Elasmobranchii
Elasmobranchii is a subclass within the class Chondrichthyes, comprising sharks, skates, and rays, characterized by endoskeletons of cartilage, five to seven pairs of gill slits exposed directly to the exterior without an operculum, and dermal denticles known as placoid scales covering the skin.[1][2][3] These fishes exhibit internal fertilization via claspers in males and lack swim bladders, relying on hydrodynamic lift from fins and oil-filled livers for buoyancy.[1][4] Elasmobranchs occupy a wide array of aquatic environments, from deep oceans to freshwater rivers, playing key roles as apex predators and influencing trophic dynamics through their predatory behaviors and life histories.[5] Their evolutionary lineage traces back over 400 million years, with a fossil record primarily of teeth and spines revealing diversification through periods of mass extinction and recovery, underscoring their resilience amid environmental upheavals.[6][7][8]Morphology and Anatomy
General Body Plan
Elasmobranchii encompass sharks, rays, and skates, exhibiting diverse body plans adapted to pelagic, benthic, and demersal habitats. Sharks typically possess a fusiform, spindle-shaped body with a pointed snout, aiding in efficient cruising through water, whereas batoids (rays and skates) feature dorso-ventrally flattened bodies with enlarged pectoral fins that extend anteriorly, facilitating undulatory locomotion along the substrate.[1][9] A defining external feature across elasmobranchs is the presence of five to seven pairs of gill slits opening individually to the exterior, without an opercular cover, allowing direct water expulsion. The skin is adorned with placoid scales—small, dentine-based structures resembling tiny teeth—that provide abrasion resistance, hydrodynamic benefits, and sensory functions. Paired pectoral and pelvic fins, along with unpaired dorsal and caudal fins, support propulsion and stability; in batoids, the pectoral fins dominate for flapping motion, while shark caudal fins are often heterocercal, with an enlarged dorsal lobe enhancing thrust.[1][9][10]Skeletal and Dermal Structures
The endoskeleton of elasmobranchs consists primarily of unmineralized hyaline-like cartilage that forms both embryonic and adult structures without undergoing ossification into true bone, distinguishing it from the bony endoskeletons of osteichthyan fishes.[11] This cartilage core is enveloped by a thin, mineralized surface layer known as tessellated cartilage, where polygonal tesserae—small blocks typically under 500 μm in diameter—tile the exterior, providing enhanced rigidity in high-stress areas such as the jaws, vertebral column, and fin supports.[12][11] Tesserae mineralization involves calcium phosphate deposits, including apatite crystals, arranged in patterns with Liesegang rings and radial spokes at intertesseral joints, developing from isolated globular islets in early embryos (around 6 cm disc width in some species) and expanding via appositional growth without the cellular remodeling seen in bone.[11] Chondrocytes reside in lacunae within the uncalcified cartilage, connected by canalicular networks, but the structure lacks osteocytes and repair mechanisms, relying instead on the fibrous perichondrium for integration.[11][12] In vertebral centra, supplementary calcification forms areolar cartilage, characterized by concentric mineralized annuli surrounding the notochordal remnant, which contribute to axial support but remain less extensively studied than tessellation.[12] Prismatic calcified cartilage may appear in specific elements like the spine, where mechanical demands necessitate denser mineralization, though overall mineral content varies (e.g., approaching levels in compact bone in some shark vertebrae).[11] Dermal structures in elasmobranchs are dominated by placoid scales, or dermal denticles, which embed in the skin as an exoskeletal armor and are developmentally homologous to gnathostome teeth, featuring similar odontogenic tissues.[13] Each denticle comprises a rectangular basal plate anchored in the dermis and a projecting, often posteriorly oriented spine that imparts a rasping texture to the skin.[13] Internally, a vascular pulp cavity supplies nutrients, surrounded by a middle layer of dentine and an outer capping of vitrodentine—a hard, enameloid material resistant to abrasion.[13] Unlike cycloid or ctenoid scales in bony fishes, placoid scales do not expand with somatic growth; juveniles add new denticles interstitially, resulting in denser coverage over time, with size, shape, and spination varying by species (e.g., more pronounced thorns in certain sharks) and body region to optimize protection or hydrodynamics.[13]Sensory Organs
