Metadata

Typhlogobius californiensis

Steindachner 1879

Typhlogobius californiensis
Typhlogobius californiensis. Drawing by Leonardo Alannis. Click it for a much better view
ORDERSUB-ORDERFAMILY
GobiiformesGobioideiGobiidae

Note

As described below, Typhlogobius californiensis lives in a perpetual obligate relationship with a crustacean host with which it shares a burrow for most of its life, and in the wild it appears to be unable to live except in this symbiotic state. In captivity, with good conditions and sufficient food supplied, it can live without the host as shown by MacGinitie (1939). The host is so critical that it is also covered in detail in the following account.

The crustacean host of Typhlogobius californiensis was described as a new species, Callianassa affinis Holmes 1900, to differentiate if from another species, Callianassa californiensis Dana 1854, found in the same area. During research on the genus Callianassa for a Ph.D. thesis Biffar (1972) discovered that Callianassa affinis Holmes 1900 is a junior primary homonym of Callianassa affinis A. Milne Edwards 1860, which is a fossil species from the Lutetian of central France. To solve his immediate problem Biffar (1972) referred to the species as “Callianassa sp. A, new name”. No new name was forthcoming until Holthuis (1991) provided Callianassa biffari Holthuis 1991. In the same year, during the revision of the American Callianassidae, Manning and Felder (1991) errected the genus Neotrypaea to contain four American species (plus four others) which they deemed were not in the genus Callianassa. So the crustacean host is now called Neotrypaea biffari (Holthuis 1991) Manning and Felder 1991. [The citing of revising authors, in this case Manning and Fleder, after the bracketed original author is not common practice in zoological literature but is allowed by Recommendation 51G of the International Code of Zoological Nomencalture].

Over the c.120 years since its description the Crustacean host of Typhlogobius has been known by numerous names. The following list, which does not pretend to be complete, gives some of them.

Callianassa affinis by MacGinitie (1939), Zander (2012), Callianassa biffari by Ahnelt and Scattolin (2003), Thalianassa californiensis by Van Tassell (2011) Neotrypaea affinis by Ellingson et al. (2014), Trypaea biffari (superseded recombination)

Synonyms

Othonops eos  Smith 1881

Country

USA: marine

Types

Only a Holotype was assigned: NMW 31175 50.2mm SL.

Distribution

Southern californian coast (USA), Santa Cruz Island (N) to San Diego (S) (Ahnelt and Scatolin 2003)

Baja california (Mexico) (Eschmeyer and Herald 1983)

Cabrillo National Monument, San Diego, California (Craig and Pondella 2006)

Todos Santos Bay B.C., Mexico (Ruiz-Campos and Hammann 1987)

Ensenada norte de San Simeon Poim, CA. E.U.A. a la Bahfa Magdalena, B.C. Sur, Mexico (Miller and Lea 1972)

Habitat

The relationship between the fish and crustacean host is usually referred to as either a symbiotic relationship or a commensal realtionship (e.g. McCosker 2006), with the following definitions of these terms being:

Symbiosis – A mutually beneficial partnership betweem organisms of different kinds (Chambers Dictionary 2008).

Commensalism – An organism living in partnership or association with another of a different species without affecting or benefiting it (Chamber Dictionary 2008).

It seems clear that, if we accept that the fish gains shelter while the crustacean is neither advantaged or disadvantages by the presence of two fishes in its burrow, we cannot consider it to be symbiosis. It also seems clear that we could use the term commensalism for this situation.

However, there are other terms available that allow a more refined and precise definition of how the two species involved are interrelating.

The term inquilinism (inquiline) is defined as:

Living in the home of, or in close association, of another (Chambers Dictionary 2008), or

The residence of individuals of one species within the nest of another species (Blackwelder and Garoian 1986:469), with the addition of three separate subterms which better define the nature of the association:

Symphile – Welcome guests that make some return to their host

Synechthran – Scavangers or predators tolerated or unsuccessfully challenged in the nest

Synoekete – Indifferently tolerated guests

It is clear that the relationship is not synechthran but it may be either of the other two. Although MacGinitie (1939), the principal authority on these animals, suggests that the fish make no return to the shrimps, he himself gives two examples which are clear, if small scale and possibly insignificant, assistances:

"Though, as has been stated before, the gobies will on occasion attempt to repel the invasion of other burrowing animals which may encroach upon their tunnels, they are not sufficiently aggressive to meet with much success in keeping out other animals. It is their hosts are ever on the alert to repel such invasions." (MacGinitie 1939:492,494).

