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Mudskipper

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Mudskipper
Atlantic mudskipper (Periophthalmus barbarus) in The Gambia
Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Chordata
Class: Actinopterygii
Order: Gobiiformes
Family: Oxudercidae
Subfamily: Oxudercinae
Gunther 1861[1]
Genera

Apocryptes
Apocryptodon
Boleophthalmus
Oxuderces
Parapocryptes
Periophthalmodon
Periophthalmus
Pseudapocryptes
Scartelaos
Zappa

Synonyms
  • Periophthalminae
  • Periophthalmidae

Mudskippers are any of the 23 extant species of amphibious fish from the subfamily Oxudercinae of the goby family Oxudercidae.[2] They are known for their unusual body shapes, preferences for semiaquatic habitats, limited terrestrial locomotion and jumping, and the ability to survive prolonged periods of time both in and out of water.

Mudskippers can grow up to 30 cm (12 in) long, and most are a brownish green colour that ranges anywhere from dark to light. During mating seasons, the males will also develop brightly coloured spots in order to attract females, which can be red, green or blue. Unlike other fish, the mudskipper's eyes protrude from the top of its flat head. Their most noticeable feature however is their side pectoral fins that are located more forward and under their elongated body. These fins are jointed and function similarly to limbs, which allow the mudskipper to crawl from place to place. Although having the typical body form of any other gobiid fish, these front fins allow the mudskipper to actively "skip" across muddy surfaces (hence the common name) and even climb low-hanging tree branches and scrubs. Mudskippers have also been found to be able to leap distances of up to 61 centimetres (24 in) by laterally flexing and pushing with their tails.[citation needed]

Taxonomy

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Oxudercinae is sometimes classified within the family Gobiidae (gobies).[3] Recent molecular studies do not support this classification, as oxudercine gobies appear to be paraphyletic relative to amblyopine gobies (Gobiidae: Amblyopinae), thus being included in a distinct "Periophthalmus lineage", together with amblyopines.[4] Mudskippers can be defined as oxudercine gobies that are "fully terrestrial for some portion of the daily cycle" (character 24 in Murdy, 1989[3]). This would define the species of the genera Boleophthalmus, Periophthalmodon, Periophthalmus, and Scartelaos as "mudskippers". However, field observations of Zappa confluentus suggest that this monotypic genus should be included in the definition.[5]

Behaviour

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Mudskippers typically live in burrows in intertidal habitats, and exhibit unique adaptations to this environment that are not found in most intertidal fishes, which typically survive the retreat of the tide by hiding under wet seaweed or in tide pools.[6] These burrows are most often characterised by their smooth and vaulted ceilings. The way the males dig these burrows has been found to be directly linked to their ability to survive submerged in almost anoxic water. It has also been found to play a crucial role in the development of the eggs within the burrow. Mudskippers are quite active when out of water, feeding and interacting with one another, for example, to defend their territories and court potential partners. Once the male has completed digging his burrow he will resurface and will begin attempting to attract a female through assorted yet typical displays. These displays consist of body undulations, different postures and energetic movements. Once the female has made her choice she will then proceed to follow the male into the burrow where she will lay hundreds of eggs and allow them to be fertilized. After fertilization occurs, the period of cohabitation between the male and female is rather short. Eventually, the female will leave and it is the male that ends up guarding the egg filled burrow from hungry predators.[citation needed]

Mudskippers are amphibious. When leaving the water and moving into a more dry environment on land, they are still able to breathe using water that is trapped inside their large gill chambers. They are also able to absorb oxygen from the lining of their mouth and throat, allowing them to stay out of water for long periods of time. It has been discovered that they spend up to three quarters of their life on land. They are found in tropical, subtropical, and temperate regions, including the Indo-Pacific and the Atlantic coast of Africa.[citation needed]

Adaptations

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Periophthalmus gracilis (from Malaysia to northern Australia)
Periophthalmus barbarus (from western Africa)

Compared with fully aquatic gobies, these specialised fish present a range of anatomical and ethological adaptations that allow them to move effectively on land as well as in the water.[7][8]

Terrestrial movement

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As their name implies, these fish use their fins to move around in a series of skips.

