Hernández-Corral, Jesús ¹ and Moraza, Maria L. ²

¹✉ CIBIO Research Institute, University of Alicante, 03690 San Vicente del Raspeig, Alicante, Spain.
²Institute of Biodiversity and Environment BIOMA, University of Navarra, Irunlarrea 1, 31008, Pamplona, Spain.

2025 - Volume: 65 Issue: 1 pages: 204-212

Original research

Keywords

Abstract

Introduction

The infraorder Mygalomorphae represents one of the three main lineages into which spiders are divided (Hedin & Bond, 2006). They are also known as "primitive" spiders because they have four book-shaped lungs or phyllotracheae and subchelate chelicerae with independent movements and arranged parallel to the sagittal body plane. The family Macrothelidae Simon, 1892, within this infraorder, is represented in Europe by three species belonging to the genus Macrothele Ausserer, 1871: M. cretica Kulczynski, 1903; M. drolshageni Özkütük, Elverici, Yağmur & Kunt, 2019 and M. calpeiana (Walckenaer, 1805), the latter is the only species with stable populations in the southern half of the Iberian Peninsula.

This species usually achieves a large body size (around 35 mm for females and 27 mm for males) compared to the majority of the spiders on the Iberian Peninsula. It is a species whose females need between four and five years to reach adulthood and can live several years as adult instar (Perry, 2002).

In addition to the specific characteristics to the species, it is worth mentioning that in the center of the dorsal prosomic shield they have a relatively large concave circular depression called fovea. This species builds silken galleries with an external visible part and an underground gallery. Only the males leave definitely their galleries during the mating season.

The dispersive capacity of the species is limited due to the absence of aerial dispersion during the juvenile life stages, since they do not travel through the air hanging from their own silk threads, an action referred to as "ballooning".

Spiders can play host to a variety of mites on the exterior of their bodies, although not all are considered parasitic (Parker & Roberts, 1974). The mites most frequently associated with spiders are phoretic forms, usually deutonymphs (hypopus) of the suborder Astigmata (Welbourn & Young, 1988), as well as deutonymphs and adult Parasitengonina. Ectoparasitic mites, such as the larvae of the order Prostigmata, are less common and some are found to be obligate parasites of mygalomorph spiders in Australia and Indonesia (Domrow, 1975). Mesostigmatid mites of the family Laelapidae have also been described in association with spiders (Oudemans, 1932; Womersley, 1956; Fain, 1989; Baker, 1991; Moraza et al., 2009). The family Laelapidae includes mites with very diverse lifestyles (Casanueva, 1993). There are some species that are free-living predators but live as parasites on vertebrates and invertebrates. Examples of the latter can be found in Mygalomorphae (Fain, 1991a), in the families Liphistiidae (Finnegan, 1933), Idiopidae (Domrow, 1975; Fain, 1991c), Theraphosidae (Oudemans, 1932; Womersley, 1956; Fain, 1989; Moraza et al., 2009), Barychelidae (Fain, 1991b), Nemesiidae (Domrow, 1975; Fain, 1991c), and in Theridiidae (Fain, 1991c).

Except for the presence of the Iberian endemism Androlaelaps pilosus Baker, 1991 on M. calpeiana (Snazell & Allison,1989; Helsdingen & Decae, 1992), no information has been found on mite communities that may be found in the galleries where M. calpeiana lives, in its webs and/or in the remains of its prey and molts. This information, together with the knowledge of the trophic guild to which the components of these communities belong, would facilitate a better understanding of their role within the trophic chain of the invertebrate community and their role in the biology and ecology of the spider.

Currently, M. calpeiana enjoys legal protection due to its inclusion in the Bern Convention and the EU Habitats Directive (Ferrández, 2011). A study recently carried out in several provinces of Andalusia, within the project of the Ministry for the Ecological Transition and the Demographic Challenge (MITECO), File P2.C4.I1.P1.S000.A1:E1, has allowed us to carry out the present work. The object of the study addresses the improvement of knowledge of the conservation status of the species M. calpeiana.

