Erythraeus (Zaracarus) rupestris (Linnaeus, 1758)

Karakurt, İbrahim, Wohltmann, Andreas, Pamuk, Eyüp Efe & Sevsay, Sevgi, 2022, Correspondence of larval and postlarval instars in two species of the subgenus Zaracarus (Acari: Erythraeidae: Erythraeus) established with laboratory rearing, Zootaxa 5150 (3), pp. 357-380 : 368-377

Erythraeus (Zaracarus) rupestris (Linnaeus, 1758)

E. (Z.) eleonorae Haitlinger, 1987 syn. nov.

E. (Z.) didonae Haitlinger, 2000 syn. nov.

For other synonyms see: Mąkol & Wohltmann (2012)

Material examined. 7 adults, 5 deutonymphs, and 4 larvae sampled in the National Park “Lower Oder Valley”, Land Brandenburg, Germany, in 1999–2001, plus 5 larvae reared from eggs deposited by three females collected at the same locality .

Depository. Vouchers representing all active instars are deposited in the acarological collection of the Senckenberg Museum für Naturkunde Görlitz, further specimens remain in the second author’s collection.

Diagnosis. Adult. Habitus as typical for the genus, palp genu without conalae and 0–2 semiconalae; palp tibia with 3–5 conalae plus 0–2 semiconalae. Anterior sensillary area of crista metopica with anterior process and with 10–16 non-sensillary setae. Dorsal opisthosomal setae of variable lengths (35–120), setiform with stout setules. Distinct serratalae present on telofemur-tibia IV, on telofemora II–III weak, absent on genua and tibiae I–III.

Deutonymph. Similar to adults but much smaller ( Table 1 ). Palp genu without conalae or semiconalae, palp tibia with 2–3 conalae and without semiconalae. Anterior sensillary area of crista metopica with 5–7 nonsensillary setae (AM). Dorsal setae (50–88) similar to those of the adults. Genital sclerite small (25), without median opening.

Larva. Habitus as typical for the subgenus, AL inflated basally, ASens moderately short (26–40), bases of ASens setae with pouch-like structures, fD = 40–44, fV = 8–10, fnbFe = 2-2-2, length of tarsus III> 120, length of tibia III 230–311.

Description. Adult ( Figs. 8–10 ) (based on 7 specimens). Metric data in Table 1 . Body length 1000–2000, width 700–1200 depending of nutritional state, habitus typical for the genus ( Fig. 8 ). Colour in live specimens reddishbrown, eyes bright red.

Gnathosoma. Chelicerae typical, of erythraeid type. Palps with relatively sparse setation. Normal, setulated setae present on palp trochanter and palp femur. Palp genu with strong, serrate setae dorsally, smooth and more slender setae laterally, without conalae but with 0–2 semiconalae. Palp tibia ( Fig. 9a ) with normal, sparsely barbed setae, with 3–5 conalae and 0–2 semiconalae. Odontus hook-like. Palp tarsus hemispherical, with the apical part overreaching the termination of odontus, densely covered with eupathidia and solenidia.

Idiosoma. Scutum ( Fig. 9b ) delicate and almost limited to crista metopica. Anterior process of ASA present, posterior process of PSA short. ASA with 10–16 setulose setae AM. ASens and PSens covered with very tiny barbs. PSens slightly longer than Asens, bases of ASens and PSens with pouch-like structures. Punctated ocular plates (50–75 × 100), located laterally to crista, at ca. half of its length, anterior and posterior lens of about the same size (diameter: 14–20). Dorsal setae ( Fig. 9c ) uniform in shape but with variable lengths (35–120), rounded at tip, covered with stout setules. Ventral setae (35–80) slender, covered with short setules. GOP surrounded by paired sclerites (genital plates: epivalves with 59–66 setae and centrovalves with 17–22 setae), located at the level of coxae III, IV. Setae covering valves shorter than VS, slender, with delicate barbs. AOP surrounded by indistinct paired valves, of those—the external valves more sclerotized with 9–11 pairs of setae. Setae covering valves similar to those covering genital plates, but shorter (10–16).

