Exploration of our largely unknown oceans continues to yield fascinating biodiversity discoveries. In addition to novel forms of life (Osborn et al. 2009), chance collecting coupled with modern molecular genetic tools allow us to better understand longstanding enigmas. For over 180 years, the “monster” larva, C. monstrosa, has been such a puzzle to zoologists. This species, first discovered in the gut contents of a dolphin in 1828 (Gray 1828), is unique in its heavy armor, thick body, and exceptional horn ornamentation (Fig. 1). Nineteenth century collections of marine plankton commonly included developmental stages of crabs, shrimps, and lobsters that differed strikingly from their adult counterparts in morphology and habitat (Williamson 1915; Gurney 1939,1942; Anger 2001). Not originally identified as a larval decapod, the single specimen of C. monstrosa was described as a “monstrous and misshapen animal” and placed within a new genus and species of primitive crustacean (Leptostraca) (Gray 1828). Although many such larvae have been subsequently linked to adult forms, C. monstrosa has eluded definitive placement despite nearly two centuries of effort due to its scarcity and extreme morphological uniqueness.
Cerataspis monstrosa is encountered only rarely in the wild with most information on this species coming from studies of gut contents of its predators, including skipjack (Katsuonus pelamis), yellowfin (Thunnus albacares) and blackfin (T. atlanticus) tuna, and dolphin (Coryphaena hippurus) (Morgan et al. 1985). Interpretations of its unusual morphology have to date suggested it might represent the larval counterpart of some abyssal adult, the proposed candidates being a yet-to-be discovered shrimp from the family Aristeidae (Penaeoidea), or perhaps even a more distant relative of penaeoids (Heegaard 1966a; Osborn et al. 2009; Hubert et al. 2010). Wild-caught planktonic larvae are often collected and reared to early postlarval stages in order to determine their adult identities (Gurney 1942; Rice and Williamson 1970). However, in the case of deep oceanic species, with highly metamorphic development involving striking vertical migrations between near-surface and deep-ocean waters, rearing protocols seldom succeed. In these instances, DNA data provide a common currency for comparison (Webb et al. 2006; Ahrens et al. 2007; Burns et al. 2008; Hubert et al. 2010).
Recently, mid-water oceanic collections in the northern Gulf of Mexico unexpectedly included a single specimen of C. monstrosa suitable for genetic analyses. We collected DNA sequence data from this specimen to compare to data in our extensive database of decapod crustacean DNA sequences (http://decapoda.nhm.org/, Table 1). Taxon selection was based on previous studies that suggested a relationship between Cerataspis and shrimp-like decapods. By the late nineteenth century, an affinity between Cerataspis to penaeoid shrimp had been proposed (Dohrn 1871; Giard and Bonnier 1892; Heegaard 1966b), and by the early twentieth century, new observations suggested this peculiar form represented a protracted pelagic larval stage of the family Aristeidae (Bouvier 1908). As previous studies suggested an affinity between Cerataspis and penaeoid shrimp, and more specifically the family Aristeidae, we sampled heavily within these groups (Boas 1880; Giard and Bonnier 1892; Bouvier 1908; Burkenroad 1934).
|Euphausiacea Dana, 1852|
|Euphausiidae Dana, 1852|
|Stenopodidea Claus, 1872|
|Stenopodidae Claus, 1872|
|Stenopus hispidus (Olivier, 1811)||KC4276||JX403879||JX403856||FJ943443||FJ943450||FJ943457|
|Caridea Dana, 1852|
|Procarididae Chace & Manning, 1972|
|Chace & Manning 1972||KC4274||JX403877||GQ487495||GQ487503||GQ487511||GQ487521|
|Atyidae de Haan, 1849|
|Hippolytidae Dana, 1852|
|Latreutes fucorum (Fabricius, 1798)||ULLZ9135||JX403873||EU868664||EU868755||JX403816||JX403896|
|Ogyrididae Holthuis, 1955|
|Ogyrides nr. alphaerostris||ULLZ7755||JX403875||EU868679||EU868772||JX403818||JX403898|
|Penaeoidea Rafinesque-Schmaltz, 1815|
|Aristeidae Wood-Mason, 1891|
|Aristaeomorpha foliacea (Risso, 1827)||KC4280||JX403863||GQ487491||GQ487500||GQ487508||GQ487517|
|Aristaeopsis edwardsiana (Johnson, 1868)||ULLZ7726||JX403872||JX403854||JX403836||JX403815||JX403895|
|Cerataspis monstrosa Gray, 1828||ULLZ11555||JX403884||JX403860||JX403842||JX403824||JX403904|
|Hemipenaeus carpenteri Wood-Mason, 1891||ULLZ8551||JX403865||JX403847||JX403829||JX403808||JX403889|
|Plesiopenaeus armatus (Bate, 1881)||ULLZ11940||JX403876||JX403855||JX403837||JX403820||JX403900|
|Benthesicymidae Wood-Mason, 1891|
|Bentheogennema intermedia (Bate, 1888)||ULLZ6701||JX403869||JX403851||JX403833||JX403812||JX403892|
|Benthesicymus bartletti Smith, 1882||ULLZ8036||JX403887||N/A||JX403845||JX403827||N/A|
|Gennadas valens (Smith, 1884)||ULLZ11476||JX403882||JX403858||JX403840||JX403822||JX403902|
|Penaeidae Rafinesque, 1815|
|Farfantepenaeus duorarum (Burkenroad, 1939)||ULLZ8365||JX403864||JX403846||JX403828||JX403807||JX403888|
|Funchalia villosa (Bouvier, 1905)||ULLZ6700||JX403870||JX403852||JX403834||JX403813||JX403893|
|Litopenaeus setiferus (Linnaeus, 1767)||ULLZ11629||JX403886||JX403862||JX403844||JX403826||JX403906|