Although mudskippers' fins do not have a joint homologous to the elbow, the joint between the radials and the fin rays serves a functionally analogous role.

— Integrative and Comparative Biology[9]

The mudskipper pectoral fin differs from most actinopterygian fishes in that the radials of the mudskipper pectoral fin are elongated and protrude from the body wall. This unusual morphology creates a pectoral fin with two fin segments (the radials and the rays) and two movable hinge joints: a 'shoulder' joint where the cleithrum meets the radials and an 'intra-fin' joint where the radials meet the rays.[7] In addition, ... the abductor superficialis muscle of the pectoral fin is divided into two sections (rather than being a single muscle, as is common with the rest of the Oxudercinae gobies) with one section inserting on the dorsal rays and the other section inserting on the ventral rays.

— The Journal of Experimental Biology[10]

Breathing

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Mudskipper at Point Calimere Sanctuary, Tamil Nadu, India
Mudskipper at Coringa Mangrove Sanctuary, Andhra Pradesh, India
Periophthalmodon septemradiatus territorial defense call and jumping ability[11]

Mudskippers have the ability to breathe through their skin and the lining of their mouth (the mucosa) and throat (the pharynx); this is only possible when the mudskippers are wet, limiting them to humid habitats and requiring that they keep themselves moist. The ability to breathe through their skin is associated with increased capillary density in their skin.[12] This mode of breathing, similar to that employed by amphibians, is known as cutaneous respiration.[6] Another important adaptation that aids breathing while out of water is their enlarged gill chambers, where they retain a bubble of air. These chambers close tightly when the fish is above water, due to a ventromedial valve of the gill slit, keeping the gills moist, and allowing them to function while exposed to air. Gill filaments are stiff and do not coalesce when out of water.[6]

Diet

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The different species have adapted to various diets on the mudflats. Boleophthalmus boddarti is detritivorous, while others will eat small crabs, insects, snails and even other mudskippers.[13]

Burrowing

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Digging deep burrows in soft sediments allows the fish to thermoregulate,[14] avoid marine predators during the high tide when the fish and burrow are submerged,[15] and lay their eggs.[16] When the burrow is submerged, several mudskipper species maintain an air pocket inside it, which allows them to breathe in conditions of very low oxygen concentration.[17][18][19]

Ammonia regulation

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To reduce toxic ammonia production, mudskippers can suppress amino acid breakdown when exposed to air.[20] Another method they use involves the partial breakdown of amino acids leading to the production of alanine, which also reduces ammonia production.[20]

Mudskippers can reduce the membrane permeability of their skin and acidify the water in their burrows to reduce levels of ammonia from the environment.[21][22]

Blinking

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Mudskippers evolved the ability to blink independently from terrestrial tetrapods. Their eyes are located high on their head compared to other gobies, and they blink by lowering their eyes as a membrane called the dermal cup rises to cover them. Although other fully aquatic goby species do not have the ability to blink, mudskippers did not evolve different muscles or glands to blink with; their blinking is accomplished with the same muscles in a different configuration. Rather than having specialized glands to produce eye lubricant, the fluid film on their cornea is likely composed of mucus secreted by their skin and water from their environment, possibly stored in the infraorbital space behind the dermal cup membrane. Mudskippers likely evolved blinking in response to conditions of terrestrial life, such as to keep their eyes wet out of water (they blink more frequently in high evaporation conditions and only when colliding with things in water) and to clean and protect the eye from debris, which may adhere to the eye or approach at a faster, more dangerous speed when in air versus when in water. Their eyes are not elevated when they are still juveniles, which are fully aquatic.[23]

Species

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The genus Periophthalmus is by far the most diverse and widespread genus of mudskipper. Eighteen species have been described.[24][25][26] Periophthalmus argentilineatus is one of the most widespread and well-known species. It can be found in mangrove ecosystems and mudflats of East Africa and Madagascar east through the Sundarbans of Bengal, Southeast Asia to Northern Australia, southeast China, Taiwan, and the Ryukyus, to Samoa and Tonga Islands.[3] It grows to a length of about 9.5 cm [3] and is a carnivorous opportunist feeder. It feeds on small prey such as small crabs and other arthropods.[27] However, a recent molecular study suggests that P. argentilineatus is in fact a complex of species, with at least three separate lineages, one in East Africa, and two in the Indo-Malayan region.[28] Another species, Periophthalmus barbarus, is the only oxudercine goby that inhabits the coastal areas of western Africa.[3]

