smith_99c - ACAROLOGYIX VOLUME 2 SYMPOSIA Glen R. Needham...

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Unformatted text preview: ACAROLOGYIX VOLUME 2 SYMPOSIA Glen R. Needham Rodger Mitchell David J. Horn W. Calvin Welbourn Editors Published by The Ohio Biological Survey Columbus, Ohio 43210 SECTION 4: PHYLOGENETIC PERSPECTIVES ON THE BIOLOGY OF THE PARASITENGONA 4.4 139 LARVAL HYDRACHNIDIA AND THEIR HOSTS: BIOLOGICAL INFERENCE AND POPULATION STRUCTURE Bruce P. Smith Biology Department, Ithaca College, Ithaca, New York 14850 Larval water mites parasitize a broad diversity of insects, and while the details may vary, there are certain recurrent themes. Bottger (1976) subdivided the association into categories based on proximity to water; type I being subaquatic, type 11 being in close proximity to water, and type 111 being completely aerial. Mitchell (1957) defined groupings of water mite life histories based on duration of association with the host; later in his paper he subdivided the Hydrachnidia into lineages, in part based upon larvae being essentially "aeria ", finding their host above the water's surface tension, or "aquatic", where the larva swims in search of its host. I have previously discussed three modifications to the general life cycle observed among some species of Hydrachnidia (B. Smith 1988): larval phoretic association prior to parasitism, the mites remaining on the host for their protonymph (nymphochrysalis), and the development of a truly aquatic larva. These three adaptations can all be absent, can occur independently or in various combinations, and undoubtedly have each evolved on several occasions (Fig. l). My classification is based on presence or absence of these adaptations and my intent is to form groupings that have ecological significance, reflected by population structure. a) Opportunist terrestrial associations ("unspecialized"): aerial larvae (sensu Mitchell), locating the host on or above the water's surface, parasitizing terrestrial/aerial insects. Larvae detach after engorgement but before transformation into a quiescent protonymph. 1' Tl’l’ical of Hydrovolzioidea, most Hydryphantoidea, and ‘. some .Eylaioidea (e. g., Limnochares spp.). b)‘Terrestrial a afsoc1ations with aquatic preparasitic attendance ( preparasitic attendance"): an aquatic larva (sensu ‘ Mitchell), locating the juvenile stage of a potential host 1 Peneath thewater's surface and attending it until the I Insect's transformation to a terrestrial/aerial adult, then :u’ansferring to the adult insect before attachment and ,engorgement. Larvae detach afier engorgement but before gallsfolrmation into the quiescent protonymph. Typical of is bertioidea, Hygrobatoidea, Arrenuroidea, ‘ tygothrombidioidea, and a few Hydryphantoidea (i.e., Wandesz'a spp.). c) Extended parasitic associations (“extended associations”): aerial or aquatic larvae (sensu Mitchell) that remain on the host for the protonymph stage. Aerial larvae may parasitize surface-dwelling insects (e.g., Neolimnochares spp. on Gerridae, some Hydryphantes spp. on Hydrometn'dae) or infest subaquatic insects by attaching within the respiratory airspace of their hosts (e.g., Eylais spp., Piersigia spp.), While aquatic larvae attach to subaquatic insects (Rhyncholimnochares spp., Hydrachna spp.) sometimes within the respiratory airspace (Rhyncholimnochares spp., some Hydrachna spp.). Typical of Hydrachnoidea, most Eylaioidea, and a few (e.g. Hydryphantes species of Hydryphantoidea tenuabilis). A - aquatic larvae B - preparasltic attendance C - extended associatlon Y’ 55“ 5 6 45 as :3 Q ”’ q, S Q o a? U a, e6 o 5 s a 0 5 at" t >. .3, re :: ~z~ 0 Q T‘ Y. Fig. 1. Occurrence of aquatic larvae, preparasitic attendance, and an extended parasitic association among the water mite superfamilies. The evolutionary relationship among superfamilies is still quite speculative, so no attempt has been made to represent this section of the phylogenetic tree. 140 MATERIALS AND METHODS Three species of water mites were used for comparison, each representing one of the three generalized types of association. Limnochares