the structure and evolution of water mite mouthparts

The Structure and Evolution of Water Mite Mouthparts

RODGER MITCHELL' University of Florida. GainesviUe, Florida

Although the differences between oral appendages cursorily described by Norden- skiold (1898) have been referred to in every important general work on water mites no one has yet made a detailed com- parison of the structure and function of water mite mouthparts. This study of the mouthpart exoskeleton and musculature is an attempt to supply those data and to explain the evolution of the mouthparts. It turned out that the mouthparts of some water mites are indistinguishable from the terrestrial Trombiculidae and Trom- bidiidae, while other water mites appeared either more primitive or more advanced than the previously mentioned assemblage. Hence, the higher terrestrial Trombidi- formes must be considered along with the water mites. An adequate sample of water mites was available but the data on terrestrial mites was not an adequate sample of the groups involved.

Because the oral appendages are supported by a capitulum which also supports all the muscles that move the appendages it is possible to consider the mouthparts as a functional unit and to understand its functions without referring to the anatomy of the body mass. The endings of the tracheae and oral gland ducts are among the mouthparts and are described, but not traced backed into the body mass proper.

Several important studies of water mite mouthparts have been published and three of these include information on internal anatomy. Schaub (1888) on Hydryphan- tes, Schmidt ('35) on Hydrodroma, van Vleet (1897) on Limnochares, and, most important, Nordenskiolds ( 1898) brief comparative study. The latter work out- lines most of the conclusions reached below and is a fine example of the usefulness of comparative anatomy in reaching an understanding of mite phylogeny. Fresh dissections of all the genera considered

in these published studies have proven the data of the above authors to be generally accurate and reliable but it is not practical to cite these authors point by point in the following descriptions.

MATERIALS AND METHODS

Most of the data were taken from microscopic mounts of materials in which various elements were exposed or dissected out prior to staining and mounting (for notes on the matter of dissection see Mitchell, '62). General notes made during dissections were checked against microscopic preparations and then a list of all the muscles was made (given as the Appendix) and a second series of animals were dissected to verify the presence or absence of each muscle. Every attempt was made to verify each point in several preparations but with such small animals it is not always easy to determine muscle insertions precisely. However, the consistency of the preliminary notes with subsequent check- ings suggest that the errors are probably few and minor.

The spectrum of forms dissected in- cluded typical examples of all the primitive families assigned to the superfamilies Hydrovolziae, Hydrachnae, and Limno- charae. In the Hydryphantae all but some of the divergent families of the tropics were available. The remaining "advanced families are very poorly sampled but there is a marked uniformity in the mouthpart exoskeleton of these families and a broader sampling of the families might have con- tributed little to the study.

The forms examined are listed by superfamily below. Where the species name is not given the species is, at present, unde- scribed. Since the external structure of

1 A portion of this work was supported through Grants-in-Aid from the Edwin S. George Reserve of the University of Michigan.

41

42 RODGER MITCHELL

the mouthparts among the species of a genus is quite uniform the lack of a species name is not ambiguous for work at this level.

Coverage (Classification according t o Viets, '56)

Hydrovolzia gerhardi Mitchell Hydovolziae -

(Fam. Hydrovolziidae)

Hydrachna stipata Lundblad (Fam. Hydrachnidae)

Hydrachnae -

Limnocharae - Limnochares aquatica (Linnaeus)

(Fam. Limnocharidae) Eylais sp. (Fam. Eylaidae) Calonyx ovata Marshall

(Fam. Protiziidae) *Partnuniella thermalis Viets

(Fam. Protziidae) Hydryphantae -

*Thyas barbigera Viets (Fam. Thasidae) Trichothyas muscicola (Mitchell)

(Fam. Thyasidae) *Marshallothyas asopos Cook

(Fam. Thyasidae) Hydryphantes ruber (Geer)

(Fam. Hydryphantidae) H y d r o d r m a despiciens (Miiller)

(Fam. Hydrodromidae) Thermacarus nevadensis Marshall

(Fam. Thermacaridae) Lebertiae -

*Lebertia sp. (Fam. Lebertiidae) *Testudacarus americanus Marshall

(Fam. Torrenticolidae) Pionae -

Unionicola fossulata (Koenike) (Fam. Unionicolidae )

Najadicola ingens (Koenike) (Fam. Unionicolidae)

Limnesia sp. (Fam. Limnesiidae) Tyrrellia circularis Marshall

(Fam. Limnesiidae) Pima sp. (Fam. Pionidae)

* Arrenurus apetiolatus Piersig

Mouthparts of the species marked with an asterisk ( * ) were not fully worked out and unless otherwise specified in the appropriate text sections, the intrinsic muscles, but not the extrinsic muscles or

Arrenurae - (Fam. Arrenuridae)

tracheae, were worked out in the forms so designated.

Functional groups of muscles are com- pared in the text that follows without giv- ing the paths and attachments of each muscle. It proved to be much more con- venient to place all the descriptions of muscles in the Appendix at the end of the paper.

