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The morphology of Laemobothrion (Laemobothrion) maximum (Phthiraptera: )

Article in Parassitologia · May 1995 Source: PubMed

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THE MORPHOLOGYOF LAEMOBOTHRION (LAEMOBOTHRION)MAXIMUM (PHTHIRAPTERA:LAEMOBOTHRIIDAE)

T.M. PEREZ,T.E. GRANADOS,I. RU1Z Departamentode BiologíaAnimal, Vegetaly Ecología,Facultadde CienciasExperimentales,Apartado 62, Universidadde ¡aen, 23071, ¡aen, Spain.

Abstract. Adult specimens of Laemobothrion (L.) maximum (Scopoli, 1763), a buzzard species, were studied using scanning electron microscopy and paying special attention to sen- sitive structures, mainly those located on the head, mouthparts, abdomen and legs. Data on shape and size of palpal and antennal sensilla, as well as post-spiracular ones, were obtained. Some modifications of the mouthparts were observed.

Key words: Laemobothrion (L.) maximum, SEM, morphology. 1

The family Laemobothrüdae comprises a num- bureo, kept in captivity in the Acebuche ber of monogeneric species characterized by Recuperation Center, Doñana National Park, their large size and parasitizing several Spain and in CREA Las Mimbres: Agencia de orders: Podicipediformes, Ciconiiformes, Fal- Medio Ambiente, Granada, Spain. For this coniformes, Galliformes and Gruiformes (Hop- study 45 specimens (20 males and 25 females) kins and Clay, 1952; Nelson and Price, 1965; were used. Clay, 1970). On the basis of their morpholog- Lice removed from the host pluniage were ical characters only a few Laemobothrion spe- fixed in a filtered 10% formaldehyde solution. cies can be distinguished as ectoparasites of Preparation routines for SEM started with Falconiformes (Nelson and Price, 1965). cleaning the material. Specimens were washed Laemobothrion (L.) maximum (Scopoli, 1763) consecutivelyin 65% ethanol, bidistilledwater, has been considered as a cosmopolitan species, 5% aqueous Triton XRand again in bidistilled being cited on 32 raptor species belonging to water. In each step (5-10 minutes) manual 18 genera (Clay, 1976). cleaning was improved with a thin brush un- Scanning electron microscopy (SEM) has der a stereoscopic microscope. After this been used for taxonomic purposes in the study process lice were sonicated for 5 minutes in ofseverallicespecies(Clay,1966; 1969;1970; 65% ethanol. Clayton and Price, 1984; Zlotorzycka and Kass- After cleaning, lice were pre-dehydrated for ner, 1986; Kassner and Zlotorzycka, 1987). 15 minutes in each 70%, 90% and 100% Cephalic organs like the antennae, mouthparts ethanol solution. Then, material was in- and palpi have been the phthirapteran struc- troduced in amyl acetate (15 minutes) and fi- tures studied most by means of SEMtechniques nally dehydrated by means of critical point at in arder to improve our knowledge of the mor- - 31 DC and 90 bars in the presence of CO2 phology and receptor function of these organs as the transition fluido Lice were mounted (Miller, 1971; Eicher and Sixl, 1974; Stendel posteriorly on standard pin type SEM mounts and Holm, 1975; Eichler et al., 1976; Slifer, using double-sided tape. 1976;Szczesna,1984;Clarke,1990;Zlotorzyc- After mounting, specimens were sputter- ka, 1990) as well as the function of mouthparts coatedwithgoldin a PolaronE 5000machine } (Smithand Titchener, 1980). and viewed in a Zeiss DSM 950. This paper supplements the existing Scales included in the photographs description of the buzzard louse, Laemobothri- represent micrometres. on (1.) maximum, and pays specialattention to cephalic and legs structures. REsULTs

