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Neocoleoidea

Neocoleoidea is a monophyletic cohort within the subclass Coleoidea of cephalopod mollusks, comprising all extant dibranchiate cephalopods excluding the Nautiloidea. This group encompasses the two primary superorders: Decapodiformes, which includes diverse taxa such as squids (Teuthida), cuttlefish (Sepiida), and bobtail squids (Sepiolida), and Octopodiformes, consisting of octopuses (Octopoda) and the vampire squid (Vampyromorphida).^[1]^[2] Neocoleoids are distinguished by several key morphological features, including a reduced, internalized, or entirely absent shell enclosed within the mantle; eight or ten circumoral arms equipped with suckers (and sometimes hooks) for prey capture; a single pair of gills (unlike the two pairs in nautiloids); and a chitinous beak-like jaw paired with a radula for feeding.^[2] Their body sizes range from approximately 2 cm in small sepiolids to over 20 m in the giant squid (Architeuthis dux), making them one of the most size-diverse groups of marine invertebrates.^[2] Neocoleoids possess advanced sensory systems, including large, camera-like eyes with lenses and a highly developed nervous system that supports complex behaviors such as learning, problem-solving, and rapid changes in color and texture via chromatophores and papillae for camouflage and communication; many deep-sea species also exhibit bioluminescence.^[2]^[1] Phylogenetically, Neocoleoidea represents the crown group of coleoids, with a fossil record that includes extinct lineages such as the belemnoids (Belemnoidea), teudopsids (Teudopseina), and plesioteuthids (Plesioteuthididae), which highlight the evolutionary diversification from shelled ancestors to modern soft-bodied forms and dates back to the Paleozoic era.^[1] Today, with fewer than 1,000 described species distributed across approximately 60 families, neocoleoids play crucial ecological roles as both predators and prey in marine ecosystems worldwide, contributing significantly to global fisheries and serving as models for studying invertebrate intelligence and neurobiology.^[2]^[1]

Taxonomy and phylogeny

Definition and classification

Neocoleoidea is defined as the cohort comprising the crown group of the subclass Coleoidea, encompassing all extant coleoid cephalopods and some extinct lineages such as Belemnoidea (nested within Decapodiformes); it is characterized by shared derived traits such as a reduced, internalized shell and an advanced ink sac system.^[3]^[1] This grouping was formally proposed by Haas in 1997 to distinguish the modern, monophyletic radiation of coleoids from earlier stem relatives, replacing earlier informal terms like "Dibranchiata."^[3] Within the broader hierarchy of Cephalopoda, Neocoleoidea occupies the position of Class Cephalopoda > Subclass Coleoidea > Cohort Neocoleoidea, from which it diverges into the two primary superorders: Decapodiformes (including squids and cuttlefish) and Octopodiformes (including octopuses and the vampire squid).^[3]^[1] Key diagnostic apomorphies of Neocoleoidea include the internalization of the shell as a flexible gladius or its complete reduction in some lineages, the presence of a single pair of gills (dibranchiate condition), a highly developed brain-to-body mass ratio (typically 2-5% of body weight, far exceeding that of Nautiloidea at less than 1%), and statocysts that provide advanced balance and orientation capabilities.^[1]^[4]^[5] The monophyly of Neocoleoidea is widely accepted in contemporary phylogenies, supported by cladistic analyses integrating morphological data from both fossil and living taxa, such as those from 2015 that resolve it as a robust clade with Belemnoidea nested within Decapodiformes; however, some molecular studies reveal unresolved basal polytomies within the group.^[1]^[6]

