The comparative morphology of pit organs in elasmobranchs

The pit organs of elasmobranchs (sharks, skates and rays) are free neuromasts of the mechanosensory lateral line system. Pit organs, however, appear to have some structural differences from the free neuromasts of bony fishes and amphibians. In this study, the morphology of pit organs was investigated by scanning electron microscopy in six shark and three ray species. In each species, pit organs contained typical lateral line hair cells with apical stereovilli of different lengths arranged in an “organ‐pipe” configuration. Supporting cells also bore numerous apical microvilli taller than those observed in other vertebrate lateral line organs. Pit organs were either covered by overlapping denticles, located in open grooves bordered by denticles, or in grooves without associated denticles. The possible functional implications of these morphological features, including modification of water flow and sensory filtering properties, are discussed. J. Morphol. 2009. © 2009 Wiley‐Liss, Inc.     

Phylogenetic trends in the abundance and distribution of pit organs of elasmobranchs

Pit organs (free neuromasts of the mechanosensory lateral line system) are distributed over the skin of elasmobranchs. To investigate phylogenetic trends in the distribution and abundance of pit organs, 12 relevant morphological characters were added to an existing matrix of morphological data (plus two additional end terminals), which was then re-analysed using cladistic parsimony methods ( paup * 4.0b10). Character transformations were traced onto the most parsimonious phylogenetic trees. The results suggest the following interpretations. First, the distinctive overlapping denticles covering the pit organs in many sharks are a derived feature; plesiomorphic elasmobranchs have pit organs in open slits, with widely spaced accessory denticles. Second, the number of pit organs on the ventral surface of rays has been reduced during evolution, and third, spiracular pit organs have changed position or have been lost on several occasions in elasmobranch evolution. The concentrated-changes test in macclade (version 4.05) was used to investigate the association between a pelagic lifestyle and loss of spiracular pit organs (the only character transformation that occurred more than once within pelagic taxa). Depending on the choice of tree, the association was either nonsignificant at P  = 0.06 or significant at P  < 0.05. Future studies, using species within more restricted elasmobranch clades, are needed to resolve this issue.     

Freshwater elasmobranchs: a review of their physiology and biochemistry

Only 5% of elasmobranch species live in freshwater (FW) compared to more than 40% of known teleost species. The factors affecting the poor penetration of elasmobranchs into FW environments are currently unknown, however, an important consideration may be the high urea requirement of many proteins in marine elasmobranchs. Urea is an important osmolyte in marine elasmobranchs and must be reduced in dilute environments. There are three identifiable stages in the successful colonization of FW. The euryhaline marine species freely entering and leaving FW represent the initial stage of FW colonization. In this group, there is an apparent inability to eliminate all urea due to protein integrity issues and this results in energy and nitrogen losses that may constrain growth and reproduction. The second stage is represented by those species that live entirely in FW but must also retain some urea. This group also suffers from the same constraints as the first group. These two groups have kidneys and sensory organs that more closely resemble strictly marine forms. The third and final stage is represented by the Potamotrygonid stingrays where the need for urea in FW has been eliminated. Consequently nitrogen and energy losses are reduced and those sections of the kidney needed for urea conservation have been eliminated. The driving force for such modifications is a reduction in urea levels and the concomitant saving of energy needed for urea synthesis. Other physiological adaptations associated with survival in FW include giving birth to live young, the capacity of sperm to be activated in freshwater and modifications of the electrosensory system to function in a low conductivity environment. The need for many anatomical, metabolic and physiological modifications for FW existence may constrain the rapidity and hence the frequency of FW colonization, compared to the situation in the more advanced osmoregulating teleosts. Once optimally adapted to FW, recolonization of sea water by elasmobranchs is problematic due to the loss of urea synthetic capacity and renal structures for urea retention.     