Legs. Serratalae ( Fig. 10 ) on telofemora II–III weak, absent on genua and tibiae I–III. Normal setae with small setulae present on all leg segments. Specialized setae distributed on bFe-Ta. Tarsi I–IV terminated in paired claws, each claw covered with fimbriae.

Deutonymph (based on 5 specimens). Metric data in Table 1 . Habitus and morphological characters similar to adults, but much smaller; body length about 600–700, width 410–750 in freshly emerged specimens, body length 900–1500, width 980–1330 in specimens collected in the field. Colour in live specimens as for adult. Palp genu without conalae or semiconalae, palp tibia with 2–3 conalae and no semiconalae. Anterior sensillary area of crista metopica with 5–7 nonsensillary setae (AM). Crista metopica well sclerotized, scutum inconspicuous with anterior process. Dorsal setae (50–88) similar to those of the adults. Genital sclerite small (25) carrying 2–3 pairs of smooth, thin setae; and without opening. Anal sclerites surrounding the anal opening elongate (70–80) and with 4–6 pairs of smooth, thin setae.

Larva ( Figs. 11–14 ) (based on 9 specimens). Metric and meristic data in Tables 2 , 3 . Freshly emerged larvae of orange-red coloration, with body length 300–400, width 220–260 ( Fig. 11 ).

Gnathosoma ( Fig. 13b ). Chelicera with cheliceral base (120–140) and movable claw, the latter with a distinct hook on the blade. Dorsal gnathosoma with a pair of smooth, pointed adoral setae (cs) (44–50) anteriorly and a pair of club-shaped supracoxal setae (elcp) (5–8) in lateral position. Ventrally a pair of smooth, pointed subcapitular (tritorostral) setae (bs) (58–78) and a pair of spine-like oral setae (as) (10–14). Palp femur and genu each with one setulose seta dorsally, seta (55–70) on palp femur always shorter than seta (70–90) on palp genu. Palp tibia with three almost smooth setae. Odontus bifid in its distal half. Palp tarsus with two long and four shorter almost smooth normal setae, one solenidion (ω) and one prominent distal eupathidium (ζ); the latter accompanied by a small seta z. Palp formula: 0-N-N-NNN 2 -NNNNNNωζ z.

Idiosoma ( Figs. 12a, b ). Scutum ( Fig. 13a ) punctate and wider than long, roughly hexagonal, anterior border straight, lateral and posterior borders rounded, carrying two pairs of serrate normal setae and two pairs of sensilla. Anterior sensilla with distinct setules in its distal half much shorter than posterior ones, which are almost smooth. Anterior trichobothrium tipped anteriorly with pouch-like structures surrounding its basis (detail in Fig. 12a ). Anterior normal setae (AL) widened near basis, much longer than posterior normal setae (PL). Laterally of scutum paired eyes, diameter of anterior lens (15–20) slightly larger than that of posterior lens (14–18). The remaining part of dorsum with smooth, folded in lines cuticle. Dorsal setae (50–90) apically pointed, serrate. Total number of dorsal and ventral idiosomal setae (NDV) ranges from 48 to 52, not considering setae located on scutum and coxae as well as intercoxal (1a, 3a) setae. Coxa I with minute (2–4) supracoxal seta (elcI), serrate seta 1b (85–101), serrate seta 1a (50–70) located outside close to coxa I. Coxa II with serrate seta 2b (40–50). Coxa III with serrate seta 3b (40–50), serrate seta 3a (40–55) located outside between coxae III. Posterior to coxae III four pseudanal setae (40–80), which are distinctly thinner than the neighbouring idiosomal setae located more posteriorly.

