Opilioacarus (Neocarus) texanus, (Chamberlin and Mulaik) (Chamberlin and Mulaik)

Klompen, J. S. H., 2000, Prelarva and larva of Opilioacarus (Neocarus) texanus (Chamberlin Mulaik) (Acari: Opilioacarida) with notes on the patterns of setae lyri ® ssures, Journal of Natural History 34 (10), pp. 1977-1992 : 1979-1989

Results

Biology

Initial collections yielded 16 specimens, four of which were kept alive in the laboratory. The specimens were kept at c. 22°C in dishes with a charcoal plaster-of-Paris substrate. Following suggestions by Walter and Proctor (1998), different kinds of food were offered, included squashed insects, live house dust mites ( Dermatophagoides sp. ) and pollen. Feeding was observed for pollen only. The animals were generally somewhat sluggish, suggesting that the rearing conditions might not have been optimal. Even so, one specimen survived for seven months.

All specimens were missing legs when arriving at the laboratory, but regained their full complement of legs in the next two months. In addition, a new cuticle was observed in the chelicerae of a slide mounted specimen with a fully developed ovipositor. This is consistent with earlier suggestions ( Coineau and Legendre, 1975) that adult moults may occur in Opilioacarida . Although probabl y a rare phenomenon among Acari , adult moults have been described previously, e.g. for Trombidiidae ( Michener, 1946) . The alternative, that the collected specimens were immatures, moulting in the laboratory to adults and mating in the laboratory, is considered less likely.

A few observations could be made on egg deposition patterns. Of the two egglaying episodes observed, the fi rst (May 27-30) yielded four eggs, the second (June 17-19) two to three. The eggs were laid in cracks at the margin of the substrate or under a rock provided as shelter. The eggs themselves are white and smooth, but when located were coated with debris (it is unclear whether this is done by the female, and if so, how). They do not show the anterior and posterior processes fi gured by Van der Hammen (1966; his figure 6 ). Based on the egg deposition pattern observed, females appear to lay only one egg at a time, depositing the next egg considerably later. The alternative, single females laying several eggs in quick succession with different females depositing at distinctly different times (weeks or months apart) is considered less likely because slide mounted females do not show more than one developing egg.

One egg was dissected and yielded a prelarva. If the prelarva hatches, it is assumed to be very short lived: none were observed out of egg. The only other studies mentioning prelarvae in Opilioacaridae , ( Coineau, 1973; Coineau and Van der Hammen, 1979) did not mention whether the prelarva of Phalangiacarus brossetti actually hatched, so comparisons for this developmental trait are not yet possible. The hatched larvae are active but extremely slow. I did not observe feeding, and the few larval specimens retained in the rearing container died without moulting.

Descriptions

Prelarva. The only specimen available ( figure 1 ) contains a partially developed larva. The general morphology appears highly similar to that of the prelarva of Phalangiacarus brossetti ( Coineau, 1973) . No sensillae were observed, but legs I -III and the palps showed signs of normal segmentation, including differentiation of basitarsi II -III. This segmentation is most reliably indicated by differentiation of the cuticular spine/scale pattern. The ecdysial line, delta (δ), is very distinct, and stretches from the base of the chelicerae to just above coxae III. Legs IV are represented by non-segmented, but rather large vestiges. The presence of vestiges of legs IV in the prelarva of a mite has not been reported previously ( Lindquist, 1984). The cuticle is covered with very small knobs and spines, changing into distinct scales on the dorsal surface of the leg and palpal segments (especially the trochanter and femur), and into even larger broader scales on the dorsal surface of the chelicerae. A line possibly corresponding to the sejugal furrow (s.f.) is weakly differentiated by the pattern of cuticular spines.

Larva. General ( figure 2 ). A total of three larvae was examined, only one of which retained legs I. The body is constricted at the level of coxae III, but the constriction is even weaker than in the post-larval instars. Ratio of idiosomal length, 470 μ m, to width, 285 μ m: 1.7 (measured in an alcohol preserved specimen). Legs long, respectively, 875, 515, and 520 μ m. Ratio of leg to idiosomal length for leg I 1.9; for legs II and III 1.1. These ratios are slightly higher than those listed for a`subadult’ by Van der Hammen (1966) (1.5, 0.7, 0.7, and 1.0 for, respectively, legs I -IV). Cuticle of the idiosoma covered with small rounded spines (as in the prelarva and post-larval instars). Spines on the cuticle of the leg, palps, and the basal segment of the chelicerae more pointed than on the idiosoma. Subcapitulum without any distinctive spine pattern. The distinctive pattern of purple bands on the idiosoma and legs of the post larval instars is not apparent in the larvae. They appear mostly white, with available pigment concentrated around the eyes and in two kidney shaped areas in the opisthosoma (not fi gured).

