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Revista chilena de anatomía

versión impresa ISSN 0716-9868

Rev. chil. anat. v.19 n.3 Temuco dic. 2001

http://dx.doi.org/10.4067/S0716-98682001000300009 

MUSCULAR SYSTEM OF THE Amblyomma americanum  LARVAE 
(ACARI: IXODIDAE)

SYSTEMA MUSCULAR DE LA LARVA DE Amblyomma americanum (ACARI: IXODIDAE)

María E. Casanueva

Departamento de Zoología, Universidad de Concepción, Chile.
This research was supported by DIUC Project Nº 97.113.041-1.0, Universidad de Concepción, Chile.

SUMMARY: The muscular system of Amblyomma americanum larvae from the morphological and functional point of view is studied.  The capitulum is moved by four muscles: two depressors and two levators. Chelicerae have three muscles: retractor, flexor and digit extensor. Each segment of the palp presents two muscles - flexor and extensor - which permit the lateral movements of the palp. Legs have a pair of muscles (flexor and extensor) with opposing action, related to each segment; coxae present two series more of muscles, the abductor and the adductor. The most evident systems of the body are dorso-ventral and they are inserted in the ventral side of the body.

KEY WORDS: 1. Muscular system; 2. Larvae; 3. Amblyomma americanum.

INTRODUCTION

Ticks are one of the most important arthropod groups from a medical and veterinary point of view. The ixodids are large, hematophagous and ectoparasitic mites, which can produce infection in man and animals, like viruses, rickettsiae, bacteria, anaplasm and filariae.

Amblyomma americanum, the lone star tick, is among the more economically important species because it is capable of transmitting Rocky Mountain spotted fever. This species occur in the states of USA bordering the Gulf of Mexico, Jamaica, Brazil, Colombia, Paraguay, Ecuador, Uruguay, Peru and Chile, and its larvae have been found on a wide range of hosts (Bishop & Trembley 1945).

In recent years, there are been progress in the study of fine structures and physiology of ixodid ticks. Several studies have been published on the external and internal anatomy, histology, chaetotaxy and geographical distribution of different ticks'species (Williams 1905, Allen 1905, Bonnet 1908, Robinson & Davidson 1913-1914, Douglas 1943, Bishop & Trembley, Dinnik & Zumpt 1949, Mitchell 1957,

Clifford & Anastos 1960, Gregson 1960, Till 1961, Sonenshine 1970, Chow & Lin 1972, Balashov 1972). However, there has been abandonment of fundamental studies of basic structures and function of these animals posteriorly.

The muscular system is highly developed in adults of Ixodidae and it has been the subject of discussion in most of the publications dealing with tick anatomy (Robinson & Davidson and Douglas), but with a single exception (Estrada-Peña et al., 1982) the existing descriptions do not include characteristics such as function and number of muscles in ticks larvae. According to Estreda-Peña et al. who studied the muscles of Rhipicephalus sanguineus, it is possible that the muscles of the idiosoma, legs, chelicerae and palps could be very similar in different families of Ixodida, showing variation only in the length of the muscles rather than in their relative position. Therefore the purpose of this paper is to give an account of the normal distribution, function and number of the body and leg muscles in larvae of Amblyomma americanum.

MATERIAL AND METHOD

All studies were done using larvae of Amblyomma americanum (Linne, 1758) reared at the Acarology Laboratory, The Ohio State University, Columbus-Ohio.

Specimens  for muscles preparations were killed in cold or warm alcoholic Bouins for 24 hours at room temperature, stored in 70% alcohol or kept in 95% EtOH for 30 minutes, cleared in carbo-xylene, for 1 hour and, finally mounted in resin (Pyccolyte mounting media). To obtain the legs in a flexting position the larvae were first killed in 8% glutaraldehyde, for 90 minutes.

The larval ticks were examined with a dissecting microscope or a compound microscope and the drawings were made with the aid of a camera-lucida. Fixed specimens were mounted for dissection purposes. Other specimens were fixed in Bouins, for 24 hours. Both dissection and observations were carried out in  concavity slides using immersion oil as temporary mounting fluid.

Some in vivo examinations were made in order to see the direct correlation of a given body movement with a corresponding sequence of muscle contraction. For this purpose some larvae were affixed to concavity slides with a double-sticky tape and tape water was used as the temporary mounting fluid.

