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First record of a hagfish anchored to a living bottlenose dolphin in the Mediterranean Sea
Abstract
An unusual observation of a hagfish (Myxine glutinosa) anchored to a living bottlenose dolphin (Tursiops truncatus) was documented in an encounter with a group of about 80 dolphins during an ongoing long-term research program on cetaceans in the central Mediterranean Sea, Italy. The body of the hagfish was observed extruding from the blowhole of the bottlenose dolphin showing a stereotypical surfacing–breathing pattern. The observation lasted 2 h; photo-identification, acoustic, and behavioral data were collected. Succorant behaviors (i.e., “standing by”) from conspecifics and overlapping vocalizations during social phases were recorded. The dolphin was encountered again after 1 month in the same area without the hagfish, apparently in healthy conditions.
... To the authors' knowledge, there is no correlation between HFA size and natural diet across different species of hagfishes. Clear differences in natural diets have not been identified between the two species studied, however, there have been more observations on the feeding behaviors in wild M. glutinosa (Auster & Barber, 2006;Cole, 1913;Gustafson, 1935;Leigh, Sparks, & Bemis, 2016;Pace, Mussi, Miragliuolo, Vivaldi, & Ardizzone, 2016;Shelton, 1978;Strahan, 1963) than in wild E. stoutii (Johnson, 1994;Worthington, 1905). Hagfishes generally feed on a variety of vertebrates and invertebrates (Martini, 1998) and use a variety of feeding modes (Glover & Bucking, 2015), which include opportunistic scavenging (e.g., Smith & Baco, 2003), predation (e.g., Zintzen et al., 2011, encounter competition (e.g., Auster & Barber, 2006), and passive transport of dissolved organic matter through their gills and skin (e.g., Glover, Bucking, & Wood, 2011). ...
... The HFAs of both M. glutinosa and E. stoutii are functionally capable of handling the tissues of baleen whale carcasses, as whale falls are a known source of for other species of Eptatretus and Myxine (Smith & Baco, 2003). Incidentally, a specimen of Myxine glutinosa has recently been observed anchoring itself to the blowhole of a live specimen of bottlenose dolphin (Pace et al., 2016). ...
Hagfish use forceful retractions of a dental plate to shear and ingest food. Retractile force is generated by the retractor muscle complex of the posterior hagfish feeding apparatus (HFA). While gross morphological descriptions exist, the organization of muscle and connective tissue fibers that form the soft tissue retractor complex do not. In this study, we used paraffin histology to prepare serial sections of Pacific (Eptatretus stoutii, Lockington, 1879) and Atlantic (Myxine glutinosa, Linnaeus, 1758) hagfishes in order to describe constituent soft tissue anatomy and fiber orientations. We generated 3D reconstructions in which digitized sections were segmented and fitted to volumetric scans of retractor complexes taken prior to microtomy. These models confirmed that the retractor complex is composed of a perpendicularis muscle that fits within the eye of a needle‐shaped clavatus muscle, which anteriorly bears the dental plate tendon, and in turn fits within a sleeve‐like tubulatus muscle. Analysis of fiber orientations within these muscles resulted in novel functional hypotheses: (a) The tubulatus muscle represents a novel tubular bipennate muscle with a considerable physiological cross‐sectional area. Its activation may indirectly create tension in the dental plate tendon: as the tubulatus muscle forcefully extends, it displaces the terminal bulb and the clavatus muscle posteriorly. (b) Within the HFA terminal bulb, the muscle fibers of the clavatus and perpendicularis muscles are mutually perpendicular and may cocontract to form a swelling stopper knot‐like muscular complex that resists being pulled through the tubulatus muscle. (c) While overall feeding apparatus muscle morphology is conserved, the physiological cross‐sectional area of the tubulatus muscle in E. stoutii, is relatively larger than that of M. glutinosa, suggesting a more forceful retraction. The tubular bipennate construction of the tubulatus may represent a novel soft robotic actuator design.
