The burrowing behavior of the nematode Caenorhabditis elegans: a new assay for the study of neuromuscular disorders

The nematode Caenorhabditis elegans has been a powerful model system for the study of key muscle genes relevant to human neuromuscular function and disorders. The behavioral robustness of C. elegans, however, has hindered its use in the study of certain neuromuscular disorders because many worm models of human disease show only subtle phenotypes while crawling. By contrast, in their natural habitat, C. elegans likely spends much of the time burrowing through the soil matrix. We developed a burrowing assay to challenge motor output by placing worms in agar‐filled pipettes of increasing densities. We find that burrowing involves distinct kinematics and turning strategies from crawling that vary with the properties of the substrate. We show that mutants mimicking Duchenne muscular dystrophy by lacking a functional ortholog of the dystrophin protein, DYS‐1, crawl normally but are severely impaired in burrowing. Muscular degeneration in the dys‐1 mutant is hastened and exacerbated by burrowing, while wild type shows no such damage. To test whether neuromuscular integrity might be compensated genetically in the dys‐1 mutant, we performed a genetic screen and isolated several suppressor mutants with proficient burrowing in a dys‐1 mutant background. Further study of burrowing in C. elegans will enhance the study of diseases affecting neuromuscular integrity, and will provide insights into the natural behavior of this and other nematodes.     

Exploring sexual differences in external morphology and limb muscles of Hylarana guentheri (Anura: Ranidae) during non-breeding season

Studying sexual dimorphism facilitates better understanding of the general intersexual divergence of the same species and gives insights into the impact of selective forces on each sex. The sexual dimorphism in anuran external morphology or limb muscles has been well studied in reproductive context, but less so outside the breeding season. Herein, the intersexual differences in 12 external morphological characteristics, 11 forelimb and 12 hindlimb muscles of Hylarana guentheri during non-breeding season were investigated. We found that the males possessed significantly greater head width and tympanum diameter, while the females had significantly larger body size and head length; there was no sexual differences in the examined limb muscles, except for the mass of flexor carpi radialis. The larger body size means greater fertility for the females, and the longer head may be related to the allometry and reduce resource competition. For the males, the wider head is likely correlated with prey size and male–male competition, and also, the larger tympanum and heavier flexor carpi radialis probably aid the productive success. This study provides the comprehensive morphological accounts about the sexual differences of H. guentheri during non-breeding season, which will contribute to clarify the sex-specific resource allocation and reproductive strategies of anurans.     

Burrowing behaviour of the European eel (Anguilla anguilla): Effects of life stage

The European eel (Anguilla anguilla) is a fascinating species, exhibiting a complex life cycle. The species is, however, listed as critically endangered on the IUCN Red List due to an amalgam of factors, including habitat loss. This study investigated the burrowing behaviour and substrate preference of glass, elver and yellow stages of A. anguilla. Preference was determined by introducing eels in aquaria with different substrates and evaluating the chosen substrate for burrowing. In addition, burrowing was recorded using a camera in all substrate types and analysed for kinematics. The experiments showed that all of these life stages sought refuge in the sediments with particle sizes ranging from sand to coarse gravel. Starting from a resting position, they shook their head horizontally in combination with rapid body undulations until half of their body was within the substrate. High-speed X-ray videography revealed that once partly in the sediment, eels used only horizontal head sweeps to penetrate further, without the use of their tail. Of the substrates tested, burrowing performance was highest in fine gravel (diameter 1–2 mm; lower burrowing duration, less body movements and/or lower frequency of movements), and all eels readily selected this substrate for burrowing. However, glass eels and elvers were able to use coarse gravel (diameter >8 mm) because their smaller size allowed manoeuvring through the spaces between the grains. Further, burrowing performance increased with body size: glass eels required more body undulations compared to yellow eels. Interestingly, the urge to hide within the sediment was highest for glass eels and elvers. Documentation of substrate preference and burrowing behaviour of A. anguilla provides new information about their potential habitat use. Considering that habitat alterations and deteriorations are partly responsible for the decline of the eel, this information can contribute to the development of more effective conservation measures.     