americana Lundblad has an unspecialized association with Leucorrhiniafrigida Hagen dragonflies, while an Arrenurus sp. (probable new species, near A. reflexus) associated with the same host species was the representative for preparasitic attendance (see W. Cook 1991 for details of methods). In 1990, daily census of hosts and parasites was conducted on Hebert Bog, located about 50 km northeast of Kingston Ontario. Newly captured dragonflies were given individualized wing markings in binary code with acrylic paint. On each capture and recapture, the number of each mite species and the code number of the host were recorded. Eylais euryhalina Smith has an extended association with the water boatman Cenocorz'xa bifida Hungerford (see B. Smith 1977 for details of methods). Thirteen lakes in central British Columbia were sampled on a two-week cycle from late April to late October 1976, and late April to mid-June 1977. Twenty-five to several hundred Cenocorixa bifida were collected in each sample, preserved in 80% ethyl alcohol, and mites were removed, identified, and counted in the laboratory. RESULTS AND DISCUSSION Note that my classification of larval parasitic association only establishes three main themes that would include the vast majority of Hydrachnidia although, there are rare exceptions that would not cleanly fit in one of the three categories. The utility of the three categories lies in that the type of relationship can be reflected in the pattern ("distribution") of mites within a host population. In theory, attachment by larval mites with the "unspecialized association" can occur-at almost any time during the host's aerial existence, including juvenile hosts if they occur above the water's surface. However, the pattern of larval mites among age and gender subgroups in the host's population may be defined by behavioral differences influencing exposure to mites (Fig. 2; L. americana). The potential also exists for hosts to accumulate larval mites over time, hence intensity of infestation may be positively correlated with age. This type of association is also typical for the majority of terrestrial parasitengonines and is presumably the ancestral (plesiotypic) condition for Hydrachnidia. It is therefore no surprise that this type of relationship is found within several distantly-related superfamilies of water mites (Fig. 1). Larval mites with an unspecialized association do not necessarily reflect the host's age and gender nor are biases necessarily consistent among species of mite and host. Mullen (1975) found that Thyasides sphagnorum Habeeb, ACAROLOGYIXZSYMPO$A was commonly found on mosquitoes of both genders, and the female mosquitoes were nulliparious. T hyasides sphagnorum have an unspecialized association, but tend to encounter hosts at or during the host's emergence and transformation to adult. In contrast, the confamilial T hyas barbigera is found only on parous female mosquitos, and colonizes hosts that are ovipositing. Limnochares americana does not have consistent gender-bias on all hosts (Cook 1991): species of dragonflies with males defending territories by perching (such as L. frigida) have a strongly male-biased infestation, while some damselfly species that exhibit contact mate-guarding have a strong female-bias. The strong female-bias relates to the male being held aloft while the female perches at the water's surface and encounters larval mites. To make meaningful interpretations involving mites characterized by unspecialized associations, an investigator must be aware of where and when the hosts and parasites typically make contact. . 69 53 74 1126 5} 40— U) a . 2 20 — ‘2 2 a o — _ S 20L (U .2 g (T: E 10 e CU .JI ‘ o A 1 l ‘.