William E. Bemis

Development and microstructure of tooth histotypes in the blue shark, Prionace glauca (Carcharhiniformes: Carcharhinidae) and the great white shark, Carcharodon carcharias (Lamniformes: Lamnidae)

Elasmobranchs exhibit two distinct arrangements of mineralized tissues in the teeth that are known as orthodont and osteodont histotypes. Traditionally, it has been said that orthodont teeth maintain a pulp cavity throughout tooth development whereas osteodont teeth are filled with osteodentine and lack a pulp cavity when fully developed. We used light microscopy, scanning electron microscopy, and high‐resolution micro‐computed tomography to compare the structure and development of elasmobranch teeth representing the two histotypes. As an example of the orthodont histotype, we studied teeth of the blue shark, Prionace glauca (Carcharhiniformes: Carcharhinidae). For the osteodont histotype, we studied teeth of the great white shark, Carcharodon carcharias (Lamniformes: Lamnidae). We document similarities and differences in tooth development and the microstructure of tissues in these two species and review the history of definitions and interpretations of elasmobranch tooth histotypes. We discuss a possible correlation between tooth histotype and tooth replacement and review the history of histotype differentiation in sharks. We find that contrary to a long held misconception, there is no orthodentine in the osteodont teeth of C. carcharias. J. Morphol. 276:797–817, 2015.

Social dynamics and dispersal in free-living prairie voles (Microtus ochrogaster)

Abstract Following dispersal from 1 group, individuals may join other established social groups. Such intergroup transfer may increase access to potential mates and decrease mate competition. We used data from 402 individuals to examine patterns of intergroup transfer in prairie voles (Microtus ochrogaster). Nearly 32% of established social groups (single female units, male–female pairs, or communal groups of at least 2 adults of the same sex) were joined by 1 or more individuals. Most individuals (76%) that joined social groups were wanderers that were either unmarked, recently marked during grid trapping, or marked transients; 70% were males. Joining a group was not contingent upon recent disappearance of residents. Total number of residents positively affected the probability of a female joining a social group, whereas number of adult female residents and population density negatively affected it. Some individuals (24%) moved directly from one group to another without an intervening wandering stage; we refer to these instances of intergroup transfer as direct transfers. Most direct transferers moved into nearby groups, but not the closest group. Males were more likely than females to directly transfer into groups with potential mates and without potential competitors. Thus, males directly transferred in a manner consistent with maximizing reproductive opportunities. In contrast, 25% of females directly transferred into groups without potential mates and 96% into groups with at least 1 adult female. Females may be less constrained by group composition with respect to potential mates because wandering males, with which females can mate, are prevalent. All-male groups almost never occur in our population, so females probably cannot avoid joining groups with competitors.

Suckling behaviour in three species of voles

Summary Domestic mammals exhibit diversity in suckling behaviour, yet little is known about suckling in most wild species, including rodents with tenacious nipple attachment. This behaviour, whereby young cling tightly to nipples, has been interpreted as an adaptation to competition within and among litters for nipples and milk. Comparative studies of suckling behaviour of tenacious and non-tenacious species are lacking, however, as are studies placing patterns of suckling in a phylogenetic context. We compared suckling in prairie voles (Microtus ochrogaster; tenacious nipple attachment), woodland voles (= pine voles, M. pinetorum; tenacious nipple attachment) and meadow voles (M. pennsylvanicus; non-tenacious nipple attachment). We hypothesized that suckling behaviour of meadow voles differs from that of the other two species. We found that meadow vole pups display higher frequencies of nipple attachment, shorter durations of nipple attachment (significantly different from prairie voles only), more frequent nipple-switching, and no preference for nipple pairs (prairie vole and woodland vole young preferred the hindmost nipples). Mapped onto a phylogeny, our data suggest a suite of behavioural characters associated with suckling in prairie and woodland voles (tenacious nipple attachment, preference for hindmost nipples, and infrequent nippleswitching) and highlight diversity of suckling behaviour among closely related species.

Litter Size Influences Maternal but not Paternal Care in Three Species of Voles, as Measured by Nest Attendance

Abstract Total parental expenditure of mammals and birds has been predicted to increase with litter or brood size, but data from rodents provide little support for this prediction. We examined the effects of natural variation in litter size on parental nest attendance in pine (= woodland), prairie, and meadow voles housed in seminatural environments. In all 3 species, mothers spent less time in the nest with large litters than with small; time spent in the nest by fathers was unaffected by litter size. We suggest that failure to meet the prediction of increased parental expenditure with increased litter size reflects basic differences in the manner in which mammals and birds feed altricial young.

