such as this alluring individual, are not your typical jellyfishes. They retain the polypoid stalk after metamorphosis and live attached to a substrate as adults. Yet aspects of their morphology clearly ally them to more standard scyphozoans. A new cladistic analysis of 87 morphological and life-history characters of medusozoans (See (Marques & Collins)) is largely congruent with recent sequence-based phylogenies. It highlights stalked jellyfishes as a separate cnidarian class and indicates some other important re-alignments within the subphylum Medusozoa. (Haliclystus octoradiatus, diameter ~12 mm, from the island of Guernsey, GB. Photo by Richard Lord ©)


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

Choanoflagellates, choanocytes, and animal multicellularity
Manuel Maldonado. pp 1-22

Cladistic analysis of Medusozoa and cnidarian evolution
Antonio C. Marques and Allen G. Collins. pp 23-42

Structure and signaling in polyps of a colonial hydroid
Neil W. Blackstone, Kimberly S. Cherry, and Sally L. Glockling. pp 43-53

Reproductive biology, development, and planula behavior in the Caribbean gorgonian Pseudopterogorgia elisabethae
Carla Gutiérrez-Rodríguez and Howard R. Lasker. pp 54-67

Anterior adhesive areas and adjacent secretions in the parasitic flatworms Decacotyle lymmae and D. tetrakordyle (Monogenea: Monocotylidae) from the gills of stingrays
Bronwen W. Cribb and Ian D. Whittington. pp 68-77

Great Gordian knots: sex ratio and sexual size dimorphism in aggregations of horsehair worms (Gordius difficilis)
Philip A. Cochran, Andrew K. Newton, and Clare Korte. pp 78-82

Cloning and characterization of a candidate nutritive glycoprotein from the albumen gland of the freshwater snail, Helisoma duryi (Mollusca: Pulmonata)
Spencer T. Mukai, Tafazzal Hoque, Fumihiro Morishita, and A. Saber M. Saleuddin. pp 83-92


Invertebrate Biology 123(1):1-22
© 2004 American Microscopical Society, Inc.

Choanoflagellates, choanocytes, and animal multicellularity Abstract. It is widely accepted that multicellular animals (metazoans) constitute a monophyletic unit, deriving from ancestral choanoflagellate-like protists that gave rise to simple choanocyte-bearing metazoans. However, a re-assessment of molecular and histological evidence on choanoflagellates, sponge choanocytes, and other metazoan cells reveals that the status of choanocytes as a fundamental cell type in metazoan evolution is unrealistic. Rather, choanocytes are specialized cells that develop from non-collared ciliated cells during sponge embryogenesis. Although choanocytes of adult sponges have no obvious homologue among metazoans, larval cells transdifferentiating into choanocytes at metamorphosis do have such homologues. The evidence reviewed here also indicates that sponge larvae are architecturally closer than adult sponges to the remaining metazoans. This may mean that the basic multicellular organismal architecture from which diploblasts evolved, that is, the putative planktonic archimetazoan, was more similar to a modern poriferan larva lacking choanocytes than to an adult sponge. Alternatively, it may mean that other metazoans evolved from a neotenous larva of ancient sponges. Indeed, the Porifera possess some features of intriguing evolutionary significance: (1) widespread occurrence of internal fertilization and a notable diversity of gastrulation modes, (2) dispersal through architecturally complex lecithotrophic larvae, in which an ephemeral archenteron (in dispherula larvae) and multiciliated and syncytial cells (in trichimella larvae) occur, (3) acquisition of direct development by some groups, and (4) replacement of choanocyte-based filter-feeding by carnivory in some sponges. Together, these features strongly suggest that the Porifera may have a longer and more complicated evolutionary history than traditionally assumed, and also that the simple anatomy of modern adult sponges may have resulted from a secondary simplification. This makes the idea of a neotenous evolution less likely than that of a larva-like choanocyte-lacking archimetazoan. From this perspective, the view that choanoflagellates may be simplified sponge-derived metazoans, rather than protists, emerges as a viable alternative hypothesis. This idea neither conflicts with the available evidence nor can be disproved by it, and must be specifically re-examined by further approaches combining morphological and molecular information. Interestingly, several microbial lineages lacking choanocyte-like morphology, such as Corallochytrea, Cristidiscoidea, Ministeriida, and Mesomycetozoea, have recently been placed at the boundary between fungi and animals, becoming a promising source of information in addition to the choanoflagellates in the search for the unicellular origin of animal multicellularity.