"The clearing from the burrow of many of the larger particles of food is, so far as I have been able to determine, the only possible benefit that Callianassa may derive from the presence of the blind gobies, that is, the fish by their omnivorous habits clean up most of the material which enters the burrow and is not used as food by the shrimp." (MacGinitie 1939:494).

The latter point is also made by Karplus (2014), a significant authority on symbiotic relationships:

"MacGinitie (1939) often observed C. affinis carrying relative large pieces of organic matter, too large for the shrimp to ingest, and dumping them in front of the fish. The goby which ingested these particles acted as a sanitarian, saving the shrimp the necessity of dumping that material at the burrow entrance. This may be the only activity of the goby that benefits the shrimp, since the fish’s ability to expel intruders is, according to MacGinitie (1939), far below that of the shrimp." (Karplus 2014:312-313).

So the alternative we need to choose between are:

* No return from fish to crustacean the fish is a synoeketic inquiline

* With return from fish to crustacea the fish is a symphilic inquiline.

If we allow the above examples as assistances, even if of not that much help, then certainly the second of these terms is the better one to use. And it is certainly possible that there are other subtle and/or infrequent acts of return which MacGinitie missed, and since his time no-one else has studied this fish in any detail at all.

Systematics

Probably now most realistically placed in the Family Oxudercidae (a synonym of this, which will also be used in some sources, is Gobionellidae) (Nelson et al. 2016).

Thacker (2003): Within the expanded monophyletic gobionelline clade, two smaller clades are present: one containing both Mugilogobius x, Mugilogobius, Gillichthys mirabilis, Typhlogobius californiensis, C. annularis, E. newberryi, A. flavimanus, G. semivestita, P. lidwilli, and the kraemeriid K. cunicularia (clade IIA).

Chakrabarty et al. (2012) show that the nearest relative to T. californiensis (anong the species they tested) is Gillichthys mirabilis. Interestingly both of these species have additional breathing capillaries in the skin and operculum (Zander 2012).

Agorreta et al. (2013) found that Lethops connectens was sister species to a group containing Clevelandia ios, Eucyclogobius newberryi and Lepidogobius lepidus, and that Typhlogobius californiensis was sister to a group of these four. These specie are all in the Acanthogobius lineage of Agorreta et al. (2013).

Biological Notes

This species lives in burrows created by the Ghost Shrimp Neotrypaea biffari (Holthuis 1991) (Crustacea: Decapoda: Callianassidae) ; see below for a number of other names that have been used in the past). The first person to describe the relationship between Typhlogobius and the Crustacean appears to be Eigenmann (1917:175) where he says: "Under the boulders a crawfish-like crustacean has its burrows, and in these burrows lives a blindfish, Typhlogobius Californiensis." Hubbs (1927:287) says: "[Typhlogobius lives] in a most definite situation: namely, beneath stones, in the thus darkened burrows of a peculiar crustacean." It is not until the major study by MacGinitie (1939:489) that we get any idea what this crustacean is when he says: "This goby has lived so long in a burrow under the rocks with Callianassa aftinis Holmes, a shrimp that, like many other fish living in similar circumstances, it is, in the adult sta!ges, both blind and pink, having lost eyes and pigment." and he goes on to provide a detailed account of the habitat shared by the shrimp and the fish.

