Mating behaviour of the water mite Arrenurus manubriator (Acari: Arrenuridae)

Water mites of the genus Arrenurus vary in male sexual dimorphism and in sperm transfer behaviour. Although it is a very large genus (≈800 spp.), mating behaviour has been described for only a few species. Here sperm transfer behaviour is described for the first time in a North American species, Arrenurus manubriator. Behaviour patterns can be divided into pre-pairing (readiness posture and cauda presentation), pre-deposition (high vertical jerking, low vertical shaking, striking/stroking and slow lateral waving), spermatophore deposition, sperm translocation, post-deposition (striking/stroking. slow lateral waving, 'tick-rock', shuttling, violent shaking), and separation. Males deposited 8–21 spermatophores in a mating. Pairs remained together for up to 31/2h. Possible adaptive functions of male courtship behaviour are discussed, including the hypothesis that male intromittant organs evolved in Arrenurus to circumvent female choice.     

Experimental evidence for a female sex pheromone in Arrenurus manubriator (Acari: Hydrachnida; Arrenuridae)

We present experimental evidence for a water-borne female-produced sex pheromone in aquatic parasitengonine mites. Water that has contained adult female Arrenurus manubriator Marshall will elicit arrestant behaviour in conspecific adult males, and if the cue is sufficiently strong, the males will assume a readiness posture (with 4th pair of legs held over the back, bent anteromedially at the genuotibial joint) that is typically a precursor to coupling. Water that has not been exposed to female mites does not induce any behavioural response from male mites. Female-conditioned water that has been passed through a C-18 column does not elicit any response from male A. manubriator, while the rehydrated residue from the column does induce arrestant behaviour and may result in the readiness posture. The results from the C-18 extraction indicate that the pheromone is nonpolar in nature. This revised version was published online in July 2006 with corrections to the Cover Date.     

Behavioural studies on eriophyoid mites: an overview

Eriophyoid mites are excellent candidates for ethological research using the approaches of behavioural ecology and sociobiology. These tiny haplodiploid mites are highly specialized plant parasites, producing galls, forming nests, inhabiting refuges or living freely on plants. They reproduce via spermatophores deposited on a substrate and without pairing, which is a fascinating, though still poorly understood, mode of reproduction widespread in some groups of arthropods. Eriophyoid males can be involved in external sperm competition. In some species they also guard pre-emergent females and deposit spermatophores beside them. Although slow-walking, the minute eriophyoid mites can disperse for long distances on air currents or specific animal carriers. After landing on a plant they can distinguish between suitable and unsuitable hosts. Biological observations on a deuterogynous species indicate that parasociality could occur among eriophyoid mites. Many eriophyoids are of economic importance. Knowledge of their behaviour may promote understanding their ecology, may resolve problems in their phylogeny and may help developing methods for their control. In this paper, attention is directed to dispersal modes of eriophyoid mites, their feeding and host acceptance, spermatophore deposition and mating, defence against predators, and social behaviour.     

Pairing and insemination patterns in a giant weta (Deinacrida rugosa: Orthoptera; Anostostomatidae)

Positive size assortative mating can arise if either one or both sexes prefer bigger mates or if the success of larger males in contests for larger females leaves smaller males to mate with smaller females. Moreover, body size could not only influence pairing patterns before copulation but also the covariance between female size and size of ejaculate (number of spermatophores) transferred to a mate. In this field study, we examine the pre-copulatory mate choice, as well as insemination, patterns in the Cook Strait giant weta (Deinacrida rugosa). D. rugosa is a large orthopteran insect that exhibits strong female-biased sexual dimorphism, with females being nearly twice as heavy as males. Contrary to the general expectation of male preference for large females in insects with female-biased size dimorphism, we found only weak support for positive size assortative mating based on size (tibia length). Interestingly, although there was no correlation between male body size and the number of spermatophores transferred, we did find that males pass more spermatophores to lighter females. This pattern of sperm transfer does not appear to be a consequence of those males that mate heavier females being sperm depleted. Instead, males may provide lighter females with more spermatophores perhaps because these females pose less of a sperm competition risk to mates.     

