Discovery of the genus Parawenhoekia Paoli (Acari: Chyzeriidae) in the Western Asian area

iscovery of the genus Parawenhoekia Paoli (Acari: Chyzeriidae) in the Western Asian area

Najmeh Kiany

School of Biology and Center of Excellence in Phylogeny of Living Organisms, College of Science, University of Tehran; Iran.

https://orcid.org/0000–0002–9258–2292

Marjan Seiedy

School of Biology and Center of Excellence in Phylogeny of Living Organisms, College of Science, University of Tehran; Iran.

https://orcid.org/0000–0002–7661–9905

Masoud Hakimitabar

Department of Horticulture and Plant Protection, College of Agriculture, Shahrood University of Technology, Shahrood, Iran.

https://orcid.org/0000–0002–0161–7008

Martin Husemann

Staatliches Museum für Naturkunde Karlsruhe, Karlsruhe, Germany.

https://orcid.org/0000–0001–5536–6681

ABSTRACT. We here present the first record of Parawenhoekia aginapaica (Haitlinger, 1999) from Iran, which also represents the first record for the genus of the whole continent (Asia). The specimens were collected in association with an Oedipodinae grasshopper of the genus Aiolopus (Orthoptera: Acrididae). The genus Parawenhoekia Paoli, 1937 has only been known from three Mediterranean countries so far (Italy, Cyprus, and Montenegro) and hence our finding represents a large area extension. This study provides new metric and meristic data and supplements the current knowledge on the species based on new specimens of P. aginapaica collected from Khumeh Zar, Mamasani County, Fars Province, Iran. Photographs of important characteristics are provided. A key to the world species of Parawenhoekia is given.

Keywords: Grasshopper, Fars province, new record, Parasitengona, Pteridopodinae

Citation: Kiany, N., Seiedy, M., Hakimitabar, M. & Husemann, M. (2025) Discovery of the genus Parawenhoekia Paoli (Acari: Chyzeriidae) in the Western Asian area. Journal of Insect Biodiversity and Systematics, 11 (x), xx–xx.

 Mites represent an important and diverse, yet largely understudied group of arachnids. Many families of mites remain relatively unknown. This is also true for the family Chyzeriidae which belongs to the superfamily Trombidioidea sensu Söller et al., 2001 and epifamily Trombelloidae Thor, 1935 associated with other arthropods (Costa et al., 2024). Within the epifamily Chyzeriidae, the subfamily Pteridopodinae is characterized by two pairs of prodorsal trichobothria and a unique cheliceral blade in the active post-larval and larval forms (Mayoral et al., 2018). Parawenhoekia Paoli, 1937 belongs to this subfamily and was described from Italy based only on larva parasitizing the bush cricket, Decticus loudoni Ramme, 1933 (Orthoptera: Tettigoniidae). As a parasite of insects, like other members of Chyzeriidae, Parawenhoekia is a generalist and is not restricted to a specific host (Saboori et al. 2008).

Based on Mayoral et al. (2018) the taxonomic position of Parawenhoekia was considered doubtful due to an incomplete description and missing type species. Hence, it has been moved between five different parasitengone families and was placed in Pteridopodinae (Chyzeriidae) by Mąkol and Wohltmann (2012). Haitlinger (1999) described Napassenia aginapaica (Haitlinger, 1999) from Cyprus as an ectoparasite of an unknown grasshopper host. After re-examining the type specimen, the genus was synonymized with Parawenhoekia by Mayoral et al. (2018). Saboori et al. (2008) described the third species of this genus, Parawenhoekia seadi from Montenegro from the heteropteran Dolycoris baccarum (Linnaeus, 1758) (Hemiptera: Pentatomidae) and an unknown grasshopper host (Orthoptera: Acrididae).

