Plant-mediated competition facilitates a phoretic association between a gall mite and a psyllid vector

Phoretic associations between mites and insects commonly occur in patchy and ephemeral habitats. As plants provide stable habitats for herbivores, herbivorous mites are rarely dependent on other animals for phoretic dispersal. However, a phoretic gall mite, Aceria pallida, which is found on plants, seasonally attaches to a herbivorous insect, Bactericera gobica, for overwintering survival. After detachment, the gall mite shares a habitat with its vector and is likely to compete with this vector for plant resources. However, excessive competition works against the sustainability of the seasonal phoretic association. How the gall mite, as an obligate phoretic mite, balances this relationship with its vector during the growing season to achieve phoresy is unknown. Here, the plant-mediated interspecific interaction between the gall mite and the psyllid after detachment was studied in the laboratory and field. The laboratory results showed that infestation by the gall mite had detrimental effects on the survival and development of psyllid nymphs. Meanwhile, the mite population and the gall size were also adversely affected. The results from the field showed that the mean densities of the mite galls and psyllids were lower in the mixed-species infestation treatment than in the single-species infestation treatment across the investigation period. However, the interspecific interaction between the gall mite and the psyllid decreased rather than accelerated leaf abscission caused by the psyllid, which promoted the persistence of the psyllid population and then indirectly contributed to phoretic association. Our results suggest that the plant-mediated competition between the phoretic gall mite and its vector after detachment facilitates the maintenance of the phoretic association.     

Importance of phoresy in the transmission of Acarina

Dispersal capacity plays a central role in the radiation of animals, facilitating the exploitation of habitats variously distributed in space or in time or both. Many living species are unable to leave a host, crawl around, and find a new host, so they must rely on external factors to be transmitted. Biotical factors may be important in passive transport and the process, by means of which an animal is passively transported by a selected carrier of different species, is known as "phoresy". Phoresy is a phenomenon in which one animal (the phoretic) seeks out and attaches to an animal of another species, with which it does not share any phase of the life cycle, for dispersal, during which time the phoretic animal becomes quiescent, stopping feeding and development. Activity starts again beginning with detachment, induced by stimuli originating from its carrier or the microhabitat. The adaptive traits of phoresy may be categorized as follow: host surface, quiescence, recognition of signals to abandon the carrier and, if needed, synchronization with the host life cycle. Phoresy is exploited by many Arthropods. In Acarina, there are basically four main types of phoresy. First, there is a type in which adult females are the only forms becoming phoretic and attachment is by means of chelicerae, palpal hooks and ambulacral claws, which grasp a seta or a fold of the integument of carrier-host. The second type is represented by mites, in which deutonymphs are phoretic; there is generally no cheliceral or sucker attachment in this group, mites instead hanging on by their ambulacral claws. The third type is similar to the second in that deutonymphs are phoretic; however, in this case, attachment to the host is by means of an anal pedicel formed by a substance, extruded through the anus, which hardens upon coming in contact with air and literally glues the mite to its host. In the fourth type there is a very highly modified deutonymph stage, called hypope, which only occurs at certain times, presumably when environmental conditions are no longer appropriate for the mite. Hypope is simplified morphologically, may have many sucker-like discs or claspers for efficient attachment, and is much more resistant to desiccation than are other stages of the life cycle.     

Review Reflections on the biology, morphology and ecology of the Macrochelidae

The Macrochelidae is a cosmopolitan family of predatory mesostigmatic mites, many of which occupy specialized and often unstable habitats. Most known species have adapted to life in dung deposits where prey is plentiful and the potential exists for rapid population growth. Phoresy on co-occurring flying insects plays a vital role in assuring niche continuity for macrochelids in these ephemeral substrates. A brief general review of some of the earlier highlights of macrochelid research is presented, followed by a discussion of the emergence of phoresy as a major survival strategy in the Macrochelidae associated with dung beetles. Special emphasis is placed on the behavioural and chemical mechanisms that mediate phoretic specificity of macrochelid species in the unique n-dimensional universes of their scarab hosts. Phylogenetic analysis of selected phoretic and non-phoretic macrochelid taxa has shown a strong correlation between phoretic state and evolutionary position, indicatin g that an increasing commitment to phoresy in the Macrochelidae is correlated with an advance from early derivative to terminal taxa. Laboratory and field observations have confirmed the importance of chemical, behavioural and ecological factors in maintaining the integrity of the relationship between phoretically specific macrochelids and their dung beetle hosts. © Rapid Science Ltd. 1998     