Elasmobranchs possess a diverse array of sensory organs finely tuned to detect chemical, mechanical, electrical, and visual stimuli in aquatic environments, enabling prey detection, navigation, and predator avoidance. These include the olfactory system for chemical cues, vision adapted for low-light conditions, electroreception via the ampullae of Lorenzini, mechanoreception through the lateral line, and audition via the inner ear.[14][15] The olfactory system features paired nares leading to olfactory sacs with rosettes containing 31 to 300 lamellae, which increase surface area by 70 to 495% through secondary folding, enhancing detection of amino acids at concentrations from 10^{-7} to 10^{-9} M; the scalloped hammerhead shark detects alanine at 10^{-11} M.[15] Olfactory bulbs can comprise over 30% of brain mass in deep-water species, reflecting specialization for odor localization via bilateral timing differences and somatotopic mapping.[15] This system drives behaviors such as prey tracking in nurse sharks, which rely on olfactory cues for feeding, and detection of sex pheromones or predator odors.[15][14] Vision occurs through duplex retinas with rods and cones, supported by a tapetum lucidum—a reflective layer of mirrored crystals behind the retina that amplifies light in dim conditions, allowing sharks to see approximately 10 times better than humans in low light.[14] Eye size varies from 0.3 cm in small dogfish to 6.2 cm in thresher sharks, with rod-dominated sensitivity peaking around 500 nm and potential dichromatic or trichromatic capabilities in some batoids and sharks via multiple cone pigments.[15] Temporal resolution reaches 20 to 45 Hz, up to 54 Hz in sandbar sharks, aiding pursuit of fast-moving prey.[15] Electroreception is mediated by the ampullae of Lorenzini, dermal pores connected by jelly-filled canals to electrosensory cells that detect electric fields as weak as 5 nV/cm, primarily in the 0.1 to 15 Hz range for bioelectric signals from prey muscle activity.[16] These organs, numbering in the hundreds around the head, facilitate prey localization even when buried or hidden, predator avoidance, and geomagnetic navigation via field polarity and intensity.[14] Sensitivity varies by species, with neural gain up to 24 spikes/s per μV/cm in some rays.[14] The lateral line system comprises fluid-filled canals beneath the skin, housing neuromasts that sense water velocity on the order of μm/s and acceleration up to mm/s², sensitive to low-frequency vibrations (≤200 Hz) from nearby movements.[14] This mechanoreceptive array detects hydrodynamic disturbances up to 1-2 body lengths away, supporting rheotaxis for odor plume tracking, school coordination, and prey localization via eddies.[14] Audition and balance are handled by the inner ear, featuring three semicircular canals and end organs including the unique macula neglecta, which enhances low-frequency detection (best sensitivity 20-300 Hz).[15] Inner ear size scales hypoallometrically with body mass and is larger in piscivorous and reef-associated species, correlating with enhanced auditory sensitivity for prey sounds and habitat-specific soundscapes; semicircular canals are smaller in pelagic forms, reflecting locomotor demands.[17]Physiology
Osmoregulation and Metabolism
Elasmobranchs maintain osmotic balance primarily through a ureosmotic strategy, retaining high concentrations of urea (typically 350–600 mmol L⁻¹) and trimethylamine oxide (TMAO, around 70–120 mmol L⁻¹) in their plasma, resulting in total osmolarities of approximately 1000–1100 mOsm L⁻¹, which is iso- or slightly hyperosmotic to seawater (about 1000 mOsm L⁻¹).[18][19] This approach minimizes passive water loss across permeable gills and skin while countering the inward diffusion of salts, differing from the hypoosmotic strategy of marine teleosts that rely on active ion extrusion.