morphology of ovipositors in oribatid mites of the superfamily crotonioidea (acari, oribatida)

ISSN 0013-8738, Entomological Review, 2011, Vol. 91, No. 8, pp. 1073–1079. © Pleiades Publishing, Inc., 2011. Original Russian Text © S.G. Ermilov, 2011, published in Zoologicheskii Zhurnal, 2011, Vol. 90, No. 10, pp. 1168–1174.

1073

Morphology of Ovipositors in Oribatid Mites of the Superfamily Crotonioidea (Acari, Oribatida)

S. G. Ermilov Consulting Center of the Federal Service for Veterinary and Phytosanitary Inspection, Nizhnii Novgorod, 603107 Russia

e-mail: [email protected] Received July 1, 2009

Abstract—The structure of ovipositors in 16 species of oribatid mites from the superfamily Crotonioidea (Acari, Oribatida) was studied. Similarities and differences in the ovipositor morphology are revealed. A brief comparative analysis of the structure of ovipositors in Macropylina (Crotonioidea) and Brachypylina oribatid mites was per-formed. DOI: 10.1134/S0013873811080112

The ovipositor morphology of lower oribatid mites (Acari, Oribatida, and Macropylina) is insufficiently studied. Grandjean (1956) described in detail the structure of ovipositors in three species (Nothrus silvestris Nicolet, 1885, Heminothrus targionii (Ber-lese, 1885), and Nanhermannia nana (Nicolet, 1885); descriptions of ovipositors in lower oribatid mites can be found only in some publications of other authors (Ermilov, 2009; Grandjean, 1954; Bayoumi and Ma-hunka, 1979; Badejo et al., 2002; Norton et al., 1996; Norton and Behan-Pelletier, 2007, 2009).

The goal of our study included examination of the ovipositor morphology of oribatid mites of the super-family Crotonioidea, characterized by Holarctic or wider geographical distribution. The following tasks were set: to study the structure of ovipositors and to reveal similarities and differences in their morphology in representatives of different taxa of Crotonioidea and to perform a comparative analysis of the structure of ovipositors in representatives of the lower oribatids of the group Macropylina (with Crotonioidea as an ex-ample) with the structure of ovipositors in higher oribatids of the group Brachypylina, examined earlier (Ermilov, 2010).

MATERIALS AND METHODS To study ovipositor morphology in oribatid mites,

adult mites of the following 16 species of 8 genera belonging to 4 families of the superfamily Crotoni-oidea were collected: Mainothrus badius (Berlese, 1905), Trhypochthoniellus longisetus (Berlese, 1904), Trhypochthonius cladonicola (Willmann, 1919), T. tectorum (Berlese, 1896), Malaconothrus monodac-

tylus (Michael, 1888), Trimalaconothrus major (Ber-lese, 1910), Nothrus anauniensis Canestrini et Fan-zago 1876, N. borussicus Sellnick 1928, N. silvestris Nicolet, 1855, Camisia biurus (Koch, 1839), C. segnis (Hermann, 1804), C. spinifer (Koch, 1835), C. solho-eyi Colloff, 1993, H. longisetosus Willmann, 1925, Heminothrus thori (Berlese, 1904), and Heminothrus peltifer (Koch, 1839). All the mites were collected in Nizhnii Novgorod Province.

For measurements, five specimens of each species were used. The mites were dissected and ovipositors were placed on temporary or constant slides. All the measurements are given in micrometers.

The system of oribatids is given according to the classification of Subias (2004, 2009); chaetotaxy and some designations in descriptions of ovipositor mor-phology are given according to Grandjean (1956).

RESULTS AND DISCUSSION

The General Structure of the Ovipositor Ovipositor is typical of oribatids, in the shape of a

hollow cylinder, subdivided into two parts: proximal (Pp) and distal (Dp); the latter part can telescopically protract forward. The base of the distal part (bDp) terminates as three small lobes (L1–L3) (Fig. 1, 1).

Integument of the ovipositor is semitransparent; its surface, except for smooth lobes, is covered with lon-gitudinal sinuous folds. The walls are soft and elastic, stretching during oviposition (Fig. 1, 2).

