Abstract
The Hawaiian sandburrowers Crystallodytes cookei and Limnichthys nitidus were found to be protandrous hermaphrodites based on a histological examination of gonad morphology and development. The majority of individuals of both species (71% and 75%, respectively) had delimited ovotestes in which ovarian and testicular tissue were divided by a connective tissue barrier. In juveniles and functional males, the ovarian and testicular regions were similar in cross-sectional area, whereas in functional females, the testicular portion was absent or greatly reduced. Reproductive females were significantly larger in body size than functional males but did not differ significantly in size with transitionals (individuals which contained both developing ova and visible spermatozoa). The complete absence of functional females at the smallest size ranges suggests that both species are monogynic; all females are derived from previously mature males. The ovotestis morphology and sequence of gonad development present in C. cookei and L. nitidus are most similar to protandrous porgies (family Sparidae). When compared to sex changing species of the closely related genus Trichonotus (family Trichonotidae), the distinct ovotestis morphology (delimited in creediids vs. mixed in Trichonotus) and differing direction of sex change (protandry vs. protogyny) suggest that sex change evolved independently in these taxa.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data Availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Asoh K, Shapiro DY (1997) Bisexual juvenile gonad and gonochorism in the fairy basslet, Gramma loreto. Copeia 1997:22–31. https://doi.org/10.2307/1447836
Barlow GW (1981) Patterns of parental investment, dispersal and size among coral-reef fishes. Environ Biol Fish 6:65–85. https://doi.org/10.1007/BF00001801
Butler EC, Childs AR, Winkler AC, Milner M, Potts WM (2018) Evidence for protandry in Polydactylus quadrifilis in the Kwanza Estuary, Angola, and its implications for local fisheries. Environ Biol Fish 101:301–313. https://doi.org/10.1007/s10641-017-0699-6
Buxton CD, Garratt PA (1990) Alternative reproductive styles in seabreams (Pisces: Sparidae). Environ Biol Fish 28:113–124. https://doi.org/10.1007/BF00751031
Casas L, Saborido-Rey F (2021) Environmental cues and mechanisms underpinning sex change in fish. Sex Dev 15:108–121. https://doi.org/10.1159/000515274
Clark E, Phole M (1996) Trichonotus halstead, a new sand-diving fish from Papua New Guinea. Environ Biol Fish 45:1–11. https://doi.org/10.1007/BF00000622
Cole KS (1990) Patterns of gonad structure in hermaphroditic gobies (Teleostei Gobiidae). Environ Biol Fish 28:125–142. https://doi.org/10.1007/BF00751032
Cozzi J, Clark E (1995) Darting behavior of a sandburrower fish, Limnichthys nitidus (Creediidae), in the Red Sea. Environ Biol Fish 44(4):327–336. https://doi.org/10.1007/BF00008247
Fricke HW (1979) Mating system, resource defense and sex change in the Anemonefish Amphiprion akallopisos. Z Tierpsychol 50:313–326. https://doi.org/10.1111/j.1439-0310.1979.tb01034.x
Froese R, Pauly D (eds) (2022) FishBase. World Wide Web electronic publication. www.fishbase.org, version (08/2022)
Ghiselin MT (1969) The evolution of hermaphroditism among animals. Q Rev Biol 44:189–208. https://doi.org/10.1086/406066
Godwin J (1994) Histological aspects of protandrous sex change in the anemonefish Amphiprion melanopus (Pomacentridae, Teleostei). J Zoology 232:199–213. https://doi.org/10.1111/j.1469-7998.1994.tb01569.x
Gosline WA (1965) Vertical zonation of inshore fishes in upper water layers of the Hawaiian Islands. Ecology 46:823–831. https://doi.org/10.2307/1934015
Greenfield DW (2003) A survey of the small reef fishes of Kāne’ohe Bay, O’ahu Hawaiian Islands. Pac Sci 57(1):45–76. https://doi.org/10.1353/psc.2003.0001
Grier HJ (1981) Cellular organization of the testis and spermatogenesis in fishes. Am Zool 21(2):345–357. https://doi.org/10.1093/icb/21.2.345
Guiguen Y, Cauty C, Fostier A, Fuchs J, Bernard J (1994) Reproductive cycle and sex inversion of the seabass, Lates calcarifer, reared in sea cages in French Polynesia: histological and morphometric description. Environ Biol Fish 39:231–247. https://doi.org/10.1007/BF00005126