|Litopenaeus vannamei (Boone, 1931)||KCpen||EU920908||EU920934||EU920969||EU921005/EU921006||EU921075|
|Sicyoniidae Ortmann, 1898|
|Sicyonia laevigata Stimpson, 1871||ULLZ7192||JX403868||JX403850||JX403832||JX403811||JX403907|
|Sicyonia ingentis (Burkenroad, 1938)||KC4279||JX403880||GQ487492||JX403838||N/A||GQ487518|
|Solenoceridae Wood-Mason, 1891|
|Hymenopenaeus debilis Smith, 1882||ULLZ8531||JX403866||JX403848||JX403830||JX403809||JX403890|
|Mesopenaeus tropicalis (Bouvier, 1905)||ULLZ8364||JX403867||JX403849||JX403831||JX403810||JX403891|
|Pleoticus robustus (Smith, 1885)||ULLZ10956||JX403881||JX403857||JX403839||JX403821||JX403901|
|Solenocera necopina Burkenroad, 1939||ULLZ6705||JX403871||JX403853||JX403835||JX403814||JX403894|
|Sergestoidea Dana, 1852|
|Sergestidae Dana, 1852|
|Sergia hansjacobi Vereshchaka, 1994||ULLZ11552||JX403883||JX403859||JX403841||JX403823||JX403903|
|Sergia nr. robusta||ULLZ8089||JX403878||EU868710||EU868807||GQ487509||GQ487519|
|Deosergestes corniculum (Krøyer, 1855)||ULLZ11598||JX403885||JX403861||JX403843||JX403825||JX403905|
Phylogenetic analysis (Fig. 2) places C. monstrosa as identical to the deep-sea penaeoid shrimp P. armatus (Figs. 1,3). Moreover, our sequencing efforts of 4136 basepairs over five genes (12S, 16S, 18S, 28S, H3) resulted in a near perfect (99.96%) genetic match between these two “species.” Individual gene trees were not in conflict, with 12S and 16S resolving shallow branches and 28S, 18S, and H3 resolving middle to deep branches. All genetic markers in our analysis were carefully selected to include enough variation to detect species-level differences and resolve systematic placement. Historically, these nuclear and mitochondrial markers have demonstrated their utility in decapod taxonomic, systematic, and barcoding studies (Bracken et al. 2010; Grave et al. 2010; Puillandre et al. 2011). For each gene, the level of divergence between P. armatus and C. monstrosa is considerably less (~0.049−0.18%) when compared with estimates among other congeneric decapod (~2.2−10%, Toon et al. 2009) and aristeid (~3%, pers. observation based on 16S GenBank data, JF899802, GU972651) species. We therefore conclude that P. armatus and C. monstrosa, respectively, represent adult and larval forms of the same species, and recommend both henceforth be referred to as P. armatus (see Taxonomy Note).
Larval–adult linkages allow for the advancement of understanding in ecology, systematics, and taxonomy, and in the case of C. monstrosa, both deep-sea and plankton biology. Linkages shed light on the distribution, ecology, and life history of a species. Known occurrences of C. monstrosa and adults of P. armatus overlap in geographic distribution, which further solidifies the larval–adult identification. Although the first report of C. monstrosa in the Gulf of Mexico was relatively recent (Franks and Russell 2008), the larval form appears to be circumglobally distributed in oceanic mid-water pelagic communities, near-surface plankton communities, or in association with surface rafts of Sargassum (Heegaard 1966a; Morgan et al. 1985). The reduced abdomen and armored thorax suggests that C. monstrosa has an extended pelagic life, as proposed in previous reports (Bouvier 1908). The adult counterpart, P. armatus, is of similar cosmopolitan distribution, albeit as a true abyssal species ranging widely in deep-ocean basins to depths of at least 5060 m (Gore 1985; Pérez Farfante and Kensley 1997). Specifically throughout the Gulf of Mexico, adults of P. armatus have been reported from depths of 1,764–3,600 m (Roberts and Pequegnat 1970; Crosnier and Forest 1973; Pérez Farfante and Kensley 1997; Felder and Camp 2009). Thus, linking of the adult to larval form provides novel insight into the life history of this species from a mid-water pelagic larva to an abyssal adult. This furthermore establishes the adult source population for larvae that are a common food of pelagic fishes. Findings from this study suggest a second known “species” of Cerataspis, C. petiti, is likely a larval stage of the only other known species of Plesiopenaeus (P. coruscans). Affinities of the closely related and equally bizarre “larval” species Cerataspides longiremus, first described as Cerataspis by Dohrn (1871) and placed in the genus Cerataspides by Bonnier (1899), may well be a larval stage of an unidentified member of the genus Plesiopenaeus or of another aristeid shrimp (Dohrn 1871; Bonnier 1899). Similar approaches, as applied here, can be used to confirm these larval–adult linkages once material of these rare individuals becomes available for molecular systematic studies.
Genetic techniques cross-validated with larval rearing protocols are the preferred method of identifying adult–larval linkages. However, molecular phylogenetic tools, as applied here, provide a powerful alternative to traditional approaches dependent on rearing of otherwise unidentifiable larvae. In this case, the combined application of modern DNA techniques with robust phylogenetic methodology allowed us to solve this 184-year-old mystery of the “monster larva” of the deep.