Relationships between environmental gradients and geographic variation in the intraspecific body size of three species of frogs (Anura)

The relationship between environmental gradients and patterns of geographic variation in body size has been a controversial topic for ectothermic organisms globally. To examine whether the patterns that generally hold in more temperate species also hold for tropical ones, we examined the intraspecific body size variation in three species of Neotropical frogs, Dendropsophus minutus, Hypsiboas faber and Physalaemus cuvieri, along different environmental gradients (e.g. temperature, precipitation and topography). We analysed four competing hypotheses: (i) the water availability hypothesis that predicts a negative relationship between body size and precipitation; (ii) the heat balance hypothesis that predicts a negative relationship between body size and temperature; (iii) the topography hypothesis that predicts a negative relationship between body size and altitude; and (iv) the mixed‐effect hypothesis that predicts that individuals occurring in wet and cold sites would be larger than individuals occurring in dry and warm sites. The spatial pattern of geographic variation in body size among populations of H. faber was associated with the mixed‐effect hypothesis. In localities with low precipitation seasonality and cold conditions, H. faber individuals were larger than in localities with high precipitation seasonality and warm conditions. Variation in the body size of D. minutus was the opposite of that predicted by the heat balance hypothesis. Individuals in localities with high temperatures were larger than in localities with low temperatures. On the other hand, variation in the body size of P. cuvieri was not associated with the variables used in this study. Our results suggest that intraspecific variation in anuran body size is more dependent on species‐specific response than on the region (i.e. temperate or tropical) where they occur.     

Food and feeding behavior of the hoplonemertean Oerstedia dorsalis

The monostiliferous nemertean Oerstedia dorsalis was collected from eelgrass (Zostera marina) beds located along the coast of New Jersey, and feeding responses to amphipods and isopods were observed in the laboratory. Tests with 46 worms showed that they fed suctorially on Ampelisca vadorum, Ampithoe longimana, Corophium acherusicum and C. tuberculata. Corophiids were preferred. Upon contact with an amphipod, the proboscis is everted and strikes the prey on the ventral side, immobilizing it in a few minutes. The worm probes the sternal region with its head and everts its proboscis one or more times during the process. The exoskeleton is eventually penetrated by the head, and the stomach is everted into the hemocoel as a flattened funnel-like structure. Peristaltic undulations of the body signify the suctorial action that removes the living contents from the exoskeleton. The actual feeding process (from head penetration to removal of the head) takes about 7 min. O. dorsalis is only the third species within the Prosorhochmidae for which the feeding behavior has been documented. The other two are terrestrial species, and are also suctorial.     

The musculature of the papuan frog Phrynomantis stictogaster (Anura,Microhylidae)

The musculature of Phrynomantis stictogaster, a burrowing Papuan microhylid frog, of the subfamily Asterophryinae, is described and compared with accounts of other frogs. P. stictogaster exhibits unusual characters: dense musculature investing an entirely adherent tongue; exceptionally massive jaw musculature; and hitherto underscribed attachments of some muscles in the manus and pes. The presence of an accessory tendon to the M. glutaeus magnus and the pattern of distal thigh tendons confirm previous diagnosis of the Microhylidae, but the presence of an accessory head to M. adductor magnus is a condition previously not noted in the family. Features of the hyoid, pectoral, and thigh muscles resemble those of members of the subfamilies Dyscophinae, Microhylinae, and Spenophryninae.     