-. . TENERAL MATURE TENERAL MATURE FEMALE MALE POPULATION SUBGROUP Fig. 2. Abundance (average number of mites per host) of larval Limnochares americana and Arrenurus sp. on Leucorrhiniafrigida, partitioned by gender and relative age of host. Sample sizes of each category are presented at the top of the fig.. Differences between categories are statistically significant for L. amen'cana (Kruskal-Wallis test statistic = 372.61, P < 0.001) and for Arrenurus SP- (Kruskal—Wallis test statistic = 612.09, P < 0.001). SECTION 4: PHYLOGENETIC PERSPECTIVES ON THE BIOLOGY OF THE PARASITENGONA 141 Host/parasite relationships involving preparasitic attendance result in a close synchrony between host and parasite. All larval mites will attach during their host’s emergence as an adult, hence the stage of development of the larval mite should directly reflect the adult age of the host. Beyond a certain age hosts should have lost all parasitic mites (Fig. 2; Arrenurus sp.). While there can be a gender-based bias when the larval mites search out potential hosts (e.g., Lanciani 1988), the host's transformation from a subaquatic juvenile to a terrestrial/aerial adult is a universal event shared among all members of the host's population so both genders should have similar exposure to parasitism. Preparasitic attendance is exhibited by some species of Hydrachna (e.g., Hydrachna virella; Lanciani 1982) and at least one species of aerial larva (Hydryphantes tenuabilis Marshall, Lanciani 1971a), however these are exceptional species best treated individually. Most species exhibiting this specialized method of host discovery and association belong to one evolutionary lineage (Fig. l, Hygrobatoidea + Lebertioidea + Arrenuroidea; 1. Smith and Oliver 1986) although at least two additional independent lineages also exist (Fig. l, Stygothrombidioidea, and Wandesia spp. within the Hydryphantoidea). The types of association and their correlations with age result in significant differences when monitoring survivorship of a population of hosts in nature. There is reduced survivorship of male L. frigida correlated with greater intensity of infestation by Arrenurus sp., which could be interpreted as parasite-induced reductions in longevity (Fig. 3). There is increased survivorship of these hosts correlated with greater intensity of infestation by Limnochares americana (L.) (Fig. 4): the longer the host survives, the more larval mites it accumulates. Estimating the impact of parasitic larval water mites on naturally- occurring host populations can only be accomplished using mites exhibiting preparasitic attendance. 1 am not the first to recognize the significance of differences in life history among water mites and the Implication for differences in infestation among population SUbgroups. The use of T hyas spp. and Arrenurus spp. for age-grading mosquitoes was discussed by various authors (reviewed by Mullen 1975) and is based on the time at Which mites attach to and detachvfrom their host. T hyas spp. are found almost exclusively on parous female mosquitoes, while Arrenurus spp. are found on both males and females, and almost exclusively on nullipars (Mullen 1975, 1977). Mitchell (1969) also demonstrated the use of A’rfmurus spp. to determine the age of dragonflies, and B. Smith and W. Cook (1991) documented the strong k negatlve covariance between Arrenurus sp. and L. ' “(nerlcana on dragonflies. These cases all amount to the I dlsnnction between an "unspecialized" association and :. aquatic preparasitic attendance. 7r 9% g‘. i. (2') _ unparasitized E H? 11-120 mites/host > (I 2) (D Z 9 p— D: O \ e m 0.2 ~ , , , , V _ \ D. o I | I I 0 1O 20 30 40 MINIMUM SURVIVAL IN DAYS Fig. 3. Minimum adult survivorship of territorial male Leucorrhinia fn’gida dragonflies relative to maximum observed intensity of Arrenurus sp. mites. Minimum adult survivorship is based upon the number of days between dates of first and last capture, and maximum intensity is the maximum number of mites on that individual for any day's observation. unparasitized g 31-115 mites / host _ o 8 _ Z . > g m 0.6 e Z 9 l— 0.4 e a: 0 g . m 0.2 — x D. r fix _ _‘ i\ * , , , , _ , o . . . \ O 10 20 30 40 MINIMUM SURVIVAL IN DAYS Fig. 4. Minimum adult survivorship of territorial male Leucorrhinia fi'igida dragonflies relative to maximum observed intensity of Limnochares americana mites. Minimum adult survivorship is based upon the number of days between dates of first and last capture, and maximum intensity is the maximum number of mites