The morphology, arrangement, and ultrastructure of a new type of microtrich sensilla in marine isopods (Crustacea, Isopoda)
© Khalaji-Pirbalouty; licensee Springer. 2014
Received: 10 August 2013
Accepted: 6 January 2014
Published: 27 January 2014
Microtrich sensilla are a special type of cuticular structures found on the external surface of amphipod and isopod crustaceans. These cuticular microstructures, being important for systematic and phylogenetic studies, display a wide diversity of shapes and distribution among different taxa. Here, the microstructure of the cuticular surface of 11 marine isopod species was investigated by scanning electron microscopy.
On the dorsal and lateral sides of all the taxa examined, only one distinct type of microtrich sensillum was found in the regular rows. While this structure is very similar to that of the Ib microtrich type (sensu Crustaceana 13:100–106, 1988), however, it is distinct from the previous type, in which it has an elongate cuticular ring or specialized collar encircling the shaft base of the microtrichs. The findings indicate that different taxa of marine isopods may show a new type of microtrich sensilla differing in morphology and arrangement.
The findings indicate that different taxa of marine isopods may show a new type of microtrich sensilla differing in morphology and arrangement.
KeywordsIsopoda Marine Cuticular surface Scanning electron microscopy
Examination of cuticular surface features of crustaceans, especially Peracarida, has been conducted for many years. Fish (1972) described the setae of the aquatic isopod Eurydice pulchra Leach, 1815 on the basis of size as either macrotrichs or microtrichs. Powell and Halcrow (1982) described the surface microstructures of several marine littoral and terrestrial isopods using SEM, and Oshel and Steele (1988) and Oshel et al. (1988) described and discussed the setae and microtrich sensilla of some amphipods. In most cases, these studies were conducted with an emphasis on only one type of cuticular structure, viz., tricorn setae (Holdich and Lincoln 1974;Schmalfuss 1978), sensory spines (Brandt 1988), pores (Halcrow and Bousfield 1987;Khalaji-Pirbalouty and Sari 2004 2006;Khalaji-Pirbalouty and Sari 2006), or microtrichs (Oshel et al. 1988;Platvoet 1985;Steele 1991;Olyslager and Williams 1993). Recently, Zimmer et al. (2009) described variation of five different kinds of cuticular structures for hyallelid amphipods, including 30 types of setae, four types of microtrich, and three types of pores. Of those, microtrich sensilla were found only on aquatic crustaceans, e.g., gammaridean amphipods and marine isopods; there is no report of these structures in terrestrial isopods. Fish (1972) used the term microtrich to refer to setae less than 10 μm in length. Later, Oshel et al. (1988) defined microtrichs as setae less than 25 μm in length with specialized sockets, and they divided microtrichs into two types, I and II, based on the socket morphology. Type I has a socket bearing a bowl-shaped, shallow depression, with a dome on one edge and is formed by 3 to 4 epidermal cells. Microtrich type II has a simple and circular socket. Type I microtrichs were further subdivided into three types (Ia, Ib, and Ic) on the basis of the setal morphology: Ia with a terminal pore directed to one side of the seta, Ib with long filaments radiating from a hood that may be one to two or more times as long as the setal shaft, and Ic a short and plumose setae whose filaments are either restricted to the apical end of the setal shaft or originate from the distal third of the shaft (see Oshel et al. 1988, pages 102 and 103, Figures two (a,b), three (a,b), and four). Microtrich sensilla type II are defined as short, longitudinally compressed seta with a bifurcate tip. Type II microtrichs also were called slide-line organ or flattened microtrichs on gammaridian amphipods by Platvoet (1985) and Platvoet et al. (2007). More recently, Kaim-Malka (2010) introduced the term ‘unispathes’ (along with spatheform organ for whole set of structures) instead of previous terms and despite the fact that spatheform is a common name for plants of the genus Arisaema. These structures have been found in many amphipods and also in some marine isopods (e.g., Platvoet 1985; Laverack and Barrientos 1985; Halcrow and Bousfield 1987; Oshel et al. 1988; Olyslager and Williams 1993; Kaim-Malka 2010). This paper describes the morphology and arrangement of a new kind of Ib microtrich sensilla sensu (Oshel et al. 1988) on marine isopods.
