Open Collections

UBC Theses and Dissertations

UBC Theses Logo

UBC Theses and Dissertations

A study of the role of the wings and their musculature in the flight of Oncopeltus fasciatus (heteroptera) Hewson, Rosemary June 1969

Your browser doesn't seem to have a PDF viewer, please download the PDF to view this item.

Item Metadata

Download

Media
831-UBC_1969_A6_7 H49.pdf [ 5.39MB ]
Metadata
JSON: 831-1.0104038.json
JSON-LD: 831-1.0104038-ld.json
RDF/XML (Pretty): 831-1.0104038-rdf.xml
RDF/JSON: 831-1.0104038-rdf.json
Turtle: 831-1.0104038-turtle.txt
N-Triples: 831-1.0104038-rdf-ntriples.txt
Original Record: 831-1.0104038-source.json
Full Text
831-1.0104038-fulltext.txt
Citation
831-1.0104038.ris

Full Text

A STUDY OF THE ROLE OF THE WINGS AND THEIR MUSCULATURE IN THE FLIGHT OF ONCOPELTUS  FASCIATUS (HETEROPTERA) by ROSEMARY JUNE HEWSON B.Sc. University of Toronto, 1966 A THESIS SUBMITTED IN PARTIAL FULFILMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in the Department of ZOOLOGY We accept this thesis as conforming to the required standard THE UNIVERSITY^CJF^BRITISH COLUMBIA June, 1969 In p r e s e n t i n g t h i s t h e s i s i n p a r t i a l f u l f i l m e n t o f t h e r e q u i r e m e n t s f o r an a d v a n c e d d e g r e e at t h e U n i v e r s i t y o f B r i t i s h C o l u m b i a , I a g r e e t h a t t h e L i b r a r y s h a l l make i t f r e e l y , a v a i l a b l e f o r r e f e r e n c e and S t u d y . I f u r t h e r a g r e e t h a t p e r m i s s i o n f o r e x t e n s i v e c o p y i n g o f t h i s t h e s i s f o r s c h o l a r l y p u r p o s e s may be g r a n t e d by t h e Head o f my Department o r by hlis r e p r e s e n t a t i v e s . It i s u n d e r s t o o d t h a t c o p y i n g o r p u b l i c a t i o n o f t h i s t h e s i s f o r f i n a n c i a l g a i n s h a l l n o t be a l l o w e d w i t h o u t my w r i t t e n p e r m i s s i o n . D e p a r t m e n t o f The U n i v e r s i t y o f B r i t i s h C o l u m b i a V a n c o u v e r 8, Canada ABSTRACT Experiments were conducted to test the relative importance of the two pairs of wing and the f l i g h t musculature of Oncopeltus fasciatus. Further, the postembryonic development of this musculature was investigated. It is shown that f l i g h t is impossible with only the hind-wings present. The fore-wings are the major propulsive organs, with the hind-wings providing only a part of t h e . l i f t component. The hind-wings are operated by the mesothoracic musculature acting through a hook mechanism which joins the two pairs of wings together. The development of the mesothoracic muscles is shown to be in two stages; the f i r s t involves the degeneration of the original muscle fibres present in the f i r s t instar insect, the second involves the aggregation of myoblasts to form fibres which mature by about the third day after the moult into the adult stage. Some evolutionary comments are offered on how the developmental processes described in this thesis, compare with those previously described in other insect orders. i i i TABLE OF CONTENTS Page ABSTRACT i i LIST OF TABLES iv LIST OF FIGURES v LIST OF GRAPHS v i i ACKNOWLEDGEMENTS v i i i INTRODUCTION 1 MATERIALS AND METHODS 4 RESULTS: 7 1. F l i g h t s tudies : 7 A . Adul t f l i g h t period 7 B. Experiments on removal of wings 9 C. Importance of hind-wings 9 D. Importance of wing-coupling apparatus 15 2. Morphological study: 16 A . Thoracic musculature of Heteroptera 16 B. Prothoracic muscle development 18 C. Mesothoracic muscle development 18 D. Metathoracic muscle development 31 E . Comparative studies on Leptocoris 31 DISCUSSION 32 A. Relat ive importance of the two pairs of wings and t h e i r thorac ic segments 32 B. Morphology and development 34 C. Some observations on evolut ion a r i s i n g from the study 40 < SUMMARY 46 REFERENCES 48 I V LIST OF TABLES TABLE PAGE Age of f l i g h t i n i t i a t i o n in adult Oncopeltus Actions of the 8 day old adult Oncopeltus on repeated f l i g h t attempts Flight response after wing removal in 8 day old adult Oncopeltus 8 10 Duration of fl i g h t of 8 day old Oncopeltus after wing removal 14 L i f t values for normal and operated 8 day old adult Oncopeltus 14 Types of development of the indirect f l i g h t muscles found in various orders of insects 42 V LIST OF FIGURES Figure Page 1 Morphology of the thorax; a. Diagrammatic longitudinal section of the thorax of a mature adult Oncopeltus 17 b. Diagram of the right wings of Oncopeltus 17 2 F i r s t instar mesothorax, cross section, 400x 20 