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NOTES ON TAXONOMY AND DISTRIBUTION OF MYRSIDEA SERINI (SÉGUY, 1944) (PHTHIRAPTERA: AMBLYCERA: MENOPONIDAE) ON SOUTHERN SOUTH AMERICAN PASSERINE BIRDS (AVES: PASSERIFORMES)

Abstracts

Myrsidea serini (Séguy, 1944) is recorded from three different passerine hosts from Argentina and Chile: Carduelis barbata (Molina, 1782) (Fringillidae), Chrysomus thilius petersi (Laubmann, 1934) and Agelaioides badius badius (Vieillot, 1819) (Icteridae). Somatic features and body measurements from available specimens belonging to these host-populations are compared with those recorded from Old World hosts, finding only some slight differences in certain body measurements (here interpreted as correlated to differences in host sizes), but none in chaetotaxy. This species was synoxenic with Myrsidea psittaci Carriker, 1955 on C. t. petersi in at least two localities in Buenos Aires Province, Argentina. Comparative studies of external chorionic architecture of the eggs, preferential sites of oviposition, prevalence has been carried out for both species, along with some remarks concerning the still problematic species, Myrsidea argentina (Kellogg, 1906), originally recorded off Carduelis magellanica (Vieillot, 1805).

Myrsidea serini; Myrsidea argentina; Icteridae; Fringillidae; Synoxeny; Egg descriptions; Carduelis; Chrysomus; Agelaioides.


Myrsidea serini (Séguy, 1944) é registrada de três passarinhos distintos como hospedeiros na Argentina e Chile: Carduelis barbata (Molina, 1782) (Fringillidae), Chrysomus thilius petersi (Laubmann, 1934) e Agelaioides badius badius (Vieillot, 1819) (Icteridae). Características somáticas e medidas corporais de exemplares disponíveis dessas populações de hospedeiros são comparados com os registrados a partir de hospedeiros do Velho Mundo, com apenas pequenas diferenças em algumas medidas no corpo (aqui interpretadas como relacionado a diferença entre o tamanho dos hospedeiros), mas similares com relação a sua quetotaxia. Esta espécie foi encontrada em sinoxenia com Myrsidea psittaci Carriker, 1955 parasitando C. t. petersi em pelo menos duas localidades na Província de Buenos Aires, Argentina. Estudos comparativos da superfície coriônica dos ovos, sítios preferenciais de oviposição, e prevalência foram realizados para ambas as espécies, além de algumas observações sobre uma espécie ainda problemática, Myrsidea argentina (Kellogg, 1906), originalmente registrada em Carduelis magellanica (Vieillot, 1805).

Myrsidea serini; Myrsidea argentina; Icteridae; Fringillidae; Sinoxenia; Descrição de ovos; Carduelis; Chrysomus; Agelaioides.


INTRODUCTION

Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.) was first described from two specimens, male and female, taken from Serinus serinus (Linnaeus, 1766) (Fringillidae). Fourty years later, (Klockenhoff 1984aKLOCKENHOFF, H.F. 1984a. Redescription of Myrsidea serini (Mallophaga: Menoponidae), a parasite from passerine birds. New Zealand Journal of Zoology, 11: 17-22.) designated the male as lectotype for this species together with a careful redescription and a comparative study of different populations of this species parasitic on representatives of two bird families in the Old World: S. canaria (Linnaeus, 1758), Carduelis carduelis britannica (Hartert, 1903), Carduelis carduelis parva Tschudi, 1901, Carduelis chloris chloris (Linnaeus, 1758) (Fringillidae) and Emberiza citrinella caliginosa Clancey, 1940 (Emberizidae). In a subsequent paper (Klockenhoff, 1984bKLOCKENHOFF, H.F. 1984b. Mallophagen der Gattung Myrsidea Waterston, 1915 von afrikanischen Webervogeln (Ploceidae) - II. Bonner Zoologische Beiträge, 35(1-3): 269-284.) this author erected the "M. serini-Artengruppe", a species-complex involving three species: M. serini, M. queleae Tendeiro, 1964 and M. textoris Klockenhoff, 1984. The latter two species were not mentioned by (Price & Dalgleish 2007 PRICE, R.D. & DALGLEISH, R.C. 2007. Myrsidea Waterston (Phthiraptera: Menoponidae) from the Emberizidae (Passeriformes), with descriptions of 13 new species. Zootaxa, 1467: 1-18.) for their "serini-species group".

