Pesq. Vet. Bras. 36(6):539-544, junho 2016
Movement anatomy of the gluteal region and thigh of the giant anteater Myrmecophaga tridactyla (Myrmecophagidae: Pilosa)1
Priscilla Rosa Queiroz Ribeiro2*, André Luiz Quagliatto Santos2, Lucas de Assis Ribeiro2, Tharlianne Alici Martins de Souza2, Daniela Cristina Silva Borges2, Rogério Rodrigues de Souza2 and Saulo Gonçalves Pereira2
ABSTRACT.- Ribeiro P.R.Q., Santos A.L.Q., Ribeiro L.A., Souza T.A.M., Borges D.C.S., Souza R.R. & Pereira S.G. Movement anatomy of the gluteal region and thigh of the giant anteater Myrmecophaga tridactyla (Myrmecophagidae: Pilosa). Pesquisa Veterinária Brasileira 36(6):539-5442016. . Laboratory for Teaching and Research on Wild Animals (LAPAS),
Brazil. E-mail: [email protected] FederalLocomotion University reveals of Uberlândia, the displacement Rua Piauí and s/n, behavior Umuarama, manner Uberlândia, of the species MG in38405-317, their dai- ly needs. According to different needs of the several species, different locomotor patterns are adopted. The shapes and attachment points of muscles are important determinants of the movements performed and consequently, the locomotion and motion patterns of living beings. It was aimed to associate anatomical, kinesiology and biomechanics aspects of the gluteal region and thigh of the giant anteater to its moving characteristics and locomotor habits. It was used three specimens of Myrmecophaga tridactyla, settled in formaldehyde -
patternsaqueous solutionof movement at 10% and and locomotion subsequently, of animals, dissected were using analyzed usual andtechniques discussed in gross in light ana of literature.tomy. The morphologicalAll muscles of characteristicsthe gluteal region of the and gluteal thigh regionof giant and anteater thigh thatshow influence parallel thear-
joint which the interpotent type biolever act. These morphological characteristics indicate rangement of the muscular fibers, being flat or fusiform. These muscles are formed in the
a greater predominance of amplitude and movement speed at the expense of strength. On andthe othershows hand, the need features of future such realization as osteometric of more index detailed and the studies observation in this subject. of giant anteater motion indicate the opposite, what reflects this animal lack of expertise in locomotor habits INDEX TERMS: Locomotion, kinesiology, biomechanics, giant anteater, Myrmecophaga tridactyla, Pilosa. RESUMO.- [Anatomia do movimento da região glútea e e movimentação dos seres vivos. Objetivou-se associar as- coxa de Myrmecophaga tridactyla tamanduá-bandeira pectos anatômicos, cinesiológicos e biomecânicos da região (Myrmecophagidae: pilosa).] A locomoção revela o modo de deslocamento e comportamento das espécies nas suas de movimentação e hábitos locomotores. Utilizaram-se três necessidades diárias. De acordo com as diferentes neces- espécimesglútea e coxa de doMyrmecophaga tamanduá bandeira tridactyla às suas características sidades das diversas espécies, diferentes padrões loco- - dos usando as técnicas usuais em anatomia, fixados macroscópica. em solução músculos são importantes determinantes dos movimentos aquosa de formaldeído a 10% e posteriormente, disseca realizadosmotores são e, adotados.por conseguinte, As formas dos e padrões pontos dede fixaçãolocomoção dos As características morfológicas da região glútea e coxa que influenciam os padrões de movimento e locomoção dos animais foram analisadas e discutidas à luz da literatura. 1 - Todos os músculos da região glútea e coxa do tamanduá 2 Received on December 8, 2015. culares, sendo planos ou fusiformes. Esses músculos for- Laboratory for Teaching and Research on Wild Animals (LAPAS), Fed- bandeira apresentam disposição paralela das fibras mus Accepted for publication on March 17, 2016. - mam nas articulações sobre as quais agem bioalavancas
*Correspondingeral University ofauthor: Uberlândia [email protected] (UFU), Rua Piauí, s/n, Umuarama, Uber indicam maior predominância de amplitude e velocidade lândia, MG 38405-317, Brazil. Master’s research supported by FAPEMIG. do tipo interpotente. Essas características morfológicas