... Some organisms have been reported on cetaceans but cannot be considered epibiotic animals (i.e., they belong to another kingdom or are not intimately associated to cetaceans). For instance, the cirolanid isopods Natatolana spp. or the hagfish Myxine glutinosa Linnaeus, 1758 are scavengers (Hale, 1926;Bowman, 1971;Pinedo et al., 1989;Martini, 1998;Keable, 2006;Zintzen et al., 2011) and records on living cetaceans are unusual (Pace et al., 2016). The following taxa, despite not being intimate associates or not belonging to the animal kingdom, can provide valuable information on cetacean biology. ...
... Roussel de Vauzème, 1834; Baylis, 1923;Skrjabin, 1959;Rice, 1963;Lorenzen, 1986 Other Taxa With Indicator Value Some organisms have been reported on cetaceans but cannot be considered epibiotic animals (i.e., they belong to another kingdom or are not intimately associated to cetaceans). For instance, the cirolanid isopods Natatolana spp. or the hagfish Myxine glutinosa Linnaeus, 1758 are scavengers (Hale, 1926;Bowman, 1971;Pinedo et al., 1989;Martini, 1998;Keable, 2006;Zintzen et al., 2011) and records on living cetaceans are unusual (Pace et al., 2016). The following taxa, despite not being intimate associates or not belonging to the animal kingdom, can provide valuable information on cetacean biology. ...
Each individual cetacean is an ecosystem itself, potentially harboring a great variety of animals that travel with it. Despite being often despised or overlooked, many of these epizoites have been proven to be suitable bio-indicators of their cetacean hosts, informing on health status, social interactions, migration patterns, population structure or phylogeography. Moreover, epizoites are advantageous over internal parasites in that many of them can be detected by direct observation (e.g., boat surveys), thus no capture or dissection of cetaceans are necessary. Previous reviews of epizoites of cetaceans have focused on specific geographical areas, cetacean species or epibiotic taxa, but fall short to include the increasing number of records and scientific findings about these animals. Here we present an updated review of all records of associations between cetaceans and their epibiotic fauna (i.e., commensals, ecto- or mesoparasites, and mutualists). We gathered nearly 500 publications and found a total of 58 facultative or obligate epibiotic taxa from 11 orders of arthropods, vertebrates, cnidarians, and a nematode that are associated to the external surface of 66 cetacean species around the globe. We also provide information on the use as an indicator species in the literature, if any, and about other relevant traits, such as geographic range, host specificity, genetic data, and life-cycle. We encourage researchers, not only to provide quantitative data (i.e., prevalence, abundance) on the epizoites they find on cetaceans, but also to inform on their absence. The inferences drawn from epizoites can greatly benefit conservation plans of both cetaceans and their epizoites.
... They reported a longer duration and higher number of inflection points in whistles emitted during nurturant behavior than in whistles produced in other contexts and hypothesized that these variations may convey information on the emotional state of the emitter [9]. Finally, [19] reported consistent whistles emission during a case of succorant behavior in bottlenose dolphins, with possible distress function. ...
Simple Summary
Death-related behaviors have been often observed in cetaceans, frequently with a female caregiver (presumed mother) supporting a dead calf by carrying, lifting, or sinking it, generally accompanied by other escorting individuals. However, how cetaceans experience death and if their behavior could be compared to human grieving is still largely unknown, as well as their acoustic production in such contexts. This report describes two cases of an adult common bottlenose dolphin (Tursiops truncatus) supporting a dead newborn and associated acoustic behavior in the Tiber River estuary area (Rome, Mediterranean Sea, Italy). In both cases, a main supporter (putative mother) was observed interacting with the carcass of a newborn by lifting (case 1) and sinking it (case 2), always escorted by another adult individual. Several vocalizations were recorded, including a signature whistle (a tonal sound with a repeated, stereotyped, individual-specific frequency modulation pattern) in the first case, likely emitted by the putative mother to seek aid from other individuals. This result appears reasonable since bottlenose dolphins are a highly vocal species, that communicates mainly through acoustic signals. These observations confirm the occurrence of death-related supportive behavior in bottlenose dolphins and report a preliminary description of associated vocalizations, providing additional information on this largely unknown topic.