The objectives of this preliminary work are, therefore: 1) to understand the mite communities present in the galleries and webs of the spider M. calpeiana; 2) to understand the trophic guild to which each of the species in this community belongs; 3) to advance in the knowledge of the trophic relationships within the communities of mites associated with M. calpeiana; 4) to provide new information on the mite species Androlaelaps pilosus.

Material and methods

Sampling

This study was carried out from 13 to 19 March 2024 and, due to the limited time available, was restricted to a few locations in the provinces of Jaén (Alcalá la Real, Cambil, Huelma, Jaén, Los Frailes, Los Villares, and Valdepeñas de Jaén) and Córdoba (Carcabuey and Lucena) (Table 1). Coordinates of these locations are not provided as this species is classified as "Vulnerable". All field work was carried out during daylight hours. The mites were collected from galleries of M. calpeiana located mostly under stones and, less often, among roots, hollows of trees or in the ground itself (Figs. 1A-C). The spider webs were collected manually, placed in hermetic bags inside a cork refrigerator with cold blocks inside, thus avoiding light, desiccation, and thermal stress.

Location of galleries and vegetation

Most of the galleries and webs studied were found under stones (Fig. 1B) or in areas with vegetation cover (Fig. 1A). Although webs were also observed in cracks and hollows in the trunks of old olive trees (Fig. 1C), they were not extracted due to the difficulty they presented, except in one case where it was possible (see Table 1). Their webs allowed us to distinguish 2 well-differentiated parts: a hidden gallery — the place where the spider takes refuge most of the time, and a more exposed, non-hidden capture-web, which is attached to nearby rigid parts by means of strong silk tensioners. Sometimes the gallery has continuity within the ground.

Mite identification

The mites located on the prosomic shield of the spiders were removed in the laboratory with a fine paintbrush using a stereo microscope and placed in 70% ethanol. The webs were introduced in hermetic bags, and, in the laboratory, the mites located on them were isolated with the help of a stereo microscope and preserved in 70% ethanol. To identify the mites, they were previously prepared using Nesbitt's solution and then mounted on permanent slides using Hoyer's solution and sealed when completely dry. Labelling of the slides and taxonomic analysis was carried out in the laboratory of the second author, with the aid of optical microscopy and the support of general and specific bibliography. The manual of Acarology has also been consulted to identify mite families (Krantz & Walter, 2009). To identify genera and species: Karg (1971) and Gilyarov (1976) for Mesostigmata mites; Gilyarov (1978) for Prostigmata mites, Perez-Iñigo (1993, 1997) for Oribatid mites; and O'Connor (1982) for Astigmata mites.

The samples are deposited in the collection of the first author (J. Hernández-Corral).

Results and discussion

General results

A total of 87 specimens of mites were identified. Of these, 69% were captured in webs with remains of prey and spider molts, and 31% were found on the spider itself (Table 3). As a result, 19 species (one Astigmata, five Mesostigmata, five Oribatida, and eight Prostigmata) belonging to 15 families have been identified, eight of them at the genus level (Amblyseius sp., Pachylaelaps sp., Pachygnatus sp, Dinothrombium sp., Erythracarus sp., Fessonia sp., Linopodes sp, and hypopus of Sancassania sp.) (Table 2).

Faunistic and taxonomic highlights

The presence of the following nominal species of mites has been found from the gallery/web of M. calpeiana (Table 2): Androlaelaps pilosus Baker, 1991; Bdella muscorum Ewing, 1909; Cyta latirostris cf. (Hermann, 1804); Damaeus flagellifer Michael, 1890; Galumna tarsipennata Oudemans, 1914; Odontoscirus iota cf. Atyeo, 1960; Oribatula tibialis (Nicolet, 1855); Pilogalumna alliferum (Oudemans, 1919); Veigaia decurtata Athias-Henriot, 1961; Zercoseius spathulifer (Leonardi, 1899); Zygoribatula cognata cf. (Oudemans, 1902).

