Collembola: Entomobryidae

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Jan 14, 2007 - HOLOTYPE: 1 male, MÈxico: Oaxaca state: Oaxaca city, 06-V-94, elevation 1,550 m asl, from Pinus oaxacana (Mirov), collection number ...


The Genus Willowsia and Its Mexican Species (Collembola: Entomobryidae) FENG ZHANG,1 J. G. PALACIOS-VARGAS,2



Ann. Entomol. Soc. Am. 100(1): 36Ð40 (2007)

ABSTRACT The present article deals with the genus Willowsia and its Mexican species. A new species, Willowsia mexicana, sp. nov., is described and illustrated from Mexico, bringing the Mexican fauna to three species. KEY WORDS Collembola, Entomobryidae, Willowsia, new species, Mexico

Shoebotham (1917) erected the genus Willowsia (Collembola: Entomobryidae) for species with 8 ⫹ 8 eyes, four-segmented antennae, scales on body but not on the ventral face of dens, dental spines, bidentate mucro, short mucronal basal spine with tip reaching anteapical tooth, and sexual dimorphism. The genus now includes many species originally described in Degeeria Nicolet 1841, Ptenura Templeton 1843, Seira Lubbock 1869, and Sira Tullberg 1872. Yoshii (1992) placed Willowsia in the subfamily Seirinae, which includes scaled genera such as Seira, Lepidosira, Lepidocyrtoides, Lepidocyrtus, and Pseudosinella. Traditionally, species identiÞcation in Willowsia has relied on body color pattern. However, differences in color pattern are not always reliable species markers. For example, Mari Mutt (1981) showed that color pattern variation in Puerto Rican populations of W. jacobsoni is related to sexual dimorphism and does not have value in circumscribing subspeciÞc taxa as proposed by previous authors (Yoshii 1942). In addition, both scales and cuticle contribute to body color pattern (R. Jordana, personal communication), so that loss of scales may cause inconsistent descriptions of color pattern by different authors. Therefore, more characters are required to reliably diagnose Willowsia species. In the current study, the following characters were found to be taxonomically useful. 1. Types of body scales. Scales are divided into at least three types: 1) striate, such as those in W. bimaculata (Bo¨ rner) 1909, W. brahma (Imms) 1912, W. ieti Yosii 1971, W. jacobsoni (Bo¨ rner) 1913,

1 Department of Biology, Nanjing University, Nanjing 210093, PeopleÕs Republic of China. 2 Corresponding author, Departamento de Ecologõ´a y Recursos Naturales, Laboratory Ecologõ´a y Sistema´tica de Microartro´ podos, Fac. Ciencias, UNAM. 04510 Me´ xico, D.F. (e-mail: [email protected]

2. 3. 4. 5. 6.

W. japonica (Folsom) 1897, W. mekila Christiansen and Bellinger 1992, W. mesothoraxa Nguyen 2001, W. nigromaculata (Lubbock) 1873, and W. platani (Nicolet) 1842 (Fig. 20b); 2) spinulate as in W. bartkei Stach 1965, W. pseudosocia Stach 1965 and W. guangxiensis Shi and Chen 2004 (Fig. 20, f and g); and 3) ribbed, such as in W. formosana Denis and W. mexicana sp. nov. (Fig. 17). Number and arrangement of setae on trochanteral organ. Number, size and position of the inner teeth of the unguis. Length ratio of the smooth (uncrenulated) part of the dens to mucro. Number of smooth and ciliate setae on the ventral tube. Labial chaetotaxy.

So far, 22 species of the genus Willowsia have been reported worldwide. Based on the Catalog for the Mexican Collembola (Palacios-Vargas 1997), only two species among them were from Mexico: W. buskii (Lubbock) 1869 (reported from Veracruz State by Palacios-Vargas and Go´ mez [1991]: 109 and PalaciosVargas and Go´ mez-Anaya [1994]: 27) and W. nigromaculata (Lubbock) 1873 (from Tabasco, Michoaca´n and Puebla States [Palacios-Vargas 1997]). A new Mexican species is described here.

Key to Mexican Species of Genus Willowsia 1. Posterior macrochaetae of second thoracic segment 9 ⫹ 9 . . . . . . . . . . . . . . . . W. buskii Posterior macrochaetae of second thoracic segment ⬍9 ⫹ 9 . . . . . . . . . . . . . . . . . . . . 2 2. Posterior macrochaetae of second thoracic segment 7 ⫹ 7 . . . . . . . . . . . W. nigromaculata Posterior macrochaetae of second thoracic segment 3 ⫹ 3 . . . . . . . . W. mexicana, sp. nov.