The anatomy of both Unionicola and Najadicola is described elsewhere (Mit- chell, '55a) and the extrinsic capitulum muscles are described for various Hydry- phantidae (Mitchell, '57) and Piersigia (Mitchell, '55b). With the exception of these genera the discussion that follows refers to data from fresh dissections of the above forms.

General description of the mouthparts

A cylindrical sclerite of compound origin surrounds the pharynx and provides articulations and attachments for the oral appendages. Dorsally there is a broad groove in which the chelicerae lie and laterally a socket provides the seat for the palpi (fig. 5). Muscles acting upon the pharynx originate on the inner dorsal wall of the capitulum whereas the lateral wall of the capitulum provides areas for the origins of muscles acting upon the basal palp segment. Thus, the capitulum functions to support the two pairs of appendages and to provide attachments for the muscles associated with feeding organs. As a general rule the form of the capitulum is closely determined by these functions and shows little or no elaboration inde- pendent of its skeletal functions.

The broad base of the capitulum lying posterior to the palp sockets is thought to be derived from the coxae of the palps and in Hydrachna there are separate postero- lateral lobes that fuse dorsalIy and ventrally to form a cylinder only at the level of the palps (fig. 5). But in all other mites the palp coxae are fully fused ventrally to form a half cylinder (fig. 15). Anterior to the palp insertions the capitulum forms a cylinder with the roof so modified as to form a pair of IongitudinaI grooves in which the chelicerae rest. As a rule the capitulum is narrowed at the level of the palps and drawn into an anterior snout-

WATER MITE MOUTHPARTS 43

like projection termed the rostrum or hypostome. This region is thought to involve the fusion of several sclerites but its com- position has not been determined.

Chelicerae rest on the dorsal surface of the capitulum so as to leave a space between the chelicerae and the capitulum (fig. 15). The mouth opens into the anterior portion of this space and the space extends posteriorly to the point where a membrane joins the chelicerae to the capitulum. This membrane is perforated by two pores through which digestive gland products pass and these fluids must flow the full length of the capitulum to reach the exterior. All the mites considered are either known or presumed to prey on other arthropods and so feeding habits are comparable throughout the group.

With this brief outline i t is appropriate to take up the components item by item.

Extrinsic capitulum muscles Free folds of the integument permit con-

siderable capitulum movement dorsally and laterally but there is little free play ventrally and consequently the postero- ventral capitulum margin approximately defines the hinge around which the capitulum moves. The plane of capitulum movement is vertical so that when the postero- dorsal margin of the capitulum is raised, the anterior tip swings out and downward. This movement is termed protraction. When the capitulum returns to the resting position, it is said to retract. The extrinsic muscles which mediate these actions originate on the dorsum of the body but the precise position of attachment is not rele- vant to this discussion and it is sufficient to say that the capitulum protractors originate dorsal or anterior to the level of their insertions. Retractors originate posterior to the level of their insertions. Water mites may bear as many as three retractors but there is never more than one protractor present.

Extrinsic capitulum muscles insert at one of three points on the posterior margin of the capitulum, a dorso-lateral insertion, a ventro-lateral insertion, and a lateral insertion. The protractor and retractor 1 insert on the ventro-lateral margin. Retrac- tor 2 inserts dorso-laterally and retractor 3 inserts laterally.

Only Eylais (fig. 6) possesses the full complement of extrinsic muscles and this sets the genus (and Piersigia according to preliminary work, Mitchell, '5%) aside from other water mites. The majority of the soft bodied red mites possess both retractor 1 and 2 (Hydrouolzia, Hydrachna (fig. l ) , Calolzyx (fig. 14), Hydrodroma, and Thermacarus) whereas the remaining forms possess but a single retractor. The divergent genus Limnochares possesses two retractors (retr. cap. 1, retr. cap. 3 , fig. 9). All the other genera retain only retractor 2.

Muscles of the palps The palps are 5 segmented grasping

organs that move in a vertical plane parallel to the long axis of the body. The segments are held together by a tight dorsal membrane but the ventral membrane is loose so that the segments telescope together and the movements of the segments produce flexion or extension of the appendage. These structural relationships are best illustrated in figures 17-22. Segments 1 and 2 are an exception for they are so tightly h e d together that they cannot move independently.

Food or other objects are grasped through the flexion of the palps and intrinsic flexor muscles that originate within the palps mediate this action. No muscles antagonize the flexors so extension must be a function of hydrostatic pressure dis- tending the folded ventral membranes.

The palp as a whole moves in a vertical plane that is determined by the two lateral articulations of segment 1 with the capitulum. Muscles attach to the base of the segment either above or below the axis of articulation and therefore elevate or depress the palp respectively, (eleu. p . 1 and depr. p . I , figs. 1 and 14). Both muscles are extrinsic to the palp and often originate as several separate slips on the postero- lateral wall of the capitulum. These muscles are always present and their placement was similar in all forms studied.