Gnathosoma and palps. Gnathosoma ( figure 3 ). General shape as in the adults. Rutellum inserted dorsally, with four blunt teeth; With’s organ weakly developed (relative to the post-larva l instars), shaped like a broad roundish spine. Poor development or even absence of this structure in early nymphs and larvae of Panchaetes dundoensis has been reported previously ( Naudo, 1963). Setation limited to two pairs of setiform hypostomal and one pair of small spinose setae (this may be seta pl1 of Van der Hammen, 1966). The presence of `pl1 ’ and With’s organ distinguish this setation pattern from that observed in all other parasitiform larvae. Lateral lips, labrum, and deutosternal groove poorly developed.

Chelicerae ( figure 4 ). Large, total length approximatel y 170 μ m. Overall structure resembling that in the adult. No setae on the basal segment. With three setae and lyri fi ssure i α on the second segment. Lyri fi ssure id on the second segment not observed in the larva, but present in the adults and possibly in the nymphal instars. The presence of three pairs of setae clearly distinguishes this taxon from nonopilioacarid Parasitiformes , which never show more than two setae on the second segment ( Evans, 1992). Dentition of the cheliceral digits poorly developed, with near complete absence of any teeth on the fi xed digit.

Palps ( figure 5 ). Very well developed, approximately 205 μ m long. As in adult Opilioacaridae with six recognizable segments. However, the tibiae and tarsi are partially fused, almost certainly disallowing independent movement. Pretarsi in the form of a pair of well developed terminal claws. Setation well developed. Trochanters without setae as in all other parasitiform larvae. Femora with setae al or ad (unclear), pd1, pd2, and pl. This arrangement appears the same as that reported for larval Allothyridae (Holothyrida) ( Klompen, 1992) and Mesostigmata ( Evans, 1963b), but slightly impoverished relative to Ixodidid larvae which carry an added anterior dorsal (nearly all Ixodida ) and ventral ( Ixodidae only) seta ( Klompen, 1992) on each femur. Genua with seven setae: al1, al2, ad1, ad2, pd1, pd2, and pl. Relative to larval Allothyridae , Argasidae (Ixodida) , and Mesostigmata, al2 (added in the deutonymph of Mesostigmata) and pd2 are added, but overall this arrangement is quite similar to the one found in larval Ixodidae (with three ad ’s and one al). All femoral and genual setae are heavily barbed and relatively blunt. None show the mucronate shape found in some dorsal femoral and genual palp setae of the adults.

Tibiae each with a total of 15 or 16 setae (one specimen carried an extra pl seta), including 3 al, 2 ad, 3 pd, 3/4 pl, and 4 v setae. Tibial setae variable in shape: the basal and pl setae are similar to the femoral and genual setae, although less blunt; the distal tibial setae are smooth or very lightly barbed, with relatively pointed tips. Some of the latter group of setae may be of the sm-type of Van der Hammen (1966), but the minor changes in morphology involved are di ffi cult to discern in these larvae. The smooth setae are dark in colour when observed under phase contrast microscopy (the previous setae all appear light,`hollow’). Tarsal setation in O. texanus includes four thin-walled and only lightly tapering dorsal setae with rounded tips, and six setae of the smooth type seen in the distal tibial setae. None of the tarsal setae exhibit the leaf-like shape seen in the tarsal pl-type setae of the adults. The adults of O. texanus also carry two lyrifissures, i α antiaxial and i π paraxial, on each tarsus ( Van der Hammen, 1966), but these lyrifissures were not observed in the larva. Comparison of this pattern of tibial and tarsal setae with patterns in other parasitiform larvae are tentative because the tibiae and tarsi in most of those taxa are partly or completely fused. Comparisons considering the combined setal complements of the tibiotarsi seem more appropriate. Total numbers of setae on each tibiotarsus (25 -26) are virtually identical to the numbers observed in larval Allothyridae (25 in two specimens examined), and only slightly higher than the usual numbers in larval Mesostigmata (23). Larval Ixodida show strong reductions in the tibiotarsus with a setal complement of no more than 12 and the absence of the pretarsal claws.

