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Article

Itching for an Answer: Gall-Forming Biological Control Agent Contains an Itch Mite Species Found at Localities Known for Periodic ‘Bite Outbreaks’

by
Ruan Veldtman
1,2,*,
Eddie Ueckermann
3 and
Kayla Liebenberg
4
1
Kirstenbosch Research Centre, South African National Biodiversity Institute, Private Bag X7, Claremont 7735, South Africa
2
Department of Conservation Ecology and Entomology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
3
Unit for Environmental Sciences and Management, Potchefstroom Campus, North-West University, Private X6001, Potchefstroom 2520, South Africa
4
Department of Botany and Zoology, Stellenbosch University, Private Bag X1, Matieland 7602, South Africa
*
Author to whom correspondence should be addressed.
Diversity 2023, 15(1), 73; https://doi.org/10.3390/d15010073
Submission received: 14 November 2022 / Revised: 30 December 2022 / Accepted: 5 January 2023 / Published: 6 January 2023
(This article belongs to the Special Issue Diversity in 2022)
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Abstract

:
Biological control is an attractive option for controlling invasive plant species that are difficult to manage otherwise. However, the release of a non-native species as a biological control agent carries risks. The most obvious risk relates to impacts on plant species other than the plant species targeted for control. There are, however, also other risks. We report on a potential unintended impact of Dasineura dielsi, a gall-forming biological control agent that was released against Acacia cyclops in South Africa in 2003. We confirmed that the galls formed by D. dielsi on A. cyclops harbor mites in the genus Pyemotes (P. cf. ventricosus) within their gall structures, which are parasites of various insect species, but are also known to cause dermatitis in humans. Sporadic biting incidences have been reported in at least two locations in South Africa. The implications are that manual clearing of A. cyclops may expose humans to itch mites and to risks of bites. Gall-forming insects and fungi are known to create niches for herbivores and other gall-associated fauna. Although every possible food web interaction cannot be predicted, enough evidence exists to require that agent screening to include non-target risks other than those pertaining to non-host plants. Testing only whether agents are compromised by interactions with non-target plant species is not sufficient during agent evaluation. If such associations are known from the native range and therefore can form in the introduced range, then any known risk to health and socio-economic activities should be disclosed. We argue for the general development of objective assessment of such risks compared with the benefits potentially accruing from successful biological control of the target plant.