As there are no published records of M. serini from Southern South American hosts, the purpose of this contribution is mainly four. First, to study morphologically and re-illustrate both sexes of M. serini. Second, to carry out a chaetotaxical and morphometric comparative study of three available populations of this species collected on three host species: Carduelis barbata (Molina, 1782) (Fringillidae) from Chile, Agelaioides badius badius (Vieillot, 1819) and Chrysomus thilius petersii (Laubmann, 1934) (Icteridae) from Argentina. Third, describe the external chorionic architecture of the egg and sites of oviposition of M. serini and M. psittaci Carriker, 1955 (sensu lato, as stated by Clay, 1968CLAY, T. 1968. Contributions towards a revision of Myrsidea Waterston. III. (Menoponidae: Mallophaga). Bulletin of the British Museum (Natural History), Entomology, 21(4): 203-243.), both often synoxenic on individuals of the latter host species. Fourth, to give some remarks concerning the still problematic species Myrsidea argentina (Kellogg, 1906KELLOGG, V.L. 1906. Mallophaga from Argentina. Journal of the New York Entomological Society, 14(1): 45-49.) originally recorded off Carduelis magellanica (Vieillot, 1805).

MATERIALS AND METHODS

Some of the adult specimens are received in vials (from M.A. Marín, Chile), and many others were collected by one of us (ACC) from freshly killed birds following procedure described below.

Each bird specimen netted and collected in the field has been immediately enveloped with absorbent paper and put in an individual plastic bag containing ca. 5 cm3 of ethyl acetate to kill the lice specimens in situ, then labeled and frozen as soon as possible.

In the laboratory, each individual bird was carefully examined feather-by-feather under a dissecting microscope by the senior author. The place where each louse was found was indicated in pre-printed cards, paying special attention to delimitate the oviposition sites. The visual examination, made by a trained person, was employed for gathering these biological data due its level of confidence (Koop & Clayton, 2013KOOP, J.A.H. & CLAYTON, D.H. 2013. Evaluation of two methods for quantifying passeriform lice. Journal of Field Ornithology, 84: 210-215.).

All feather carrying lice eggs were removed and stored in coded vials, preserving some of them in 3% Glutaraldehyde in a PO4HNa2 5% solution for SEM studies. Lice specimens were mounted in slides following regular procedures and using Canada Balsam as mounting medium (Cicchino & Castro, 1978CICCHINO, A.C. & CASTRO, D.C. 1978. Contribución al conocimiento de los Malófagos Argentinos III. Sobre algunos Menoponidae de la avifauna bonaerense: Menacanthus eurysternus (Burmeister) y M. pici (Denny) (Insecta Mallophaga). Revista de la Sociedad Entomológica Argentina, 37(1-4): 77-83.).

Eggs were prepared for SEM studies following Abrahamovich & Cicchino (1985)ABRAHAMOVICH, A.H. & CICCHINO, A.C. 1985. Estudios bioecológicos, sistemáticos y filogenéticos de los malófagos parásitos de Guira guira Gmelin (Aves, Cuculidae): Vernoniella bergi (Kellogg, 1906) (Philopteridae) y Osborniella guiraensis (Kellog, 1906) (Menoponidae). I. Identificación de los huevos. Historia Natural, 5(25): 209-216.. For light microscope eggs were cleared in a pheno-ethanol 3:1 vol/vol mixture during 6-12 hours, mounted in concave slides using this medium, covered with a thin cover slip to observation and drawn at various magnifications. Identities of eggs were checked by dissections of gravid females of both species found.

Measurements of adult lice are in millimeter and taken from mounted specimens. Body parameters used are those employed by Klockenhoff et al. (1979: 207), and identified by the following abbreviations: HL = head length, OW = maximum width of the head (at occipital level), PL = prothorax length, PW = prothorax width, PTL = pterothorax length, PTW = pterothorax width, AL = length of the abdomen, AW = width of the abdomen, and TL = total length of the body.

Repository of specimens: voucher specimens are in personal collection of the senior author (ACC) and in the collection of the Museu de Zoologia da Universidade de São Paulo (MZUSP). The bird names, common and scientific, and family classification follow those in Dickinson (2003)DICKINSON, E.C. (Ed.) 2003. The Howard & Moore complete checklist of the birds of the world. 3.ed. London, Christopher Helm. 1040p..

RESULTS

Order Phthiraptera Haeckel, 1896 Suborder Amblycera Kellogg, 1896 Family Menoponidae Mjöberg, 1910 Genus Myrsidea Waterston, 1916 Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.) (Figs. 1-33)

Figures 1-5
Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.) male: thorax and abdomen, dorsal view (1); metasternum and abdomen, ventral view (2); external genitalia, dorso-ventral views (3); genital sclerites from three individuals (4); spermatophore (5)

Figures 6-9
Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.) female: thorax and abdomen, dorsal view (6); metasternum and abdomen, ventral view (7); bursa copulatrix (8); vulvar margin in detail, setae omitted (9)

FIGURES 10-17
Eggs: Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.) in lateral view (10), operculum in detail (11), operculum in polar view (14) and surface of the proximal third of amphora in detail (16); Myrsidea psittaci Carriker, 1955 in lateral view (12); operculum in detail (13), operculum in polar view (15), surface of the proximal third of amphora in detail (17). ac = air chambers, ap = apical phanerum. Bars = 100 μm