It is worth quoting Packard on some aspects of the biology of Typhlogobius:

"In his essay on the Fishes of San Diego, Professor Eigenmann briefly refers to and gives four figures (P1. XXIV) of the embryo of Typhlogobius, Mr C. L. Bragg having been fortunate enough to discover the egg in the summer of 1891. "The eyes develop normally, and those of Fig. 4 differ in no way from the eyes of other fish embryos." In this case, then, we have the simplest and clearest possible proof of the descent of this blind fish from individuals with eyes as perfect as those of its congeners. We have been permitted by the Director of the United States National Museum to reproduce Professor Eigenmanns excellent figures on the embryo, which tell the story of degeneration of the eye from simple disease of the organ, the species being exposed to conditions of life strikingly different from those of its family living in the same bay. Before the discovery of the eggs, the youngest individual ever seen is represented in PI. XXIII, fig. 7, its eyes being though small, yet distinct, and "apparently functional." Packard (1894)

Conservation Status

MG [NE]

Museum Holdings

UCLA W 62-92 (cove north of San Simeon Point, identifier unknown, specimen pending accession at SIO, pers. comm. HJ Walker, Oct 2017) (Burton and Lea 2019).

USNM 27466 (I), USNM 34746 (4) (Birdsong et al. 1988)

SIO-87-26 N = 1 (Campos and Hammann ????)

Internet Resources

Genbank sequences for Typhlogobius

Smithsonian Institution specimen

AF391345 (Thacker 2003)

AF391417 (Thacker 2003)

AF391489 (Thaker 2003)

EU380932.1 (Thacker 2009)

EU450653.1 Unpublished. Gruenthal,K.M., Ellison,C.K., Tat,C.A., Walker,H.J., Hastings,P.A. and Burton,R.S.

DQ132488.1 Unpublished. Byrne,R.J., Walker,H.J., Hastings,P.A. and Burton,R.S.

GU440562.1 Unpublished. Hastings,P. and Burton,R.

Key References

The most critical sources of information on Typhlogobius are as follows:

Eigenmann (1890) - The Point Loma blind fish and its relatives

Ritter (1893) - On the eyes, integumentary sense papillae, and the integument of the San Diego blind fish (Typhlogobius californiensis Steindachner)

Eigenmann (1909) - Cave vertebrates of America, a study in degenerative evolution

Hubbs (1927) - The origin of the blind goby of the California reefs

MacGinitie (1939) - The natural history of the blind goby, Typhlogobius californiensis Steindachner. THE most important source

Coonfield (1942) - Development and reactions of melanophores of embryos and larvae of Typhlogobius californiensis Steindachner

Scheich et al. (1972) - Capillary dilatation in response to hypoxia In the brain of a gobiid fish

Congleton (1974) - The respiratory response to asphyxia of Typhlogobius californiensis (Teleostei: Gobiidae) and some related gobies

McNulty (1978) - A light and electron microscopic study of the pineal in the blind goby, Typhlogobius californiensis (Pisces: Gobiidae)

Ahnelt and Scattolin (2003) - The lateral line system of a blind goby, Typhlogobius californiensis Steindachner, 1879 (Teleostei: Gobiidae)

Ellingson (2012) - Phylogenetics and phylogeography of North Pacific bay gobies: adaptive convergence, relictual endemism, and climate-driven population structure

Ellingson et al. (2014) - Convergent evolution of ecomorphological adaptations in geographically isolated Bay gobies (Teleostei: Gobionellidae) of the temperate North Pacific