1. Introduction

Classical biological control involves the deliberate introduction and release of exotic yet host-specific agents (e.g., insects, mites, pathogens, etc.) on targeted invasive species, which have the potential to provide long-term control [1,2]. While some agents or “natural enemies” target the vegetative structures of invasive alien weeds, others reduce fecundity by attacking reproductive structures [1,3,4].
Initially, ecological concerns of introducing weed biological control agents (i.e., herbivores) focused on direct non-target effects [5,6,7,8], but more recent studies suggest that unintended impacts can extend far beyond the primary host–control agent interaction [9,10]. Indirect non-target impacts can include direct [11], and apparent competition [12]. Through such indirect effects, even the introduction of highly host-specific biological control agents can have ramifications for recipient native ecosystems [12,13].
Weed biological control agents that are gall-formers are considered low risk because they are usually host species-specific, and therefore unlikely to attack non-target hosts [1]. One group in particular, the seed biological control of invasive Australian Acacia (wattles) is a lauded example of success which has been a major focus in invasive alien management in terms of effort and funding [3,14,15]. However, gall formers change the architecture of the plant, and can create resources that are then available for invertebrates that are inquilines [16,17], and so can be considered to act as ecosystem engineers [18,19,20]. Gall-producing weed biological control agents can thus create a novel resource for indigenous invertebrates feeding on gall tissue [9]. Another drawback is that when the weed is abundant and the agent is not able to reduce it, the galling biological control agents can become superabundant and have great potential to subsidize food webs with additional resources for parasitoids or predators of native insect herbivores [12,21,22,23].
Australian Acacias are invasive species that have severe transformative impacts in many parts of the world [24]. These species have a long-lived seedbank that makes mechanical control efforts difficult [25,26]. In South Africa, several biological control agents have been introduced to reduce seed output without damaging non-reproductive parts of the target plant, with the aim of limiting spread without compromising cultivation of beneficial species [27]. In the case of Acacia cyclops (rooikrans) in South Africa, the release in 1994 of the seed-attacking weevil Melanterius servulus Pascoe (Coleoptera: Curculionidae) achieved sparse establishment and limited seed reduction potential due to short-distance dispersal [4,28]. The release of the mobile flower-galling midge Dasineura dielsi Rübsaamen (Diptera: Cecidomyiidae) (Figure 1) in 2003 resulted in widespread establishment and dramatic seed reduction by inducing abnormal ovarian growths (i.e., “galls”) in the florets via oviposition [28,29]. Biological control of A. cyclops is currently regarded as successful and a good example of ideal control [14] although the ecological evidence for such control has been questioned for three other Acacias under similar biological control [26,30].
There are reports of people living in small coastal towns plagued by itch bite outbreaks which are situated close to A. cyclops-dominated plant communities where D. dielsi galls are found [32,33]. In a monthly report of the Fransmanshoek Conservancy (southern coast of the Western Cape Province of South Africa), it was reported that first D. dielsi was suspected of being responsible for these bites and later its associated parasitoid wasp species, due to the abundance of galls in the landscape and bites occurring when people interact with A. cyclops trees [32]. This explanation was initially ruled out by Prof. Henk Geertsema who suggested that house mites from another source are probably responsible for the itching bites. Subsequently, gall material near the offices of the Fransmanshoek Conservancy was collected by Kei Heyns on 3 April 2019 from the same vicinity of the 2017 bite outbreak and sent to one of the authors (RV) from which six species of mites were extracted by M. Vermaak. This indicated that mites are indeed occupying the galls formed by D. dielsi in this coastal locality. Another community in Shelley Point (west coast of the Western Cape Province) reported in a newsletter that itch mites were thought to be responsible for biting people from some ‘certain vegetation’ [33]. However, both communities live in an A. cyclops-infested habitat currently under biological control by D. dielsi. A review of the biological control literature revealed that Impson et al. [31] described the presence of itch mites of the genus Pyemotes from galls formed by D. dielsi. Their anecdotal observations indicated that these mites are predators of the gall midge but that periodic “outbreaks” of these mites were not consistent and that D. dielsi populations would not be negatively affected. Similar published studies have documented mites living in Dasineura strobila galls on Leptospermum laevigatum also found invading terrestrial ecosystems near the coast [34,35]. Mite outbreaks associated with gall-forming biological control agents are thus not uncommon and have been linked to warmer, more humid weather conditions [35,36].
In this study we aimed to describe the mite species associated with D. dielsi galls from localities with A. cyclops-dominated vegetation. We were also specifically interested to identify mite species capable of biting humans, in the galls of D. dielsi. We aimed to sample across the distribution of A. cyclops, focusing on areas where ‘bite’ outbreaks have been reported.