中国雄尾螨二新纪录种记述(蜱螨亚纲,水螨群,雄尾螨科)

记述了采自宁夏和福建的中国雄尾螨科2新纪录种:雄尾螨属Arrenurus Duges,1834的大雪山雄尾螨A.(A.)daisetsuensis Imamura,1951和旗月雄尾螨A.(A.)velifer Lundblad,1969,并对这2个种进行描述和补充绘图。     

Review Canalized pathways of change and constraints in the evolution of reproductive modes of microarthropods

This study investigates how the course of evolutionary change of an organismal pattern is canalized by organismal properties. As an example we use the mechanisms of indirect sperm transfer of some microarthropod groups. Miniaturized droplet spermatophores, characterized by a rather similar pattern of structural and functional components, are shown to have evolved independently in the Acari–Actinotrichida and the Pseudoscorpiones within the Arachnida and in the Entognatha (Collembola and Diplura–Campodeoidea), Symphyla, Pauropoda and Pselaphognatha within the Antennata. At least in the phylogenetic lineages leading to the various antennatan groups, evolution of miniaturized spermatophores took place in a similar sequence of transformation steps. It is likely that – originally – large sac spermatophores with a rigid sheath were deposited on the ground. The subsequent sequence of evolution involved carrying structures, a viscous sheath of the spermatophore-droplets, a stable water balance of the spermatophore under habitat conditions and miniaturized spermatophore droplets with immobilized sperm cells. Finally, mate dissociation became a common mode of behaviour in all groups mentioned. Each of the transformation steps was not only an adaptation to a particular selective condition, but additionally a precondition for further adaptive innovation. In this way the sequence of evolutionary change was rigidly determined. Moreover, integration of subsequently evolved components of the spermatophores into a complex network of interacting components obviously caused constraints of interaction, which in turn have caused a remarkable evolutionary stability of the character patterns. Using water mites as an example, it is shown how in a changed environment few behavioural changes have initiated an evolutionary sequence which has finally led convergently in several lineages to semi-direct or direct sperm transfer and to a massive repatterning of the original reproduction pattern. © Rapid Science Ltd. 1998     

Daily production of spermatophores, sperm number and spermatophore size in two eriophyoid mite species

Under dissociated sperm transfer, (non-pairing) males deposit spermatophores on a substrate, while females seek spermatophores and pick up sperm on their own. Spermatophore expenditures of non-pairing males should be high, due to the increased uncertainty of sperm uptake by a female. In this study I examined spermatophore expenditures in two eriophyoid species that differed in the degree of dissociation between sexes: (1) Aculus fockeui (Nalepa and Trouessart) males rarely visit quiescent female nymphs (QFNs), and mostly deposit spermatophores all over the leaves, whereas (2) Aculops allotrichus (Nalepa) males guard QFNs for many hours and deposit several spermatophores beside them. Males of both species were collected from the field and tested in solitude. Aculus fockeui males deposited on average 19.1 spermatophores per day, whereas A. allotrichus deposited only 3.6 spermatophores per day, and had a very large coefficient of variation. Males and spermatophores of A. allotrichus were significantly smaller and contained less sperm than those of A. fockeui. In both eriophyoids, spermatophore size was fitted to the size of female genitalia and the height of females. The ratio between the diameter of spermatophore head and the width of a female genital coverflap was 0.6, whereas the ratio between the female leg and the length of spermatophore stalk was 0.5. Several factors could be responsible for the discrepancy in spermatophore expenditures between species. Among other factors, the effects of male size, male reproductive strategy and female genitalia size on spermatophore output and size of spermatophores are discussed.     

Immune expression in a damselfly is related to time of season, not to fluctuating asymmetry or host size

1. Variation in immune responsiveness within and among species is the subject of the emerging field of ecological immunology. The work reported here showed that individuals of Lestes forcipatus Rambur differ in their likelihood of mounting immune responses, and in the magnitude of those responses, against a generalist ectoparasite, the water mite Arrenurus planus Marshall. 2. Immune responses took the form of melanotic encapsulation of mite feeding tubes, occurred in the few days after host emergence, and resulted in mites dying without engorging. Such immune responses were more probable and stronger for hosts sampled later rather than earlier in the season. Such responses may act as selection affecting seasonal patterns of egg hatching and larval abundance of mites. 3. Contrary to expectation, metrics of host size (wing length) and wing cell fluctuating asymmetry were not related to the likelihood of immune responses. 4. The importance of season on immune expression of insects has not been explored in detail. These results suggest possible trade‐offs in allocation of melanin (or its precursors) to maturation versus immunity, and indicate the need for studies on the synergistic effects of weather and parasitism on host species that use melanotic encapsulation to combat parasites and pathogens.     

