African Butterfly Fish Research Articles

Expression of acetylcholine, its contribution to regulation of immune function and O2 sensing and phylogenetic interpretations of the African butterfly fish Pantodon buchholzi (Osteoglossiformes, Pantodontidae)

Acetylcholine (Ach) is the main neurotransmitter in the neuronal cholinergic system and also works as a signaling molecule in non-neuronal cells and tissues. The diversity of signaling pathways mediated by Ach provides a basis for understanding the biology of the cholinergic epithelial cells and immune cells in the gill of the species studied.NECs in the gill were not found surprisingly, but specialized cells showing the morphological, histochemical and ultrastructural characteristics of eosinophils were located in the gill filaments and respiratory lamellae.Much remains unknown about the interaction between the nerves and eosinophils that modulate both the release of acetylcholine and its nicotinic and muscarinic receptors including the role of acetylcholine in the mechanisms of O2 chemosensing. In this study we report for the first time the expression of Ach in the pavement cells of the gill lamellae in fish, the mast cells associated with eosinophils and nerve interaction for both immune cell types, in the gill of the extant butterfly fish Pantodon buchholzi. Multiple roles have been hypothesized for Ach and alpha nAChR in the gills. Among these there are the possible involvement of the pavement cells of the gill lamellae as O2 chemosensitive cells, the interaction of Ach positive mast cells with eosinophils and interaction of eosinophils with nerve terminals. This could be related to the use of the vesicular acetylcholine transporter (VAChT) and the alpha 2 subunit of the acetylcholine nicotinic receptor (alpha 2 nAChR). These data demonstrate the presence of Ach multiple sites of neuronal and non-neuronal release and reception within the gill and its ancestral signaling that arose during the evolutionary history of this conservative fish species.

Spermatogenesis in the inseminating African butterflyfish Pantodon buchholzi (Teleostei: Osteoglossiformes: Pantodontidae) with the revision of residual bodies formation.

The aim of this study was to analyse spermatogenesis in the African butterflyfish, Pantodon buchholzi, using transmission electron microscopy and scanning electron microscopy. P. buchholzi is the most basal teleost that exhibits insemination and produces a highly complex introsperm with the most elongate midpiece known in teleost fishes. Their early stages (spermatogonia and spermatocytes) do not differ greatly from those of other fishes, with the exception of Golgi apparatus degradation appearing as spindle-shaped bodies (SSBs). In round, early spermatids, the development of the flagellum begins after the migration of the centriolar complex towards the nucleus. Later, the elongation of the midpiece coincides with the displacement of the mitochondria and their fusion to produce nine mitochondrial derivatives (MDs). In these spermatids, the nucleus is situated laterally to the midpiece, with condensing chromatin in the centre of the nucleus. Within the midpiece, the flagellum is located within a cytoplasmic canal and is surrounded by a cytoplasmic sleeve containing fibres, MDs and a great amount of cytoplasm located on one side. During the next phase, nuclear rotation, the highly condensed chromatin is displaced to a position above the centriolar apparatus, whereas chromatin-free nucleoplasm is transferred to the cytoplasm. Later, this nucleoplasm, still surrounded by the nuclear membrane, is eliminated into the cyst lumen as the nucleoplasmic packet. Within the highly elongate spermatids, other excess organelles (SSBs, endoplasmic reticulum and mitochondria) are eliminated as residual bodies (RBs). Fully developed spermatozoa, which contain conical-shaped nuclei, eventually coalesce to form unencapsulated sperm packets (spermatozeugmata) that are surrounded by RBs at the level of the extremely elongate midpieces. Later, RBs are removed at the periphery of the cyst by means of phagocytosis by Sertoli cells.