Evolutionary history

Neocoleoidea originated in the late Paleozoic, during the Late Devonian to Early Carboniferous, evolving from bactritoid or early orthoconic nautiloid-like ancestors through early coleoid forms characterized by internal shells and ink sacs.^[7] Phylogenetic analyses place the divergence of Neocoleoidea between approximately 398 and 335 million years ago, with a median estimate around 363 million years ago, coinciding with the Mississippian subperiod's marine reorganization and the rise of nektonic lifestyles.^[8] These early forms transitioned from external, chambered shells to reduced internal structures, marking a shift toward greater mobility.^[7] Within the broader Coleoidea subclass, neocoleoids represent the crown group, with a fossil record including early forms from the Carboniferous; post-Permian-Triassic extinction recovery facilitated Mesozoic radiation involving key adaptations such as the loss of buoyancy-regulating chambers in the phragmocone and enhanced efficiency in jet propulsion via a more muscular mantle and funnel system, enabling faster and more agile swimming compared to nautiloid ancestors.^[9]^[10]^[8] Fossil evidence highlights key milestones, with the earliest recognized neocoleoids from the Carboniferous (e.g., Gordoniconus), and Early Jurassic examples like Plesioteuthis, which preserved gladius and mantle imprints indicating squid-like forms.^[7]^[11] Diversification accelerated during the Cretaceous, when decapodiform (squid-like) and octopodiform (octopus-like) lineages diverged, driven by ecological specialization in open oceans and benthic habitats.^[10] This period saw increased morphological variety, including fin development and arm specialization, amid a backdrop of global warming and sea-level changes.^[12] A 2015 cladistic analysis using 137 morphological characters across 77 taxa confirmed the monophyly of Neocoleoidea, with stem groups such as Trachyteuthididae positioned as basal to octopodiforms, supporting a Jurassic origin for major crown clades.^[1] Mass extinctions profoundly shaped this history; at the Cretaceous-Paleogene (K-Pg) boundary, neocoleoids survived through deep-sea refugia, where reduced oxygen and predation pressures preserved soft-bodied lineages like vampyromorphs and early octopods.^[12] The fossil record of Neocoleoidea remains incomplete, particularly for soft tissues, due to their rapid decay and rarity in preservation; identifications often rely on gladius imprints or phosphatic remnants, limiting insights into mantle, arm, and nervous system evolution.^[13] Exceptional Lagerstätten, such as Solnhofen, provide glimpses but underscore gaps in pre-Jurassic and post-Cretaceous transitions.

Morphology and physiology

External anatomy

Neocoleoidea display a bilaterally symmetric body plan adapted for agile swimming and predation, featuring a well-developed head with prominent eyes, a muscular mantle enclosing the viscera, and eight or ten appendages encircling the mouth. The head integrates sensory organs and the beak, while the mantle cavity contains gills and the funnel—a muscular, siphon-like structure that expels water for jet propulsion, enabling rapid bursts of speed. This configuration contrasts with the external shell of nautiloids, emphasizing flexibility and hydrodynamic efficiency in neocoleoids.^[2] The appendages include eight arms in all members, with decapodiforms (squid and cuttlefish) bearing two additional, elongate tentacles specialized for prey capture. Arms and tentacles function as muscular hydrostats, lined with suckers or chitinous hooks arranged in rows; suckers feature acetabula for adhesion, while hooks provide grasping power in predatory species. Cirrate forms, such as some deep-sea octopods, possess oral cirri alternating with suckers for enhanced sensory and manipulative capabilities, whereas incirrate forms rely solely on suckers. Males across neocoleoids have one arm modified into a hectocotylus, equipped with reduced suckers or papillae to transfer spermatophores during reproduction.^[14]^[15] The external integument is a dynamic layer rich in specialized cells, including expandable chromatophores for pigmentation, iridophores for structural coloration via light reflection, and papillae for texture alteration. These elements allow rapid shifts in hue, pattern, and surface relief, facilitating camouflage against diverse backgrounds or signaling during interactions; deep-sea taxa often incorporate photophores—luminescent organs—for counter-illumination or communication. The gladius, a vestigial internal chitinous structure, supports the dorsal mantle and is visible in some preparations, varying from the rigid, chambered cuttlebone in sepiids to the slender, flexible pen in teuthids, though entirely absent in octopods.^[16]^[17] Size variation is extreme, spanning from approximately 1.5–2 cm in mantle length for pygmy squids such as Idiosepius pygmaeus to up to approximately 13–18 m in total length for the giant squid (Architeuthis dux), with the colossal squid (Mesonychoteuthis hamiltoni) reaching weights up to 500 kg. Sexual dimorphism is prevalent, frequently with females larger and more robust than males, as seen in species like Ommastrephes bartramii where mature females attain mantle lengths over twice those of males. The gladius provides essential internal rigidity for mantle musculature in most forms, linking external mobility to underlying support.^[18]

