Phoretic Mites Research Articles

Metagenomic Approach with the NetoVIR Enrichment Protocol Reveals Virus Diversity within Ethiopian Honey Bees (Apis mellifera simensis).

Metagenomics studies have accelerated the discovery of novel or divergent viruses of the honey bee. However, most of these studies predominantly focused on RNA viruses, and many suffer from the relatively low abundance of viral nucleic acids in the samples (i.e., compared to that of the host). Here, we explored the virome of the Ethiopian honey bee, Apis mellifera simensis, using an unbiased metagenomic approach in which the next-generation sequencing step was preceded by an enrichment protocol for viral particles. Our study revealed five well-known bee viruses and 25 atypical virus species, most of which have never been found in A. mellifera before. The viruses belong to Iflaviridae, Dicistroviridae, Secoviridae, Partitiviridae, Parvoviridae, Potyviridae, and taxonomically unclassified families. Fifteen of these atypical viruses were most likely plant-specific, and the remaining ten were presumed to be insect-specific. Apis mellifera filamentous virus (AmFV) was found in one sampling site out of 10. Two samples contained high read counts of a virus similar to Diatraea saccharales densovirus (DsDNV), which is a virus that causes high mortality in the sugarcane borer. AmFV and the DsDNV-like virus were the only DNA viruses found. Three viruses that primarily infect Drosophila spp. were also discovered: La Jolla virus (LJV), Kilifi virus (KiV), and Thika virus. Our study suggests that phoretic varroa mites are involved in the transmission of LJV and KiV and that both viruses replicate in mites and adult bees. We also found an overwhelming dominance of the deformed wing virus type B variant, which fits well with the apparently harmless infestation by Varroa destructor. It was suggested that Ethiopian bees have developed tolerance against virus infections as the result of natural selection.

Estimates of phoretic mite abundance on bark beetles as affected by beetle capture method: a case study with Mesostigmata mites and Ips typographus (Coleoptera: Curculionidae).

The spectrum of Mesostigmata mite species that are phoretic on the bark beetle Ips typographus has been well described. However, phoretic mite abundance has mostly been quantified by researchers who used only a single method for capturing bark beetles: pheromone traps. We therefore compared mite abundance using two beetle-capture methods. At a single location with high numbers of I. typographus in the eastern Czech Republic in 2013, beetles were collected with pheromone traps and from infested logs placed in emergence traps. In total 29,589 I. typographus beetles were captured using the two methods. Mite abundance was assessed on 2400 beetles from pheromone traps and on 955 beetles from emergence traps; in total 5805 phoretic mesostigmatid mites were detected. Six species of phoretic mites were captured using pheromone traps and four species using emergence traps. The number of phoretic mites per beetle was higher for beetles captured in emergence traps than for beetles captured in pheromone traps. The most abundant mite species overall were Dendrolaelaps quadrisetus, Uroobovella ipidis, and Trichouropoda polytricha. The seasonal dynamics of phoretic mites paralleled the seasonal dynamics of their hosts.

Patterns of Diversity in the Symbiotic Mite Assemblage of the Mountain Pine Beetle, Dendroctonus Ponderosae Hopkins

The mountain pine beetle, Dendroctonus ponderosae (Coleoptera: Scolytinae), is an economically important bark beetle species with a wide geographic range spanning from the southwestern United States into northern Canada. This beetle causes extensive tree mortality to 13 pine species. Mites (Acari) are common and abundant symbionts of mountain beetles that may influence their fitness through positive and negative interactions. We present a unique assessment of the mite associates of mountain pine beetles using measures of alpha and beta diversity. We sampled phoretic mites from five beetle populations: Arizona, Colorado, South Dakota, Utah (USA), and Alberta (Canada) that varied in host tree species, local climate, and beetle population level. We collected 4848 mites from 8 genera and 12 species. Fifty to seventy percent of beetles carried mites in flight with the highest mite loads occurring in middle and southern populations; decreasing in northern populations. Mite assemblages (i.e., both richness and composition) varied along a south to north latitudinal gradient and were driven by species turnover (i.e., species replacement). Differences in mite composition increased with distance between populations. We discuss climatic variation, environmental filtering, and host tree differences as factors that could affect differences in mite composition between beetle populations and discuss implications for functional shifts. Our results could represent a model for estimating diversity patterns of mite symbionts associated with other major insect pests in coniferous forest systems.

