Electroreception in marine fishes: chondrichthyans

Electroreception in marine fishes occurs across a variety of taxa and is best understood in the chondrichthyans (sharks, skates, rays, and chimaeras). Here, we present an up-to-date review of what is known about the biology of passive electroreception and we consider how electroreceptive fishes might respond to electric and magnetic stimuli in a changing marine environment. We briefly describe the history and discovery of electroreception in marine Chondrichthyes, the current understanding of the passive mode, the morphological adaptations of receptors across phylogeny and habitat, the physiological function of the peripheral and central nervous system components, and the behaviours mediated by electroreception. Additionally, whole genome sequencing, genetic screening and molecular studies promise to yield new insights into the evolution, distribution, and function of electroreceptors across different environments. This review complements that of electroreception in freshwater fishes in this special issue, which provides a comprehensive state of knowledge regarding the evolution of electroreception. We conclude that despite our improved understanding of passive electroreception, several outstanding gaps remain which limits our full comprehension of this sensory modality. Of particular concern is how electroreceptive fishes will respond and adapt to a marine environment that is being increasingly altered by anthropogenic electric and magnetic fields.     

Special cutaneous receptor organs of fish. IV. Ampullary organs of the nonelectric catfish, Kryptopterus

Ampullary organs of the transparent catfish, Kryptopterus bicirrhus, are present in large numbers on the head and in a regular pattern of lines on the body and fins. The organs lie in the epidermis, and have a pore that opens to the surface. Flattened cells form a roof and walls. On the floor of the organ there are a “sensory hillock,” composed of spherical receptor cells and columnar supporting cells, and a “secretory hillock” composed of columnar secretory cells. The receptor cells are nonciliated and have only afferent innervation. The organ cavity is filled with jelly. The organs are compared with ampullary organs of the weakly electric fish Eigenmannia, ampullae of Lorenzini of Raja, and small pit organs of Amiurus. Structural characteristics of the ampullary organs of Kryptopterus make them especially suitable for electrophysiological studies.     

Electroreception,electrogenesis and electric signal evolution

Electroreception, the capacity to detect external underwater electric fields with specialised receptors, is a phylogenetically widespread sensory modality in fishes and amphibians. In passive electroreception, a capacity possessed by c. 16% of fish species, an animal uses low-frequency-tuned ampullary electroreceptors to detect microvolt-range bioelectric fields from prey, without the need to generate its own electric field. In active electroreception (electrolocation), which occurs only in the teleost lineages Mormyroidea and Gymnotiformes, an animal senses its surroundings by generating a weak (< 1 V) electric-organ discharge (EOD) and detecting distortions in the EOD-associated field using high-frequency-tuned tuberous electroreceptors. Tuberous electroreceptors also detect the EODs of neighbouring fishes, facilitating electrocommunication. Several other groups of elasmobranchs and teleosts generate weak (< 10 V) or strong (> 50 V) EODs that facilitate communication or predation, but not electrolocation. Approximately 1.5% of fish species possess electric organs. This review has two aims. First, to synthesise our knowledge of the functional biology and phylogenetic distribution of electroreception and electrogenesis in fishes, with a focus on freshwater taxa and with emphasis on the proximate (morphological, physiological and genetic) bases of EOD and electroreceptor diversity. Second, to describe the diversity, biogeography, ecology and electric signal diversity of the mormyroids and gymnotiforms and to explore the ultimate (evolutionary) bases of signal and receptor diversity in their convergent electrogenic–electrosensory systems. Four sets of potential drivers or moderators of signal diversity are discussed. First, selective forces of an abiotic (environmental) nature for optimal electrolocation and communication performance of the EOD. Second, selective forces of a biotic nature targeting the communication function of the EOD, including sexual selection, reproductive interference from syntopic heterospecifics and selection from eavesdropping predators. Third, non-adaptive drift and, finally, phylogenetic inertia, which may arise from stabilising selection for optimal signal-receptor matching.     

Electroreception and magnetoreception in simple and complex organisms

A considerable body of evidence now indicates that electromagnetic and geomagnetic detection systems exist in both simple, unicellular organisms and in more complex species such as avians, bees, and marine animals. A major challenge that faces researchers in this field is the identification of physiological mechanisms through which the detection of weak fields provides significant somatosensory cues for direction finding, foraging, and predation. Many of the anatomical, physiological, and biophysical approaches that are being taken in studies of this nature are described in the series of review articles that appear in this issue of Bioelectromagnetics.     