Chaetom. 12 simple (unmodified) setae are present on ovipositor lobes, 4 on each lobe (Fig. 1, 1). The

ERMILOV

ENTOMOLOGICAL REVIEW Vol. 91 No. 8 2011

1074

first lobe (L1) distinctly differs from the other two lobes: two setae ψ1 are situated on the apex of the lobe, their thecae converging; two setae ψ2 are situated lower and also converge. On the apices of lobes L2 and L3 (clockwise in relation to L1) a single seta τ1 is present; setae τ2–4 are situated lower. The length and relative arrangement of setae on ovipositor lobes con-siderably differ in different species.

The base of the distal part of the ovipositor bears several short setae; the number of these setae varies in different species (4 or 6).

The Peculiarities of the Ovipositor Structure in Mites of Different Species

The family Trhypochthoniidae. The following four species of three genera were examined (table): Mai-

nothrus badius, Trhypochthoniellus longisetus, Trhy-pochthonius cladonicola, and T. tectorum. The distal part of the ovipositor in the species examined usually 49–82 μm long and 28–53 wide. The longest oviposi-tor was found in M. badius (90–110 μm); the widest (up to 65 μm), in representatives of Trhypochthonius Berlese, 1904. The width of the ovipositor varies even in specimens of the same species. The base of the dis-tal part is longer than the length of the blade. In M. badius (Fig. 2, 1) and T. longisetus (Fig. 2, 2), se-tae ψ2 and τ2–4 are twice or thrice as long as those on the lobes and τ1. In T. tectorum (Fig. 2, 3) and T. cla-donicola, all the setae are spine-shaped; τ1 are ap-proximately twice as long as ψ2 and τ2–4. In M. badius, setae τ3 and τ4 converge; they are situated approxi-mately in the middle of the lobes; setae τ2 are attached

Fig. 1. Ovipositor of Nothrus anauniensis: (1) general view; (2) during oviposition; (Pp) proximal part; (bDp) base of distal part; (L1–L3) lobes; (ψ, τ, k) setae; (G) genital cap; (g) genital setae; (E) egg. Scale 100 μm.

MORPHOLOGY OF OVIPOSITORS IN ORIBATID MITES


1075

considerably lower. In T. longisetus, setae τ2–4 are diagonally arranged on lobes (τ2 is the lower and τ4 is the uppermost seta). In T. tectorum and T. cladonicola, bases of setae τ2–4 form a triangle: seta τ3 is situated in the apex of this triangle and setae τ2 and τ4, in basal angles; τ2 is situated lower than τ4. In all the species of the family, 6 setae k are present; these setae are similar in structure to setae ψ2 and τ2–4 on the lobes of the ovi-positor.

The family Malaconothridae. Two species were examined: Malaconothrus monodactylus and Tri- malaconothrus major (table). Their ovipositors are small. In M. monodactylus and T. major, their size is 49–57 × 28–36 μm and 28–36 × 36–49 μm, respec-tively. The basal length of the distal part is virtually similar to that of the lobes. In M. monodactylus (Fig. 2, 4), the lobe setae are comparatively short; setae ψ1 and τ1 are longer than setae ψ 2 and ψ 2–4. In T. major (Fig. 2, 5), all these setae are small, approxi-mately of the same size. In both species, setae τ2–4 are

arranged on the lobes approximately at the same level (along a weakly expressed diagonal). Six small setae k are found in the base of the distal part of the oviposi-tor.

The family Nothridae. Three species were exam-ined (table): Nothrus anauniensis (Fig. 1, 1, 2), N. borussicus Sellnick, 1928, and N. silvestris Nicolet, 1855. The ovipositors possess a similar structure in all the species examined. They are large (135–159 × 69–86); the length of the base of the distal part exceeds that of the lobes. Setae ψ1 and τ1 are long, several times as long as setae ψ2 and τ2–4. Setae τ2–4 are arranged on lobes L2 and L3 transversely, forming a triangle (setae τ 3 are attached only slightly higher than τ 2 and τ4). The base of the distal part of the ovi-positor bears 4 setae k.