Hydrachna possesses a unique extrinsic muscle that inserts laterally on the base of segment 1 and must act to abduct the segment (abd. p . 1 , fig. 1 ) . The lateral articulation is absent in Hydrachna leav- ing one articulation that is situated exactly

44 RODGER MITCHELL

mesal to the insertion of the abductor. Adduction of the palp must be a function of hydrostatic pressure stretching out the lateral membrane between the capitulum and palp segment 1.

Palp segments 3,4, and 5 are acted upon by flexors and the insertions of these muscles are always ventrally placed on the base of the segment that is acted upon. Flexor 3 is absent in two of the forms studied, Partnuniella and Limnochres (fig. 9). There is considerable variation in the origins of these muscles.

The flexor of segment 5 (flex. p . 5 ) originates as several slips on the dorsal wall of segments 3 and 4 (figs. 6, 14, and 16-22) except in Limnochares (fig. 9) where it originates in segment 3 and in Hydrachna (fig. 1) where it originates dorsally in segments 2 and 3.

As a rule the flexor of segment 4 (flex. p . 4) originates dorsally in segment 2 (figs. 9, 14, and 16-22). The exceptions to this are found in the genus Hydrachna (fig. 1 ) where segment 1 is so inordinately enlarged as to provide areas for the origins of the flexors of both segments 3 and 4; and in Eylais (fig. 6) where the first slip originates in segment 2 and the second slip in segment 3.

Origins of the flexor of segment 3 (flex. p . 3) are quite variable. In Hydrachna (fig. 1) and Eylais (fig. 6 ) the origins are in segment 1. In Hydrovolzia (fig. 17), Themacarus (fig. 19), and Lebertia (fig. 20) at least one slip originates in segment 1 while other slips originate in segment 2. Hydrovolzia (fig. 17), Ther- macarus (fig. 19), the Protziidae (fig. 14), and the Hydryphantidae (fig. 18) have three slightly separated insertions of the muscles on segment 3 and these muscles must adduct, as well as flex, segment 3. This appears to be a set of homologous features. The remaining mites all have the muscle origins in segment 2 and all the slips inserting together on the base of segment 3 (figs. 16, 21, and 22).

Cheliceral muscles As a rule, the elongate cylindrical che-

licerae bear a cIaw at the tip end and muscles elevate and depress the claw. Move- ments of the claw, in conjunction with the protraction and retraction of the chelicerae

probably tears an opening in the body wall of the prey. The unsegmented chelicerae of Hydrachna (figs. 3 and 4) are the only exception. These are clearly piercing de- vices.

Movements of the chelicerae must be a simple muscle mediated protraction and retraction in Hydrachna for a dorsal groove of the capitulum (figs. 3 and 5) surrounds the chelicerae. Two pairs of muscles originate on the sigmoid piece or tracheae, and insert on the base of the chelicerae (prow. chel. 1 and 2, figs. 3 and 4) and these are the protractors of the chelicerae. Only one retractor of the chelicerae (retr. chel., figs. 1 and 4) is present.

Although the cheliceral muscles of the other mites are similar to those of Hy- drachna the action of the muscles is al- tered because the chelicerae articulate with the sigmoid piece. In Hydrachna the sigmoid piece is articulated (perhaps immov- ably attached) to the dorsal wall of the capitulum and is not attached to the chelicerae in any way but in all other water mites an antero-dorsal projection of the sigmoid piece engages the base of the chelicerae (figs. 7,10, 15, and 16). The opera- tion of the cheliceral complex is not a simple matter of protraction that can be interpreted from dissections. Instead the contraction of the cheliceral protractor would appear to lift the posterior extension of the sigmoid piece and the consequent rotation of the sigmoid piece around its articulation with the capitulum would cause the anterior tip of the sigmoid piece to push the chelicerae anteriorly. In Lim- nochares where the tips of the chelicerae are engaged by a locking groove of the capitulum (fig. 13) the only possible cheliceral movements are protraction and retraction. It is obvious that the cheliceral protractor must move the chelicerae by rotating the sigmoid piece in this instance. But in all the other mites studied the chelicerae lie freely on the capitulum and could be elevated as well as protracted when the cheliceral protractor contracts.

It appears that cheliceral movement in mites assigned to the super-families Hy- drovolziae, Limnocharae (fig. 15) (except for the families Eylaidae and Limnochari- dae) and Hydryphantae involves a com- bined protraction-elevation of the chelic-


eral tip mediated by the cheliceral protractor. But in Eylais (fig. 7) and all the advanced mites examined (superfam- dies Lebertiae, Pionae (fig. 16), and Ar- renurae) the chelicerae are in a more nearly vertical position and it appears that the dominant movement of the chelicerae is one of elevation of the cheliceral tip caused by a depression of the cheliceral- sigmoid piece articulation. That is clearly the case in Eylais (fig. 7) and in Unioni- cola (Mitchell, '55a) but it is not certain that protraction is negligible in other cases among the superfamilies listed above (e.g. Tyrrellia, fig. 16).

The cheliceral protractor is opposed by a retractor (retr. chel.) in all the forms examined except Unionicola (Mitchell, '55a), Trichothyas, and perhaps Thyas and Eylais. In the last two cases it was not possible to be absolutely sure that no muscle inserted on the chelicerae. When- ever the cheliceral retractor is present the muscle is comparable in placement and action to the situation described for Hy- drachna above (cf. fig. 1 with figs. 9 and 14).