Electroreception in the Guiana dolphin (Sotalia guianensis)

Passive electroreception is a widespread sense in fishes and amphibians, but in mammals this sensory ability has previously only been shown in monotremes. While the electroreceptors in fish and amphibians evolved from mechanosensory lateral line organs, those of monotremes are based on cutaneous glands innervated by trigeminal nerves. Electroreceptors evolved from other structures or in other taxa were unknown to date. Here we show that the hairless vibrissal crypts on the rostrum of the Guiana dolphin (Sotalia guianensis), structures originally associated with the mammalian whiskers, serve as electroreceptors. Histological investigations revealed that the vibrissal crypts possess a well-innervated ampullary structure reminiscent of ampullary electroreceptors in other species. Psychophysical experiments with a male Guiana dolphin determined a sensory detection threshold for weak electric fields of 4.6 μV cm(-1), which is comparable to the sensitivity of electroreceptors in platypuses. Our results show that electroreceptors can evolve from a mechanosensory organ that nearly all mammals possess and suggest the discovery of this kind of electroreception in more species, especially those with an aquatic or semi-aquatic lifestyle.     

Electroreception in early vertebrates: survey,evidence and new information

Electroreception is widespread in living vertebrates, and is often considered to be a primitive vertebrate character. However, the early evolution of electroreception remains unclear. A variety of structures in early vertebrate fossils have been put forward as potential electroreceptors, but these need to be reassessed in light of the now substantial literature on electroreceptors in living vertebrates. Here we review the evidence for all putative electroreceptors in early vertebrates, and provide new information from CT scans. In the jawless osteostracans, the pore canal system in the dermal skeleton and the lateral and dorsal fields do not resemble electroreceptors in living species. Nevertheless, the presence of a recurrent ramus of the anterior lateral line nerve in osteostracans suggests that electroreceptors were present, by comparison with lampreys. In placoderms, cutaneous sense organs on arthrodire cheek plates are possible electroreceptors. CT data shows that the orientation of these pits is anomalous for electroreceptors, and intimately associated with bone growth. A newly identified type of cheek pit, for which the term ‘Young's apparatus’ is introduced, is known from only two arthrodire specimens. It is closely associated with the underlying jaw joint, but its precise function is unknown. In osteichthyans, the ‘pore group’ clusters of early sarcopterygians may have housed electroreceptors. CT data from Devonian lungfish support this interpretation, showing internal morphology consistent with electroreceptors, and innervation via the rostral tubuli underlying the dermal bone of the snout. The early osteichthyan Ligulalepis has pit structures which may be electroreceptors, and were possibly innervated by lateral line nerves. Specialized electroreceptor systems, including elaborated ‘pore group’ pits in Devonian lungfish and rostral organs in the earliest coelacanths, show that electroreception may have had an important role in niche specialization in early vertebrates. Finally, fossil data does not support the hypothesis that vertebrate hard tissues initially evolved to shield electroreceptors.     

Fixing Content and Function in Neurobiological Systems: The Neuroethology of Electroreception

Are attributions of content and function determinate, or is there no fact of the matter to be fixed? Daniel Dennett has argued in favor of indeterminacy and concludes that, in practice, content and function cannot be fixed. The discovery of an electrical modality in vertebrates offers one concrete instance where attributions of function and content are supported by a strong scientific consensus. A century ago, electroreception was unimagined, whereas today it is widely believed that many species of bony fish, amphibians, sharks, skates, and rays possess this non-human sensory modality. A look at the history of science related to this discovery reveals a highly interdisciplinary endeavor, encompassing ethology, behavioral analysis, neuroscience, and evolutionary biology. While each area provides important evidence, none is sufficient on its own to fix content and function. Instead, I argue that an interdisciplinary, neuroethological approach is required to carry out such determinations. Further, a detailed consideration of biological research suggests that while content and function claims are empirically underdetermined and uncertain, there is insufficient reason to believe in an additional problem of indeterminism. In particular, Dennett's indeterminism arises from a research methodology -- logical adaptationism -- that generates evidence from only one of the areas of neuroethology. However, logical adaptationism does not reflect adaptationism as it is practiced in contemporary biology. I conclude that Dennett is faced with a dilemma: On the one hand, he can hold to logical adaptationism and the indeterminism that results from it, while giving up the relevance of his arguments to biological practice. On the other, he can embrace a more accurate version of adaptationism -- one which plays a role in a larger neuroethological framework -- but from which no strong indeterminacy claims follow.     