2. Materials and Methods

Study Sites

For our study, we targeted two areas that are known for periodic itch bite outbreaks, namely Fransmanshoek Conservancy and Shelley Point [32,33]. Sampling was undertaken at the following sites: Shelley Point (SP) (SP1, 32°43′01″ S, 17°58′09″ E; SP2, 32°43′04″ S, 17°58′27″ E; SP3, 32°42′52″ S, 17°58′41″ E); Fransmanshoek Conservancy (FC) (FC1, 34°17′45″ S, 18°27′28″ E; FC2, 34°17′56″ S, 21°55′09″ E; FC3, 34°17′45″ S, 21°54′55″ E); and one random locality where A. cyclops and D. dielsi galls were abundant, namely the Melkbosstrand Conservation Area (MKB1, 33°42′31″ S, 18°27′07″ E; MKB2, 33°42′39″ S, 18°26′54″ E; MKB3, 34°18′01″ S, 21°54′57″ E).
Between 24 April and 19 May 2021, each study site was assigned a one- or two-day sampling effort (i.e., SP: 24 April; FC: 1–2 May; MKB: 19 May) to sample 15 trees per site, which led to a combined total of 45 mature A. cyclops trees with flowers and galls being sampled. We selected trees that were at least 2 m tall, had a basal stem diameter of at least 9 cm, and had at least 100 galls [28]. Subsequently from the 15 trees per site, 5 galls were selected. From these 5 galls, the presence of mites and their identity were determined. Therefore, a total of 225 galls per site can yield any number of mites and other insects.
Our sampling coincided with the mid-summer/early autumn peak in A. cyclops flowering phenology [28]; the attainment of maximum gall densities on host plants between March and June [28]; and the time period in which reports of “bites” increase at Fransmanshoek Conservancy (February–April) and Shelley Point (February–March) [32,33]. Each study site consisted of three pre-selected sample points 500 m apart to ensure independence [19,37]. The total number of trees per sample point were then estimated and five trees (at least 25 m apart) were randomly selected to be visually inspected for galls over a period of 10 min [28]. These selected trees also had their tree height and gall loads (i.e., both mature and senescent loads) estimated, their GPS co-ordinates and elevation values recorded using a handheld GPS, and their basal stem diameter measured [19,28].
Sterilized pruning shears were used to cut five golden-yellow mature gall clusters (diameter: >15–25 mm; branch segment: 5 cm below gall cluster) from the branches of each tree [9]. Due to the unpredictability of pupae emerging as adults, collected gall clusters were immediately stored in separate rearing cages sterilized with 70% ethanol [38]. Five cuttings from each tree were placed into a cylindrical 1 L container with green oasis foam at the bottom to stabilize the cuttings; and covered with fine, ventilated mesh cloth (dimensions: 30 × 22 cm) fixed with an elastic band to allow ventilation but trapping emerging invertebrates [39].
A shake-and-wash mite extraction technique described by Pratt et al. [40] was also used to evaluate mite diversity in the field. Each location was divided into three sample points that were 500 m apart to ensure independent sampling and then 5 trees (at least 25 m apart) were randomly selected per sample point [19,37]. For each study point at a particular location, 5 galls with ostioles (openings on the gall tube) were trimmed and placed into a 350 mL container filled with 100 mL of 70% ethanol. These containers were fastened with air-tight lids before being manually shaken for 30 s, left to settle for one minute, and then shaken again for another 30 s [40]. Preserved mites that consequently settled at the bottom of the container were then processed in the laboratory by KL using a binocular stereoscope 40X magnification (described below) [40,41]. All extracted mites were then placed into morphospecies-specific Eppendorfs filled with 5 mL of 70% ethanol and were identified by EU. All oribatid mites were lodged at the National Museum of Bloemfontein for identification by Dr. Lizel Coetzee Hugo.
In the laboratory, the galls (n = 15 per study site) used in the ethanol wash were stored in a fridge and later dissected using a sterilized scalpel [28]. This provided insight into the insect diversity hosted within the galls in addition to the prevalence of mites within these galls [12,28]. It was confirmed that both midge larvae and mites were recovered from the hollow chambers of the galls.
The permanent mounting of mites onto microscope slides was performed using PVA following the methods described by Ueckermann and Grout [42]. Mounted mite specimens were dried in an oven at 45–50 °C for 24 h and examined under a Zeiss Axioskop TM Research microscope [43]. In addition, RV provided slides of mites mounted with Hoyer’s solution [44] that were retrieved from an ethanol wash conducted at Fransmanshoek Conservancy during April 2019 (the period in which “itch” bites spiked [32]). The slides were compared with the recently collected mite specimens. It was confirmed that several of the same mite species were recovered, including Pyemotes cf. ventricosus.

3. Results

Across the 45 Acacia cyclops trees sampled from the three study sites, a total of 460 mite specimens comprising of 18 morphospecies were recovered from 594 gall clusters (i.e., 45 galls washed in ethanol + 549 galls used for rearing). From this, Pyemotes cf. ventricosus specimens were retrieved (Figure 2), while three new mite species were identified and several other mite species were recovered (see Table 1). In addition, gall dissections confirmed these mites to be present inside the individual galls of a cluster based on the cohort of galls that were dissected.
We found mites of several species across the three sites we sampled per locality which indicates both rare and abundant taxa (Table 2). There were 1 to 7 species of mite found at a locality and the rearing boxes yielded more mites that the ethanol wash method.

