Frequency-dependent host selection by parasitic mites: a model and a case study

Previous studies on frequency-dependent food selection (changing food preferences in response to changes in relative food abundance) have focused on predators and parasitoids. These organisms utilize several victims during their lifetime. We introduce the case of parasites which, having accepted a host, do not change it. We propose two alternative models to explain the biased occurrence of parasites on different host types: (1) through the option of rejecting less-preferred hosts prior to accepting one of them; (2) by differential parasite survival on different host types. These models predict that host rejection, but not differential survival, can create frequency-dependent parasitism (FDP). Unlike previously described factors responsible for frequency dependence of food selection, which act through changing the foraging behaviour of individual predators or parasitoids, FDP involves no adjustment of parasite foraging strategy according to previous feeding experience. The mite Hemisarcoptes coccophagus is an obligate parasite of armoured scale insects (Homptera: Diaspididae). Our field data show that H. coccophagus is found more frequently on ovipositing than on young host females. Our model, combining the effects of host rejection and differential survival, is used to estimate the relative contribution of these factors to parasite biased occurrence on different hosts. The contribution of differential survival was dominant in H. coccophagus, and overode any effect of host rejection. Nevertheless, our prediction that FDP may be found in parasites is supported by literature data about a parasitic water mite.     

Parasite in peril? A new species of mite in the genus Ophiomegistus Banks (Parasitiformes: Paramegistidae) on an endangered host,the pygmy bluetongue lizard Tiliqua adelaidensis (Peters) (Squamata: Scincidae)

Host‐parasite relationships are generally understudied in wild populations but have a potential to influence host population dynamics and the broader ecosystem, which becomes particularly important when the host is endangered. Herein we describe a new species of parasitic mite from the genus Ophiomegistus (Parasitiformes: Mesostigmata: Paramegistidae) of an endangered South Australian skink; the pygmy bluetongue lizard (Tiliqua adelaidensis). Adult mites were observed on lizard hosts in three different host populations, among which prevalence varied. No temporal trend in prevalence was evident over two spring‐summer seasons of monitoring. We hypothesise that the reliance on burrows as refuges by T. adelaidensis may be essential for the completion of the mite life cycle and also for horizontal transmission. The conservation implications of not only its effect on the host, but also its potential status as an endangered species itself, are considered.     

Predatory — prey relationships in subtropical zooplankton: water mite against cladocerans in an Argentine lake

Summary In a small lake in northern Argentina pelagic water mite Piona sp. had the maximum of population density in January following with a five-day delay after the peak of zooplankton dominant — Daphnia laevis. The mite density was highly predicted by the previous variations of Daphnia density during 4 months of observation (December–March). Daphnia density was a negative delayed function of the predator density but only in December–January when Piona was abundant. During that period Daphnia death rate, d was also correlated with the mite density (r ²=0.80, P<0.005). In laboratory experiments water mites killed 1–7 Daphnia · predator^-1 · hour^-1 in a broad range of prey density. Another zooplankton component, Diaphanosoma birgei, was consumed at the same rates. The mite hardly consumed any copepods. In the pelagium during 24 hours the mite was more associated with Daphnia, than with Diaphanosoma, probably, because of the coincidence in photoreactions with Daphnia. Piona contribution to the death rates of its prey estimated by using the data on functional and numerical responses as well as by means of Edmondson-Paloheimo model, could reach 53% for Daphnia and 40% for Diaphanosoma. A computer experiment on the reconstruction of prey dynamics after subtraction of predator influence showed that the mite could have caused a depression in Daphnia numbers observed in the lake, but the declines in Diaphanosoma population were caused by other factors. After the removal of mite pressure model Daphnia population increased its average density 10-fold. Experiments on Piona feeding revealed a strong effect of interference among predators. This was eliminated by putting one mite per experimental vessel, which led to a 20-fold increase in predation rate. The effect explains the low feeding rates of Piona obtained by the previous authors who ignored the possibility of interference.     