The species A. pilosus was initially cited in Pedregoso, Cádiz (Southern Spain). The author describes this species based on specimens captured and provided by Snazell and Allison, collectors who had already observed its presence on the spider's cephalothorax, specifically within and around the fovea (Fig. 1E). Baker (1991) described the adults of both sexes and immature protonymphal and deutonymphal instars.

This species has now been observed in three municipalities in the province of Jaén (Huelma, Los Frailes and Valdepeñas de Jaén) and one in Córdoba (Lucena) (Table 2). It has also been found in Cádiz (Prado del Rey) (iNaturalist 1), in Málaga near the municipality of Monda (iNaturalist 2), and in the province of Seville near the municipality of El Real de la Jara (Gutiérrez-Biodiversidad Virtual).

The genus Androlaelaps is common in bird and mammal nests and on the bodies of small vertebrates, mostly rodents and has been observed preying on small arthropods, nematodes, and their eggs (Baker, 1991). A. pilosus is not considered a phoretic species, given its presence on the spider of both sexes and on all instars in its lifecycle (except the larva). These facts do not fit the phoretic patterns or dispersal strategy described to date for other mesostigmatid mites (Faris & Axell, 1971; Athias-Binche, 1994; Camerik, 2010; Seeman & Walter, 2023) (Table 3). The phoretic instar is known to be: (a) only adult females (gravid or virgin females), using the chelicerae grasping a seta or folding of the integument in Macrochelidae; (b) n Parasitidae, Sejidae, Digamasellidae, and Halolaelapidae, only deutonymphs (both sexes), hanging on by its ambulacral claws; in Uropodidae only deutonymphs using an anal pedicel.

Curiously, all the specimens studied by us correspond to adult females, with no confirmed presence of males and immatures instars (Fig. 1D). However, we must not forget that the capture of these specimens took place over a period of a week during the month of March, a period during which the species might not be in its reproductive period. The holotype is labelled "coll. R. Snazell, 1985 (BMNH reg. no. 1989.10.11.1)" and the paratype [females, males, and immatures, same data as holotype (BMNH reg. nos. 1989.10.11.2-12)]; this material was collected in late fall.

Another fact worth mentioning is that this species has only been observed on adult or subadult spiders, all having a large, deep fovea (Fig. 1E), but not in other juvenile stages with a smaller fovea.

Discussion

There are certain aspects of the relationship between M. calpeiana and A. pilosus that remain unresolved. The benefit that both arachnids obtain from this association is yet unknown. According to Baker (1991), who rules out phoresy, the mite may be seeking protection by locating itself in the fovea, a safe place to rest and remain isolated from its enemies. As such, Baker considers it to merely be an association which benefits only the mite.

We have observed that the mites were not firmly attached to the fovea nor to other parts of the spider, being relatively easy to separate them with a paintbrush. The foveal area seems to be a safe zone for the mite, since it is difficult for the spider to access it. We have not only observed this species of mite in the fovea, but also wandering around on the back of the prosomic shield, between the prosoma and opisthosoma (Fig. 1E) and on the coxae. In one case, a mite was found on the respiratory stigma. In the case of an ectoparasitic mite, its chelicerae need to pierce the spider's integument and remain firmly attached to the spider's body during food intake. In the case of a phoretic mesostigmatid mite, it is firmly attached to the host using the structures mentioned above. In our opinion, the mite does not seem to be feeding on the spider, so it would need to temporarily abandon the spider to look for food or to feed on spider excretions.

Based on our observations, the relationship between mite and spider may be close and fairly specific. The spider does not seem to feel any physical constraints (no spend more energy to maintain its activity and limit its movement), does not seem to modify its behavior by the mite's presence and it could be that the mite aids in keeping the spider's body and surroundings free of other bothersome parasitic or phoretic mites (see table 3). In all the localities where A. pilosus has appeared on M. calpeiana, no other species of mites has been found on the spider body (Table 2), which would mean the lack of spatial competition with other mites.