A review of the systematic biology of fossil and living bony-tongue fishes, Osteoglossomorpha (Actinopterygii: Teleostei)

ABSTRACT The bony-tongue fishes, Osteoglossomorpha, have been the focus of a great deal of morphological, systematic, and evolutionary study, due in part to their basal position among extant teleostean fishes. This group includes the mooneyes (Hiodontidae), knifefishes (Notopteridae), the abu (Gymnarchidae), elephantfishes (Mormyridae), arawanas and pirarucu (Osteoglossidae), and the African butterfly fish (Pantodontidae). This morphologically heterogeneous group also has a long and diverse fossil record, including taxa from all continents and both freshwater and marine deposits. The phylogenetic relationships among most extant osteoglossomorph families are widely agreed upon. However, there is still much to discover about the systematic biology of these fishes, particularly with regard to the phylogenetic affinities of several fossil taxa, within Mormyridae, and the position of Pantodon. In this paper we review the state of knowledge for osteoglossomorph fishes. We first provide an overview of the diversity of Osteoglossomorpha, and then discuss studies of the phylogeny of Osteoglossomorpha from both morphological and molecular perspectives, as well as biogeographic analyses of the group. Finally, we offer our perspectives on future needs for research on the systematic biology of Osteoglossomorpha.

Karyotype and Mapping of Repetitive DNAs in the African Butterfly Fish Pantodon buchholzi, the Sole Species of the Family Pantodontidae

The monophyletic order Osteoglossiformes represents one of the most ancestral groups of teleosts and has at least 1 representative in all continents of the southern hemisphere, with the exception of Antarctica. However, despite its phylogenetic and biogeographical importance, cytogenetic data in Osteoglossiformes are scarce. Here, karyotype and chromosomal characteristics of the lower Niger River population of the African butterfly fish Pantodon buchholzi, the sole species of the family Pantodontidae (Osteoglossiformes), were examined using conventional and molecular cytogenetic approaches. All specimens examined had 2n = 46 chromosomes, with a karyotype composed of 5 pairs of metacentric, 5 pairs of submetacentric, and 13 pairs of acrocentric chromosomes in both sexes. No morphologically differentiated sex chromosomes were identified. C-bands were located in the centromeric/pericentromeric region of all chromosomes and were associated with the single AgNOR site. FISH with ribosomal DNA probes revealed that both 5S and 18S rDNA were present in only 1 pair of chromosomes each, but did not colocalize. CMA₃⁺ bands were observed near the telomeres in several chromosome pairs and also at the 18S rDNA sites. The mapping of di- and trinucleotide repeat motifs, Rex6 transposable element, and U2 snRNA showed a scattered distribution over most of the chromosomes, but for some microsatellites and the U2 snRNA also a preferential accumulation at telomeric regions. This study presents the first detailed cytogenetic analysis in the African butterfly fish by both conventional and molecular cytogenetic protocols. This is the first of a series of further cytogenetic and cytogenomic studies on osteoglossiforms, aiming to comprehensively examine the chromosomal evolution in this phylogenetically important fish order.

The Asian arowana (Scleropages formosus) genome provides new insights into the evolution of an early lineage of teleosts.

The Asian arowana (Scleropages formosus), one of the world’s most expensive cultivated ornamental fishes, is an endangered species. It represents an ancient lineage of teleosts: the Osteoglossomorpha. Here, we provide a high-quality chromosome-level reference genome of a female golden-variety arowana using a combination of deep shotgun sequencing and high-resolution linkage mapping. In addition, we have also generated two draft genome assemblies for the red and green varieties. Phylogenomic analysis supports a sister group relationship between Osteoglossomorpha (bonytongues) and Elopomorpha (eels and relatives), with the two clades together forming a sister group of Clupeocephala which includes all the remaining teleosts. The arowana genome retains the full complement of eight Hox clusters unlike the African butterfly fish (Pantodon buchholzi), another bonytongue fish, which possess only five Hox clusters. Differential gene expression among three varieties provides insights into the genetic basis of colour variation. A potential heterogametic sex chromosome is identified in the female arowana karyotype, suggesting that the sex is determined by a ZW/ZZ sex chromosomal system. The high-quality reference genome of the golden arowana and the draft assemblies of the red and green varieties are valuable resources for understanding the biology, adaptation and behaviour of Asian arowanas.

Enigmatic orthology relationships between Hox clusters of the African butterfly fish and other teleosts following ancient whole-genome duplication.