Specimens for this study were collected primarily from intertidal and subtidal habitats along the Iranian coastline of the Persian Gulf. Collecting techniques included sieving sand and washing algae and sea grass, as well as direct capture. Excirolana sp., Dynamenella granulata (Javed and Ahmed 1988), Sphaeroma khalijfarsi (Khalaji-Pirbalouty and Wägele 2010 (Stebbing), Sphaeroma walkeri 1905), Sphaeromopsis sarii Khalaji-Pirbalouty and Wägele 2010), Cymodoce sp., Lanocira sp., and Atarbolana (Dana sp. were collected from the beach of the Persian Gulf. In addition, specimens of Excirolana orientalis 1853), Sphaeromopsis amathitis (Holdich and Jones 1973 Loyola e Silva ), and Sphaeromopsis mourei 1960 were obtained from Copenhagen Museum and the Museum of Tropical Queensland. Of these, Excirolana sp., E. orientalis, Lanocira sp., and Atarbolana sp. belong to the family Cirolanidae, and D. granulata, S. khalijfarsi, S. walkeri, Cymodoce sp., S. sarii, S. amathitis, and S. mourei belong to the family Sphaeromatidae. Scanning electron microscopy (SEM) specimens were washed in chilled 1% sodium acetate solution for 10 min and then cleaned using an ultrasonic cleaner to remove the attached sediment and debris from the cuticle. After the specimens were dehydrated in an ethanol series and after a final 100% ethanol, they were transferred to 100% hexamethyldisilazane (HMDS) through a three-graded series of ethanol-HMDS mixtures (100% E 2:1, 1:1, 1:2, 100% HMDS) in a fume hood. For the final step, the specimens were immersed in a HMDS container for 15 to 60 min, depending on their size. The samples were then mounted on stubs using double-sided carbon tapes before being coated with gold in a sputter coater to 40-nm thickness. The SEM micrographs were taken using a Hitachi S-2460 N SEM (Tokyo, Japan).
Description of microtrich structures on the cuticular surface of some representatives of marine isopods
Cuticular depressions are furnished with three to four knobs arranged in a semi-circular row; collar short, oval, anterior margin shorter than posterior one; shaft short with a tuft of long filaments (Figures 2B and 3B).
Cuticular depressions are furnished with three to five knobs arranged in a semi-circular row; collar short, anterior margin shorter than posterior one; shaft short with a tuft of long filaments (Figures 2A and 3A).
Simple cuticular depression; collar very short, oval; shaft very short with a tuft of long filaments (Figure 2C).
Collar very short, round; shaft long.
Shallow, flower-shaped cuticular depression; collar spool-shaped, large; shaft large with a tuft of long filaments (Figure 3E).
10 to 12
Shallow, flower-shaped cuticular depression; collar spool-shaped, large; shaft large with a tuft of long filaments (Figure 3F).
Collar short; shaft long with long filaments (Figure 4B).
4 to 5
Collar medium, shaft short with long filaments (Figure 4C).
In contrast to the previous taxa, on S. khalijfarsi Khalaji-Pirbalouty and Wägele 2010, microtrichs are located in ten rows (rather than six rows), and there are two rows on the mid-dorsal surface of the pleotelson and one row on each marginal surface (Figure 1C). Each microtrich bears a short cuticular collar, an elongate shaft and a tuft of approximately eight long distal filaments (Figures 2F and 4 Stebbing A). Similarly, on S. walkeri 1905, each structure has a short collar, a long shaft, and a few distal filaments (Figure 4B). However, on Cymodoce sp., each structure possesses a longer collar, very long shaft, and long distal filaments (Figures 2G and 4D).
The cuticular microstructures of a few aquatic species of crustaceans like amphipods and isopods have been studied previously by SEM (e.g., Schmalfuss 1978; Meyer-Rochow 1980; Powell and Halcrow 1982; Holdich 1984; Laverack and Barrientos 1985; Platvoet 1985; Oshel et al. 1988; Olyslager and Williams 1993; Halcrow and Bousfield 1987; Read and Williams 1991; Khalaji-Pirbalouty and Sari 2006; Zimmer et al. 2009; Kaim-Malka 2010). The majority of these studies investigated the cuticular surface of Amphipoda, and only few attempts have been conducted to study the microscopic structures on the tegument surface of aquatic isopods (e.g., Wägele 1993; Escobar et al. 2002; Brandt 1988; Kaim-Malka 2010). Different types of cuticular structures such as scales, setae, microtrichs, setules, pores, or denticles were observed in marine isopods. Of these, microtrich sensilla type II were found only in a few marine isopods. However, microtrich sensilla type II were observed in several amphipods (Platvoet 1985; Oshel et al. 1988; Zimmer et al. 2009; Kaim-Malka 2010). Recently, Kaim-Malka (2010 (Norman) found similar kinds of microtrich sensilla type II in Eurydice truncata 1868 (Lilljeborg) and Natatolana borealis 1851) and named them as ‘unispathes’. The structures reported here are very similar to type Ib microtrichs (sensu Oshel et al. 1988) reported for Amphipoda. However, the type Ib microtrichs reported here differ from those observed by previous authors for the majority of amphipods and also some isopods, because they have a cuticular collar that arises from the cuticular surface in the basal part of the seta. Moreover, the type Ib microtrichs reported here are arranged in regular and symmetrical rows on the body surface. Microtrich sensilla type II were not found in any species in this study. Kaim-Malka (2010 Norman) reported microtrich sensilla type II in the marine isopods E. truncata 1868 Lilljeborg and N. borealis 1851, both species are found in marine subtidal environments. E. truncata is restricted to depths of 50 to 200 m (Schotte 2012), and N. borealis is found more broadly at 5 to 1,478 m (Keable and Bruce 1997; Johansen and Brattegard 1998). These data suggest that microtrich sensilla type II may characterize swimming species. In addition, Kaim-Malka (2010) stated that this structure may be less well developed or completely absent among species less able to swim and living in intertidal habitats. The type Ib microtrichs reported here are well developed on the dorsal and lateral sides of the examined marine species.