Additional key words: animal evolution, invertebrate larvae, metazoan ancestor, poriferan gastrulation, sponge development


Invertebrate Biology 123(1):23-42
© 2004 American Microscopical Society, Inc.

Cladistic analysis of Medusozoa and cnidarian evolution Abstract. A cladistic analysis of 87 morphological and life history characters of medusozoan cnidarians, rooted with Anthozoa, results in the phylogenetic hypothesis (Anthozoa (Hydrozoa (Scyphozoa (Staurozoa, Cubozoa)))). Staurozoa is a new class of Cnidaria consisting of Stauromedusae and the fossil group Conulatae. Scyphozoa is redefined as including those medusozoans characterized by strobilation and ephyrae (Coronatae, Semaeostomeae, and Rhizostomeae). Within Hydrozoa, Limnomedusae is identified as either the earliest diverging hydrozoan lineage or as the basal group of either Trachylina (Actinulida (Trachymedusae (Narcomedusae, Laingiomedusae))) or Hydroidolina (Leptothecata (Siphonophorae, Anthoathecata)). Cladistic results are highly congruent with recently published phylogenetic analyses based on 18S molecular characters. We propose a phylogenetic classification of Medusozoa that is consistent with phylogenetic hypotheses based on our cladistic results, as well as those derived from 18S analyses. Optimization of the characters presented in this analysis are used to discuss evolutionary scenarios. The ancestral cnidarian probably had a sessile biradial polyp as an adult form. The medusa is inferred to be a synapomorphy of Medusozoa. However, the ancestral process (metamorphosis of the apical region of the polyp or lateral budding involving an entocodon) could not be inferred unequivocally. Similarly, character states for sense organs and nervous systems could not be inferred for the ancestral medusoid of Medusozoa.

Additional key words: Staurozoa, Scyphozoa, Hydrozoa, Cubozoa


Invertebrate Biology 123(1):43-53
© 2004 American Microscopical Society, Inc.

Structure and signaling in polyps of a colonial hydroid Abstract. After feeding, polyps of colonial hydroids contract regularly, dispersing food throughout the colony via the gastrovascular fluid. Such contractions may trigger signaling pathways that allow colonies to grow in an adaptive manner, i.e., to initiate development of more polyps in food-rich areas and to suppress polyp development in food-poor areas. In this context, we investigated the structure and potential signaling of the junction between polyps and stolons in colonies of the hydroid Podocoryna carnea. Using transmission electron microscopy, we found that the density of mitochondrion-rich epitheliomuscular cells was low in polyp and stolon tissues except at or near the polyp-stolon junction, where many of these mitochondrion-rich cells occur in ectodermal tissue. In vivo fluorescence microscopy suggests that these mitochondria are a principal source of the metabolic signals of the colony. Both native fluorescence of NAD(P)H and fluorescence from peroxides (visualized with H2DCFDA) co-localize to this region of the polyp. Rhodamine 123 fluorescence suggests that both these metabolic signals emanate from mitochondria. To test whether such metabolic signals may be involved in colony pattern formation, inbred lines of P. carnea were used. Colonies of a runner-like inbred line grow with widely spaced polyps and long stolonal connections, much like wild-type colonies in a food-poor environment. Colonies of a sheet-like inbred line grow with closely spaced polyps and short stolonal connections, similar to wild-type colonies in a food-rich environment. Polyp-stolon junctions in runner-like and sheet-like colonies were imaged for the fluorescence of H2DCFDA. Densitometric analysis of this signal indicates that the mitochondria in epitheliomuscular cells of runner-like polyps emit greater amounts of peroxides. Because peroxides and other reactive oxygen species are frequently intermediaries in metabolic signaling pathways, we suspect that such signaling may indeed occur at polyp-stolon junctions, affecting colony pattern formation in these inbred lines and possibly in hydroid colonies in general.

Additional key words: epitheliomuscular cell, mitochondria, Podocoryna, Podocoryne, reactive oxygen species


Invertebrate Biology 123(1):54-67
© 2004 American Microscopical Society, Inc.

Reproductive biology, development, and planula behavior in the Caribbean gorgonian Pseudopterogorgia elisabethae Abstract. The reproductive biology, development, and planula behavior of the gorgonian Pseudopterogorgia elisabethae were studied at 2 sites in the Bahamas between 1996 and 2001. Colonies were gonochoric, and females brooded planulae on the colony surface. Gonads were observed only in colonies 18 cm high or larger. Spawning was asynchronous within and between sites but was concentrated 2-10 days after the new moons from late November through early January. Fertilized eggs developed into planulae over 1-2 days and the planulae remained attached to the surface of the female colony for an additional 2-4 days. Planulae were negatively buoyant and field observations suggest that larvae may settle within tens of meters of the maternal colony. P. elisabethae is harvested for natural products, and information on the reproduction of this commercially important species is crucial to the understanding of its population biology and to the development of management plans for the conservation of the species.