Numerous ancient whole-genome duplications (WGD) have occurred during eukaryote evolution. In vertebrates, duplicated developmental genes and their functional divergence have had important consequences for morphological evolution. Although two vertebrate WGD events (1R/2R) occurred over 525 Ma, we have focused on the more recent 3R or TGD (teleost genome duplication) event which occurred approximately 350 Ma in a common ancestor of over 26,000 species of teleost fishes. Through a combination of whole genome and bacterial artificial chromosome clone sequencing we characterized all Hox gene clusters of Pantodon buchholzi, a member of the early branching teleost subdivision Osteoglossomorpha. We find 45 Hox genes organized in only five clusters indicating that Pantodon has suffered more Hox cluster loss than other known species. Despite strong evidence for homology of the five Pantodon clusters to the four canonical pre-TGD vertebrate clusters (one HoxA, two HoxB, one HoxC, and one HoxD), we were unable to confidently resolve 1:1 orthology relationships between four of the Pantodon clusters and the eight post-TGD clusters of other teleosts. Phylogenetic analysis revealed that many Pantodon genes segregate outside the conventional “a” and “b” post-TGD orthology groups, that extensive topological incongruence exists between genes physically linked on a single cluster, and that signal divergence causes ambivalence in assigning 1:1 orthology in concatenated Hox cluster analyses. Out of several possible explanations for this phenomenon we favor a model which keeps with the prevailing view of a single TGD prior to teleost radiation, but which also considers the timing of diploidization after duplication, relative to speciation events. We suggest that although the duplicated hoxa clusters diploidized prior to divergence of osteoglossomorphs, the duplicated hoxb, hoxc, and hoxd clusters concluded diploidization independently in osteoglossomorphs and other teleosts. We use the term “tetralogy” to describe the homology relationship which exists between duplicated sequences which originate through a shared WGD, but which diploidize into distinct paralogs from a common allelic pool independently in two lineages following speciation.

Nucleus Rostrolateralis: An Expansion of the Epithalamus in Some Actinopterygii

The diencephalic nucleus rostrolateralis (RL) in the African butterfly fish (Pantodon buchholzi) is a brain nucleus identified in fewer than a dozen of the ∼25,000 species of actinopterygian fishes. Located in the rostrolateral diencephalon, this nucleus in Pantodon receives direct and indirect visual input from the superior visual field. Its lack of precedent or consistent phylogenetic expression creates a difficulty in interpreting the functional role of this nucleus within the visual system. By tracing experiments, RL was found to be afferent to nucleus interpeduncularis (IP) and the target of cells from the subpallium of the telencephalon. RL is a component of a descending telencephalic pathway involved in at least one behavior at the intersection of limbic and somatic activities--feeding. The parallelism between the ventral telencephalon--RL--IP and the limbic/striatal--habenula--IP pathway (the dorsal diencephalic conduction system, DDCS) suggests that RL is a component within the DDCS. Moreover, the hodological connections of RL suggest that RL is likely a hypertrophy of the lateral habenula.

A Generalized Neural Circuit that Specifically Enhances the Probability of Predation Success in the African butterfly fish