Reproduction of parasitic mites Varroa destructor in original and new honeybee hosts

The ectoparasitic mite, Varroa destructor, shifted host from the eastern honeybee, Apis cerana, to the western honeybee, Apis mellifera. Whereas the original host survives infestations by this parasite, they are lethal to colonies of its new host. Here, we investigated a population of A. cerana naturally infested by the V. destructor Korea haplotype that gave rise to the globally invasive mite lineage. Our aim was to better characterize traits that allow for the survival of the original host to infestations by this particular mite haplotype. A known major trait of resistance is the lack of mite reproduction on worker brood in A. cerana. We show that this trait is neither due to a lack of host attractiveness nor of reproduction initiation by the parasite. However, successful mite reproduction was prevented by abnormal host development. Adult A. cerana workers recognized this state and removed hosts and parasites, which greatly affected the fitness of the parasite. These results confirm and complete previous observations of brood susceptibility to infestation in other honeybee host populations, provide new insights into the coevolution between hosts and parasites in this system, and may contribute to mitigating the large‐scale colony losses of A. mellifera due to V. destructor.     

Host and parasite life history interplay to yield divergent population genetic structures in two ectoparasites living on the same bat species

Host–parasite interactions are ubiquitous in nature. However, how parasite population genetic structure is shaped by the interaction between host and parasite life history remains understudied. Studies comparing multiple parasites infecting a single host can be used to investigate how different parasite life history traits interplay with host behaviour and life history. In this study, we used 10 newly developed microsatellite loci to investigate the genetic structure of a parasitic bat fly (Basilia nana). Its host, the Bechstein's bat (Myotis bechsteinii), has a social system and roosting behaviour that restrict opportunities for parasite transmission. We compared fly genetic structure to that of the host and another parasite, the wing‐mite, Spinturnix bechsteini. We found little spatial or temporal genetic structure in B. nana, suggesting a large, stable population with frequent genetic exchange between fly populations from different bat colonies. This contrasts sharply with the genetic structure of the wing‐mite, which is highly substructured between the same bat colonies as well as temporally unstable. Our results suggest that although host and parasite life history interact to yield similar transmission patterns in both parasite species, the level of gene flow and eventual spatiotemporal genetic stability is differentially affected. This can be explained by the differences in generation time and winter survival between the flies and wing‐mites. Our study thus exemplifies that the population genetic structure of parasites on a single host can vary strongly as a result of how their individual life history characteristics interact with host behaviour and life history traits.     

Ectoparasite‐induced increase in Drosophila host metabolic rate

Parasites exert numerous effects upon their hosts, including physiological and metabolic changes that can in turn influence various aspects of host life history. Using flow‐through respirometry, we investigated how infection intensity of an ectoparasitic mite (Macrocheles subbadius) affects the respiratory rate (CO₂ production) of its host Drosophila nigrospiracula. Mean fly respiratory rate increased with infection intensity with the strongest effect, a 40% increase relative to uninfected controls, occurring with three mites attached. We also verified the causal relationship between elevated respiration rate and mite attachment by examining changes in host respiration before and after mite exposure. We found that the rate of CO₂ production increased by 11% for individual flies following parasite attachment. Fly locomotor activity was not significantly different between infected and uninfected individuals. Metabolic rate of hosts increased as a result of infection in an intensity dependent manner and was not simply due to changes in host activity. These results demonstrate that parasites can have a significant influence on the energy requirements of their host, which may account for the parasite‐mediated loss in host fitness.     

Host-parasite relations betweenAllomyces andRozella

Summary Zoospores of the obligately parasitic chytridRozella allomycis encyst all over the hyphae of a susceptible host, the water-moldAllomyces arbuscula, but many of them fail to penetrate. At the sites of successful penetration lomasomes occur, and the inner layer of the host cell-wall grows and invaginates around a papilla, through the center of which the parasite enters. This host response resembles instances of normal, localized inward growth of fungal cell-walls. The response may also be related to a defense reaction of walled cells which form callosities to block the invasion of fungi.Rozella appears to utilize this response and to depend upon it—probably in order to enter the host cell with minimal disruption. A similar relationship may control the penetration of various obligately parasitic plant-pathogens into their hosts.     