Abstract
Epimeletic behavior toward dead calves has been frequently reported in cetaceans, mostly with females (presumed mothers) showing supportive behaviors such as carrying, lifting, or sinking, often assisted by “escort” individuals. However, information on acoustic production in such contexts is scarce. This report describes two observations of epimeletic behavior toward dead newborns in bottlenose dolphins and associated acoustic production. Data were collected at the Tiber River estuary (Rome, Mediterranean Sea, Italy) with one hydrophone for passive acoustic monitoring and two digital cameras. In both cases, an individual (presumed mother) acting as the main supporter and directly interacting with the carcass by lifting it (case 1) or sinking it (case 2) was observed. Another adult individual (escort) was present in both encounters showing standing-by and excitement behaviors (case 1) and supportive behavior (case 2). In both encounters, whistles, pulsed sounds, and bray-call elements were recorded. The consistent vocal activity observed likely conveyed context-specific information. A signature whistle in the first encounter was also recorded, likely emitted by the putative mother as a distress call. This report confirms the occurrence of epimeletic behavior in bottlenose dolphins and reports a preliminary description of the acoustic production when a dead calf is involved, providing additional information on this largely unknown topic.
The form and function of the support skeleton, musculature and teeth were examined in an ontogenetic series of Pacific hagfish Eptatretus stoutii spanning about a six-fold range in total length (L(T)). Tooth area, feeding apparatus length, basal plate size, theoretical dental plate retractile force, penetration force and applied tooth stress were measured relative to body size. Morphological variables (e.g. tooth area and basal plate size) scaled with positive allometry and functional variables (e.g. retractile force and applied tooth stress) scaled isometrically with L(T). These results suggest that juveniles do not undergo ontogenetic dietary changes and consume functionally equivalent prey to adults, although adults can grasp proportionally larger portions of food. Low tooth stress in juveniles and adults imposes mechanical constraints to puncturing and tearing, which are circumvented by a preference for softer prey tissue or the inclusion of knotting behaviours for reducing tougher prey.
This study adds the Atlantic spotted dolphin
Stenella frontalis to the list of species displaying nurturant
behavior as a response to perinatal mortality. It is based on two
in situ behavioral observations off Madeira Island (Portugal)
(but with only one continuing uninterrupted). Additionally,
postmortem exams were carried out on four fresh neonate
carcasses, two from the previous events and two from distinct
events where carcasses were found floating with no individuals
in the vicinity. The in situ observations show that adult
Atlantic spotted dolphins try to support their dead calves at
surface, either involving a single individual (presumably the
mother) or several individuals. The highly fresh condition of
the carcasses suggests that the adults abandon them after a
short period of time (hours). The postmortem exams suggest
that the four neonates died from natural causes, and not from
anthropogenic causes, predation, or other intra- or interspecific
behavioral interaction as described in some cetacean populations.
Accurate lengths at birth are also provided, which are
scarce in literature for this species.
This report describes the epimeletic (or "caregiving") behavior produced by members of a group of Atlantic bottlenose dolphins (Tursiops truncatus) and the possible role of the ailing animal's distress call in eliciting such behavior. Epimeletic behavior in cetaceans most typically involves forms of support provided to a distressed, injured, or dying animal (Caldwell & Caldwell, 1966). Analyses of underwater video and corresponding acoustic recordings revealed a distressed dolphin (the DD) that frequently produced what are most likely distress calls, often paired with the emission of long bubble streams. The frequency of her whistle production was positively correlated with the frequency of the supporting behaviors the DD received from other dolphins. These helping behaviors included raft formations, lifts, and stimulating pushes that were predominantly directed toward the upper third of the DD's body, all of which appeared to be directed towards bringing the DD toward the surface so that she could breathe. This is the first documented underwater account of multiple wild bottlenose dolphins providing epimeletic care to a distressed conspecific, and highlights the possible role of distress calls in such scenarios.