Data on Aiolopus spp. as a host of parasitengona mites is scarce; however, it has been recorded in some papers e.g. three larvae of Cretessenia leoni Haitlinger, 1999 (Chyzeriidae) and Eutrombidium robauxi Southcott, 1993 (Microtrombidiidae) have been collected from Aiolopus strepens (Latreille, 1804) (Haitlinger, 1999; Antonatos & Emmanouel, 2014; Felska et al., 2018), and one larva of Eutrombidium tehranicum Karimi Iravanlou, Kamali & Talebi, 2000; two larvae of Eutrombidium australiense Southcott, 1993, and Eutrombidium trigonum from Aiolopus thalassinus (Fabricius, 1781) (Key, 1994; Karimi Iravanlou et al., 2000; Nayeem & Usmani, 2012). Leptus (Leptus) aeolopae Chinniah & Mohanasundaram, 1998 was found on Aiolopus thalassinus tamulus (Fabricius, 1798) and two larvae of Charletonia kaliksti Haitlinger, 2003 on Aiolopus sp. (Haitlinger, 2003, 2013).

This study is part of a two-year faunistic survey (2020–2021) in the southeastern parts of the Zagros Mountains. Members of Aiolipus in different locations with their parasite mites were collected, including 47 and six larvae of Eutrombidium sorbasiensis Mayoral & Barranco, 2004 on Aiolopus sp. and Aiolopus simulatrix (Walker, 11870), respectively and four larvae of Charletonia baluchestanica Tashakor & Hakimitabar 2015 on Aiolopus sp. Here, we report Parawenhoekia aginapaica collected as an ectoparasite of Aiolopus sp. (Orthoptera: Acrididae) from Khumeh Zar, Mamasani County, Fars Province, Iran on 19 August 2020 by N. Kiany. This is the first record of this genus from Asia. The original description of the species was insufficient in terms of leg chaetotaxy (see Table 2); hence, we here supplement the original description with additional data based on the six specimens collected from Iran to more completely reflect the morphology of the species.                                                       

MATERIAL AND METHODS

As part of a larger study on parasitic mites on Orthoptera, grasshopper hosts were collected in southern Iran (Fars Province) using insect nets (Kiany et al., 2022, 2023, 2024). All grasshoppers were searched for mites. Here, we focus on the mites found hidden under the pronotum of an undetermined Aiolopus species. Mites were detached with an insect pin and preserved in 75% ethanol, then were cleared in Nesbitt's fluid and mounted on glass slides using Faure medium (Dhooria, 2016; Walter & Krantz, 2009). All microscopic images of the specimens were taken using a Canon^® EOS 90D mounted on a Carl Zeiss^® Jena compound microscope and stacked with Zerene Stacker (ver. 1.04). Measurements were recorded using an eyepiece graticule attached to a Carl Zeiss Jena microscope. The terminology and abbreviations of body parts follow Southcott (1986) and Wohltmann et al. (2007). All measurements are given in micrometers (μm).

RESULTS

Taxonomic hierarchy

Class Arachnida Lamarck, 1801

Order Trombidiformes  Reuter, 1909

Family Chyzeriidae Womersley, 1954

Subfamily Pteridopodinae, Southcott, 1987

Genus Parawenhoekia Paoli, 1937

Parawenhoekia aginapaica (Haitlinger, 1999)

Type specimen: Parawenhoekia aginapaica Haitlinger 1999:4, Cyprus, Agi Napa, the Museum of Natural History, Wroclaw University (MNHWU).

Material examined. Six larvae (ZUTC15003a–f) on Aiolopus sp. 1♂, Khumeh Zar, Mamasani County, Fars Province, Iran (29°58'43.92"N, 51°37'41.15"E, 1186 m a.s.l.), 19-VIII-2020.

Habitat. The main natural vegetation in our sampling location include Crataegus azarolus L., Ziziphus sp. Mill. (1754), Prunus sp., Carthamus oxyacantha Bieb., Phragmites australis (Cav.) Trin. ex Steud., Vitex sp. L., Echinops sp. L., Heliotropium europaeum L., Hyoscyamus reticulatus L. There were also corn and paddy fields near the sampling site (Fig. 1). The vegetation provides sufficient humidity for Aiolopus sp. to survive even during intense evaporation through the summer months.