Shark teeth as edged weapons: serrated teeth of three species of selachians

Prior to European contact, South Pacific islanders used serrated shark teeth as components of tools and weapons. They did this because serrated shark teeth are remarkably effective at slicing through soft tissues. To understand more about the forms and functions of serrated shark teeth, we examined the morphology and histology of tooth serrations in three species: the Tiger Shark (Galeocerdo cuvier), Blue Shark (Prionace glauca), and White Shark (Carcharodon carcharias). We show that there are two basic types of serrations. A primary serration consists of three layers of enameloid with underlying dentine filling the serrations base. All three species studied have primary serrations, although the dentine component differs (orthodentine in Tiger and Blue Sharks; osteodentine in the White Shark). Smaller secondary serrations are found in the Tiger Shark, formed solely by enameloid with no contribution from underlying dentine. Secondary serrations are effectively serrations within serrations that allow teeth to cut at different scales. We propose that the cutting edges of Tiger Shark teeth, equipped with serrations at different scales, are linked to a diet that includes large, hard-shelled prey (e.g., sea turtles) as well as smaller, softer prey such as fishes. We discuss other aspects of serration form and function by making analogies to man-made cutting implements, such as knives and saws.

Identification of Shark Teeth (Elasmobranchii: Lamnidae) from a Historic Fishing Station on Smuttynose Island, Maine, Using Computed Tomography Imaging

Abstract - Two incomplete shark teeth were recovered during archaeological excavation of a historic fishing station on Smuttynose Island, ME. Specimens were identified to the species-level using non-destructive computed tomography (CT) imaging techniques. Their external and internal morphology is described and illustrated. Both teeth are from large sharks in the Order Lamniformes. The larger specimen is a developing tooth from the upper jaw of a Carcharodon carcharias (White Shark). The second specimen is a broken tooth from the lower jaw of a Lamna nasus (Porbeagle). The Smuttynose excavations provide an opportunity to examine faunal assemblages and the islands historic 17th-through 19th-century fisheries. Criteria for identifying teeth of common pelagic sharks of the Western North Atlantic are offered, and the role of sharks in the historic Gulf of Maine fishery is discussed.

Evolution of the Branchiostegal Membrane and Restricted Gill Openings in Actinopterygian Fishes

A phylogenetic survey is a powerful approach for investigating the evolutionary history of a morphological characteristic that has evolved numerous times without obvious functional implications. Restricted gill openings, an extreme modification of the branchiostegal membrane, are an example of such a characteristic. We examine the evolution of branchiostegal membrane morphology and highlight convergent evolution of restricted gill openings. We surveyed specimens from 433 families of actinopterygians for branchiostegal membrane morphology and measured head and body dimensions. We inferred a relaxed molecular clock phylogeny with branch length estimates based on nine nuclear genes sampled from 285 species that include all major lineages of Actinopterygii. We calculated marginal state reconstructions of four branchiostegal membrane conditions and found that restricted gill openings have evolved independently in at least 11 major actinopterygian clades, and the total number of independent origins of the trait is likely much higher. A principal component analysis revealed that fishes with restricted gill openings occupy a larger morphospace, as defined by our linear measurements, than do fishes with nonrestricted openings. We used a decision tree analysis of ecological data to determine if restricted gill openings are linked to certain environments. We found that fishes with restricted gill openings repeatedly occur under a variety of ecological conditions, although they are rare in open‐ocean pelagic environments. We also tested seven ratios for their utility in distinguishing between fishes with and without restricted gill openings, and we propose a simple metric for quantifying restricted gill openings (RGO), defined as a ratio of the distance from the ventral midline to the gill opening relative to half the circumference of the head. Functional explanations for this specialized morphology likely differ within each clade, but its repeated evolution indicates a need for a better understanding of diversity of ventilatory morphology among fishes. J. Morphol. 276:681–694, 2015.

Parental behaviour of prairie voles (Microtus ochrogaster) and meadow voles (M. pennsylvanicus) in relation to sex of offspring