Idiosoma. The dorsum of larval O. texanus shows a division between an anterior and a posterior area, indicated by the presence of setae, absence of lyrifissures, and absence of lengthwise arranged rows of muscle scars in the former, and the presence of transverse rows of lyrifissures, setae, glands, and muscle scars in the latter. It is not immediately obvious what idiosomal division these two areas reflect. Two hypothese s have been considered. The posterior section might begin at the opisthosomal segments (VII/VIII), and thus be post-pedal, as suggested by Van der Hammen (1966), or it may begin at the hysterosomal segments (V/VI, i.e. the segments of legs III and IV). For positional reasons, I tentatively prefer segment V, the fi rst hysterosomal segment, as the fi rst on which cuticular structures can be designated: such an arrangement does not require massive distortions of the segmental boundaries between the dorsal and ventral surfaces. However, this particular question needs to be examined in a more comprehensive comparative study.

The anterior part of the idiosoma includes a number of setae in a more or less random arrangement, and two pairs of subequal eyes. A slightly raised area near the anterior margin carries the most anterior pair of median barbed setae. Setation includes a median arrangement of fi ve to seven pairs of robust, heavily barbed setae, and several pairs of smaller and more slender setae with few barbs (often terminally bi fi d). The latter set includes one pair anterior, two pairs internal, and one pair postero-lateral to the eyes, and two pairs in line with the j and z series of lyrifissures on the hysterosoma (the pair postero-lateral to the eyes could be interpreted as in line with the s series of hysterosomal lyrifissures). Similarly, glands are present in two patterns: one consisting of four to six unpaired glands arranged lengthwise between the median barbed setae (one pair near the anterior pair of these setae), the other arranged transverse and in line with the gland series on the hysterosoma. Muscle scars include a less distinct but comparable lengthwise arrangement between the median setae and eyes, and a few muscle scars following the transverse arrangement seen for the hysterosoma. Based on the variability in the position and number of the median setae and glands observed within and among individuals, these structures are not considered to be designatable (idionymic). In contrast, the transversely arranged setae, glands, and muscle scars do appear to be idionymic. The lack of variability among the three specimens examined and the match with the observed regular pattern of the remaining hysterosomal structures, fi t that hypothesis.

Hysterosoma. The arrangement of the lyrifissures, glands, and to some extent setae and muscle scars on the posterior part of the idiosoma (segments V -XVIII in fi gures 6 and 7) is clearly not random. Three pairs of dorsal, and three pairs of ventral series of lyrifissures are distinguishable, interspersed with two dorsal, one lateral, and one ventral series of glands. This pattern of lyrifissures, glands, and setae is easily reconciled with the modi fi ed Hirschmann system of nomenclature ( Lindquist and Evans, 1965), as adapted for larval Ixodidae ( Klompen et al., 1996) . Within that system the lyrifissures include the j, z, and s series in dorsal positions, and the jv, zv, and sv series in ventral positions (from central to marginal in both cases). Glands are inserted between the j and z, z and s, s and sv, and zv and jv series. Most remarkably, and unlike the patterns for any Mesostigmata or Ixodida studied so far, the pattern is nearly complete. The only`deviations’ observed are on the venter. The lyrifissures in series jv, zv, and sv on segments VIII and IX, and the glands in series jv on segment IX were not observed, but the available specimens did not allow accurate assessments in this region of the venter. Similarly it is unclear whether the ventral sv gland on segment X (indicated by the arrow in figure 7 ) is indeed a gland or a lyri fi ssure. The structure is extremely di ffi cult to observe and is only provisionally designated as a gland. On the other hand, the reduction in cuticular structures of the terminal segments (XVI, XVII) does appear to be real. A possible explanation for the absence of glands or lyrifissures on the venter of these segments might be that the slightly ventral position of the anal cone severely restricts the available ventral surface area of especially segment XVII. The arrangement of the lyrifissures and glands is consistent with the arrangement of the muscle scars, an arrangement used previously to indicate segmentation in adult Opilioacarida ( Van der Hammen, 1966) . I thus conclude that the arrangement of the lyrifissures and glands most probably reflects the ancestral segmentation pattern. The total number of hysterosomal segments in these larvae (13, perhaps 14 if segments VII and VIII are separate) is the same as in the adults.