Figure 1. Habitat and collecting site of Parawenhoekia aginapaica (Haitlinger, 1999) in Fars Province, Iran with its vegetation cover.

Distribution. Cyprus, Iran (new country record)

Specimen deposition. The mite specimens (ZUTC15003a–f) and grasshopper host are deposited in the Zoological Museum, Faculty of Biology, University of Tehran, Iran.

Diagnosis (based on original description and new larval materials).

Larva. Cheliceral blades with (18–21) small teeth (Figs 2A & 3D), scutum trapezoidal with nasus (Figs 2B & 3E), coxalae 1b conical, thick, short, with fine barbs and pointed tip; coxalae 2b thick and short, with fine barbs and bifid blunted tip (Figs. 2C–D, 3A–B); Ge III with 7–11 solenidia, Ge I and II each with one solenidia. Dorsal and ventral idiosomal, AL and PL setae with a blunted tip.

Haitlinger (1999) stated the palptarsus has seven setae of which only one seta being smooth. He also mentioned that this part of the prepared slide was badly visible so, errors can be considered, but our specimens showed a palptarsus with 10 setae including seven barbed, and one short nude seta, one nude eupathidium (ζ) and one short solenidion (ω). After comparison of legs specialized setae of the specimen from Cyprus with our specimens it was evident that no famulus setae (ε) were mentioned on Tarsus I in Cyprus specimen in comparison to our specimen which has one; no eupathidium (ζ) on Ta I– III were mentioned but one N seta on each tarsi were referred; solenidia (φ) on tibia I & II (1 vs. 2); solenidia (σ) on Ge I & II (0 vs. 1) and on Ge III (8 vs 7–11). The ranges of metric and meristic data are also given (Table 1 & Table 2).

Re-description (based on the new materials, n = 6).

Scutum. Dorsal scutum trapezoidal with nasus, anterior and posterolateral angles rounded. Anterior and anterolateral margins slightly concave and posterolateral margins slightly convex; Scutum punctated in all parts except in nasus and its base which has fine and scattered punctation (Fig. 2B). Setae AM and SE barbed in distal half. Setae AL and PL barbed and blunt-ended; AL shorter than PL (AL/PL (0.83–0.92)). AM and SE situated between AL and PL; SE longer than AM (SE/AM (2.08–2.81)). Each lateral eye pair on the punctate ocular plate, about 53–60 × 31–36. Eyes circular, anterior 24, posterior 19. Urstigma oval, attached to coxa II, 36–38 × 22–24.

Table 1. Comparison of metric data of Parawenhoekia aginapacia (Haitlinger, 1999) (present study, (ZUTC15003a–f); from Cyprus (g); and Parawenhoekia seadi Saboori, Pesic & Hakimitabar, 2008 (h).

­­­Figure 2. Parawenhoekia aginapaica (Haitlinger, 1999) (larva, Zagros Mountains). A. Gnathosoma (ZUTC15003a); B. Scutum (ZUTC15003e); C. Coxalae 1b and coxalae 2b (ZUTC15003d); D. Coxalae 1b and coxalae 2b (ZUTC15003f); E. Dorsal view (ZUTC15003d); F. Aiolopus sp. (female), dorsal view.

Figure 3. Parawenhoekia aginapaica (Haitlinger, 1999) (larva, Zagros Mountains, ZUTC15003a). A. Coxa– Tarsus I; B. Coxa– Tarsus II; C. Coxa– Tarsus III. D. Gnathosoma, left, dorsal view; right, ventral view;
E. Scutum.

Dorsum (Fig. 2E). Dorsal idiosomal setae arrangement is not distinct due to idiosomal damage in all specimens but seems to be 6, 6, 6, 6, 6 and the ventral and dorsal view could not be separated clearly. Each seta barbed, blunt-ended, and arises from a small circular pointed plate.