The chelicerae are free to act separately in all water mites except those assigned to the families Limnocharidae (figs. 11-13) and Eylaidae. Both these groups have the chelicerae fused together mesally but the terminal claws remain separate and acted upon by separate pairs of antagonistic muscles.

Except for Hydrachna all the mites possess a movable cheliceral claw at the end of the cheliceral shaft. This claw articu- lates with the shaft by two lateral articulations and swings up and down in a vertical plane. Elevators and depressors of the cheliceral claw (elev. chel. cl., depr. chel. c l . ) are present in all the mites (figs. 7, 10, 15, and 16).

Terminus of the tracheae Anteriorly the two tracheae terminate in

simple stigmata lying in the membrane between and just over the base of the chelicerae. The tracheal opening is ob- scure and unmodified. It may be sealed off by a very fine membrane but there is no way to be absolutely certain of this fact in the material at hand. All the genera

investigated showed quite similar tracheal arrangements.

From the stigmata the two tracheae, lying side by side, pass ventrally between the chelicerae and enter subterminally on the posterior surface of the sigmoid piece (figs. 3, 7, 10, 15, and 16). A cavity runs through the sigmoid piece and opens into a typical trachea posteriorly. It would appear that the sigmoid piece is an elaborate sclerotization of the tracheal wall that secondarily assumes a role in cheliceral movement. Its usual form is shown in figure 15 and this is typical of all of the mites examined. In spite of the differences in the cheliceral protractor muscles and sigmoid piece action that characterize Hydrachna (fig. 3) there is no real differ- ence in arrangement of the stigma or tracheae.

Van Vleet (1897) argues that there is not a continuous passage through the sigmoid piece in Limnochares. There is a passage observable in sections (fig. 12) and so Van Vleet's technique for filling the tracheae with air was either faulty or else the passage in the sigmoid piece is bor- dered by membranes at either end. Such membranes might be difficult to discrimi- nate in either sections or whole mounts.

In Eylais (fig. 7 ) and Limnochares (figs. 10, 12) the tracheal terminus penetrates the mid-dorsal surface of the fused chelicerae but the pathway of the tracheae is no different from that seen in forms with separate chelicer ae .

Just posterior to the capitulum base the tracheae abruptly divide into a great mass of tiny tubes that weave about in the body tissues. Brown ('52) did not find tracheae in Trombicula and the report of tracheae in Blankaartia by Mitchell ( '62) is in error. The available data suggest that tracheae are not found in the Trombiculi- dae but they are present in the Trombidi- idae (e.g., Allothrombidium Henking, 1882).

Pha y n x From the opening of the mouth near

the tip of the hypostome the pharynx passes along the ventral wall of the capitulum where ligaments secure the pharynx to the capitulum. The pharynx is U-shaped or crescent-shaped in cross section with

46 RODGER MITCHELL

the dorsal wall concave (figs. 8 and 12). extensible the oral gland duct doubles back Muscles, which originate high on the lat- on itself to allow for capitulum extension. eral surfaces of the capitulum, insert on In other forms the path of the oral gland the concave dorsal surface of the pharynx duct is fairly direct to its opening just lat- and their contractions dilate the pharynx eral to the sigmoid piece. No variations by pulling the dorsal pharyngeal wall dor- were seen in the ducts as they passed sally (d i l . phar.). This dilation of the through the capitulum. pharynx draws any. available fluid into

DISCUSSION the pharynx from the mouth. Depression of the dorsal pharyngeal wall would then In most mites the feeding organs con- pump fluids out of the pharynx. The elas- sist of the two pairs of appendages and ticity of both dorsal and ventral pharyngeal numerous sclerites that have accessory walls must oppose the action of the phar- feeding and sensory functions but in the yngeal dilators. Parasitengona (as defined by Hughes, ’59)

Closing of the pharynx can also be medi- these elements are fused into a single ated by muscles attached to the dorso- compound sclerite, the capitulum, which lateral horns of the pharynx (figs. 7-8) provides skeletal support for the appen- and no really satisfactory term could be dages and their muscles as weU as for the found to apply to the muscle. It is often pharynx and pharyngeal muscles. termed a constrictor (Brown, ‘52) but this Among the mites examined in this study suggests that the muscles encircle the there does appear to be a general set of pharynx, instead all the muscles occupy adaptive trends involving the function of only one surface of the pharynx (flex. the palps, the chelicerae, and the pharynx. p h a ~ . ) . This muscle is found in all the These trends parallel, in a general way, Hydrovolziae, Limnocharae (Partnunia the current taxonomic arrangements al- could not be checked for this muscle), and though they are at marked variance with the Hydryphantae (except for Hydrodroma the present classification in many details. and Themacarus which lack the muscle). A rigorous testing of views on the phy- All the other forms lack this muscle and logeny of these mites is impossible until pharyngeal closure is entirely due to the there are more thorough and internally elasticity of the pharyngeal walls. consistent analyses of the evolutionary

When present the pharyngeal flexor con- trends in specific functions. The argu- sists of slips that interdigitate with the ments below are meant to develop an in- dilators of the pharynx (figs. 7, 8, and ternally consistent interpretation for the 15) but in Limnochares (fig. 10) there is evolution of mouthparts without reference a single slip situated posterior to the phar- to unrelated features. As such it cannot yngeal dilators. Its action is probably that be used independently as evidence of the of a valve. In all the other mites the relations between these mites but must be muscle serves to oppose the dilators by used in conjunction with other sets of flexing the dorsal pharyngeal wall. characters.