3 Fi r s t instar, longitudinal section, lOOx 20 4 Fi r s t instar, longitudinal section, 400x 20 •5 Second instar, longitudinal section, lOOx '21 6 Second instar, longitudinal section, 400x 21 7 Second instar, longitudinal section, lOOx 21 8 Second instar, longitudinal section, 400x 21 9 Fourth instar, newly moulted, cross section of mesothorax, lOOx 23 10 Fourth instar, newly moulted, longitudinal section, lOOx 23 11 Fourth instar plus four days, cross section of the mesothorax, LOOx 24 12 Fourth instar plus four days, cross section of the mesothorax, 400x 24 13 Fifth instar, newly moulted, cross section of mesothorax, lOOx 2 5 14 Fifth instar plus four days, cross section of mesothorax, 400x 2 5 15 Fifth instar plus four days, cross section of mesothorax, lOOx 2 5 16 Fifth instar plus four days, cross section of the mesothorax, 400x 2 5 V I 17 Fifth instar plus ten days, cross section of mesothorax, 400x 2 6 18 Fifth instar plus ten days, cross section of mesothorax, 400x, PAS-Alcian blue stain 26 19 Teneral adult, newly moulted, cross section of mesothorax, 400x 2 7 20 Adult plus 12 hours, cross section of mesothorax, 40x. 2 7 21 Adult plus 12 hours, cross section of mesothorax, lOOx 28 22 Adult plus 12 hours, cross section of mesothorax, 400x 28 23 Adult plus two.; days, cross section of mesothorax, lOOx 28 24 Adult plus two days, cross section of mesothorax, 400x 28 2 5 Adult plus three days, cross section of mesothorax, 400x 3° 2 6 Adult plus eight days, cross section of mesothorax, 400x 30 2 7 Adult plus two months, cross section of mesothorax, 400x 30 28 Diagrammatic representation of the various processes associated with maturation of the dorso-longitudinal muscles in Oncopeltus 3 7 v i i LIST OF GRAPHS GRAPH PAGE Speed of flig h t of 8 day old male and female adult Oncopeltus calculated in ten second intervals during the f i r s t 1% minutes and in 1 minute intervals thereafter 11 v i i i ACKNOWLEDGEMENTS I would like to thank Dr. G. G. E. Scudder for his assistance in the research and in the writing of this thesis, and for the financial assistance received from his grant from the National Research Council of Canada. I would also like to thank Drs. A. B. Acton and C. V. Finnegan for their useful constructive criticism of this thesis. 1 INTRODUCTION Most flying insects possess two pairs of wings, the fore-wings on the mesothorax and the hind-wings on the metathorax. For adequate fl i g h t with these wings, i t is necessary that they provide propulsion, l i f t , and s t a b i l i t y . Propulsion is attained by the movement of the wings, which are acted upon by two sets of muscles in each pterothoracic segment; the direct f l i g h t muscles control the camber of the wings, and the indirect f l i g h t muscles cause the up and down motion of the wings through deformation of the thoracic box (Pringle, 1957). L i f t is a function of wing area and shape. Stability is a function of the shapes of both the wings and the body of the insect (Maynard Smith, 1953; Pringle, 1957). Many variations of this generalized scheme are seen among the insects. In primitive insects such as the Odonata (Smith, 1960) and the Isoptera, both pairs of wings are morphologically the same, membranous, and equally important in f l i g h t . The Orthopteran insects show morphological dissimilarities; the fore-wings are lightly sclerotized and leathery, while the hind-wings remain membranous. However, both pairs of wings are s t i l l equally important in f l i g h t (Weis-Fogh, 1956). The mesothorax of the Lepidoptera and the Hymenoptera is considered more important in fl i g h t than the metathorax; the two pairs of wings are securely coupled together (Imms, 1960) and the power for propulsion is mainly provided by the mesothoracic musculature, acting through both the coupling mechanism and the mesothoracic muscles (Pringle, 1961). 2 In the Coleoptera, the fore-wings are reduced and heavily sclerotized, forming the elytra which act as covers for the large membranous hind-wings. In flight, the elytra generally act as stabilizers, with only a small contribution to l i f t (Burton and Sandeman, 1961); they do not function as propulsive organs. The hind-wings are the more important, providing a l l the propulsion as well as the major l i f t component. Thus, the metathorax in the Coleoptera must be the more significant segment with respect to f l i g h t . This is confirmed by the comparison of the musculature in flying and flightless beetles of the same species. The metathoracic indirect f l i g h t muscles are the ones that are