Figures 18-21
Hatching organ of Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.): general view of the distal set and medial row with lancets (18); distal set in detail (ds, 19); and medial row in detail (mr, 20-21). * points the areas of vitelline membrane. Bars = 100 μm (18) and 25 μm (19-21)

Figures 22-24
Hatching organ of Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.): from two different embryos (22-23); apical set of Fig. 22, in other position (24). For further explanations, see text

Figures 25-31
Oviposition sities of Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.) in seven different individuals of Chrysomus thilius petersii at Laguna Bellaca, San Vicente District, Buenos Aires Province, when alone, or synoxenic with M. psittaci, Philopterus cf agelaii and Machaerilaemus laticorpus. For further explanations, see text

Figures 32
Host geographic distribution and collections sites (white circles): Chrysomus thilius petersii; Agelaioides badius badius; Carduelis barbata; Carduelis chloris

Figures 33-34
Third nymphal instar of Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.) (ex Agelaioides badius badius) (33) and of "female" of Myrsidea argentina (Kellogg, 1906KELLOGG, V.L. 1906. Mallophaga from Argentina. Journal of the New York Entomological Society, 14(1): 45-49.) (ex Carduelis magellanicus) (after Kellogg, 1906KELLOGG, V.L. 1906. Mallophaga from Argentina. Journal of the New York Entomological Society, 14(1): 45-49.: 34)

Menopon seriniSéguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.: 80, fig. 84.

Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.): (Hopkins & Clay 1952HOPKINS, G.H.E. & CLAY, T. 1952. A check list of the genera & species of Mallophaga. London, British Museum of Natural History. 362p.: 233); (Negru 1963NEGRU, S. 1963. Mallophaga new to the fauna of Rumania (Mallophaga Nitzsch). Comunicarile Academii Republicii Populare Romine, 13(11): 989-993. [in Romanian]: 11); (Negru 1965NEGRU, S. 1965. Contribution à la connaissance des Mallophages (Mallophaga Nitzsch) du Serinus canaria serinus (L.). Travaux du Museum d' Histoire Naturelle Grigore Antipa, 5: 495-501.: 499, fig. 1e); (Klockenhoff 1984aKLOCKENHOFF, H.F. 1984a. Redescription of Myrsidea serini (Mallophaga: Menoponidae), a parasite from passerine birds. New Zealand Journal of Zoology, 11: 17-22.: 18-22, figs. 1-4, Tables 1-2); (Price et al. 2003PRICE, R.D., HELLENTHAL, R.A. & PALMA, R.L. 2003. World checklist of chewing lice with host associations and keys to families and genera. In: Price, R.D.; Hellenthal, R.A.; Palma, R.L.; Johnson, K.P. & Clayton, D.H. The chewing lice: world checklist and biological overview. Illinois. p. 1-448. (Illinois Natural History Survey Special Publication 24).: 131-132); (Price & Dalgleish 2007PRICE, R.D. & DALGLEISH, R.C. 2007. Myrsidea Waterston (Phthiraptera: Menoponidae) from the Emberizidae (Passeriformes), with descriptions of 13 new species. Zootaxa, 1467: 1-18.: 12, fig. 39).

Table 1
Body chaetotaxy of Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.) taken from three host populations. Ter = tergites, Ste = sternites, Ple = pleurites

Table 2
External differences of the eggs of Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.) and Myrsidea psittaci Carriker, 1955, both ex Chrysomus thilius petersii (Laubmann, 1934) from Laguna Bellaca, San Vicente, Buenos Aires Province, Argentina. Measurements are given for ten eggs chosen at random.

Liquidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.): (Złotorzycka 1964ZŁOTORZYCKA, J. 1964. Mallophaga parasitizing Passeriformes and Pici I. Subfamilies Dennyinae, Machaerilaeminae, Colpocephalinae. Acta Parasitologica Polonica, 12(17): 165-192.: 169, 176).

Material examined: 1 male and 2 females (ACC), ex Chrysomus thilius petersii, Bartolomé Bavio, Magdalena Partido, Buenos Aires Province, Argentina, 30.XII.1984, A.C. Cicchino coll. 1 female (MZUSP #5810), ex C. t. petersii, Laguna Bellaca, San Vicente Partido, Buenos Aires Province, Argentina, 5.I.1990, A.C. Cicchino coll. 2 males, 2 females and 3NIII (ACC), 2 males and 1 female (MZUSP #5811-5813), ex Agelaioides badius badius, Bartolomé Bavio, Magdalena Partido, Buenos Aires Province, Argentina, 9.VII.1985, A.C. Cicchino coll. 1 male, 4 females and 1NII (ACC), 1 male and 4 females (MZUSP #5814-5817), ex Carduelis barbata, Coquimbo, Chile, 5.VIII.1981, M.A. Marín coll.