"Instantaneous" growth rates of fish scales and their use in studies of fish populations

A technique has been devised for measuring the incorporation of ¹⁴C-glycine into fish scales. This provides an indication of the rate of growth of the scale at the time of sampling. The growth of fish scales is classically considered to be related to the growth of the whole fish' hence the method devised has been used to investigate aspects of fish growth in a number of environmental situations.     

Coding "what" and "when" in the Archer fish retina

Traditionally, the information content of the neural response is quantified using statistics of the responses relative to stimulus onset time with the assumption that the brain uses onset time to infer stimulus identity. However, stimulus onset time must also be estimated by the brain, making the utility of such an approach questionable. How can stimulus onset be estimated from the neural responses with sufficient accuracy to ensure reliable stimulus identification? We address this question using the framework of colour coding by the archer fish retinal ganglion cell. We found that stimulus identity, “what”, can be estimated from the responses of best single cells with an accuracy comparable to that of the animal''s psychophysical estimation. However, to extract this information, an accurate estimation of stimulus onset is essential. We show that stimulus onset time, “when”, can be estimated using a linear-nonlinear readout mechanism that requires the response of a population of 100 cells. Thus, stimulus onset time can be estimated using a relatively simple readout. However, large nerve cell populations are required to achieve sufficient accuracy.

Authors Summary

In our interaction with the environment we are flooded with a stream of numerous objects and events. Our brain needs to understand the nature of these complex and rich stimuli in order to react. Research has shown ways in which a ‘what’ stimulus was presented can be encoded by the neural responses. However, to understand ‘what was the nature of the stimulus’ the brain needs to know ‘when’ the stimulus was presented. Here, we investigated how the onset of visual stimulus can be signalled by the retina to higher brain regions. We used archer fish as a framework to test the notion that the answer to the question of ‘when’ something has been presented lies within the larger cell population, whereas the answer to the question of ‘what’ has been presented may be found at the single-neuron level. The utility of the archer fish as model animal stems from its remarkable ability to shoot down insects settling on the foliage above the water level, and its ability to distinguish between artificial targets. Thus, the archer fish can provide the fish equivalent of a monkey or a human that can report psychophysical decisions.     

Galanin-like immunoreactivity in the brain and pituitary of the "four-eyed" fish, Anableps anableps

The distribution of galanin (GAL)-like immunoreactivity was investigated in the brain and pituitary of the "four-eyed" fish, Anableps anableps. GAL-immunoreactive (GAL-ir) perikarya were located in the area ventralis telencephali pars supracommissuralis, nucleus preopticus periventricularis, nucleus preopticus pars parvocellularis, nucleus preopticus pars magnocellularis, nucleus lateralis tuberis ventralis, nucleus lateralis tuberis lateralis, and nucleus lateralis tuberis posterior. A few scattered, GAL-ir neurons were also observed in or adjacent to the nucleus recessus lateralis, nucleus recessus posterioris and lobus facialis (VII). GAL-ir fiber networks were widespread in the brain, with a comparatively higher density in the ventral telencephalic, preoptic and infundibular regions. The neurohypophysis showed GAL-ir innervation and there were GAL-ir cells in the adenohypophysis. The presence of GAL-ir cells in the hypothalamus and in the pituitary is an important asset for the supposed role of GAL-like peptide in neuroendocrine regulation of brain and pituitary functions.     

Diversity and distribution of fish tapeworms of the "Bothriocephalidea" (Eucestoda)

Recent studies have demonstrated the invalidity of the Pseudophyllidea, a long-term recognised order of tapeworms (Platyhelminthes: Cestoda), typical in possessing two dorsoventrally situated attachment organs called bothria. In fact, cestodes parasitic in tetrapods, especially mammals including man, form a relatively basal group called provisionally the "Diphyllobothriidea", whereas tapeworms occurring in freshwater and marine fish, with a few taxa known from amphibians (frogs and newts), belong to a more derived clade, for which the name "Bothriocephalidea" is tentatively proposed. Revision of the "Bothriocephalidea", based on literary data, study of type- and voucher specimens and extensive newly collected material made it possible to critically review the species composition of the group and to prepare a tentative list of its valid species. Out of 305 nominal taxa, only 125 species are considered to be valid. In addition, the spectrum of definitive hosts and geographical distribution of bothriocephalideans are briefly discussed.     

