Sains Malaysiana 52(9)(2023): 2485-2498
http://doi.org/10.17576/jsm-2023-5209-02
Systemic Histology of the Marine
Water-Strider Halobates hayanus (Heteroptera, Gerridae)
(Histologi Sistemik Water-Strider Marin Halobates hayanus (Heteroptera, Gerridae))
SINLAPACHAI SENARAT1,2, NARITSARA SAELUEA2,
EZRA MONGKOLCHAICHANA3, NATTHAWUT CHAROENPHON4, WISUT
SITTICHAYA5, NARIT THAOCHAN5,*, PISIT POOLPRASERT6,
ANAN KENTHAO7, KORRAWAT ATTASOPA8 & PIYAKORN
BOONYOUNG9
1Division of Biological Sciences, Faculty of Science, Prince of Songkla University, Songkhla 90110, Thailand
2Department of Marine Science and Environment, Faculty of Science and
Fisheries Technology, Rajamangala University of Technology Srivijaya, Trang
Campus, Trang 92150, Thailand
3Department of General Education, Faculty of Science and
Health Technology, Navamindradhiraj University, Bangkok 10300, Thailand
4Department of Anatomy,
Faculty of Medical Science, Naresuan University, Phitsanulok 65000, Thailand
5Innovation and Management Division (Pest
Management), Faculty of Natural Resources, Prince of Songkla University,
Songkhla 90110, Thailand
6Department of Entomology, Faculty of Argriculture, Kasetsart University, Chatuchak, Bangkok 10900, Thailand
7Department of Biology, Faculty of Science, Naresuan
University, Phitsanulok 65000, Thailand
8Department of Entomology and Plant
Pathology, Faculty of Agriculture, Chiang Mai University, Chiang Mai 50200,
Thailand
9Division of Health and Applied Sciences, Faculty of
Science, Prince of Songkla University, Songkhla 90110, Thailand
Received: 4 January
2023/Accepted: 10 August 2023
Abstract
The structure and cell types of the organs of Halobates hayanus from Libong Island, Thailand, were investigated using a histological method. The
integumentary system of this species consists of three layers: epicuticle, exocuticle, and endocuticle. Throughout
the body, the muscular system
exclusively included skeletal muscle. In the
excretory system, we found four fully formed Malpighian tubules, each one lined
with a straightforward cuboidal epithelium harbouring secretory granules. The
digestive system comprised a foregut, midgut, and
hindgut. The midgut had three distinct cell types: basal
cells, epithelium, and absorptive cells. The nervous system comprised two regions: A ventral
nerve cord and a frontal ganglion, which is connected to the eye structure. The
frontal ganglion was composed of two lobes each containing an outer cortex and
inner medulla. The
outer cortex presented neurosecretory cells, neuroglia cells, and neurons. The
neurosecretory cells were large and contained secretory granules in their
cytoplasm. This
histological study also showed the reproductive system of this gerrid species, including the reproductive tract, and the
accessory organ.
Keywords: Histological
structure; Libong Island; oceanic Halobates species;
systemic organs
Abstrak
Struktur dan jenis sel organ Halobates hayanus dari Pulau Libong,
Thailand, dikaji menggunakan kaedah histologi. Sistem integumen spesies ini terdiri daripada tiga lapisan: epikutikel, eksokutikel dan endokutikel. Pada seluruh badan, sistem otot secara eksklusif merangkumi otot rangka. Dalam sistem perkumuhan, kami menjumpai empat tubul Malpighian yang telah terbentuk sepenuhnya, setiap satu dilapisi dengan epitelium kuboid lurus yang menyimpan butiran rembesan. Sistem pencernaan terdiri daripada usus depan, usus tengah dan usus belakang. Usus tengah mempunyai tiga jenis sel yang berbeza: sel basal, epitelium dan sel penyerap. Sistem saraf terdiri daripada dua kawasan: kord saraf ventral dan ganglion frontal, yang bersambung dengan struktur mata. Ganglion frontal terdiri daripada dua lobus setiap satu mengandungi korteks luar dan medula dalam. Korteks luar membentangkan sel neurorembesan, sel neuroglia dan neuron. Sel neurorembesan adalah besar dan mengandungi butiran rembesan dalam sitoplasmanya. Kajian histologi ini juga mendedahkan sistem pembiakan spesies gerrid ini, termasuk saluran pembiakan dan organ aksesori.