In both sexes members of the "M. serini-Artengruppe" (Klockenhoff, 1984bKLOCKENHOFF, H.F. 1984b. Mallophagen der Gattung Myrsidea Waterston, 1915 von afrikanischen Webervogeln (Ploceidae) - II. Bonner Zoologische Beiträge, 35(1-3): 269-284.), or serini species-group (Price & Dalgleish, 2007PRICE, R.D. & DALGLEISH, R.C. 2007. Myrsidea Waterston (Phthiraptera: Menoponidae) from the Emberizidae (Passeriformes), with descriptions of 13 new species. Zootaxa, 1467: 1-18.).

General dorsal (fig. 1 and 6) and ventral (fig. 2 and 7) habitus of the male and female, respectively. Both sexes, with reduced hypopharynx and metanotum non-enlarged. In females the abdominal tergites I-III almost unmodified and slightly convex, tergites II-VIII with a noticeably gap separating the marginal posterior setae in a right and a left portion (in the male it is most apparent from tergite III), bursa copulatrix as in Fig. 8, strongly spiculate posterior margin on the subgenital plate (Fig. 9); in males the external genitalia (Fig. 3) and the genital sclerites (Fig. 4) distinctives.

Chaetotaxy of the head - length of dorsal head setae 10 and 11 are diagnostic for separating M. serini from the other species inc1uded in serini species-group (Klockenhoff, 1984bKLOCKENHOFF, H.F. 1984b. Mallophagen der Gattung Myrsidea Waterston, 1915 von afrikanischen Webervogeln (Ploceidae) - II. Bonner Zoologische Beiträge, 35(1-3): 269-284.: 271). Their va1ues match (or fall near) those given by (Klockenhoff 1984aKLOCKENHOFF, H.F. 1984a. Redescription of Myrsidea serini (Mallophaga: Menoponidae), a parasite from passerine birds. New Zealand Journal of Zoology, 11: 17-22.: 18), and are given: dhs10/11 - C. barbata 0.08-0.09/0.08, ratio 1.0 (male, n = 2) and 0.08/0.07-0.09, ratio 1.0-1.1 (female, n = 8); A. b. badius 0.08-0.09/0.08, ratio 1.0-1.1 (n = 4) and 0.08-0.10/0.08-0.10, ratio 1.1 (n = 3); C. t. petersii 0.08/0.09, ratio 0.9 (n = 1) and 0.08-0.10/0.09-0.10, ratio 0.9-1.0 (n = 3); Klockenhoff (1984a)KLOCKENHOFF, H.F. 1984a. Redescription of Myrsidea serini (Mallophaga: Menoponidae), a parasite from passerine birds. New Zealand Journal of Zoology, 11: 17-22. 0.05-0.09/0.06-0.09, ratio 0.9-1.0 (n = 25) and 0.05-0.09/0.07-0.10, ratio 0.7-0.9 (n = 35).

Chaetotaxy of the thorax and abdomen (Table 1) - counting of setae match those given by Klockenhoff et al. (1979)KLOCKENHOFF, H.F.; SCHIRMERS, G. & ZYSK, M. 1979. Populationsstudien an Tierläusen (Phthiraptera) I. Myrsidea obovata (Piaget, 1880) (Menoponidae: Mallophaga). Bonner Zoologische Beiträge, 30(1-2): 204-216., (Klockenhoff 1980KLOCKENHOFF, H.F. 1980. Populationsstudien an Tierläusen (Phthiraptera) II. Myrsidea cornicis (DeGeer, 1778) (Menoponidae: Amblycera). Bonner Zoologische Beiträge, 30(3-4): 410-430., 1984aKLOCKENHOFF, H.F. 1984a. Redescription of Myrsidea serini (Mallophaga: Menoponidae), a parasite from passerine birds. New Zealand Journal of Zoology, 11: 17-22.: 18-19). Our account neither includes the post-spiraculars nor its accessories, since metanotum to tergite VIII. These data revealed a few differences in chaetotaxy among the three populations, but are expected to find in hosts at least partially isolated and/or the small samples available to both studies. Similar results were achieved by Klockenhoff et al. (1979)KLOCKENHOFF, H.F.; SCHIRMERS, G. & ZYSK, M. 1979. Populationsstudien an Tierläusen (Phthiraptera) I. Myrsidea obovata (Piaget, 1880) (Menoponidae: Mallophaga). Bonner Zoologische Beiträge, 30(1-2): 204-216. for M. obovata (Piaget, 1880) and Klockenhoff (1980)KLOCKENHOFF, H.F. 1980. Populationsstudien an Tierläusen (Phthiraptera) II. Myrsidea cornicis (DeGeer, 1778) (Menoponidae: Amblycera). Bonner Zoologische Beiträge, 30(3-4): 410-430. for M. cornicis (DeGeer, 1778).