reduced considerably in the flightless insects, there being l i t t l e or no change associated with loss of f l i g h t found in comparable muscles in the mesothorax (Jackson, 1956; Smith, 1964). The Hemiptera (Heteroptera) possess two pairs of dissimilar wings; the fore-wings are modified and partially sclerotized, referred to as hemielytra, and the hind-wings are thin and membranous. The two pairs of wings are normally hooked together during f l i g h t by a wing-coupling apparatus (Weber, 1930). Comparing the Heteroptera with the Coleoptera, i t would seem that the hemielytra should play l i t t l e part in flight, the major propulsion being provided by the hind-wings. However, a comparison with the Lepidoptera suggests that the fore-wings could be the more important, and consequently that the hind-wings of the Heteroptera receive their power through the wing-coupling mechanism. The studies of Scudder (1967) on f l i g h t muscle 3 polymorphism in Notonectidae shew that the mesothoracic f l i g h t muscles may be reduced in the flightless insects of this group, with l i t t l e or no change in the metathoracic musculature. Consequently, i t would seem that the mesothoracic segment with it s hemielytra is the more important segment in the f l i g h t of these insects. However, to date there has been l i t t l e testing of this supposition. In the present study, experiments to test the functions and the relative importance of the two pairs of wings were carried out. The differences observed prompted an investigation into the musculature of these segments, and these observations in turn led further to an investigation into the development of the various muscles associated with f l i g h t in both pterothoracic segments. Finally, the development of the muscles found in the thoracic segment without wings, the prothorax, was compared to that of the mesothorax and metathorax. 4 MATERIALS AND METHODS The milkweed bug, Oncopeltus fasciatus (Dallas), was chosen for this study because i t is a typical terrestrial bug (Hemiptera-Heteroptera, Family Lygaeidae), and, as i t has been used as an experimental animal for some f i f t y years, there is an extensive literature on i t s general morphology and biology (Andre, 1935; Neiswander, 1951; Beck, Edwards and Medler, 1958). There also exist some previous observations on i t s f l i g h t activity (Dingle, 1965; 1966). It is easy to maintain a breeding population in the laboratory on a diet of milkweed seeds and water. The l i f e cycle involves five nymphal instars. In the present study, the animals were kept at an average temperature of 76°F (73° during the dark ranging to 78° in the light), absolute humidity of 28°/6, and a light-dark cycle of 14 hours light and 10 dark. Under these conditions, the l i f e cycle from egg to adult lasted 30 t 1 days and the adults lived for an average of two months. Flight experiments were carried out to determine the more important thoracic segment in f l i g h t . I n i t i a l l y , tests were made to determine the age of the adult when i t is f i r s t able to f l y , and the best age for further testing was decided. Flight speed and duration tests were then performed on intact insects at a known age (eight days after the fi n a l moult); these tests were carried out on a f l i g h t m i l l with a circumference of 69.11 cm. To compare the mesothoracic wings and the metathoracic wings with respect to their separate contributions to flight, experiments were performed in which wings were 5 removed, and the a b i l i t y to fl y , speed of flight, and f l i g h t duration of insects lacking a pair of wings were tested. The wings were carefully removed with scissors, and only insects which had previously flown were used in these experiments. Certain observations were made using a Xenon stroboscope. Flight was initiated in the untethered adult insect by a toss into the air, and in the tethered insect, by blowing from the anterior and simultaneously removing tarsal contact (Pringle, 1957). The untethered adult was considered to exhibit true f l i g h t when i t flapped i t s wings and moved in a more or less horizontal direction from takeoff; true fl i g h t also included f l i g h t in a diagonally downward direction, but did not include a vertical drop even i f the wings were flapping. A tethered adult when flying caused the f l i g h t m i l l to move in a circular direction, and f l i g h t was judged to occur on forward motion of the m i l l . For histological work, both adults and nymphs were fixed in Bouin's f l u i d and embedded in