Kiany, Najmeh ¹ ; Seiedy, Marjan ² ; Hakimitabar, Masoud ³ and Husemann, Martin ⁴

¹School of Biology and Center of Excellence in Phylogeny of Living Organisms, College of Science, University of Tehran, Iran.
²✉ School of Biology and Center of Excellence in Phylogeny of Living Organisms, College of Science, University of Tehran, Iran.
³Department of Horticulture and Plant Protection, College of Agriculture, Shahrood University of Technology, Shahrood, Iran.
⁴Leibniz Institute for the Analysis of Biodiversity Change, Museum der Natur, Zoologie, Hamburg, Germany.

2023 - Volume: 63 Issue: 4 pages: 1260-1270

ZooBank LSID: 305A5B3D-9C52-4666-AC1F-E2B58827975E

Original research

Keywords

Abstract

Introduction

The Eutrombidiinae Thor, 1935 are a subfamily of mites within the Microtrombidiidae Thor, 1935 and currently include 13 genera (Wohltmann et al. 2007; Mąkol and Wohltmann 2012; Sevsay and Elverici 2023). Eutrombidium Verdun, 1909 is a genus within this subfamily that mainly parasitizes Orthoptera (Southcott 1993; Felska et al. 2018). Eutrombidium consists of 44 valid species, of which 23 species have been described based on larval stages only, three species both on larval and post-larval stages, and 18 species are only known from active post-larval stages (Mąkol and Wohltmann 2012, 2013; Haitlinger 2015; Noei and Šundić 2020).

The 17 species for which larval stages are known have small bilobed coxala with an incision in their distal half. These include E. robauxi Southcott, 1993, E. feldmanmuhsame Feider, 1977, E. fathipouri Karimi Iravanlou, Kamali & Talebi, 2000, E. aegyptium Karimi Iravanlou, Kamali & Talebi, 2000, E. tehranicum Karimi Iravanlou, Kamali & Talebi, 2000, E. elburzensis Karimi Iravanlou, Kamali & Talebi, 2000 and E. sorbasiensis Mayoral & Barranco, 2004 from the Palearctic region, E. trigonum (Hermann, 1804) from the Palearctic, Nearctic and Neotropical regions, E. orientale Southcott, 1993 from Nearctic, E. indicum Southcott, 1993 and E. sigirijanum Haitlinger, 2006 from the Indomalayan region, E. macfarlanei Southcott, 1993, E. pelebinum Haitlinger, 2007 and E. africanum Southcott, 1993 from the Afrotropical region, E. verdense Southcott, 1993 from the Afrotropical and Palearctic regions, E. australiense Southcott, 1993 from the Australasian region and E. fortunatae Haitlinger, 2005 from the Neotropics (Haitlinger 2015; Mąkol and Wohltmann 2012, 2013; Noei and Šundić 2020). These species can be separated from the other groups; i.e. six species that have lateral coxalae I and coxalae II and III with fully separated lobes and the incision extending about 3/4 of the length of the scobillum from the apex, the coxalae length for this group is larger in comparison to the previous one (\textgreater14 μm) (Saboori et al. 2000; Saboori and Nemati 2001; Saboori and Pesic 2006; Noei and Šundić 2020).

In this paper, we describe a new species of Eutrombidium from Iran with lateral coxalae I and coxalae II and III, with incisions in their distal half. The new species was found parasitizing the grasshopper Sphodromerus luteipes Uvarov, 1933 (Insecta: Acrididae: Calliptaminae).

Material and methods

Grasshoppers were collected with insect sweep nets during surveys in the Zagros Mountains, Fars province, by Najmeh Kiany and Mohsen Kiany. Sampling was conducted on 3 June 2020 in Kazerun, Fars Province (Iran). The grasshopper host was determined as S. luteipes based on the keys by Beĭ-Bienko and Mistshenko (1963) and with the help of the OSF (Cigliano et al. 2023) and input from Josip Skejo and Slobodan Ivkovic. Three mite larvae were detached from the hindwings of the grasshopper host using an insect pin. Specimens were preserved in 75% alcohol, cleared in Nesbitt's fluid, and mounted on microscopic slides using Faure's medium (Walter and Krantz 2009; Dhooria 2016).