0013-8746/07/0036Ð0040$04.00/0 䉷 2007 Entomological Society of America

January 2007



Materials and Methods Specimens were mounted under a coverslip in HoyerÕs solution for study. They were studied under a phase contrast microscope. The type species are deposited in Laboratorio de Ecologõ´a y Sistema´tica de Microartro´ podos, Facultad de Ciencias, UNAM. Me´ xico, except for three paratypes that were kept at the Department of Biology, Nanjing University, China. Results and Discussion Willowsia mexicana, sp. nov. (Figs. 1Ð17) Synonym. As W. nigromaculata Palacios-Vargas 1997. Body Length. Maximum body length up to 2.5 mm. Color Pattern. Ground color yellow. Eye patches dark blue. An arch-shaped dark band connects eye patches. Blue pigment on antennae gradually turning darker toward tip of each segment. Th. IIÐAbd. I with a dark dorsolateral band; Abd. IIÐIII with 1 ⫹ 1 dark blue patches, most of Abd. IVÐVI covered by a dark blue middorsal stripe, femora and median part of tibiotarsi blue (Fig. 1). Head. Eyes 8 ⫹ 8. Antenna 1.8 Ð2.3 times as long as head. Ratio of antennal segments I:II:III:IV as 1:(1.3Ð 1.8):(1Ð2.3):(1.3Ð2.6). Scales present on Ant. I. Ant. IV with apical bulb (Fig. 3). Setae 2 and 3 of Ant. III organ (Chen and Christiansen 1993) small curved rods (Fig. 2). All antennal segments with many smooth setae. Labral papillae large, with two to four apical denticles. Labral and prelabral setae 4-5-5-4 all smooth; a2 slightly shorter than a0 and a1, b2 slightly shorter than b0 and b1 (Fig. 4). Outer differentiated seta of labial appendage E (Fjellberg 1999) straight, as thick as normal setae, tip not reaching apex of papilla (Fig. 5). Labial triangular setae M1, E, L1, and L2 all ciliate (Fig. 6). Dorsal cephalic chaetotaxy (Szeptycki 1973) as Þve antennal (A), three ocellar (0), four sutural (S); interocular setae as pqrst (Mari Mutt 1986) (Fig. 7a, b). Thorax. Dorsal macrochaetotaxy as in Fig. 8: Th. IIÐ3 ⫹ 3; Th. IIIÐ3 ⫹ 3 on medial and 3 ⫹ 3 on posterior margin. Femora scaled. Trochanteral organ with 18 Ð24 smooth setae (Fig. 9). Metatibiotarsi without differentiated setae; smooth metatibiotarsal seta present (Fig. 10). Unguis with four small inner teeth; paired teeth with tip reaching 0.4 Ð 0.5 distance from base to apex of ventral edge; median tooth at ⬇0.7Ð 0.8 distance from base; distal tooth on ⬇0.8 Ð 0.9 distance from base. Unguiculus acuminate with outer edge clearly serrate. Tenent hair slender and strongly clavate, apparently longer than unguiculus (Fig. 11). Abdomen. Abd. IV ⬇3Ð 4 times longer than Abd. III. Dorsal macrochaetae and mesochaetae as in Fig. 8: Abd. IÐ1 ⫹ 1. Abd. IIÐtwo inner and one lateral to M3 arch (being m3, m3e and m5); Abd. IIIÐtwo dorsocentral and three lateral on each side; Abd. IVÐ 4 ⫹ 4

Figs. 1–17. W. mexicana, sp. nov. (1) Body color pattern. (2) Ant. III organ. (3) Apical bulb of Ant. IV. (4) Labrum. (5) Outer labial papilla and its differentiated seta. (6) Labial triangule setae. (7a) Cephalic dorsal chaetotaxy. (7b) Interocular setae. (8) Semidiagrammatic body dorsal chaetotaxy. (9) Trochanteral organ. (10) Tibiotarsal inner differentiated setae. (11) Hind foot complex. (12) Tenaculum. (13) Anterior face of ventral tube. (14) Manubrial plate. (15) Base of dens (bs1 and bs2, basal setae; pi, proximalinternal seta). (16) Mucro. (17) Body scales.