Event Abstract Back to Event A Generalized Neural Circuit that Specifically Enhances the Probability of Predation Success in the African butterfly fish William Saidel1, 2* 1 Rutgers, the State University of New Jersey, Biology, United States 2 Rutgers, the State University of New Jersey, Center for Computational and Integrative Biology, United States The diencephalic Nucleus Rostrolateralis (RL) in the African butterfly fish (Pantodon buchholzi) has few equals. It is a brain nucleus that has been identified in less than two dozen of the ~25000 species of fishes. Located in the rostrolateral diencephalon, this nucleus receives direct and indirect visual input from the superior visual field. Its lack of precedent or consistent phylogenetic expression creates a difficulty in interpreting the functional role of this nucleus in the visual pathway. By tracing experiments, RL was found to be afferent to Nucleus Interpeduncularis (IP) and the target of cells in the ventral pallium of the telencephalon. RL appears to be a component of a descending limbic pathway involved in at least one behavior associated at the intersection of limbic and somatic activities - predatory feeding. The parallelism between the ventral pallium - RL - IP and telencephalon - habenula - IP pathway (the Dorsal Diencephalic Conducting System) suggests that RL is a component of the DDCP and is potentially involved with increasing predation success by enhancing motor actions. Acknowledgements This work was supported in part by a grant from the Charles and Johanna Busch Memorial Fund at Rutgers, The State University of New Jersey. I thank Dr. Ann Butler of the Krasnow Institute, George Mason University, Fairfax, VA, for the years of insightful discussions about this system. Keywords: African butterfly fish, DiI tract tracing, Dorsal Diencephalic Conducting System, Nucleus Interpeduncularis, Nucleus Rostrolateralis Conference: Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012. Presentation Type: Poster (but consider for Participant Symposium) Topic: Sensorimotor Integration Citation: Saidel W (2012). A Generalized Neural Circuit that Specifically Enhances the Probability of Predation Success in the African butterfly fish. Conference Abstract: Tenth International Congress of Neuroethology. doi: 10.3389/conf.fnbeh.2012.27.00182 Copyright: The abstracts in this collection have not been subject to any Frontiers peer review or checks, and are not endorsed by Frontiers. They are made available through the Frontiers publishing platform as a service to conference organizers and presenters. The copyright in the individual abstracts is owned by the author of each abstract or his/her employer unless otherwise stated. Each abstract, as well as the collection of abstracts, are published under a Creative Commons CC-BY 4.0 (attribution) licence (https://creativecommons.org/licenses/by/4.0/) and may thus be reproduced, translated, adapted and be the subject of derivative works provided the authors and Frontiers are attributed. For Frontiers’ terms and conditions please see https://www.frontiersin.org/legal/terms-and-conditions. Received: 28 Apr 2012; Published Online: 07 Jul 2012. * Correspondence: Prof. William Saidel, Rutgers, the State University of New Jersey, Biology, Camden, NJ, 08102, United States, saidel@camden.rutgers.edu Login Required This action requires you to be registered with Frontiers and logged in. To register or login click here. Abstract Info Abstract The Authors in Frontiers William Saidel Google William Saidel Google Scholar William Saidel PubMed William Saidel Related Article in Frontiers Google Scholar PubMed Abstract Close Back to top Javascript is disabled. Please enable Javascript in your browser settings in order to see all the content on this page.

Extraordinarily Quick Visual Startle Reflexes of Skipper Butterflies (Lepidoptera: Hesperiidae) are Among the Fastest Recorded in the Animal Kingdom