Legs ( Fig. 14 ). Segmentation formula: 7-7-7. For leg chaetotaxy and morphometric data see Tables 2 , 3 . Solenidia on genu I and tibia I small (20–37), both solenidia (φ) on tibia I in distal half of the segment, distal solenidion on tibia I with accompanying seta z. Solenidion (ω) on tarsus I prominent (30–40), famulus (ε) (4–5) small, inconspicuous. Subterminal eupathidium on tarsus I long (40–50) and with accompanying seta z (7–14), ‘pretarsal’ eupathidium shorter (25–27), without z. All solenidia on leg II short (20–28); solenidia on tibia II close to the distal and proximal border of the segment, respectively. Subterminal eupathidium on tarsus II long (45–58) and with accompanying seta z (7–15), ‘pretarsal’ eupathidium shorter (20–25). Solenidion on tibia III short (25–33) and close to the proximal border of the segment, ‘pretarsal’ eupathidium short (20–25). Median empodium of pretarsi I–III claw-like, with small lateral barbs. Anterior lateral claw with, posterior lateral claw without terminal hook. Both lateral claws with several branching setules (aliform).

Distribution. Western Palaearctic ( Mąkol & Wohltmann 2012).

Taxonomic remarks. No obvious differences were detected when comparing laboratory reared and field-born larvae of E. (Z.) rupestris . Because of particular design of AL as well as the orientation of anterior sensilla in the larva, the species undoubtedly belongs to the subgenus Zaracarus . The larva of E. (Z.) eleonorae Haitlinger, 1987 collected in Poland fits in all characters ( Haitlinger & Šundić 2015b) to larvae reared from E. (Z.) rupestris adults and is considered as subjective junior synonym. The single larva described as E. (Z.) didonae Haitlinger, 2000 collected in Turkey and a second specimen collected in Syria ( Barbar 2018) show minor differences in metric parameters ( Table 2 ) and is also considered as a subjective junior synonym. The separation of E. (Z.) didonae and E. (Z.) eleonorae in the key published by Xu et al. (2019) is based on the erroneous inclusion of E. (Z.) eleonorae into the group of species having three normal setae on basifemora I–III. Haitlinger (2000) and Barbar (2018) both stated in their descriptions that the basis of AL is not inflated in E. (Z.) didonae ; however, the drawings ( Haitlinger 2000) and microphotograph ( Barbar 2018) unambiguously show a basal widening of setae AL comparable to the state described for E. (Z.) rupestris .

For differences of E. (Z.) rupestris and E. (Z.) budapestensis see above. Erythareus (Z.) rupestris differs from E. (Z.) kurdistaniensis and E. (Z.) arminouensis by the longer seta on palp genu (>55 vs <50) and the longer seta AL (>190 vs <176), along with the larger average sizes in several other characters of which, however, ranges overlap.

Biology. Field data. The phenology of E. (Z.) rupestris was analyzed by regular samplings at four localities in the National Park “Lower Oder Valley” (Land Brandenburg, Germany) three times a month during 1999–2001. All sampling areas nearby the city Schwedt (around Lake Mariensee, close to a ditch at Teerofen, nearby Mummert creek) on fresh meadows in the inundation area. Vegetation naturally dominated by Carex spp. and Phragmites autralis , regular mowing leads to a dominance of sweet grasses ( Poaceae ). Postlarval instars were captured manually; moreover, sweep nets were used to collect larvae and its hosts. Localities in the National Park inhabited by E. (Z.) rupestris are characterized through annual inundation during winter. Active instars appeared as soon as water levels decrease. Larvae (n = 85) were captured from June to September ( Fig. 15 ) with maximum abundance in late July and August. Hosts (n = 22) of the parasitic larvae always were Cicadomorpha (Homoptera: Auchenorrhyncha), in most cases only one E. (Z.) rupestris larva was found on a host, maximum parasitic load was four mites. One of the hosts was additionally parasitized by one larva of the genus Leptus Latreille, 1795 . The percentage of parasitized hosts compared to all potential hosts captured did not exceed 10% at any sample location or date. Few protonymphs (n = 4) were found within the hollow stem of dead grass or crevices in the litter layer, in August–September and in April just after the end of the flooding period. Deutonymphs (n = 13) were abundant in May, tritonymphs (n = 5) were also captured in May hidden in the litter layer. Adults (n = 48) appeared in May and were present until the end of June. The annual appearance of instars did not differ in the years of observation.