Hitchhiking mites

Phoresy is an association between two species in which one transports another. Burying beetles (Nicrophorus spp), also known as carrion beetles, carry mites. There are about 20 phoretic mites on this Nicrophorus beetle, seen in the Great Lakes–St Lawrence forest near Gravenhurst, Canada, and these mites will remain attached until they arrive at the beetle's next carcass. Male Nicrophorus beetles first locate the carcasses of small mammals or birds, and then prepare them by stripping off the fur or feathers. After locating a suitable male and mating, the female lays her eggs inside the prepared carrion. Males and females then bury the carcass in a ~20-cm-deep grave (which will become the beetle's brood chamber) by gradually excavating soil beneath it and covering it with antimicrobial secretions. Burying beetles are unusual in that both males and females take part in raising their young. The American burying beetle (Nicrophorus americanus) historically inhabited 35 states and three Canadian provinces but is now found in only five states and one province. In 1989, the US Fish and Wildlife Service listed it as endangered.

Temperature stress induces mites to help their carrion beetle hosts by eliminating rival blowflies.

Ecological conditions are known to change the expression of mutualisms though the causal agents driving such changes remain poorly understood. Here we show that temperature stress modulates the harm threatened by a common enemy, and thereby induces a phoretic mite to become a protective mutualist. Our experiments focus on the interactions between the burying beetle Nicrophorus vespilloides, an associated mite species Poecilochirus carabi and their common enemy, blowflies, when all three species reproduce on the same small vertebrate carrion. We show that mites compete with beetle larvae for food in the absence of blowflies, and reduce beetle reproductive success. However, when blowflies breed on the carrion too, mites enhance beetle reproductive success by eating blowfly eggs. High densities of mites are especially effective at promoting beetle reproductive success at higher and lower natural ranges in temperature, when blowfly larvae are more potent rivals for the limited resources on the carcass.

Ophiostomatoid fungi associated with mites phoretic on bark beetles in Qinghai, China

Bark beetle galleries are complex ecosystems where many microbes and other arthropods co-exist with the beetles. Fungi isolated from these galleries are often referred to as ‘beetle associates’, but the nature of these associations are poorly understood. The possibility that many of these fungi might in fact be mite associates is often overlooked. Several recent studies explored the diversity of fungi from conifer-infesting bark beetles and their galleries in China, but only one study considered phoretic mites and their fungi from conifer-infesting bark beetles in Yunnan, southwestern China. We studied the mites and fungi from galleries of four spruce-infesting bark beetle species in the high altitude forests of Qinghai province, western China. Mites were identified based on morphological characteristics, and fungi based on DNA sequences of four gene regions. In total, 173 mite individuals were collected belonging to 18 species in 11 genera. A total of 135 fungal isolates were obtained from the mites, representing 14 taxa from the Ophiostomatales. The most frequently isolated fungus was Ophiostoma nitidum, which represented 23.5% of the total isolates. More fungal species were found from fewer mites and bark beetle species than from the study in Yunnan. Although we could not elucidate the exact nature of interactions between mites and their fungi, our results re-enforce that these organisms should not be ignored in pest risk assessments of bark beetles, that often focus only on the beetles and their fungi. Three new species are described: Grosmannia zekuensis, O. manchongi, and O. kunlunense spp. nov., and our data revealed that O. typographi, recently described from China, is a synonym of O. ainoae.

Distribution and New Records of Lymexylidae (Coleoptera: Lymexyloidea) in Guatemala and Mexico

Lymexylidae is a small family of beetles with worldwide distribution. Only two species are recorded from Guatemala and Mexico: Atractocerus brasiliensis Lepeletier and Audinet-Serville and Melittomma brasiliensis (Laporte). New distributional records from Guatemala and Mexico are presented for these species. A distribution map and comments about a phoretic mite interaction are provided.