Kata kunci: Organ sistemik; Pulau Libong; spesies Halobates lautan; struktur histologi
REFERENCES
Andersen, N.M. & Cheng, L. 2004. The
marine insect Halobates (Heteroptera: Gerridae): biology, adaptations, distribution, and phylogeny. Oceanography and Marine Biology 42: 119-180.
Andersen,
N.M. &
Foster, W.A. 1992. Sea
skaters of India, Sri Lanka, and the Maldives, with a new species and a revised
key to Indian Ocean species of Halobates and Asclepios (Hemiptera, Gerridae). Journal of Natural History 26: 533-553.
Andersen, N.M. & Weir, T.A. 1994. The sea
skaters, genus Halobates eschscholtz (Hemiptera: Gerridae), of Australia: Taxonomy, phylogeny and
zoogeography. Invertebrate Taxonomy 8(4): 861-909.
Arab, A. & Caetano, F.H. 2002. Segmental
specializations in the Malpighian tubules of the fire ant Solenopsis saevissima Forel 1904 (Myrmicinae): An electron microscopical study. Arthropod Structure and Development 30: 281-292.
Areekul, S. 1957. The comparative internal larval anatomy of
several genera of Scarabaeidae (Coleoptera). Annuals of the
Entomology Society of America 50(6): 562-577.
Barbosa,
P.,
Berry, D.L. & Kary, C.S. 2015. Insect
Histology: Practical
Laboratory Techniques. Oxford: Wiley Blackwell.
Berridge, M.J. & Oschman, J.L. 1969. A
structural basis for fluid secretion by malpighian tubules. Tissue & Cell 1: 247-272.
Billen, J. & Wilson, E.O. 2008. Social
insect histology from the nineteenth century: The magnificent pioneer sections of Charles Janet. Arthropod Structure & Development 37(3): 163-167.
Bushchini, M.L.T. 2007. Life-history
and sex allocation in Trypoxylon(syn. Trypargilum) lactitarse (Hymenoptera; Crabronidae. Journal of
Zoological Systematics and Evolutionary Research 45(3): 206-213.
Candan, S., Özyurt Koçakoğlu, N. & Suludere, Z. 2018. Morphological
and histological structure of the male reproductive system of the water strider Gerris lacustris (Linnaeus 1758) (Gerridae, Heteroptera). Microscopy
Research and Technique 81(7): 770-780.
Chapman,
R.F. 1998. The
Insects: Structure and Function (4th ed.). Cambridge University Press.
Cheng,
L. 1985. Biology
of halobates(Heteroptera: Gerridae). Annual
Review of Entomology 30: 111-135.
Cheng,
L. 1974. Notes
on the ecology of the oceanic insect Halobates. Marine
Fisheries Review 36(2): 1-7.
Cheng, L. & Mishra, H. 2022. Why did only one genus of insects, Halobates,
take to the high seas? PLoS Biolplogy 20(4): e3001570.
da Cruz-Landim, C. 2001. Organization of the cysts in bee (Hymenoptera, Apidae) testis: Number of spermatozoa per cyst. Iheringia, Série Zoologia 91: 183-189.
Dai, L., Yang, B., Wang, J., Zhang, Z., Yang, R., Zhang, T., Ren, Z. & Lin, C. 2019. The anatomy and ultrastructure of
the digestive tract and salivary glands of Hishimonus lamellatus (Hemiptera: Cicadellidae). Journal of Insect Science 19(4): 3.
Dallai, R., Gottardo, M. & Beutel,
R.G. 2016. Structure and evolution of insect
sperm: New interpretations
in the age of phylogenomics. Annual Review of Entomology 61(1): 1-23.
Eichler, K., Li, F., Litwin-Kumar, A., Park, Y., Andrade, I., Schneider-Mizell, C.M., Saumweber,
T., Huser,
A., Eschbach,
C., Gerber, B., Fetter, R.D., Truman,
J.W., Priebe, C.E., Abbott, L.F., Thum,
A.S., Zlatic, M. & Cardona, A. 2017. The complete connectome of
a learning and memory centre in an insect brain. Nature 548(7666): 175-182.
Elelimy, H.A.S., Ghazawy, N.A., Omar,
A.H. & Meguid, A.A. 2017. Morphology, histology and ovary development of the female reproductive system
of Spilostethus pandurus (Scopoli) (Hemiptera: Lygaeidae).African
Entomology 25: 515-522.
Fialho, M.D.C.Q., Zanuncio, J.C., Neves, C.A., Ramalho, F.S. & Serrão, J.E. 2009. Ultrastructure
of the digestive cells in the Midgut of the predator Brontocoris tabidus (Heteroptera: Pentatomidae) after different feeding
periods on prey and plants. Annals
of the Entomological Society of America 102(1): 119-127.