Phoresy in animals: review and synthesis of a common but understudied mode of dispersal

Phoresy is a type of interaction in which one species, the phoront, uses another species, the dispersal host, for transportation to new habitats or resources. Despite being a widespread behaviour, little is known about the ecology and evolution of phoresy. Our goal is to provide a comprehensive review of phoretic dispersal in animals and to bring renewed attention to this subject. We surveyed literature published between 1900 and 2020 to understand the extent of known higher-level taxonomic diversity (phyla, classes, and orders) and functional aspects of animals that use phoretic dispersal. Species dispersing phoretically have been observed in at least 13 animal phyla, 25 classes, and 60 orders. The majority of known phoronts are arthropods (Phylum Euarthropoda) in terrestrial habitats, but phoronts also occur in freshwater and marine environments. Marine phoronts may be severely under-represented in the literature due to the relative difficulty of studying these systems. Phoronts are generally small with low mobility and use habitats or resources that are ephemeral and/or widely dispersed. Many phoronts are also parasites. In general, animals that engage in phoresy use a wide variety of morphological and behavioural traits for locating, attaching to, and detaching from dispersal hosts, but the exact mechanisms behind these activities are largely unknown. In addition to diversity, we discuss the evolution of phoresy including the long-standing idea that it can be a precursor to parasitism and other forms of symbioses. Finally, we suggest several areas of future research to improve our understanding of phoresy and its ecological and evolutionary significance.     

Phoretic association of a uropodid mite and a lepidopteran larva

Unidentified uropodid mite deutonymphs have been found in phoretic association with a late‐instar larva of Wiseana cervinata (Lepidoptera: Hepialidae). This is thought to be the first record of phoresy between such mites and a lepidopteran larva. Scanning electron micrographs of the mites and their attachments are presented.     

环境因子对温室白粉虱携播 侧多食跗线螨的影响

侧多食跗线螨Polyphagotarsonemus latus(Banks)能够附着在温室白粉虱Trialeurodes vaporariorum胫跗节上进行远距离扩散,即携播。笼罩试验表明：温室白粉虱对侧多食跗线螨的携播是它们在正常情况下普遍发生的一种现象,18～25℃,50%～75%RH是其发生的最适条件;高温(32～39℃)虽能加速携播,使得1～2 h达到携播高峰,但携播率低,白粉虱不易存活;光照强度对携播率没有显著影响。适温高湿有利于温室白粉虱携带多个跗线螨,随着螨密度的增加,温室白粉虱的携播率和携螨数明显增大。85%携播螨采取翘式附着(呈45°)。显微镜照片清晰显示,携播中侧多食跗线螨的口针插入温室白粉虱足内。     

Phoresy in the field: natural occurrence of Trichogramma egg parasitoids on butterflies and moths

Phoretic insects utilize other animals to disperse to new environments. We recently discovered how egg parasitoids use an exciting phoretic strategy to reach egg-laying sites of their butterfly hosts. In the laboratory, female Trichogramma wasps detect and mount mated female cabbage white butterflies that emit an anti-aphrodisiac pheromone. Hardly any information exists about the natural occurrence of phoresy in wasps of this genus. Therefore, we monitored the presence of phoretic Trichogramma wasps on lepidopteran hosts in the field. Only female wasps were found at low prevalence on six lepidopteran species. Wasps were mostly found on female hosts and mainly on abundant solitary host species. This is the first report of phoretic Trichogramma wasps on butterflies in nature. We suggest that phoresy is only one of several strategies used by these polyphagous egg parasitoids. The evolution of phoresy is discussed in relation to the nutritional ecology of egg parasitoids.     