Co-evolution between ectoparasites and their insect hosts: a simulation study of a damselfly–water mite interaction

1. A simulation model investigating the co‐evolution of water mites infesting their aquatic insect hosts during emergence is presented. The model is based on field and experimental studies of the ectoparasitic water mite Arrenurus cuspidator and the damselfly Coenagrion puella. 2. Three scenarios were studied: (1) Only the host was allowed to evolve timing of emergence, while the timing of the parasites' infestation opportunity was held constant. (2) Both host and parasite were allowed to evolve. (3) Only the parasite's timing was allowed to evolve, while the host was constrained completely. 3. In the first two scenarios, parasite abundances decreased in the course of evolution and reached values well below those found in the field, whereas in the third scenario, parasite abundances were maintained at a level close to that found in the field. In the second scenario (co‐evolution), the host seemed to be the leader in the evolutionary race. 4. It is concluded that water mite parasitism is capable of shaping emergence patterns in aquatic insects and, despite the same life‐cycle length for host and parasite, the parasite evolves fast enough to shape its hatching pattern to match the emergence pattern of its host.     

Population growth rate of the parasitic rotifer Proales gigantea,and susceptibility to parasitization in the snail Lymnaea acuminata at different stages of embryonic development

Developing eggs of the host snail Lymnaea acuminata were experimentally parasitized with the parasitic rotifer Proales gigantea to study the population growth rate of the parasite within the snail egg capsule and the susceptibility of the host eggs at different stages of embryonic development. The population growth rate of P. gigantea was 0.46 ± 0.07 individual^–1 day^–1 at the ambient temperature of 18–22 °C. Snail eggs were most susceptible to rotifer attack during the initial stages of development, becoming progressively more resistant after the hippo stage. Yet, regardless of the stage of development, the host embryo was doomed to die without hatching even if one individual rotifer gained entry inside the egg capsule. The presence of P. gigantea within the parasitized egg capsules or in the mucilage had no effect on the developmental rates and hatching success of non-parasitized eggs within the same egg mass.     

Stimuli inducing detachment of larvalArrenurus danbyensis (Hydrachnidia: Arrenuridae) from adultCoquillettidia perturbans (Diptera: Culicidae)

In this study, potential cues for detachment of parasitic larvalArrenurus danbyensis Mullen mites fromCoquillettidia perturbans (Walker) mosquitoes were investigated. Contact with water did not induce a dramatic rate of dissociation. Crushing the host's abdomen was not as effective as crushing the head or thorax; although general body trauma has an effect, it is not sufficient to explain these results. Crushing the host's head following application of a ligature slowed the rate of mite detachment. We infer that haemolymph-borne cues, possibly hormones, are released by crushing the head or thorax of the host and induce rapid mite detachment. External application of Ringers solution or body fluids from mosquitoes significantly increased rate of mite detachment. It is possible that two separate mechanisms stimulate detachment of mites: external haemolymph reception signifying damage to the host and internal reception of haemolymph-borne cues associated with oviposition behavior.     

Two’s company,three’s a crowd: Exploring how host–parasite–microbiota interactions may influence disease susceptibility and conservation of wildlife