Karplus (2014) - Symbiosis in fishes: The biology of interspecific partnerships

All references

Steindachner, F Journal Article 1879 Ichthyologische Beiträge (VIII)
Smith, R. Journal Article 1881 Description of a new gobioid fish (Othonops eos), from San Diego, California
Packard, A. S. Book 1888 The cave fauna of North America, with remarks on the anatomy of the brain and origin of the blind species
Eigenmann, R.S. Journal Article 1890 Note on Typhlogobius californiensis
Eigenmann, C.H. Journal Article 1890 The Point Loma blind fish and its relations
Eigenmann, C.H. Journal Article 1892 The Fishes of San Diego
Ritter, W. E. Journal Article 1893 On the eyes, integumentary sense papillae, and the integument of the San Diego blind fish (Typhlogobius californiensis Steindachner)
Packard, A.S. Journal Article 1894 On the origin of the subterranean fauna of North America
Holmes, S.J. Journal Article 1900 Synopsis of California stalk-eyed Crustacea
Eigenmann, C.H. Book 1909 Cave vertebrates of America, a study in degenerative evolution
Eigenmann, C. H. Journal Article 1917 The homes of blind fishes
Hubbs, C.L. Journal Article 1926 Notes on the gobioid fishes of California, with descriptions of two new genera
Hubbs, C.L. Journal Article 1927 The origin of the blind goby of the California reefs.
Whitley, G.P. Journal Article 1935 Studies in ichthyology. No. 9
MacGinitie, G.E. Journal Article 1937 Notes on the natural history of several marine Crustacea
MacGinitie, G.E. Journal Article 1938 Notes on the natural history of some marine animals
Lebour, M.V. Journal Article 1938 The newly-hached larva of Callianassa affinis Holmes
Noble, E.R. Journal Article 1939 Myxosporidia from tide pool fishes of California
MacGinitie, G.E. Journal Article 1939 The natural history of the blind goby, Typhlogobius californiensis Steindachner
Noble, E.R. Journal Article 1941 On distribution relationships between California tide pool fishes and their Myxosporidian (Protozoan) parasites
Coonfield, B.R. Journal Article 1942 Development and reactions of melanophores of embryos and larvae of Typhlogobius californiensis Steindachner
MacGinitie, G.E., and MacGinitie, N. Book 1949 Natural history of marine animals
Anonymous Journal Article 1950 Blind fish in California
Laird, M. Journal Article 1953 The Protozoa of New Zealand intertidal zone fishes
Dearolf, K. Journal Article 1956 Survey of North American cave vertebrates
Dotu, Y. and Fujita, S. Journal Article 1963 The nesting behavior, egg development and larva of the gobiid Fish, Lubricogobius exiguus Tanaka
Breder, C. M. and Rosen, D. R. Book 1966 Modes of reproduction in fishes
Luling, K.H. Journal Article 1970 Uber die lebensweise des “Point-Loma- Blindfisches” (Typhlogobius californiensis) und seiner Verwandten
Macdonald, C.K. Thesis 1972 Aspects of the life history of the arrow goby, Clevelandia ios (Jordan and Gilbert), in Anaheim Bay, California, with comments on the cephalic-lateralis system in the fish family Gobiidae
Biffar, T.A. Thesis 1972 A study of the eastern Pacific representatives of the genus Callianassa (Crustacea, Decapoda, Callianassidae)
Hinegardner, R. and Rosen, D.E. Journal Article 1972 Cellular DNA Content and the evolution of teleostean fishes
Scheich, H., Honegger, H.W., Warrell, D.A. and Kennedy, G. Journal Article 1972 Capillary dilatation in response to hypoxia In the brain of a gobiid fish
Miller, D.J. and Lea, R.N. Journal Article 1972 Guide to the coastal marine fishes of California
Congleton, J.L. Journal Article 1974 The respiratory response to asphyxia of Typhlogobius californiensis (Teleostei: Gobiidae) and some related gobies
McNulty, J.A. Journal Article 1978 A light and electron microscopic study of the pineal in the blind goby, Typhlogobius californiensis (Pisces: Gobiidae).
Haig, J. and Abbott, D.P. Book Section 1980 Macrura and Anomura: The Ghost Shrimps, Hermit Crabs and allies
Hoffman, C.J. Thesis 1980 Associative behavior of the Arrow Goby, Clevelandia ios (Jordan and Gilbert) and the Ghost Shrimp, Calliaassa californiensis Dana
Hoffman, C.J. Journal Article 1981 Associations between the Arrow Goby Clevelandia ios (Jordan and Gilbert) and the Ghost Shrimp Callianassa californiensis Dana in natural and artificial burrows