The main difference with observed patterns in Mesostigmata and Ixodida is that the pattern in this larval opilioacarid is dominated by lyrifissures, instead of setae. This may not be a major problem. Both setae and lyrifissures are mechanoreceptors with similar innervation ( Altner and Prillinger, 1980; Evans, 1992), distinctly different from typical glands which lack innervation. Within Opilioacaridae , these two types of sensillum appear at least partly interchangeable. The observations that the setae on segment V (dorsal) and XVI (ventral) are directly in line with the series of lyrifissures (j V, z V, and zv XVI positions) suggests that these two types of structure fi t in the same sensillar distribution pattern. Among-species comparisons provide some additional support. Larvae of both species examined for this characteristic carry a limited number of lyrifissures on each hysterosomal segment, with setae restricted to the most anterior and most posterior segments ( Naudo, 1963; this study). In contrast, adult Opilioacarida carry a very large number of nondesignatable cuticular structures on the hysterosoma. These can be either lyrifissures (e.g. Opilioacarus ) or setae (e.g. Panchaetes or Salfacarus ). In the latter case the number of lyrifissures remains small and possibly idionymic ( Van der Hammen, 1977). The observation that the added receptors can be either lyrifissures or setae is consistent with the hypothesis that the two types of structure are homologous. Occasional switches between lyrifissures and setae are also known from other Parasitiformes (e.g. Athias-Henriot, 1980), although they are often ignored or treated as teratologies.

Venter. The ventral podosoma carries three pairs of sternal setae, but no setae on the genital verrucae. Lyri fi ssures are absent, but two pairs of glands are present near sternals 2 and 3, a condition not known from other parasitiform larvae. The tritosternal branches are separate and weakly developed, each with a single pair of barbed setae and a pointed tip. The latter structure is replaced by a second pair of tritosternal setae in the post-larval instars. As in larval Phalangiacarus brosseti ( Coineau, 1973) and Panchaetes dundoensis ( Naudo, 1963) , legs IV are represented by unsegmented vestiges. Vestigial legs IV in the larva are unknown for Ixodida and Mesostigmata, but have been described for some primitive Acariformes ( Travé, 1976) and Ricinulei ( Pittard and Mitchell, 1972). They have also been observed in larval Allothyridae (suborder Holothyrida ) (Kethley, pers. comm.).

Legs. Segmentation. Leg segmentation in the larva is simple. All legs examined show a single trochanter, undivided femur (basifemoral scissure absent), and divided tarsus (basitarsal scissure well developed) ( figure 2 ). Trochanters III -IV and femora, tibiae, and telotarsi I are divided in the adults ( Van der Hammen, 1966). The pretarsi of legs II -III carry a pair of well developed claws and two pairs of setae. Pretarsi I with claws similar in shape and size to those on legs II -III, but lacking pretarsal setae.

Setation. Setation patterns in the post-larval instars appear to be too variable to allow worthwhile comparisons with other taxa ( Van der Hammen, 1966). However, the leg setation in the larva is relatively consistent ( table 1 ), and does allow some comparisons. The coxal setation pattern is unusual in the presence of a small anterior dorsal seta on coxae I -II positioned on a small, elongated tubercle ( figure 7 ). The overall coxal setation pattern of 3-5-3 (including the dorsal setae) is notably richer than any observed in other parasitiform larvae (2-2-2; in some Ixodidae 3-3-3).

Non-tarsal segments. Trochanters of all legs with seven setae each. Starting with the femora and extending towards the tarsus, the setal complement on segments of legs I is much larger than that for legs II -III. For femora I, this pattern appears to include at least six whorls of setae, compared to a maximum of two to three in other Parasitiformes . Femora II -III each carry elements of probably four whorls, including 4 ad, 4 pd, and one median unpaired (md) dorsal setae. An unpaired median dorsal seta is also present on tibiae I -III, but not on the genua or on tarsi II -III. It has not been reported in these positions for other larval Parasitiformes or for post-larval Mesostigmata. Trochanters and femora III carry no setae in a pd position. This most likely has a functional explanation. Given the observed position of legs III relative to the body, these surfaces may not require any sensory equipment. Genua I carry fi ve or six whorls of setae and tibiae I at least seven, but both genua II -III and tibiae II -III carry only three whorls. Complete leg formulae are presented in table 1 .

Tarsi I ( figure 8 ). As usual for Parasitiformes , the setation of tarsus I is very complex, without obvious patterns of distribution. No attempts have been made to homologize setae across instars, among different opilioacarid taxa, or among different parasitiform suborders. Even so, a few comments can be made. The female carries two porose setae/solenidia subcuticular in a cavity in the tarsus ( figure 9 , arrow). Similar subcuticular setae have been documented on tarsi I of Holothyrida , Ixodida (part of Haller’s organ), and Ricinulei (on both tarsi I and II). These subcuticular setae are present in all instars of Ixodida , but absent in larval O. texanus ( figure 8 ), larval Allothyridae (Kethley, pers. comm.), and Ricinulei ( Pittard and Mitchell, 1972). This suggests that the absence of subcuticular setae in all instars of Mesostigmata may well represent an ontogenetic shift.