The neural control of feeding in elasmobranchs: A review and working model

A working model of the neural control of feeding in elasmobranchs is presented and summarized in graphic form. The model is based on a review of studies in sharks and batoids augmented by suggestions and comparisons from research in mammals and teleosts. The focal point of the model is a proposed Hypothalamic Feeding Area (HFA) that encompasses the medial periventricular zone in the inferior lobe and a small area immediately dorsal to it. Electrical stimulation in the HFA has evoked feeding in nurse sharks and neuropeptides and neurotransmitters known to influence feeding in mammals and teleosts have been localized immunocytochemically in the region in several elasmobranchs. The HFA of elasmobranchs appears to be analogous to and possibly homologous with ??hypothalamic feeding centers?? in bony fishes and tetrapods. Such ??centers?? are thought to integrate external and internal stimuli and control feeding in relation to available energy stores. The HFA??s strong olfactory connections in elasmobranchs are consistent with smell-induced feeding activities. In elasmobranchs, the HFA has reciprocal connections with the central pallium of the telencephalon, a region that processes visual, acoustic, mechanoreceptive and electroreceptive lateral line and possibly somatosensory information. These pathways may provide multisensory control in feeding. HFA connections with the cerebellum, brainstem and spinal cord most likely mediate hypothalamic co-ordination of the sensorimotor components of elasmobranch feeding. The review and model help to identify areas for suggested research.     

The behavioural role of pit organs in the epaulette shark

Epaulette sharks Hemiscyllium ocellatum in three treatments, pit organs (free neuromasts) ablated, sham-operated and normal ( n  = 8 for each treatment), showed a significant preference for facing upstream in a flume ( P  < 0·05). There were no significant differences in the mean angles or angular variances among treatments. Individuals with ablated pit organs, however, spent significantly less time moving around than controls ( P  < 0·05), suggesting that pit organs contributed to motivation for activity. Pit organs do not appear to make an important contribution to rheotaxis in H. ocellatum . It is suggested that this may be due to structural differences in the pit organs of H. ocellatum compared with other species.     

Crotaline pit organs analyzed as warm receptors

Afferent impulses from single-fiber preparations of the trigeminal nerve in Agkistrodon blomhoffi brevicauduswere recorded during steady and dynamic temperature stimulation of the sensory membrane in the facial pit. The thermoreceptors of the pit showed high sensitivity to the rate of change in receptor temperature. Changing the heat capacity of the pit membrane (a drop of water in the pit in the case of the laser and halogen lamp, and a drop of water covered by a plastic film in the case of flowing water) changed the pattern of response. When the heat capacity of the pit membrane is increased, responses approach those obtained in other warm receptors. The spatial gradient theory of Williams, whereby a reversal of heat energy flow is supposed to produce a reverse of response, was shown to be inapplicable to the pit receptors. Reversal of heat energy flow in the pits produced neither off-silence nor depression of response, and therefore direction of heat flow is not an important component of the stimulus for these receptors. This research was made possible by aid from The Netherlands Organization for Advancement of Pure Research (ZWO).     

Python pit organs analyzed as warm receptors

The infrared receptor neurons of Python reticulatuspit organs were all found to have bimodal sensitivity, responding to both infrared and touch stimuli with fairly rapid adaptation. The majority (22 of 29 neurons) had no background discharges at any temperature between 20 and 33°C. The receptive areas were 150–250 µm in diameter and identical for both modalities. There was only one receptive area for each neuron. These facts suggest the possibility that some kinds of temperature sensitive neurons can also function as touch neurons and vice versa, not only in this species, but also in other animals.     

The paraventricular and posterior recess organs of elasmobranchs: A system of cerebrospinal fluid-contacting neurons containing immunoreactive serotonin and somatostatin

Summary The paraventricular organ (PVO) and the posterior recess organ (PRO) of two elasmobranch species, the spiny dogfish,Squalus acanthias, and the skate,Raja radiata, were investigated by use of scanning and transmission electron microscopy and immunocytochemistry employing a series of primary antisera. The PVO and PRO contained four types of cerebrospinal fluid (CSF)-contacting neurons. One type was free of secretory granules and projected a dendrite-like process into the ventricle. The other three types were distinguished according to the size of their secretory granules. The ventricular extensions of these cells were filled with secretory granules. By means of immunocytochemistry three types of CSF-contacting neurons were observed in the PVO and PRO. Type I contained only serotonin; type 2 displayed only somatostatin; type 3 was endowed with both serotonin and somatostatin. Type I dominated in the PRO, whereas type 3 was the most frequent in the PVO. The latter cells appear to be the site of origin of a loose tract formed by serotonin- and somatostatinimmunoreactive fibers projecting from the PVO into the neuropil of the PRO. Compact bundles formed exclusively by serotonin fibers were also shown to extend between the PVO and PRO. The basal processes of the CSF-contacting neurons of the PRO penetrated into the underlying neuropil. This neuropil is rich in synapses and can be regarded as an integrative area to which the basal processes of the local CSF-contacting neurons, serotonin and somatostatin fibers from the PVO, and fibers containing immunoreactive thyrotropin-releasing hormone of unknown origin, support a conspicuous input. The present findings indicate that the PVO and PRO of elasmobranchs are functionally integrated structures.Dedicated to Professor Erik Dahl on the occasion of his 75th birthday.     