Grodowitz, M.J.,
Reed, D.A., Elliott, B. & Perring, T.M. 2019. Female
reproductive system morphology and the development of a physiological age-grading system for Bagrada hilaris (Hemiptera: Pentatomidae). Journal of Insect Science 19(2): 1-9.
Gullar, P.J. &
Cranston, P.S. 2014. The Insects: An Outline of Entomology. 5th ed. Wiley Blackwell.
Happ, G.M. 1984. Insect ultrastructure, Volume I,
edited by King, R.C. & Hiromu, A. BioScience 34(1): 52.
Himuro, C. & Fujisaki, K. 2008. Males of the seed bug Togo hemipterus(Heteroptera: Lygaeidae) use accessory gland substances to
inhibit remating by females. Journal of Insect Physiology 54(12): 1538-1542.
Howard, S.R., Avarguès-Weber, A.,
Garcia, J.E., Greentree, A.D. &
Dyer, A.G. 2018. Numerical
ordering of zero in honeybees. Science 360: 1124-1126.
King, M., Eubel, H.,
Millar, A.H. & Baer, B. 2011. Proteins within the seminal fluid are crucial to keep sperm
viable in the honeybee Apis mellifera. Journal of Insect Physiology 57(3): 409-414.
Klowden, M. 2013. Physiological
Systems in Insects. 3rd ed. Elsevier
Science.
Koçakoğlu, N.Ö., Candan, S. & Suludere,
Z. 2019. Notes
on the morphology and histology of the ovarioles of Gerris lacustris(L.)(water
strider)(Insecta: Hemiptera: Heteroptera: Gerridae). Zoologischer Anzeiger 278: 84-89.
Langkawong, K., Senarat, S., Chantarasawat,
N., Boonyoung, P. & Poolprasert, P. 2013. Identification
of some organ by histology and histochemistry of
female blister beetles, Epicauta waterhousei(Haag-Rutenberg, 1880): The
abdominal part. Journal of Science and Technology, Ubonratchathane University 15: 1-10.
Li, K.,
Zhang, J-H., Yang,
Y-J., Han,
W. &
Yin, H. 2018. Morphology
and fine organization of the midgut of Gampsocleis gratiosa (Orthoptera: Tettigoniidae). PLoS ONE 13(7): e0200405.
Lino-Neto, J., Dolder, H., Mancini,
K., Mercati, D. & Dallai, R. 2008. The
short spermatodesm of Arge pagana (Hymenoptera: Symphyta). Tissue
and Cell 40(3): 185-193.
Liu, L. & Hua, B.Z. 2018. Ultrastructure
of the larval Malpighian tubules in Terrobittacus implicatus (Mecoptera: Bittacidae). Protoplasma 255(4): 1121-1128.
Mahadik, G.A., Agustí, S. & Duarte, C.M. 2019. Distribution
and characteristics of Halobates germanus population in the Red Sea. Frontiers
in Marine Science 6: 408.
Mahadik, G.A.,
Hernandez-Sanchez, J.F., Arunachalam, S., Gallo Jr., A.,
Cheng, L., Farinha,
A.S., Thoroddsen, S.T.,
Mishra, H. & Duarte, C.M. 2020. Superhydrophobicity and size reduction enabled Halobates (Insecta: Heteroptera, Gerridae) to colonize the open ocean. Scientific Reports 10(1): 7785.
Marana,
S.R.,
Ribeiro, A.F.,
Terra, W.R. &
Ferreira, C. 1997. Ultrastructure
and secretory activity of Abracris flavolineata (Orthoptera: Acrididae) midguts. Journal
of Insect Physiology 43(5): 465-473.
Moreira,
P.A., Araújo, V.A., Zama,
U. &
Lino-Neto, J. 2008. Morphology
of male reproductive system in three species of Trypoxylon (Trypargilum) Richards (Hymenoptera: Crabronidae). Neotropical Entomology 37(4): 429-435.
Munhoz, I.L.A., Serrão, J.E., Dias, G., Lino-Neto, J., de Melo, A.L. & Araújo, V.A. 2021. Anatomy and
histology of the male reproductive tract in giant water bugs of the genus Belostoma Latreille,
1807 (Heteroptera, Belostomatidae). International
Journal of Tropical Insect Science 41: 303-311.