4. Discussion

Here we show that D. dielsi galls harbor a diverse mite community associated with the galls, including three species new to science and one species of Pyemotes (confirming the anecdotal observation of Impson et al. [31]). Worldwide there are about 20 species of Pyemotes described [54] with this genus being split into the scolyti and ventricosus, some species in the latter are known to have venom [55]. However, species identification resulted in this species being classified as Pyemotes cf. ventricosus or the straw itch mite (a full species identification cannot yet be made due to the absence of male mites required for morphological species identification). Pyemotes mites are very small (85–325 microns) with males being smaller than females. All offspring are born as sexually mature adults, of which 95–99% are females [54]. This may explain why males were rare in our study.
Species of the genus Pyemotes are known globally to be responsible for incidental bites on humans, which can cause severe allergic reactions which in extreme cases lead to hospitalization [45,56,57]. Broce et al. [45] actually discovered that a human itch bite outbreak was caused by Pyemotes herfsi, feeding of the oak galler Contarinia sp. in North America. These mites, which feed on midge larvae by injecting them with an immobilizing neurotoxin paralyses the larvae and allows the mite to feed on the static larvae. This same toxin can induce lesions in humans consisting of an urticarial papule capped with a very small vesicle [45,56]. These authors carefully searched a range of habitats with several sampling methods, however, the leaf roll galls caused by gall midge which larvae created prey and habitat for P. herfsi. The genus Pyemotes has the characteristic of searching for hosts that are found in protected habitats such as inflorescences, beetle galleries and galls. It was Impson et al.’s [31] observation that the galls of D. dielsi create an ideal habitat for Pyemotes mites which also undergo periodic “outbreaks” during preliminary monitoring (reported as unpublished data).
This species can thus incidentally fall on humans passing through or working within A. cyclops populations. Itch bite outbreaks can be exacerbated when mites are dispersed by wind into human dwellings as reported by Shelley Point residents whose houses are surrounded by A. cyclops trees [33]. Pyemotes herfsi was documented as ballooning into houses from galled oak trees by Broce et al. [45]. The two reports of outbreaks are difficult to track, because “itch bite” incidents are more prominent during certain months, at specific locations, and “itch bite” symptoms can vary in severity based on the individual’s allergic reaction to the injected neurotoxin [45]. Furthermore, there is the challenge of finding non-gravid female mites biting humans because the painless process of being bitten masks the 16 h window to observe bites manifesting, and the temporal irregularity of these outbreaks [45]. Pyemotes mites are commonly referred to as itch mites because their tendency to ‘bite’ with stylet mouthparts [57,58] are considered worse than vertebrate parasitic mites which have pinching mouth parts which they use to access a blood meal [59,60,61]. It was also interesting to find P. cf. ventricosus within the Fransmanshoek Conservancy gall samples from 2019, the same “itch bite” outbreak locality reported by Blignaut et al. [32]. Although we have no direct evidence that P. cf. ventricosus is responsible for the “itch bite” outbreaks experienced by residents in these localities (i.e., sampled from the skin of affected persons) (see also Broce et al. [45] which also could not directly link the mites from galls and residents being bitten), the anecdotal reports of shared “itch bite” symptoms [32,33] and the presence of only one Pyemotes mite species in association with A. cyclops previously also described as having periodic outbreaks [31], provides compelling evidence that this species living in the D. dielsi galls is indeed responsible for human bites.
We propose several avenues for future research in this system: (i) to conduct experiments (with necessary ethical clearance) to confirm the suggested link between dermatitis caused by Pyemotes mites experienced by residents in close contact with D. dielsi galls in A. cyclops stands (specifically the two regular outbreak areas); (ii) to investigate whether similar mite communities can be obtained from similar gall structures made by other gall midges used for biological control, e.g., Dasineura rubiformis galls on Acacia mearnsii [62] and Dasineura strobila galls on Leptospermum laevigatum [33,63]; (iii) to determine why “itch bite” outbreaks are more pronounced in certain years (i.e., [32]); and (iv) to identify the factors underlying this spatio-temporal variation in mite richness and abundance to further investigate why these “itch bite” outbreaks are localized events and tend to occur during specific months (February–April at Fransmanshoek Conservancy and February–March at Shelley Point respectively; [32,33]). The authors are also currently investigating the diversity of insects associated with D. dielsi galls on A. cyclops in the same system, which includes a rich fauna of parasitoids and inquilines interacting with the gall (Liebenberg et al. unpublished). In summary, the native fauna associated with D. dielsi and its invasive host is a diverse multi-faceted system which requires more investigations to enhance our understanding of these novel interactions.
What is the significance of finding a harmful species associated with a released gall-forming biocontrol agent, i.e., a genus known to bite humans firmly established as living in the galls of the biological control agent [31]? Firstly, this is another study providing evidence that galls form habitats for a local species and has a potential cost for humans. Seymour and Veldtman [19] found that the false codling moth (Thaumatotibia leucotreta), a major pest of citrus crops, occurs and completes its development in the galls of the agent Uromycladium morrisii (formerly U. tepperanium), the gall-forming agent released on Acacia saligna. When these trees occur next to citrus orchards these galls provide an additional niche and potential source for this pest [19]. Similarly, galls of Trichilogaster acaciaelongifoliae released in 1982 on A. longifolia were found to contain, amongst several other inquilines [9], the litchi moth (Cryptoplebia peltastica) which is a known pest of several tree crops. These associations by species of the same families (e.g., Tortricidae) are also found in the native range [9], and it has been proposed that investigating ecological interactions before release of galling agents can identify potentially problematic non-target associations. Pearson et al. [64] recently developed an assessment framework to identify how deliberate species introductions (such as biological control agents) and eradication actions can affect the receiving communities. They show that by doing a basic ecology interaction web, ‘surprising’ non-target effects can be identified prior to species introductions.
The field of weed biocontrol has gone to great lengths to minimize direct non-target impacts of biocontrol agent release (herbivore agents not interacting with native plants) [65]. However, concerns of indirect non-target risks are not sufficiently considered with very little pre-release investigations (see [23] as a rare example where a native gall community is studied before the release of a gall-forming biological control agent). Galls in particular have been mentioned to increase the chances of indirect non target interactions [19]. In the case of galling biological control agents, low direct non-target impacts may come at the expense of high indirect non-target impacts. More caution should proceed in the selection and use of galling agents, making use of ecological principles [19,64]. At all times, beneficiaries of released agents should be made aware of the potential consequences of such non-target effects and not simply the potential benefits of control. It has been argued that the risk of the invasive plant should be compared with the risk of the release of the biological control agent to improve a risk averse strategy to biological control [66]. However, as we show here for galling agents, the potential associations with non-target species are to a certain extent predictable and any level of study prior to release would be informative on the actual risk posed by release of the agent.