Van Vleet (1897) discusses various in- Aquatic mites are all derived from ter- terpretations of pharyngeal function and restrial mites and in the related terrestrial correctly interprets the pharyngeal passage mites the palp functions primarily as a (Schaub, 1888, had confused this point). sensory probe. Elongate segments allow The argument of Van meet with Michael a wide range of movement and compIex (1895) as to “valves” (i.e. flexor muscles setae on the palp tip sense the substances of the pharynx) was the consequence of on the substrate. Eylais (fig. 6) illustrates Van Vleet assuming that what he found a general form common to a probing and in Limnochares must also hold for Thyas sensing appendage but due to the fact that petrophila (now Trichothyas). The as- the basic capitulum form i s drastically sumption was incorrect. modified (c f . figs. 6 and 14) the palps of

Eyluis can press the prey to the anterior surface of the capitulum so the chelicerae can act to tear open the prey. Since chemo- receptors need not be on a probing appen-

Oral gland ducts In forms such as Limnochares (fig. 9)

and Themacarus where the capitulum is

47 WATER MITE MOUTHPARTS

dage or localized on the palp tips in an aquatic animal, it is not surprising to find that there are no elaborate setae tipping the palp or to find the palps of water mites secondarily modified into grasping organs.

Hydruchna (fig. 1 ) like Eykzis, uses the palps to press objects to the tip of the pharynx but does so with the pointed tip end of the segment that can obtain a pur- chase on rough surfaces. When a Hy- drachna drills oviposition holes in plant stems it first digs the palp tips into the substrate and then presses the capitulum tip to the plant so that the chelicerae may be brought into action. Feeding has not been described for this mite. The palp is modified from the typical trombidif orm pattern in a way that most certainly in- creases its effectiveness as a grasping device. Segment 1 (fig. 1) is very broad in diameter so that the insertions of muscles on its base are far removed from the axis of movement. The two muscles originating on segment 1 (flex. p . 3 and 4) occupy most of the cavity of the enlarged segment. All these modifications point to a clear grasping function for the palp.

Both Hydrachna and EyZuis represent divergent lines which have developed grasping palps in a way that is very different from any other water mite. Ordinarily, segment 1 is reduced to a mere collar im- movably articulated to the base of segment 2 and may not even bear muscle origins. Since the palp of these mites is movable only at the bases of segments 1, 3, 4, and 5 it must be viewed as function- ally four segmented. As a rule, objects are grasped between segments 2 and 4 (figs. 16-22) and often the flexor surfaces of these segments are toothed or convex. Among the mites of the superfamilies Lim- nocharae (fig. 14) (excluding the Limno- charidae and Eylaidae) and Hydryphantae the capitulum is so long as to project between the palps and palp action is not known in these groups. The appendages have not been seen in use and the structure of the palp does not clearly indicate any specific palp function. But mites of the superfamilies Lebertiae, Pionae, and Arrenurae do have a foreshortened capitulum that leaves the palp free to grasp the prey (fig. 16) and in the first two groups grasping modifications are commonly

found on the flexor surfaces of segments 2 and 4, but the Arrenurae are quite unique in having segment 5 opposed by a massive extension of segment 4 (fig. 22). The latter is a device for grasping an appendage of the prey whereas the Lebertiae and Pionae grasp the body of the prey.

The foreshortened capitulum is corre- lated with still another feature, the action of the chelicerae which was considered in detail above. The ripping and tearing action of the chelicerae is characteristic of mites with a foreshortened capitulum so it appears the change in capitulum shape results in alterations in the action of both the chelicerae and the palps.

Finally there is the loss of all the flexor muscles of the pharynx. It seems signifi- cant to note that in these mites of aquatic or very moist habitats the oral glands are larger than in any other group of mites (Bader, '38 and Hughes, '59). Perhaps external digestion by the secretions of these glands is favored in moist situations and, indeed, becomes so effective as to permit a reduction in the efficiency of the pharyngeal pump.

Certainly the prey's tissues could be reduced to the proper fluidity if the oral gland secretions were introduced through a small hole pierced in the prey as is certainly the case with both Hydrachna and Limnochares. Yet there is a clear ten- dency for the chelicerae to take on a tearing type of action in all the more advanced aquatic mites. These mites apparently tear relatively large holes in the prey, pass oral gland secretions into the wound, and then the very simple pharygeal pump draws in only very fluid nutrient. Perhaps it is impossible to feed in a terrestrial situation if a large wound is made and impossible to reduce food to a thin fluid. In water these things may be possible and allow the pharyngeal pump to be reduced. Admittedly this scheme is only an attempt to rationally assign functions to the structures observed and to account for the evolutionary trends.