on that individual for any day’s observation. With an extended association the parasitic relationship includes the protonymph, the duration of the parasitic relationship has usually been greatly extended and the degree of engorgement is generally much greater. Mites exhibiting the other two themes of parasitic association almost always have a comparatively short-term association (1 to 7 days) with larvae engorging to about 5 to 100 times 142 VARIANCE 10“ 1 o" 1 0° 101 ABUNDANCE Fig. 5. Taylor Power Law relationship for abundance and variance of larval Limnochares americana on territorial male Leucorrhinia frigida. Regressions are based upon 41 samples of a total of 1,057 dragonflies and 26,072 mites. Partitioning data by date of sample or by relative age of host (determined by presence or absence of Arrenurus sp.) had no effect on the relationship (log variance = 1.419 X log abundance + 0.350, r = 0.98). their original volume (Smith 1988). In contrast, some species of Eylais and Hydrachna extend the relationship as long as ten months (e.g., Davids 1973, Davids et al. 1977, Davids and Schoots 1975) and larvae may engorge to 600 times their original volume (Hydrachna conjecta Koen., Davids 1973). In many extended associations the degree of engorgement on the host represents a significant proportion of the host's volume, and an individual host probably cannot support more than a small number of larval mites. The pattern of mites among hosts can shift dramatically over time as engorgement progresses: early on, mites may be "clumped" (certain individual hosts carry the majority of the larval mites), while later in the relationship the pattern will approach a random or even tend towards a uniform pattern in the host's population (Smith 1988). Presumably this reflects mortality among heavily-infested individuals. This shift in pattern can be demonstrated by comparing variance with the abundance of mites (= arithmetic . mean). Howeve, it is not independent of abundance; the relationship is best described by the Taylor Power Law. The Taylor Power Law for an unspecialized association is illustrated in Fig. 5: the relationship is stable over the season. In comparison, clumping does change over the duration of an extended association as indicated by a decreasing slope in the Taylor Power Law when data are partitioned by season (Fig. 6). Species with the extended association represent a progression towards greater dependency on the host for feeding, with some Eylais spp. attaining over 40% of their ACAROLOGY IX: SYMPOSIA adult size during their larval and protonymphal stages (Lanciani 1971b). This trend is opposite to that exhibited by the main lineage exhibiting preparasitic attendance (Lebertioidea + Hygrobatoidea + Arrenuroidea), a trend for decreasing both the duration and degree of larval engorgement while increasing growth during the deutonymphal stage (1. Smith and Oliver 1987). The extended association has apparently evolved independently several times: Limnochares spp. retained the plesiotypic condition of an "unspecialized" parasitic association, yet other Eylaioidea have an extended association as do the presumably unrelated Hydrachnoidea and at least one species of Hydryphantoidea (Fig. 1). /A 102 - V summer .// ‘ ~~ autumn/early spring / e v late spring 5/ /» 10‘ — " / LU . / c23 10" S E > 10" r 10'2 — 10'3 I I I 10‘3 10‘2 10" 10° 10‘ ABUNDANCE Fig. 6. Taylor Power Law relationships for abundance and variance of larval Eylais euryhalina on Cenocorixa bifida. Each point represents one sampling date from one of the 13 lakes, with a total of 112 samples of a total of 40,164 water boatmen and 10,312 mites. There was no significant relationship between host's gender and parasitism, however partitioning data by date of sample did significantly alter the Taylor Power Law (summer: log variance = 1.476 X log abundance + 0.730, r = 0.98; autumn/early spring: 10g variance = 1.081 X log abundance + 0.148, r = 0.98; late spring: log variance = 0.955 X log abundance — 0.060, r = 0.99). SUMMARY Parasitic associations of larval water mites with insect hosts are categorized