Internal systems

The nervous system of neocoleoids represents a pinnacle of invertebrate neural complexity, featuring the largest brain among invertebrates with approximately 500 million neurons in species like the common octopus (Octopus vulgaris).^[19] This central brain, encircling the esophagus, is divided into supraesophageal, subesophageal, and optic lobes, with the optic lobes alone containing 120–180 million neurons dedicated to advanced visual processing and memory formation.^[20] Complementing this centralization is a decentralized architecture, where arm-specific ganglia enable semi-autonomous control of the arms, allowing coordinated movements independent of the central brain and supporting behaviors like manipulation and camouflage.^[21] Neocoleoids possess a closed circulatory system, unique among mollusks, which efficiently supports their active, predatory lifestyles through high-pressure blood flow. This system includes three hearts: two branchial hearts that pump deoxygenated blood through the gills for oxygenation, and a single systemic heart that distributes oxygenated blood to the body.^[22] Respiratory exchange occurs via a pair of gills housed in the mantle cavity, where water is drawn in through the mantle opening and expelled via the funnel, facilitating oxygen uptake in oxygen-poor marine environments. The digestive system is adapted for rapid processing of prey, featuring a powerful chitinous beak at the mouth for tearing flesh, which works in conjunction with radular structures to grasp and ingest food.^[18] An ink sac, connected to the hindgut, provides a defensive mechanism by ejecting dark melanin-based ink to confuse predators, a trait present in most neocoleoids, though secondarily lost in some deep-sea octopods of the suborder Cirrata.^[23] Excretion is managed by renal appendages—branched structures within the renal sac that filter waste from the blood—along with the branchial hearts' complex, which aids in ammonia elimination through the gills.^[24] Reproduction in neocoleoids is sexual and gonochoristic, with males transferring spermatophores—elongated sperm packets—via a specialized arm (hectocotylus) during complex courtship displays involving visual and tactile cues. Developmental modes vary: octopods typically exhibit direct development from large, yolk-rich eggs hatching as miniature adults, while many decapods produce paralarvae—planktonic larvae that undergo significant metamorphosis before settling.^[25] Semelparity predominates, with adults often dying after a single reproductive event, such as females brooding eggs until hatching, which aligns with their high-energy investment in offspring survival.^[26] Sensory capabilities are highly advanced, enabling precise navigation and predation. The eyes are camera-type structures convergent with vertebrates, featuring a single lens, retina, and no blind spot, which resolve fine details like shape, color, and motion in low-light conditions.01175-2) Chemoreceptors distributed across the arms and suckers detect chemical cues from prey and mates, facilitating foraging and social interactions. Balance and orientation are maintained by statocysts—fluid-filled sacs containing otoliths that detect gravity and acceleration—integrated with the nervous system for rapid adjustments during jet propulsion.^[27]