Phoretic mites on South American bumblebees (Bombus spp.) as parasite carriers: a historical input

Phoretic mites associated with bumblebees are considered commensals that represent little or no risk for their hosts. The aim of the present study was to assess the potential role of the phoretic mites Pneumolaelaps longanalis and Parasitellus fucorum, as carriers of parasites that are known to affect bees. Mites were extracted from bumblebees dating between 1945 and 1981 which belong to museum collections, and from a freshly collected queen. The DNA was extracted and amplified, and the final products were sequenced and analyzed. Parasite’s DNA was found in all samples. Ascosphaera spp., Crithidia bombi, Lotmaria passim, and Nosema ceranae were present in both mite species. Moreover, DNA from Apis mellifera filamentous virus (AmFV), Apicystis bombi, Ascosphaera apis, Nosema apis, and Nosema bombi was found in P. longanalis. This study represents the oldest report of parasite’s DNA in bumblebee phoretic mites, highlighting the relevance of museum samples for historical studies in parasitology.

Genetic variation and heteroplasmy of Varroa destructor inferred from ND4 mtDNA sequences.

Varroa destructor, a parasitic mite of the western honey bee, Apis mellifera L., is a serious threat to colonies and beekeeping worldwide. Population genetics studies of the mite have provided information on two mitochondrial haplotypes infecting honey bee colonies, named K and J (after Korea and Japan, respectively, where they were originally identified). On the American continent, the K haplotype is much more prevalent, with the J haplotype only detected in some areas of Brazil. The aims of the present study were to assess the genetic diversity of V. destructor populations in the major beekeeping region of Argentina and to evaluate the presence of heteroplasmy at the nucleotide level. Phoretic mites were collected from managed A. mellifera colonies in ten localities, and four mitochondrial DNA (mtDNA) regions (COXI, ND4, ND4L, and ND5) were analyzed. Based on cytochrome oxidase subunit I (COXI) sequencing, exclusively the K haplotype of V. destructor was detected. Furthermore, two sub-haplotypes (KArg-N1 and KArg-N2) were identified from a variation in ND4 sequences and the frequency of these sub-haplotypes was found to significantly correlate with geographical latitude. The occurrence of site heteroplasmy was also evident for this gene. Therefore, ND4 appears to be a sensitive marker for detecting genetic variability in mite populations. Site heteroplasmy emerges as a phenomenon that could be relatively frequent in V. destructor.

Factors restraining the population growth of Varroa destructor in Ethiopian honey bees (Apis mellifera simensis).

Worldwide, the ecto-parasitic mite Varroa destructor has been assigned as an important driver of honey bee (Apis mellifera) colony losses. Unlike the subspecies of European origin, the honey bees in some African countries such as Uganda and Ethiopia may not be as threatened or suffer less from mite-infestations. However, only little is known about the factors or traits that enable them to co-exist with the mite without beekeepers’ intervention. Hence, this study was designed to investigate these factors or traits that limit the Varroa mite population in Ethiopian honey bees (Apis mellifera simensis). The study was conducted in the primary honey producing region of Ethiopia, i.e. Tigray. Mite infestation levels were shown to be lower in traditional hives (when compared to framed hives) and when colonies were started up from swarm catching (when compared to colony splitting). However, the influence of the comb cell size on mite infestation was not observed. With respect to the bee biology, the hygienic behavior was shown to be high (pin-test: 92.2% removal in 24 hours) and was negatively correlated with phoretic mite counts (Pearson; r = -0.79; P < 0.01) and mite infestation levels in brood (Pearson; r = -0.46; P < 0.001). Efforts to estimate the Varroa mite reproductive capacity were seriously hampered by an extremely low brood infestation level. From the 133 founder mites found (in 6727 capped brood cells) only 18.80% were capable of producing a reproductive progeny. Failure to produce adult male progeny was unexpectedly high (79.70%). We have suggested a few adaptations to the test protocols allowing to estimate the protective traits of honey bee colonies under very low Varroa pressure. Apart from that, this study demonstrates that the honey bees from Ethiopia are suitable targets to further decipher the genetic predisposition of resistance against V. destructor. It is still unclear to what extent simensis differs from the more common scutellata subspecies.