The family Camisiidae. The following four species of the genus Camisia Heyden, 1826 and three species of the genus Heminothrus Berlese, 1913 were exam-

Characters of the ovipositor structure in oribatids of the superfamily Crotonioidea

Taxon lDp wbDp lψ1, τ1 lΨ2 lτ2 l τ3 l τ4 lIk Numberof setae,

k Mainothrus badius (Berlese, 1905) 90–110 41–53 20–28 10–12 10–12 10–12 10–12 8–12 6 Trhypochthoniellus longisetus

(Berlese, 1904) 49–61 28–45 20–24 6–8 6–8 6–8 6–8 4–6 6

T. cladonicola (Willmann, 1919) 65–82 36–41 28–32 12–16 12–16 12–16 12–16 12–16 6 Trhypochthonius tectorum

(Berlese, 1896) 61–77 41–65 16–28 12–16 12–16 12–16 12–16 12–20 6

Malaconothrus monodactylus (Michael, 1888)

49–57 28–36 12–16 4–8 4–8 4–8 4–8 2–6 6

Trimalaconothrus major (Berlese, 1910)

28–36 36–49 6–8 6–8 6–8 6–8 6–8 2–4 6

Nothrus anauniensis Canestrini et Fanzago, 1876

135–143 69–77 73–86 20–24 20–24 20–24 20–24 16–20 4

N. borussicus Sellnick, 1928 135–147 69–82 77–86 20–24 20–24 20–24 20–24 16–20 4 N. silvestris Nicolet, 1855 139–159 73–86 82–98 20–24 20–24 20–24 20–24 16–20 4 Camisia biurus (Koch, 1839) 69–82 49–65 49–53 8–12 16 32–41 12 12–16 6 C. segnis (Hermann, 1804) 61–77 45–53 20–28 4–8 12–16 12–16 12–16 8–12 6 C. spinifer (Koch, 1835) 77–86 53–65 36–45 10–12 12–16 12–16 12–16 4–6 6 C. sowej Colloff, l993 69–82 49–61 10 6–8 8–10 8–10 8–10 8 6 Heminothrus longisetosus

Willmann, 1925 106–127 53–61 49–57 16–20 16–20 16–20 16–20 16 6

H. thori (Berlese, 1904) 143–155 73–94 28–41 8 8 8 8 8 6 H. peltifer (Koch, 1839) 147–159 82–102 53–57 20 16–20 20–24 16–20 16 6 Notes: (l) length; (w) width; (Dp) distal part of ovipositor; (bDp) base of distal part of the ovipositor; (ψ, τ) setae on lobes; (k) setae at

base of the distal part of ovipositor.

ERMILOV


1076

ined (table): C. biurus, C. segnis, C. spinifer, C. solho-eyi, H. longisetosus, H. peltifer, and H. thori. Grand-jean (1956) examined the structure of the ovipositor in Heminothrus targionii (Berlese, 1855). In representa-tives of the genus Camisia, the ovipositors are of me-dium size (61–86 × 45–65). The length of the distal part slightly exceeds the width of the ovipositor. The ovipositors of C. biurus (Fig. 2, 6), C. segnis (Fig. 2, 7), and C. spinifer are structurally similar. Setae ψ1 and τ1 are long, setae τ2–4 are shorter; setae ψ2 are the shortest. In representatives of C. segnis and C. spinifer, setae τ2–4 are approximately of the same size; in C. biurus, they distinctly differ in length (τ2 16, τ3 32–41, τ4 12). In the mites C. solhoeyi (Fig. 2, 8), all the setae on lobes are short and ap-proximately of the same size. In all the species, setae τ2–4 on lobes L2 and L3 are arranged diagonally; the base of the distal part bears 6 setae k.