Using 3D-digital photogrammetry to examine scaling of the body axis in burrowing skinks

Three-dimensional (3D) modeling techniques have been increasingly utilized across disciplines for the visualization and analysis of complex structures. We employ 3D-digital photogrammetry for understanding the scaling of the body axis of 12 species of scincid lizards in the genus Brachymeles. These skinks represent a diverse radiation which shows tremendous variation in body size and degree of axial elongation. Because of the complex nature of the body axis, 3D-methods are important for understanding how the body axis evolves. 3D-digital photogrammetry presents a flexible, inexpensive, and portable system for the reconstruction of biological forms. As body size increased among species, the cross-sectional area and circumference of the head and other portions of the body axis increased isometrically, which indicates that species of differing sizes possess proportionally similar head and body shapes. These results suggest that there are no substantial head and body shape changes with body size among the sampled species, but further comparative studies with larger sample sizes and functional studies of size and morphology effects on burrowing or above-ground locomotion are needed.     

Postmetamorphic ontogenetic allometry and the evolution of skull shape in Nest‐building frogs Leptodactylus (Anura: Leptodactylidae)

Allometry constitutes an important source of morphological variation. However, its influence in head development in anurans has been poorly explored. By using geometric morphometrics followed by statistical and comparative methods we analyzed patterns of allometric change during cranial postmetamorphic ontogeny in species of Nest‐building frogs Leptodactylus (Leptodactylidae). We found that the anuran skull is not a static structure, and allometry plays an important role in defining its shape in this group. Similar to other groups with biphasic life‐cycle, and following a general trend in vertebrates, ontogenetic changes mostly involve rearrangement in rostral, otoccipital, and suspensorium regions. Ontogenetic transformations are paralleled by shape changes associated with evolutionary change in size, such that the skulls of species of different intrageneric groups are scaled to each other, and small and large species show patterns of paedomorphic/peramorphic features, respectively. Allometric trajectories producing those phenotypes are highly evolvable though, with shape change direction and magnitude varying widely among clades, and irrespective of changes in absolute body size. These results reinforce the importance of large‐scale comparisons of growth patterns to understand the plasticity, evolution, and polarity of morphological changes in different clades.     

Burrowing behavior and burrowing energetics of a bioindicator under human disturbance

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Bony-tailed tadpoles: the development of supernumerary caudal vertebrae in larval megophryids (Anura)

The axial skeleton in most anuran families consists of or=7). Tadpoles from each genus are typically found in streams, where their extended caudal skeleton anchors muscles that facilitate tadpoles wiggling between plant debris and rocks or even burrowing into the stream bed. The extra centra of megophryids ossify differently in each genus. In Leptobrachella and Ophryophryne, the caudal centra ossify around the entire notochord, whereas in Megophrys and Xenophrys each develops from dorsal and ventral pairs of ossifications that expand to meet each other. The evolutionary loss of caudal centra, an apomorphic anuran trait, is reversed in larval megophryids and confirms that the machinery for caudal vertebral development has been retained in some modern anurans. A likely driving force in the reappearance of the trait in megophryids is the selective pressure associated with a riparian lifestyle.     

Multiple predator effects on size-dependent behavior and mortality of two species of anuran larvae

This study examined the effects of multiple predators on size‐specific behavior and mortality of two species of anuran larvae. Particularly, we focused on how trait changes in predators and prey may be transmitted to other species in the food web. In laboratory experiments, we examined the effects of bluegill sunfish, Lepomis macrochirus, and the odonate larva Anax junius on behavior and mortality of tadpoles of the bullfrog, Rana catesbeiana, and the green frog R. clamitans. Experiments were conducted with predators alone and together to assess effects on behavior and mortality of the tadpoles. The experiments were replicated on five size classes of the tadpoles to evaluate how responses varied with body size.
Predation rates by Anax were higher on bullfrogs than on green frogs, and both bullfrogs and green frogs suffered greater mortality from Anax than from bluegill. Bluegill only consumed green frogs. Predation rates by both predators decreased with increasing tadpole size and decreased in the non‐lethal (caged) presence of the other predator. Both anuran larvae decreased activity when exposed to predators. Bullfrogs, however, decreased activity more in the presence of Anax than in the presence of bluegill, whereas green frogs decreased activity similarly in the presence of both predators. The largest size class of green frogs, but not of bullfrogs, exhibited spatial avoidance of bluegill. These responses were directly related to the risk posed by the different predators to each anuran species. Anax activity (speed and move frequency) also was higher when alone than in the non‐lethal presence of bluegill. We observed decreased predation rate of each predator in the non‐lethal presence of the other, apparently caused by two different mechanisms. Bluegill decreased Anax mortality on tadpoles by restricting the Anax activity. In contrast, Anax decreased bluegill mortality on tadpoles by reducing tadpole activity. We discuss how the activity and spatial responses of the tadpoles interact with palatability and body size to create different mortality patterns in the prey species and the implications of these results to direct and indirect interactions in this system.     