Guidelines for use of wild mammal species are updated from the American Society of Mammalogists (ASM) 2007 publication. These revised guidelines cover current professional techniques and regulations involving mammals used in research and teaching. They incorporate additional resources, summaries of procedures, and reporting requirements not contained in earlier publications. Included are details on marking, housing, trapping, and collecting mammals. It is recommended that institutional animal care and use committees (IACUCs), regulatory agencies, and investigators use these guidelines as a resource for protocols involving wild mammals. These guidelines were prepared and approved by the ASM, working with experienced professional veterinarians and IACUCs, whose collective expertise provides a broad and comprehensive understanding of the biology of nondomesticated mammals in their natural environments. The most current version of these guidelines and any subsequent modifications are available at the ASM Animal Care and Use Committee page of the ASM Web site (http://mammalsociety.org/committees/index.asp).
Isolated populations can be strongly influenced by patterns in the local production of food, and by subsidies from outside sources. We used stable-isotope analysis to investigate the rela- tive importance of autochthonous food resources versus pelagic subsidies in the diet of the isolated population of bottlenose dolphins Tursiops sp. inhabiting Doubtful Sound, New Zealand. Samples of the primary carbon sources (macroalgae, phytoplankton and chemoautotrophs) as well as potential food sources (fish and squid) were collected from Doubtful Sound and analysed for δ 13 C and δ 15 N. Iso- topic signatures of fishes fell along a gradient from very depleted values for deep benthic species, particularly hagfish Eptatretus cirrhatus (δ 13 C -23.6, δ 15 N 6.3), to intermediate values for pelagic spe- cies (δ 13 C -18.1, δ 15 N 11.3) and more enriched values for reef-associated species (δ 13 C -16.1, δ 15 N 14.4). Exfoliated skin tissue was collected from live dolphins (n = 11) and used to estimate the isotopic signature of dolphin diet (δ 13 C -15.4, δ 15 N 14.2). The position of this estimate at the most enriched end of the range of isotopic signatures indicated that there was likely minimal mixing of resources from different habitats and that a majority of the dolphin population's diet came from rocky reef and dem- ersal habitats. Estimates of δ 13 C and δ 15 N for dolphin diet were compared with isotopic signatures of the different primary carbon sources using a multiple-source mixing model. Both results suggest that the diet of this population was primarily made up of autochthonous carbon production with a large contribution from benthic macroalgae, rather than pelagic subsidies from outside of the Sound.
The occurrence of the pod weed, Halidrys siliquosa, is recorded
for the first time on the Portuguese coast. Several specimens of this brown
algae were observed attached to the rocky surface in tide pools at
41º44′10″N 8º52′34″W,
extending southward its previously known geographical distribution. The observed
shift is inconsistent with general predictions of species migrations under
warming climate conditions, which anticipate poleward shifts rather than
southern expansions. Although more data will be required to undoubtedly uncover
its cause, the recently observed range expansion raises important questions
about the generalization of the previously stated biogeographic rules.
Background
Whilst there is a body of scientific literature relating to the epibiotic macrofauna on large whales, there is little information on the cetaceans in Icelandic waters. Common minke whales, Balaenoptera acutorostrata Lacépède, 1804, are a common sighting between the months of April to November, however, the migration and distribution of the population in winter requires establishing. The present study provides baseline information on the species composition, geographic distribution and abundance of the epibiotic macrofauna on minke whales landed in Icelandic waters and comments on their acquisition.
Methods
The epibiotic macrofauna and skin lesions on 185 and 188 common minke whales respectively, landed in Icelandic waters between April to September 2003-2007 were determined. For each whale, the fluke and one lateral side was examined.
Results
A total of seven epibiotic species were found: the caligid copepod Caligus elongatus (prevalence (P) = 11.9%, mean intensity (M.I) = 95.5); the pennellid copepod Pennella balaenopterae (P = 10.3%, M.I = 1.6); the cyamid amphipod Cyamus balaenopterae (P = 6.5%, M.I = 37.0); the lepadid cirripedes Conchoderma virgatum (P = 0.5%, M.I = 4.0) and Conchoderma auritum (P = 0.5%, M.I = 1.0), the balanid cirriped Xenobalanus globicipitis (P = 1.6%, M.I = 5.3) and the sea lamprey Petromyzon marinus (P = 2.7%, M.I = 1.0). In addition, the hyperparasitic monogenean Udonella caligorum was found on C. elongatus (P = 6.6%) on 8 of the 22 whales infected with the copepod. No significant relationship was observed between parasite intensity and host body length for either C. balaenopterae or C. elongatus, while the proportion of infected hosts was higher in August-September than earlier in the summer for C. balaenopterae (χ2 = 13.69; p<0.01: d.f.=1) and C. elongatus (χ2 = 28.88; p<0.01: d.f.=1).