Paraplast; the age of each insect was recorded in days from the previous moult. Some of the larger insects required treatment with a vacuum i n f i l t r a t o r for complete i n f i l t r a t i o n . The insects were sectioned at 8 u for f i r s t and second instars, 10 u for third and fourth instars, and 12 u for f i f t h instar and adult insects. Both longitudinal and transverse sections were cut. The sections were stained with Ehrlich's haematoxylin and eosin, and mounted in Permount or HSR resin. Some of the sections of f i f t h instar larvae and adults were stained with the PAS-Alcian blue technique to test for mucopolysaccharides 6 (Culling, 1963). From these slides, the dorso-longitudinal muscles in each thoracic segment were examined, with particular emphasis on the suspected important segment in f l i g h t . The development of other indirect f l i g h t muscles was also noted. The muscle lengths were determined by measurement from both the longitudinal and the transverse serial sections, and the cross-sectional areas of the dorso-longitudinal muscles were also measured from the transverse sections. The segment length and the muscle length were considered to be equal, as the dorso-longitudinal muscles extend the entire length of the segment. Comparisons were made with Leptocoris trivittatus (Say) (Coreidae), which were available at the time. 7 RESULTS 1. FLIGHT STUDIES A. Adult f l i g h t period The tests carried out on adults of various ages showed that the adults would not f l y until three days after the moult into the adult stage. Flight i n i t i a t i o n attempted prior to this time resulted in the animal f a l l i n g directly to the ground, occasionally opening it s wings, but never exhibiting true fl i g h t (Table 1). It was concluded that adult Oncopeltus fasciatus do not f l y prior to three days after the last moult, and hence, insects used in succeeding experiments could not be less than three days old. In these f l i g h t period experiments, i t was found that insects more than three days old would fl y , but that the number of insects flying did not exceed 60% of the number attempted; i t could not be determined why apparently healthy adults resisted a l l efforts to initiate f l i g h t . Flight tests on older adults showed a fl i g h t activity similar to that seen in the three day old adults; only 60% of the older adults would f l y . In experiments on adult insects of various ages, Dingle (1965) found that the eight day old Oncopeltus adults flew faster and longer than adults at any other age. This was also observed in these experiments, and consequently, eight day old adults were used for a l l succeeding experiments. It was noticed that normal, flying insects, once flown on the f l i g h t m i l l , showed a distinct lack of f l i g h t on a 8 TABLE 1 Age of fl i g h t i n i t i a t i o n in adult Oncopeltus Age of adult # tossed # that flew action observed Teneral 10 0 none 1 day 10 0 wings extended 2 days 10 1 fluttering 3 days 10 5 flapping 4 days 10 6 flapping TABLE 2 Actions of 8 day old adult Oncopeltus on repeated f l i g h t attempts I n i t i a l f l i g h t Tethered Tethered Untethered Untethered Second attempt Tethered Untethered Tethered Untethered Action observed on second attempt No fli g h t Flight Poor f l i g h t Flight 9 subsequent mi l l test. The reason for this is unkown, but would not appear to be due to exhaustion. Previously tethered f l i e r s would f l y again untethered (Table 2), and insects were often observed to commence mating behaviour minutes after being removed from the f l i g h t m i l l . Flight periods were usually short, 2 minutes to a half hour, and the rest periods between attempts ranged between ten minutes and 24 hours. Since not a l l adult insects would fly , i t was necessary to test each insect for a positive f l i g h t response prior to the removal of wings. However, once flown on a f l i g h t m i l l , most insects would not undertake tethered f l i g h t again. Thus testing of insects before and after wing removal of necessity had to be carried out on untethered individuals, and this precluded the measurement of many desired parameters. B. Experiments on removal of wings In these experiments, the insect had either the fore-wings or the hind-wings removed after i n i t i a l l y showing a positive f l i g h t response. The experiments showed that the insects could s t i l l f l y with only the fore-wings present, but were unable to f l y lacking fore-wings. In this latter case, the hind-wings were extended but no flapping