539 Priscilla Rosa Queiroz Ribeiro et al.
540 de movimento em detrimento da força. Por outro lado, ca- performance of biological roles, such as obtaining food, de- da movimentação do tamanduá bandeira indicam o oposto, fenseand, consequently,and locomotion. it reflects on the functionality on the racterísticas como os índices osteométricos e a observação The shapes and attachment points of the muscles in the aos hábitos locomotores e sinaliza a necessidade da reali- bones are important determinants of movements perfor- zaçãoo que refletefutura dea falta estudos de especialização mais detalhados desse a esse animal respeito. quanto med in the different joints and therefore are determinants TERMOS DE INDEXAÇÃO: Locomoção, cinesiologia, biomecânica, of the locomotion and motion patterns of living beings. So, tamanduá-bandeira, Myrmecophaga tridactyla, Pilosa. knowing motion anatomy aspects, as well as kinesiology
INTRODUCTION shape and arrangement, points of muscles origin and in- sertion,and basic biolever biomechanics types, strength aspects, arms such and as muscular resistance fibers and The giant anteater belongs to Myrmecophagidae family that mechanical advantage of body segments, becomes crucial has three subspecies, and they are found in southeastern to understanding the animal movement. This article aimed to associate the anatomical, kinesiology and biomechanics silent and peaceful nature, in the wild, they are always alo- aspects of the gluteal region and thigh of giant anteater to Mexico, Central and South America (Nowak 1999). Solitary, its moving characteristics and locomotor habits. captivity they accept living together. Giant anteaters have ne, except in mating season or mother offspring, while in anatomical, behavioral and physiological adaptations con- MATERIALS AND METHODS cerned to feeding, which is consisted of ants, termites and It was used three male adult specimens of their eggs, and the larvae of beetles. They have long skull, Myrmecophaga tridac- tyla - tube like and long muzzle, relatively small eyes and ears, a lections of Laboratory for Teaching and Research on Wild Animals very long portable tongue, developed salivary glands and (LAPAS), Linnaeus from (1758) Federal that University belong to of the Uberlândia didactic and (UFU) scientific and from col the Laboratory of Anatomy of Federal University of Goiás Campus Specie of the Pilosa order, the giant anteater is listed as Catalão (UFG). This study was approved by the Ethics Committee they have no teeth (Medri 2003). - national Union for Conservation of Nature and Natural Re- a potentially vulnerableMyrmecophaga animal to extinction tridactyla by the Inter on AnimalThe animals use of used UFU were(Protocol settled 039/11) in formaldehyde and it is in aqueous accordance so- threat is mainly due to destruction of habitats in order to with Normative Instruction 03/2015 of IBAMA. - sources (IUCN 2011). extinction taining the same concentration of solution. Their preparation for analysislution at followed10% and the then anatomical preserved conventional immersed in techniques opaque vats propo con- giveLocomotion place to pastures reveals andthe monocultures,displacement fires,and poachingbehavior The basic kinesiology and biomechanics aspects observed mannerand roadkill of the (Takami species et in al their 1998). daily needs such as feeding, weresed by the Rodrigues form and (2005). fascicular arrangement of the muscles of glute- al region and thigh, and the set up biolever systems in the hip and to the different needs of the several species, different loco- - mating and escape (Densmore 1983). This way, according ment and locomotion patterns of the animals were analyzed and - discussedknee joints. in The accordance influences with of thethese proposals characteristics of Tortora in the & Grabomove- motor patterns are adopted. According to Oliveira (2001) structuralthe Myrmecophagidae features related do not to varioushave expertise types of about adaptation, the lo wski (2010) for these characteristics. suchcomotor as terrestrial, habit. Instead, climbing they and show digging. a mix Theof anatomical giant anteater and RESULTS AND DISCUSSION The giant anteater gluteal region consists of these muscles, nodes of the hands joints on the ground. When it feels in - walks with clenched fists and with the lateral portion and fundus, m. gemelli, m. quadrates femoral and m. obturator - m. gluteus superficiallis, m. gluteus medius, m. gluteus pro werfuldanger, claws. its natural reaction is to flee, gallopping somewhat tensor fasciae latae, m. biceps femoris, m. semitendinosus, disorderly, fighting only if forced, when then it uses its po- m.internus semimembranosus, (Table 1 and Figurem. abductor 1). The cruris thigh caudalis, muscles m.are gra m.