Ventral. Ventral idiosomal setae are similar to dorsal ones but slightly smaller and thinner. Two sternalae (3a) between coxae III. Anus oval shaped, a pair of sclerites anal valves present with two setae [there is one seta each on the right and left valve but in one specimen there is only one seta on the left valve (abnormally)].

Coxala 1a tapering; pointed and barbed, coxalae 1b conical, thick, short, with fine barbs and pointed tip; coxalae 2b thick and short, with fine barbs and bifid blunted tip (Figs 2C–D, 3A–3B). Coxala 3b tapering, barbed and pointed. Each leg tarsus with two small lateral claws and a middle falciform empodium.

Legs (Fig. 3A–C). Leg segmentation formula: 7-7-7. Leg setal formula (Based on new materials): Leg I: Ta–1ω, 1ε, 2ζ, 37–41n; Ti– 2φ, 1κ, 8n; Ge– 1σ, 1κ, 4n; TFe– 5n; BFe– 1n; Tr– 1n; Cx– 2n (Fig 3A). Leg II: Ta– 1ω, 1ε, 1ζ, 35–36n; Ti– 2φ, 8n; Ge– 1σ, 1κ, 4n; TFe– 4n; BFe– 2–3n; Tr– 1n; Cx– 1n (Fig 3B). Leg III: Ta– 34–37n; Ti– 1φ, 7n; Ge– 7–11σ, 4n; TFe– 4n; BFe– 2n; Tr– 1n; Cx–1n (Fig 3C). (see Table 2 for species collected from Cyprus).

Table 2. Chaetotaxy of Parawenhoekia aginapacia (Haitlinger, 1999) (present study, (ZUTC15003a–f); from Cyprus (g) and Parawenhoekia seadi Saboori, Pesic & Hakimitabar, 2008 (h)

Gnathosoma (Figs 2A & 3D). Cheliceral blades straight with serrated teeth on the ventral side except in the basal half. Oral setae (or₁) and bs (subcapitular) setae pointed, and barbed. Supracoxal seta (eP) cone-like and 5 long. Palpal setal formula: 0-B-B-BBB₂-7BNωζ. Palpfemur and palpgenu each with one barbed seta. Tibia with three barbed setae. Palptarsus with one solenidion, one eupathidium, seven barbed setae, and one nude seta (Fig. 3D). Palpal tibial claw with two pointed tines, of them one is shorter.

Key to species of Parawenhoekia of the world (larva)

There are no measurements and detailed leg chaetotaxy data for P. dectici. The holotype of P. dectici was not available and we could not check it. Saboori et al. (2020) and Hakimitabar and Saboori (2022) stated metric data and the number of normal and sometimes specialized setae on TFe-Ta are too variable to be used as criteria for taxonomic decisions. The new identification key is prepared to include P. aginapaica

1 ..... Setae AL and PL stout and subequal. .....................  P. seadi Saboori, Pesic & Hakimitabar, 2008

—...... Setae AL and PL setiform and PL longer than AL. ............................................................................ 2

2 ..... Setae SE semi-equal with AM. ......................................................................  P. dectici Paoli, 1937

—...... Setae SE more than twice as long as AM. .................................... P. aginapaica (Haitlinger, 1999)

DISCUSSION

Until now, only three species of Parawenhoekia have been described: P. dectici Paoli, 1937 from Italy on Decticus loudoni Ramme, 1933 (Orthoptera: Tettigoniidae); P. aginapaica (Haitlinger, 1999) from Cyprus on an unidentified Orthoptera and P. seadi Saboori, Pesic & Hakimitabar, 2008 from Montenegro on an unidentified grasshopper (Orthoptera: Acrididae) and Dolycoris barbarum (Linnaeus, 1758) (Heteroptera: Pentatomidae). It seems that the members of the genus are relatively rare, but certainly remain understudied in most regions. The original description of Parawenhoekia aginapacia was incomplete and their drawings were unclear; especially those of the shape of the gnathosoma, the number of setae on palptarsus and leg segments; also type specimen is not in good condition (Mayoral et al., 2018). Our collected specimens are considerably similar to the type, but there are some differences, which could be due to insufficient data caused by describing the species based on one single specimen. The coxalae 2b is bifurcate in all specimens not truncate; however, the viewing angle after slide fixation may have an effect on the final decision (comparing Fig. 2C with Fig. 2D); and our specimens show bifurcate and truncate even on different sides of one specimen. Dorsal and ventral setae are with a blunt tip, there are 7–11 solenidia on genu III with some abnormality. This could be a geographical variation but we could consider the habitat stresses as an influencing factor because there are abnormalities in the number of solenidia in Ge III on different sides of some specimens (Table 2) and also a specimen (ZUTC15003d) had three AL setae which are abnormal. The biometry of leg segments is similar to the original description, except for Ta I (192–209 vs. 166).