occurred. There was no difference observed in the results from males and females (Table 3). C. Importance of the hind-wings The observation that Oncopeltus can f l y lacking hind-wings raises the question of the necessity of these wings in the fl i g h t of the insect. Experiments conducted to investigate TABLE 3 Flight response after wing removal in 8 day old adult Oncopeltus Male # operated on # flying after operation Female # operated on # flying after operation fore-wings removed 8 12 hind-wings removed 20 16 20 17 11 Graph 1 Speed of f l i g h t of 8-day o l d male and female adult Oncopeltus, calculated i n ten second int e r v a l s during the f i r s t lh minutes and i n 1 minute i n t e r v a l s thereafter (Average speed + standard error) o CD in E o Q L U L U GL-CO 70 60 to zero 30 4-x normal males n = 10 i no rma l females n = 16 1 1 V 1 0 3 T I M E 4 5 NUTES) 6 7 12 the function of the hind-wjjigs included measurement of f l i g h t duration and speed, and l i f t characteristics in normal insects and in insects lacking hind-wings. (a) Flight duration and speed could only be measured accurately on a f l i g h t m i l l , and since the insects usually refused to f l y a second time on this instrument, good values for duration and speed in insects lacking hind wings could not be obtained. However, a few readings were possible. Speed was measured on the f l i g h t mill in ten second intervals for the f i r s t two minutes and in 30 second intervals after 2 minutes. It was impossible to obtain instantaneous readings for speed without sophisticated equipment, so the recorded speeds are averaged over the ten second or thirty second intervals. Both normal males and females showed an i n i t i a l burst of speed, and slowed to a steady speed after two minutes for the males and three minutes for the females. Over the f i r s t minute, the average speeds were 63 ± 3 cm per second for the males and 54 t 3 cm per second for the females. The steady speed maintained was 57 ± 2.5 cm per second for the males, and 42 ± 5 cm per second for the females. The f l i g h t speed in cm/sec is shown in Graph 1. From Graph 1, i t would seem that the best time to test f l i g h t speed would be after the i n i t i a l burst, while the steady speed is being maintained. This is possible for the normal insects, as they can f l y for several hours i f permitted to do so (Dingle, 1965). However, as has been noted above, insects with the hind wings removed w i l l either not f l y again on the 13 fl i g h t m i l l or w i l l f l y less than ten seconds. In the present experiments, the longest duration recorded for insects lacking hind-wings on the f l i g h t mill was 9 seconds. Several operated insects flew in 2 to 5 second bursts, but no sustained f l i g h t was recorded on the f l i g h t m i l l by this group (Table 4) . The average speed for the few insects which flew on the fl i g h t m i l l following the removal of the hind-wings was computed to be 18 to 20 cm/sec, a value well below those seen for the normal insect. (b) L i f t is d i f f i c u l t to measure accurately, and so a subjective judgement had to be used. Four values could be assigned; "3" for insects flying diagonally upward, with l i f t greater than the insects weight; "211 for insects flying directly horizontally, the l i f t equal to the weight of the insect; "1" for a f l i g h t diagonally downwards, the l i f t being less than the insect's weight; and "0" for a vertical drop, as no l i f t is present. By using such numerical values, the l i f t could be averaged over a number of insects. The l i f t value was assigned after watching the insect take off and f l y from the finger two or three times. A l l normal insects showed l i f t equal to or greater than the weight of the insect; insects lacking hind-wings had a significantly lower l i f t value, being on the average less than the insect's weight. Insects which lacked fore-wings exhibited no l i f t at a l l . Thus only with both pairs of wings could adequate l i f t be maintained (Table 5). 