Serous gland dimorphism in the skin of Melanophryniscus stelzneri (Anura: Bufonidae)

Two serous gland types (I and II) in the skin of the Argentine toad Melanophryniscus stelzneri were discovered using light and electron microscopy. Glands of the two types differ in several traits: features of the products (both mature and immature), organelles involved in biosynthesis, and paths of serous maturation. No consistent differences, however, were detected between the myoepithelial sheaths encircling the secretory units. Type I glands manufacture vesicles containing a single dense body with a repeating substructure and conform to the fundamental secretory line of bufonid skin, a secretory line involved in biosynthesis of steroids. Type II glands synthesize granules of varying densities and seem to belong to a line of glands that secrete proteinaceous products. The occurrence of the two serous gland types in Melanophryniscus stelzneri is discussed in a comparison with current literature on the morphofunctional characteristics of anuran poison glands, which perform both regulative and defensive roles. It is suggested that di- or polymorphism in serous glands is an adaptive trait that allows differential release of active molecules on the body surface. J. Morphol. 237:19–32, 1998. © 1998 Wiley-Liss, Inc.     

Influence of age and environmental factors on burrow-making behavior of the short-tailed cricket,Anurogryllus muticus (De Geer) (Orthoptera: Gryllidae)

For the short-tailed cricket, Anurogryllus muticus, burrow-making behavior is essential. All nymphal instars construct burrows, but in the adult stage the rate of burrowing behavior is age dependent. Increases in photophase and light intensity stimulate burrowing, and the explicit negative phototaxis is correlated with the cricket's inability to exist under dry conditions. Ingestion of substrate during burrow construction may serve to acquire additional moisture. There is no evidence of burrow recognition, and crickets can construct a burrow when needed. The natural distribution of burrows at the plot investigated on Moorea supports the notion thatA. muticus builds burrows where the preferred food plantAlysicarpus vaginalis is most abundant. By minimizing the traveling distance to food sources when foraging they can retreat to their burrow again.     

Histology and microscopic anatomy of the thyroid gland during the larval development of Pseudis platensis (Anura,Hylidae)

Several hormones regulate anuran larval development, most notably thyroid hormones (THs). In anurans, metamorphosis fails when the thyroid gland is absent or inactivated, resulting in giant tadpoles. Larval gigantism occurs naturally in neotropical frogs of the genus Pseudis as a result of a prolonged larval period. Its thyroid function is poorly investigated and the focus of this study. We describe qualitative and quantitative variations in larval development for field-captured specimens of Pseudis platensis and compare those to the development of two sympatric species, Phyllomedusa sauvagii and Pithecopus azureus, which have small tadpoles and a shorter larval period. We describe morphological changes in the thyroid glands of larval and adult specimens. In contrast to other species with similar ecological requirements, P. platensis exhibits distinct glandular activity. During premetamorphosis, there was little or no thyroid activity, a period in which the tadpole reached 70% of its maximum size. Development and degree of activity of the thyroid gland determine the duration of the early stages of the larval period. Thyroid gland histology in tadpoles appears to correlate with the TH activity, and in turn with the diversity in anuran life history transitions.     