Conclusions
The higher prevalence of C. balaenopterae on male whales (χ2 = 5.08; p<0.05: d.f.=1), suggests possible different migration routes by the sexes. A likely explanation of the occurrence of P. marinus attached to the minke whales may be due to the gradually rising sea temperature in the area in recent years. This study represents the first known record of C. elongatus on a cetacean host.
Hagfishes (Myxinidae), a family of jawless marine pre-vertebrates, hold a unique evolutionary position, sharing a joint ancestor with the entire vertebrate lineage. They are thought to fulfil primarily the ecological niche of scavengers in the deep ocean. However, we present new footage from baited video cameras that captured images of hagfishes actively preying on other fish. Video images also revealed that hagfishes are able to choke their would-be predators with gill-clogging slime. This is the first time that predatory behaviour has been witnessed in this family, and also demonstrates the instantaneous effectiveness of hagfish slime to deter fish predators. These observations suggest that the functional adaptations and ecological role of hagfishes, past and present, might be far more diverse than previously assumed. We propose that the enduring success of this oldest extant family of fishes over 300 million years could largely be due to their unique combination of functional traits.
This note reports the first observation of epimeletic behavior for wild rough-toothed dolphins, Steno bredanensis in Brazil. Although these observations consist of a single case, they shed some light into the social behavior of this little-studied species.
In areas where hagfish are found, they are ecologically important for the following reasons:
1.
Hagfish may be one of the most abundant groups of demersal fishes in many areas, in terms of numbers and/or biomass.
2.
Where present at high densities, hagfish burrowing and feeding activities have a significant impact on substrate turnover.
3.
Hagfish are significant as predators on benthic invertebrates and, in some cases, mesopelagic invertebrates and vertebrates.
4.
Hagfish represent one of the most important mechanisms for the rapid cleanup and processing of carrion-falls. In areas subject to intensive commercial fisheries, hagfish probably play a key role in the removal and recycling of discarded by-catch.
5.
Hagfish adults, juveniles, and eggs can represent a significant prey item for marine mammals and large predatory invertebrates.
The belief that dolphins have an extraordinary ability to generate propulsive power or can modify the water flow over their bodies to the low-resistance laminar flow is pervasive in the perception of the animals by the public and by some of the biology communities. I analyzed measured swimming speeds for dolphins of the Stenella-Delphinus morphology. A conservative hydrodynamics model equivalent to 119% of the drag of a rigid fusiform body (the added 19% compensates for the drag induced by propulsion) and a metabolic rate of 13.4 times the projected resting metabolic rate are consistent with measured maximum steady-state speeds. Measured routine swimming speeds are also consistent with this same hydrodynamics model and with metabolic rates for routine activity of other swimming and terrestrial homeotherms. Energy expenditure for swimming dolphins is entirely within expected ranges and no extraordinary mechanisms are necessary to explain observations.
In this note we contribute new evidence of epimeletic behaviour in Steno bredanensis in Brazilian waters. On 2 April 2007 we received information from lifeguards about a dead stranded rough-toothed dolphin at Prainha, Arraial do Cabo, east coast of Rio de Janeiro State, Brazil. The dolphin was a male juvenile, 187 cm in total body length from the tip of the upper jaw to the caudal notch, and it was in a moderate state of decomposition. The results presented here, in addition to previous studies, indicate that rough-toothed dolphins display a highly complex social structure.
A bstract
Stomach contents of 112 bycaught harbor porpoises ( Phocoena phocoena ) collected between 1989 and 1996 in the Kattegat and Skagerrak seas were analyzed to describe diet composition and estimate prey size, to examine sample size requirements, and to compare juvenile and adult diets. Although porpoises preyed on a variety of species, only a few contributed substantially to the diet. Atlantic herring ( Clupea harengus ) was the dominating prey species for both juveniles and adults. Our results, in combination with those from previous studies, suggest that where herring is a dominant food source, porpoises prey primarily on size classes containing mature or maturing individuals. Further, we also show that Atlantic hagfish ( Myxine glutinosa ) may be an important food resource, at least for adult porpoises. Examination of sample size requirement showed that, depending on the taxonomic level used to describe the diet, a minimum of 35–71 stomachs are needed to be confident that all common prey species will be found.