Classification

Extant superorders

The extant superorders of Neocoleoidea comprise Decapodiformes and Octopodiformes, representing the two primary living lineages of advanced cephalopods that diverged during the Mesozoic Era. Molecular phylogenetic analyses, incorporating multiple mitochondrial and nuclear genes, support this bifurcation, with divergence estimates ranging from the Middle Triassic (approximately 241 million years ago) to the late Paleozoic (around 276 million years ago), marking a key event in coleoid evolution. Both superorders share neocoleoid characteristics such as internalized shells, complex camera-type eyes with a lens, and chromatophores for rapid color change, but they differ markedly in appendage morphology, locomotion, and ecological niches, with Decapodiformes tending toward pelagic lifestyles and Octopodiformes exhibiting greater benthic diversity.^[28]^[29] Decapodiformes, often referred to as decabrachians, are defined by the presence of ten appendages: eight shorter arms and two longer, specialized tentacles equipped with terminal clubs for prey capture. This superorder encompasses several orders, including Teuthida (squids), Sepiida (cuttlefishes), and Sepiolida (bobtail squids), along with minor groups like Idiosepida and Spirulida. A prominent feature is the gladius, a chitinous internal shell remnant that provides structural support within the mantle, varying from a slender pen in squids to a broad cuttlebone in cuttlefish. Many species, particularly in pelagic Teuthida families such as Ommastrephidae and Histioteuthidae, possess luminous organs (photophores) for bioluminescence, enabling counter-illumination camouflage in open water or signaling during mating. Jet propulsion via a well-developed funnel dominates locomotion, facilitating rapid escapes and hunting in midwater environments.^[18]^[30]^[18] In contrast, Octopodiformes feature eight arms without distinct tentacles, emphasizing flexibility and dexterity in manipulation. This superorder includes the order Vampyromorphida, represented by the vampire squid (Vampyroteuthis infernalis), and the diverse order Octopoda (octopuses), subdivided into incirrate (lacking cirri) and cirrate forms. Most species lack fins and prominent internal shells, with only a reduced gladius present in Vampyromorphida; instead, they rely on muscular hydrostat arms for propulsion. Advanced camouflage is a hallmark, achieved through specialized skin papillae and iridophores that allow texture and pattern mimicry, surpassing the color-changing capabilities of Decapodiformes. Cirri—fleshy, hair-like filaments flanking the suckers—are characteristic of cirrate octopods (suborder Cirrata), aiding in filter-feeding on detritus in deep-sea habitats. Locomotion often involves crawling or slow swimming, suiting benthic and demersal lifestyles, though some octopods are pelagic.^[31]^[30]

Extinct groups

The extinct groups related to Neocoleoidea primarily encompass Mesozoic lineages that exhibit transitional morphologies between earlier belemnoids and crown-group neocoleoids, providing critical insights into the evolution of internal shell structures and soft-part anatomy. Basal families such as Trachyteuthididae, known from the Jurassic to Cretaceous periods, are often placed incertae sedis due to their primitive gladius forms characterized by a median field, hyperbolar zone, and lateral fields, which represent early stages in the reduction of the internal shell. These fossils, including genera like Trachyteuthis and Glyphiteuthis, preserve evidence of octobrachiate affinities with circular suckers and two pairs of fins, highlighting their role in early diversification of octopod-like forms.^[32] Other notable orders include Phragmoteuthida and Loligosepioida, both from the Mesozoic and showing features transitional to modern squid-like neocoleoids; the phylogenetic position of Phragmoteuthida remains debated, with placements as stem-neocoleoids, stem-decabrachians, or stem-octobrachians. Phragmoteuthida, spanning the Late Triassic to Early Jurassic (Carnian to Sinemurian), is distinguished by a mineralized phragmocone with an apical angle of 10–30 degrees and a tripartite, fan-like pro-ostracum—a shell precursor—attached to the phragmocone, along with hook-bearing arms and a multi-layered conotheca but lacking a rostrum or guard. Fossils such as Phragmoteuthis bisinuata and P. polzbergensis reveal ten arms with differentiated hooks and preserved ink sacs, underscoring their plesiomorphic state in coleoid arm armature. Loligosepioida, restricted to the Early Jurassic (Toarcian), includes genera like Loligosepia with a gladius-bearing body, eight equal-length arms lacking hooks or tentacles, and a phosphatized arm crown, suggesting affinities with vampyropods rather than decabrachians and marking a shift toward streamlined, squid-like propulsion.^[33]^[34]^[35] Key characteristics across these groups include the presence of a pro-ostracum as a precursor to the gladius, with evidence from exceptional fossil preservation showing gladius vanes, rachis, and occasional belemnite-like guards in related stem forms, though absent in Phragmoteuthida. These features, documented in gladius fossils from lagerstätten like Lebanon and Polzberg, illustrate the progressive internalization and reduction of the shell in neocoleoid evolution. Phylogenetically, these lineages serve as stem groups bridging Belemnoidea and Neocoleoidea; a 2015 cladistic analysis incorporating both fossil and living taxa positions Trachyteuthididae as sister to the total-group Octopoda and Loligosepioida as a basal assemblage to the crown Octopoda within Octopodiformes, thus clarifying the monophyly of Neocoleoidea exclusive of belemnoids.^[1]^[32] Many of these extinct neocoleoid groups declined sharply after the Cretaceous, with diversity peaking in the Mesozoic before a post-Cretaceous-Paleogene (K/Pg) boundary reduction, potentially driven by intensified competition from rapidly diversifying teleost fishes that assumed dominant pelagic roles in the early Paleocene. This pattern is evident in the fossil record, where gladius-bearing taxa like Trachyteuthididae vanish by the late Cretaceous, while stem neocoleoids such as Phragmoteuthida had already waned by the Early Jurassic.^[36]^[1]