A large body of research has demonstrated that host‐associated microbiota—the archaeal, bacterial, fungal and viral communities residing on and inside organisms—are critical to host health (Cho & Blaser, 2012). Although the vast majority of these studies focus on humans or model organisms in laboratory settings (Pascoe, Hauffe, Marchesi, & Perkins, 2017), they nevertheless provide important conceptual evidence that the disruption of host‐associated microbial communities (termed “dysbiosis”) among wild animals may reduce host fitness and survival under natural environmental conditions. Among the myriad of environmental factors capable of inducing dysbiosis among wild animals (Trevelline, Fontaine, Hartup, & Kohl, 2019), parasitic infections represent a potentially potent, yet poorly understood, factor influencing microbial community dynamics and animal health. The study by DeCandia et al. in this issue of Molecular Ecology is a rare example of a host–parasite–microbiota interaction that impacts the health, survival and conservation of a threatened wild animal in its natural habitat. Using culture‐independent techniques, DeCandia et al. found that the presence of an ectoparasitic mite (Otodectes cynotis) in the ear canal of the Santa Catalina Island fox (Urocyon littoralis catalinae) was associated with significantly reduced ear canal microbial diversity, with the opportunistic pathogen Staphylococcus pseudintermedius dominating the community. These findings suggest that parasite‐induced inflammation may contribute to the formation of ceruminous gland tumours in this subspecies of Channel Island fox. As a rare example of a host–parasite–microbiota interaction that may mediate a lethal disease in a population of threatened animals, their study provides an excellent example of how aspects of disease ecology can be integrated into studies of host‐associated microbiota to advance conservation science and practice.     

Bird predation alters infestation of desert lizards by parasitic mites

Theory predicts that predators can reduce parasite abundance on prey by reducing prey density and through disproportionate predation on heavily infested individuals. We experimentally tested this prediction by examining the effects of bird predation on parasitic mite infestation of the prey lizard Acanthodactylus beershebensis. We manipulated predation by adding perches to arid scrubland, allowing avian predators to hunt for lizards in a habitat the birds would not normally use. Host density influenced parasite abundance in hatchlings, but not in older aged individuals and parasite abundance did not affect lizard host survival. Contrary to expectation mite abundance on adult lizards increased under low predation intensities. We explain these results by suggesting a novel hypothesis based on the assumption that the two components of predation, i.e. actual removal of prey and risk, exert contradictory effects on macroparasite abundance.     

Host influence on germination and reproduction of the facultative hemi‐parasitic weed Rhamphicarpa fistulosa

Rice Vampireweed, Rhamphicarpa fistulosa, was a minor parasitic weed until recently when rice cultivation in sub‐Saharan Africa was expanded into marginal wetlands, that are the parasite's natural habitat. Unlike most of the parasitic weeds, R. fistulosa is facultative, meaning that the parasite is able to complete its life cycle without a host. However, when not connected to a host plant, its biomass and seed production is lower. Because very little is known regarding the germination ecology of the parasite, the main objective of our study was to identify the cues that favour germination. We hypothesised that, first, being a wetland species, germination of R. fistulosa is stimulated by light and high soil moisture. Second, we hypothesised that if host plant presence increases its reproductive output then a germination stimulatory effect from host presence is likely to have developed. A Petri‐dish and pot experiment showed that light and completely saturated soils were a requirement for germination, demonstrating that germination requirements of R. fistulosa are typical of species that grow in environments with fluctuating water levels. A pot experiment in which five infestation levels of R. fistulosa were installed in the absence and presence of a rice plant, showed that host plant presence resulted in a 3.7 times higher seed production rate and a 15% larger average seed size. Despite this reproductive advantage, a pot experiment with three rice cultivars, selected because of their difference in strigolactone production, showed that host plant presence, regardless of the development stage, did not influence the emergence rate of R. fistulosa. In a follow‐up study, the germination stimulation effect of root exudates collected from the same three rice cultivars and a treatment consisting of an artificial germination stimulant (GR24) was compared with a treatment consisting of plain water. In these treatments, seeds of R. fistulosa were compared with seeds of the obligate parasite Striga hermonthica. Germination of S. hermonthica was strongly advanced by the presence of root exudates and GR24 but was completely absent in water, whereas germination of R. fistulosa in all treatments was similar to that in plain water. The absence of a host recognition mechanism at the germination stage suggests that the regulation of germination through light and soil moisture is near optimal. Our finding might also indicate that for this facultative parasitic plant species, a more opportunistic germination strategy is superior. Implications of the findings for management of R. fistulosa in rice cultivation are discussed.     