The nature of the arena surface affects the outcome of host-finding behavior bioassays in Varroa destructor (Anderson & Trueman).

Varroa destructor, an acarian parasite of the Western honey bee Apis mellifera L., is a serious threat to colonies and beekeeping worldwide. The parasite lifecycle occurs in close synchrony with its host development. The females have to discriminate between different developmental stages of the host and trigger an appropriate behavioral response. Many studies have focused on these behavioral aspects, whether it is the choice of a precise host stage or the reproduction of female mites. Behavioral tests often require laboratory settings that are very different from the mite's environment. Our first experiment was designed to study the impact of the surface of test arena on the mite behavior. We found that plastic from Petri dishes commonly used as test arenas disturbs the female mites and can cause death. We searched for a substrate that does not harm mites and found that gelatin-coated plastic Petri dishes responded to these expectations. We then investigated the host choice behavior of phoretic mites confronted with larval stages of the bee on gelatin-coated arenas to watch if the well-documented orientation towards 5th instar larva was observable in our conditions. Pupal stages were included in the host choice experiments, initially to act as neutral stimuli. As white-eyed pupae were revealed attractive to the mite, several pupal stages were then included in a series of host choice bioassays. These additional experiments tend to show that the positive response to the white-eyed pupa stage depends on cues only delivered by living pupae. Further investigation on the nature and impact of these cues are needed as they could shed light on key signals involved in the parasite lifecycle.

Dose-independent virulence in phoretic mites that parasitize burying beetles

Virulence, the negative impact of parasites on their hosts, typically increases with parasite dose. Parasites and hosts often compete for host resources and more parasites will consume more resources. Depending on the mechanism of competition, increasing host resources can benefit the host. Additional resources can also be harmful when the parasites are the main beneficiaries. Then, the parasites will thrive and virulence increases. While parasite dose is often easy to manipulate, it is less trivial to experimentally scale host resources. Here, we study a system with external host resources that can be easily manipulated: Nicrophorus burying beetles reproduce on vertebrate carcasses, with larger carcasses yielding more beetle offspring. Phoretic Poecilochirus mites reproduce alongside the beetles and reduce beetle fitness. The negative effect of mites could be due to competition for the carrion between beetle and mite offspring. We manipulated mite dose and carcass size to better understand the competition between the symbionts. We found that mite dose itself was not a strong predictor of virulence. Instead, the number of mite offspring determined beetle fitness. At larger doses, there was strong competition among adult parental mites as well as mite offspring. While increasing the carcass size increased both host and parasite fitness, it did surprisingly little to alleviate the negative effect that mites had on beetles. Instead, relative virulence was stronger on large carcasses, indicating that the parasites appropriate more of the additional resources. Our results demonstrate an ecological influence on the selection of parasites on their hosts and suggest that virulence can be dose-independent in principle.

Overwintering status and species identification of gall mite in major wolfberry production areas

To identify the wolfberry gall mite species and their overwintering situation in different wolfberry production areas and to provide a scientific basis for their prevention and control. We investigate the phoresy overwintering situation of gall mite, and identify the species of gall mite. Our results showed that the phoretic gall mite was Aceria pallida in all the production areas. The phoresy of gall mite was a common occurrence in different production areas, and the phoresy probability was above 75%. The phoretic behavior of wolfberry gall mite occurred commonly in the other production areas. The control of this mite in different production areas should pay attention to their phoretic behavior.