In the studied species of the genus Heminothrus, the ovipositors are large (106–159 × 53–102). The ratio between the lengths of the basal part of the ovipositor and of the lobes differs: in H. longisetosus and H. peltifer (Fig. 2, 10), the length of the base of the distal part considerably exceeds that of the lobes; in Heminothrus thori (Fig. 2, 9), on the contrary, the base is considerably shorter. In H. longisetosus and H. peltifer, lobe setae ψ1 and τ1 are long, 2–3 times as long as setae ψ2 and τ2–4. In Heminothrus thori, all the setae are spicular; ψ1 and τ1 are large spines; ψ2 and τ2–4, are small spines. The ovipositor of H. targionii (Grandjean, 1956) is structurally similar to the ovi-positors of H. longisetosus and H. peltifer. In all the species of the genus Heminothrus, setae τ2–4 on lobes L2 and L3 are arranged diagonally; the base of the distal part bears 6 setae k.

The Main Differences in the Ovipositor Structure in Representatives of Crotonioidea

The shape and size of the ovipositor. The oviposi-tors are elongate; the total length of the distal part exceeds its basal width, except for a single species, T. major. The difference between the length and width of the distal part may be significant (e.g., in species of the genera Nothrus and Heminothrus, and in the spe-cies Mainothrus badius, Trhypochthoniellus long-isetus, and Malaconothrus monodactylus) or very in-significant (in species of the genera Trhypochthonius and Camisia).

The smallest ovipositor is characteristic of that in species of the family Malaconothridae; medium size,

in species of the family Trhypochthoniidae and the genus Camisia; the largest, in species of the family Nothridae and the genus Heminothrus.

In all the species, the basal length of the distal part exceeds the length of the lobes or these lengths are approximately equal, except for Heminothrus thori, in which the lobes are considerably longer.

Differences in the chaetom of the ovipositor. Dif-ferences were observed in the structure of lobe setae, arrangement of setae τ2–4, and the number of setae k. In the majority of species examined, lobe setae are more or less long and fine; setae ψ1 and τ1 are longer than others, and setae ψ2, τ2, τ3, and τ4 are nearly of the same length; in T. major and C. solhoeyi, all the setae are small, of approximately the same size; in species of the genus Camisia, setae ψ2 are shorter than τ2–4; in C. biurus, setae τ2–4 distinctly differ from each other in length. In Heminothrus thori and species of the genus Trhypochthonius, setae are spicular.

The arrangement of lobe setae τ 2–4 is also different. In some species, their thecae form a triangle of longer (species of the genus Trhypochthonius) or shorter (species of the genus Nothrus) height; in other species, they are arranged along a single (more or less inclined) line; in M. badius, seta τ2 is situated considerably lower than the converging setae τ 3 and τ 4.

In the majority of the examined species, 6 setae k were found; only representatives of the genus Nothrus possess 4 setae.

Comparative Analysis of the Ovipositor Structure in Representatives of Macropylina (with Crotonioidea

as the Example) and Brachypylina

It seems expedient to compare the structure of ovi-positors in species of Crotonioidea as representatives of the lower oribatids (Macropylina) with the oviposi-tor morphology in previously studied 60 species of the higher oribatid mites (Brachypylina) (Ermilov, 2010). The following morphological criteria were compared: (1) the shape of the ovipositor, (2) the ratio between the lengths of the base of the distal part and the lobes; and (3) the structure of the chaetom.

The shape of the ovipositor varies inconsiderably. In the overwhelming majority of Brachypylina, both cylindrical part and lobes are well-developed, strongly elongate; in many species of Crotonioidea, they are wider and shorter. Only some species of Brachypy- lina (species of the genus Damaeus Koch, 1835), and



1077

Fig. 2. Ovipositors of species of Crotonioidea: (1) Mainothrus badius, (2) Trhypochthoniellus longisetus, (3) Trhypochthonius tectorum, (4) Malaconothrus monodactylus, (5) Trimalaconothrus major [dorsal view], (6) Camisia biurus, (7) С. segnis, (8) C. solhoeyi, (9) Heminothrus thori, (10) H. peltifer. Scale 50 μm.

ERMILOV


1078

also of Crotonioidea (species of the genera Trhypoch-thonius and Camisia) are characterized by a very wide distal part of the ovipositor: its diameter is only slightly shorter than the length of the lobes (Figs. 2, 3, 6–8).