Review. When to leave the brood chamber? Routes of dispersal in mites associated with burying beetles

Most nests of brood-caring insects are colonized by a rich community of mite species. Since these nests are ephemeral and scattered in space, phoresy is the principal mode of dispersal in mites specializing on insect nests. Often the mites will arrive on the nest-founding insect, reproduce in the nest and their offspring will disperse on the insect's offspring. A literature review shows that mites reproducing in the underground brood chambers of burying beetles use alternative routes for dispersal. For example, the phoretic instars of Poecilochirus spp. (Mesostigmata: Parasitidae) disperse early by attaching to the parent beetles. Outside the brood chamber, the mites switch host at carcasses and pheromone-emitting male beetles, where juvenile and mature burying beetles of several species congregate. Because they preferably switch to beetles that are reproductively active and use all species of burying beetles within their ranges, they have a good chance of arriving in a new brood chamber. Other mite associates of burying beetles (Alliphis necrophilus and Uropodina) disperse from the brood chamber on the beetle offspring. We suggest that these mites forgo the possible time gain of dispersing early on the parent beetles because their mode of attachment precludes host switching. Their phoretic instars, once attached, have to stay on their host and so only dispersing on the beetle offspring guarantees that they are present on reproducing burying beetles of the next season. The mites associated with burying beetles providean example of multiple solutions to one life history problem – how to find a new brood chamber for reproduction. Mites that have mobile phoretic instars disperse on the parent beetles and try to arrive in the next brood chamber by host switching. They are independent of the generation cycle of a single host and several generations of mites per host generation are possible. Mites that are constrained by their mode of attachment disperse on the beetle offspring and wait until their host becomes mature and reproduces. By doing this they synchronize their generation time with the generation time of their host species. Exp Appl Acarol 22: 621–631 © 1998 Kluwer Academic Publishers     

Species traits and environmental characteristics together regulate ant‐associated biodiversity

Host‐associated organisms (e.g., parasites, commensals, and mutualists) may rely on their hosts for only a portion of their life cycle. The life‐history traits and physiology of hosts are well‐known determinants of the biodiversity of their associated organisms. The environmental context may strongly influence this interaction, but the relative roles of host traits and the environment are poorly known for host‐associated communities. We studied the roles of host traits and environmental characteristics affecting ant‐associated mites in semi‐natural constructed grasslands in agricultural landscapes of the Midwest USA. Mites are frequently found in ant nests and also riding on ants in a commensal dispersal relationship known as phoresy. During nonphoretic stages of their development, ant‐associated mites rely on soil or nest resources, which may vary depending on host traits and the environmental context of the colony. We hypothesized that mite diversity is determined by availability of suitable host ant species, soil detrital resources and texture, and habitat disturbance. Results showed that that large‐bodied and widely distributed ant species within grasslands support the most diverse mite assemblages. Mite richness and abundance were predicted by overall ant richness and grassland area, but host traits and environmental predictors varied among ant hosts: mites associated with Aphaenogaster rudis depended on litter depth, while Myrmica americana associates were predicted by host frequency and grassland age. Multivariate ordinations of mite community composition constructed with host ant species as predictors demonstrated host specialization at both the ant species and genus levels, while ordinations with environmental variables showed that ant richness, soil texture, and grassland age also contributed to mite community structure. Our results demonstrate that large‐bodied, locally abundant, and cosmopolitan ant species are especially important regulators of phoretic mite diversity and that their role as hosts is also dependent on the context of the interaction, especially soil resources, texture, site age, and area.     

Occurrence of Poecilochirus austroasiaticus (Acari: Parasitidae) in forensic autopsies and its application on postmortem interval estimation