Additional key words: brooder, Anthozoa, Octocorallia, Alcyonacea, Holaxonia, larval dispersal


Invertebrate Biology 123(1):68-77
© 2004 American Microscopical Society, Inc.

Anterior adhesive areas and adjacent secretions in the parasitic flatworms Decacotyle lymmae and D. tetrakordyle (Monogenea: Monocotylidae) from the gills of stingrays Abstract. The monogeneans Decacotyle lymmae and D. tetrakordyle (Monocotylidae: Decacotylinae), from gills of the dasyatid stingrays Taeniura lymma and Pastinachus sephen, respectively, have a single aperture for adhesive secretion on each side of the anterior ventrolateral region. Rod-shaped bodies (S1) and electron-dense spherical secretion (S2) exit through specialised ducts opening adjacent to one another within these apertures. The S1 bodies are 230 x 11 nm wide and 4 &186;m long in D. lymmae and 240 x 9 nm wide and 3.3 &186;m long in D. tetrakordyle. The S2 bodies have a diameter of 88 x 7 nm in D. lymmae and 65 x 6 nm in D. tetrakordyle. The apertures are unusual in being extremely small (internal diameter, 3-5 &186;m). Each aperture has a slit-like surface opening as small as 160 nm wide, surrounded by muscle fibres indicating that they may be opened and closed. The aperture is also surrounded and underlain by muscle fibres that may aid in secretion from, or even eversion of, the tissue within the aperture. Sensilla/cilia are also found within the apertures. Additional secretions from anteromedian and anterolateral glands (body glands), each containing granular secretions, occur in profusion and exit anteriorly and posteriorly to the position of the apertures, through duct openings in the general body tegument. These granular secretions do not appear to be associated with anterior adhesion. Both species show similarities in aperture, underlying tissue, sense organ, and secretion detail, in accordance with findings from other monogenean genera, and which supports the importance of such data for phylogenetic studies.

Additional key words: attachment, biological glue, tissue adhesion, Platyhelminthes, fish parasites


Invertebrate Biology 123(1):78-82
© 2004 American Microscopical Society, Inc.

Great Gordian knots: sex ratio and sexual size dimorphism in aggregations of horsehair worms (Gordius difficilis) Abstract. Large knots (>100 individuals) of adult horsehair worms (Gordius difficilis) were collected in several spring-fed habitats in Wisconsin and Minnesota. These aggregations were dominated numerically by males. Although distributions of length and diameter of males and females overlapped, females tended to be significantly longer and wider than males. Moreover, at any given length, females were wider than males. These findings confirm and add statistical support to previously published reports.

Additional key words: Nematomorpha, Gordiaceae


Invertebrate Biology 123(1):83-92
© 2004 American Microscopical Society, Inc.

Cloning and characterization of a candidate nutritive glycoprotein from the albumen gland of the freshwater snail, Helisoma duryi (Mollusca: Pulmonata) Abstract. The albumen gland is a female accessory sex gland that synthesizes and secretes perivitelline fluid around pulmonate eggs. The perivitelline fluid is composed of mainly galactogen and proteins, and is thought to provide nourishment to the embryos during development. We have previously identified the major secretory protein of the albumen gland of the freshwater snail Helisoma duryi as a native glycoprotein of 288 kDa, consisting of four 66-kDa subunits. In this study, the major albumen gland protein in H. duryi was purified, cloned, and the full-length cDNA sequence determined. Nucleotide sequence analysis revealed that the albumen gland protein (HdAGP) shared 83% identity with a partial cDNA sequence from a developmentally regulated albumen gland protein in Biomphalaria glabrata. The HdAGP mRNA was detected by RT-PCR in the albumen gland, ovotestis, mantle and digestive gland. SDS-PAGE analysis of the albumen gland protein in egg masses at different stages of development showed that the amount of HdAGP steadily decreased during embryogenesis, suggesting its possible catabolism by the developing embryos. Protein domain searches suggested that the HdAGP shared limited sequence identity, and adopted a similar three-dimensional conformation to the bactericidal, permeability increasing, protein family, raising the possibility of a potential bactericidal function for this important reproductive/developmental protein.

Additional key words: egg production, glycosylation