Invertebrate Biology

Cover image for Vol. 135 Issue 2

Edited By: Michael W. Hart

Impact Factor: 1.23

ISI Journal Citation Reports © Ranking: 2015: 62/103 (Marine & Freshwater Biology); 64/160 (Zoology)

Online ISSN: 1744-7410

Cover Gallery


Volume 135, Issue 1
Volume 135, Issue 2
Many invertebrates live out of sight in subterranean habitats. In the ocean, these habitats include underground lakes with distinctive faunas and specific adaptations for life underground. On land, these habitats include the unusual faunas of caves. Hypogeal ecosystems are less well understood by ecologists (compared to above-ground ecosystems) because the animals and their interactions are often difficult to study. In this issue, Mammola and Isaia (pp. 20–30) analyze the habitat and distribution of an endemic Alpine subterranean spider belonging to the genus Troglohyphantes (shown on the cover). They used a cleverly chosen field site: a small abandoned graphite mine in the Italian Alps, where the regularity of the mine excavation allowed the authors to map the distribution of spiders, their prey organisms, and the key environmental features of the hypogeal habitat (especially temperature, light intensity, and humidity). These distributional analyses allowed the authors to characterize the ecological niche of T. vignai. Spider abundance and distribution varied little over the seasons, and was mainly affected by a tradeoff between a preference for the darkest parts of the habitat (which are found far from the “twilight zone” at the mine entrance) and a need to forage for arthropod prey (which are more abundant near the mine entrance). Hypogeal habitats may be especially useful places to develop ecological niche models, and to identify such tradeoffs, because of the relatively simple structure of these underground communities. (Photograph of Troglohyphantes bornensis, body length ~3.5 mm, by F. Tomasinelli.) Animals that change types of food and ways of feeding during the life cycle are of broad general interest because such diet shifts can involve simultaneous changes in behavior, physiology, morphology, habitat use, and other traits. Several examples of diet shifting are known among decapod crabs, which use a pair of large claws (or chelipeds) for feeding. However, these chelipeds have other well-known uses and adaptive significance, including defense against predators. In crabs of the family Ocypodidae (the ghost crabs and fiddler crabs), the chelipeds may also show sexual dimorphism and left-right asymmetry associated with their use in mating behavior. In such species, diet shifting and its morphological basis may be especially interesting because it evolves under the influence of selection on feeding as well as selection on other adaptive features of the chelipeds. In this issue, Lim and colleagues (pp. 117–126) explored the morphological basis for diet changes in the ghost crab Ocypode gaudichaudii from the tropical eastern Pacific of Panama. Analysis of gut contents resolved conflicts among previous studies, and showed that these ghost crabs are predators as small juveniles but expand the diet to a mixture of animal prey and benthic diatoms as larger adults. This change to a generalist diet is associated with a specialized shape of the cheliped tip to form a truncated or blunt shovel used for collecting sediment and feeding on diatoms. The development of a specialized form (the truncated claw) associated with a generalized diet (predation plus diatom grazing) seems paradoxical, and might be related to constraints on feeding imposed by the ghost crab environment (especially few animal prey to support large, energetic adults), or constraints imposed by the other functional features of the chelipeds. (Photograph of Ocypode gaudichaudii by A. Y. P. Yong; body width ~3 cm.)