Tarsi II -III ( figure 10 ) show a major departure from the pattern observed in other Parasitiformes , by having three complete whorls of setae on each basitarsus (only one in all other Parasitiformes ). The telotarsi of larval O. texanus include at least fi ve complete whorls for a total of at least eight. Allothyrid larvae may have fi ve or six whorls ( Klompen, 1992), but the remaining Parasitiformes show signs of only four whorls on tarsi II -III ( Evans, 1969).

Despite their relatively large size, leg setation patterns in larval and adult O. texanus never feature whorls of eight setae, as noted for larval Allothyridae ( Klompen, 1992) . Instead the whorls of six setae known from larval Ixodida and all instars of Mesostigmata are retained. Despite this, the overall number of setae per segment is generally higher in these larvae than in any other larval Parasitiformes , including larval Allothyridae . The difference reflects an increase in the number of setal whorls per segment. A plot of number of whorls per segment vs segment length ( figure 12 ) suggests a functional explanation. Assuming segment length as an approximation of surface area per segment, surface area and number of setae are clearly correlated, possibly to allow effective sensory coverage.

Non-setal cuticular structures. In addition to setae, the legs carry two additional types of cuticular structure. The poor condition of the two legs I available did not allow an accurate assessment of the presence and pattern of such structures on the basitarsus and non-tarsal leg segments of leg I. The following is therefore restricted to legs II -III. The fi rst type of structure is fairly large, resembling a lyri fi ssure. These structures are present on the femora (basal, ventral, at the level of the basifemoral scissure in the post-larval instars), basitarsi (one basal, antero-lateral; another distal, ventral), and telotarsi (distal, postero-dorsa l) ( figure 11 ). This distribution resembles that of the`Tarsal Slit Sense Organs’ as described by Hess and Vlimant (1986) for adult ixodid ticks and of the slit organs or lyrifissures in postlarval Mesostigmata ( Evans, 1992). The presence of the basal structure on the basitarsi, which is not added until the nymph in Ixodidae ( Hess and Vlimant, 1986) , suggests an ontogeneti c shift relative to Ixodidae . The second type of cuticular structure is much smaller. It appears round with a diagonal line, suggesting two fl aps closing off an opening. These structures are present dorsally on trochanters, genua, tibiae, and basitarsi II, and on telotarsi II -III; antero-lateral, between the antero-lateral and antero-ventral setae, on femora II and on genua and tibiae II -III; postero-lateral, between the postero-lateral and postero-ventra l setae, on trochanter III, genua, tibiae, and basitarsi II -III; and ventral on femora II. In nearly all cases single structures are present in each position, but three to fi ve are present dorsally on basitarsi II and telotarsi II -III ( figure 11 ). This distribution (and general shape) is remarkably similar to another type of structure described by Hess and Vlimant (1986) for Ixodidae , the`fi ssures’. These authors suggest that fi ssures are not glands but true sensillae, perhaps equivalent to the campaniform sensillae of insects. A more detailed study of these structures would be needed to determine their function. The`glands’ on the legs of some Mesostigmata (e.g. Athias-Henriot, 1977) may be homologous to these structures.

Figures

FIGS 6, 7. Opilioacarus texanus (Chamberlain and Mulaik), larva: (6) dorsal view; (7) ventral view. Hypothesized segmental designation indicated in roman numerals. Arrow: structure of unclear nature.

FIG. 1. Opilioacarus texanus (Chamberlain and Mulaik), prelarva. Structures indicated by dashed lines are larval. Abbreviations: s.f.: sejugal furrow; δ: ecdysial line.

FIG. 2. Opilioacarus texanus (Chamberlain and Mulaik), larva. General body shape and body/leg dimensions.

FIGS 3-5. Opilioacarus texanus (Chamberlain and Mulaik), larva: (3) gnathosoma, ventral; (4) chelicera, anterior view; (5) palp, postero-lateral view.

FIGS 8, 9. Opilioacarus texanus (Chamberlain and Mulaik), distal part tarsus I: (8) larva; (9) female. Sensillae presumed to have only mechanoreceptor functions are not fully drawn, but are indicated by circles showing their position. Arrow: subcuticular setae.

FIGS 10, 11. Opilioacarus texanus (Chamberlain and Mulaik), larva, postero-dorsal view: (10) tarsus III, basitarsus and telotarsus III; (11) leg II sensillae and glands.

FIG. 12. Opilioacarus texanus (Chamberlain and Mulaik), larva. Regression of number of setal whorls on the length of the leg segments.