Burrow residence of males and females of the mudskipper Periophthalmus modestus during reproduction

Hieu Van Mai, Kiyoshi Soyano, Atsushi Ishimatsu

Abstract

Pre-spawning reproductive behavior on the mudflat surface was reported previously for the mudskipper, Periophthalmus modestus, but it remains unknown how a pair spawns and fertilizes eggs within the spawning chamber of a burrow. In this study, we recorded reproductive behaviors from burrow entry of a pair to the departure of a female. In those cases, where spawning was suspected from a drastic reduction in the distension of the female’s belly (N = 4), the female remained inside a burrow for 240-350 min without coming out onto the mudflat surface. In contrast, the male often but irregularly emerged from the burrow. In one case, a second male entered a burrow 169 min after the burrow entry of a female, resulting in her desertion from the burrow without spawning. During burrow cohabitation of the pair, burrow openings were often clogged by mud from inside. After the female left the burrow, the male remained inside the burrow for variable periods. Then, the male guarded the burrow for about one week. Upon termination of the burrow guarding, the male began excavating a new burrow near the previous one or repaired the burrow that he had guarded. A hypothesized scenario is proposed for the reproduction of this species for further investigation.

Keywords

Courtship, Mudskipper, Periophthalmus modestus, reproduction.

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References

Akiyama N., Ogasawara Y. (1994). Reproductive behavior of the ice goby Leucopsarion petersii in captivity. Aquaculture Science, 42: 577-584.

Alvariño J.M.R., Zanuy S., Prat F., Carrillo M., Mañanos E. (1992). Stimulation of ovulation and steroid secretion by LHRHa injection in the sea bass (Dicentrarchus labrax): effect of time of day. Aquaculture, 102: 177-186.

Baeck G.W., Takita T., Yoon Y.H. (2008). Lifestyle of Korean mudskipper Periophthalmus magnuspinnatus with reference to a congeneric species Periophthalmus modestus. Ichthyological Research, 55: 43-52.

Bardon-Albaret A., Saillant E.A. (2016). Effects of hypoxia and elevated ammonia concentration on the viability of red snapper embryos and early larvae. Aquaculture, 459: 148-155.

Chowdhury I., Joy K. (2007). Seminal vesicle and its role in the reproduction of teleosts. Fish Physiology and Biochemistry, 33: 383-398.

DePasquale E., Baumann H., Gobler C.J. (2015). Vulnerability of early life stage Northwest Atlantic forage fish to ocean acidification and low oxygen. Marine Ecology Progress Series, 523: 145-156.

Dôtu Y., Tsutsumi T. (1959). The reproductive behaviour in the gobiid fish, Pterogobius elapoides (Günther). Bulletin of the Faculty of Fisheries, Nagasaki University, 8: 186-190.

Dzyuba V., Cosson J. (2014) Motility of fish spermatozoa: from external signaling to flagella response. Reproductive Biology, 14: 165-175.

Elshout P., Dionisio Pires L., Leuven R., Wendelaar Bonga S., Hendriks A. (2013). Low oxygen tolerance of different life stages of temperate freshwater fish species. Journal of Fish Biology, 83: 190-206.

Fishelson L. (1991). Comparative cytology and morphology of seminal vesicles in male gobiid fishes. Japanese Journal of Ichthyology, 38: 17-30.

Goetz F.W., Garczynski M. (1997). The ovarian regulation of ovulation in teleost fish. Fish Physiology and Biochemistry, 17: 33-38.

Gordon M.S. (1995). Functional evidence from living vertebrates. In: M.S. Gordon, E.C. Olson (Ed.). Invasions of the land. Columbia University Press. pp: 216-250.

Hassell K.L., Coutin P.C., Nugegoda D. (2008). Hypoxia impairs embryo development and survival in black bream (Acanthopagrus butcheri). Marine Pollution Bulletin, 57: 302-306.

Hong W., Chen S., Zhang Q., Wang Q. (2007). Reproductive ecology of the mudskipper Boleophthalmus pectinirostris. Acta Oceanologica Sinica, 26: 72-81.

Ip Y.K., Chew S.F., Wilson J.M., Randall D.J. (2004). Defences against ammonia toxicity in tropical air-breathing fishes exposed to high concentrations of environmental ammonia: a review. Journal of Comparative Physiology, B 174: 565-575.

Ishimatsu A., Aguilar N.M., Ogawa K., Hishida Y., Takeda T., Oikawa S., Kanda T., Khoo K.H. (1999). Arterial blood gas levels and cardiovascular function during varying environmental conditions in a mudskipper, Periophthalmodon schlosseri Journal of Experimental Biology, 202: 1753-1762.

Ishimatsu A., Graham J.B. (2011) Roles of environmental cues for embryonic incubation and hatching in mudskippers. Integrative and Comparative Biology, 51: 38-48.

Ishimatsu A., Hishida Y., Takita T., Kanda T., Oikawa S., Takeda T., Khoo K.H. (1998). Mudskippers store air in their burrows. Nature, 391: 237-238.

Ishimatsu A., Mai H.V., Martin K.L. (2018). Patterns of fish reproduction at the interface between air and water. Integrative and Comparative Biology, 58: 1064-1085.

Ishimatsu A., Takeda T., Tsuhako Y., Gonzales T.T., Khoo K.H. (2009). Direct evidence for aerial egg deposition in the burrows of the Malaysian mudskipper, Periophthalmodon schlosseri. Ichthyological Research, 56: 417-420.

Ishimatsu A., Yoshida Y., Itoki N., Takeda T., Lee H.J., Graham J.B. (2007). Mudskippers brood their eggs in air but submerge them for hatching. Journal of Experimental Biology, 210: 3946-3954.