References

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  1. ^ Richard van der Laan; William N. Eschmeyer & Ronald Fricke (2014). "Family-group names of Recent fishes". Zootaxa. 3882 (2): 001–230. doi:10.11646/zootaxa.3882.1.1. PMID 25543675.
  2. ^ Nelson, JS; Grande, TC & Wilson, MVH (2016). "Classification of fishes from Fishes of the World 5th Edition" (PDF). Retrieved 10 May 2018.
  3. ^ a b c d e Murdy EO (1989). "A Taxonomic Revision and Cladistic Analysis of the Oxudercine Gobies (Gobiidae: Oxudercinae)". Records of the Australian Museum. Suppl 11: 1–93. doi:10.3853/j.0812-7387.11.1989.93.
  4. ^ Agorreta A.; San Mauro D.; Schliewen U. & Rüber L. (2013). "Molecular phylogenetics of Gobioidei and phylogenetic placement of European gobies". Molecular Phylogenetics and Evolution. 69 (3): 619–633. doi:10.1016/j.ympev.2013.07.017. hdl:10261/123985. PMID 23911892.
  5. ^ Polgar G.; Sacchetti A. & Galli P. (2010). "Differentiation and adaptive radiation of amphibious gobies (Gobiidae: Oxudercinae) in semi-terrestrial habitats". Journal of Fish Biology. 77 (7): 1645–1664. doi:10.1111/j.1095-8649.2010.02807.x. PMID 21078024.
  6. ^ a b c Graham JB, ed. (1997). Air–breathing Fishes. Evolution, Diversity and Adaptation. San Diego California: Academic Press.
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  8. ^ Pace CM, Gibb AC (2009). "Mudskipper pectoral fin kinematics in aquatic and terrestrial environments". Journal of Experimental Biology. 212 (14): 2279–2286. doi:10.1242/jeb.029041. PMID 19561218.
  9. ^ S. M. Kawano; R. W. Blob (August 2, 2013). "Propulsive Forces of Mudskipper Fins and Salamander Limbs during Terrestrial Locomotion: Implications for the Invasion of Land". Integrative and Comparative Biology. 53 (2): 283–294. doi:10.1093/icb/ict051. PMID 23667046.
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  11. ^ Polgar G, Malavasi S, Cipolato G, Georgalas V, Clack JA, Torricelli P (2011). "Acoustic Communication at the Water's Edge: Evolutionary Insights from a Mudskipper". PLOS ONE. 6 (6): e21434. Bibcode:2011PLoSO...621434P. doi:10.1371/journal.pone.0021434. PMC 3125184. PMID 21738663.
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  13. ^ Ecology of Kalimantan: Indonesian Borneo
  14. ^ Tytler P, Vaughan T (1983). "Thermal Ecology of the Mudskippers Periophthalmus koelreuteri (Pallas) and Boleophthalmus boddaerti (Pallas), of Kuwait Bay". Journal of Fish Biology. 23 (3): 327–337. doi:10.1111/j.1095-8649.1983.tb02912.x.
  15. ^ Sasekumar A, Chong VC, Lim KH, Singh HR (1994). "The Fish Community of Matang Mangrove Waters, Malaysia". In Sudara S, Wilkinson CR, Chou LM (eds.). Proceedings, Third ASEAN-Australia Symposium on Living Coastal Resources. Research papers. Vol. 2. Bangkok: Chulalonghorn University. pp. 457–464.
  16. ^ Brillet C (1969). "Etude du comportement constructeur des poissons amphibies Periophthalmidae". Terre et la Vie (in French). 23 (4): 496–520.
  17. ^ Ishimatsu A, Hishida Y, Takita T, Kanda T, Oikawa S, Takeda T, Khoo KH (1998). "Mudskipper Store Air in Their Burrows". Nature. 391 (6664): 237–238. Bibcode:1998Natur.391..237I. doi:10.1038/34560. S2CID 4429394.