Distributional, morphological and genetic consequences of dispersal for temporary pond water mites

1. To determine the consequences of dispersal and gene flow for temporary pond water mites (Hydrachnida), we compared distributional, genetic and morphological characters in the closely related species Arrenurus angustilimbatus and A. rufopyriformis. The former has larvae that parasitise and disperse on adult mosquitoes, whereas larvae of the latter forego any association with hosts. 2. Allometrically adjusted egg size and gonopore size were found to be useful characters for distinguishing between females of the two species. 3. Arrenurus angustilimbatus possesses a broader and more continuous geographic distribution than its ‘direct developing’ counterpart. Allozyme heterozygosity was higher and population differentiation lower in A. angustilimbatus. In addition, populations of A. rufopyriformis were morphologically divergent, whereas populations of A. angustilimbatus were not. Isolation by distance analyses on both genetic and morphological characters indicated that the results were not biased by different sampling regimes for the two species. 4. These results demonstrate the importance of mosquito parasitism for maintaining ecological and genetic linkages between A. angustilimbatus populations. More broadly, we hypothesise that insect‐mediated dispersal has contributed to the ecological and evolutionary success of water mites, because the Hydrachnida lack other obvious adaptations for dispersing in space or time.     

Indirect sperm transfer and male mating strategies in soil invertebrates

Summary

Many soil invertebrates transfer their sperm indirectly by means of spermatophores. Among the different taxa there is great variation in spermatophore architecture, auxiliary structures and behaviour. The behaviour, ranging from elaborate courtship rituals to seemingly indifferent scattering of spermatophores, can roughly be classified as association and dissociation. Which of the two is adaptive depends on many factors which can be summarized in a simple functional response model showing that in some cases the best choice depends on density.     

The effect of the presence of quiescent female nymphs, males and their spermatophores on spermatophore placement in two species of eriophyoid mites

Under sex dissociated sperm transfer, females seek spermatophores and pick up sperm without male assistance. In several species males adjust spermatophore deposition rate to the presence of conspecifics. It is not known, however, which factors could favor such elasticity in non-pairing males. In this paper, we compare male response towards conspecifics between the sex dissociated eriophyoid mites Aculus fockeui (Nalepa and Trouessart) and Aculops allotrichus (Nalepa). The species differ significantly in male reproductive strategies and, consequently, the intensity of male–male-competition. Aculus fockeui males deposit spematophores all over the leaves and occasionally leave single spermatophores beside quiescent female nymphs (QFNs). In contrast, A. allotrichus males guard QFNs and encircle them with spermatophores. In this study, males of both species deposited spermatophores close to and apart from the rival spermatophores. Aculops allotrichus males had similar spermatophore output whether they were kept alone or in a group of seven males. They did not change spermatophore output in the presence of five rival spermatophores, a QFN or a QFN and varying number of rivals, either. In contrast, A. fockeui males increased spermatophore output in the presence of rival spermatophores or when on the arena with a QFN the male number increased to eight males. They did not respond, however, to the presence of a QFN and one rival or a QFN alone. The possible effect of the species-specific intensity of male–male competition, population density, the availability of receptive females and the rate of spermatophore output on the flexibility of eriophyoid spermatophore deposition is discussed.     

Fine structure of spermiogenesis, spermatozoa and spermatophore of Saxidromus delamarei (Saxidromidae, Actinotrichida, Acari)

Ultrastructural details of spermiogenesis, spermatozoa and the spermatophore of the early derived actinedid mite Saxidromus delamarei are described. Spermatids and mature sperm cells are provided with up to four acrosomal complexes and nuclei derivatives (chromatin bodies). Due to this reason, the sperm cells may be classified as synspermia, a sperm type found only in some spiders until now. The acrosomal complex is composed of a remarkably complicated vacuole and filament. Other peculiarities of sperm structure correspond to those found in prostigmatic mites, i.e. penetration of the chromatin body by the acrosomal filament and the presence of peripheral invaginations of the plasmalemma. The sperm cells are covered by a thin secretion layer of probably proteinaceous material. Stalked spermatophores are rather large, but simply structured and contain relatively few sperm cells. The results are discussed taking systematical and behavioural aspects into account. In particular, it is suggested that the peculiar mating behaviour of these mites secures both sperm transfer and first male's sperm priority and that this allowed reduction of sperm numbers.     