Measurements: differences found among the three populations here examined were slight and considered non-significant for taxonomic purposes, including when compared with published data (Klockenhoff, 1984aKLOCKENHOFF, H.F. 1984a. Redescription of Myrsidea serini (Mallophaga: Menoponidae), a parasite from passerine birds. New Zealand Journal of Zoology, 11: 17-22.).

Males

C. barbata (n = 2) = HL 0.26, OW 0.35, PL 0.13-14, PW 0.26, PTL 0.18-0.20, PTW 0.36-0.37, AL 0.66-0.69, AW 0.44-0.48, TL 1.21-1.28.

A. b. badius (n = 4) = HL 0.28-0.29, OW 0.42, PL 0.16, PW 0.27-0.29, PTL 0.21-0.22, PTW 0.38-0.41, AL 0.75-0.77, AW 0.53-0.54, TL 1.39-1.41.

C. t. petersii (n = 1) = HL 0.29, OW 0.39, PL 0.16, PW 0.28, PTL 0.17, PTW 0.37, AL 0.70, AW 0.51, TL 1.30.

Klockenhoff (1984a)KLOCKENHOFF, H.F. 1984a. Redescription of Myrsidea serini (Mallophaga: Menoponidae), a parasite from passerine birds. New Zealand Journal of Zoology, 11: 17-22. (n = 25) = HL 0.27-0.30, OW 0.34-0.39, PL 0.12-0.15, PW 0.23-0.26, PTL 0.18-0.22, PTW 0.32-0.37, AL 0.60-0.71, AW 0.42-0.52, TL 1.11-1.30.

Females

C. barbata (n = 8) = HL 0.27-0.29, OW 0.38-0.40, PL 0.14-19, PW 0.27-0.28, PTL 0.21-0.23, PTW 0.39-0.43, AL 0.80-0.91, AW 0.55-0.62, TL 1.42-1.56.

A. b. badius (n = 3) = HL 0.29-0.30, OW 0.45-0.46, PL 0.17-0.20, PW 0.30, PTL 0.23, PTW 0.47-0.48, AL 0.94-1.01, AW 0.65-0.71, TL 1.63-1.71.

C. t. petersii (n = 3) = HL 0.31-0.32, OW 0.46, PL 0.18, PW 0.18-0.20, PTL 0.24-0.25, PTW 0.46-0.51, AL 0.98-1.05, AW 0.67-0.70, TL 1.70-1.80.

Klockenhoff (1984a)KLOCKENHOFF, H.F. 1984a. Redescription of Myrsidea serini (Mallophaga: Menoponidae), a parasite from passerine birds. New Zealand Journal of Zoology, 11: 17-22. (n = 35) = HL 0.27-0.31, OW 0.36-0.43, PL 0.14-0.19, PW 0.22-0.29, PTL 0.21-0.28, PTW 0.40-0.47, AL 0.80-0.82, AW 0.57-0.70, TL 1.41-1.65.

Spermatophore: moderately fusiform (Fig. 5), with a short neck or tube which co-adapts with the medial notch of paired male sclerite (Fig. 4).

Bursa copulatrix: small-less than 50 μm wide- and feeb1y sclerotized (Fig. 8). It shows two lateral swellings that ho1d the blunt apica1 ends of the paired male genital sclerite, and the medial portion is designed to hold the neck of spermatophore (Clay, 1968CLAY, T. 1968. Contributions towards a revision of Myrsidea Waterston. III. (Menoponidae: Mallophaga). Bulletin of the British Museum (Natural History), Entomology, 21(4): 203-243.).

Morphology of the egg

General morphology of egg structures are those employed by Abrahamovich & Cicchino (1985)ABRAHAMOVICH, A.H. & CICCHINO, A.C. 1985. Estudios bioecológicos, sistemáticos y filogenéticos de los malófagos parásitos de Guira guira Gmelin (Aves, Cuculidae): Vernoniella bergi (Kellogg, 1906) (Philopteridae) y Osborniella guiraensis (Kellog, 1906) (Menoponidae). I. Identificación de los huevos. Historia Natural, 5(25): 209-216.. Differences between egg features of M. serini are given in Table 2 together of those of M. psittaci, because they can occur synoxenically in the same host individual. As these two species are easily identified by the external morphology of their eggs (Table 2), the presence of unhatched eggs in studies with museum skins might be used to determine differential prevalence in different geographic areas, and also to detect degrees abundance linked to host's breeding season or plumage molts (Foster, 1969aFOSTER, M.S. 1969a. The eggs of three species of Mallophaga and their significance in ecological studies. Journal of Parasitology, 55(2): 453-456., bFOSTER, M.S. 1969b. Synchronized life cycles in the orange-crowned warbler and its mallophagan parasites. Ecology, 50(2): 315-323.).