Few data exist on the marine distribution and host organisms of the parasitic sea lamprey, Petromyzon marinus. Some observers have speculated that cetaceans serve as hosts for these fish based on scars, but few lamprey – cetacean interactions have been described in detail in the literature. Here we discuss 35 previously unreported records of sea lampreys that were observed while attached to western North Atlantic right whales, Eubalaena glacialis, during the period 1984 – 2002. Of these observations, 11 were photographically documented with images of sufficient quality to identify the lamprey as P. marinus based on morphological characteristics. The majority of the attachments were recorded in the Bay of Fundy during the summer months when P. marinus are preparing to spawn. It is unknown how lampreys might benefit from this association or what cost may be incurred by their right whale hosts. Feeding and transport are two possible reasons for the attachments.
Sea lampreys Petromyzon marinus were observed on 109 occasions on 47 individual minke whales Balaenoptera acutorostrata. Bloody lesions could be identified as previous attachment sites, indicating P. marinus feeding on B. acutorostrata blood.
The hagfishes (cyclostomes) are known to secrete copious amounts of mucus mainly by the holocrine mode from the slime glands. Stressed animals release two types of cells (gland thread cells, GTCs; gland mucous cells. GMCs) which rupture on contact with water and rapidly form a mass of viscous mucus. Herein we report some key sequential events of this process and document a novel role for cytoskeletal polymers. After electrostimulation of Pacific hagfish (Eptatretus stouti), the exudate was collected in a stabilization buffer and GTCs segregated from GMC vesicles. Water was added progressively to mixtures of known quantities of these entities. The changing mucous composition and properties were monitored by light- and electron microscopy, viscometry and immunogold assay. Sequentially, the threads uncoil from GTCs, aggregate with the vesicles, the vesicles rupture and release mucin-like substances, at least some of which adhere to the thread. It was found that the intermediate filament (IF)-rich threads markedly facilitate hydration and modulate the viscoelastic and cohesive properties of the resultant mucus. It was speculated that the thread abets localization of mucus in an aqueous environment and promotes adhesion of mucus to surfaces such as the fish integument. As judged by immunostaining in situ, GTCs, as well as several cell-types in the epidermis, contain keratin-like components. The role of biopolymers on the properties of teleost and mammalian mucus is discussed.
The mucus layer on the surface of fish consists of several antimicrobial agents that provide a first line of defense against invading pathogens. To date, little is known about the antimicrobial properties of the mucus of Arctic char (Salvelinus alpinus), brook trout (S. fontinalis), koi carp (Cyprinus carpio sub sp. koi), striped bass (Morone saxatilis), haddock (Melanogrammus aeglefinus) and hagfish (Myxine glutinosa). The epidermal mucus samples from these fish were extracted with acidic, organic and aqueous solvents to identify potential antimicrobial agents including basic peptides, secondary metabolites, aqueous and acid soluble compounds. Initial screening of the mucus extracts against a susceptible strain of Salmonella enterica C610, showed a significant variation in antimicrobial activity among the fish species examined. The acidic mucus extracts of brook trout, haddock and hagfish exhibited bactericidal activity. The organic mucus extracts of brook trout, striped bass and koi carp showed bacteriostatic activity. There was no detectable activity in the aqueous mucus extracts. Further investigations of the activity of the acidic mucus extracts of brook trout, haddock and hagfish showed that these fish species had specific activity for fish and human pathogens, demonstrating the role of fish mucus in antimicrobial protection. In comparison to brook trout and haddock, the minimum bactericidal concentrations of hagfish acidic mucus extracts were found to be approximately 1.5 to 3.0 times lower against fish pathogens and approximately 1.6 to 6.6 folds lower for human pathogens. This preliminary information suggests that the mucus from these fish species may be a source of novel antimicrobial agents for fish and human health related applications.
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