Nocelli, R., Cintra-Socolowski, P., Roat, T., Silva-Zacarin, E. & Malaspina, O. 2016. Comparative
physiology of Malpighian tubules: Form and function. Open Access Insect Physiology 6: 13-23.
Novais, A.M., Dias, G. & Lino-Neto, J. 2017. Testicular,
spermatogenesis and sperm morphology in Martarega bentoi (Heteroptera: Notonectidae). Arthropod
Structure & Development 46(4): 635-643.
Özyurt, N., Amutkan, D., Polat, I., Kocamaz, T., Candan, S. & Suludere, Z. 2017. Structural
and ultrastructural features of the Malpighian tubules of Dolycoris baccarum(Linnaeus 1758), (Heteroptera: Pentatomidae). Microscopy Research and Technique 80(4): 357-363.
Polilov, A.A. &
Makarova, A.A. 2020. Constant neuropilar ratio in the insect brain. Scientific Reports 10: 21426.
Poolprasert, P. & Senarat, S. 2014. Structural
systems of Oligotoma saundersii (Embioptera: Oligotomidae) in
Thailand. Journal
of Science and Technology RDI KPRU 1(1): 35-46.
Poolprasert, P., Senarat, S., Kettratad,
J. Kaneko, G., Mongkolchaichana,
E., Charoenphon, N. & Thaochan, T. 2022. Comprehensive structure of the female marine water-strider Asclepios annandalei Distant, 1915 from Pranburi River Estuary, Thailand: New information for the Genus Asclepios. Tropical
Life Sciences Research 33(3): 47-60.
Poolprasert, P., Chitchamnong, A., Boonyoung, P., Senarat, S., Dokchan, P., Mongkolchaichana, E., Likittrakulwong, W. & Berry, G. 2020. COI
nucleotide sequence confirms the species of common posy butterfly, Drupadia ravindra Horsfield, 1829 and histological feature reveals its microanatomical structure of nervous system and sense
organs. Khon Kaen Agriculture Journal 1: 755-764.
Presnell, J.K. & Schreibman,
M.P. 1997. Humason’s Animal Tissue Techniques. Johns Hopkins University
Press.
Roelfstra, L., Vlimant, M., Betschart,
B., Pfister, K. & Diehl, P.A. 2010. Light
and electron microscopy studies of the midgut and
salivary glands of second and third instars of the
horse stomach bot, Gasterophilus intestinalis. Medical and
Veterinary Entomology 24(3): 236-249.
Rothman,
J.E. & Orci,
L. 1992. Molecular
dissection of the secretory pathway. Nature 355(6359): 409-415.
Scheys, F.,
Van Damme, E.J.M., De Schutter, K., Staes, A., Gevaert,
K. & Smagghe, G. 2018. Evolutionarily conserved and
species-specific glycoproteins in the N-glycoproteomes of diverse insect species. Insect
Biochemistry and Molecular Biology 100: 22-29.
Standlea, P.P. & Yonke, T.R. 1968. Clarification
of the description of the digestive system of Heliothis zea. Annuals of the Entomology Society of America 61(6): 1478-1481.
Stöckl, A.L. & Heinze, S. 2015. A
clearer view of the insect brain-combining
bleaching with standard whole-mount
immunocytochemistry allows confocal imaging of pigment-covered brain areas for 3D reconstruction. Frontiers in Neuroanatomy 121: 1-8.
Suvarna, S.K.,
Layton, C. & Bancroft, J.D. 2013. Bancroft’s Theory and Practise of
Histological Techniques. 7th ed. Churchill Livingstone.
Triplehorn, C.A. & Johnson, N.F. 2005. Borror and
Delong’s
Introduction of the Study of Insect. 7th ed. Belmont: Peter
Marshall Publishing.
Utiyama, A.H., Terra, W.R. & Ribeiro, A.F. 2016. The
digestive system of the leafhopper Bucephalogonia xanthophis (hemiptera, cicadellidae): The organization
of the luminal membrane complex. Journal of
Entomological Research 40(4): 339.
Vandenborre, G., Smagghe, G., Ghesquière,
B., Menschaert, G.,
Rao, R.N., Gevaert,
K. & Van Damme, E.J.M. 2011. Diversity in
protein glycosylation among insect species. PLoS ONE 6(2): e16682.
White,
F.B. 1883. Report
on the pelagic Hemiptera procured during the
voyage of H.M.S. Challenger,
in the years 1873-1876. Zoology 7: 1-85.
*Corresponding
author; email: narit.t@psu.ac.th
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