5. Conclusions

We found a species-rich mite community associated with the galls of D. dielsi, released to control A. cyclops which included Pyemotes cf. ventricosus. Impson et al. [31] stated that the rich community of invertebrates associated with the galls of D. dielsi is not surprising given the complex structure and abundance of the gall resource. Biological control prizes the host specificity, ready establishments, rapid spread, and high abundance of their released agents. However, in the case of galling agents such as those in Australian wattle biological control in South Africa (and now also Portugal based on the reported South African success), this transforms plant–insect sterile biomass into a major biomass of plant–insect interaction [67,68], providing the foundation for a multitude of higher trophic interactions. Thus, investigations in the native range of the insect can possibly show that galls are inhabited by Pyemotes mites (itch mites) [9], but seeing as the survival of the agent is the main focus (e.g., [31]), the possible ramifications of this indirect non-target association have not been considered. Consider for a moment that A. cyclops leaves and branches are a desert for mites subject to desiccation and high solar radiation. However, with the addition of D. dielsi, the sterile biomass of A. cyclops is transformed in an ‘oasis’ with convoluted surfaces that provide refuge (and prey) for mites which they can reproduce in. In this first scientific report of Pyemotes cf. ventricosus mites are present in D. dielsi galls at localities where there has been itch bite outbreaks, where residents also referred to “muggie tyd”, translated to midge season. As we show through several correlative results in this study, it is likely that galls on A. cyclops galls elevated the abundance of itch mites in the study area. Even the mere possibility that a released biocontrol agent can provide a habitat for a biting mite is enough to warrant better consideration of potential ecological consequences of biocontrol agent release prior to release [23]. If current ecological theory and case studies indicate that such interactions are likely, why do we first need to document a major impact before the potential ecological consequences of release are better investigated? Indirect non-target interactions require more attention and should not be dismissed just because they potentially complicate agent release.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d15010073/s1.