MATERIALS ANO METHOOS The base of the maxillary palpi and labium, and the regían between these structures, bear Adult Laemobothrion (L.) maximum were col- numerous small prolongations as shown in lected from several infested buzzards, Buteo Figure 1. Figure 2 shows another cuticular Figs 1-6. Laemobothrion (L.) maximum. Fig. 1. Base of the maxillary palpi, labium and regían between these structures. Fig. 2. Cuticular modification at the base of the mandibies. Fig. 3. End of a maxillary palpus. A, B, C: basiconic sensilla. Fig. 4. Apex of a labial palpus. Fig. 5 Third antennal segment. Fig. 6. Head, lateral view. E: eyes; AP: antennal pit; CCT: cephalic ctenidia. Scales represent micrometres. Figs 7-12, Laemobothrion (L.) maximum Flg, 7. Tarsal claws, Arrows show the inner protuberances Fig. 8, Baslconic sensilla (B8) surrounding the tarsal orilice located between the tarsal claws. Fig. 9, Tibial extreme, Cllmbing organ. Fig. 10. Postspiracular seta (P) and adjacent sensilla (A). Fig. 11. Oetail 01the cuticular surface 01 the abdominal terguites, Fig. 12. Mlcrotrichia located laterally on abdominal sternites IV and V, 8cales represent mlcrometres. 48 /.M. Perez, /.E. Granadas, 1. Ruiz