Fig. 18. Body color pattern. (a) W. buskii (Christiansen and Bellinger 1998). (b) W. nigromaculata (Stach 1965). (c) W. jacobsoni (Mari Mutt 1981).

dorso-central and 12 lateral on each side. Tenaculum with one large striate seta (Fig. 12). Ventral tube anteriorly with 4 ⫹ 4 large, 2 ⫹ 2 moderate, and many small ciliate setae (Fig. 13a); posteriorly with 21Ð23 small smooth setae, each lateral ßap with nine smooth setae. Ratio Manubrium: (Dens ⫹ Mucro) ⫽ 1.0:1.2Ð 1.8. Manubrium covered with scales ventrally. Manubrial plaque with three setae and two pseudopores (Fig. 14). Dens without spines, basal setae (bs1 and bs2) and proximal-internal seta (pi) (Li and Chen 1997) ciliate; bs1 and bs2 subequal and apparently shorter than pi (Fig. 15). Uncrenulate part of dens ⬇2.0 Ð2.6 times length of mucro. Mucronal teeth subequal, tip of subapical teeth slightly surpassing

Vol. 100, no. 1

Fig. 20. Body scale morphology. (a) W. buskii (Gisin 1960). (b) W. nigromaculata (Christiansen and Bellinger 1998). (c) W. pseudosocia (Stach 1965). (d) W. formosana (Denis 1929). (e) W. jacobsoni (Mari Mutt 1981). (f and g) W. guangxiensis (Shi and Chen 2004).

half mucro). Basal spine just reaching apex of anteapical tooth (Fig. 16). Male genital plate not seen clearly. Body Scales. Mostly yellow and leaf-like with several distinct longitudinal ribs. Rib number varies greatly in the same individual in different parts of the trunk (Fig. 17); scales along the hind margin of thoracic segments enlarged. Ecology. Under the bark of trees, from litter of mangrove in the forest, elevation from 750 m above sea level (asl) to 2,900 m asl.

Fig. 19. Body dorsal chaetotaxy. (a) Th. IIÐAbd. IV of W. buskii (Christiansen and Bellinger 1998). (b) Th. IIÐAbd. IV of W. nigromaculata (Christiansen and Bellinger 1998). (c) (c1.) Th. II, (c2.) Th. III, (c3.) Abd. I, (c4.) Abd. II, (c5.) Abd. III, and (c6.) Abd. IV of W. jacobsoni (Mari Mutt 1981).

January 2007 Table 1.



Comparison of W. mexicana, sp. nov., with other Mexican species

W. mexicana, sp. nov.

Body scales Scales on Ant. I Scales on legs Antenna bulb Labral papilla Labral setae pelabral Setae of labial base Trochanteral organ setae Ungual inner teeth Basal pair of ungual teeth distance from base Large ciliate setae on anterial face of ventral tube Th. II posterior central Macrochaetae Th. III macrochaetae Anterior row Media row Posterior row Abd. I central macrochaetae Abd. II macrochaetae M3 arch Inner to M3 arch Lateral to M3 arch Abd.III macrochaetae Central Lateral Abd. IV macrochaetae Central Anterior row Media row Þrst row Second row Posterior row Lateral

Several ribs Present Present Single Each with 2Ð4 apical denticles

W. nigromaculata sensu Christiansen (1998) Striate Bilobed

4:5:5/4 smooth M1EL1L2 18Ð24 4 0.4Ð0.5

W. buski sensu Christiansen (1998) and Mills (1934) Striate Absent Absent Bilobed Unisetose 4:5:5/4 prelabral barbed M1EL1L2

3 0.7

4 ⫹ 4 large 2 ⫹ 2 median 3⫹3




3⫹3 1⫹1

10 4

W. jacobsoni sensu Mari Mutt (1981) Striate Absent Absent Single Each with 3Ð5 denticles 4:5:5/4 ciliate (M1, M1s) M2RE L1Ð2 16 4 0.6

5 ⫹ 5 large


4 ⫹ 4 median 9⫹9


3⫹3 3⫹3

2⫹2 1⫹1 3⫹3 3⫹3

3⫹3 4 (5) ⫹ 4 (5)

2 0 1

2 1 1

2 2 1

2 0 1

2⫹2 3⫹3

3⫹3 3⫹3

3⫹3 3⫹3

2⫹2 5⫹5



2⫹2 2⫹2 2⫹2

1⫹1 1⫹1 2⫹2

1⫹1 1⫹1 2⫹2 12 (13) ⫹ 12 (13)

Types. HOLOTYPE: 1 male, Me´xico: Oaxaca state: Oaxaca city, 06-V-94, elevation 1,550 m asl, from Pinus oaxacana (Mirov), collection number 06/05/1994(3), E. Lo´ pez. ALLOTYPE. One female, Me´ xico: Veracruz state: El Xico, 21-VII-1979, elevation 1,228 m asl, from bark of trees, collection number 21-VII-79(3), J. Palacios coll. PARATYPES. One female, Me´ xico: Distrito Federal: Contreras, 2-III-76, elevation 2,900 m asl, forest of Pinus, ex litter, J. Castro coll.; two females, Puebla state: Tzicuila´n, 25-VII-76, elevation 750 m asl, Road, bark of trees, J. Palacios; two females, Michoaca´n State: El Tren: Km 38 Cd. Hidalgo-Charo, 27-V-76, forest of Pinus, ex litter, J. G. Palacios-Vargas coll.; one female, Me´ xico: Tabasco state: Cabo Santa Ana, 27-I78, litter of mangrove, collection number 261, J. Palacios coll.; two females, Me´ xico: Oaxaca State; three females, Me´ xico: Oaxaca State: Oaxaca city, 06-V-1994, elevation 1,550 m asl, E. Lo´ pez coll. Etymology. Named after Mexico, the country where types were collected.