  18. ^ Ishimatsu A, Takeda T, Kanda T, Oikawa S, Khoo KH (2000). "Burrow environment of mudskippers in Malaysia". Journal of Biosciences. 11 (1–2): 17–28.
  19. ^ Lee HJ, Martinez CA, Hertzberg KJ, Hamilton AL, Graham JB (2005). "Burrow air phase maintenance and respiration by the mudskipper Scartelaos histophorus (Gobiidae: Oxudercinae)". The Journal of Experimental Biology. 208 (Pt 1): 169–177. doi:10.1242/jeb.01361. PMID 15601887.
  20. ^ a b Ip, Y. K.; Chew, S. F.; Randall, D. J. (2004-09-01). "Five Tropical Air‐Breathing Fishes, Six Different Strategies to Defend against Ammonia Toxicity on Land". Physiological and Biochemical Zoology. 77 (5): 768–782. doi:10.1086/422057. ISSN 1522-2152. PMID 15547795. S2CID 20545085.
  21. ^ Randall, D. J.; Ip, Y. K.; Chew, S. F.; Wilson, J. M. (September 2004). "Air Breathing and Ammonia Excretion in the Giant Mudskipper, Periophthalmodon schlosseri". Physiological and Biochemical Zoology. 77 (5): 783–788. doi:10.1086/423745. ISSN 1522-2152. PMID 15547796. S2CID 36864021.
  22. ^ Randall, D. J.; Wilson, J. M.; Peng, K. W.; Kok, T. W. K.; Kuah, S. S. L.; Chew, S. F.; Lam, T. J.; Ip, Y. K. (1999-12-01). "The mudskipper, Periophthalmodon schlosseri, actively transports NH 4 + against a concentration gradient". American Journal of Physiology. Regulatory, Integrative and Comparative Physiology. 277 (6): R1562–R1567. doi:10.1152/ajpregu.1999.277.6.R1562. ISSN 0363-6119. PMID 10600900. S2CID 29598011.
  23. ^ Aiello, Brett R.; Bhamla, M. Saad; Gau, Jeff; Morris, John G. L.; Bomar, Kenji; da Cunha, Shashwati; Fu, Harrison; Laws, Julia; Minoguchi, Hajime; Sripathi, Manognya; Washington, Kendra; Wong, Gabriella; Shubin, Neil H.; Sponberg, Simon; Stewart, Thomas A. (April 24, 2023). "The origin of blinking in both mudskippers and tetrapods is linked to life on land". PNAS. 120 (18): e2220404120. doi:10.1073/pnas.2220404120. PMC 10160996. PMID 37094121.
  24. ^ Larson HK, Takita T (2004). "Two new species of Periophthalmus (Teleostei: Gobiidae: Oxudercinae) from northern Australia, and a re-diagnosis of Periophthalmus novaeguineaensis". The Beagle, Records of the Museums and Art Galleries of the Northern Territory. 20: 175–185. doi:10.5962/p.286325. S2CID 131712323.
  25. ^ Jaafar Z, Perrig M, Chou LM (2009). "Periophthalmus variabilis (Teleostei: Gobiidae: Oxudercinae), a valid species of mudskipper, and a re-diagnosis of Periophthalmus novemradiatus". Zoological Science. 26 (4): 309–314. doi:10.2108/zsj.26.309. PMID 19798926. S2CID 31647216.
  26. ^ Jaafar Z, Larson HL (2008). "A new species of mudskipper, Periophthalmus takita (Teleostei: Gobiidae: Oxudercinae), from Australia, with a key to the genus". Zoological Science. 25 (9): 946–952. doi:10.2108/zsj.25.946. PMID 19267605. S2CID 10659541.
  27. ^ Milward, NE (1974). Studies on the taxonomy, ecology and physiology of Queensland mudskippers (unpubl. Ph.D. dissertation ed.). Brisbane: University of Queensland.
  28. ^ Polgar G, Zane L, Babbucci M, Barbisan F, Patarnello T, Rüber L, Papetti C (2014). "Phylogeography and demographic history of two widespread Indo-Pacific mudskippers (Gobiidae: Periophthalmus)". Molecular Phylogenetics and Evolution. 73: 161–176. doi:10.1016/j.ympev.2014.01.014. PMID 24486991.
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