The terminology applied to the morphological features and muscles of the larvae is the same used by Balashov, Sonenshine, Dinnik & Zumpt and Estrada-Peña et al.

RESULTS

Capitulum musculature: The capitulum moves only in the ventral plane by the action of four muscles: two depressors and two levators which are antagonistic muscles.

Palp musculature: The extrinsic musculature of the palp includes palp abductor or flexor (plp abd) that originates on the pedipalp coxa and on the subcheliceral shelf, and palp adductor or extensor (plp add) originated on the palp coxa. On the other hand, the intrinsic musculature consists of two major groups of fibers that originate on the genua and femur and they flex the tibia-tarsus (Ti-Ta flx) (Fig. 1). The contraction of the flexor muscle deflects the entire palp in a lateral direction while the extensor by its action in the opposite direction restores the palp to its normal position.  The terminal segment (tibio-tarsus) receives only the insertion of the muscles, which are contained within the femur and genua.


Fig. 1. Larva of A.  americanum. Ventral aspect of the gnathosoma diagram.

An identical palp musculature occurs in Rhipicephalus sanguineus (Fig. 2) and shows that the development of the cornua is not a way to increase the surface area of muscles insertion.


Fig. 2. Larva of R. sanguineus. Ventral aspect of the gnathosoma diagram.

Leg musculature: Like the palps the musculature of legs consists of a pair of muscles, which are related to each segment and present opposite movements.  The insertion and origin of the muscles in each  leg's segment  are summarized in Table I.

On Fig. 3 it is possible to distinguish the cuticular anatomy of coxa 1, in a dorsal view, showing the large postero-media apodeme (apd).  The anterior-posterior movement, that is protaction and retraction, is acomplished by the opposite muscles: the trochanter protractors (Tr prt) and retractors (Tr retr) (Fig. 4). In addition, there is one basal tergocoxal (Trg Cxl) and two distal tergocoxal muscles (not shown), which probably have function in generating hydrostatic pressure for leg extension.


Figs. 3 and 4.  Larva of A. americanum. Dorsal aspects of coxa I diagrams.

Table I. Insertion and origin of the muscles on segments of legs in A. americanum larvae

Segment Muscle
Insertion
Origin

Pretarsus (Ptr) lev "near base of claws" Dorsal proximal (basal)surface tarsus
  depr Basal stalk of pretarsus Dorsal basal surface of tarsus and distal dorsal surface of tibia
       
Tarsus  (Ta) flx Ventral basal margin of tarsus Dorsal basal half of tibia and distal dorsal third of genu
       
Tibia (Ti) flx Ventral basal margin of tibia Dorsal basal half of genu and distal dorsal third of femur
       
Genu (Ge) flx Ventral and lateral basal margin of genu Dorsal middle third of femur and trochanter (?)
       
Femur (Fe) ext Dorsal basal margin of femur Dorsal margin of trochanter
  flx Ventral basal margin of femur (?) Ventral and ventro-lateral basal half of trochanter
       
Trochanter (Tr) retr (flx) Ventral basal margin of femur Dorsal basal surface of subcoxa
  prt (ext) Dorsal basal margin of femur Basal surface of subcoxa

From the coxa originates the extensors of the femur (Fe ext) and the femoral flexors (Fe flx) originate in the trochanter (Fig. 5). The muscles inserting on the genua, tibia and tarsus are all flexors and not extensors (Fig. 6). The extension of these leg segments must be accomplished  by hydrostatic pressure, as is true in other arachnids. This observation is not in agreement with published statement on leg musculature on other Ixodids.


Figs. 5 and 6. Larva of  A. americanum.  Fig. 5. Dorsal aspect of coxa and trochanter I diagram. Fig. 6.  Lateral aspect of leg I diagram.

The musculature of the terminal segment, pretarsus, is typical of Arachnida. There is a pretarsus levator (Ptr lev) that reaches the ambulacrum and a pretarsus depressor (Ptr depr) that flexes the claws.

Opisthosoma musculature:  For comparison purposes a generalized pattern of muscles scars or sigillotaxy in Mesostigmata mites is shown in Fig. 7. Note the small number of opisthosomal muscles which are dorso-ventral muscles concerned with hydrostatic pressure and with opening the anus.