Impact of parasitic mite infection on a terrestrial snail

Summary

Although parasitic infections have been shown to be critical for growth, reproduction and survival of many vertebrates, little is known about the impact of parasites on invertebrate hosts and particular on molluscs. Therefore, it is of interest how parasites may affect their invertebrate hosts and how hosts can manage the detrimental effect of infections. In the present study, the naturally widespread parasitic mite Riccardoella limacum, which has been suggested to play an important role in the ecology of the land snail Arianta arbustorum, was artificially transferred to A. arbustorum. We experimentally examined the effect of the parasite on the food consumption, shell growth, and survival of its host. Surprisingly, we found minor impacts in some traits, i.e. we found that infected and uninfected snails similarly completed their shell growth, attained sexual maturity, and allocated equal energy into their albumen glands. However, infected snails consumed less and showed a significantly higher mortality after winter than uninfected snails.     

Movement of protein and macromolecules between host plants and the parasitic weed Phelipanche aegyptiaca Pers.

Little is known about the translocation of proteins and other macromolecules from a host plant to the parasitic weed Phelipanche spp. Long-distance movement of proteins between host and parasite was explored using transgenic tomato plants expressing green fluorescent protein (GFP) in their companion cells. We further used fluorescent probes of differing molecular weights to trace vascular continuity between the host plant and the parasite. Accumulation of GFP was observed in the central vascular bundle of leaves and in the root phloem of transgenic tomato plants expressing GFP under the regulation of AtSUC2 promoter. When transgenic tomato plants expressing GFP were parasitized with P. aegyptiaca, extensive GFP was translocated from the host phloem to the parasite phloem and accumulated in both Phelipanche tubercles and shoots. No movement of GFP to the parasite was observed when tobacco plants expressing GFP targeted to the ER were parasitized with P. aegyptiaca. Experiments using fluorescent probes of differing molecular weights to trace vascular continuity between the host plant and the parasite demonstrated that Phelipanche absorbs dextrans up to 70 kDa in size from the host and that this movement can be bi-directional. In the present study, we prove for the first time delivery of proteins from host to the parasitic weed P. aegyptiaca via phloem connections, providing information for developing parasite resistance strategies.     

The interplay between host toxins and parasitism by Amoebophrya

The parasitic dinoflagellate Amoebophrya sp. ex Karlodinium veneficum was used to test two hypotheses: (1) infection of cells decreases with increasing host toxicity and (2) parasitism causes the catabolism of host toxin. To test the first hypothesis, host strains differing in toxin content were inoculated with dinospores of Amoebophrya sp. derived from infected cultures of toxic and non-toxic K. veneficum, with resulting infections assessed following 24-h incubations. Contrary to expectations, infection of K. veneficum by Amoebophrya sp. was positively correlated with host toxicity. To examine the second hypothesis, synchronous infection with >80% of cells being parasitized was induced using a toxic strain of K. veneficum, and total toxin concentration (intracellular plus extracellular levels of KmTX1) was followed over the 3-day infection cycle. Toxin content ml⁻¹ increased with growth of K. veneficum in uninfected control cultures, but declined in infected cultures as the parasite completed its life cycle. On a cellular basis, toxin content of infected and uninfected cultures differed little during the experiment, suggesting that the parasite does not actively catabolise host toxin. Rather, infection appears to promote degradation of toxins via death of host cells and subsequent bacterial activity. Results indicate that Amoebophrya sp. ex K. veneficum has greater potential to impact toxic strains relative to non-toxic host strains in natural systems. Thus, Amoebophrya sp. ex. K. veneficum may limit the occurrence of toxic K. veneficum blooms in marine and estuarine environments, while simultaneously functioning as a pathway for dissipation of host toxin.     