All the trends just discussed parallel each other and can form the basis for proposing a phylogenetic sequence and there are 4 natural groups into which the various families fall.

RODGER MITCHELL 48

1. The superfamily Hydrachnae. There trial forms) which lies under a dorsal ex- is little these mites have in common with tension Of Segment 4. other water mites and they may, indeed, Although this information indicates a be quite unrelated. Both appendages, the considerable degree of uniformity in the palps and the chelicerae, are completely above group much more data are needed different from any other water mite in on the two terrestrial families to test the

extent of correspondence between the ter- both musculature and function. The pos- restrial and aquatic groups. tero-lateral pair of lobes of the capitulum 4. At the highest level of specialization Seem to be evidence that fusion Of the the flexor muscles of the pharynx are lost coxal bases is not as complete as in other and at this level are found all the so-called water mites. If the Hydrachnae are related “advance$ water mites as well as one fam- to the stock that gave rise to water mites ily of “primitive” mites (sometimes called the relationship is very distant indeed. “red mites”), the Hydrodromidae. The 2. All succeeding groups have the PalP highly adapted aquatic forms that deserve

coxae fully fused and the first palp seg- to be called “advanced” are assigned to ment very greatly reduced. At this level the superfamilies Lebertiae, Pionae, Axo- the first palp segment does have muscles nopsae, Mideopsae, Krendowskiae, and originating on its inner surface. The cap- Arrenurae and they are a rather closely itulum is generally elongate so that the related assemblage. Internally the mor- chelicerae tend to move in a horizontal phology of the mouthparts of these forms plane and the palps are not highly modi- is uniform (except for Lebertia) but there fied. The flexors of the pharynx are vari- are some secondary specializations in capi- able in their development. There seem to tulum and palp structure in several fam- be three very divergent lines in this group- ilies. Generally, the capitulum axis is ing; (A) the Hydrovolziae which are not rotated so that the pharyngeal and chelic- secondarily specialized in any way, (B) the eral axes are nearly vertical (see Unioni- Thermacaridae that lack pharyngeal flex- cola in Mitchell, ’55a). The chelicerae are ors, and (C) the highly modified Eylaidae. often greatly foreshortened, and this is Although the eylaid palp is a grasping regularly accompanied by great changes organ and the capitulum is foreshort- in the proportions and shape of the che- ened, these modifications are not accom- liceral claws. But within each superfamily plished in the same way as they are in there are unspecialized forms that hardly higher mites and Eylais retains a simple differ in general form from the example palp and pharyngeal musculature. Reduc- given in figure 16. tion of the palp size makes it impossible The first anomaly here involves the to place the Limnocharidae but the general Hydrodromidae that are clearly unrelated similarities of the Eylaidae and Limno- to the other mites of this group because charidae would seem to indicate a close of their elongate capitulum and curiously relationship. shaped palp. Both structures resemble

3. The next specialization is the elimi- most closely the mites at level 3 so it seems nation of muscle origins from palp seg- likely that the Hydrodromidae are a di- ment 1 which is accompanied by the ex- vergent line paralleling but unrelated to pansion of segment 2 which provides the other mites at this level. origins for the flexors of segments 3 and Lebertia is a troublesome exception 4. Both sets of pharyngeal muscles are among the very uniform “advanced mites present. The mites that share this set of for it clearly has all the characteristics of characteristics are the terrestrial Trombi- this level except for having the origin of culidae (Brown, ’52; Mitchell, ’62) prob- the flexor of segment 3 on segment 1. A ably the Trombidiidae (this placement is detailed study of the super-family Leber- provisional), and the water mite families tiae is clearly needed. Protziidae, Hydryphantidae, and Thyasi- dae. All these mites also have the fifth SUMMARY palp segment represented as a small lobe 1. Several interconnected trends seem (bearing highly modified setae in terres- to be shown among those water mites


least modiiied for aquatic life and the trends culminate in a highly specialized set of mouthparts that is common to the great bulk of the mites most highly adapted to aquatic life.

2. First the palp looses its chemotactic functions and, as it becomes modified into a grasping organ, the intrinsic palp muscles are reduced and modified. Coupled with this is a foreshortening of the capitulum that withdraws the elongate capitulum tip from between the palps as well as forcing the chelicerae to move in such a way as to tear rather than pierce the prey.

3. The fact that an extraordinarily developed set of oral glands is found in these animals and that the pharyngeal pump shows a progessive reduction in musculature suggests that external digestion may be especially effective in these animals. It is suggested that only an aquatic mite would be unrestricted by a feeding device that tears relatively large holes in the prey as well as requiring predigestion of the prey to liquefy the nutrients so that they could be drawn in by a very weak pharyngeal Pump.