Hatching organ

It is a special differentiation of the embryonary membrane to tear the serosa and vitelline membranes during the hatching of first nymph (Figs. 19-24), usually set in a different way in distinct taxa (Blagoveshtchensky, 1955BLAGOVESHTCHENSKY, D.I. 1955. К морфологии яйцйа Пухоедов (Mallophaga). [Notes on eggs of Mallophaga]. Trudy Zoologischenskiy Institut Akademia Nauk USSR, 21: 262-270. [in russian], 1959BLAGOVESHTCHENSKY, D.I. 1959. Пухоеды (Mallophaga). [Nasekomye puchoedy (Mallophaga)]. Fauna SSSR 1 (1), Zoologischenkiy Institut Akademia Nauk SSSR, Nova Serie, (72):1-202. [in russian]; Eichler, 1963EICHLER, W. 1963. Arthropoda. Insecta. Phthiraptera I. Mallophaga. In: Bronns, H.G. (Ed.). Klassen und Ordnungen des Tierreichs. III. Insecta. 7b Phthiraptera. Leipzig, Verlagegesellschaft Geost & Portig K.G. p. 1-291.). This organ of M. serini is essentially similar in shape and structure to that of Menacanthus bonariensis Cicchino, 2003CICCHINO, A.C. 2003. Menacanthus bonariensis new species (Phthiraptera: Menoponidae), parasitic on the White-bellied Sparrow, Zonotrichia capensis hypoleuca (Todd, 1915) (Aves: Passeriformes: Fringillidae) in Buenos Aires Province, Argentina. Zootaxa, 358: 1-11. (another Menoponidae, see Cicchino, 2003CICCHINO, A.C. 2003. Menacanthus bonariensis new species (Phthiraptera: Menoponidae), parasitic on the White-bellied Sparrow, Zonotrichia capensis hypoleuca (Todd, 1915) (Aves: Passeriformes: Fringillidae) in Buenos Aires Province, Argentina. Zootaxa, 358: 1-11.): a tongue-like shaped and tiny pigmented plate composed of three portions (Figs. 19 and 22): a distal set of prominent of lancets of different lengths (Fig. 24), 7-10 in number and clustered together (Figs. 18-19, 22-23); a medial row of 5 shorter lancets (Figs. 18, 20-21); and a basal cluster of up to 18 tubercles or tuberiform thickenings of the membrane (Figs. 22-23). The hatching organ of M. serini differs from that of Menacanthus bonariensis by less number of medial lancets in M. serini (vs 7-8 in M. bonariensis), and caudal tooth with one central spine in basal cluster in M. bonariensis (absent in M. serini).

Sites of oviposition

Eggs were found glued by means of a moderate amount of hygroscopic spumaline (Hinton, 1977HINTON, H.E. 1977. Function of shell structures of pig louse and how egg maintains a low equilibrium temperature in direct sunlight. Journal of Insect Physiology, 23: 785-800.) to the underside of the rachis (less frequently to the overside) of feathers of the front, chin, face, auricular region and upper portion of the neck (Figs. 25-27). Usually there is one egg per feather, but two or often more are found in heavy infestations. Myrsidea psittaci apparently prefers the feathers of the front, loreal area, face, peri-auriculars and adjacent areas of the upper neck. When both species are in synoxenism, apparently there is 1ittle or no competition for oviposition sites: in either light or heavy infestations each species tends to oviposite on the feathers in the regions cited above, and although some degree of over1ap do exists it was no observed eggs of both species in the same feather (Figs. 26-27).

Spatial relationships of Myrsidea serini with other louse species found on South American passerines

Since no adequate studies have been made on possible competition for sites of oviposition among different genera of lice occurring in the same individual host, some observations taken in January 1990 from a flock of 10 individuals of C. t. petersi in Laguna Bellaca (San Vicente Partido, Buenos Aires Province, Argentina) may be of interest. They suggest some degree of exclusion among M. serini, M. psittaci, Machaerilaemus laticorpus (Carriker, 1903) (Amblycera, Menoponidae) and Philopterus cf agelaii (Osborn, 1896) (Ischnocera, Philopteridae). After a general picture showing how these species share the host body, notes on the synoxenic distribution and prevalence of this widely spread Myrsidea species is presented below.

In individuals heavily infested by P. cf agelaii (8 males, 12 females, 12 nymphs) (Fig. 28), sites of oviposition of M. serini extends from the nuchal area to the chin and upper neck. In synoxenism of heavily infested individuals by M. serini (8 males, 14 females, 14 nymphs, and more than 35 operculated eggs) and lightly infestations of both P. cf agelaii and M. laticorpus (Fig. 29), M. serini lays its eggs in the auricular and upper neck area, whilst P. cf agelaii does in the upper head, and M. laticorpus in the middle neck, without overlapping. When M. serini and M. psittaci occurs synoxenically in moderate infestations (up to 6 individuals) together with P. cf agelaii (Fig. 30), eggs of the two Myrsidea species are laid on the lores, face, chin, upper neck and the external peri-auriculars, occupying P. cf agelaii the remaining peri-auriculars until the nuchal area. In individuals heavily infested with M. serini, M. psittaci and P. cf agelaii (more than 10 individuals), the sites of oviposition of the two Myrsidea species extend to the middle neck, not overlapping those of the Philopterus species (Fig. 31).