Volume 134, Issue 1
Volume 134, Issue 2
Sponges undergo a variety of asexual reproductive processes, including budding—the formation of small clusters of cells that can break off of the parent sponge and develop into independent individuals. Though the phenomenom of budding has been described in numerous species of sponges, little is known about the dynamics of bud production in natural habitats. In this issue (pp. 19–30), Singh and Thakur describe seasonal patterns of budding in nature in the marine demosponge Cinachryella cavernosa. An adult of this sponge (~4 cm in diameter) is shown on this issue’s cover; the bright yellow objects on its surface are buds. Several settled buds can be seen on the rock to the lower right of the adult. Singh and Thakur quantified budding patterns in individual sponges in the low intertidal zone over a period of two years, finding that budding is highly seasonal, and that its frequency is closely correlated with water temperature. They also examined the morphology of developing buds, and the growth rates of settled buds. Such studies are essential for understanding the role of budding in sponge life histories. (Photograph by Anshika Singh and Narsinh Thakur.) Sizes of Florida populations of the giant Caribbean sea anemone, Condylactis gigantea, have declined in the past two decades, perhaps due to environmental changes, or perhaps due to increased harvest pressure. The histories of other populations (e.g., in southeast Brazil) suggest that such declines increase the risk of local extinction due to Allee effects. Understanding this sea anemone’s reproduction is clearly key to its conservation. In this issue (pp. 116–128), Sheridan, Fautin, & Garrett report on gametogenesis and reproductive periodicity of C. gigantea in the Florida Keys. An adult of that species, ~10 cm in oral disk diameter, is pictured on our cover. In addition to directly informing the decisions of population managers, their results—which include the demonstration of gonochory, and identification of the spawning season—will be extremely useful in designing studies to study other parameters (e.g., fecundity and recruitment) critical to the maintenance of these populations. (Photograph by Nancy Sheridan.)

Volume 134, Issue 3
Volume 134, Issue 4
Cave habitats are unusual among terrestrial habitats because most of their trophic resources are ultimately derived by transport from surface communities.The amount and distribution of these resources in caves may have strong effects on the biology of cave-dwelling species. In this issue, Manenti et al. (pp. 242–251) surveyed the “twilight zones” of many caves in two regions of Italy for the presence and abundance of a large invertebrate predator, the spider Meta menardi. An adult of that species ~17 mm in body length (excluding legs) is shown on our cover. They also quantified a variety of cave physical parameters and the abundance of a prey species, the fly Limonia nubeculosa. Across all caves surveyed, spiders were most likely to be found in caves with the highest abundance of prey species. Their results suggest that the distribution of trophic resources plays a large role in controlling the distribution of this predator; further, they suggest that the abundance of the easily surveyed spider may be a good indicator of the quantity of trophic resources available in a cave. (Photograph by Enrico Lunghi.) Female spiders deposit eggs within egg sacs made primarily of a type of silk produced in tubuliform glands. Silk produced in these glands is used only for egg sac production. In spiders that reproduce repeatedly, the silk-synthetic activity of the secretory cells of the tubuliform gland may be linked to the stage of the reproductive cycle. In this issue, Herrera et al. (pp. 332–340) examine cyclical changes in the morphology of the tubuliform gland and the ultrastructure of its secretory epithelial cells over the reproductive cycle of the Western black widow spider. They observed striking and reproducible changes in the structure of the gland over the reproductive cycle. For example, as shown on this issue’s cover, early in vitellogenesis, secretory cells of the tubuliform gland contain concentric lamellar rings of rough endoplasmic reticulum surrounding abundant, lightly staining granules (in the cover image, each of the six granules shown is ~1.5 μm in diameter). These granules presumably consist of silk proteins, as they appear to be exocytosed in the gravid spider. The striking cyclical patterns in cell activity and form Herrera et al. observed suggest that the tubuliform gland may be an excellent model for study of the regulation of silk protein gene expression, endomembrane transport, and exocytosis. (Transmission electron micrograph by Merri L. Casem.)