[20] Urea serves as the primary osmolyte, synthesized in the liver via the ornithine-urea cycle and actively reabsorbed in the kidneys through specialized urea transporters (e.g., UT family proteins), preventing excessive urinary loss despite glomerular filtration rates of 15–20% of plasma flow.[21][22] Excess sodium and chloride ions gained from seawater are excreted via the rectal gland, a specialized organ that secretes a fluid isoosmotic to plasma but with high NaCl concentrations (up to 500 mmol L⁻¹ each), driven by Na⁺/K⁺-ATPase pumps and coupled chloride channels.[19] The gills contribute minimally to ion extrusion compared to teleosts but handle some Na⁺ and Cl⁻ uptake regulation, while the kidney produces dilute urine (200–400 mOsm L⁻¹) relative to plasma, aiding water conservation.[20] In euryhaline species, such as bull sharks (Carcharhinus leucas), reduced salinity triggers downregulation of urea synthesis and retention, lowering plasma urea to 100–300 mmol L⁻¹ to avoid toxicity in hypoosmotic environments, supplemented by increased active ion uptake at gills and kidneys.[23] TMAO counteracts urea's perturbing effects on proteins, maintaining cellular function at these elevated levels.[18] Elasmobranch metabolism is generally ectothermic and lower than in comparably sized teleosts, with routine metabolic rates scaling at 1.5–3.0 mg O₂ kg⁻¹ h⁻¹ for many species at 20°C, reflecting adaptations to intermittent feeding and energy conservation in cartilaginous skeletons that reduce structural mass.[24] Preferred fuels include lipid-derived ketones (e.g., β-hydroxybutyrate) over glucose, enabling sustained activity during fasting via efficient hepatic ketogenesis, though amino acids contribute during protein catabolism.[25] Select taxa, such as lamniform sharks (e.g., great white, Carcharodon carcharias), exhibit regional endothermy via vascular counter-current heat exchangers, elevating red muscle temperatures by 10–20°C above ambient to support burst swimming, which increases metabolic scope but raises overall energy demands by 2–3 times compared to ectothermic congeners.[26] In rays, benthic habits correlate with even lower rates (0.5–2.0 mg O₂ kg⁻¹ h⁻¹), with diel rhythms showing peaks at dusk in species like epaulette sharks (Hemiscyllium ocellatum), independent of temperature fluctuations.[27] Osmoregulatory costs, including urea synthesis (about 10–15% of total energy budget), integrate with metabolism, as high protein turnover for urea production demands dietary nitrogen intake exceeding that of teleosts.[20]Locomotion and Respiration
Elasmobranchs demonstrate specialized locomotion adapted to aquatic environments, with sharks relying on lateral undulations of the body and tail that propagate from an anguilliform to thunniform mode depending on speed and species. The heterocercal caudal fin, featuring a larger dorsal lobe, generates thrust by producing a posteroventral water jet angled 40–45° below horizontal, simultaneously providing lift to counteract negative buoyancy.[28] Swimming speeds typically range from 0.5 to 2.0 body lengths per second, with body angle decreasing toward horizontal at higher velocities for streamlined efficiency.[28] Pectoral fins in sharks contribute minimally to steady propulsion but adjust dynamically for vertical maneuvers, such as increasing chord angle to +14° for ascent.[28] In batoids (rays and skates), propulsion shifts to undulatory or oscillatory motions of enlarged pectoral fins, which form a disc-like structure enabling hovering, precise turns, and benthic punting via pelvic fins in some species.[28] Chimaeras employ pectoral fin flapping combined with body undulations. Dermal denticles covering the skin reduce drag by aligning flow and minimizing turbulence, particularly evident in fast-swimming forms.[28] These mechanisms optimize energy use, with undulation suiting slow, maneuverable swimming and oscillation favoring sustained cruising.[28] Respiration in elasmobranchs occurs through 5 to 7 pairs of external gill slits per side, facilitating water flow over vascularized gill lamellae for oxygen extraction via counter-current exchange.[29] Ventilation modes include ram ventilation, where forward motion passively streams water through the open mouth and over the gills, predominant in active pelagic species, and buccal pumping, involving pharyngeal contractions to actively draw and expel water, common in demersal forms.