Laboratory data. Adult mites were kept individually or in small groups eggs were deposited in clusters of 51– 157 eggs, preferably in crevices. Eggs were ovoid (280 × 300 µm) and of an orange-reddish colour when deposited. Within 24 hours the colour of eggs changed to deep black. No parental care was observed. When an orange band appeared due to the split of egg shells, eggs have reached the prelarval stage. Larvae hatched 30–41 days (at 20 °C, n = 350 eggs) and 67–70 days (at 15 °C, n = 62 eggs) after deposition of eggs. The active larvae displayed positive phototactic responses; without exposure to potential hosts they survived for up to 20 days (20 °C, n = 150). Each 10–15 unfed larvae were exposed to various arthropods sampled in the field (Opilionida, Diptera, Heteroptera, Coleoptera, Cicadelloidea ) in standard rearing boxes; however, only representatives of Auchenorrhyncha were parasitized. Attachment to the host was very quick and occurred at first contact to the host. As a result, E. (Z.) rupestris larvae did not display any particular site preference but were found to attach to various body parts of the host. The duration of the parasitic phase was not observed in laboratory; larvae captured parasitic on hosts in the field continued the parasitic phase at maximum for three days in the lab (20 °C). Usually postparasitic larvae entered the calyptostatic protonymph 1–2 days after leaving the host, preferably in crevices of the substratum. If no such crevices were available, the postparasitic active phase of larvae was prolonged and specimens spent up to 22 days (20 °C) in searching for suitable places to hide before they finally entered the protonymph on the flat ground of rearing boxes. The further development stopped in an early protonymphal phase. No development to the deutonymph took place in specimens exposed to constant 20 °C (n = 5, maximum exposure 235 days). After exposure to 5 °C for 114–157 days all protonymphs developed into deutonymphs within 8–14 days after re-exposure to 20 °C (n = 8, natural light conditions). However, in all specimens (n = 5) which were re-exposed to 20 °C in March (daily illumination <12 hours), deutonymphs remained within the protonymphal exuvia and did not hatch. Rising of temperature up to 25 °C did also not induce hatching. Of these specimens, three hatched to deutonymphs 55–60 days later, when daily illumination was>12 hours. These deutonymphs displayed deformations of legs and had difficulties in the coordination of leg movement. None of these specimens reached the tritonymph. Those protonymphs (n = 3) which were re-exposed to 20 °C in May (daily illumination>12 hours) after chilling did develop into deutonymphs and hatched 19 days later. These deutonymphs displayed normal movement, no malformations were detected. One of the specimens was preserved after emergence for taxonomic investigations, the other two reached the tritonymph and subsequently the adult instar. One protonymph was exposed to 76% relative humidity generated above saturated salt solution according to Winston & Bates (1960) for 18 days, during this time it developed into the deutonymph as other protonymphs kept at saturated relative humidity (100%) did. Larvae of ants, nymphs and adults of aphids, adults of Microtrombidium pusillum and Atractothrombium sylvaticum (Parasitengona: Microtrombidiidae ) were offered to E. (Z.) rupestris deutonymphs as potential food: all of them were attacked and at least partially sucked out by E. (Z.) rupestris . Moreover, intraspecific predation was observed in deutonymphs and adults of E. (Z.) rupestris . Regularly fed specimens entered the calyptostatic tritonymph 16–17 days (n = 2, 20 °C) after emergence of the deutonymph. The duration of the tritonymph until the emergence of adults was 10–12 days (n = 5, 20 °C). Adults fed on the same prey as deutonymphs. Spermatophores were deposited 16 days after emergence of the adult instar at subsaturated humidity conditions; spermatophores consist of a whitish stalk and a red sperm droplet.