Volume 133, Issue 1
Volume 133, Issue 2
Ctenophores are gelatinous marine animals that use cilia for an unusually wide range of purposes, including locomotion, feeding, escape, and sensory responses, coordinated in part via epithelial and mesogleal nerve nets. In this issue (pp. 1–46), Tamm reviews a large body of work on the form, function, control, and development of ciliary structures in ctenophores. These data are particularly useful given the recent release of the whole genome of the ctenophore Mnemiopsis leidyi, along with phylogenomic analyses suggesting that ctenophores are the earliest living animals, a finding important for our understanding of the evolution of mesoderm and nervous systems. In addition to providing a timely review of the role of cilia in the life of ctenophores, Tamm also provided our cover illustration, a cut paper collage showing a lobate ctenophore like Mnemiopsis leidyi dining on copepods (printed and distributed by Local Colors Gallery, Woods Hole, Massachusetts at Invertebrate biologists have long been making observations of the fine structure of invertebrate sperm, with the aims of using these data to evaluate phylogenetic hypotheses and to understand how the functional requirements of sperm transfer and fertilization have shaped the evolution of sperm form. In this issue (pp. 146–157), Eckelbarger & Hodgson describe the formation and ultrastructure of the sperm of the spionid annelid Spio setosa. These cells have several unusual features, including a highly coiled nucleus. This is clearly seen in the cover illustration, a transmission electron micrograph of numerous sperm packed together in the spermatheca of a female of S. setosa (the largest nuclei visible in this section are about 10 µm in length along the axis of coiling). In addition, mature sperm in the male contain numerous membrane-bounded inclusions; these are absent from sperm stored in the female spermatheca, suggesting a function during transfer or storage. Additional comparative studies are required to fully understand the phylogenetic significance of these observations, and functional studies are needed to understand how sperm form is related to sperm function in this species. (Micrograph by Kevin Eckelbarger and Alan Hodgson.)

Volume 133, Issue 3
Volume 133, Issue 4
The evolution of segmentally arranged structures has long been a focus of intense research, especially in chordates, arthropods, and annelids. In this issue, Oliveira et al. (pp. 274–280) investigate the segmental arrangement of annuli in the integument of members of a different taxon, the peripatid onychophorans. While the dorsal integument of nearly all peripatids is composed of a conserved number of 12 annulations, or plicae, per segment, members of one species – Plicatoperipatus jamaicensis – have 24 annulations per segment. The “extra” 12 annulations might have arisen as duplicates of the original plicae, or may represent novel structures. Oliveira et al. show that, like in other peripatids, embryos of P. jamaicensis have only 12 segmental plicae, which persist in adults (indicated in blue in the cover image; each plica is ~50 µm wide). However, 12 additional rows of dermal papillae (which they term pseudoplicae; orange) are inserted between the plicae later in development. The pseudoplicae differ in position and structure from the plicae, as evidenced, for example, by the distribution of hyaline organs (purple). While in other peripatids these structures occur in the furrows between plicae, they lie on the pseudoplicae in P. jamaicensis. Oliveira et al. suggest that P. jamaicensis still have the ancestral pattern of 12 segmental plicae observed in other peripatids, but that this pattern was partially masked by the evolution of pseudoplicae. The functional significance (if any) of these novel structures is unknown. Comparative studies of the development of peripatids may be useful for understanding the molecular basis of this evolutionary novelty. (Scanning electron micrograph by Ivo de Sena Oliveira.) One common method for testing hypotheses of structural homology is to compare the developmental processes that generate those structures: homologous structures are generally expected to be formed by similar morphogenetic processes. In this issue, Tilic et al. (pp. 354–370) use this method to evaluate whether the hooded hooks (a type of chaeta) of eunicidan annelids arose independently of the hooded hooks of capitellid and spionid annelids. A hooded hook of one of their study species, the lumbrinerid Lumbrineris tetraura, is shown on the cover; its shaft is ~12 µm in width. Tilic et al. used light and electron microscopy to describe the arrangement and ultrastructure of the hooded hooks, as well as to make inferences about their formation, a process that is mediated by dynamic microvilli of chaetoblast cells. They found numerous differences in the formation of the chaetae of lumbrinerids compared to those of capitellids and spionids, and conclude that the hooded hooks of these two sets of taxa did indeed evolve independently. Their conclusion is consistent with inferences based on phylogenetic analyses. Such analyses will eventually help us to understand how annelid chaetae, which are critically important in the systematics of the group, have evolved. (Light micrograph by Ekin Tilic.)