Author Contributions

Conceptualization and methodology, R.V. and K.L.; investigation, K.L., R.V. and E.U.; formal analysis, K.L.; writing—original draft preparation, R.V. and K.L.; writing—review and editing, E.U.; supervision, R.V.; project administration, R.V. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by The South African Department of Forestry, Fisheries and the Environment (DFFtE), noting that this publication does not necessarily represent the views or opinions of the DFFtE or its employees. The APC was funded by Diversity.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Mite species recovered per tree, site and locality from ethanol wash and rearing experiment are available from Supplementary Materials.

Acknowledgments

We thank Shelley Point Homeowner’s Association (SPHOA) and Fransmanshoek Conservancy for study sites, and to Cape Nature and the City of Cape Town Municipality for permits to sample at the Melkbosstrand Conservation Area. Joshua Bransgrove provided assistance with field work. Thanks are also due to the field rangers at Fransmanshoek Conservancy (Erich Goold, Zandré Durand, and Tristan Dedekind), the Agricultural Research Council (ARC) and by Lizel Coetzee Hugo of the National Museum of Bloemfontein for identifying invertebrate specimens. The mounting of slides from 2017 collections was completed by Mia Vermaak. Matthys Strydom and Antoinette Veldtman are respectively thanked for commenting on an earlier and revised draft of the manuscript. Three anonymous reviewers are also thanked for their constructive criticisms.

Conflicts of Interest

The authors declare no conflict of interest. The funder had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