A comparison of these microtrichs shows that the number of distal filaments has correlation with living habit on different habitats. The result suggests that swimming species (e.g., Excirolana and Lanocira) have microtrichs with high number of distal filaments (15 to 30 filaments), whereas cirolanid isopods living in low algal turfs over rocky shore, e.g., Atarbolana sp., have microtrichs bearing few distal filaments (approximately five). In less-able swimming sphaeromatid isopods examined here, this structure has clearly low number of distal filaments. For example, in S. walkeri, S. khalijfarsi, D. granulata (all living in burrows or beneath stones in intertidal habitats), and Cymodoce sp. (live amongst algal and seagrass beds in subtidal habitats), the microtrichs have approximately four to eight distal filaments. Whereas, in S. sarii, S. mourei, and S. amathitis (mainly occur and swim in intertidal tide pools and partly on low algal turfs), this structure has approximately 8 to 12 filaments. In conclusion, the number of distal filaments on these structures has close correlation with the habitat structure. Swimming species in water column have more filaments than low swimmer species and species that living in burrows and beneath stones in intertidal habitats. According to Halcrow and Bousfield (1987), Watling (1989), Halcrow and Powell (1992), Khalaji-Pirbalouty and Sari (2006), Zimmer et al. (2009), and Kaim-Malka (2010), the kind and number of cuticular structures represent diagnostic traits for the identification of crustaceans, e.g., copepods and amphipods, as well as isopods, both on genus and species level. Therefore, the arrangement, diversity, and morphology of these elements constitute important tools for taxonomic analyses among genera of marine isopods or among species within a genus. For example, the arrangement and number of rows of these cuticular structures, their collar shape, shaft, and the number of filaments are commonly similar in two examined species of the genus Excirolana and three species of Sphaeromopsis. However, the shape of the cuticular collar, length of shaft, and the number of filaments are different between the examined species.
There are a variety of sensory receptors that transmit information to the central nervous system of crustaceans. Among the most obvious of these sensory structures are the different types of setae and sensilla that cover various regions of the body. A mechanosensory function is suggested by several authors for these kinds of cuticular structures (Fish 1972; Rider 1978; Bush and Laverack 1982; Platvoet 1985; Brandt 1988; Wägele 1993; Escobar et al. 2002). In addition, according to Brandt (1988), Laverack (1989), Felgenhauer (1992), and Escobar et al. (2002), sensory movable setae without a terminal pore have a mechanosensory function. As the cuticular structure reported here has no terminal pore on the apical part and also due to their arrangement and distribution over the body, a mechanosensory function can be supposed. These structures may provide the animals with information about the direction and possibly velocity and changes of water currents and hydrodynamic pressure. However, further investigations are necessary to clarify in greater detail the function of these structures in marine isopods.
This study suggests that the new type of microtrich sensilla reported here differ from those observed by previous authors for amphipod and isopod crustaceans, in which they have a cuticular collar that arises from the cuticular surface in the basal part of the seta. They are arranged in regular and symmetrical rows on the body surface. Notably, this structure with a relatively small number of distal filaments was observed in species with lower swimming ability.
I am very grateful to Dr. J. Olesen (Zoologisk Museum, University of Denmark, Copenhagen) and Mr. D. Potter (Museum of Tropical Queensland) for the loan of material. I thank especially Prof. J. W. Wägele (Zoologisches Forschungsmuseum Alexander Koenig, Bonn, Germany), Dr. F. D. Ferrari (retired), Mrs. M. Schotte (Smithsonian Institution Natural Museum of Natural History) for providing useful comments and language editing. Anonymous referees are appreciated for reviewing the manuscript and providing valuable comments and advices.