Volume 132, Issue 1
Volume 132, Issue 2
Effective monitoring and conservation of animal populations requires knowledge of their dynamics, but these long time-series data are relatively rare in the literature, especially for threatened invertebrates. In this issue (pp. 46–51), Lawrence, Samways, Kelly, and Henwood describe a long time-series study of the population dynamics of the Seychelles Giant Millipede, Sechelleptus seychellarum, a large (the specimens pictured on the cover are ~20 cm in length) millipede endemic to granitic islands of the Seychelles. For 11 years, they monitored populations of this species on Cousine Island, the only Seychelles granitic island that is free of potentially predatory invasive mammals. Millipedes were most abundant and active during high rainfall months, leading the authors to suggest that any population manipulations (e.g., translocations, augmentations) should be done during this season. In addition, they suggest that control efforts for the invasive African big-headed ant, which involve the use of a pesticide that may affect millipedes, should be confined to low rainfall months, when millipede activity is at its lowest. (Image by James Lawrence.) Most living cephalopods can alter the color of their skin on fine spatial scales and rapid time scales, producing stunning visual displays that are important in prey capture, predator avoidance, mating, and communication. These color changes are driven in large part by the expansion or retraction of many thousands of pigmented chromatophore organs. In cephalopod chromatophore organs, pigment cell expansion is controlled by the contraction of radially arranged muscle cells. A number of chromatophore pigment cells surrounded by their radial muscles are shown in the cover image; the largest, most central pigment cell is roughly 400 μm in diameter. How radial muscles adhere to the flexible, elastic skin is an important, but previously undescribed, anatomical feature that enables chromatophore function. In this issue (pp. 120–132), Bell et al. use confocal and electron microscopy to show that the distal ends of the chromatophore radial muscle fibers of the squid Doryteuthis pealeii branch extensively, and that these branches are connected to the underlying basal lamina by costamere-like projections. These detailed observations of the form and function of cephalopod chromatophores may be useful as a source of “bio-inspiration” for the design of soft, flexible, adaptive displays. (Confocal micrograph by George Bell and Trevor Wardill.)

Volume 132, Issue 3
Volume 132, Issue 4
Methods to mark individuals are extremely useful in studies of the growth or dispersal of individuals. Animals that build calcitic skeletons can often be marked using fluorescent compounds – e.g., calcein or tetracycline – that are incorporated into their growing skeletons, and can later be viewed under appropriate illumination. In this issue (pp. 251–269), Johnson et al. report on a careful analysis of mark persistence and allometries of growth in the green sea urchin, Strongylocentrotus droebachiensis, after marking with four different fluorochromes. Marks were externally visible (thus allowing non-lethal examination) for nearly a year, and visible on internal structures (such as the 1.3 mm long jaw demipyramid labeled with calcein shown on the cover) for at least two years. Their results will aid in the design and interpretation of both laboratory and field studies of the growth, ecology, and evolution of sea urchins. (Fluorescence micrograph by Jonathan Allen and Amy Johnson.) Siboglinid annelids have long interested biologists because of their lack of a functional gut, their obligate nutritional symbioses with bacteria, and the unusual marine habitats (e.g., cold seeps and hydrothermal vents) they inhabit. Members of the siboglinid genus Osedax, first discovered in 2002, occupy yet another unusual habitat – burrows in the bones of dead vertebrates on the seafloor (hence their common name of “boneworms”). The macroscopic boneworms that were first discovered were females; males are microscopic, and live in harems in the gelatinous tubes formed by females. For several years it has been known that females spawn fertilized primary oocytes, as shown in the cover image of a female of an undescribed species of Osedax, O. ‘orange collar’ (the female’s trunk is ~0.4 mm in diameter). This suggests that fertilization is internal, but the mechanism of sperm transfer and location of fertilization have not been identified. In this issue (pp. 368–385), Katz and Rouse address those questions using a detailed analysis of the morphology of the female reproductive system in four species of Osedax. Their results show that males transfer unpackaged sperm to females, where it is stored in ovarian tissue before being used to fertilize oocytes. In addition to enhancing our understanding of the reproductive biology of boneworms, their data are useful in assessing homologies in the reproductive systems of siboglinids more broadly. (Macro photograph by Greg Rouse.)