Figures were drawn and measurements (given in micrometres) were taken using a BX51 phase contrast Olympus microscope equipped with a Camera Lucida. Images were captured and then stacked with Zerene Stacker Version 1.04. Digital drawings were prepared using the Adobe Illustrator version 23.1 based on the original pencil line drawings. Photographs were taken with a digital camera attached to a BX51 phase contrast Olympus microscope. The terminology and abbreviations were adapted from Southcott (1993) and Wohltmann et al. (2007).

Results

Family Microtrombidiidae Thor, 1935

Subfamily Eutrombidiinae Thor, 1935

Genus Eutrombidium Verdun, 1909

Eutrombidium parishanensis Kiany, Seiedy & Hakimitabar sp. n.

ZOOBANK: 28413E5E-59AC-4A0E-8405-41220C84DDA4x

(Figures 1–6)

Diagnosis

Distal bilobed setae on coxae I-III, small and with incisions on their distal half; coxalae 1b, 2b, and 3b bifurcate with two approximately equal lobes; h₂ (118–120) > h₁ (101 in holotype, not clear in paratypes); Ti III (53–55).

Description (larva)

(n = 3)

Dorsum — (Figure 1). Dorsal surface of idiosoma with 24 barbed setae in the holotype (in paratypes, the counting was impossible due to their abdomen damage). Dorsal setae arranged in 5 rows, c_1–3 (c₁ on scutellum), d_1–3 , e_1–3, f_1–2 and h_1–2, setae C₂ , d₁ and h_1–2 arise from punctate circle plates, d₁ plate (22–24 × 17–19) larger than C₂ (15–17 × 11–13), fD = 4+6+6+4+4= 24 (Figure 1). Scutum rectangular, punctate, and reticulate, with the upper part without reticular marks but lower and median parts strongly reticulated (Figures 5A and 5C) with two chitinous bars near AM setae, bearing three pairs of non-sensillary setae (AM, AL and PL) and one pair of sensilla (SE). The anterior part of the scutum convex, the posterior border concave between the bases of sensillary setae (SE); and the lateral borders straight. Sensillary setae (SE) thin and smooth, inserted between PL and AL. AM setiform and thinner than AL and PL, all setae nude. PL < AM < AL (AL, 1.7–1.8 times longer than PL; AM 1.3–1.5 times longer than PL).

One pair of eyes situated on the punctate ocular plate (46 ×24–26), anterior lens (diameter 17–19) larger than the posterior one (diameter 12–14). Posterior dorsal scutum (scutellum) trapezoidal, punctate and reticulated (Figures 5B and 5D); anterior border of scutellum convex, posterolateral and posterior borders straight, with one pair of nude scutalae (c₁) arising from anterior part.

Venter — (Figure 2). Ventral side of idiosoma with one pair of barbed and pointed sternal setae (3a) and with five pairs of barbed and pointed setae behind coxa III (fV). Coxa I with setae 1a; slender and nude, coxalae 1b, 2b and 3b bifurcate with two approximately equal lobes, 2b and 3b two times longer than the coxalae incision depth but in 1b, the depth looking shallower (Figure 6); and the coxalae length about 2–2.5 times incision depth, of course, the visual angle error after fixation of microscopic slides could be considered, Claparede's organ oval (12–14) diameter. Coxal plates punctate. NDV = 24+10 = 34.

Gnathosoma — (Figure 3). Gnathosoma projecting beneath anterior part of the scutum, oral ring horseshoe-like with open ends; hypostomal setae (bs) of conical shape, adoral setae (cs) short and pointed; chelicerae robust; cheliceral blade sickled-shaped with one tooth subterminally, 24–29 long. Palp femur and palp genu, each with one nude minute seta. Palp tibia with three nude setae; one long (26–30), the others short (7 and 3), of which one is situated close to the tibial claw (paradont) with a blunt tip. Palp tibial claw bifid with two diverging tines and a rounded tip. Palptarsus with three long and three short nude setae, a solenidion, and an eupathidium. fPp =0–N–N–NNN₂–6Nωζ.

Legs — (Figure 4). Leg segmentation formula 6–6–6. Leg setal formulae: Leg I: Ta 1ω, 1ε, 2ζ, 18n; Ti 2φ, 1κ, 6n; Ge 2σ, 1κ, 4n; Fe 6n; Tr 1n; Cx 2n (Figure 4A); Leg II: Ta 1ω, 1ε, 1ζ, 14n; Ti 2φ, 5n; Ge lσ, K, 2n; Fe 5n; Tr 1n; Cx 1n (Figure 4B); Leg III: Ta 13n; Ti 5n; Ge lσ, 2n; Fe 4n; Tr 1n; Cx 1n (Figure 4C).

