Tetraodontidae

Reconstruction of Eotetraodon pygmaeus, copyright Apokryltaros.

Belongs within: Tetraodontiformes.
Contains: Takifugu, Canthigaster, Sphoeroides, Tetraodon, Arothron.

In a pufferfish’s garden
Published 9 January 2015
Bullseye puffer Sphoeroides annulatus, copyright Geoffrey W. Schultz.

I don’t know if it applies in other parts of the world, but one animal that you are guaranteed to see in the estuary here in Perth is pufferfish. One of the most instantly recognisable fish families, pufferfish (Tetraodontidae) are of course famed for their high toxicity, the determination of some people to eat them despite aforementioned toxicity, and their habit of swallowing air or water when threatened to inflate their distendible bellies. That last feature makes them a favourite of children (or at least of yours truly as a child), because their slow swimming style makes them one of the few fish that can be easily captured by hand (you just have to make sure you don’t allow the fish to give you a nasty bite with their beak). The first feature makes them a lot less popular with fishermen who have to experience the frustration of reeling in a line to find that the bait has been taken by a puffer, then trying to remove the puffer from the hook while avoiding the aforementioned beak.

Oceanic puffer Lagocephalus lagocephalus, from Baino96.

There are a little under 200 known pufferfish species worldwide. Most of them are found in coastal marine and brackish waters, but there are also several species found in fresh water in South America, Africa and southeast Asia. Some marine species are also resistant to fresh water and may spend extended periods away from the sea. Some southeast Asian brackish-water Tetraodon species even make regular appearances in the the aquarium trade labelled as ‘freshwater’ puffers (Yamanoue et al. 2011), though their long-term survival requires more appropriate water conditions. The toxin associated with pufferfishes is not produced by the fish itself, but accumulated through its diet. As such, the exact level of toxicity of a pufferfish may vary according to season.

Grass puffer Takifugu niphobles, copyright OpenCage.

A molecular phylogenetic analysis of pufferfish by Yamanoue et al. (2011) identified four main clades in the family. These clades were also supported by a subsequent analysis by Santini et al. (2013), though the deeper relationships between the clades differed between the analyses. Yamanoue et al. (2011) identified a small number of freshwater clades (only one for each continent with freshwater taxa) and inferred that the transition from marine to fresh water had happened only rarely. Santini et al. (2013), in contrast, supported a higher number of transitions in tetraodontid history, though at least some of the difference between the two studies can be explained by differing definitions of ‘freshwater’. For instance, some species of Takifugu usually live in brackish water but spawn in fresh water; Santini et al. counted these as freshwater species, but Yamanoue et al. did not.

Papuan toby Canthigaster papua, photographed by Dwayne Meadows.

One of the major clades identified within the Tetraodontidae includes the genus Lagocephalus, a group of relatively long-bodied puffers including some of the few pelagic puffer species. This genus may be the sister taxon of the remaining puffers (as found by Yamanoue et al.), or it may have a more nested position as sister to a clade including the mostly West Atlantic-East Pacific genera Sphoeroides and Colomesus (as found by Santini et al.). This latter clade includes South America’s only freshwater puffer, the Amazon species Colomesus asellus. Santini et al. identified the basalmost tetraodontid clade as an Indo-West Pacific assemblage including the genus Takifugu and related taxa, which Yamanoue et al. had found as sister to the final clade including taxa related to the genus Tetraodon. This last clade includes the African and southeast Asian freshwater puffers (except for a few members of the Takifugu clade that cross into fresh water at times). It also includes the genus Canthigaster, the sharpnose pufferfish. In contrast to the more or less globular form of all other puffers, sharpnose puffers have a laterally compressed body form that superficially looks a bit more like a triggerfish than a puffer. Most Canthigaster species are reef-dwellers, a somewhat unusual habitat for a puffer (the other main group of reef-dwelling puffers being the genus Arothron, also in the Tetraodon clade).

Circular underwater ‘nest’ constructed by a pufferfish, from Spoon & Tamago.

One of the most remarkable characteristics of any puffer, though, was not discovered until quite recently. In 2012, it was announced that large structures observed off the coast of Japan by underwater photographer Yoji Ookata were in fact the work of pufferfish. These structures, circular and regular geometric patterns in the sea bed about 1.5 metres in diameter, were made by male puffers swimming against the sand. The structures are believed to function in attracting females, and also function as nests in which the females lay their eggs. Rather frustratingly, I haven’t found any indication exactly which species of puffer is involved!