Synoxenic distribution

It has been possible to study this phenomenon in flocks of C. t. petersi of two localities of NE Buenos Aires Province: Laguna Bellaca (data given above) (n = 10) and General Mansilla, Magdalena District (n = 12) (Fig. 32). In both flocks synoxenia of M. serini-M. psittaci was of frequent occurence, reaching ca. 50% of the individuals parasitized (n = 8). It must be noted that in one or both species of a synoxenic pair may have polyxenic distribution (sensu Nelson, 1972NELSON, B.C. 1972. A revision of the New World species of Ricinus (Mallophaga) occurring on Passeriformes (Aves). University of California Publications in Entomology, 68: 1-130.: 5), that is, parasitizes different species of hosts. According with this, M. serini should be the most polyxenic species of the pair M. serini-M. psittaci, parasitizing not closely related hosts belonging to three different passerine families, as shown in Table 3. Myrsidea psittaci is also a polyxenic species but with a more restricted range, parasitizing several genera of Icteridae (Chrysomus Swainson, 1837, Agelaioides Cassin, 1866, Gnorimopsar Richmond, 1908, Amblyramphus Leach, 1814, Pseudoleistes Sclataer, 1862 and Scaphidura Gmelin, 1788) in South America, and, in turn, it may also be synoxenic with Myrsidea species other than M. serini (Valim & Cicchino, in prep.).

Table 3
Host and locality records for Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.)

Although the distribution of each synoxenic species usually does not follow any definite geographical pattern within the ranges of their respective hosts (Fig. 32), M. serini seems a primary parasite (sensu Rheinwald, 1968RHEINWALD, G. 1968. Die Mallophagengattung Ricinus DeGeer, 1778. Revision der ausseramerikanischen Arten. Mitteilungen aus dem Hamburg Zooloichen Museum Institute, 65: 181-326.) of an Old World Cardueline finchs (Fringillidae), spreading secondarily on other passerines, as Emberizidae and Icteridae in New Zealand and New World, respectively. Whereas M. psittaci seems a primary parasite of certain Icteridae such as Agelaioides, Pseudoleistes and Scaphidura, and secondarily has invaded other genera of this same family as Amblyramphus, Gnorimopsar and Agelaius.

Klockenhoff (1984a)KLOCKENHOFF, H.F. 1984a. Redescription of Myrsidea serini (Mallophaga: Menoponidae), a parasite from passerine birds. New Zealand Journal of Zoology, 11: 17-22. found M. serini in three passerine species (Table 3) introduced in New Zealand from Europe, being Carduelis chloris one of them. As this finch has been introduced successfully in Uruguay and adjacent part of Argentina (Montaldo, 1979MONTALDO, N.H. 1979. Presencia de Chloris chloris en la Argentina. Hornero, 12: 57-58.; Olrog, 1979OLROG, C.C. 1979. Nueva lista de la avifauna argentina. Tucumán. Opera Lilloana, 27:1-324., 1984OLROG, C.C. 1984. Las aves argentinas: Una nueva guía de campo. Buenos Aires, Administración de Parques Nacionales. 352p.), M. serini is also expected to be found on this host, but not reported to date. (Price & Dalgleish 2007)PRICE, R.D. & DALGLEISH, R.C. 2007. Myrsidea Waterston (Phthiraptera: Menoponidae) from the Emberizidae (Passeriformes), with descriptions of 13 new species. Zootaxa, 1467: 1-18. stated that it is an atypical species, considering the host distribution patterns presented in Myrsidea genus, due its occurence on, at least, two different host families (Price et al., 2003). Such unusual host and geographical distribution of M. serini could be explained by the straggling and subsequent establishment of this species on other hosts from canaries in Argentina, Chile and in New Zealand as well.