Hesp SA, Potter IC, Hall NG (2004) Reproductive biology and protandrous hermaphroditism in Acanthopagrus latus. Environ Biol Fish 70:257–272. https://doi.org/10.1023/B:EBFI.0000033344.21383.00
Hodge JR, Santini F, Wainwright PC (2020) Colour dimorphism in labrid fishes as an adaptation to life on coral reefs. Proc R Soc B 287:20200167. https://doi.org/10.1098/rspb.2020.0167
Kusen JD, Nakagawa K, Yogo Y, Nakazono A (1991) Protogynous hermaphroditism in the Sand Diver Trichonotus filamentosus. Nippon Suisan Gakkaishi 57(1):35–40. https://doi.org/10.2331/suisan.57.35
Kuwamura T, Sunobe T, Sakai Y, Kadota T, Kota S (2020) Hermaphroditism in fishes: an annotated list of species, phylogeny, and mating system. Ichthyol Res 67:341–360. https://doi.org/10.1007/s10228-020-00754-6
Langston RC (2004) Gonad morphology and sex change in sandburrowers (Teleostei: Creediidae). Dissertation, Univ of Hawaii. https://scholarspace.manoa.hawaii.edu/server/api/core/bitstreams/d0763489-6c12-4828-ac8b-4eac8c43697a/content
Leis JM (1982) Hawaiian creediid fishes (Crystallodytes cookei and Limnichthys donaldsoni): development of eggs and larvae and the use of pelagic eggs to trace coastal water movements. Bull Mar Sci 32(1):166–180
Longenecker K (2007) Devil in the details: high-resolution dietary analysis contradicts a basic assumption of reef-fish diversity models. Copeia 2007:543–555. https://doi.org/10.1643/0045-8511(2007)2007[543:DITDHD]2.0.CO;2
Longenecker K, Gill A, Kelokelo M, Langston R, Donaldson TJ, Franklin EC (2020) Rapid reproductive analysis and weight-length relation of the humpnose big-eye bream, Monotaxis grandoculis (Actinopterygii: Perciformes: Lethrinidae), from Micronesia with implications for fisheries. Acta Ichthyol Piscat 50(4):493–500. https://doi.org/10.3750/AIEP/02965
Miya M, Nemoto T (1985) Protandrous Sex Reversal in Cyclothone atraria (Family Gonostomatidae). Jpn J Ichthyol 31(4):438–440. https://doi.org/10.11369/jji1950.31.438
Moyer JT (1976) Geographical variation and social dominance in Japanese populations of the anemonefish Amphiprion clarkii. Jpn J Ichthyol 23:12–22
Moyer JT (1980) Influence of temperate waters on the behavior of the tropical anemonefish Amphiprion clarkii at Miyake-Jima. Jpn Bull Mar Sci 30(1):261–272
Munday P, Jones G (1998) The ecological implications of small body size among coral-reef fishes. Oceanog Mar Biol 36:373–411
Neat FC (2001) Male Parasitic spawning in two species of triplefin blenny (Tripterygiidae): contrasts in demography, behavior and gonadal characteristics. Environ Biol Fish 61:57–64. https://doi.org/10.1023/A:1011074716758
Nelson JS (1985) On the interrelationships of the genera of Creediidae (Perciformes: Trachinoidei). Jpn J Ichthyol 32(3):283–293. https://doi.org/10.11369/jji1950.32.283
Nelson JS (1986) Some Characters of Trichonotidae, with Emphasis to those distinguishing it from Creediidae (Perciformes: Trachinoidei). Jpn J Ichthyol 33(1):1–6
Nelson JS, Randall JE (1985) Crystallodytes pauciradiatus (Perciformes), a new creediid fish species from Easter Island. Proc Biol Soc Wash 98(2):403–410
Nelson JS, Grande TC, Wilson MVH (2016) Fishes of the world, 5th edn. John Wiley & Sons Inc, Hoboken
Pettigrew JD, Collin SP, Fritsches K (2000) Prey capture and accommodation in the sandlance, Limnichthyes fasciatus (Creediidae; Teleostei). J Comp Physiol 186:247–260. https://doi.org/10.1007/s003590050425
Pla S, Maynou F, Piferrer F (2021) Hermaphroditism in fish: incidence, distribution and associations with abiotic environmental factors. Rev Fish Biol Fish 31:935–955. https://doi.org/10.1007/s11160-021-09681-9
Rasotto MB, Mazzoldi C (2002) Male traits associated with alternative reproductive tactics in Gobius niger. J Fish Biol 61:173–184. https://doi.org/10.1111/j.1095-8649.2002.tb01744.x
Reinboth R (1970) Intersexuality in Fishes. Mem Soc Endocrinol 18:515–543
Sadovy de Mitcheson Y, Liu M (2008) Functional hermaphroditism in teleosts. Fish Fish 9:1–43. https://doi.org/10.1111/j.1467-2979.2007.00266.x
Sadovy Y, Shapiro DY (1987) Criteria for the diagnosis of hermaphroditism in fishes. Copeia 1987:136–156. https://doi.org/10.1007/s003590050425
Schultz LP (1943) Fishes of the Phoenix and Samoan Islands collected in 1939 during the expedition of the U.S.S. “Bushnell”. Smithsonian Institution United States National Museum. Bulletin 180