Diversity and ecology

Species diversity

Neocoleoidea encompasses approximately 800 described species of extant cephalopods (as of 2024), predominantly distributed across the two superorders Octopodiformes and Decapodiformes.^[37] Within Octopodiformes, the order Octopoda alone accounts for over 300 species, including well-known examples such as the common octopus (Octopus vulgaris), while the order Vampyromorpha contributes a single species, the vampire squid (Vampyroteuthis infernalis).^[38] In Decapodiformes, the order Teuthida (squids) comprises around 300 species, exemplified by the Humboldt squid (Dosidicus gigas), and the order Sepiida (cuttlefish) includes about 120 species, such as the European common cuttlefish (Sepia officinalis).^[39]^[40] This distribution highlights Decapodiformes as the more speciose superorder, with approximately 500 species, compared to roughly 300 in Octopodiformes, though exact counts vary due to ongoing taxonomic revisions.^[41] Many additional species remain undescribed, particularly in deep-sea environments, where exploratory efforts have revealed numerous novel forms, such as brooding squids in the family Gonatidae and octopods in remote basins.^[42] These undescribed taxa likely number in the hundreds, underscoring the incomplete inventory of neocoleoid biodiversity in abyssal habitats, with recent discoveries (e.g., four new deep-sea octopus species in 2024) continuing to expand known diversity.^[43]^[44] Biodiversity hotspots for Neocoleoidea are concentrated in the Indo-Pacific region, particularly the Central Indo-Pacific and Java Sea ecoregions, which harbor elevated species richness for octopuses and cuttlefish due to diverse coastal and shelf environments.^[41] Squids exhibit more cosmopolitan distributions across global oceans, with peaks in the Pacific. Endemism is notable in extreme niches, including hydrothermal vents—where species like the pearl octopus (Muusoctopus spp.) are confined—and polar regions, which support specialized taxa adapted to cold, low-oxygen conditions.^[45] Conservation challenges for Neocoleoidea include overfishing, which has depleted stocks of commercially important species like the Humboldt squid (Dosidicus gigas) through targeted fisheries and bycatch.^[46] Climate change exacerbates vulnerabilities by altering ocean temperatures and acidification, impacting paralarval survival and recruitment in species such as the Humboldt squid.^[47] According to IUCN assessments, most neocoleoid species are data deficient, but notable examples include the giant Pacific octopus (Enteroctopus dofleini), listed as least concern yet facing localized declines, and several deep-sea octopods vulnerable due to habitat degradation.^[48]