- tor system are responsible for the locomotion diversity ob- cillis, m. pectineus, m. quadriceps femoris, mm. brevis lon- Toledo (1998) states that the variations of the locomo- gus and magnus adductors and m. sartorius (Table 2 and logical changes are related to the limbs mechanical ability Figure 2). served in modern mammals. For Oliveira (2001) morpho Table 1. Attachment points of the gluteal region muscles of giant anteater Muscle Origin Insertion
M. Gluteus medius Gluteal surface of ilium and iliac crest. Greater trochanter of the femur. M. Gluteus profundussuperficiallis IliumLateral body. sacral crest, crest. sacrotuberous ligament and iliac GreaterLateral sidetrochanter of the third of the proximal femur, of femur. cranial and distal to the gluteus medius. M. Gemelli Side surface of the ilium body, caudal to gluteus profundus. Medial surface of the greater trochanter of the femur. M. Quadratus femoris Ventral side of the ilium up to the ischial tubercle. Medial surface of the greater trochanter of the femur distal to the twin. M. Obturatorius internus Pubis and ischium, at the medial side edge of the obturator foramen. Greater trochanter of the femur.
Pesq. Vet. Bras. 36(6):539-544, junho 2016 Movement anatomy of the gluteal region and thigh of the giant anteater Myrmecophaga tridactyla (Myrmecophagidae: Pilosa)
541 All the muscles of the gluteal region and thigh of the -
giant anteater show parallel arrangement of the muscle fi anbers, important and they role are in or the flat balance or fusiform. between According strength to and Tortora mo- & Grabowski (2010) the fascicular disposition represents
lengthvement and amplitude. orientation Lieber of them & Bodine-Fowler have a considerable (1993) effect state onthat muscular all muscles function. are made The up relationship of muscular between fibers, and, muscle the
(how much the muscle can shorten) and this shortening architecture and muscular function is that the excursion strenght is proportional to the total physiological cross- velocity is proportional to the length of the fiber, while the
giant-sectional anteater area muscles, of muscular it infers fibers. that this animal shows gre- aterThrough amplitude the andshape movement and arrangement speed and of thelower fibers strenght, of the - se found in the gluteal region and thigh of the giant ante- since the muscles with fibers parallel arrangement, as tho lower amount of fascicles that span the entire length of the muscle,ater, when generating, compared thus, to penniform broader and muscle faster fibers, movements show a
with less strenght. This way, Hildebrand & Goslow (2006) point out that the maximum strenght a muscle can exert, is equalThe to muscles the contraction of the gluteal strength region of its and fibers, thigh multiplied of the giant by anteaterthe total numberform in ofthe fibers. joint and over them act interpotent type biolevers. Figure 3 shows the muscular insertion re- gions, in other words, the point of strenght application of these muscles, as well as the point of resistance, illustra- ting the type of established biolevers. Such kind of biolever Fig.1. Photography of the gluteal region muscles of giant anteater. found, also suggests predominance of amplitude and mo- A - superficial side view: SGM, superficiallis gluteus muscle; ImS, intermuscular septum; TFLM, tensor fasciae latae muscle; strenght application (muscular insertion) is closer to the B - deep side view: GeM, gemelli muscle; GMeM, gluteus medius vement speed at the expense of strength, since the point of muscle (far for better visualization of the deep muscles); GPrM, gluteus profundus muscle; MQFe,Table quadratus 2. Attachment femoris muscle. points of the rotationgiant anteater axis (joint) thigh musclesthan the resistance (the body segment Muscle Origin Insertion M. Tensor fasciae latae Thigh tuberosity. Fasciae latae and through this muscle into the
M. Biceps femoris Ischial tuberosity. Cranial part: fasciae latae and through this muscle in the lateral condyle of the tibia and fibular head. third of the crural fascia and common calcaneal tendon. M. Semitendinosus Ischial tuberosity. Middleproximal skull part surface of the cruralof the medialfasciae. third Caudal of thepart: middle tibia body and common calcaneal tendon.
