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Midshipman fish

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Midshipman fish
Temporal range: Late Miocene to Present[1]
Plainfin midshipman (Porichthys notatus)
Scientific classification
Kingdom:
Animalia
Phylum:
Chordata
Class:
Actinopterygii
Order:
Batrachoidiformes
Family:
Batrachoididae
Genus:
Porichthys

Girard, 1854
Species

See text.

Midshipman fish belong to the genus Porichthys of toadfishes. They are distinguished by having photophores (which they use to attract prey and after which they are named, reminding some of a naval uniform's buttons) and four lateral lines. Typical midshipman fishes, such as the plainfin midshipman (Porichthys notatus), are nocturnal and bury themselves in sand or mud in the intertidal zone during the day. At night they float just above the seabed. Some species have venomous dorsal spines and are capable of inflicting serious injuries if handled.

There are three genders of midshipman fish: females, type I males, and type II males. Type I and type II males have different reproductive strategies, and can be distinguished from each other based on physical characteristics. Type I males are eight times larger in body mass, and have much larger vocal organs. Type II males’ reproductive organs are seven times larger in size than those of type I males.[2] Female and type II male midshipman fish can be distinguished from each other by the female’s slightly larger size, and the type II male midshipman’s large reproductive organs.[3]

Species

Atlantic midshipman (Porichthys plectrodon)
Closeup of photophores on an Atlantic midshipman. Midshipman fish are named after their photophores.

There are currently 14 recognized species in this genus:[4]

Biology

Reproduction and vocalization

Mating in midshipman fishes depends on auditory communication. Male midshipman fish produce several different vocalizations while females only make grunts in non-breeding situations.[2]

Calling

Typical Type I male calls are divided into short grunts that last for milliseconds or are produced in a series of grunts called a “grunt train,” mid-duration growls, and long duration advertisement hums that can last up to an hour.[5] These calls can be recorded naturally. They can also be produced in a laboratory, a procedure known as “fictive calling.[3][6]” In nature, two muscles contracting on the swim bladder produce these sounds. In the laboratory, sounds are produced by a stimulating electrode placed on the periaqueductal gray (PAG) and a recording electrode placed on the occipital nerve that leads to the sonic muscles of the fish.[6][7]

Steroid mediation

The vocalizations of male midshipman fish are androgen and estradiol steroid mediated. There are high blood levels of these hormones during the transition from non-calling to calling before midshipman breeding season,[8] suggesting that higher hormone levels are needed for making advertisement calls. Feeding 11-ketotestosterone coated scallops to toadfish increases their calling behavior,[9] which identifies 11-ketotestosterone, an androgen hormone, as a mediator of midshipman fish vocalization. There are also high levels of aromatase, an estrogen-generating enzyme, in the hindbrain vocal motor region. Estradiol steroids and their receptors are present in the same areas already concluded to be involved in male midshipman calling.[10]

The three genders of midshipman fish have different steroid-mediated reproductive behaviors. Type I territorial males use vocalizations via paired muscles in the swimming bladder to attract females, while type II males invest in larger reproductive organs.[2] Type II males then “sneak” into nests because they look much like females and fertilize laid eggs. This behavior is referred to as cuckoldry or satellite-spawning.[3] Type II males and females are incapable of long duration calls.[11] 11-Ketotestosterone is the major steroid present in Type I males’ vocalization systems, while Type 2 males’ and females’ vocalizations are primarily mediated by testosterone.[12] The specific mechanisms by which these steroids act are still unknown.[10]

The sounds produced by male midshipman fish cause reproductive females to develop a hormone-mediated selective sensitivity to this sound, and they respond by laying eggs in the rock nest of a singing male. This selective sensitivity to higher frequency correlates to increased levels of testosterone and estradiol.[13]

Neuron connectivity

The neuronal pathway for midshipman vocalization starts at the ventral medullary nucleus and continues to a hindbrain vocal pattern generator, which contains both pre-pacemaker and pacemaker nuclei.[6] For each action potential fired in their vocal pattern generator, there is exactly one sonic motor neuron that fires, and there is exactly one sound pulse.[14] The two motor nuclei fire in phase in toadfish, leading to the paired contraction of the sonic muscles.[15]

The duration of calls is controlled by the pre-pacemaker neurons in the hindbrain. The duration is encoded by a long depolarization of these pre-pacemaker neurons. Exposing pacemaker neurons to different levels of the anesthetic lidocaine alters the duration of the calls, but not the frequency Pacemaker neurons code for the frequency of signals using “ultrafast” rhythmic oscillations in membrane potential. As midbrain stimulus increased, the oscillations increased in amplitude.[7]