The ratio between the lengths of the base of the distal part and lobes of the ovipositor differs in oribatid mites belonging both to Macropylina, and to Brachypilina. According to this character, all the mites can be conditionally subdivided into three groups: (1) species with lobes considerably longer than the basal length of the distal part; (2) species with the basal length of the distal part exceeding the length of the lobes; and (3) species with equal length of the mentioned parts. Species belonging to one of these groups are found both among the lower and the higher oribatid mites; the majority of the species belongs to the second and the third group.

The structure of the chaetom. Such characters as the number of setae, their structure, arrangement, and size, were analyzed. In all the studied species of Macropylina and virtually in all representatives of Brachypylina, 12 setae on lobes were found; only in three species of the higher mites (Oppia nitens Koch, 1836, Ramusella clavipectinata (Michael, 1885), and R. alejnicovae (Krivolutsky et Gatilova, 1974)), 10 setae were found (τb are absent on lobes L2 and L3).

Arrangement of setae τ2–4 and τa–c is an important character distinguishing representatives of Crotoni-oidea and Brachypylina.1

In the majority of Crotonioidea (Mainothrus badius, Trhypochthoniellus longisetus, representatives of Ma-laconothridae and Camisiidae), setae τ 2–4 are arranged diagonally; we do not know any representative of the higher oribatids with such an arrangement of τa–c.

A relative similarity in the arrangement of setae τ 2–4 (τ a–c) was observed in mites of the genera Nothrus and Trhypochthonius (Macropylina) and Damaeus riparius (Brachypylina). In these species, the setae are situated close to each other and their thecae form a triangle. It should be noted that nearly in all the species of _____________ 1 We follow designations assumed by Grandjean (1956), who used

designations τ 2–4 for τ setae on lobes L2 and L3 for ovipositors of mites of the group Macropylina, and designations τa–c, for re-presentatives of Brachypylina, because it is not clear whether these setae are homologous in representatives of the higher and the lower oribatids.

Brachypylina, setae τb are situated considerably higher than setae τa and τ c.

In the majority of the examined Macropylina and Brachypylina, the setae on the lobes are long; the length ratio is the following: ψ1 ≈ τ1 > ψ2 ≈ τ2 ≈ τ 3 ≈ τ 4 and τ1 > ψ2 ≈ τa ≈ τb ≈ τc. However, in some species of both the lower and the higher oribatids, all the setae on the lobes can be, e.g., spicular or small; they may be of the same length (Figs. 2, 3, 5, 8, 9; Ermilov, 2010).

The number of setae k may differ in representatives of each group. In the majority of Macropylina, 6 well-developed setae are present; species of the genus Nothrus, with their 4 setae, are an exception. Repre-sentatives of Brachypylina usually possess 6 setae k; in some species, they are very small and in some spe-cies they were totally absent.

No identity in all the compared characters was re-vealed between representatives of the higher and the lower oribatids; it was found, that the closest similar-ity was characteristic of the mites of the genera Trhy-pochthonius (Macropylina) and Damaeus (Brachy-pylina), differing only in the ratio between the lengths of the setae on the lobes.

The ovipositor morphology in representatives of Macropylina, even belonging to the same genus, may be similar (e.g., in species of the genus Nothrus), or may strongly differ (e.g., in species of the genus Heminothrus); at the same time, representatives of the higher oribatids examined by me, possess the same structure of the ovipositor within the same genus. However, further accumulation of information con-cerning the morphology of ovipositors in Brachypylina may also reveal some differences in some genera.

CONCLUSION The structure of ovipositors was examined in

16 mite species of the superfamily Crotonioidea. Simi-larity in the ovipositor structure in all the species of Crotonioidea includes its basic structure, folded in-tegument, and the presence of 12 setae on lobes. The differences concern the shape and size of the oviposi-tor and relative basal length of the distal part and lobes. Differences between the species of the super-family concern the length and arrangement and, less frequently, the shape of setae on lobes of the oviposi-tor; the number of setae k in different species can vary (6 or 4). Ovipositor morphology in species belonging to the same genus may be virtually identical (e.g., in species of the genus Nothrus) or may strongly vary (as in species of the genus Heminothrus).