A scientific note on the effect of oxalic acid on honey bee larvae

The approval of oxalic acid as a treatment for Varroa destructor infestation of honey bee hives gives beekeepers an additional option for controlling this devastating parasite and disease vector, but the effects of oxalic acid on developing bees are not completely understood. In this study, we find that doses of oxalic acid not reported to be toxic to adult bees are toxic to larval bees. While it has been recommended that oxalic acid only be used during broodless periods because it does not penetrate cappings and is only effective in killing phoretic mites, it is tempting to use it at other times of the year because of the dearth of effective treatment options. Knowing whether oxalic acid is toxic to larvae and at what doses is important for beekeepers as they manage their colony population throughout the year.

Phoretic mite communities associated with bark beetles in the maritime and stone pine forests of Setúbal, Portugal.

The phoretic mite communities of prominent bark beetle pests associated with pine stands of southern Portugal were sampled to determine whether they vary across bark beetle species and stand type. Bark beetles were sampled for mites from two primary (aggressive) bark beetle species (Ips sexdentatus and Orthotomicus erosus) and the most common secondary species (Hylurgus ligniperda) in maritime pine (Pinus pinaster) and stone pine (Pinus pinea) in the Setúbal province of Portugal. Twelve mite species, spanning diverse ecological roles, are found associated with these bark beetle systems. The relative abundances of the 12 species that make up the phoretic mite communities of maritime and stone pine varied significantly between host beetle species as well as between stand type, indicating that the phoretic host and dominant tree type are important drivers of mite community composition. The functional roles of these mites are outlined and their ecological significance in pine forest ecosystems is discussed.

Phoretic mites associated to Bombus pauloensis and Bombus bellicosus (Hymenoptera: Apidae) from Uruguay

Bumble bees (Bombus spp.), considered as important angiosperm pollinators, harbor several mite species associated with their nests. In the present study, 403 bumble bees – B. pauloensis (n = 285) and B. bellicosus (n = 118) – were surveyed at five departments from Uruguay: Canelones, Colonia, Montevideo, Florida and Soriano. The mite species Kuzinia spp. Pneumolaelaps longanalis, P. longipilus, Scutacarus acarorum, and Tyrophagus putrescentiae were found associated with both bumble bee species. At least one mite was present on 30% of the bumble bees. We compared the mite prevalence, abundance, intensity and Simpson’s diversity index between bumble bee species and castes. Bumble bee caste was the most influential factor on mite presence, and also on the composition of the phoretic mite community. The assemblages described here could be relevant for future studies focusing on potential threatens for native bumble bees. In combination with a pathogen screening, this data could be proposed as a relevant approach for monitoring native pollinators, especially in areas where they are threatened. The establishment of descriptive indices for threatened and healthy populations would be then of great value for species conservation.

Varroa chemosensory proteins: some are conserved across Arthropoda but others are arachnid specific

The tight synchronization between the life cycle of the obligatory parasitic mite Varroa destructor (Varroa) and its host, the honeybee, is mediated by honeybee chemical stimuli. These stimuli are mainly perceived by a pit organ located on the distal part of the mite's foreleg. In the present study, we searched for Varroa chemosensory molecular components by comparing transcriptomic and proteomic profiles between forelegs from different physiological stages, and rear legs. In general, a comparative transcriptomic analysis showed a clear separation of the expression profiles between the rear legs and the three groups of forelegs (phoretic, reproductive and tray-collected mites). Most of the differentially expressed transcripts and proteins in the mite's foreleg were previously uncharacterized. Using a conserved domain approach, we identified 45 transcripts with known chemosensory domains belonging to seven chemosensory protein families, of which 14 were significantly upregulated in the mite's forelegs when compared to rear legs. These are soluble and membrane bound proteins, including the somewhat ignored receptors of degenerin/epithelial Na+ channels and transient receptor potentials. Phylogenetic clustering and expression profiles of the putative chemosensory proteins suggest their role in chemosensation and shed light on the evolution of these proteins in Chelicerata.

The early-life environment and individual plasticity in life-history traits.