[30] Most elasmobranchs are facultative, switching modes to rest without suffocation, but obligate ram ventilators—such as great white sharks (Carcharodon carcharias), shortfin makos (Isurus oxyrinchus), and whale sharks (Rhincodon typus)—lack sufficient buccal musculature and must swim continuously to maintain gill perfusion, achieving high respiratory efficiency at speeds above 0.5 body lengths per second.[31] [32] Batoids supplement primary ventilation with spiracles—vestigial first gill slits posterior to the eyes—that intake oxygenated water from above the head, crucial for buried or substrate-resting postures where the mouth ingests sediment.[33] Gill function yields efficient oxygen uptake, often exceeding arterial partial pressure relative to expired water, supporting active metabolisms despite urea-based osmoregulation.[34]Evolutionary History
Origins and Early Diversification
The origins of Elasmobranchii, the subclass encompassing modern sharks, skates, and rays, trace to the Devonian Period, with the earliest evidence of shark-like chondrichthyans appearing approximately 410 million years ago in the Early Devonian. Fossils such as teeth from Doliodus problematicus exhibit primitive features including multiple cusps and vascularization patterns indicative of early cartilaginous fish dentition, marking the onset of chondrichthyan evolution before the full diversification of elasmobranch-specific traits.[35] These forms likely arose from stem-group chondrichthyans amid the adaptive radiation of aquatic vertebrates following the Silurian, driven by ecological opportunities in marine predation niches.[36] By the Middle Devonian (late Givetian stage, around 383 million years ago), unambiguous total-group elasmobranchs emerged, represented by Phoebodus, whose dental morphology and skeletal elements from Late Devonian (Famennian) deposits in Morocco reveal hybodontiform affinities with cladodont teeth suited for grasping prey.[36] This genus underscores the transition from basal chondrichthyans to more derived elasmobranchs, featuring enhanced jaw mechanics and body streamlining for active swimming. Early diversification accelerated in the Late Devonian and extended into the Carboniferous, where fossil assemblages from regions like the Canning Basin in Western Australia document at least 18 shark taxa, including ctenacanthiforms with robust, multi-cuspidate teeth adapted to durophagous diets.[37] These developments coincided with the proliferation of reefal and nearshore habitats, facilitating niche partitioning among predatory forms.[8] Carboniferous elasmobranchs, such as Ctenacanthus and cladoselachians, exemplify early morphological experimentation, with elongated bodies, heterocercal tails, and calcified cartilage skeletons preserving well in anoxic sediments.[38] Diversity peaked with over 20 genera in some assemblages, reflecting adaptations to both marine and freshwater incursions during the period's climatic fluctuations. However, Paleozoic elasmobranchs remained stem-like compared to Mesozoic neoselachians, lacking the specialized fins and placoid scales of modern lineages, and many lineages experienced bottlenecks at the Permo-Triassic extinction.[39] This early phase laid foundational traits like internal fertilization and viviparity precursors, setting the stage for subsequent radiations.[6]Fossil Record and Extinctions
The fossil record of Elasmobranchii, comprising sharks, rays, and skates, is dominated by disarticulated elements such as teeth, fin spines, and calcified vertebral centra, as their cartilaginous endoskeletons rarely preserve intact. Earliest elasmobranch remains appear in the Devonian Period, around 400 million years ago, with primitive taxa like ctenacanthiforms documented from Late Devonian deposits.[40] Diversification accelerated in the Carboniferous and Permian, encompassing diverse morphologies including hybodonts, before a Mesozoic radiation of neoselachians around 250 million years ago.[41] All modern orders and most families have fossil representatives, with sharks exhibiting deeper temporal ranges than rays; for instance, extant genera trace back to the Early Jurassic (~190 million years ago), and some species to the Late Cretaceous (~66 million years ago).