Fig. 7. Sigillotaxy of Mesostigmata diagram. 1.»Direct gnathosomal muscles»; 2 and 3. Cheliceral retractors; 4. Parasaggital suspensors; 5. Leg muscles (direct); 6 and 7. Lateral suspensors; 8. Anterior antiaxial suspensors; 9. Posterior antiaxial suspensors; 10. Anterior opisthosomals; 11. Opithosomal tergoternals; 12. Anal muscles.

Muscles scars are not apparent on the opistosoma of the ixodid larva but tendons of the muscles in clear specimens are obvious.  The pattern of the dorso-ventral and anal muscles is shown on a dorsal (Fig. 8) and a ventral (Fig. 9) view of  Amblyomma americanum larva. All muscles are inserted in the ventral side of the body.


Figs. 8 and 9.  Larva of A. americanum.  Fig. 8. Dorsal aspect of the opisthosomal sigillotaxy diagram. Fig. 9. Ventral aspect of the opisthosomal sigillotaxy diagram.

DISCUSSION

Balashov suggests that the adult tick body musculature is formed by several dorso-ventral muscle groups (marginal, genital and anal). In  A. americanum larva the muscles of the body are also dorso-ventral, but this larva does not have the genital muscle groups. The most developed muscle group is the marginal; their presence is clearly indicated by the external marginal discs in the upper and lower surface of the body.

Muscles that originates on the body wall may have two distinct functions. The dorso-ventral muscles and certain anal muscles are attached at either end to the body wall or immovable sclerites. The movement of these muscles gives the body of the larvae much of their form and shape and develops interanal body pressure (hydrostatic presure), which apparently acts to extend the legs segments (Balashov).

Each segment of the palp of the larva of A. americanum presents bundles of flexor and extensor muscles, which permit only lateral movements. This result disagrees with those presented by Estrada-Peña et al. because they mention that the first palpal segment  of the larva of  R. sanguineus has three muscles and the following have only two muscles. It was impossible to find three muscles in the first palpal segment of the A. americanum larva. These authors, probably, identify as a third muscle in the first segment of the palp one muscle which runs from the body wall and is inserted on the base of the palp's coxa. However, this muscle belongs to the dorso-ventral body muscle groups and it does not have a role in the palp movement.  Estrada-Peña et al. also say that the chelicera can be protracted and retracted by "a common oscyllator system" but this system is not present in larvae of A. americanum since they have three retractile muscles, which are easy to observe and identify.

The leg musculature is apparently constant in all acarids. Mitchell studying the muscular system in legs of some aquatic mites found that the segments are flexed by muscles that insert on the basal margin of the respective segment and originate in the anterior segment to their insertion. The results of this study also show that the legs of A. americanum larvae present the same pattern of origin and insertion. In general, it is possible to mention that the tick larva presents legs which resemble very closely the arthropod type with telescoping segments and intersegmental musculature of two types: flexors and extensor muscles.

Finally, it is important to remark that more studies related with the muscular system in larvae of different species of ticks or other mites are necessary to understand their locomotory adaptations as well as the similarities or differences between the different stages of development.

ACKNOWLEDGMENTS

Special thanks to Dr. Donald E. Johnston (deceased) for review and comments on this manuscript.

RESUMEN: Se estudia la morfo-funcionalidad del sistema muscular en larvas de Amblyomma americanum. Cuatro músculos, dos depresores y dos elevadores, mueven el capítulo. Los quelíceros presentan tres músculos: retractor, flexor y extensor. En cada segmento de los palpos existen dos músculos - un flexor y un extensor- que  le permiten los movimientos laterales. Las patas poseen un par de músculos de acción opuesta (flexor y extensor) en cada segmento; las coxas además tienen un par de músculos abductores y aductores. La musculatura más evidente del idiosoma es dorso-ventral, que se encuentra inserta en el lado ventral del cuerpo.

PALABRAS CLAVE: 1. Sistema muscular; 2. Larvas; 3. Amblyomma americanum.

Dirección para correspondencia:
Prof. Dra. María E. Casanueva
Departamento de Zoología
Universidad de Concepción.
Casilla 160-C
Concepción, CHILE

E-mail: mcasanue@udec.cl

Recibido : 11-07-2001
Aceptado: 05-09-2001

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