We tested whether the early‐life environment can influence the extent of individual plasticity in a life‐history trait. We asked: can the early‐life environment explain why, in response to the same adult environmental cue, some individuals invest more than others in current reproduction? Moreover, can it additionally explain why investment in current reproduction trades off against survival in some individuals, but is positively correlated with survival in others? We addressed these questions using the burying beetle, which breeds on small carcasses and sometimes carries phoretic mites. These mites breed alongside the beetle, on the same resource, and are a key component of the beetle's early‐life environment. We exposed female beetles to mites twice during their lives: during their development as larvae and again as adults during their first reproductive event. We measured investment in current reproduction by quantifying average larval mass and recorded the female's life span after breeding to quantify survival. We found no effect of either developing or breeding alongside mites on female reproductive investment, nor on her life span, nor did developing alongside mites influence her size. In post hoc analyses, where we considered the effect of mite number (rather than their mere presence/absence) during the female's adult breeding event, we found that females invested more in current reproduction when exposed to greater mite densities during reproduction, but only if they had been exposed to mites during development as well. Otherwise, they invested less in larvae at greater mite densities. Furthermore, females that had developed with mites exhibited a trade‐off between investment in current reproduction and future survival, whereas these traits were positively correlated in females that had developed without mites. The early‐life environment thus generates individual variation in life‐history plasticity. We discuss whether this is because mites influence the resources available to developing young or serve as important environmental cues.

Analysis of the phoretic relationships between mites of the genus Trichouropoda Berlese (Parasitiformes: Uropodina) and the longhorn beetle Plagionotus detritus (Linnaeus) (Coleoptera: Cerambycidae) based on multiannual observations in Białowieża Primeval Forest, Central Europe

ABSTRACTWe studied the phoretic relationships between the mites of the genus Trichouropoda Berlese, 1916 (Uropodina) and the longhorn beetle Plagionotus detritus (Linnaeus, 1758) based on large samples of specimens (2050 beetles and 19,216 mites) collected in the Białowieża Primeval Forest in Central Europe. Phoresy was studied over the years 2014, 2015, and 2016, with the emphasis on multi-annual trends in host–phoront associations, seasonal changes in intensity of phoresy, proportion of carriers of mites in the beetle population, and preferences of phoretic deutonymphs for specific parts of the host’s body. The high repeatability in all the variables we studied indicates high stability of the phoretic relationships, probably resulting from the synchronization of life cycles of beetle dispersants and phoretic mites. The long-term coevolution of phoronts and carriers in a natural forest ecosystem, as well as the expected close association of mites with specific beetle-generated microhabitats in larval galleries, may be important factors affecting the strength of the phoretic relationship.

Risk assessment and predation potential of Stratiolaelaps scimitus (Acari: Laelapidae) to control Varroa destructor (Acari: Varroidae) in honey bees.

The biocontrol of the honey bee ectoparasite Varroa destructor is an underexploited but promising avenue that would benefit from being integrated in a Varroa management program. Our study aimed to investigate the potential of the predatory mite Stratiolaelaps scimitus to control Varroa infestations in honey bees. Tests on safety and predation were carried out to: (1) assess the risk of predation of the honey bee brood by S. scimitus under laboratory conditions and within the colony, and (2) evaluate the predation potential of S. scimitus on phoretic Varroa mites. Under laboratory conditions, S. scimitus was able to feed upon free Varroa mites, but also attacked every unprotected honey bee brood stages with a strong preference for bee eggs. When introduced inside colonies, however, S. scimitus does not have negative effects on the survival of the bee brood. Moreover, observations made in the laboratory revealed that S. scimitus does not attack Varroa mites when they are attached to the body of bees. However, all Varroa mites that had naturally fallen from the bees were predated upon by S. scimitus and died in less than 24h. This study provides evidence that S. scimitus does not represent a significant threat to the bee brood, but also suggests that its effect in Varroa control will probably be limited as it does not attack phoretic Varroa mites. Our results represent a first step in assessing the potential of S. scimitus to control V. destructor and provide novel information about the predator’s behavior inside the honey bee colony.