Despite the fact that mites were used at the dawn of forensic entomology to elucidate the postmortem interval, their use in current cases remains quite low for procedural reasons such as inadequate taxonomic knowledge. A special interest is focused on the phoretic stages of some mite species, because the phoront-host specificity allows us to deduce in many occasions the presence of the carrier (usually Diptera or Coleoptera) although it has not been seen in the sampling performed in situ or in the autopsy room. In this article, we describe two cases where Poecilochirus austroasiaticus Vitzthum (Acari: Parasitidae) was sampled in the autopsy room. In the first case, we could sample the host, Thanatophilus ruficornis (Küster) (Coleoptera: Silphidae), which was still carrying phoretic stages of the mite on the body. That attachment allowed, by observing starvation/feeding periods as a function of the digestive tract filling, the establishment of chronological cycles of phoretic behavior, showing maximum peaks of phoronts during arrival and departure from the corpse and the lowest values in the phase of host feeding. From the sarcosaprophagous fauna, we were able to determine in this case a minimum postmortem interval of 10 days. In the second case, we found no Silphidae at the place where the corpse was found or at the autopsy, but a postmortem interval of 13 days could be established by the high specificity of this interspecific relationship and the departure from the corpse of this family of Coleoptera.     

Phoresy of Trichouropoda shcherbakae Hirschmann, 1972 (Acari: Mesostigmata) on beetles of the genus Tetropium Kirby, 1837 (Coleoptera: Cerambycidae) in Białowieża Forest, Poland

The aim of this study was to assess the phoretic relationship between two beetle species of the genus Tetropium and mites from order Mesostigmata. The study was conducted in the Bia?owie?a Forest, which is recognized as one of Europe’s last natural forest areas. Insects were caught over a period of 8 weeks in 72 attractant traps (type Intercept IPM). In total 1250 specimens of genus Tetropium were collected. We analyzed 524 beetles, including 295 specimens of T. castaneum and 229 specimens of T. fuscum. On 49 beetles (9.4%) there were 785 individuals of Trichouropoda shcherbakae (Trematuridae). Mites were more common on T. fuscum, which carried 82% of all collected deutonymphs. Most of the mites found on beetles were attached to their legs. This study reports on changes in the intensity of phoresy in time and location of mite deutonymphs on their host species.     

Host Selection by the Herbivorous Mite Polyphagotarsonemus latus (Acari: Tarsonemidae)

This study examined the host-selection ability of the broad mite Polyphagotarsonemus latus (Banks) (Acari: Tarsonemidae). To make long-distance-shifts from one host plant patch to another, broad mites largely depend on phoretic association with whiteflies. However, the host plants of whiteflies and broad mites are not necessarily the same. We determined the host-preference and acceptance of free-moving and phoretic broad mites using two behavioral bioassays. We used a choice test to monitor host selection by free-moving mites. In the case of phoretic mites, we compared their rate of detachment from the phoretic vector Bemisia tabaci placed on leaves taken from various host plants. The suitability of the plant was further determined by monitoring mite’s fecundity and its offspring development. We compared the mites’ responses to young and old cucumber (Cucumis sativus cv. ‘Kfir’) leaves (3rd and 8–9th leaf from the apex, respectively), and two tomato (Solanum lycopersicum cvs. ‘M82’ and ‘Moneymaker’). Free-moving mites of all stages and both sexes preferred young cucumber leaves to old cucumber leaves and preferred young cucumber rather than young tomato leaves, demonstrating for the first time that broad mites are able to choose their host actively. As for phoretic mated females, although eventually most of the mites abandoned the phoretic vector, the rate of detachment from the whitefly vector was host dependent and correlated with the mites’ fitness on the particular host. In general, host preference of phoretic female mites resembled that of the free-moving female. Cues used by mites for host selection remain to be explored.     

Potential role of parasitism in the evolution of mutualism in astigmatid mites: Hemisarcoptes cooremani as a model

Phoresy is a symbiotic interaction that results in dispersal, benefiting the relocated organism without negatively impacting the phoretic host. It has long been considered that phoresy among astigmatid mites is somehow an intermediate precursor to the evolution of parasitism within the group. In astigmatid mites, only the heteromorphic deutonymph (hypopode) participates in phoretic dispersal, and the plesiomorphic hypopode may be the key to understanding the dynamics of the evolution of that parasitism. Hypopodes of Hemisarcoptes cooremani (Acari: Acariformes) and their phoretic beetle host Chilocorus cacti (Coleoptera: Coccinellidae) have become the experimental focus for studies concerned with the potential forces that influence the transition of a free-living life style into various coevolved relationships. Previous radiolabeling studies applied to H. cooremani and C. cacti determined that hypopodes of H. cooremani acquired resources from adults of C. cacti while in transit, negating the paradigm that the heteromorphy was purely phoretic. To further probe this relationship, we tested whether materials could be passed from the mites to their hosts. We report here a study using a tritium radiolabel, which indicated that beetles also acquire resources from the hypopodes. These results have implications for understanding the complex relationship between H. cooremani and C. cacti. We propose that this relationship should now correctly be defined as mutualistic (not phoretic) and develop a general model for the potential role of parasitism in the evolution of mutualism among the Astigmata.     