Habitats and distribution

Neocoleoidea, encompassing modern coleoid cephalopods such as squids, octopuses, and cuttlefish, are ubiquitous across all marine environments worldwide, ranging from intertidal zones to the abyssal depths of the ocean floor at up to 6,957 meters, as observed for the cirrate octopus Grimpoteuthis sp. in the Indian Ocean.^[49] They occupy diverse habitats including pelagic zones where squid species form schools in the open ocean, benthic areas on coral reefs and seafloors utilized by octopuses, and demersal regions over coastal sediments preferred by cuttlefish.^[50]^[51] No neocoleoid species are known to inhabit freshwater ecosystems, likely due to physiological constraints on osmoregulation in low-salinity conditions.^[52] Key adaptations enable neocoleoids to exploit these varied niches, such as the accumulation of ammonium ions in tissues for neutral buoyancy in many squid species, allowing sustained midwater existence without energy-intensive swimming.^[53] Octopuses often den in self-constructed burrows on soft sediments or rocky crevices for protection and ambush hunting, while deep-sea species like certain squids and octopuses undertake diel vertical migrations to optimize foraging and evade predators across depth gradients.^[54]^[55] Distribution patterns of neocoleoids exhibit latitudinal gradients, with species richness peaking in tropical regions due to stable warm waters supporting complex food webs, as seen in coastal cephalopod assemblages from the western Atlantic.^[56] Many species display migratory behaviors, including ommastrephid squids that undertake seasonal migrations to specific spawning grounds influenced by ocean currents and temperature.^[57] Human activities significantly impact these distributions through commercial fisheries targeting neocoleoids in productive upwelling zones, where nutrient-rich waters enhance prey availability, and incidental bycatch in demersal trawling operations that capture non-target individuals.^[58]^[59]

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The IUCN Red List is updated. For each Red List update, IUCN provides summaries of the numbers of species in each category, by taxonomic group and by country.An Expanding Red List... · Table 7: Species Changing... · Table 8: Endemic Species By...Missing: overfishing | Show results with:overfishing
[48]
First in situ observation of Cephalopoda at hadal depths (Octopoda
May 26, 2020 · The demersal cirrate octopod Grimpoteuthis sp. was observed at both 5760 and 6957 m in the Indian Ocean. These observations extend the known ...
[49]
A multi-gene phylogeny of Cephalopoda supports convergent ...
Jul 28, 2012 · Modern cephalopods occupy nearly every habitat of the marine environment from the rocky intertidal to the deep sea, making them an excellent ...Missing: Neocoleoidea | Show results with:Neocoleoidea<|control11|><|separator|>
[50]
Common cuttlefish (Sepia officinalis) - MarLIN
It is a demersal species and prefers moderately warm, shallow coastal waters as well as continental shelves. Depth range. 0-200 m. Identifying features. They ...
[51]
Are there any freshwater cephalopods? › Ask an Expert (ABC Science)
Jan 16, 2013 · "While we can't be 100 per cent certain, it's unlikely that there have ever been freshwater cephalopods," says cephalopod expert and Head of ...
[52]
Ammonium content and buoyancy in midwater cephalopods
The majority of squid families (Teuthoidea: Cephalopoda) exchange sodium for ammonium, creating a low-density fluid that imparts lift for neutral buoyancy.
[53]
Den ecology of <i>Octopus vulgaris</i> Cuvier, 1797, on soft sediment
Mar 30, 2004 · Common octopus settled in human-altered Mediterranean coastal waters: from individual home range to population dynamics. ICES Journal of Marine ...<|control11|><|separator|>
[54]
Vertical Distribution Patterns of Cephalopods in the Northern Gulf of ...
Feb 20, 2020 · Vertical distribution and migration patterns (both diel and ontogenic) are not known for the majority of deep-water cephalopods. These varying ...
[55]
[PDF] Ecological biogeography of cephalopod molluscs in the Atlantic Ocean
Here we undertake a comprehensive survey of the latitudinal gradients of species richness (LGSR) of coastal cephalopod fauna in the western (WA) and eastern ...
[56]
Transport of the ommastrephid squid Todarodes pacificus under ...
T. pacificus, an oceanic ommastrephid squid, migrates seasonally off Japan between its southern spawning grounds and northern feeding grounds (Okutani, 1983).
[57]
Full article: World Squid Fisheries - Taylor & Francis Online
Jun 9, 2015 · A variety of ecosystems, including continental shelves, major currents and upwelling zones, gulfs, seas, and open oceans were evaluated.
[58]
Assessing Cephalopods Fisheries in the Strait of Sicily by Using ...
Nov 24, 2021 · Bottom trawl fisheries regard cephalopods as a valuable bycatch, whereas for SSF, they are among the main target species. Cephalopods account ...