Adaptive sympatric speciation of polychromatic "roundfin" sailfin silverside fish in Lake Matano (Sulawesi)

The significance of sympatric speciation is one of the most controversial topics in evolutionary biology. Theory suggests that different factors can lead to speciation in full geographical contact, including selection and nonrandom mating. Strict criteria have been established for assessing sympatric speciation, which have been met in only a very few cases. Here, we investigate differentiation among sympatric morphospecies and color morphs of "roundfin" sailfin silversides (Telmatherinidae), small freshwater fish endemic to ancient Lake Matano in Central Sulawesi (Indonesia). Morphospecies are distinct according to body shape (geometric morphometrics), population structure (population-level amplified fragment length polymorphism [AFLP] markers), ecology, and mating behavior (habitat transects, stomach contents). Explorative genome scans based on AFLPs indicate that divergent selection affects only 1.3-4.2% of the analyzed loci, suggesting an early stage of speciation. Transect data demonstrate strong assortative mating and adaptive niche differentiation. However, we find no restrictions in gene flow among the conspicuous male color morphs. In summary, our data are consistent with a sympatric mode of divergence among three morphospecies under conditions effectively ruling out allopatric scenarios. Substantial, but incomplete, reproductive isolation suggests an early stage of speciation, most likely due to ecological selection pressure.     

Carbohydrate structure and serological behaviour of "antifreeze" glycoproteins from an Antarctic fish.

The carbohydrate moiety of the “antifreeze” glycoprotein from $\text{Trematomus borchgrevinki}$ was found to be β-D-galactosyl 1–3 N-acetyl galactosamine by gasliquid chromatography. The glycoprotein inhibited anti-T antibody from human serum and $\text{Arachis hypogoea}$ lectin, but was inactive against $\text{Vicia graminea}$. Native “antifreeze” glycoprotein did not inhibit the agglutinins from $\text{Helix pomatia}$ or $\text{Cepaea hortensis}$, although after Smith degradation showed a strong inhibition towards them. Inhibition of the latter agglutinin demonstrates the carbohydrate-protein linkage to be α-linked. The presence of the Thomsen-Friedenreich antigen (T-antigen) on the “antifreeze” glycoprotein and its relation to tumour cell surfaces is briefly discussed.     

Basal actinopterygian relationships: a mitogenomic perspective on the phylogeny of the "ancient fish"

The basal actinopterygians comprise four major lineages (polypteriforms, acipenseriforms, lepisosteids, and Amia) and have been collectively called "ancient fish." We investigated the phylogeny of this group of fishes in relation to teleosts using mitochondrial genomic (mitogenomic) data, and compared this to the various alternative phylogenetic hypotheses that have been proposed previously. In addition to the previously determined complete mitochondrial DNA (mtDNA) sequences from 14 teleosts and two outgroups, we used newly determined mitogenomic sequences of 12 purposefully chosen species representing all the ancient fish lineages plus related teleosts. This data set comprised concatenated nucleotide sequences from 12 protein-coding genes (excluding the ND6 gene and third codon positions) and 22 transfer RNA (tRNA) genes (stem regions only) and these data were subjected to maximum parsimony, maximum likelihood, and Bayesian analyses. The resultant trees from the three methods were well resolved and largely congruent, with most internal branches being supported by high statistical values. Mitogenomic data strongly supported not only the monophyly of the teleosts (osteoglossomorphs and above), but also a sister-group relationship between the teleosts and a clade comprising the acipenseriforms, lepisosteids, and Amia, with the polypteriforms occupying the most basal position in the actinopterygian phylogeny. Although the tree topology differed from any of the previously proposed hypotheses based on morphology, it exhibited congruence with a recently proposed novel hypothesis based on nuclear markers.     

Hormones and fish hepatocyte metabolism: "the good, the bad and the ugly!"

This short review examines some of my personal experiences with Dr. Peter Hochachka, as a mentor and friend, and how his encouragement led to the research undertaken in my laboratory over the past three decades. Specifically, our work using the fish hepatocyte preparation as a model cell system is reviewed. The hepatocyte is an ideal cellular system that can be used to probe hepatic physiology and biochemistry. The impact of insulin, glucagon and related peptides, and catecholamines is discussed from the perspective of core and diverse functions of these key vertebrate metabolic hormones. Each hormone that operates in fish species was studied in manners similar to that of mammals, but it appears that the role of glucagon-like peptide-1 (GLP-1) in particular differs substantially from that in mammals. The receptors for each of these fish hormones seem structurally and in some cases functionally quite distinct from those in mammals. Few fish hormone receptor sequences are available, but fish genomists are rapidly adding new sequence information to the existing databases, so our view of the evolution of vertebrate hormone receptors will become clearer very quickly.