Puffer in the process of building a nest, also from Spoon & Tamago.
Systematics of Tetraodontidae
<==Tetraodontidae
    |--Eotetraodon pygmaeus (de Zigno 1887)AS09, P93
    `--+--CanthigasterND13
       `--+--SphoeroidesND13
          `--+--TetraodonND13
             `--ArothronND13
Tetraodontidae incertae sedis:
  Ephippion Bibron in Duméril 1855M15
    `--E. guttiferEA03
  Amblyrhynchote Bibron in Duméril 1855 [=Amblyrhynchotes (l. c.)]M15
    `--A. hypselogenion (Bleeker 1852) [=Tetrodon hypselogenion]M58
  Torquigener Whitley 1930M15
    |--T. albomaculosus Matsuura 1914M15
    |--T. flavomaculosus Hardy & Randall 1983M15
    |--T. gloerfelti Hardy 1984M15
    |--T. marleyi (Fowler 1929) [=Sphoeroides marleyi; incl. T. balteus Hardy 1989]M15
    |--T. meraukensis (de Beaufort 1955) [=Sphoeroides meraukensis]M58
    |--T. pleurogramma (Regan 1903) [=Tetrodon pleurogramma]M58
    |--T. pleurostictus (Günther 1871) [=Tetrodon pleurostictus; incl. Te. fasciatus Weber 1908]M58
    `--T. randalli Hardy 1983M15
  Lagocephalus Swainson 1839 [Lagocephalidae]M15
    |--L. gloveri Abe & Tabeta 1983M15
    |--L. guentheri (Miranda Ribeiro 1915)M15
    |--L. inermisM15
    |--L. laevigatus (Linnaeus 1766)M15
    |--L. lagocephalus (Linnaeus 1758)LD09
    |--L. lunaris (Bloch & Schneider 1801)PC01
    `--L. spadiceus (Richardson 1845) [incl. L. wheeleri Abe et al. 1984]M15
  TakifuguM15
  Auriglobus Kottelat 1999M15
  Carinotetraodon Benl 1957M15
    |--C. lorteti (Tirant 1885) [incl. *C. chlupatyi Dekkers 1975]M15
    |--C. imitator Britz & Kottelat 1999M15
    |--C. irrubesco Tan 1999M15
    `--C. salivator Lim & Kottelat 1995M15
  Chelonodontops Smith 1958M15
    |--C. pleurospilus (Regan 1919) [=Chelonodon pleurospilus; incl. *Chelonodontops pulchellus Smith 1958]M15
    |--C. laticeps (Smith 1948) [=Chelonodon laticeps]M15
    `--C. patoca (Hamilton 1822) [=Tetrodon patoca, Chelonodon patoca]M15
  Colomesus Gill 1884M15
    |--C. asellus (Müller & Troschel 1848)M15
    |--C. psittacus (Bloch & Schnedier 1801)M15
    `--C. tocantinensis Amaral et al. 2013M15
  Contusus Whitley 1947M15
    `--C. brevicaudus Hardy 1981M15
  Dichotomyctere Duméril 1855M15
    |--D. erythrotaenia (Bleeker 1853)M15 [=Tetraodon erythrotaeniaM15, Monotretus erythrotaeniaM58]
    |--D. fluviatilis (Hamilton 1822) [=Tetraodon fluviatilis]M15
    |--D. kretamensis (Inger 1953)M15
    |--D. nigroviridis (Marion de Procé 1822) [=Tetraodon nigroviridis]M15
    |--D. ocellatus (Steindachner 1870)M15
    `--D. sabahensis (Dekkers 1975)M15
  Feroxodon Su, Hardy & Tyler 1986M15
    `--*F. multistriatus (Richardson 1854) [=Anchisomus multistriatus]M15
  Guentheridia Gilbert & Starks 1904M15
  Javichthys Hardy 1985M15
    `--*J. kailolae Hardy 1985M15
  Leiodon Swainson 1839 [=Chelonodon Müller 1841]M15
    `--L. cutcutia (Hamilton 1822) [=Tetrodon cutcutia, *Chelonodon cutcutia]M15
  Marilyna Hardy 1982M15
    |--M. darwinii (Castelnau 1873)MM14
    |--M. meraukensis (De Beaufort 1955)MM14
    `--M. pleurosticta (Günther 1872)MM14
  Omegophora Whitley 1934M15
    `--O. cyanopunctata Hardy & Hutchins 1981M15
  Pao Kottelat 2013M15
    |--*P. leiurus (Bleeker 1850) [=Tetraodon leiurus]M15
    `--P. palustris (Saenjudaeng et al. 2013) [=Tetraodon palustris]M15
  Pelagocephalus Tyler & Paxton 1979M15
    |--*P. coheni Tyler & Paxton 1979M15
    `--P. marki Heemstra & Smith 1981M15
  Polyspina Hardy 1983M15
    `--P. piosae Whitley 1955BR90
  Reicheltia Hardy 1982M15
  Tetractenos Hardy 1983M15
    `--T. hamiltoniOC03
  Tylerius Hardy 1984M15
    `--*T. spinosissimus (Regan 1908) [=Sphoeroides spinosissimus]M15
  Chonerhinos Bleeker 1854M15
    |--C. amabilis Roberts 1982M15
    |--C. nefastus Roberts 1982M15
    `--C. silus Roberts 1982M15
  Xenoptere Bibron in Duméril 1855 [=Xenopterus (l. c.)]M15
  CheilichthysHP80
  Archaeotetraodon winterbottomiAS09