Dynamic associations between <Emphasis Type="Italic">Ips sexdentatus</Emphasis> (Coleoptera: Scolytinae) and its phoretic mites in a <Emphasis Type="Italic">Pinus pinaster</Emphasis> forest in northwest Spain

The relationship between the pine bark beetle Ips sexdentatus and its phoretic mites in a Pinus pinaster forest in northwest Spain was studied during 2014. Four species of mites were collected, three of them from the body of the beetle—Histiostoma ovalis, Dendrolaelaps quadrisetus and Trichouropoda polytricha—the fourth, Cercoleipus coelonotus, was collected from the sediments. The main aims of this study were to explore (1) mite diversity and related parameters, (2) the location on the body of the (male and female) beetle, as well as mite assemblages, and (3) the seasonal dynamic association between mite species and the beetle. Results indicated that the diversity oscillated around 0.71 through the study period and the most dominant, frequent and abundant mite was H. ovalis. Histiostoma ovalis was found attached to almost all parts of the body (mainly on the elytral declivity and ventral thorax), whereas D. quadrisetus was exclusively found under the elytra, and T. polytricha displayed affinity towards the elytral declivity as well as the ventral thorax. None of the mite species displayed any preference for the sex of the beetle and the most frequent mite assemblage was H. ovalis, T. polytricha and D. quadrisetus all together. Maximum abundance of each phoretic mite species was related with each of the flight peaks of the beetle that would indicate that these mite species use phoresy as a primary method of transport for colonizing new food sources.     

Phoretic association betweenMacrocheles muscaedomesticae (Acari: Macrochelidae) and flies inhabiting poultry manure in Peninsular Malaysia

The phoretic association betweenMacrocheles muscaedomesticae and flies that inhabited poultry manure in a poultry farm in Sungai Buloh, Selangor, Malaysia was studied. The effects of temperature, relative humidity and fly abundance on phoretic rates also were in vestigated.The most abundant fly species found wasMusca domestica; Musca sorbens, Chrysomyia megacephala andOphyra chalcogaster were present in relatively large numbers.Representatives of ten families of mites were found on collectedMu. domestica. The most common mite wasMa. muscaedomesticae (Macrochelidae), found on all four species of flies mentioned above. The highest infestation (2.0%) occurred onO. chalcogaster butMu. domestica had the highest average number infested (5.7).The ventral part of the housefly's abdomen was the most common site of mite attachment. Usually only one mite was found attached per fly.The highest phoretic rate recorded was 64.4Ma. muscaedomesticae per 1000Mu. domestica. There was no correlation between phoretic rates andMa. muscaedomesticae abundance, nor was relative humidity a factor. However, a positive correlation was recorded in this host species between phoretic rates and temperature.This paper forms part of the Ph. D. thesis of the author submitted to the Universiti Sains Malaysia, Malaysia, in March 1988.     

Failed predation or transportation? Causes and consequences of phoretic behavior in the pseudoscorpionDinocheirus arizonensis (Pseudoscorpionida: Chernetidae)

The pseudoscorpion Dinocheirus arizonensisinhabits rotting saguaro cactus in the Sonoran Desert and has also been found attached to the legs of the cactophilic neriid fly, Odontoloxozus longicornis.Laboratory experiments demonstrated a higher incidence of phoresy on eclosing versus postteneral adult flies, a female bias in phoresy, and an increased rate in female phoresy through time. The pseudoscorpion may also prey on the fly, but predation rate was unaffected by fly category, pseudoscorpion gender, or food deprivation. A study of pseudoscorpion colonization in the field indicated that females were the first to colonize and the first to abandon the transient habitat of a saguaro rot and, thus, corroborated patterns of phoretic behavior in the laboratory. Taken together, these results establish that phoresy is a behavior functioning specifically for dispersal. The hypothesis that pseudoscorpion transport by other arthropods is accidental, motivated by hunger, and occurs because pseudoscorpions are incapable of consuming their hosts is rejected.     