The fossil record of extant elasmobranchs

Sharks and their relatives (Elasmobranchii) are highly threatened with extinction due to various anthropogenic pressures. The abundant fossil record of fossil taxa has allowed the tracing of the evolutionary history of modern elasmobranchs to at least 250 MYA; nonetheless, exactly how far back the fossil record of living taxa goes has never been collectively surveyed. In this study, the authors assess the representation and extent of the fossil record of elasmobranchs currently living in our oceans by collecting their oldest records and quantifying first appearance dates at different taxonomic levels (i.e., orders, families, genera and species), ecological traits (e.g., body size, habitat and feeding mechanism) and extinction risks (i.e., threatened, not threatened and data deficient). The results of this study confirm the robust representation of higher taxonomic ranks, with all orders, most of the families and over half of the extant genera having a fossil record. Further, they reveal that 10% of the current global species diversity is represented in the geological past. Sharks are better represented and extend deeper in time than rays and skates. While the fossil record of extant genera (e.g., the six gill sharks, Hexanchus) goes as far back as c. 190 MYA, the fossil record of extant species (e.g., the sand shark, Carcharias taurus Rafinesque 1810) extends c. 66 MYA. Although no significant differences were found in the extent of the fossil record between ecological traits, it was found that the currently threatened species have a significantly older fossil record than the not threatened species. This study demonstrate that the fossil record of extant elasmobranchs extends deep into the geologic time, especially in the case of threatened sharks. As such, the elasmobranch geological history has great potential to advance the understanding of how species currently facing extinction have responded to different stressors in the past, thereby providing a deep-time perspective to conservation.     

Categorising use patterns of non-marine environments by elasmobranchs and a review of their extinction risk

Reviews in Fish Biology and Fisheries - As the state of non-marine aquatic environments (freshwater and estuarine environments with salinities?≤?30&nbsp;ppt) continues to...     

The dorso-lateral pit organs of the Port Jackson shark contribute sensory information for rheotaxis

Resting Port Jackson sharks Heterodontus portusjacksoni with dorso-lateral pit organs ablated oriented with a mean angle of 263° to the current direction in a flume. This was significantly different ( P <0·01) to controls (normal and sham operated) who had a pooled mean angle of 44° to the current. Thus the dorso-lateral pit organs of H. portusjacksoni , like the free neuromasts of some teleosts, provide sensory information for rheotaxis.     

Sense organs in Pycnogonida: A review

The Pycnogonida or sea spiders are exclusively marine invertebrates, numbering about 1,300 described species worldwide. Given their remarkable position in phylogeny as basal chelicerates or even basal euarthropods, the structure of their sense organs can reveal important characters, which—in a comparative framework—provide arguments to phylogenetic discussions and help to develop scenarios of evolutionary transformations. This review summarizes current knowledge and presents new original data on the sense organs in pycnogonids, that is, the eyes, the lateral sense organs and the ciliary or sensillar sense organs. Except for the eyes, there are not many detailed studies available. The ultrastructure of the R‐cells of the four eyes located on the ocular tubercle is described as “pseudoinverted”. The eyes are innervated to two visual neuropils located in the protocerebrum. The features of the lateral sense organ, also located on the ocular tubercle, are hitherto not conclusively resolved, a chemo‐ or thermoreceptive function is suggested. Finally, an overview of the various ciliary or sensillar sense organs distributed all over the body is given and the fine structure of branched setae is shown for the first time. The morphology of the sense organs of pycnogonids is compared with that of other arthropod taxa and assessed against the background of current theories of arthropod evolution.     