into three general themes. The utility of this classification is that the three themes are reflected in the pattern ("distribution") of mites within host populations. An unspecialized association is opportunistic and hence encounters are largely dependent on the host's behavior: infestation can be positively correlated with the SECTION 4: PHYLOGENETIC PERSPECTIVES ON THE BIOLOGY OF THE PARASITENGONA 143 host's age and highly dependent on the host's gender. ACKNOWLEDGMENTS Associations typified by preparasitic attendance usually lack any gender—bias, but infestation is negatively I thank Wanda Cook, who collected the data on L. correlated with the host's age. Extended associations amerz’cana and Arrenurus spp. parasitic mites on L. involve the mite remaining on the host for the protonymph; frigida, dragonfly. I thank Frank Phelan and Floyd the association is usually prolonged and engorgement is Connor for their support. The research was funded with extreme, and over time, associations tend to shift from a NSERC grants to myself (dragonfly/mite association) and pattern of clumped mites within the host's population to a to G.G.E. Scudder (water boatrnan/mite association). pattern approaching a random distribution. LITERATURE CITED BOttger, K. 1976. Types of parasitism by larvae of water mites (Acari: Hydrachnellae). Freshwater Biol. 6: 497-500. Cook, W. J. 1991. The parasitism 0f dragonflies by the water mite Limnochares americana Lundblad (Acari: Parasitengona; Limnocharidae). MSc. thesis, University of New Brunswick, Fredericton, Canada. 96 pp. Davids, C. 1973. The water mite Hydrachna conjecta Koenike, 1895 (Acari: Hydrachnellae), bionomics and relation to species of Corixidae (Hemiptera). Neth. J. Zool. 23: 363-429. —, G. J. Nielsen, and P. Gehring. 1977. Site selection and growth of the larvae of Eylais discreta Koenike, 1897 (Acari: Hydrachnellae). Bijdr. Dierk. 46: 180-184. —, and C. J. Schoots. 1975. The influence of the water mite species Hydrachna conjecta and Hydrachna cruenta (Acari: Hydrachnellae) on the egg production of the Corixidae Sigara striata and Cymatia coleoptrata (Hemiptera). Verh. int. Verein. Limnol. 19: 3079-3082. Lanciani, C. A. 1971a. Host exploitation and synchronous development in a water mite parasite Of the marsh treader Hydrometra myrae (Hemiptera: Hydrometridae). Arm. Ent. Soc. Amer. 64: 1254-1259. —. 1971b. Host—related size of parasitic water mites of the genus Eylais. Am. Midl. Nat. 85: 242-247. —. 1982. Parasite-mediated reductions in survival and reproduction of the backswimmer Buenoa scimitra (Hemiptera: Notonectidae). Parasitology 85: 593-603. —. 1988. Sexual bias in host selection by parasitic mites Of the mosquito Anopheles crucians (Diptera: Culicidae). J. Parasit. 74: 768-773. Mitchell, R. D. 1957. Major evolutionary lines in water mites. Syst. Zoo]. 6: 137-148. —. 1969. The use of parasitic mites to age dragonflies. Am. Mid]. Nat. 82: 359-366. Mullen, G. R. 1975. Parity determinations in adult mosquitoes parasitized by aquatic mites (Acarina: Hydrachnellae). Proc. N. J. Mosq. Exterm. Assoc. 62: 90-94. —. 1977. Acarine parasites of mosquitoes. IV. Taxonomy, life history and behavior of Ihyas barbigera and T hyasides sphagnorum (Hydrachnellae: Thyasidae). J. Med. Ent. 13: 475-485. Smith, B. P. 1977. Water Mite Parasitism of Water Boatmen (Hemiptera: Corixidae). MSc. Thesis, University of British Columbia, Vancouver, Canada. 117 pp. —. 1988. Host-Parasite interaction and impact of larval water mites on insects. Annu. Rev. Entomol. 33: 487-507. —, and W. J. Cook. 1991. Negative covariance between larval Arrenurus sp. and Limnochares americana (Acari: Hydrachnidia) on male Leucorrhinia frigida (Odonata: Libellulidae) and its relationship to the host's age. Can. J. Zool. 69: 226—231. Smith, I. M., and D. R. Oliver. 1986. Review of parasitic associations of water mites (Acari: Parasitengona; Hydrachnidia) with insect hosts. Can. Ent. 118: 407-472. ...
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smith_99c - ACAROLOGYIX VOLUME 2 SYMPOSIA Glen R. Needham...

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