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Figure 1. (A) Adult Dasineura dielsi (lateral view) on an Acacia cyclops inflorescence. (B) Intact A. cyclops seed pods, which encase black oval-shaped seeds with distinctive red funicles. (C) Gall cluster resulting from D. dielsi oviposition, whereby the ovary wall evaginates from the resultant larvae feeding and this prevents seed production of the inflorescence [31]. Adult midges then emerge from the ostioles (i.e., emergence holes) observed along the gall cluster. ©Kayla Liebenberg.
Figure 1. (A) Adult Dasineura dielsi (lateral view) on an Acacia cyclops inflorescence. (B) Intact A. cyclops seed pods, which encase black oval-shaped seeds with distinctive red funicles. (C) Gall cluster resulting from D. dielsi oviposition, whereby the ovary wall evaginates from the resultant larvae feeding and this prevents seed production of the inflorescence [31]. Adult midges then emerge from the ostioles (i.e., emergence holes) observed along the gall cluster. ©Kayla Liebenberg.
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Figure 2. Number of Pyemotes cf. ventricosus mites counted and sites of sample localities, comparing the ethanol wash and gall rearing method (see Materials and Methods).
Figure 2. Number of Pyemotes cf. ventricosus mites counted and sites of sample localities, comparing the ethanol wash and gall rearing method (see Materials and Methods).
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Table
Table 1. Native mite species extracted from Dasineura dielsi galls collected from Acacia cyclops trees in the Western Cape of South Africa. These mite species were recovered from both rearing cages and the ethanol wash experiment. Feeding guild was assigned based on published literature where possible.
Table 1. Native mite species extracted from Dasineura dielsi galls collected from Acacia cyclops trees in the Western Cape of South Africa. These mite species were recovered from both rearing cages and the ethanol wash experiment. Feeding guild was assigned based on published literature where possible.
Family (/Order)SpeciesFeeding Guild aTotal Abundance
Trombidiformes
PyemotidaePyemotes cf. ventricosusParasitic [45,46]91
TarsonemidaeTarsonemus sp.Fungivorous *47
Tarsonemus waiteiFungivorous [47]4
TydeidaeTydeus grabouwiGeneralist [42]22
Genus indet.unknown15
IolinidaeLourus sp. *Predatory [48]2
Pausia sp. *Predatory [48]19
AdamystidaeAdamystis sp. *Predatory [49]6
TriophtydeidaeTriophtydeus immanisGeneralist [50]15
Sarcoptiformes
AcaridaeTyrophagus fanetzhangorumMycophagous4
WinterschmidtiidaeAcalvolia sp.Mycophagous [50,51]203
CheyletidaeGenus indet.Predatory [50]2
Mesostigmata
PhytoseiidaeTyphlodromus (Anthoseius) sp.Predatory [52]2
Ueckermannseius munsteriensisPredatory [50]4
Family indet.Genus indet.unknown1
OripodidaeDometorina (Siculobata) sicula bMycophagous [53]4
Dometorina (Dometorina) plantivaga cMycophagous, predatory [53]8
CeratozetidaeAntarctozetes sp. dMycophagous, detritophagous, necrophagous [53]2
a Feeding guild of mites were categorized as ‘parasitic’, ‘predatory’ (i.e., prey on other mites), ‘mycophagous’, ‘detritophagous’, ‘necrophagous’, ‘fungivorous’, and ‘generalist’ (i.e., feed on pollen, fungi, and predatory). All oribatei mites were lodged at the National Museum of Bloemfontein and the accession numbers were provided. b NMB4726, NMB4728, NMB4729; c NMB4727, NMB4732, NMB4733; d NMB4730, NMB4731. * Mite species indicated with an asterisk are new to science.
Table
Table 2. Mite community data matrix (sampling sites by species abundance) across feeding guilds and locations situated in the Western Cape, South Africa. Columns labelled, “Sampling sites” indicate total captures per mite species for the ethanol wash experiment. Any additional mite specimens retrieved from the rearing experiments were indicated in brackets. SP—Shelly Point; FC—Fransmanshoek Conservancy; MKB—Melkbosrtrand.
Table 2. Mite community data matrix (sampling sites by species abundance) across feeding guilds and locations situated in the Western Cape, South Africa. Columns labelled, “Sampling sites” indicate total captures per mite species for the ethanol wash experiment. Any additional mite specimens retrieved from the rearing experiments were indicated in brackets. SP—Shelly Point; FC—Fransmanshoek Conservancy; MKB—Melkbosrtrand.
Feeding GuildSampling Sites
SpeciesSP1SP2SP3FC1FC2FC3MKB1MKB2MKB3
Parasitic
Pyemotes cf. ventricosus1(1)051(8)1(3)01(34)0(11)1(17)
Fungivorous
Tarsonemus sp.3013(9)2(2)0(16)0(2)0(4)3
Tarsonemus waitei000000400
Generalists
Triophtydeus immanis0130000(1)0(6)4
Tydeus grabouwi1(1)100(3)70001
Mycophagous
Acalvolia sp.00054(41)35(13)0(36)0(4)0(5)0
Dometorina (Siculobata) sicula0000(1)12000
Tyrophagus fanetzhangorum00000(1)0(3)000(1)
Mycophagous, predatory
Dometorina (Dometorina) plantivaga061000000
Mycophagous, detritophagous, necrophagous
Antarctozetes sp.0000(1)00010
Predatory
Adamystis sp. *0000(3)0(1)0(1)000
Cheyletidae000000100(1)
Lourus sp. *0000(1)00000
Pausia sp. *2160002(4)0(1)1(2)
Typhlodromus (Anthoseius) sp.000000011
Ueckermannseius munsteriensis000130000
Unknown
Tydeidae0(1)000007(5)01
Species richness4(3)454(6)6(5)1(4)5(5)2(5)7(4)
Total abundance7(3)91659(25)49(20)2(55)15(41)2(27)11(21)
All mite species indicated with an asterisk (*) are new to science.
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Veldtman, R.; Ueckermann, E.; Liebenberg, K. Itching for an Answer: Gall-Forming Biological Control Agent Contains an Itch Mite Species Found at Localities Known for Periodic ‘Bite Outbreaks’. Diversity 2023, 15, 73. https://doi.org/10.3390/d15010073

AMA Style

Veldtman R, Ueckermann E, Liebenberg K. Itching for an Answer: Gall-Forming Biological Control Agent Contains an Itch Mite Species Found at Localities Known for Periodic ‘Bite Outbreaks’. Diversity. 2023; 15(1):73. https://doi.org/10.3390/d15010073

Chicago/Turabian Style

Veldtman, Ruan, Eddie Ueckermann, and Kayla Liebenberg. 2023. "Itching for an Answer: Gall-Forming Biological Control Agent Contains an Itch Mite Species Found at Localities Known for Periodic ‘Bite Outbreaks’" Diversity 15, no. 1: 73. https://doi.org/10.3390/d15010073

APA Style

Veldtman, R., Ueckermann, E., & Liebenberg, K. (2023). Itching for an Answer: Gall-Forming Biological Control Agent Contains an Itch Mite Species Found at Localities Known for Periodic ‘Bite Outbreaks’. Diversity, 15(1), 73. https://doi.org/10.3390/d15010073

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