Figs 13, 14. Laemobothrion (L.) maximum. Fíg. 13. Male. Tip 01 the abdomen. Fig. 14. Female. Vulvar regían. Scales represent micrometres. modification found on the base of the mandi- Richards and Davies, 1977), located at the bles and near them consisting of rigid prolon- apex of the tibia. An abundant pilosity with gations with a variable number of indentations. some interspersed trichoid sensilla can be ob- The 4-segmented maxillary palpi (Fig. 3) served. present several trichoid sensilla and > 15 basi- In each side of the pleural region of some conic sensilla located apically. Three types of abdominal segments (11to VIII) a postspiracu- these structures have been distinguished ac- lar seta (P) is inserted (Fig. 10). This structure cording to their size and appearance. Sensil- is a very long hair associated with two small lum type A is a single one basally folded and adjacent sensilla (A). Each of them are in- partially imbedded in the cuticle. Its length is dependentIy inserted. ea. 10 ¡.Lm.Sensilla named type B are normal Figure 11 shows the reticulated cuticle of basiconic sensilla with variable size. Finally the tergal abdominal surface. A detail of the there is a very globular sensillum (type C). On small combs, or microtrichia, located lateral- the extreme of the labial palpi (Fig. 4) usually ly on abdominal sternites IV and V is depict- five sensilla are inserted, with a IDean length ed in Figure 12. In this species, this kind of > 15 ¡.Lm.Their surface is grooved and they structure also occurs on the ventral surface of might be considered as basiconic sensilla. femur III. The four-segmented antennae are located In Figure 13 the terminal region of the in the antennal pits. The third segment shows male abdomen shows a wide opening bordered severallong hairs (Fig. 5). Figure 6 showsa by numerous long hairs; the female vulvar pleural view of the head at the level of the two region is shown in Figure 14, and is charac- eJes (E). Justin front of them the antennalpit terized by the insertion of a large number of (AP) is surrounded by long hairs and trichoid chaetic sensilla, both on the external and in- sensilla. Near the eJes there is a row of trichoid ternal surfaces. sensilla measuring about 50 ¡.Lmin length and, below them, several rows of rigid spines, the DISCUSSION cephalic ctenidia. Tarsal claws are perpendicularly articulat- One of the most common receptors found in ed to the tarsus (Fig. 7) and there is a termi- L. maximum were trichoid sensilla, with vari- nal orifice bordered by basiconic sensilla (BS) able size, type of insertion and thickness. Many (Fig.8). Clawmovementsseemto be limited of these structures operate as mechanical or by two cuticular protuberances. The structure tactile receptors (Slifer, 1960). We have ob- represented in Figure 9 is the climbing organ tained no evidence of the existence of pares on (according to the terminology given by the surface of these structures. Nevertheless, in Morphology 01 Laemobothrion (L.) maximum 49 some cases (in legs) superficial longitudinal served on the apex of the labial palpi (Fig. 4). grooves were observed in trichoid sensilla. This Depending on the location, ultrastructure, wall type of trichoid sensilla has been also fOund thickness and innervation of the non-paraos in other lice species, e.g. antennal apices of De- basiconic sensillathey mar acquire several func- geeriellafulva (Giebel, 1874) and Craspedor- tions, such as termoreceptors, hygrareceptors or rhynchus platystomus (Burmeister, 1838) and mechanoreceptors (Slifer, 1970; Altner, 1977). abdominal terguites of Colpocephalum meridi- However, complementary ultrastructural and onale Pérez et al., 1988 (Perez, 1990), as well electrophysiological studies are needed in ord- as in other orders: Diptera (McIver, er to know the exact function of each sensillum. 1971; Mercer and McIver, 1973), Hymenop- Neither placoid sensilla, also named "cir- tera (Cave and Gaylar, 1987) or Coleoptera cular areas" (Clay, 1970), nor "porous argans" (Bland, 1984) among others. These graoved (Agren,1975;Szczesna,1984;Zlotorzyclaand trichoid sensilla might operate as olfactory Kassner,1986),nor coeloconic,nor campani- receptors, since the graoves would replace the farm sensillawerefoundin L. maximum.Such characteristic pore-tubule system of sensilla are typical for ischnoceran Phthirap- chemoreceptors found in various other tera (Kimand Ludwig, 1982). (Bay and Pitts, 1976; Slifer, 1976; Altner, With regards to the mouthparts, the most 1977). conspicuous modification observed, apart fram Apart fram the taxonomic impartance of the sharp mandibles, were the indented rigid the presence/absence, shape and size of the pralongations located clase to these organs post-spiracular seta and adjacent sensilla (Clay, (Fig. 2). In our opinion, these structures, as 1954) we believe that these structures might act well as the mandibles, might be involved in ob- as amplifying the mechanical stimuli, in that taining host blood. Haematophagy has been when the seta is bent it stimulates the adjacent reportedin thisspecies(Perezet al., 1994),as sensilla. wellas in Laemobothrion(L.) vulturis (Zlotor- Basiconic sensilla can be distinguished zycka and Danecki, 1969; Srivastava, 1974). fram trichoid ones by the thicker aspect of their The arrangement, articulation, size and de- prajected portion. Thickness of their cuticular velopment of the legs of L. maximum might be wall is variable, and the surface of these sen- associated with the species very fast locomo- silla can be graoved, sculptured or paraos. tion in practically any direction: lateral, These structures usually respond to diverse posterior-anterior and anterior-posterior, move- chemical stimuli (Richards and Davies, 1977). ments we have actually seen in live specimens This type of sensilla is also widely distributed during sampling. Moreover, the climbing or- in phthirapteran species, mainly in cephalic or- gan makes the locomotion of this louse on very gans, such as the maxillary palpi (Clay, 1966; smooth surfaces like glass, metal or plastic very 1969; Perez, 1990), antennal ends (Clay, 1969; easy. This behaviour might compensate for its 1970; Miller, 1971; Ubelaker et al., 1973; poor resistance to adverse conditions. Slifer, 1976; Szczesna, 1984; Kassner and There is evidence that combs (both cephal- Zlotorzycka,1987; Clarke, 1990),or the gu- ic, femoral and sterno-abdominal) provide ad- Iar arca of several amblyceran species (Clay, ditional methods by which the lice attach to 1969). Basiconic sensilla have also been com- host feathers. The mechanism of combs might monly reported from cephalic organs of other also be regarded as an adaptation that resists insectorders: Plecoptera(Kapoor, 1989),Or- dislodgement, or capture, by the host, as in the thoptera (Bland, 1982), Diptera (Mercer and case of fleas (Humphries, 1967; Kim, 1985) McIver, 1973), or Coleoptera (Arbogast et al., and other ectoparasitic insect groups. 1972) among others. However,Marshall(1980)argued that combs As in the case of the trichoid sensilla we in all ectoparasites, merely pratect mobile have found no pares on the basiconic sensilla joints and the membrane beneath. surface, but in the species studied short and graoved basiconic sensilla have been observed ACKNOWLEDGEMENTS at the antennal apices. This type of sensilla was also found in the antennal end ofLaemobothri- We wish to acknowledge the staff of the Grana- on (L.) vulturis(Fabricius,1775)(Clay,1970). da University Electron Microscopy Unit far their Longer grooved basiconic sensillawere also ob- valuable assistance in this work. We are also in- 50 lM. Perez, lE. Granadas, 1. Ruiz