*Type species of generic name indicated

References

[AS09] Alfaro, M. E., F. Santini, C. Brock, H. Alamillo, A. Dornburg, D. L. Rabosky, G. Carnevale & L. J. Harmon. 2009. Nine exceptional radiations plus high turnover explain species diversity in jawed vertebrates. Proceedings of the National Academy of Sciences of the USA 106 (32): 13410–13414.

[BR90] Black, R., A. I. Robertson, C. H. Peterson & N. M. Peterson. 1990. Fishes and benthos of near-shore seagrass and sandflat habitats at Monkey Mia Shark Bay, Western Australia. In: Berry, P. F., S. D. Bradshaw & B. R. Wilson (eds) Research in Shark Bay: Report of the France-Australe Bicentenary Expedition Committee pp. 245–261. Western Australian Museum.

[EA03] Écoutin, J.-M., & J.-J. Albaret. 2003. Relation longueur-poids pour 52 espèces de poissons des estuaires et lagunes de l’Afrique de l’Ouest. Cybium 27 (1): 3–9.

[HP80] Holmes, J. C., & P. W. Price. 1980. Parasite communities: the roles of phylogeny and ecology. Systematic Zoology 29 (2): 203–213.

[LD09] Li, B., A. Dettaï, C. Cruaud, A. Couloux, M. Desoutter-Meniger & G. Lecointre. 2009. RNF213, a new nuclear marker for acanthomorph phylogeny. Molecular Phylogenetics and Evolution 50: 345–363.

[M15] Matsuura, K. 2015. Taxonomy and systematics of tetraodontiform fishes: a review focusing primarily on progress in the period from 1980 to 2014. Ichthyological Research 62 (1): 72–113.

[MM14] Moore, G. I., S. M. Morrison, J. B. Hutchins, G. R. Allen & A. Sampey. 2014. Kimberley marine biota. Historical data: fishes. Records of the Western Australian Museum Supplement 84: 161–206.

[M58] Munro, I. S. R. 1958. The fishes of the New Guinea region: a check-list of the fishes of New Guinea incorporating records of species collected by the Fisheries Survey Vessel “Fairwind” during the years 1948 to 1950. Papua and New Guinea Agricultural Journal 10 (4): 97–369 (reprinted: 1958. Territory of Papua and New Guinea Fisheries Bulletin no. 1).

[ND13] Near, T. J., A. Dornburg, R. I. Eytan, B. P. Keck, W. L. Smith, K. L. Kuhn, J. A. Moore, S. A. Price, F. T. Burbrink, M. Friedman & P. C. Wainwright. 2013. Phylogeny and tempo of diversification in the superradiation of spiny-rayed fishes. Proceedings of the National Academy of Sciences of the USA 110 (31): 12738–12743.

[OC03] Olson, P. D., T. H. Cribb, V. V. Tkach, R. A. Bray & D. T. J. Littlewood. 2003. Phylogeny and classification of the Digenea (Platyhelminthes: Trematoda). International Journal for Parasitology 33: 733–755.

[P93] Patterson, C. 1993. Osteichthyes: Teleostei. In: Benton, M. J. (ed.) The Fossil Record 2 pp. 621–656. Chapman & Hall: London.

[PC01] Pichelin, S., & T. H. Cribb. 2001. The status of the Diplosentidae (Acanthocephala: Palaeacanthocephala) and a new family of acanthocephalans from Australian wrasses (Pisces: Labridae). Folia Parasitologica 48: 289–303.

Santini, F., M. T. T. Nguyen, L. Sorenson, T. B. Waltzek, J. W. Lynch Alfaro, J. M. Eastman & M. E. Alfaro. 2013. Do habitat shifts drive diversification in teleost fishes? An example from the pufferfishes (Tetraodontidae). Journal of Evolutionary Biology. doi: 10.1111/jeb.12112.

Yamanoue, Y., M. Miya, H. Doi, K. Mabuchi, H. Sakai & M. Nishida. 2011. Multiple invasions into freshwater by pufferfishes (Teleostei: Tetraodontidae): a mitogenomic perspective. PLoS ONE 6 (2): e17410. doi:10.1371/journal.pone.0017410.

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