Although midshipman fish have been known to wake houseboat owners,[16] research surrounding their vocalizations could be beneficial to humans. Midshipman fish are model organisms for studying both human speech and hearing. Recently, it was found that midshipman fish can decrease their own hearing sensitivity by stiffening their inner ear hair cells while they are vibrating their calling muscles.[17] This behavior is also found in bats, and may lead to an understanding a similar mechanism humans use to turn down their ear sensitivity to retain their hearing longer.[16] There are conserved patterns of vocal, auditory, and neuroendocrine mechanisms between teleosts and tetrapods, which include midshipman fish and humans, respectively. This model organisms’ simple system could lead to a deeper understanding of human speech and auditory pathways,.[2][7][18] This evolutionary connection could be important in modern medicine because these fish have homologous brain structures to humans. An example of which is for patients with lesions in the brain that become mute after having a stroke.[19] August 9, 1974 composer Charlie Morrow performed a concert for fish using what he understood to be decoded toadfish language, similar to his decoded field peeper language. Morrow's observed that choruses of multiple toadfish are have shifting leadership for call and response by strong individuals. He notated the patterns for human performance, in one version numbering each individual for identification and spatial location. The night before, Richard Nixon resigned as U.S. president. Major media covered the concert. New York Times music critic, John Rockwell, wrote a review with the headline, "Fish Silent".

References

  1. ^ Sepkoski, Jack (2002). "A compendium of fossil marine animal genera". Bulletins of American Paleontology. 364: 560. Retrieved 2008-01-08. {{cite journal}}: Cite has empty unknown parameter: |coauthors= (help)
  2. ^ a b c d Brantley RK and Bass AH. 1994. Alternative male spawning tactics and acoustic signaling in the plainfin midshipman fish, Porichthys notatus. Ethology 96: 213-232.
  3. ^ a b c Lee SFL and Bass AH. 2006. Dimorphic male midshipman fish: reduced sexual selection or sexual selection for reduced characters? Behavioral Ecology 17(4): 670-675.
  4. ^ Froese, Rainer; Pauly, Daniel (eds.). "Species in genus Porichthys". FishBase. April 2012 version.
  5. ^ Rubow TK and Bass AH. 2009. Reproductive and diurnal rhythms regulate vocal motor plasticity in a teleost fish. The Journal of Experimental Biology 212: 3252-3262.
  6. ^ a b c Bass AH and Baker R. 1997. Phenotypic specification of hindbrain rhombormeres and the origins of rhythmic circuits in vertebrates. Brain, Behavior, and Evolution '50: 3–16.
  7. ^ a b c Chagnaud BP, Baker R, and Bass AH. 2011. Vocalization frequency and duration are coded in separate hindbrain nuclei. Nature Communications 2: 346.
  8. ^ Reamage-Healey L and Bass AH. 2005. Rapid elevations in both steroid hormones and vocal signaling during playback challenge: a field experiment in gulf toadfish. Hormonal Behavior 47(3): 297–305.
  9. ^ Remage-Healey L and Bass AH. 2006. From social behavior to neurons: steroid hormones in the control of reproductive behavior. Brain Research 1126: 27–35.
  10. ^ a b Forlano PM, Dietcher DL, and Bass AH. 2005. Distribution of estrogen receptor alpha mRNA in the brain and inner ear of a vocal fish with comparison to sites of aromatase expression. The Journal of Comparative Neurology 483(1): 91–113.
  11. ^ Forlano PM, Marchaterre M, Deitcher DL and Bass AH. 2010. Distribution of androgen receptor mRNA expression in vocal, auditory, and neuroendocrine circuits in a teleost fish. The Journal of Comparative Neurology 518(4): 493–512.
  12. ^ Reamage-Healey L and Bass AH. 2007. Plasticity in brain sexuality is revealed by the rapid actions of steroid hormones. Journal of Neuroscience 27(5): 1114–1122.
  13. ^ Sisneros JA, Forlano PM, Deitcher DL, and Bass AH. 2004. Steroid-dependent auditory plasticity leads to adaptive coupling of sender and receiver. Science 305: 404–407.
  14. ^ Skoglund CB. 1961. Functional analysis of swimbladder muscles engaged in sound production of the toadfish. Journal of Biophysics and Biochemistry Cytology 10: 187–200.
  15. ^ Bass AH and Baker R. 1990. Sexual dimorphisms in the vocal control system of a teleost fish: morphology of physiologically identified neurons. Developmental neurobiology 21(8): 1155–1168.
  16. ^ a b Bubnoff AV. 2005. Humming fish solves noisy crash. Nature <http://www.nature.com/news/2005/050711/full/news050711-1.html> Accessed 12 Mar 2012.
  17. ^ Weeg MS, Land BR, and Bass AH. 2005. Vocal pathways modulate efferent neurons to the inner ear and lateral line. The Journal of Neuroscience 25(25): 5967–5974.
  18. ^ Bass AH. 2007. Steroid-dependent plasticity of vocal motor systems: novel insights from teleost fish. Brain Research Reviews 57(2): 299–308.
  19. ^ Holstege G. 1998. The organization of vocalization in mammals and the relation with vocalization and speech in humans. Presented at INABIS '98 - 5th Internet World Congress on Biomedical Sciences at McMaster University, Canada, Dec 7–16th. Invited Symposium. <http://www.mcmaster.ca/ inabis98/brudzynski/holstege0261/index.html> Accessed 11 Feb 2012.
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