14 TABLE 4 Duration of f l i g h t of 8-day old adult Oncopeltus after wing removal # insects tested # flying on fl i g h t m i l l after wing removal duration of f l i g h t : Avg. (range) male female 10 10 0 4 3 seconds (1-9 seconds) male female TABLE 5 L i f t values for normal and operated 8-day old adult Oncopeltus # insects tested 47 46 Normal insects average l i f t value 2.1 2.4 Insects lacking hind-wings # insects average l i f t tested value 14 12 1.3 1.2 15 D. Importance of the wing-coupling apparatus Several experiments were performed on insects with the wing-coupling apparatus removed from the fore-wings. The results were the same as those from the insects lacking hind-wings; the l i f t and f l i g h t speed were reduced. The hind-wings did not appear to be moving on these insects. In order to determine whether or not the hind-wings were moving the insects were observed flying illuminated solely by a stroboscope, such that the actual wing movements could be observed. Most of the insects with the wing-coupling apparatus removed refused to f l y long enough for adequate observations. However, one intact insect, flying in front of the stroboscope, served to be very useful in this respect; the wing-coupling mechanism became disengaged some five minutes after f l i g h t commenced. After several attempts to reconnect the wings, the insect continued to fly, but only the fore-wings were flapping; the hind-wings did not flap on their own, but were merely held, vibrating, at an upward angle. After several minutes, the hind-wings folded over the back of the insect, assuming the resting position. The fore-wings s t i l l continued to flap on their own for a further ten minutes. It is not known whether the speed was reduced during f l i g h t with the wings uncoupled, as this insect was held in a stationary tether and not on the f l i g h t m i l l . A l l further flights with this insect resulted in coupled flig h t ; i t was the only insect that exhibited this phenomenon, and i t showed i t only once. 16 2. MORPHOLOGICAL STUDY A. Thoracic musculature of Heteroptera The indirect f l i g h t musculature of Hemiptera (Heteroptera) consists of three pairs of major muscles; the dorso-longitudinal muscles extending the length of the segment from prephragma to postphragma; the tergo-sternal or dorso-ventral muscles which extend between the tergum (or notum) and the sternum or the coxa of the leg; and the intersegmental oblique, or dorso-oblique muscles which run from the tergum to the ventral area of the phragma from one segment to the following (Larsen, 1945; Pipa, 1955) (See Figure l a ) . Tiegs (1955) defines a fibre as a bundle of sarcostyles enclosed in a sarcolemma: this definition is adopted in this study, In transverse section, these sarcostyles are seen to be small and too numerous to count accurately. Tiegs noted that the sarcostyles are not single f i b r i l s but are composed of several f i b r i l s bound into a unit by an amorphous i n t e r s t i t i a l substance. These sarcostyles are embedded in sarcoplasm and the whole is ensheathed in a sarcolemma or membrane. The nuclei of the sarcoplasm can be seen protruding from the surface of the fibre. In fully-formed and functional fibres, the sarcoplasm stains with eosin in the preparations made for this study. Immature fibres stain with haematoxylin (blue); this colour slowly changes to pink as the muscle becomes f u l l y developed. Nuclei of both mature (fully-formed) and immature fibres stain Figure 1 Morphology of the thorax Figure la (From Pipa, 1955). Diagrammatic longitudinal section of the thorax of a mature adult Oncopeltus  fasciatus showing the approximate location of the mesothoracic indirect f l i g h t muscles. Figure lb The right wings of Oncopeltus fasciatus, the hind-wing veins named according to the system of Slater and Hurlbutt (1957). Figure l a : cl# c2/ c3 ~ Pro-, meso-, and meta-thoracic coxal cavities DLM - Dorso-longitudinal muscles DOM - Dorso-oblique muscles DVM - Dorso-ventral muscles H. - Hemielytra Hd. - Head Pi - Prephragma of mesothoracic muscles P2 - Postphragma of mesothoracic muscles Tj, T2, T3 - Pro-, meso-, and meta-thoracic terga Figure lb: C - Corium CI. - Clavus Mb. - Membrane Sc. - Subcosta R. - Radius DC - Discal c e l l H. - Hamus M - Media Cu. - Cubitus VF - Vannal Folds AV - Anterior Vannal PV - Posterior Vannal JF - Jugal Fold Figure lb 18 b lue , although the s ize of the n u c l e i i s great ly reduced i n the mature f i b r e . Myoblasts s t a i n densely with haematoxylin and the n u c l e i appear i n the center of these c e l l s . B. Prothoracic muscle development The prothorax i s the most anter ior thoracic segment, and bears no wings, only legs . I t i s not thought to have any funct ion i n f l i g h t . During the l i f e of the insect i t increases i n length some 4.2 times. In the f i r s t i n s t a r , there are s ix fu l ly - formed f ibres of dorso - long i tud ina l muscle which can be seen on each side dorsa l to the gut. In the adul t , the same s ix f ibres are s t i l l seen on each side