4. It is believed that several steps in the perfection of this feeding mechanism are shown by various extant groups of water mites and that an internally consistent phylogeny can be based on the structure of the mouthparts.

ACKNOWLEDGMENTS

I am very much indebted to the late Philip F. Bonhag whose enthusiastic inter- est and professional integrity I've admired and whose advice and example have been valuable guides and an immense help to me.

APPENDIX

Muscles extrinsic to the capitulum protr. cap. (protractor of the capitulum) Origi-

nates on the dorsal body wall dorsal or anterior to the base of the capitulum and attached to the ventro-lateral marain of the

retr. capitulum base.

(retractor of the capitulum) Origi- nates on the dorsal body wall posterior to the base of the capitulum and attaches with the above muscle on the ventro-lateral margin of the capitulum base. (Sometimes two slips from widely separated origins are present, i.e.. Hydrachnu, fig. 1).

- cap. I

retr. CUP. 2 (retractor of the capitulum) Origi- nates with the posterior slip of the previous muscle but inserts dorso-laterally on the capitulum base (absent in Limnochares).

(retractor of the capitulum) Origi- nates or the ventral ligament and inserts on the center of the lateral margin of the capitulum base. (Present in Eykis, Limno- chares, and Piersigia.)

retr. cap. 3

Palp muscles abd. p. I (abductor of palp segment 1) Origi-

nates postero-laterally on the inner capitulum wall and attaches laterally to the base of palp segment 1. (Present only in Hydrachna. )

(depressor of palp segment 1) Usu- ally originates as several slips on the postero-lateral capitulum wall and attaches ventrally to the base of palp segment 1.

(elevator of palp segment 1) Usually originates as several slips on the postero- lateral capitulum wall and attaches dorsally to the base of palp segment 1.

(flexor of palp segment 3) Inserts ventrally on the base of palp segment 3 and may originate in palp segments 1 or 2. (See the text for variations and exceptions.)

(flexor of palp segment 4) Originates dorsally in palp segment 2 and inserts ventrally on the base of palp segment 4. (The variations are discussed in the text.)

(flexor of palp segment 5 ) Inserts ventrally on the base of palp segment 5 and originates dorsally in segment 3 but may also originate in segments 2 or 4. (The variations are discussed in the text.)

depr. p . 1

elev. p. I

flex. p . 3

flex. p . 4

flex. p. 5

CheliceTal muscles depr. chel. cl. (depressor of the cheliceral claw)

Originates dorso-posteriorly on the inner wall of the cheliceral shaft and inserts dorsally on the base of the cheliceral claw. (Absent in Hydrachna.)

(elevator of the cheliceral claw) Originates ventro-posteriorly on the inner wall of the cheliceral shaft and inserts dorsally on the base of the cheliceral claw. (Absent in Hydrachnu. Origin on the dor- sa l cheliceral surface in Limnochares.)

(protractor of the chelicera) Origi- nates on the postero-ventral surface of the sigmoid piece and inserts posteriorly on the ventral surface of the cheliceral shaft.

(protractor of the chelicera) Orid- nates on the trachea dorsal to the sigmoid piece and inserts on the posterior tip of the cheliceral shaft. (Present only in Hydrachna. )

(retractor of the chelicera) Originates with the posterior slip of reh. cap. 1 on the dorsal body wall and inserts on the lateral wall of the chelicera just anterior to the articulation of the chelicera with the sigmoid piece,

elev. chel. cl.

protr. chel. I

protr. chel. 2

retr. chel.

50 RODGER MITCHELL

Pharyngeal muscles dil. phur. (dilator of the pharynx) A series of

origins occur laterally along the roof of the capitulum and the slips pass ventrally to a series of insertions along the mid-line of the concave dorsal pharyngeal wall.

(flexor of the pharynx) Several slips lie on the dorsal surface of the capitulum and are attached to the dorsally projecting lateral margins of the pharynx. (The variations are discussed in the text.)

flex. phar.

LITERATURE CITED Bader, C. 1938 Beitrag zur Kenntnis der Ver-

dauungsvorgange bei Hydrachniden. Rev. Suisse Zool., 45: 721-806.

Brown, J. R. C. 1952 The feeding organs of the common “chigger.” J. Morph., 91: 15-51.

Henking, H. 1882 Beitrage zur Anatomie, Ent- wicklungsgeschichte und Biologie von Trombi- d ium fuliginosum Herm. Zeitsch. Wiss. Zool.,

Hughes, T. E. 1959 Mites, or the Acari. Athlone Press, London, 225 + vii pp.

Michael, A. D. 1895 A study of the internal anatomy of Thyas petrophilus, an unrecorded hydrachnid found in Cornwall. Proc. Zool. SOC., London, 1895: 174-209.

37: 553-663, PIS. 34-36.

Mitchell, R. 1955a Anatomy, life history and evolution of the mites parasitizing fresh water mussels. Misc. Publ. Mus. Zool. Univ. Mich., no. 89, 28 pp.

1955b Two water mites from Illinois. Trans. Amer. Micros. SOC., 74: 333392.