Eschmeyer, W.N. and Herald, E.S. Book 1983 A field guide to Pacific Coast fishes of North America from the Gulf of Alaska to Baja California
Ruiz-Campos, G. and Hammann, M.G. Journal Article 1987 A species list of the rocky intertidal fishes of Todos Santos bay, Baja California, Mexico
Birdsong, R.S., Murdy, E.O. and Pezold, F. Journal Article 1988 A study of the vertebral column and median fin osteology in gobioid fishes with comments on gobioid relationships.
Holthuis, L.B. Journal Article 1991 Marine lobsters of the world. An annotated and illustrated catalogue of species of interest to fisheries known to date
Manning, R.B. and Felder, D.L. Journal Article 1991 Revision of the American Callianassidae (Crustacea: Decapoda: Thalassinidea)
Thacker, C.E. Journal Article 2003 Molecular phylogeny of the gobioid fishes (Teleostei: Perciformes: Gobioidei)
Ahnelt, H. and Scattolin, G. Journal Article 2003 The lateral line system of a blind goby, Typhlogobius californiensis Steindachner, 1879 (Teleostei: Gobiidae)
Sakai, K. Journal Article 2005 Callianassoidea of the World (Decapoda, Thalassinidea)
McCosker, J.E. Book Section 2006 Symbiotic relationships
Craig, M.T. and Pondella, D.J. Journal Article 2006 A survey of the fishes of the Cabrillo National Monument, San Diego, California
Wirtz, P. Journal Article 2008 The Gulf of Guinea goby‐shrimp symbiosis and a review of goby‐thalassinidean associations
Kneer, D., Asmus, H., Ahnelt, H. and Vonk, J.A. Journal Article 2008 Records of Austrolethops wardi Whitley (Teleostei: Gobiidae) as an inhabitant of burrows of the thalassinid shrimp Neaxius acanthus in tropical seagrass beds of the Spermonde Archipelago, Sulawesi, Indonesia
Liu, H.T.H., Kneer, D., Asmus, H. and Ahnelt, H. Journal Article 2008 The feeding habits of Austrolethops wardi, a gobiid fish inhabiting burrows of the thalassinidean shrimp Neaxius acanthus
Campos, E., De Campos, A.R. and Manriquez, I. Journal Article 2009 Intertidal Thalassinidean shrimps (Thalassinidea, Callianassidae and upogebiidae) of the west coast of Baja California, Mexico: annotated checklist, key for identification, and symbionts
Van Tassell, J.L. Journal Article 2011 Gobiiformes of the Americas
Zander, C.D. Book Section 2012 Gobies as predator and prey
Zander, C.D. Book Section 2012 Morphological adaptations to special environments of gobies
Chakrabarty, P., Davis, M.P. and Sparks, J.S. Journal Article 2012 The first record of a trans-oceanic sister-group relationship between obligate vertebrate troglobites
Ellingson, R.A. Thesis 2012 Phylogenetics and phylogeography of North Pacific bay gobies: adaptive convergence, relictual endemism, and climate-driven population structure
Agorreta, A., San Mauro, D., Schliewen, U., Van Tassell, J.L., Kovacic, M., Zardoy, R. and Rüber, L. Journal Article 2013 Molecular phylogenetics of Gobioidei and phylogenetic placement of European gobies
Ellingson, R.A., Swift, C.C., Findley, L.T. and Jacobs, D.K. Journal Article 2014 Convergent evolution of ecomorphological adaptations in geographically isolated Bay gobies (Teleostei: Gobionellidae) of the temperate North Pacific
Karplus, I. Book 2014 Symbiosis in fishes: The biology of interspecific partnerships
Poore, G.C.B., Dworschak, P.C.,Robles, R., Mantelatto, F. and Felder, D.L. Journal Article 2019 A new classification of Callianassidae and related families (Crustacea: Decapoda: Axiidea) derived from a molecular phylogeny with morphological support
Burton, E.J. and Lea, R.N. Journal Article 2019 Annotated checklist of fishes from Monterey Bay National Marine Sanctuary with notes on extralimital species
Point Loma, California. Under the rocks are burrows of a shrimp in which live Typhlogobius californiensis (from Eigenmann 1917)
Blind-fish rocks at base of Point Loma, San Diego, California. Photograph from Eigenmann 1909
Juvenile (above) with eyes and adult (below) without. From Eigenmann 1926
George E. MacGinitie, 4th May 1889-9th June 1989, who is, so far, the only person to have studied in detail the biology and life history of Typhlogobius californiensis