Glyphosate inhibits the translocation of green fluorescent protein and sucrose from a transgenic tobacco host to<Emphasis Type="Italic"> Cuscuta campestris</Emphasis> Yunk.

The parasitic plant Cuscuta campestris is dependent on its host for water, assimilates and amino acids. It can be controlled by the herbicide glyphosate, which inhibits 5-enolpyruvylshikimate-3-phosphate synthase (EPSPS), resulting in shikimate accumulation. In this study, C. campestris was parasitic on transgenic tobacco plants expressing green fluorescent protein (GFP) in the phloem. Changes in [¹⁴C]sucrose and GFP accumulation in the parasite were used as indicators of the herbicides effect on translocation between the host and parasite. Host plants were treated with glyphosate 22 days after sowing. Shikimate accumulation in the parasite 1 day after glyphosate treatment (DAGT) confirmed EPSPS inhibition in C. campestris. No damage was visible in the host plants for the first 3 DAGT, while during that same time, a significant reduction in [¹⁴C]sucrose and GFP accumulation was observed in the parasite. Thus, we propose that the parallel reduction in GFP and sucrose accumulation in C. campestris is a result of a glyphosate effect on the parasites ability to withdraw assimilates from the host.Abbreviations CLSM Confocal laser-scanning microscope - DAGT Days after glyphosate treatment - DAS Days after sowing - EPSPS 5-Enolpyruvylshikimate-3-phosphate synthase - GFP Green fluorescent protein     

Effects of maternal parasite load on offspring life-history traits in the common lizard (Lacerta vivipara)

We studied the effect of maternal ectoparasite load (measured at parturition) on the life-history traits of the offspring of the host Lacerta vivipara, the European common lizard. The ectoparasite, a mite belonging to the family Laelapidae, had a detrimental effect on its host: parasite load was associated with increased host mortality, and was negatively correlated with host body mass. Parasite load was persistent over time, suggesting that parasite load can be predictable. Offspring of highly parasitised mothers had higher values of several fitness components early in life than offspring of parasite-free mothers or lightly infested mothers. This was expressed in terms of increased F₁ yearling growth rate, and reproductive investment at first reproduction (measured as F₂ hatchling mass). These results are interpreted as a host adaptation to attenuate the impact of parasites. Indeed, if high parasite loads arise from long exposure time to a constant population of parasites, and if the negative effects of parasites are additive over time, hosts could reduce the impact of parasites simply by investing more during the earlier stages of life. Naturally, having better performance early in life should lead to higher mortality rates and/or lower fecundity later in life.     

DEVELOPMENT OF JANCZEWSKIA MORIMOTOI (CERAMIALES) ON ITS HOST LAURENCIA NIPPONICA (CERAMIALES,RHODOPHYCEAE)1

Janczewskia morimotoi Tokida was successfully cultured from spore to reproductive maturity on its host Laurencia nipponica Yamada. The spore penetrates the host without requirement for wound or abrasion sites, growing between host cortical cells and developing a superficial and an endophytic system simultaneously. During the juvenile period, when the parasite is nonpigmented, it differentiates a cortex and the proliferating endophytic filaments enlarge causing a displacement of layers of host cells into the parasitic tissue. Host cells contacted by cells of the parasite exhibit increased wall thickness, cytoplasmic density and vesicle formation. Pit connections between host and parasite cells were rarely observed whereas penetration of host cell walls was seen commonly. As the parasite increases in size, its cells become pigmented evenly throughout the cortex and host cells show less obvious reactions to the parasite. At this same time, the parasite develops branches and reproductive structures. Host plant segments less than 3 cm long failed to grow when infected with spores of the parasite whereas longer segments were not significantly affected by the parasite. In the absence of the host, the parasite cannot complete its development. Although J. morimotoi is well pigmented at maturity, the absence of pigmentation in the juvenile stage, penetration of host cells, and effect on host growth in culture strongly suggest that it is parasitic during at least its early development.