Monogamous parents are predicted to invest equally in male and female offspring whereas polygynous parents in good condition are predicted to invest more in male than female offspring. Sex-biased parental investment can occur in three ways: (1) mothers and fathers invest different amounts of care in their offspring (effect of parent sex); (2) parents invest different amounts of care in male and female offspring (effect of offspring sex); and (3) one parent, but not the other, invests different amounts of care in male and female offspring (interaction between parent sex and offspring sex). Studies of parent–offspring interactions in rodents have focused on either effect of parent sex or effect of offspring sex, but not the interaction between parent sex and offspring sex, and most studies have examined only one species. We studied prairie voles (Microtus ochrogaster), a monogamous species, and meadow voles (M. pennsylvanicus), a polygynous (or promiscuous) species, under laboratory conditions designed to simulate field conditions. For each species, we recorded the frequency and duration with which mothers and fathers licked their male and female offspring. We found that meadow vole fathers licked male offspring for longer durations than female offspring. However, prairie vole fathers, prairie vole mothers, and meadow vole mothers did not lick male and female pups for different durations. From the standpoint of the pups, male prairie vole pups, female prairie vole pups, and female meadow vole pups were licked for longer durations by their mothers than by their fathers. In contrast, for male meadow vole pups there was no difference in the duration with which they were licked by mothers and fathers. We also detected effects of litter size: as litter size increased, the frequency and duration of pup licking decreased for mothers and increased for fathers. For duration (but not frequency) of pup licking, these changes were more dramatic in meadow voles than in prairie voles. Our data are generally consistent with predictions that monogamous parents, such as prairie voles, should invest equally in male and female offspring whereas polygynous (or promiscuous) parents, such as meadow voles, should invest more in male offspring when conditions are favourable. Our data also highlight the complexity of parent–offspring interactions in rodents and emphasize the need to examine whether male and female offspring within a species differ in their behaviour or ability to obtain parental care.

Functional morphology of gill ventilation of the goosefish, Lophius americanus (Lophiiformes: Lophiidae)

The goosefish, Lophius americanus, is a dorso-ventrally compressed marine fish that spends most of its life sitting on the substrate waiting to ambush prey. Species in the genus Lophius have some of the slowest ventilatory cycles recorded in fishes, with a typical cycle lasting more than 90s. They have a large gill chamber, supported by long branchiostegal rays and ending in a siphon-like gill opening positioned underneath and behind the base of the pectoral fin. Our goals were to characterize the kinematics of gill ventilation in L. americanus relative to those of more typical ray-finned fishes, address previous assertions about ventilation in this genus, and describe the anatomy of the gill opening. We found that phase 1 of ventilation (during which both the buccal and gill chamber are expanding) is greatly increased in duration relative to that of typical ray-finned fishes (ranging from 62 to 127s), and during this phase, the branchiostegal rays are slowly expanding. This slow expansion is almost visually imperceptible, especially from a dorsal view. Despite this unusually long phase 1, the pattern of skeletal movements follows that of a typical actinopterygian, refuting previous assertions that Lophius does not use its jaws, suspensorium, and operculum during ventilation. When individuals were disturbed from the sediment, they tended to breathe more rapidly by decreasing the duration of phase 1 (to 18-30s). Dissections of the gill opening revealed a previously undocumented dorsal extension of the adductor hyohyoideus muscle, which passes from between the branchiostegal rays, through the ventro-medial wall of the gill opening, and to the dorsal midline of the body. This morphology of the adductor hyohyoideus shares similarities with that of many Tetraodontiformes, and we suggest that it may be a synapomorphy for Lophiiformes+Tetraodontiformes. The specialized anatomy and function of the gill chamber of Lophius represents extreme modifications that provide insight into the potential limits of the actinopterygian gill ventilatory system.

Benthic walking, bounding, and maneuvering in flatfishes (Pleuronectiformes: Pleuronectidae): New vertebrate gaits

Video-based observations of voluntary movements reveal that six species of pleuronectid flatfishes use sequential portions of long-based dorsal and anal fins as feet (hereafter, fin-feet) to move on the substrate. All six species used a gait that we term walking, which produced constant forward movement, and several of these species also used a second gait that we call bounding for intermittent movements over the substrate. We selected Pacific Sand Sole, Psettichthys melanostictus, and English Sole, Parophrys vetulus, for kinematic analyses of these two gaits. Psettichthys melanostictus consistently used walking for benthic locomotion; Parophrys vetulus primarily used a bounding gait. During forward walking, a fin ray swings up off the substrate, protracts and converges with neighboring fin rays to contribute to a fin-foot. The fin-foot pushes down on the substrate and rotates posteriorly by sequential recruitment of fin rays, a pattern known as a metachronal wave. As one fin-foot passes off the posterior end of the fin, a new fin-foot forms anteriorly. During bounding, undulations of the body and tail assist one or two waves of fin-feet, producing rapid but intermittent forward acceleration of the body. Flatfishes also use fin-feet to maneuver on the substrate. The Starry Flounder, Platichthys stellatus, performs near zero displacement rotation by running waves of fin-feet in opposing directions along the dorsal and anal fins. Although other teleosts use specialized pectoral fin rays for bottom walking (e.g., Sea Robins: Triglidae), the duplication of structures and patterns of movement in the median fins of flatfishes more closely resembles metachronal motions of millipede feet or the parapodia of polychaete worms. Sequential use of median fin rays in flatfishes resembles that of other teleosts that swim with elongate median fins, including Amiiformes, Gymnotiformes, and some Tetraodontiformes, but flatfishes offer a novel form of substrate locomotion based on dorsal and anal fins.