Kagawa H. (2013). Oogenesis in teleost fish. Aqua-BioScience Monographs, 6: 99-127.

Kobayashi T., Dotsu Y., Takita T. (1971). Nest and nesting behavior of the mud skipper, Periophthalmus cantonensis in Ariake Sound. Bulletin of the Faculty of Fisheries, Nagasaki University, 32: 27-40.

Little C. (2000). The biology of soft shores and estuaries. Oxford University Press. 252 p.

Mai V.H., Tran L.X., Dinh Q.M., Tran D.D., Murata M., Sagara H., Yamada A., Shirai K., Ishimatsu A. (2019). Land invasion by the mudskipper, Periophthalmodon septemradiatus, in fresh and saline waters of the Mekong River. Scientific Reports, 9: 14227.

Marconato A., Rasotto M.B., Mazzoldi C. (1996). On the mechanism of sperm release in three gobiid fishes (Teleostei: Gobiidae). Environmental Biology of Fishes, 46: 321-327.

Martin K., Ishimatsu A. (2017). Review of reproductive strategies. In: Jaafar Z., Murdy E. (Ed.) Fishes out of water: biology and ecology of mudskippers. CRC Press. pp: 209-235.

Mashiko K. (1976). Reproductive behavior of an eleotrid goby Odontobutis obscurus in aquaria. Japanese Journal of Ichthyology, 23: 69-78.

Matoba M., Dotsu Y. (1977). Prespawning behavior of the mud skipper Periophthalmus cantonensis in Ariake Sound. Bulletin of the Faculty of Fisheries, Nagasaki University, 43: 23-33.

Matsuo T., Takahama H. (2001). Courtship and spawning behavior of Eleotris oxycephala in an aquarium. Japanese Journal of Ichthyology, 48: 53-57.

Mazzoldi C., Patzner R., Rasotto M.B. (2011). Morphological organization and variability of the reproductive apparatus in gobies. In: Patzner R., Van Tassell J.L., Kovačić M., Kapoor B.G. (Ed.) The biology of gobies. Science Publisher. pp: 367-402.

Miller P.J. (1984). The tokology of gobioid fishes. In: G.W. Potts, R.J. Wootton (Ed.). Fish reproduction: strategies and tactics. Academic Press. pp: 119-153.

Shein N.L., Chuda H., Arakawa T., Mizuno K., Soyano K. (2004). Ovarian development and final oocyte maturation in cultured sevenband grouper Epinephelus septemfasciatus. Fisheries Science, 70: 360-365.

Ota D., Marchesan M., Ferrero E.A. (1996). Sperm release behaviour and fertilization in the grass goby. Journal of Fish Biology, 49: 246-256.

Pankhurt N.W., Porter M.J.R. (2003). Cold and dark or warm and light: variations on the theme of environmental control of reproduction. Fish Physiology and Biochemistry, 28: 385-389.

Rombough P.J. (1988). Respiratory gas exchange, aerobic metabolism, and effects of hypoxia during early life. In: W.S. Hoar, D.J. Randall (Ed.) Fish physiology Vol. XI. The physiology of developing fish, Part A eggs and larvae. Academic Press. pp: 59-161.

Rupp H.-G. (2018). The secret life of mudskippers. Practical Fish Keeping, June 2018: 22-27.

Samarini A.M., Polica T., Lahnsteiner F. (2015). Fish oocyte ageing and its effect of egg quality. Reviews in Fisheries Science and Aquaculture, 23: 302-314.

Senta T., Wada I. (1970). The reproductive behavior in the gobiid fish Glossogobius olivaceus (Temminck and Schlegel) in an aquarium. Japanese Journal of Ichthyology, 17: 7-13.

Shimizu N., Sakai Y., Hashimoto H., Gushima K. (2006). Terrestrial reproduction by the air-breathing fish Andamia tetradactyla (Pisces; Blenniidae) on supralittoral reefs. Journal of Zoology, London, 269: 357-364.

Shiraishi T., Ketkar S.D., Kitano H., Nyuji M., Yamaguchi A., Matsuyama M. (2008). Time course of final oocyte maturation and ovulation in chub mackerel Scomber japonicus induced by hCG and GnRHa. Fisheries Science, 74: 764-769.

Soyano K., Higuchi T., Kobayashi M., Takushima M., Aoki J., Nagae M. (2008a). Gonadal development and spawning rhythm in mudskipper (Periophthalmus modestus). Cybium, 32: 234-234.

Soyano K., Sakakura Y., Hagiwara A. (2008b). Reproduction and larviculture of seven-band grouper, Epinephelus septemfasciatus. In: I.C. Liano, E.M. Leaño (Ed.). The aquaculture of groupers. Asian Fisheries Society. pp: 1-27.

Takegaki T., Nakazono A. (1999). Reproductive behavior and mate fidelity in the monogamous goby, Valencinnea longipinnis. Ichthyological Research, 46: 115-123.

Takita T., Ishimatsu A. (2015). Fish emerging from water – the mudskipper's challenge. Kaiyusha Publishers. 168 p.

Tavolga W.N. (1954). Reproductive behavior in the gobiid fish Bathygobius soporator. Bulletin of the American Museum of Natural History, 104: 427-260.

Toba A., Ishimatsu A. (2014). Roles of air stored in burrows of the mudskipper Boleophthalmus pectinirostris for adult respiration and embryonic development. Journal of Fish Biology, 84: 774-793.

Wells K.D. (2007). The ecology and behavior of amphibians. The University of Chicago Press. 1148 p.

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