of the gut. Comparing the s ize of these f ibres i n the f i r s t i n s t a r with t h e i r s ize i n the 8 day o l d adul t , a t h r e e - f o l d increase i n cros s - s ec t iona l area i s noted. There i s ne i ther f ibre cleavage nor myoblast accumulation during post-embryonic development; the f ibres present i n the f i r s t ins tar are the same f ibres present i n the adu l t . The other i n d i r e c t f l i g h t muscle counterparts (dorso-ventra l and dorso-oblique muscles) develop i n the same manner, there being merely an increase i n s ize i n post-embryonic development. C. Mesothoracic muscle development The mesothorax i s the anter ior wing-bearing segment, and, as seen from the f l i g h t experiments, i s the dominant segment i n f l i g h t . This region undergoes considerable growth throughout post-embryonic development, there being a for ty 19 fold increase in length between the f i r s t instar and the eight day old adults. The dorso-longitudinal muscles undergo considerable change during the l i f e of the insect. In the f i r s t instar, five fully-formed dorso-longitudinal muscle fibres can be seen on either side of the gut in the mesothorax (Figures 2, 3, 4). The fibres are located such that they appear se r i a l l y homologous to those seen in the prothorax. In the second instar the original five fibres are absent from the newly moulted insect (Figures 5, 6). After two days, a small aggregation of myoblasts can be seen medial to the dorsd-ventral muscles, extending most of the length of the segment. They do not occupy the same position as the dorso-longitudinal muscles in the f i r s t instar; a l l traces of serial homology have been lost. The muscles in the second instar l i e between the gut and the dorso-ventral muscles, rather than between the gut and the notum as seen in the f i r s t instar insect. It is not possible to say whether several chains of myoblasts or a bundle of elongated myoblasts is involved (Figures 7, 8). In the third instar insect, the number of myoblasts appears to have increased. In some sections, the myoblasts are closely associated with a trachea. In this instar, the other indirect f l i g h t muscles are commencing formation anterior to the existing functional dorso-ventral muscles and posterior to the dorso-oblique muscles. These existing muscles were seen in the f i r s t and second instar, and do not degenerate like the dorso-longitudinal muscles. 20 Figure 2 First instar mesothorax, cross section, 400x. Five fibres of dorso-longitudinal muscle can be seen dorsal to the gut. Figure 3 F i r s t instar, longitudinal section, lOOx. The relative lengths of the three thoracic segments can be seen. Most of the body is occupied by the gut, much more than in later stages. Figure 4 Fi r s t instar, longitudinal section, 400x. Detail of Figure 3. DLM - Dorso-longitudinal muscle H - Head Ms - Mesothorax Mt - Metathorax Pr - Prothorax 21 Figure 5 Second instar, longitudinal section, lOOx. The dorso-longitudinal muscles in both the prothorax (Pr) and the metathorax (Mt) can be seen; the f i r s t few myoblasts of the dorso-longitudinal muscle in the mesothorax (Ms) have appeared. Figure 6 Second instar, longitudinal section, 400x. Detail of Figure 5. Figure 7 Second instar, longitudinal section, lOOx. This section, taken two days after those seen in Figures 5 and 6, shows the aggregation of myoblasts commecning to form fibres in the mesothorax (Ms). Figure 8 Second instar, longitudinal section, 400x. Detail of Figure 7. Note the close association of the myoblasts with a trachea. Pr - Prothorax Ms - Mesothorax Mt - Metathorax DLM - Dorso-longitudinal muscle P-L - Prephragma of mesothorax T - Trachea 22 By the fourth instar, the pair of mesothoracic dorso-longitudinal muscles are becoming well formed; the fibres in the newly moulted fourth instar being densely packed and strongly basiphilic when stained (Figures 9,10). After four days, at the end of the instar, these fibres appear thicker and slightly more widely spaced, but they remain strongly basiphilic (Figures 11,12). In the f i f t h instar, the fibres continue to enlarge and separate. They remain angular in cross section, with large protruding nuclei, but there is a slight change in the staining of the sarcoplasm. While at the beginning of the instar the fibres are densely basiphilic (Figures 13,14), at the end of the 12 day long instar they are becoming somewhat acidophilic (Figures 15,16,17). The fibres remain with the distance between the fibre less than the fibre width. Staining the muscle sections