caudal part in part of the pelvic symphysis. tibia body. Cranial part: medial condyle of the tibia. M. AbductorSemimembranosus cruris caudalis IschialThe two tuberosity, parts in the common ischial totuberosity semitendinous. and the MiddleCaudal part:part of proximal the fasciae surface crural. and medial skull of the M. Quadriceps femoris Retus femoris: acetabular caudal tuberosity. Tibial tuberosity. Vastus medialis: medial surface of the femur body. Vastus lateralis: lateral surface of the femur body. Vastus intermedius: lateral surface of the femoral body, common to the vastus lateralis M. Gracilis Superior pubis ramus and pelvic Medial skull surface of the middle third of the tibia symphysis, caudal pubic ramus. body and common calcaneal tendon. M. Adductor brevis Ischial ramus, close to the pelvic symphysis. Medial surface of the middle third of the femur. M. Adductor longus Ischial ramus, close to the pelvic symphysis. Medial part: medial and caudal surface and distal to femoral body. Lateral side: medial femoral epicondyle. M. Adductor magnus Ischial ramus, close to the pelvic symphysis. Side surface to the lateral epicondyle of the femur. M. Pectineus Superior pubis ramus. Middle surface of the medial third of the femur, distal to the adductor brevis. M. Sartorius Thigh tuberosity. Cranial surface of the tibia.
Pesq. Vet. Bras. 36(6):539-544, junho 2016 Priscilla Rosa Queiroz Ribeiro et al.
542
Fig.2. Photograph of the giant anteater thigh muscles. A - superficial side view: TFLM, tensor fasciae latae muscle; VLM, vastus lateralis muscle; CrPBFM, cranial part of the biceps femoris muscle; ACCM, abductor cruris caudalis muscle; StM, semitendinosus muscle; CPSmM, caudal part of the semimembranosus muscle; CPBFM, caudal part of the biceps femoris muscle; B - superficial medial view: GM, gracilis muscle; PM, pectineus muscle; SM, sartorius muscles; RFM, rectus femoris muscle; VMM, vastus medialis muscle; C - deep caudal-medial view: RFM, rectus femoris muscle; VMM, vastus medialis muscle; ABM, adductor brevis muscle; AMM, adductor- magnus muscle; CPSmM, caudal part of the semimembranosus muscle; D - deep cranial view: VLM, vastus lateralis muscle; VIM, vastus intermedius muscle; VMM, vastus medialis muscle; E - deep medial view: ABM, adductor brevis muscle; AMM, adductor mag- nosusnus muscle; muscle. CrPSmM, cranial part (deep) of the semimembranosus muscle; F - deep medial view: RFM, rectus femoris muscle; VMM, vastus medialis muscle; PM, pectineus muscle; ABM, adductor brevis muscle (bicaudal); CrPSmM, cranial part of the semimembra - the distal surface of the bone, as well as speed in the mo- - vement, when the opposite occurs, we observe slower and vorand the / or amplitude external resistance),and the movement forming speed, interpotent with loss biole of strength.vers, which, according to Tortora & Grabowski (2010) fa In contrast to what is shown in this study, where the The interpotent joints are the most commonly found in morphologicalless extended activity characteristics with high analyzed tension levels.indicate a greater the limbs. This type of biolever causes mechanical disad- predominance of amplitude and movement speed at the vantage because it has a greater resistance arm and smaller - - speed,expense indicating of strength, the a use study of slowerby Oliveira but more(2001), vigorous using oste mo- arm strength. According to Clair (1986) the proximal mus ometric index, pointed strength emphasis at the expense of cle insertion in the bone end, indicates greater excursion to Pesq. Vet. Bras. 36(6):539-544, junho 2016 Movement anatomy of the gluteal region and thigh of the giant anteater Myrmecophaga tridactyla (Myrmecophagidae: Pilosa)
543
patterns, as well as its movements. limitationAlthough seems it has to predominantly influence the slow giant movements, anteater activity Gam- baryan et al gallopping, although running is a secondary adaptation for these animals,. (2009) as state evidenced that the by giant the greater anteater proportion is able of of muscles in the forelimbs compared to pelvic. Farley & apud - ds walk at low speeds, trot at moderate speeds and gallop atTaylor higher (1991 speeds, so Ribeiro, the giant 2006) anteater state capacity that the of quadrupe galloping indicates its ability to perform movements at high speeds, although it is not the most common in its locomotor pat- tern. Another inference that can be made based on the mor- phology of the muscles of the gluteal region and thigh of the giant anteater is that a greater quantity and dimension, and