The abilities of animals in movement and coor dination frequently surpass our own abilities and fascinate us. New record speeds found among ani mals, when recorded by the scientific literature, tend to be widely publicized. Such is the case of the trap-jaw ant, Odontomachus bauri Emery, whose mandibles close in 0.13 s at a rate of 35.5 meters per second (ms'1) during a predatory strike, the fastest movement recorded among all animals (Patek et al. 2006). The fastest tactile reflex time belongs to the star-nosed mole, Condylura cristata L., which uses 22 nasal appendages to navigate through soil and can react in just 120 ms, when one of these appendages comes in contact with food (Catania & Remple 2004). Here, I would like to report the startle reflex time in skipper butter flies, which is among the fastest recorded for the animal kingdom and which is at least twice as fast as startle eye-blink reflex of humans. Startle reflexes have evolved as fast defensive (usually escape) responses in animals, engaging subcortical reflex mechanism that bypasses cere bral processing and voluntary movement. Be cause circuits involved are shorter, the latencies of the startle reactions are much shorter than those of voluntary reactions. In terms of elec tromyographic responses recorded in vitro, acous tic startle reflexes tend to be very short. In rats, for example, electromyographic responses can be as fast as 5-10 ms, and in humans as fast as 14 ms (Yeomans & Frankland 1995). The actual behavioral responses recorded in vivo tend to be longer. For example, in the African butterfly fish, Pantodon buchholzi Peters, the fastest response time to an acoustic startle stim ulus recorded on an electromyogram is 5 ms. The fish's fins initiate a motion 10 ms later, hence with the possible reflex time (ballistic jump) ca. 15 ms (Starosciak 2008). The eye-blink reflex of humans elicited by an air puff is 30-50 ms (e.g., Halmagyi & Gresty 1983). Compared to that, voluntary reaction time to a visual 'go' signal in humans is around 150 ms (Brown et al. 1991), and it takes an average of 700 ms for a human driver to move the foot from the accelerator to the brake peddle after seeing a red light (Green 2000). Just like butterfly fish, skipper butterflies rely on ballistic movements to evade preda tors, but they propel themselves through the air, not the water. They are, in fact, named for their quick, darting flight habits. They differ in several morphological characters from other butterflies (e.g., Ackery et al. 1999), most notably in having stockier bodies with stronger wing muscles. While photographing butterflies with a digital camera for several years, I have become convinced that skippers possess an extraordinary reflex time when startled by a photographic flash. Their star tle reflex is faster than I have observed in any other butterfly. Even though other butterflies and other insects are frequently startled by a photographic flash and flee after their picture is taken, their motor re sponse is normally slower than the shutter speed of the camera. Thus, even if they are startled by the flash, they appear still in photographs. Skippers, however, react so quickly to the flash, that their re action is frequently captured by the camera. In the specific camera settings I used in the photographs in Fig. 1, the shutter was open for 1/ 60 sec =17 ms. The flash, synchronized with the shutter, occurred during this time. During this ex posure time, skippers startled by the flash fre quently jumped into the air, and their image was captured in flight near the substrate. They tended to return to their original position imme diately, so that they appeared still to the human eye, and their movement was captured only by the camera. In pairs of photographs (Fig. 1: A1-A2, B1-B2, and C1-C2), one individual was recorded in the act of jumping above the same plant when star tled repeatedly. These shots were captured by fir ing the camera with intervals of ca. 20 s. It was noted by previous studies that habituation (de cline and disappearance of response during repet itive stimuli) occur with other types of startle re flexes (Yeomans & Frankland 1995). I observed the same with the jumping skippers: if they did not escape after the first shot, their jumping re sponse ceased after 2-3 repeated firings of the flash (Fig. 1: C3, D2). These photographs illustrate the unique quickness of skipper reflexes among all the other insects that I have photographed. They document what might be one of the fastest reflex times (<17 ms) so far recorded for the animal kingdom.

Spatial distribution of a fusiform cell in the optic tectum of Pantodon buchholzi, the African butterfly fish (Teleostei, Osteoglossomorpha)

Pantodon buchholzi, the African butterfly fish, inhabits an ecological niche just below the water surface. At that position, each eye necessarily views into the air through the surface of the water and into the water. Since Pantodon is an obligatory surface feeder, the ventral retina viewing the aerial environment provides all visual information for prey acquisition. The visual pathway of this fish reflects the divided visual field with structural differences in the retina and brain corresponding to the different views. In this study, we describe a specific type of neuron in the tectum that, due to its intrinsic structure, likely integrates visual and mechanoreceptor inputs. Because of its spatial distribution, this type of neuron is a candidate as a basic element in a network involved with prey acquisition.

Fast and Singular Muscle Responses Initiate the Startle Response of Pantodon buchholzi (Osteoglossomorpha)

The startle response of Pantodon buchholzi, the African butterfly fish, is a complete or incomplete ballistic jump resulting from abduction of the pectoral fins. This study analyzed the neuromuscular basis for such a jump by recording in vivo electromyograms (emgs) from the muscles of abduction, the muscularis abductor superficialis (MAS) and the muscularis abductor profundus (MAP). The motor neurons innervating the MAS muscle were localized by retrograde transport of biocytin. The latency between stimulus and the evoked emg in the MAS was less than 5 ms; the latency of the MAP was about 6.5 ms. A single emg was recorded per jump. High speed video demonstrated that onset of a startle movement began within 10 ms of the onset of fin abduction. The emg associated with this movement is short (<2 ms) and followed by a variably-shaped, slower and smaller potential of 10–30 ms duration. The brief period between stimulus and startle response of Pantodon suggests a Mauthner neuron-related response, only with the behavior occurring in the vertical plane. The MAS may act only in a startle response, whereas the MAP might have a role in other behaviors. Elicited jumping habituates after a single trial. Electrophysiological evidence is presented indicating that the innervating motor neurons are suppressed for seconds following a stimulus. The neurons innervating the MAS are located at the medullary-spinal cord junction and possess an average radius of ∼17.9 µm. These fish have been historically described as ‘fresh water’ flying fish. As a single emg occurs per startle response, repetitive pectoral activity generating flying cannot be supported. Pantodon ‘flight’ is ballistic.