A comparison of crayfish burrow morphologies: Triassic and Holocene fossil,paleo‐ and neo‐ichnological evidence,and the identification of their burrowing signatures

The architectural and surficial morphologies of crayfish burrows from the Upper Triassic Chinle Formation and Holocene sediments were compared in order to determine: 1) if Triassic burrows could truly be attributed to crayfish activity; 2) how comparable the burrowing mechanisms are; and 3) whether or not a common set of burrowing signatures could be identified for both ancient and modern freshwater crayfish. Materials used in this study include burrows from the members of the Upper Triassic Chinle Formation, casts of modern burrows constructed by Procambarus clarkii Hobbs and Procambarus acutus acutus (Girard) in the laboratory, and casts of naturally constructed modern burrows of Cambarus diogenes di‐ogenes (Girard).

Triassic and Holocene crayfish burrow morphologies exhibit simple to complex architectures, varying degrees of branching, chamber, and chimney development. They also exhibit relatively textured surficial morphologies (bioglyphs) such as scrape and scratch marks, mud‐ and lag‐liners, knobby and hummocky surfaces, pleopod striae, and body impressions. Holocene crayfish construct distinctive burrows due to their conservative limb arrangement, functional morphology, and behavior with respect to environmental stimuli. Similarities between Holocene and Triassic crayfish burrows suggest that extant and Triassic crayfish employed identical burrowing mechanisms. Features of the surficial and architectural morphologies impart a distinctive signature to burrows of both ancient and modern freshwater burrowing crayfish.

Burrowing signatures of crayfish can be used to identify new and previously misinterpreted continental trace fossils. These are useful in studies of the paleohydrogeology, paleoclimatology and paleoecol‐ogy of burrow‐bearing deposits.     

An assessment of endemism and species richness patterns in the Australian Anura

Aim To assemble a continental‐scale data set of all available anuran records and investigate trends in endemism and species richness for the Anura. Location Continental Australia. Methods 97,338 records were assembled, covering 75% of the continent. A neighbourhood analysis was applied to recorded locations for each species to measure richness and endemism for each half‐degree grid square (c. 50 km) in the continent. This analysis was performed for all anurans, and also for each of the three main anuran families found in Australia. A Monte Carlo simulation was used to test a null hypothesis that observed centres of endemism could result simply from an unstructured overlapping of species ranges of different sizes. Results Eleven main centres of anuran endemism were identified, the most important being the Wet Tropics and the south‐west near Bunbury‐Augusta and near Walpole. With the exception of south‐western Australia, all of the identified significant endemic centres are in the northern half of the continent. The regions identified as significant for endemism differed from those identified for species richness and are more localized. Species richness is greatest in the Wet Tropics and the Border Ranges. High species richness also occurs in several areas not previously identified along the east and northern coasts. Main conclusions Weighted endemism provides a new approach for determining significant areas for anuran conservation in Australia and areas can be identified that could be targeted for beneficial conservation gains. Patterns in endemism were found to vary markedly between the three main anuran families, and south‐eastern Australia was found to be far less significant than indicated by previous studies. The need for further survey work in inland Australia is highlighted and several priority areas suggested. Our results for species richness remain broadly consistent with trends previously observed for the Australian Anura.     

Polystomatidae (Monogenea) of African Anura: Polystoma dawiekoki n. sp. parasitic in Ptychadena anchietae (Bocage)

Polystoma dawiekoki n. sp. is described as a new species of the Polystomatidae parasitic in the urinary bladder of the plain grass frog Ptychadena anchietae. This parasite was collected at Mkuze town and Mkuze Game Reserve in northern Kwazulu-Natal Province, in the Kruger National Park in Mpumalanga Province, South Africa, and at Bulwa in Tanga Province, East Usambara Mountains, Tanzania. It is distinguished from other African Polystoma species by a combination of characters, including the body size, size and shape of marginal hooklets and the haptor length to body length ratio. The presence of adult, as well as subadult, parasites in the same individuals, as is known for Eupolystoma, represents a significant evolutionary departure from the pattern of transmission typical of Polystoma in most of the other anuran hosts.