debted to Mrs C. Sánchez and Mr M. Arias, Hopkins GHE, Clay T (1952). A check-list of the genera Doñana National Park, and Mr F. Aranda, Agen- and species of . British Museum (Natural cia de Medio Ambiente (Granada), for their col- History), London, 362 pp. laboration in collecting specimens. Humphries DA (1967). Function of combs in ectopara- sites. Nature 215: 319. REFERENCES KapoorNN (1989). Distribution and inervation of sen- silla on the mouthparts of the carnivoraus stonefly Agren L (1975). Comparison between air drying and nymph, Paragnetita media (Walker) (Plecoptera: Per- critical point drying for SEM studies of the anten- lidae). Can J Zool 67: 831-838. nae of Apis mellifera L. (Hymenoptera: Apidae). Kassner 1, Zlotorzycka J (1987). The problems of the Zoon 3: 155-158. preparation of the antennal sensilla of insects in Altner H (1977). Insect sensillum specificity and struc- scanning electron micrascope. Wiad Parazytol 33: , ture: an approach to a new typology. In: Olfaction 93-97. , and taste (J Le Magnen, P McLeod, eds) París: Kim KC (1985). Co-evolution of parasitic 295-303. and . John Wiley and SaTIs, New York, }. Arbogast RT, Roppel RM, Carthon M (1972). 800 pp. Hygrareceptors of adult sawtoothed grain beetles, Kim KC, Ludwig HW (1982). Parallel evolution, cladis- Oryzaephilus surinamensis (L.) (Coleoptera, Cucuj- tics and classification of parasitic . Ann En- idae). Can J Zool 50: 1147-1153. tamal Soc Am 75: 537-548. Bay DE, Pitts CW (1976). Antennal olfactory sensilla Marshal AG (1980). The function of combs in ectopara- of the face fly, Musca autumna/is De Geer (Diptera: sitic insects. In: Fleas (R Traub, H Starcke, eds) A.A. Muscidae). Int J Insect Morphol Embryol 5: 1-16. Bakelma, Rotterdam, pp 79-87. Bland RG (1982). Morphology and distribution of sen- Mclver S (1971). Comparative studies on the sense or- silla on the antennae and mouthparts of Hypoch- gans on the antennae and maxillary palps of select- lora alba (Orthoptera: Acrididae). Ann Entomol Soc ed male culicine mosquitoes. Can J Zool 49: Am 75: 272-283. 235-239. Bland RG (1984). Mouthpart sensilla and mandibles of Mercer KL, Mclver S (1973). Studies on the antennal the adult alfalfa weevil Hypera postica and the Egyp- sensilla of selected black-flies (Diptera: Simulidae). tian alfalfa weevil H. brunneipennis(Coleoptera: Cur- Can J Zool 51: 729-734. culionnidae). Ann Entomol Soc Am 77: 182-190. Miller FH (1971). Scanning electro n microscopy of Cave RD, Gaylor MJ (1987). Antennal sensilla of male Echinophthirus horridus (Von Olfers), Antarctophthi- and female Telenomus reynoldsi Gordh and Coker rus callorhini (Osborn) and Proechinophthirus fluc- (Hymenoptera: Scelionidae). Int J Insect Morphol tus (Ferris) with emphasis on the antennal structures Embryol 16: 27-39. (Anoplura: Echinophthiridae). J Parasitol 57: Clarke AR (1990). External morphology of the anten- 668-674. nae of Damalinia avis (Phthiraptera: Trichodecti- Nelson RC, Price RD (1965). The Laemobothrion (Mal- dae). J Morphol 203: 203-209. lophaga: Laemobothriidae) of the Falconiformes.J Clay T (1954). The post-spiracular seta and sensillum Med Entomol 2: 249-257. in the Mallophaga (Insecta). Ann Mag Nat Hist ser 12 7: 716-718. Perez JM (1990). Sobre algunos aspectos de la parasita- ción por malófagos en aves de presa. PhMD The- Clay T (1966). A new species of Apterigon (Mallopha- sis, Granada University. ga: ). The Entomologist 99: 290-293. Perez JM, Extremera AL, Ruiz I (1994). Bacteriologi- Clay T (1969). A key to the genera of the Menoponi- cal study of the feathers and lice of captive com- dae (: Mallophaga: Insecta). Bull Brit Mus mon buzzards (Buteo Buteo). Avian Pathol 23: (Nat Hist) Entomol 24: 75-98. 163-168. Clay T (1970). The Amblycera (Phthiraptera: Insecta). Bull Brit Mus (Nat Hist) Entomol 25: 1-26. Richards OW, Davies RG (1977). Imm's General Text- Clay T (1976). Geographical distribution of the avian book of Entomology. Chapman and Hall, London, l lice (Phthiraptera): a review. J Bombay Nat Hist Soc 418 + 1354 pp. Slifer EH (1960). A rapid and sensitive method for iden- 71: 536-547. ~ Clayton DH, Price RD (1984). of the tifying permeable afeas in the body wall of insects. Ent News 71: 179-182. cursitansgroup (lschnocera: Philopteri- dae), parasites of owls (Strigiformes). Ann Entomol Slifer EH (1970). The structure of Soc Am 77: 340-363. chemoreceptors. Ann Rev Entomol 15: 121-142. Eichler W, Sixl W (1974). Rasterelektronen- Slifer EH (1976). Sense organs on the antennal flagel- mikroskopische aufnahmen van Eomenacanthus lum of a (Mallophaga). J New York En- stramineus. Angew Parasitol 15: 151-156. tamal Soc 84: 159-165. Eichler W, Sixl W, Gunther KK (1976). Smith HV,' Titchener RN (1980). Mouthparts of ec- Rasterelektranen-mikroskopische bilder des tauben- toparasites and host damage. Prac Roy Soc Edin- federlings. Angew Parasitol 17: 218-221. burgh 79: 139-141. Morphology 01 Laemobothrion (L.) maximum 51