alongconsequently with the greater changes contractile of the lumbar capacity spine of of the this extensor animal, muscles of the thigh in relation to flexor muscles, is what,- tuations, a bipedal posture, being supported on the hind described by Endo (2009), allows it to assume, in some si that distinguish the Xenarthras. limbs and tail, what, according to Alho (1993) is a feature- tension, the gluteal muscles which are: the m. gluteus su- Fig.3. Schematic drawing of the strenght application points of the Two groups are responsible for conducting the hip ex gluteal region and thigh muscles and point of resistance in giant anteater. Rectangle, insertion region of the muscles of - pubic-groupperficiallis, m. of gluteus the thigh medius, muscles, m. thegemelli muscles and m.participating quadrates infemoral this movement that operate are: inm. thisbiceps movement; femoris, m. and semimembra the ischium- the gluteal region; Circle, insertion regions of the thigh mus nosus, m. semitendinosus, m. abductor cruris caudalis, m. vements.cles; Star, This resistance shown divergencepoint. in relation to movements gracilis and m. adductor magnus. These different groups of the hind limbs of the giant anteater when using different have muscular insertion, and therefore they show points morphological characteristic as a source of information, of strength application in different regions of the limbs, so - they also have different adaptations to the movement (Fi- comotor habit, and they show anatomical characteristics gure 3). relatedmay reflect to various the lack types of expertise of adaptation, of these such animals as terrestrial, about lo climbing and digging, as indicated by the same author. group, there is a greater adaptation for the performance Observing the motion of the giant anteater we notice According to Oliveira (2001), in the case of the gluteal that it has slow movements. Since this animal also has mor- phological characteristics that favor the amplitude and mo- theof rapid ischium-pubic movements, group what is isbetter more adaptedimportant to atmore the vigofinal- vement speed, it infers that this slowness in carrying out rousof the but animal slower start, movements, to promote what an isincrease more important in speed; atwhile the movements may occur mostly due to its large size and ea- beginning of locomotion during start, when the movement ting habits with low calories, having low metabolic rate and is slower and resistance is greater. This way, once again it body temperature, than the morphological characteristics is evident the diversity of movements features that can be of the limbs themselves. performed by the limbs of giant anteater. The presence of characteristics that indicate speed and body and the locomotion manner, are closely related to movement amplitude presented in this study, while other According to Hildebrand (1995) the structure of the increases linearly with the increasing speed, and the me- tabolicenergetic. waste According to move to a Ribeirogram of (2006)body mass the metabolicduring certain cost features, such as osteometric index show prevalence of distance, decreases with increased body mass. Since the strenght in the giant anteater moving, they reflect the lack - the need of future performance of more detailed studies in of expertise of this animal on its locomotor habits and sign comotion, the locomotor movement patterns of the giant this subject. metabolic rate and body mass factors may influence the lo the great body mass presented by this animal. CONCLUSION anteater are possibly influenced by low metabolic rate and- ater feeding habit affects not only its mastication and di- gestiveIn this structures, sense Naples but also (1999) the behavior, states that metabolic the giant rate ante and andThe interpotentmorphological biolevers characteristics demonstrate identified favoring and of analyzed the am- in this study, muscles with parallel arrangement of fibers locomotor function. Medri & Mourão (2005) state that food plitude and movement speed at the expense of strength. Pesq. Vet. Bras. 36(6):539-544, junho 2016 Priscilla Rosa Queiroz Ribeiro et al.
544 Acknowledgements.- The authors thank Lucélia Gonçalves Vieira, for her contribution in the illustration work, and Zenon Silva and Daniela Cristi- www.iucnredlist.org na de Oliveira Silva for the cession of material and physical space for the sources. IUCN Red List of Threatened Species. 2011. Disponível em:- research.
Pesq. Vet. Bras. 36(6):539-544, junho 2016