Seiwald M, Patzner RA (1987) Ultrastructure of the testicular gland of Blennius pavo (Pisces, Teleostei). Zoomorphology 107:26–32. https://doi.org/10.1007/BF00312126
Shihab I, Gopalakrishnan A, Vineesh N, Muktha M, Akhilesh KV, Vijayagopal P (2017) Histological profiling of gonads depicting protandrous hermaphroditism in Eleutheronema tetradactylum. J Fish Biol 90(6):2402–2411. https://doi.org/10.1111/jfb.13324
Shimada K, Yoshino T (1984) A new trichonotid from the Yaeyama Islands, Okinawa Prefecture Japan. Jpn J Ichthyol 31(1):15–19. https://doi.org/10.11369/jji1950.31.15
Shinomiya A, Yamada M, Sunobe T (2003) Mating system and protandrous sex change in the lizard flathead, Inegocia japonica (Platycephalidae). Ichthyol Res 50:383–386. https://doi.org/10.1007/s10228-003-0182-6
Shitamitsu T, Sunobe T (2017) Notes on protandry in the creediid fishes Limnichthys fasciatus and L. nitidus (Teleostei: Creediidae). Ichthyol Res 64:365–367. https://doi.org/10.1007/s10228-016-0566-z
Smith DG, Johnson GD (2007) A new species of Pteropsaron (Teleostei: Trichonotidae: Hemerocoetinae) from the Western Pacific, with notes on related species. Copeia 2007:364–377. https://doi.org/10.1643/0045-8511(2007)7[364:ANSOPT]2.0.CO;2
Sunobe T, Sakaida S, Kuwamura T (2016) Random mating and protandrous sex change of the platycephalid fish Thysanophrys celebica (Platycephalidae). J Ethol 34:15–21. https://doi.org/10.1007/s10164-015-0439-3
Taylor RG, Whittington JA, Grier HJ, Crabtree RE (2000) Age, growth, maturation, and protandric sex reversal in common snook, Centropomus undecimalis, from the east and west coasts of South Florida. Fish Bull 98:612–624
Tobin AJ, Sheaves MJ, Molony BW (1997) Evidence of protandrous hermaphroditism in the tropical sparid Acanthopagrus berda. J Fish Biol 50:22–23. https://doi.org/10.1111/jfb.1997.50.1.22
Wallace RA, Selman K (1981) Cellular and dynamic aspects of oocyte growth in teleosts. Am Zool 21:325–343. https://doi.org/10.1093/icb/21.2.325
Warner RR (1988) Sex change and the size-advantage model. Trends Ecol Evol 3(6):133–136. https://doi.org/10.1016/0169-5347(88)90176-0
Yoshino T, Kon T, Okabe S (1999) Review of the genus Limnichthys (Perciformes: Creediidae) from Japan, with description of a new species. Ichthyol Res 46(1):73–83. https://doi.org/10.1007/BF02674950
Acknowledgements
I am grateful to the following individuals for help with field collections: E. Baumgartner, J. Collier, A. Dehn, T. Fitzgerald, J. Garrison, K. Longenecker, J. Mahon, M. Mohlman, D. Strang, and T. Leedom. Photographic assistance was provided by C. Brown, J. Fox, A. Moriwake, V. Moriwake, B. Nedved, S. Robinow, and A. Whittle. Several lots of fishes were kindly supplied by D. Greenfield. S. Haley and S. Spielman provided facilities and materials for microtechnique. K. Longenecker provided feedback on the draft manuscript. I am especially indebted to K. Asoh, K. Cole, and T. Yoshikawa for their assistance in evaluating gonad sections as well as their guidance and encouragement. All research was conducted through the University of Hawaii Department of Zoology, Hawaii Institute of Marine Biology, and Windward Community College Department of Natural Sciences.
Funding
This study was supported, in part, by a Grant-in-Aid of research from Sigma Xi.
Author information
Authors and Affiliations
Contributions
R.L. performed all tasks associated with this paper including project conception, data generation and analysis, and manuscript preparation.
Corresponding author
Ethics declarations
Ethics approval
The care and use of experimental animals complied with the United States Animal Welfare Act. Specimens collected during this study were obtained under Hawaii Department of Land and Natural Resources scientific collecting permit SCP 2000–27 and University of Hawaii Institutional Animal Care and Use Committee protocols 98–001 and 22–3864.
Conflict of interest
The author declares no competing interests.
Additional information
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Langston, R. Histological evidence of sequential hermaphroditism in Hawaiian sandburrowers Crystallodytes cookei and Limnichthys nitidus. Environ Biol Fish 106, 61–78 (2023). https://doi.org/10.1007/s10641-022-01373-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10641-022-01373-y