1 (2) ⫹ 1 (2) 1⫹1 2⫹2 14 ⫹ 14

Discussion The new species is distinguished from other Willowsia spp. by color body, scale type, and dorsal chaetotaxy (Figs. 17Ð19). In most species of Willowsia, scales are spinulate (Fig. 19c and e, f and g) or striate (Fig. 19b). W. mexicana has ribbed body scales and has only been reported for W. formosana from Taiwan, China (Fig. 18d). The body chaetotaxy of the new species is similar to W. jacobsoni reported from Java and Puerto Rico (Figs. 17Ð19). The differences among W. mexicana n. sp., W. jacobsoni, and other Mexican species are shown in Table 1. Acknowledgments Shi-Xi (Department of Biology, University of Nanjing, Nanjing, Jiangsu, China) collaborated on this project; Felipe Soto Adames (Department of Biology, University of Vermont, Burlington, VT) kindly reviewed the manuscript and gave criticism and important information; and Jose´ Carlos Simo´ n (Facultad de Ciencias, Universidad Auto´ noma de Madrid, Madrid, Spain) gave comments and suggestions. The current study was supported by National



Nature Science Foundation of China 30370175 and 39970097.

References Cited Chen, J.-X., and K. Christiansen. 1993. The Genus Sinella with special reference to Sinella s. s. (Collembola: Entomobryidae) of China. Oriental Insects 27: 1Ð54. Christiansen, K. A. 1998. New species of Pseudosinella (Collembola) from Ascension Island. J. Nat. His. 32: 149Ð156. Christiansen, K. A., and P. Bellinger. 1998. The Collembola of North America north of the Rio Grande, a taxonomic analysis, I-III. Grinnell College, Grinnell, IA. Fjellberg, A. 1999. The labial palp of Collembola. Zool. Anz. 237: 309Ð330. Gisin, H. 1960. Collembolen fauna Europas. Gedruckt mit Unterstutzung des Schweizerischen Nationalfonds fur Wissenschaftliche Forschung. Museum DÕhistoire Naturelle. Li, L., and J.-X. Chen. 1997. A new species of the genus Homidia from Anhui province China (Collembola: Entomobryidae). Entomol. Sin. 4: 202Ð205. Mari Mutt, J. A. 1981. Redescription of Willowsia jacobsoni (Bo¨ rner), an entomobryid with conspicuous sexual dimorphism (Insecta: Collembola). J. Agric. Univ. PR 65: 361Ð373.

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Mari Mutt, J. A. 1986. Puerto Rican species of Lepidocyrtus and Pseudosinella (Collembola: Entomobryidae). Carib. J. Sci. 22: 1Ð 48. Mills, H. B. 1934. A monograph of the Collembola of Iowa. Collegiate Press, Ames, IA. Palacios-Vargas, J. G. 1997. Cata´logo de los Collembola de Me´ xico. Coordinacio´ n de servicios editoriales, Fac. Ciencias, UNAM. Palacios-Vargas, J. G., and J. A. Go´ mez. 1991. Los cole´ mbolos y su relacio´ n con los hongos. XXVI Congreso Nacional de Entomologõ´a. I Simposio Nacional sobre la interaccio´ n Insecto-Hongo. Mem. 99 Ð114. Palacios-Vargas, J. G., and J. A. Go´ mez-Anaya. 1994. Lista actualizada de cole´ mbolos miceto´ Þlos de Me´ xico (Hexapoda: Entognatha). Fol. Entomol. Mex. 92: 21Ð30. Shoebotham, J. W. 1917. Notes on the Collembola, part 4. The classiÞcation of the Collembola; with a list of genera known to occur in the British Isles. Ann. Mag. Nat. Hist. 8: 425Ð 436. Stach, J. 1965. On some Collembola of North Vietnam. Acta Zool. Cracov 10: 345Ð372. Szeptycki, A. 1973. North Korean Collembola. I. The genus Homidia Bo¨ rner 1906 (Entomobryidae), Acta Zoologica Cracoviensia, Tom XVIII, Nr 2, Krako´ w 31: 23Ð 40. Yosii, R. 1942. Japanische Entomobryinen (Ins., Collemb.). Arch. Naturg., N. F. 10: 476 Ð 495. Received 19 August 2005; accepted 12 September 2006.

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