Preface: feeding ecology of elasmobranchs

Elasmobranchs are apical predators in most marine communities where they occur, often playing a substantial role in the food web dynamics of those communities. However, despite their high trophic status they are often poorly studied compared to most commercially important teleosts. Furthermore, despite efforts towards ecosystem-based management, elasmobranchs are still often lumped into generic categories referred to as ??shark?? or ??skate?? unclassified, with limited effort to identify individual species. The role of elasmobranchs in ecosystems has never been more important to our understanding of marine ecology due to high levels of exploitation of many species. Similar to other high trophic level predators, many elasmobranchs have life-history characteristics that make them vulnerable to over-exploitation. Elasmobranch populations are now heavily targeted in many fisheries throughout the world. Increasing exploitation of this group is especially alarming because their feeding ecology is poorly studied and by extension their influence in shaping ecosystems. Given recent increased attention on elasmobranchs in the scientific literature, management and conservation circles, and the general news media, researchers over the past decade have begun to more closely examine the ecological role of this important taxon of fishes. Due to this increasing awareness, and the development of new and innovative methods and analytical techniques, it prompted us to organize an international symposium on the ??Feeding Ecology of Elasmobranchs??. The symposium was held on 10 July 2010, in conjunction with the 27^th annual meeting of the American Elasmobranch Society meetings in Providence, Rhode Island.     

A review of capture and post‐release mortality of elasmobranchs

There is a need to better understand the survivorship of discarded fishes, both for commercial stocks and species of conservation concern. Within European waters, the landing obligations that are currently being phased in as part of the European Union's reformed common fisheries policy means that an increasing number of fish stocks, with certain exceptions, should not be discarded unless it can be demonstrated that there is a high probability of survival. This study reviews the various approaches that have been used to examine the discard survival of elasmobranchs, both in terms of at‐vessel mortality (AVM) and post‐release mortality (PRM), with relevant findings summarized for both the main types of fishing gear used and by taxonomic group. Discard survival varies with a range of biological attributes (species, size, sex and mode of gill ventilation) as well as the range of factors associated with capture (e.g. gear type, soak time, catch mass and composition, handling practices and the degree of exposure to air and any associated change in ambient temperature). In general, demersal species with buccal‐pump ventilation have a higher survival than obligate ram ventilators. Several studies have indicated that females may have a higher survival than males. Certain taxa (including hammerhead sharks Sphyrna spp. and thresher sharks Alopias spp.) may be particularly prone to higher rates of mortality when caught.     

The postorbital palatoquadrate articulation in elasmobranchs

Although modern hexanchiforms are the only extant elasmobranchs with a postorbital articulation, according to most morphological and molecular cladistic analyses they are not basal, suggesting that Huxley ( 1876 Proc Zool Soc 1876;24–59) correctly identified this articulation as “an altogether secondary connection.” A postorbital articulation is present in many Paleozoic sharks, but differs from that found in hexanchiforms in its morphology, topographic position on the braincase, and inferred ontogenetic origins. Furthermore, a postorbital articulation is absent in hybodonts (the putative extinct sister group to neoselachians). It is proposed that the term amphistylic should be restricted to the modern hexanchiform condition, where the articular facet is located on the primary postorbital process. An identical articulation probably existed in some extinct galeomorphs (e.g., ?Synechodus dubrisiensis, ?Paraorthacodus), but is not widespread within elasmobranchs generally. The term archaeostylic (“ancient pillar”) is proposed here for the suspensorial arrangement in Paleozic sharks with a postorbital articulation on the ventrolateral part of the lateral commissure. Such an articulation is not known in other gnathostomes and may represent a basal chondrichthyan synapomophy (especially if ?Pucapampella is a stem chondrichthyan), suggesting that the autodiastylic pattern is not primitive for chondrichthyans and that holocephalans have secondarily lost a postorbital articulation. The amphistylic condition may have arisen from the archaeostylic, or it could have been acquired independently within neoselachians, but in either case it is most parsimoniously viewed as apomorphic. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.