Fine structure of the male genital system of the predatory mite Rhagidia halophila (Rhagidiidae,Prostigmata, Actinotrichida)

The male genital system of the actinotrichid mite Rhagidia halophila is described and compared with other mites and arachnids. The large testes are composed of germinal and glandular parts and produce numerous small sperm cells. The glandular parts are connected via a testicular bridge. Spermiogenesis occurs in cysts containing spermatids in equal stages of development. Cysts of spermatids are embedded in huge somatic cells. The nuclei of the spermatids loose their envelope. Mature sperm cells are simple exhibiting a ring‐shaped chromatin body and lacking an acrosomal complex. They are most similar to the sperm cells of the related mite Linopodes motatorius. The spermatopositor contains the ejaculatory duct divided into a dorsal channel and a ventral channel that are connected via a narrow passage. At its distal end, the spermatopositor is divided into three eugenital lips. The function of the spermatopositor during deposition of the peculiar thread‐like spermatophores is discussed. Details of the sensilla of the spermatopositor and the progenital lips are reported. The genital papillae located on the inner side of the progenital lips exhibit characteristics of cells performing transport of ions and/or water. The results confirm the overall similarity of actinotrichid genital systems, which is profoundly different from that of anactinotrichid mites. With reference to other Arachnida it is corroborated that testes and sperm structure of Actinotrichida are most similar to that of Solifugae. However, synapomorphies between sperm cells of Rhagidia and Solifugae that could suggest a closer relationship between these two taxa as was suggested in earlier studies were not recognizable. On the contrary, the sperm cells of Rh. halophila being devoid of an acrosomal complex appeared to be more apomorphic than those of many other actinotrichid mites as well as Solifugae. J. Morphol. 276:832–859, 2015. © 2015 Wiley Periodicals, Inc.     

Recapture of male and female dragonflies in relation to parasitism by mites, time of season, wing length and wing cell symmetry

For aquatic mites parasitic on dragonflies, completion of their life cycle depends on their being returned to appropriate water bodies by their hosts, after completion of engorgement. We examined whether differences among hosts in timing of emergence or phenotypic attributes might affect their probability of return to an emergence pond, and hence success of mites. Parasitized males and females of the dragonfly Sympetrum obtrusum (Hagen) did not differ in overall recapture rates. Females that had wing cell symmetry and emerged early were more likely to be recaptured than females that emerged later or had wing cell asymmetry, but there were no consistent relations between these variables and parasitism by mites. No such relations between wing cell asymmetry, emergence date, and recapture likelihood were found for males. Using randomization tests, we found that mean intensities of Arrenurus planus (Marshall) mites at host emergence were the same for recaptured females and females not recaptured; however, males that were recaptured had lower mean intensities of mites at emergence than males not recaptured. Further, mature females carried more mites than mature males, and the latter had fewer mites than newly emerged males not recaptured. Biases in detachment of engorging mites do not explain the differences in parasitism between mature males and females, nor the differences in mite numbers between mature males and newly emerged males that were not recaptured. Rather, heavily parasitized males appear to disperse or die and are not recaptured, which should have implications for dispersal of mites and fitness of male hosts.     

Different sperm number in the spermatophores of Orchesella villosa (Geoffroy) (Entomobryidae) and Allacma fusca (L.) (Sminthuridae)

Members of the basal hexapod group Collembola perform indirect sperm transfer; males deposit spermatophores on the soil and these are then picked up by females for insemination. Orchesella villosa exhibits a dissociated mating behavior, while Allacma fusca has either associated mating behavior or, more commonly, produces spermatophores without pairing. Sperm ultrastructure in the two species has been studied by TEM and SEM observations to estimate the volume of these cells. The sperm number into each spermatophore has been determined by counting the fluorescent nuclei after Hoechst staining of sperm droplets squash preparations. Sperm droplets at the apex of spermatophores contain numerous spermatozoa of typical appearance, wound up and with a long anterior appendage (peduncle). Sperm droplets of Orchesella villosa are smaller (about 10 times) than in A. fusca, however they contain substantially more sperm cells (about three times). These differences could be explained as follows: (a) sperm of O. villosa are shorter than those of A. fusca (58 and 107 μm, respectively) and thus the volume of a single sperm of O. villosa is about 10 times smaller than in A. fusca; (b) considering the volume of sperm droplets and of sperm cells, the estimated number of sperm cells would be higher in A. fusca than in O. villosa; and (c) the conspicuous reduction of the sperm cells observed in A. fusca is likely linked to the aberrant meiosis present in this species, as well as in all Symphypleona studied so far, that causes a loss of 50% of their sperm.     