[41] Elasmobranchs demonstrated resilience across major mass extinctions, surviving the end-Permian event (~252 million years ago) through habitat contraction into deep-sea refugia, as evidenced by the persistence of stem chondrichthyan lineages into the Cretaceous.[42] The Cretaceous-Paleogene extinction (66 million years ago) inflicted heavier tolls on neoselachians, extinguishing 17% of families (7 of 41) and 56% of genera (60 of 107), with disproportionate impacts on batoids (rays and skates) and open-marine apex predators like anacoracid sharks, while benthopelagic and deep-water forms fared better.[43] Post-extinction recovery involved the emergence of modern families such as Carcharhinidae by the Danian stage of the Paleocene, restoring diversity by the early Eocene.[43] Overall, elasmobranchs endured at least four mass extinctions with selective survivorship favoring adaptable, ecologically flexible lineages.[40]Modern Evolutionary Patterns
The Cretaceous-Paleogene (K-Pg) mass extinction event, occurring approximately 66 million years ago, resulted in the loss of over 60% of elasmobranch diversity, with net diversification rates turning strongly negative during this interval. Recovery followed in the Paleocene and Eocene, marked by increased speciation in surviving lineages, though overall rates remained subdued compared to ray-finned fishes (teleosts), which experienced more pronounced post-extinction radiations due to higher speciation efficiencies. Elasmobranch persistence is evidenced by the survival of basal groups like Hexanchiformes, contributing to a modern total of over 1,200 species across sharks, skates, and rays.[44][45] Cenozoic diversification showed episodic bursts, particularly in the Oligocene and Miocene, linked to biogeographic drivers such as continental drift, tectonic uplift, and eustatic sea-level changes that fragmented habitats and opened new niches. For instance, Carcharhiniformes (requiem sharks) and Orectolobidae (wobblegills) exhibited rapid cladogenesis during these periods, coinciding with the proliferation of coastal and reef environments. Batoids (rays and skates) displayed relatively higher diversification within Elasmobranchii, with molecular phylogenies indicating Cenozoic radiations tied to benthic adaptations and viviparity, contrasting slower turnover in shark-dominated Selachii. Key innovations, such as bioluminescence in deep-sea Etmopteridae, further accelerated speciation in isolated oceanic realms by facilitating prey detection and mate recognition.[44][44] Trophic ecology has profoundly shaped modern patterns, with tooth morphology and dietary specialization driving partitioning rather than direct competition. Time-calibrated phylogenies reveal stable dental disparity in Carcharhiniformes since the Mesozoic, peaking with generalist diets amid Eocene coral reef expansions, while Lamniformes experienced Late Cretaceous highs followed by post-K-Pg declines and Holocene recoveries, correlating with piscivory and environmental shifts like sea-level regression. Gigantism evolved convergently multiple times (e.g., in filter-feeding rhincodontids and lamnids), tied to resource abundance in open oceans, but increased extinction vulnerability in apex predators during Miocene-Pliocene cooling. Biotic interactions, including prey availability and competitor exclusion, underscore low net rates, with viviparous lineages diversifying at roughly twice the pace of oviparous ones due to enhanced maternal investment and juvenile survival.[46][44][47]Systematics and Taxonomy
Higher Classification
Elasmobranchii is recognized as a subclass within the class Chondrichthyes, which encompasses all cartilaginous fishes distinguished by their endoskeleton composed primarily of cartilage rather than bone, multiple unpaired gill slits, and placoid scales in most species.[48][49] The class Chondrichthyes diverged from bony fishes (Osteichthyes) approximately 420–450 million years ago during the Silurian-Devonian periods, forming one of the two major lineages of jawed vertebrates (Gnathostomata).[50] This division is supported by molecular phylogenies, including mitochondrial genome analyses, which confirm Elasmobranchii's monophyly alongside the sister subclass Holocephali (chimaeras).[49] Higher in the hierarchy, Chondrichthyes belongs to the subphylum Vertebrata (craniates with a vertebral column), phylum Chordata (characterized by a notochord, dorsal nerve cord, pharyngeal slits, and post-anal tail at some life stage), and kingdom Animalia.