Tarsi I and II with two sickle-like claws and a slender empodium (1), the posterior claw (p) thicker (3) than the anterior claw (a) (2). The outer claw of Ta III normal and falciform, but its inner claw modified into smilum, empodium curved and elongated. Tarsus III with one scopa (with six setules in the holotype and one paratype (ZUTC15001t)); five setules in another paratype (ZUTC15001u) and six–branched lophotrix. Metric data in Table 1.

Etymology

The species name is derived from the dried-up Parishan Lake. The grasshopper host specimen was collected from nearby mountains.

Type material and type location

The holotype (ZUTC15001s) and two paratype larvae (ZUTC15001t–u) were collected by M. Kiany 3 June 2020 in desiccated Parishan Lake, Kazerun, Fars Province, Iran (29°29′34.39″ N, 51°52′51.24″E; 842 m a.s.l.) (Figure 7). The main vegetation cover included Capparis spinosa, Heliotropium europaeum, Salsola sp., Astragalus sp., Carthamus sp., Tamarix sp., Alhagi sp., and Salicornia sp.; there were also corn and watermelon fields in the lakebed.

Type deposition

The holotype and one paratype (ZUTC15001s, ZUTC15001t) are deposited in the Zoological Museum, School of Biology, College of Science, University of Tehran, Iran. The grasshopper host is also kept in this museum. The second paratype (ZUTC15001u) is deposited in the Acarological Collection, Jalal Afshar Zoological Museum, Faculty of Agriculture, University of Tehran, Karaj, Iran.

Remarks

The new species belongs to the species group with the distal bilobed setae on coxae I-III, small and with an incision in the distal half. There are seventeen species in this group; among them, five species have reticulated scutum and scutellum (for metric and meristic data, see Table 2) like E. parishanensis Kiany, Seiedy & Hakimitabar sp. n.

Eutrombidium parishanensis Kiany, Seiedy & Hakimitabar sp. n. differs from E. orientale by longer L (158–161 vs. 120–145), PLN (24–26 vs. 14–18), h₂ (118–120 vs. 75–90), Ti I (60–65 vs. 38–50), Fe I (74–77 vs. 47–59), Ta II (96–98 vs. 63–74), Fe II (72–74 vs. 47–52), Ta III (77–84 vs. 51–62), Fe III (77–79 vs. 47–58), number of solenidia on Ge II (1 vs. 2); from E. australiense by longer AW (120–122 vs. 73–97), PW (125 vs. 89–113), SB (98–103 vs. 63–84), MSA (72–77 vs. 34–50), ASB (113–134 vs. 77–100), L (158–161 vs. 95–121), W (144–149 vs. 100–126), AMB (74–77 vs. 35–58), SE (101–108 vs. 56–80), h₂ (118–120 vs. 52–79), Ta I (101–108 vs. 48–74), Ti I (60–65 vs. 23–36), Fe I (74–77 vs. 36–51), Ta II (96–98 vs. 41–63), Ti II (50–53 vs. 20–30), Fe II (72–74 vs. 35–48), Ta III (77–84 vs. 35–51), Ti III (53–55 vs. 27–40), Fe III (77–79 vs. 38–55); from E. indicum by longer MA (74–82 vs. 57), AW (120–122 vs. 100–102), PW (125 vs. 104–106), SB (98–103 vs. 77–79), MSA (72–77 vs. 56), ASB (113–134 vs. 107), L (158–161 vs. 134), W (144–149 vs. 122–125), AMB (74–77 vs. 57–64), SE (101–108 vs. 80–90), PLN (24–26 vs. 19–20), PSW (130–134 vs. 113–115), QW (50–53 vs. 42–45), Ta I (101–108 vs. 90), Ti I (60–65 vs. 44–50), Fe I (74–77 vs. 54–59), Ta II (96–98 vs. 66), Ti II (50–53 vs. 36–38), Fe II, (72–74 vs. 54–56), Ta III (77–84 vs. 63–64), Fe III (77–79 vs. 59–63), shorter AM (38 vs. 45–48), QL (41–48 vs. 67–70); from E. robauxi by longer MA (74–82 vs. 54–57), AW (120–122 vs. 84–97), PW (125 vs. 90–98), SB (98–103 vs. 63–72), MSA (72–77 vs. 48–56), ASB (113–134 vs. 80–98), L (158–161 vs. 102–121), W (144–149 vs. 102–116), AL (46–48 vs. 29–38), AMB (74–77 vs. 47–57), SE (101–108 vs. 70–91), PSL (77 vs. 56–66), PSW (130–134 vs. 90–100), QW (50–53 vs. 27–43), h₂ (118–120 vs 81–98), Ta I (101–108 vs. 67–73), Ti I (60–65 vs. 36–40), Ge I (34–36 vs. 25–27), Fe I (74–77 vs. 44–57), Ta II (96–98 vs. 59–66), Ti II (50–53 vs. 29–34), Fe II, (72–74 vs. 44–52), Ta III (77–84 vs. 47–55), Ti III (53–55 vs. 36–40), Fe III (77–79 vs. 49–55); from E. macfarlanei by longer AW (120–122 vs. 91), PW (125 vs. 98), SB (98–103 vs. 75), MSA (72–77 vs. 25), ASB (113–134 vs. 59), L (158–161 vs. 82), W (144–149 vs. 110), AL (46–48 vs. 36), AMB (74–77 vs. 55), SE (101–108 vs. 84), PSL (77 vs. 70), PSW (130–134 vs. 98), QW (50–53 vs. 36), h₂ (118–120 vs. 96), Ti I (60–65 vs. 40), Fe I (74–77 vs. 55), Ta II (96–98 vs. 67), Ti II (50–53 vs. 34), Fe II (72–74 vs. 52), Ta III (77–84 vs. 61), Ti III (53–55 vs. 44), Fe III (77–79 vs. 59) and shorter QL (41–48 vs. 55).