Repeated visitations of spermatophores and polyandry in females of eriophyoid mites

Eriophyoid females store sperm either asymmetrically in one spermatheca, or symmetrically in both spermathecae. Previous studies have suggested that species in which females store sperm asymmetrically pick up sperm from only one spermatophore, while those with symmetrical sperm storage pick up sperm from two or more spermatophores during their lifetime. The aim of this study was to examine spermatophore visitation behaviour and symmetry of sperm storage in Aculops allotrichus from the black locust tree and Cecidophyopsis hendersoni from the yucca. This would indicate monandry or polyandry in these species. In both eriophyoids, the spermatophore visitation consisted of three phases: mounting, lying on the spermatophore and dismounting. Aculops allotrichus stored sperm asymmetrically. However, nearly one-third of the observed females visited two spermatophores, rather than only one in their lives. When A. allotrichus females visited two spermatophores they spent a similar amount of time at the first and at the second visitation. Also, the times of visitation of the first of the two spermatophores and the single spermatophore in a female lifetime did not differ significantly. This would suggest that apart from monandry, double insemination also occurs in this species. By contrast, C. hendersoni females were polyandrous. They stored sperm symmetrically and visited several spermatophores, on average 1.54 (max 6) per day, and up to 33 spermatophores in their lives. The benefits of repeated spermatophore visitation and the possible mechanisms of sperm storage in both species are discussed.     

Distant Lovers: Spermatophore Deposition and Destruction Behavior by Male Springtails

Males of the springtail Orchesella cincta transfer their sperm indirectly using spermatophores. The present study aimed to investigate how individual males maximize their reproductive success. In an experiment examining the role of chemical communication, it appeared that the males deposit their spermatophores preferentially on patches which have been conditioned with conspecifics. Varying conditioning intensity resulted in a response which can be described by a saturation curve. In a comparison involving a related species the conditioning effect was strictly species specific. An experiment where the sexes were compared showed that conditioning with males exerts a slightly stronger effect than conditioning with females. In another experiment spermatophore depositing males showed a strong preference for patches with spermatophores of previous males, which they replaced with their own. An explanation for this may be that the males parasitize each other's scent marks. When a number of males are kept together they destroy most of each other's spermatophores. The destruction behavior is specifically displayed by males in their reproductive phase. Video recordings showed that deliberate destruction of spermatophores takes place by eating them and that the males are able to recognize and spare their own spermatophores.     

The Vas Deferens of the Spanish Lobster,Scyllarus chacei

Summary

The male reproductive tract of Scyllarus chacei consists of paired testes and vasa deferentia that conduct sperm containing spermatophores to the genital pores at the base of each fifth walking leg. The testis is joined to the vas deferens which can be divided into four regions: (1) the anterior vas deferens can be further divided into three regions. It is highly convoluted and is the region in which the sperm become encapsulated in ovoid spermatophores of approximately 100 sperm as well as produces seminal fluids. (2) The middle vas deferens is the primary site of sperm storage and adds to seminal fluids which formed in the anterior region. (3) The posterior region is highly muscularized and may serve for limited sperm storage. (4) The most distal portion is the ejaculatory duct which is highly muscularized for extruding the spermatophoric mass for transfer to the female. A final seminar product is added here.     

THE EVOLUTION OF COPULATION IN WATER MITES: A COMPARATIVE TEST FOR NONREVERSING CHARACTERS

Although copulation is a widespread behavior with multiple origins, hypotheses about selective forces behind its evolution have not been tested by the comparative method. Because copulation has arisen many times in the water mites (Acari: Parasitengona), they are good subjects for a comparative study of copulation. I determined that copulation evolved 91 times in the 343 extant genera. There was no evidence of reversals to noncopulation; therefore, Ridley's (1983) contingency-table comparative test was not appropriate. I designed a comparative test for instances in which there is no loss of the derived trait of interest. This test determines whether independent evolutions of a trait cooccur with a predictor more often than expected by chance. Two hypotheses were tested: 1) that copulation would be selected for in running-water habitats because of disruption of pheromonal communication; 2) that copulation would be selected for in swimming mites because females are less likely to contact spermatophores deposited on a substrate. Independent evolutions of copulation among running-water mites were not more frequent than expected by chance (P > 0.4), but there were more evolutions of copulation than expected among swimming mites (P < 0.005). Endoparasitism, secondary loss of swimming hairs, production of spermatophore fields, courtship, and benthivorous habits may explain why some mites copulate but do not swim while others swim but do not copulate.