[48] This placement reflects shared deuterostome traits with other vertebrates, including internal fertilization and advanced sensory systems, though Chondrichthyes uniquely retain urea-based osmoregulation and spiral valve intestines. Taxonomic ranks above subclass remain stable in contemporary classifications, with no major revisions altering Elasmobranchii's position since the integration of molecular data in the early 2000s.[51] Phylogenetic studies, such as those using mitogenomic sequences from over 80 species, reinforce Elasmobranchii as a well-supported clade within Chondrichthyes, excluding Holocephali based on differences in jaw suspension, cloacal structure, and reproductive anatomy.[49] While some early classifications elevated Elasmobranchii to class rank, current consensus subordinates it to subclass to accommodate the basal split with Holocephali, avoiding paraphyly.[52] This hierarchy aligns with fossil evidence from Devonian deposits, where primitive elasmobranch-like forms predate holocephalan diversification.[53]Major Orders and Families
The subclass Elasmobranchii comprises approximately 1,192 species across 14 orders and 60 families, representing the sharks, rays, skates, and allied forms.[54] These taxa are united by features such as multiple rows of replaceable teeth, placoid scales, and a spiral valve intestine, with modern diversity concentrated in the superorder Euselachii under the subclass. Extant elasmobranchs divide into two primary clades: Selachimorpha (sharks, ~500 species in ~34 families) and Batoidea (batoids, including rays and skates, ~689 species in ~42 families), reflecting adaptations to predatory and benthic lifestyles.[55] Phylogenetic analyses confirm this bipartition, with Selachimorpha branching earlier and exhibiting greater morphological disparity in body form compared to the dorsoventrally flattened batoids.[54] Within Selachimorpha, eight principal orders encompass the shark diversity, each characterized by distinct dentition, fin morphology, and habitat preferences:- Hexanchiformes: Primitive six- or seven-gilled sharks, including families Hexanchidae (e.g., bluntnose sixgill shark) and Chlamydoselachidae (frilled shark), totaling ~6 species; these retain archaic traits like multiple gill slits.[56]
- Squaliformes: Dogfish and gulper sharks, with families such as Squalidae and Centrophoridae (~100 species); known for luminescent organs and deep-sea adaptations.[56]
- Squatiniformes: Angel sharks (family Squatinidae, ~20 species), ambush predators with pectoral fins fused to the head, resembling flattened rays.[56]
- Pristiophoriformes: Sawsharks (family Pristiophoridae, ~7 species), distinguished by elongate rostral teeth used for prey manipulation.[56]
- Heterodontiformes: Bullhead sharks (family Heterodontidae, ~9 species), with molariform posterior teeth for crushing mollusks.[56]
- Orectolobiformes: Carpet sharks, including families Orectolobidae (wobbegongs) and Hemiscylliidae (~45 species); feature barbels and nocturnal habits in tropical reefs.[56]
- Lamniformes: Mackerel sharks, with families Lamnidae (e.g., great white shark) and Alopiidae (thresher sharks, ~60 species); noted for regional endothermy and high-speed cruising.[56]
- Carcharhiniformes: Ground sharks, the most speciose order (~280 species in ~8 families like Carcharhinidae and Scyliorhinidae); includes requiem and catsharks, dominant in coastal and pelagic zones.[56][55]
- Rhinopristiformes: Guitarfishes, wedgefishes, and sawfishes (families Rhinobatidae, Pristidae; ~60 species); transitional forms between sharks and rays, with sawfishes possessing rostral serrations for hunting.[56]
- Torpediniformes: Electric rays (families Torpedinidae, Narcinidae; ~60 species), equipped with paired electric organs derived from kidney tissue for prey stunning and defense.[56]
- Rajiformes: Skates (families Rajidae, Arhynchobatidae; ~200 species), oviparous benthic forms with thorned dorsal surfaces and tail fins for propulsion.[56]
- Myliobatiformes: Stingrays, eagle rays, and manta rays (families Dasyatidae, Myliobatidae; ~300 species); venomous tail spines and diamond-shaped discs, with some species performing benthic "aquatic flight" via pectoral undulations.[56]