Prevalence

Locally at Laguna Bellaca, in a population of C. thilius petersi, 3 of 5 individuals (60%) were parasitized with M. serini, being in two also synoxenic with M. psittaci. As these two species are easily identified by the external morphology of their eggs (see above), the presence of unhatched eggs in museum study skins can be used to determine differential prevalences in different geographic areas, and also to detect degrees abundance linked to host's breeding season or plumage molts (Foster, 1969aFOSTER, M.S. 1969a. The eggs of three species of Mallophaga and their significance in ecological studies. Journal of Parasitology, 55(2): 453-456., bFOSTER, M.S. 1969b. Synchronized life cycles in the orange-crowned warbler and its mallophagan parasites. Ecology, 50(2): 315-323.). At a larger scale encompassing the northeastern quadrant of Buenos Aires Province, in this same host (n = 15), 4 were parasitized with P. cf agelaii only, 1 with Myrsidea psittaci, 6 with the former species together with Myrsides psittaci (in 2 this species synoxenic with M. serini), and 1 with the three cited species plus Machaerilaemus laticorpus, in addition to 3 other individuals with no lice. At the same scale level, and regarding Agelaioides badius badius (n = 36), 9 individuals were parasitized by Philopterus sp. nov. only, 1 with Myrsidea serini only, 4 with the latter two species together, 8 with Philopterus sp. nov. and Brueelia badia Cicchino & Castro, 1996, 6 with these latter species plus Machaerilaemus laticorpus, 1 with all the four lice species together, in addition to 5 other individuals which bear no lice.

Myrsidea serini vs. Myrsidea argentina (Kellogg, 1906KELLOGG, V.L. 1906. Mallophaga from Argentina. Journal of the New York Entomological Society, 14(1): 45-49.)

Myrsidea argentina was described from a single specimen, supposedly a female, taken from Chrysomitris icterica (= Carduelis magellanica) from Argentina, collected by Dr. Carlos Berg in 1902 (Kellogg, 1906KELLOGG, V.L. 1906. Mallophaga from Argentina. Journal of the New York Entomological Society, 14(1): 45-49.). (Clay 1968CLAY, T. 1968. Contributions towards a revision of Myrsidea Waterston. III. (Menoponidae: Mallophaga). Bulletin of the British Museum (Natural History), Entomology, 21(4): 203-243.: 238) believed that Kellogg's specimen was a nymph, not a female. After a careful examination of Kellogg's figure and certain details in his description, we agree with Clay's contention, and most probably it is a third nymphal instar. In absence of specimens from C. magellanica, that M. argentina be or be not the same as M. serini is open to question, because some morphological features are difficult to reconcile even with those of the third nymphal instar of M. serini, as shown in Table 4. Nevertheless, these differences deserve the following comments:

  • - Dimensions: slight differences in OW and TL probably must be correlated with dimensions of their hosts. In fact, specimens from Icteridae tend to be noticeably larger than those from Fringillidae, so the three nymph III examined from Agelaioides b. badius are expected to exhibit larger dimensions than those from C. magellanica.

  • - Marginal setae of the metanotum: Kellogg pointed out that "the straight posterior margin with four marginal hairs". The specimens ex A. b. badius have unmistakably 6 marginal central setae. Perhaps some of the setae in Kellogg's specimen be missing because no such a gap as illustrated by him (Fig. 34 and Kellogg, 1906KELLOGG, V.L. 1906. Mallophaga from Argentina. Journal of the New York Entomological Society, 14(1): 45-49.: fig. 7) separate the marginal setae from the long angular and short adjacent setae each side of the metanotum.

  • - Number of tergocentral setae in abdomen: some significant differences do exist in segments V-VIII. It is probable that the number of setae illustrated by Kellogg is result of partial superposition of dorsal and ventral views. This contention is based in the lacking of the noticeable gap that divides the tergo-central in a right and left portion (cf Figs. 33-34).

  • - Number of setae of the dorsal anal fringe: Kellogg's figure illustrates ca. 15 setae, in agreement with our specimens from Agelaioides. This feature, in absence of other definitive details, led us to agree with (Clay 1968CLAY, T. 1968. Contributions towards a revision of Myrsidea Waterston. III. (Menoponidae: Mallophaga). Bulletin of the British Museum (Natural History), Entomology, 21(4): 203-243.) in that this specimens is not a female but a nymph, and most probably a third instar nymph, taking in mind that the adult female of M. serini has more than 30 hairs in the dorsal anal fringe.

Table 4
Measurements and chaetotaxy of third nymphal instar of Myrsidea serini (Séguy, 1944SÉGUY, E. 1944. Insectes ectoparasites (Mallophages, Anoploures, Siphonaptères). Faune de France, 43: 23-407.) (ex Agelaioides badius badius) and of "female" of Myrsidea argentina (Kellogg, 1906KELLOGG, V.L. 1906. Mallophaga from Argentina. Journal of the New York Entomological Society, 14(1): 45-49.) (ex Carduelis magellanicus) (after Kellogg, 1906KELLOGG, V.L. 1906. Mallophaga from Argentina. Journal of the New York Entomological Society, 14(1): 45-49.)

ACKNOWLEDGMENTS

This work was supported in part by the FAPESP - São Paulo Research Foundation 2011/11420-5 and 2012/06951-4 to MPV.

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Publication Dates

  • Publication in this collection
    2015

History

  • Accepted
    27 Feb 2015
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