This is the first observation of the genus Parawenhoekia outside of the Mediterranean region. However, the host genus Aiolopus has a wide distribution and also occurs in many Mediterranean countries. Hence, the grasshopper host may play an important role in the spread of P. aginapaica outside of the Mediterranean region. Further, the Zagros Mountains have a continental climate somehow similar to the Mediterranean precipitation regime: warm and dry summers and cold and wet winters (Noroozi, 2020). This represents optimal habitat conditions for Aiolopus, whose preferred biotopes include marshlands, edges near streams, lakes, banks of rivers, coastal habitats, ponds, and salt marshes and they feed mainly on grasses around these regions (Beĭ-Bienko & Mischchenko, 1963; Hodjat & Tork, 2014). Saboori et al. (2008) already claimed that Parawenhoekia mites also generally like high relative humidity and live in semi-aquatic habitats. Our observation corresponds to these suggestions as the grasshopper host was found near a paddy field beside a riverbank (Fig. 1). This habitat, hence, may also be considered preferable for P. aginapaica.

Unfortunately, the location where the species was found is under severe damage caused by drought and water withdrawal. During the following year’s sampling, the river was desiccated completely and the host species could not be collected anymore. Future monitoring would be important to clarify the conservation status of the species, which may be a victim of habitat destruction and climate change. Carlson et al. (2017) predicted that habitat loss due to climatic changes could be responsible for 5–10% of parasite species extinction by 2070 and these species might experience redistribution, range contract and extinction. Punčochář (2022) also mentioned the abundance of water mites found in 14 small watercourses in the Czech Republic in 2018 decreased to about half (47%) in comparison to 1964. Generally, more studies and surveys are needed to better understand the ecology, systematics, and distribution of this and other mites, as they represent an essential and diverse taxon, which deserves more attention.

AUTHOR′S CONTRIBUTION

The authors confirm their contribution to the paper as follows: N. Kiany, M. Seiedy and M. Hakimitabar: designed the study; M. Seiedy provided resources, supplies, and lab space and oversaw the research; N. Kiany collected and identified the specimens and also designed them, then prepared a manuscript; M. Seiedy, M. Hakimitabar and M. Husemann re-examined the specimens and revised the manuscript; all authors agreed on the content of the final draft for submission. All authors contributed substantially in all aspects of the research. The authors read and approved the final version of the manuscript.

FUNDING

This work was supported by the University of Tehran.

AVAILABILITY OF DATA AND MATERIAL

The specimens listed in this study are deposited in the Zoological Museum, Faculty of Biology, University of Tehran, Iran, and are available from the curator, upon request.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

This study only included arthropod material, and all required ethical guidelines for the treatment and use of animals were strictly adhered to in accordance with international, national, and institutional regulations. No human participants were involved in any studies conducted by the authors for this article.

CONSENT FOR PUBLICATION

Not applicable.

CONFLICT OF INTERESTS

The authors declare that there is no conflict of interest regarding the publication of this paper.

ACKNOWLEDGMENTS

We are thankful to Dr. Mohsen Kiany for his cooperation during the fieldwork. We also thank Dr. Ahmad Reza Khosravi, Shiraz University for his help in identifying vegetation cover. The research was supported by the University of Tehran, which is greatly appreciated.