1957 Locomotor adaptations of the family Hydryphantidae. Abh. nat. Ver. Bremen,

- 1962 The musculature of an adult trombiculid mite, Blankaartia ascoscutellaris (Walch). Annals Ent. SOC. Amer. ( i n press).

Nordenskiold, E. 1898 Zur Kenntnis der Mor- phologie und Systematik der Hydrachniden. Act. SOC. Sci. Fenn., 24: no. 5, 75 pp., 2 pl.

Schaub, R. V. 1888 Wber die Anatomie von Hydrodroma ( C . L. Koch). Stitz. Acad. Wiss. Wien d. mathem.-naturw. CI., 97: 98-151.

Schmidt, U. 1935 Beitrage zur Anatomie und Histologie der Hydrachniden, besonders von Diplodontus despiciens. Zeitschr. Morph. i3kol. Tiere, 30: 99-176.

Viets, K. 1956 Die Milben des Susswassers und des Meeres. G. Fischer, Jena, vols. 2-3, 870 pp.

Van Vleet, A. H. 1897 On the mouthparts and respiratory organs of Limnochares hol- serkea Latreille. Diss. Leipzig, 41 pp., 1 pl.

35: 75-100.

PLATE 1

EXPLANATION OF FIGURES

Hydrachna stipata Lundblad

Lateral aspect of the mouthparts and extrinsic muscles showing all the components in their usual orientation but with the lateral walls of the palp segments and the capitulum basal to the palp removed to show papal muscles.

Ventral aspect of the capitulum and appendages with the floor of the capitulum removed on one side.

Mesal aspect of a capitulum split exactly through the midline and showing the sectioned pharynx and its muscles, and the medial aspect of one chelicera and its muscles.

Ventral aspect of the chelicerae in their normal relationship to each other and with the full complement of muscles illustrated on one side.

Dorsal aspect of capitulum with one palp and both chelicerae removed. Muscles are illustrated on only one side.

(Abbreviations and general muscle descriptions &e given in the Appendix.)

WATER MITE MOUTHPARTS Rodger Mitchell

PLATE 1

protr. cap '' kA 1 ,dil phar

P z ' 3

eleu p. I

flex. p. 4

igmoid piece

trachea

protr chel I

protr. chel. 2

dil. phar. / elev P. I

51

PLATE 2


Eylais sp.

6 Lateral aspect of the mouthparts and the extrinsic muscles showing their normal orientation. A section of the lateral wall of the capitulum has been removed from below the palp socket to show the extrinsic palp muscles. Lateral walls of the palp segments have been removed to show the intrinsic musculature.

Mesal aspect of a capitulum split exactly through the mid-line showing one of the fused chelicerae and the muscles of the pharynx and chelicerae.

Dorsal aspect of the pharynx and the floor of the capitulum on one side.

7

8

(Abbreviations and general muscle descriptions are given in the Appendix.)

52


PLATE 2

flex. p.

P. 4

5

nerve

7 protr. chel. I

dil. phar. u

53

PLATE 3


Limnochares aquatica Linnaeus

9 Lateral aspect of the mouthparts, their extrinsic muscles, and the dorsal shield showing their normal orientation. Only the lateral walls of the palp segments are removed. Extrinsic palp muscles, which lie within the capitulum, are shown by dotted lines.

Mesal aspect of a capitulum cut lateral to the sigmoid piece so as to show the path of the oral gland duct. All pharyngeal and cheliceral muscles are shown.

Drawings traced from sections illustrating cross sec- tional relationships at the levels indicated by arrows on figure 10.

10

11-13


54


PLATE 3

dorso-ventral muscles

I 0.5 mm. I

,elev. chel. CI orotr chel I

55

PLATE 4


Calonyx ovata Marshall

14 Lateral aspect of the mouthparts and their extrinsic muscles showing their normal orientation. The lateral walls of the palpal segments are removed to show the intrinsic palp muscles and the path of the extrinsic palp muscles in the capitulum is shown by dotted lines.

Mesal aspect of the capitulum split exactly through the mid-line with the mesal wall of the chelicera removed in order to show the muscles of the chelicera and the capitulum.

15

Tyrrellia circularis Marshall

16 Mesal aspect of the capitulum split exactly through the mid-line with the mesal walls of the chelicera and palp segments removed.


56


PLATE 4

0.l mm. U etev p. I

15. trachea

1 elev chel. cl.

sigmoid piece

I 6. protr. chel h elev chel. cI ,flex. p. 3

57

PLATE 5


Mesal aspect of the right palp showing the placement of the muscles. All scales indicate a length of 0.1 mm.

17 Hydrovolzia gerhardi Mitchell

18 Hydryphantes ruber (Geer)

19 T h a c a r u s nevadensis Marshall

20 Lebertiu sp.

21 Hydrodroma despiciens (Miiller)

22 Arrenurus sp.


58


PLATE 5

flex p. 3

flex.p.5

22 flex. p. 5

flex. p. 5 flex. p. 3 flex. p. 4 flex. p 3

59

the structure and evolution of water mite mouthparts

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