1079

In all the lower oribatids, 12 setae on the lobes were found; the higher oribatids are characterized by the presence of 12 and 10 setae; differences in the number of setae k are observed in representatives of both groups. Arrangement of setae on lobes in both groups can be similar when their thecae are arranged in the shape of a triangle; at the same time, their diagonal arrangement was noted only in Macropylina. Differ-ences in the structure of ovipositors in some species of the lower and higher oribatids can be more or less considerable; however, no cases of the identical struc-ture of ovipositors were revealed in both groups. The closest morphological similarity was observed in ovi-positors of species of the genera Trhypochthonius (Macropylina) and Damaeus (Brachypylina).

ACKNOWLEDGMENTS

The author is grateful to R.A. Norton (State Univer-sity of New York, College of Environmental Science and Forestry, USA) for providing reprints of scientific publications necessary for the preparation of the manuscript.

REFERENCES

1. Badejo, M.A., Woas, S., and Beck, L., “Redescription of Archegozetes magnus (Sellnick, 1925) (Trhypo-chthonioidea) from Brazil and Description of Two New Species of Nanhermanniid Mites: Bicyrthermannia ni-geriana and Mastermannia seropedica (Nanhermanni-oidea) (Acari: Oribatida),” Genus 14 (1), 125–149 (2002).

2. Bayoumi, B.M. and Mahunka, S., “Ergebuisse der Bhu-tan-Expedition 1972 des naturhistorischen museums in Basel. Acari: fam. Oribatatidae (part I),” Entomologica Basiliensia 4, 13–30 (1979).

3. Ermilov, S.G., “Individual Development of the Oribatid Mite Nanhermannia coronata (Acari, Oribatida, Nan-hermanniidae),” Zool. Zh. 88 (4), 429–437 (2009) [En-tomol. Rev. 89 (3), 314–322 (2009)].

4. Ermilov, S.G., “The Structure of Ovipositors in Higher Oribatid Mites (Acari, Oribatida, Brachypylina),” Zool. Zh. 89 (6), 694–702 (2010) [Entomol. Rev. 90 (6), 783–792 (2010)].

5. Grandjean, F., “Étude sur les Palaeacaroides (Acariens, Oribates),” Mem. Mus. Nat. Hist. Natur. Paris (N.S.). Ser. A. Zool. 7, 179–274 (1954).

6. Grandjean, F., “Caracteres chitineux de l’ovipositeur, en structure normale, chez les oribates (Acariens),” Arch. Zool. Exp. Gen. Notes et Revue 93 (2), 96–106 (1956).

7. Norton, R.A., Behan-Pelletier, V.M., and Wang, H.-f., “The Aquatic Oribatid Mite Genus Mucronothrus in Canada and the Western USA (Acari: Trhypochthonii-dae),” Can. J. Zool. 74, 926–949 (1996).

8. Norton, R.A. and Behan-Pelletier, V.M., “Eniochtho-nius mahunkai sp. n. (Acari: Oribatida: Eniochthonii-dae), from North American Peatlands, with a Redescrip-tion of Eniochthonius and a Key to North American Species,” Acta Zool. Hung. 53, 295–333 (2007).

9. Norton, R.A. and Behan-Pelletier, V.M., “Oribatida. Chapter 15,” in A Manual of Acarology. (Texas Tech Univ., Lubbock, 2009), pp. 430–564.

10. Subías, L.S., “Listado sistémático, sinonímico y bio-geográfico de los acáros oribátidos (Acariformes: Oribatida) del mundo (excepto fósiles),” Graellsia 60 (número extraordinario), 3–305 (2004) (Online version actualized in April 2009; http: //www.ucm.es/info/zoo/ Artropodos/Catalogo.pdf.

morphology of ovipositors in oribatid mites of the superfamily crotonioidea (acari, oribatida)

Documents