We are not aware of any physiological adaptations involved in this relationship, nor what could be the cause of the beginning of this relationship. At least during their association, both species look to share the same habitat, the same need for humidity and temperature. In addition, both avoid exposure to direct sunlight and seek low lighting levels. Assuming that there is no phyletic relationship between the two species, and that the spider activities affect the survival of the mites, we could be talking about an eco-behavioral relationship.

We do not know the level of specificity of this mite for this spider. There is no evidence that A. pilosus has been reported on other species of spiders or arthropods in the living area of M. calpeiana. Until now it is unknown whether it can be found freely outside the spider's body and its web. However, it is logical to assume that, by choosing to live on or in proximity to M. calpeiana, the mite has sufficient food thanks to the presence of other mites and/or small arthropods that live or visit the spider's galleries and webs. In this case, it should temporarily leave the spider's body to hunt (Table 3), as evidenced by the presence of seven individuals of A. pilosus found in galleries and webs (Table 2). Another possible explanation, which would support a degree of specificity, is that it could be that the mite is attracted to this species of spider due to the microenvironment created by the spider itself.

Welbourn & Young (1988) and Domrow (1975) listed a total of five species of obligate parasitic (non-protelean) mites of the genus Ljunghia (Oudemans) of mygalomorph spiders (Liphistiidae, Idiopidae, Nemesiidae and Theraphosidae), in Australia, Indonesia and Malaysia. Moraza et al. (2009) described all instar of another Ljunghia species on a mygalomorph spider in captivity. In all the cases, while all instars were found on the host, their habits are unknown. A. pilosus can now be added to this list.

Few mites have been reported from spiders in general. Welbourn & Young (1988) summarizes 38 records of parasitic mites associated with spiders of at least 18 families. We now report the existence of another species of mites that could be phoretic, ectoparasitic, or simply taking advantage of the remains of the spider's prey and even the fungi that can flourish on them.

Among the species found in the community of mites related to M. calpeiana webs, the most abundant mite has been the phoretic deutonymphs of Sancassania sp. (Astigmata, Acaridae) and non-sexed specimens of Erytracarus sp., Prostigmata of the family Anystidae. The presence of parasites of the prostigmatic cohort Parasitengona, such as members of the family Smarididae (deutonymphs of Fessonia sp.), and the family Trombidiidae, represented by only one specimen of Dinothrombium sp., should be also noted. These two families account for a good number of protelean spider parasites, with records of the genus Trombidium (Fabricius) on European and North American spiders, Allothrombium, larvae and adults on spiders in Canada and Panama (Michener 1946; Moss 1960). Specimens of the predatory Linopodes sp., and the oribatid species collected in this work, live in a wide variety of habits (crop fields, forests, caves, under stones, etc.) and we are not able to directly relate their biology and ecology with the spider, however, members of this community would be a good trophic resource for A. pilosus (Table 3).

In our study, we do not know whether the association M. calpeiana – A. pilosus is permanent or temporary or, if temporary, for how long this association lasts and what biotic and abiotic parameters trigger the association or disassociation. This relationship could be "commensal", with a tendency toward phoresy. In this commensal relationship, the mite benefits by using the adult spider male as a means of transportation. Although the females carry mites, they remain in the same gallery throughout their life, and the juveniles disperse without mites. It is this wandering male moving from one place to another, which helps the mite find new environments or hosts. The spider not does not seem to be harmed or helped by the presence of the mite; it simply seems to carry the mite along without any significant impact

More work is needed to have enough evidence and better understand the specific and unique relationship between these two arachnids and to certify the relationship that exists between this spider and the other members of the mite community described.

Acknowledgements

We would like to thank the Ministry of Ecological Transition and the Demographic Challenge (MITECO) for the permission necessary for the undertaking of this study. We would also thank Miguel A. Ferrández for his participation in the fieldwork. We thank anonymous reviewer, whose comments and annotations improved this work.

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