Discussion on Biology Erythraeoidea are adapted to withstand desiccation ( Wohltmann 2000; Wohltmann et al. 2001) and usually found in xeric environments. Erythaeus (Z.) rupestris represents an exception in habitats, because it colonizes amphibious biotopes, where it survives inundation periods hidden in crevices and dead grass ( Wohltmann 2005). However, since protonymphs do not dry out at 76% relative air humidity, desiccation resistance seems comparable to that of other Erythraeoidea ( Wohltmann 1998) and is obviously not decreased.

The strictly univoltine life cycle of E. (Z.) rupestris follows the general pattern of Erythraeoidea ( Wohltmann 2000). The protonymph is the only hibernating instar; hibernation takes place in obligatory diapause. No environmental trigger inducing the diapause is evident, thus the beginning of the diapause is obviously correlated to reaching a particular ontogenetic phase as found in other terrestrial Parasitengona ( Wohltmann 2000). In E. (Z.) rupestris , the early protonymph seems to induce diapause. A chilling phase of about 100 days has been found in other Parasitengona as a necessary step to break the diapause ( Wohltmann 2000), and this seems also the case in E. (Z.) rupestris . In other Parasitengona, e.g. Johnstoniana spp. ( Eggers 1995) , a raise in temperature subsequent to the chilling phase is sufficient to break the diapause and to induce continued development. In E. (Z.) rupestris , such increase in temperature results in the development of the deutonymph, but for leaving the protonymph exuvia by the deutonymph, additionally prolonged daily illumination is necessary. This is first evidence for the day-length constituting a factor in breaking the diapause in Parasitengona.

Figures

FIGURE 8. Erythraeus (Zaracarus) rupestris (Linnaeus, 1758), adult: Habitus, dorsal view.

FIGURE 9. Erythraeus (Zaracarus) rupestris (Linnaeus, 1758), adult: a—palp genu, tibia and tarsus (lateral view) and medial view of palp tibia and tarsus, b—scutum with crista metopica and position of lateral eyes, c—posterior dorsal body setae.

FIGURE 10. Erythraeus (Zaracarus) rupestris (Linnaeus, 1758), adult: Leg setae.

FIGURE 11. Erythraeus (Zaracarus) rupestris (Linnaeus, 1758), larva: Habitus of unfed larva in dorsal view.

FIGURE 12. Erythraeus (Zaracarus) rupestris (Linnaeus, 1758), larva: a—dorsal view of idiosoma with details of posterior dorsal seta and anterior sensillum, b—ventral view of idiosoma with detail of seta ps.

FIGURE 13. Erythraeus (Zaracarus) rupestris (Linnaeus, 1758), larva: a—scutum. b—gnathosoma, ventral view. Abbreviations: AL—anterior lateral seta, ASens—anterior sensillum (AM of other authors), PL—posterior lateral seta, PSens—posterior sensillum, as—oral spine like seta, bs—hypostomal seta, cs—adoral seta, elcp—supracoxala, ω—solenidion, ζ—eupathidium.

FIGURE 14. Erythraeus (Zaracarus) rupestris (Linnaeus, 1758), larva: Legs I–III. Details of tarsus (ta) I–III (normal setae omitted). Abbreviations: elcI—supracoxal seta, z—accompanying seta, ω—solenidion on tarsus, ζ—eupathidium, φ—sole- nidion on tibia, ε—famulus, κ—microseta, σ—solenidion on genu.

FIGURE 15. Erythraeus (Zaracarus) rupestris (Linnaeus, 1758), Phenology based on cumulated data of regular field samplings 2000–2001 in the National Park ‘Lower Odra Valley’. LA—larva (n=85), PN—protonymph (n=4), DN—deutonymph (n=13), TN—tritonymph (n=5), AD—adult (n=48).