The associations of phoretic mites (Acarina: Chelicerata) with sand-hoppers (Amphipoda: Crustacea) on the South Wales coast

Mites of the genera Halolaelaps and Phaulodinychus (Gamasida), together with Histiostoma (Acaridida) (Acarina: Chelicerata), occur amongst tidal debris strandlines on the sandy shores of the South Wales coast. Phoretic deuteronymphs of all three mites are dispersed between strandlines via talitrid amphipods (Talitridae: Amphipoda: Crustacea) which provide two principal advantages over the insect hosts used by most other phoretic Acarina. First, amphipods migrate between strandlines throughout the year allowing continual phoretic mite dispersal, and second, even juvenile Talitridae are sufficiently large to transport several mites. The highly aggregated populations of all three mites are distributed independently of amphipod age, sex and species, suggesting that host selection is primarily influenced by other factors. The most likely factors are those related to host behaviour and, in particular, monthly/diurnal quiescence when the mites encounter, and are boarded by, the desiccation-sensitive phoretic mites. The discrete site selection exhibited by each mite species is at least partly influenced by attachment mechanisms.     

Phoretic mites associated with animal and human decomposition

Phoretic mites are likely the most abundant arthropods found on carcases and corpses. They outnumber their scavenger carriers in both number and diversity. Many phoretic mites travel on scavenger insects and are highly specific; they will arrive on a particular species of host and no other. Because of this, they may be useful as trace indicators of their carriers even when their carriers are absent. Phoretic mites can be valuable markers of time. They are usually found in a specialised transitional transport or dispersal stage, often moulting and transforming to adults shortly after arrival on a carcase or corpse. Many are characterised by faster development and generation cycles than their carriers. Humans are normally unaware, but we too carry mites; they are skin mites that are present in our clothes. More than 212 phoretic mite species associated with carcases have been reported in the literature. Among these, mites belonging to the Mesostigmata form the dominant group, represented by 127 species with 25 phoretic mite species belonging to the family Parasitidae and 48 to the Macrochelidae. Most of these mesostigmatids are associated with particular species of flies or carrion beetles, though some are associated with small mammals arriving during the early stages of decomposition. During dry decay, members of the Astigmata are more frequently found; 52 species are phoretic on scavengers, and the majority of these travel on late-arriving scavengers such as hide beetles, skin beetles and moths. Several species of carrion beetles can visit a corpse simultaneously, and each may carry 1–10 species of phoretic mites. An informative diversity of phoretic mites may be found on a decaying carcass at any given time. The composition of the phoretic mite assemblage on a carcass might provide valuable information about the conditions of and time elapsed since death.     

Ectoparasitic and phoretic arthropods of Virginia opossums (Didelphis virginiana) in central Tennessee

Thirteen species of ectoparasitic (12) or phoretic (1) arthropods were collected from 26 adult Virginia opossums, Didelphis virginiana, live-trapped from April through September 1987 in Davidson County, Tennessee. The cat flea Ctenocephalides felis and the American dog tick Dermacentor variabilis were the predominant species with respect to mean intensity and prevalence. The macronyssid mite Ornithonyssus wernecki and the atopomelid mite Didelphilichus serrifer, both specific parasites of this host, showed high intensities but low prevalences. Other fleas collected were Cediopsylla simplex, Ctenophthalmus pseudagyrtes, and Orchopeas howardi. The tick Amblyomma americanum, the myobiid mite Archemyobia inexpectatus, and the trombiculid (chigger) mites Eutrombicula splendens, Leptotrombidium peromysci (first record from this host) and Neotrombicula cavicola (first record from this host), were also recorded. One phoretic species, the glycyphagid mite Marsupialichus brasiliensis, was noted.