Srivastava RK (1974). Studies on the anatomy and louse, Phthirus pubis (Linnaeus, 1758). J Parasitol histology of various organ systems of Laemobothri- 59: 913-919. on percnopteris (Gervais) (Mallophaga: Amblycera). Zlotorzycka J (1990). Ultrastructure of head surface of PhMO Thesis, Banaras Hindu University. some Bovicolidae (Mallophaga, ). Wiad Stendel W, Holm R (1975). Surface structures ofmouth Parazytol 36: 39-45. parís and attachment organs of some ectoparasites. Zlotorzycka J, Oanecki J (1969). Effects of a mass oc- Vet Med Rev 1975: 207-227. currence of bird !ice Mallophaga belonging to the Szczesna Z (1984). The sense organs on antennae of subespecies Laemobothrion vu/turis daneckii zlot. on Pediculus h. humanus (L.) (Anoplura, Pedicu!idae) a specimen of Lammergeier Gypaetus barbatus (L.). in post-embryonic development stages. Acta Parasitol Przeg Zool 13: 331-332. Poi 29: 395-404. Zlotorzycka J, Kassner J (1986). Morphologische über Ubelaker JE, Payne E, Allison VF, Moore OV (1973). die fühlersinnesorgane van Ischnozeren vogel- Scanning electron microscopy of the bullan pubic Mallophagen. Angew Parasitol 27: 241-251.

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