Discussion

Eutrombidium is considered the most frequent parasite of grasshoppers and can be easily seen attached to the hind and forewings of adults and wing pads of nymph grasshoppers (Anderson 2019). Despite very similar morphology, the diversity in this genus is relatively large, with more than 40 species, and new species are frequently discovered. We here add a new species from Iran to the list.

Collected individuals of E. parishanensis Kiany, Seiedy & Hakimitabar sp. n. were larvae attached to the hind wings (basal part) of their host, like other Eutrombidium. Parishan Lake, adjacent areas, and nearby locations (Arjan and Dashtebarm) were sampled several times, but only at the first visit this host and its ectoparasites were recorded. Parishan Lake, the biggest freshwater Lake in Iran, has dried up entirely in recent years. The main factor responsible for dryness was aquifer depletion caused by over-pumping water for agriculture consumption, but also climate change affects the region strongly (Rahmani and Fattahi 2020; Ghazali 2012). While during the first year of collecting, the precipitation rate was high, the following year, apart from the water withdrawing for agriculture, the habitat suffered under severe drought, and the vegetation cover was poor compared to the previous year.

It remains unclear whether E. parishanensis might needs more humidity to survive or its host prefers a high vegetation cover, which was not available during the drought. It may also be helpful to better understand the species' phenology as we may have been too early or too late for the host to occur and hence missed the best time for collecting.

We report the calliptamine grasshopper Sphodromerus luteipes as a new as host for Parasitengona mites. This grasshopper has been recorded previously from a nearby city (Kazerun) 15 km to Parishan Lake by (Hashemi 1976). We collected many other Acrididae species from this location; none of them were infested with E. parishanensis, but some had E. sorbasiensis Mayoral and Barranco, 2004 instead, which seems to be a species with a wide distribution range from Europe to Iran and the co-occurrence of this species with other parasitengone species in many habitats has been reported (Haitlinger 2015). Many studies and the description of Eutrombidium in general so far have not focused on the hosts, and the main focus was on the ectoparasite alone. Providing more information about the host range, attachment sites, and habitats may help us in the future to better understand prevalence of mites and their host range.

Acknowledgements

The authors would like to express their gratefulness to Prof. Alireza Saboori, University of Tehran and Dr. Mohammad Mehrabadi and Dr. Hamidreza Khadem-Safdarkhani, Tarbiat Modares University, for their generous help and for providing lab equipment. We wish to thank Dr. Mohsen Kiany for his valuable cooperation during the surveys. Thanks to Josip Skejo and Slobodan Ivkovic for help with grasshopper identification. The research was supported by the University of Tehran, which is greatly appreciated.

Disclosure statement

No potential conflict of interest was reported by the authors.

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