Characterization of the Aerial Escape Response of the African Butterfly Fish, Pantodon buchholzi Peters

We studied the startle response of the African butterfly fish, Pantodon buchholzi (Osteoglossomorpha, Osteoglossoidea). It is an upward movement, mediated by abduction of the pectoral fins, and is elicited by mechanical and visual stimuli. Because this fish inhabits the first few centimeters beneath the water surface, its startle response results in an aerial excursion that may be described as ballistic-like, following a motion as defined by linear acceleration. We show that the aerial excursion is well-modeled by a parabola. On average, a fish jumps no more than twice its height and travels horizontally about five times its standard length. The fish may exhibit variable in-flight trunk and fin movements, but neither increases the travel distance in air following the initial in-water propulsive event. Similar vertical jumps also occur entirely within the water column suggesting that this motor behavior of Pantodon is a general escape behavior analogous to a Mauthner neuron-induced escape response. The variability in its posture in air and its direction of motion after reentering the water enhances this act of vertical flight as a step in this fish's escape behavior. The aerial aspect of its escape behavior is only a consequence of its position in the water column.

Simultaneous analysis of five molecular markers provides a well-supported phylogenetic hypothesis for the living bony-tongue fishes (Osteoglossomorpha: Teleostei)

Fishes of the Superorder Osteoglossomorpha (the “bonytongues”) constitute a morphologically heterogeneous group of basal teleosts, including highly derived subgroups such as African electric fishes, the African butterfly fish, and Old World knifefishes. Lack of consensus among hypotheses of osteoglossomorph relationships advanced during the past 30 years may be due in part to the difficulty of identifying shared derived characters among the morphologically differentiated extant families of this group. In this study, we present a novel phylogenetic hypothesis for this group, based on the analysis of more than 4000 characters from five molecular markers (the mitochondrial cytochrome b, 12S and 16S rRNA genes, and the nuclear genes RAG2 and MLL). Our taxonomic sampling includes one representative of each extant non-mormyrid osteoglossomorph genus, one representative for the monophyletic family Mormyridae, and four outgroup taxa within the basal Teleostei. Maximum parsimony analysis of combined and equally weighted characters from the five molecular markers and Bayesian analysis provide a single, well-supported, hypothesis of osteoglossomorph interrelationships and show the group to be monophyletic. The tree topology is the following: ( Hiodon alosoides, ( Pantodon buchholzi, ((( Osteoglossum bicirrhosum, Scleropages sp.), ( Arapaima gigas, Heterotis niloticus)), (( Gymnarchus niloticus, Ivindomyrus opdenboschi), (( Notopterus notopterus, Chitala ornata), ( Xenomystus nigri, Papyrocranus afer)))))). We compare our results with previously published phylogenetic hypotheses based on morpho-anatomical data. Additionally, we explore the consequences of the long terminal branch length for the taxon Pantodon buchholzi in our phylogenetic reconstruction and we use the obtained phylogenetic tree to reconstruct the evolutionary history of electroreception in the Notopteroidei.

Determination of source distance in the surface-feeding fish Pantodon buchholzi Pantodontidae

The African butterfly fish Pantodon buchholzi localizes its prey by means of surface waves of the water. Pantodon also responds and orientates well to artificial, short lasting prey-like signals (clicks), produced by a single air-puff or by dipping a small rod once into the water. When stimulated with clicks, which contain many frequencies, Pantodon determines the source distance (test range 5–20 cm) very precisely, regardless of stimulus amplitude, amplitude modulation and frequency band width. However, when the signal is a sine wave at a single frequency (sf) or with upward frequency modulation (ufm), the distance determination is generally impaired, i.e. the distance covered by the fish is too small to reach the wave source. However, the fish can also be tricked into moving too far by presenting it with a sine wave signal which, at a source distance of only 7 cm has a frequency modulation equivalent to a click at 15 cm. In contrast to distance determination, the ability to estimate the target angle is independent of the kind of wave signal presented. The results are discussed with respect to possible mechanisms used for prey localization.