- Brandt A: Morphology and ultrastructure of the sensory spine, a presumed mechanoreceptor of Sphaeroma hookeri (Crustacea, Isopoda), and remarks on similar spines in other peracarids. J Morph 1988, 198: 219–229. 10.1002/jmor.1051980208View ArticleGoogle Scholar
- Bush BMH, Laverack GA: Mechanoreception. In The biology of crustacea. Edited by: Atwood HL, Sanderman DL. Academic, New York; 1982. vol 3.Google Scholar
- Dana JD: Crustacea. United States Exploring Expedition during the years 1838, 1839, 1840, 1841, 1842, under the command of Charles Wilkes, U.S.N 13th edition. 1853. pp i–viii. 1–685 (1852), 686–1618 (1853)Google Scholar
- Escobar E, Oseguera L, Vá́zquez-Nin GH, Alcocer J: The external micro-anatomy of the cephalon of the asellotan isopod Creaseriella anops . Hydrobiol 2002, 467: 57–62. 10.1023/A:1014976329076View ArticleGoogle Scholar
- Felgenhauer BE: External anatomy and integumentary structures. In Decapod crustacea. Microscopic anatomy of the invertebrates. Wiley-Liss, New York; 1992:7–43. vol 10.Google Scholar
- Fish S: The setae of Eurydice pulchra (Crustacea, Isopoda). J Zool 1972, 166: 163–177.View ArticleGoogle Scholar
- Halcrow K, Bousfield EL: Scanning electron microscopy of surface microstructures of some gammaridean amphipod crustaceans. J Crust Biol 1987, 7: 274–287.View ArticleGoogle Scholar
- Halcrow K, Powell CVL: Ultrastructural diversity in the pore canal systems of amphipod crustaceans. Tissue Cell 1992,24(3):417–436. 10.1016/0040-8166(92)90058-FView ArticleGoogle Scholar
- Holdich DM: The cuticular surface of woodlice: a search for receptors. Symp Zool Soc Lond 1984, 53: 9–48.Google Scholar
- Holdich DM, Jones DA: The systematics and ecology of a new genus of sand beach isopod (Sphaeromatidae) from Kenya. J Zool 1973, 171: 385–395.View ArticleGoogle Scholar
- Holdich DM, Lincoln RJ: An investigation of the surface of the cuticle and associated sensory structures of the terrestrial isopod, Porcellio scaber . J Zool 1974, 172: 469–482.View ArticleGoogle Scholar
- Javed W, Ahmed R: Two new species of the genus Dynamenella from the northern Arabian Sea (Isopoda). Crustaceana 1988, 55: 234–241. 10.1163/156854088X00320View ArticleGoogle Scholar
- Johansen PO, Brattegard T: Observations on behaviour and distribution of Natatolana borealis (Lilljeborg) (Crustacea, Isopoda). Sarsia 1998, 83: 347–360.Google Scholar
- Kaim-Malka RA: The spatheform organ: a ballasting organ in crustacean Peracarid species (Amphipods and Isopods). Memorie del Museo Civico di Storia Naturale di Verona – 2, serie. Sezione Scenziedelle vita 2010, 20: 3–68.Google Scholar
- Keable SJ, Bruce NL: Redescription of the North Atlantic and Mediterranean species of Natatolana (Crustacea: Isopoda: Cirolanidae). J Mar Biol Assoc UK 1997,77(3):655–706. 10.1017/S0025315400036134View ArticleGoogle Scholar
- Khalaji-Pirbalouty V, Sari A: Biography of amphipods (Crustacean: Amphipoda: Gammaridae) from the central Zagros Mountains, Iran with description of two new species. J Natur Hist 2004, 38: 2425–2445. 10.1080/00222930310001647406View ArticleGoogle Scholar
- Khalaji-Pirbalouty V, Sari A: Description of Gammarus baloutchi n. sp. (Amphipoda: Gammaridae) from Iran, based on light and electron microscopy. Zool Med Leiden 2006, 8: 91–100.Google Scholar
- Khalaji-Pirbalouty V, Wägele JW: A new species and a new record of Sphaeroma Bosc, 1802 (Sphaeromatidae: Isopoda: Crustacea) from intertidal marine habitats of the Persian Gulf. Zoota 2010, 2631: 1–18.Google Scholar
- Laverack MS: The diversity of chemoreceptors. In Sensory biology of aquatic animals. Edited by: Atema J, Fay RR, Popper AN, Tavolga WN. Springer, New York; 1989:287–312.Google Scholar
- Laverack MS, Barrientos Y: Sensory and other superficial structures in living marine crustaceans. T Roy Soc Edin-Earth 1985, 76: 123–136. 10.1017/S0263593300010397View ArticleGoogle Scholar
- Lilljeborg W: Norges crustaceer. 8th edition. Ofversigtaf Kongliga Vetenskapsakademiens, Forhandlingar, Stockholm; 1851:19–25.Google Scholar
- Loyola e Silva JD: Sphaeromatidae do litoral Brasiliero (Isopoda: Crustacea). Bolet da Univers do Parana Zoolog 1960, 4: 1–182.Google Scholar
- Meyer-Rochow VB: Cuticular surface structures in Glyptonotus antarcticus —a marine isopod from the Ross Sea (Antarctica). Zoomorphologie 1980, 94: 209–216. 10.1007/BF01081935View ArticleGoogle Scholar
- Norman AM: On two isopods, belonging to the genera Cirolana and Anilocra , new to the British Islands. Ann Mag Natural History 1868, 42: 421–422.View ArticleGoogle Scholar
- Olyslager NJ, Williams DD: Function of the type II microtrich sensilla on the lotic amphipod, Gammarus pseudolimnaeus Bousfield. Hydrobiol 1993, 259: 17–31. 10.1007/BF00005961View ArticleGoogle Scholar
- Oshel PE, Steele DH: Comparative morphology of Amphipod setae, and a proposed classification of setal types. Crustaceana 1988, 13: 90–99.Google Scholar
- Oshel PE, Steele VJ, Steele DH: Comparative morphology of amphipod microtríquia sensilla. Crustaceana 1988, 13: 100–106.Google Scholar
- Platvoet D: Slide-line organ in gammarid (Crustacea: Amphipoda). Beaufortia 1985,35(7):129–133.Google Scholar
- Platvoet D, Song Y, Li S, Van der Velde G: Description of the lateral line organ of Dikerogammarus villosus (Sowinsky, 1894), with discussion on its function (Peracarida, Amphipoda). Amphipod Pilot Species Project (AMPIS)-Report 4. Crustaceana 2007,80(11):1373–1392. 10.1163/156854007782605619View ArticleGoogle Scholar
- Powell CVL, Halcrow K: The surface microstructure of marine and terrestrial isopods (Crustacea, Peracarida). Zoomorphologie 1982, 101: 151–164. 10.1007/BF00312430View ArticleGoogle Scholar
- Read AT, Williams DD: The distribution, external morphology, and presumptive function of the surface microstructures of Gammarus pseudolimnaeus (Crustacea: Amphipoda), with emphasis on the calceolus. Can J Zool 1991, 69: 853–865. 10.1139/z91-129View ArticleGoogle Scholar
- Rider H: Die Sinnesorgane der Antennula von Ligidiumhypnorum (Cuvier) (Isopoda, Crustacea). Zool Jahrb Anat Ontog Tiere 1978, 100: 514–541.Google Scholar
- Schmalfuss H: Morphology and function of cuticular micro-scales and corresponding structures in terrestrial isopods (Crust., Isop., Oniscidea). Zoomorpholgie 1978, 91: 263–274. 10.1007/BF00999815View ArticleGoogle Scholar
- Schotte M: World marine, freshwater and terrestrial isopod crustaceans database. 2012.Google Scholar
- Stebbing TRR: Report on the Isopoda collected by Professor Herdman at Ceylon, in 1902. Report to the Government of Ceylon on the Pearl Oyster Fisheries of the Gulf of Manaar, Supplementary Report 4. Supplementary Reports, 23. 1905, 1–64.Google Scholar
- Steele VJ: The distribution and frequency of the type II microtrichs in some gammaridean amphipods. Hydrobiolo 1991, 223: 35–42. 10.1007/BF00047626View ArticleGoogle Scholar
- Wägele JW: Isopoda. Microscopic anatomy of invertebrates. In Crustacea. Edited by: Harrison FW, Hames AG. Wiley-Liss, New York; 1993:529–617. vol 9.Google Scholar
- Watling L: A classification system for crustacean setae based on the homology concept. Crustacean issues 6. A. A. In Functional morphology of feeding and grooming in crustacea. Edited by: Felgenhauer BE, Watling L, Thistle AB. Balkema, Rotterdam; 1989:15–26.Google Scholar
- Zimmer A, Araujo PB, Bond-Buckup G: Diversity and arrangement of the cuticular structures of Hyalella (Crustacea: Amphipoda: Dogielinotidae) and their use in taxonomy. Zoologia 2009,26(1):127–142. 10.1590/S1984-46702009000100019View ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.