at this time with the PAS-Alcian Blue technique shows a dense blue-staining mucopolysaccharide substance between the fibres (Figure 18). Sections of newly moulted, or teneral, adults show that the fibres in the dorso-longitudinal muscles stain as in the late f i f t h instar, but are slightly rounded and very much more separated; the distance between the fibres is now equal to, or slightly greater than, the fibre width (Figure 19). Insects sectioned 12 hours after moulting show an increase in fibre size but no further increase in fibre spacing is evident (Figure 20,21,22). Staining for mucopolysaccharides (PAS-Alcian Blue technique) shows no dense blue colour between the fibres. The sarcoplasm of the fibres stains in a more acidophilic manner than previously, but the nuclei remain stained with 23 Figure 9 Fourth instar, newly moulted, cross section of the mesothorax, lOOx. The dorso-longitudinal muscles (DLM) can be seen as a very narrow body of deeply staining tissue. Compared to later sections, i t is s t i l l extremely small. Figure 10 Fourth instar, newly moulted, longitudinal section, lOOx. The dorso-longitudinal muscle (DLM) now extends the length of the mesothorax. Ms - Mesothorax Mt - Metathorax DVM - Dorso-ventral muscle DLM - Dorso-longitudinal muscle Pi - Prephragma of the mesothorax P2 - Postphragma of the mesothorax 24 Figure 11 Fourth instar plus four days, cross section of the mesothorax, lOOx. The dorso-longitudinal muscle (DLM) has increased in cross sectional area, and is not situated as close to the dorso-ventral muscle as was seen in Figure 9. Figure 12 Fourth instar plus four days, cross section of the mesothorax, 400x. Detail of Figure 11. Note the DLM fibres becoming wider spaced and thicker. 25 Figure 13 F i f t h instar, newly moulted, cross section of mesothorax, lOOx. The clumps of fi b r e s are becoming more separated; this separation w i l l l a t e r be l o s t as the i n d i v i d u a l f i b r e s increase i n s i z e . Figure 14 F i f t h instar, newly moulted, cross section of mesothorax, 400x. Detail of Figure 13. Figure 15 F i f t h i n s t a r plus four days, cross section of mesothorax, lOOx. The muscle i s becoming s t i l l larger i n cross sectional area. Figure 16 F i f t h instar plus four days, cross section of mesothorax, 400x. The f i b r e separation i s becoming increasingly evident. Dorso Dorso Dorso -longitudinal muscle -ventral muscle -oblique muscle 2 6 Figure 17 F i f t h in s tar plus 10 days, cross sect ion of mesothorax, 400x. The f ibre separation has increased a great deal over the previous s ix days, making i t no longer possible to f i t the ent ire muscle i n the 400x f i e l d . Figure 18 F i f t h i n s t a r plus ten days, cross sec t ion of mesothorax, 400x„ PAS-Alcian blue s t a i n . The accumulation of the substance between the f ibres (mucopolysaccharide) appears to be the cause of the f ibre separat ion. 27 Figure 19 Teneral adult (newly moulted), cross section of mesothorax, 400x. The fibres in the dorso-longitudinal muscle are at their maximum • separation. Figure 20 Adult plus 12 hours, cross section of mesothorax 40x. The relative size of the dorso-longitudinal muscles compared to the other indirect f l i g h t muscles can be seen, also the great increase in the size of the muscle can be noted. F - Fibre T - Trachea DLM - Dorso-longitudinal muscle DVM - Dorso-ventral muscle DOM - Dorso-obligue muscle C - Coxa 28 Figure 21 Adult plus 12 hours, cross section of mesothorax, lOOx. Detail of Figure 20. Figure 22 Adult plus 12 hours, cross section of mesothorax 400x. Detail of Figure 21. The fibre separation has decreased because of "continuing fibre growth. The nuclei can clearly be seen as prominant protrusions from the fibre surface. Figure 23 Adult plus two days, cross section of mesothorax, lOOx. Fibres-separation has further decreased. Figure 24 Adult plus two days, cross section of mesothorax, 400x. The nuclei have become less prominant, and the fibres further increased in size. The sarcostyles can be seen in the cross section of each fibre. T F N - Trachea - Fibre - Nucleus m m 588 5. ! • t* 29 haematoxylin and are s t i l l large and protruding from the fibre surface. The fibres increase in size over the next two to three days, and this is accompanied by further decrease in basiphilia. By this time, the nuclei are somewhat smaller and less prominant (Figures 23,24). The third day after the fi n a l moult to the* adult, l i t t l e further increase in fibre size was detected, and there was l i t t l e trace of basic staining (Figure 2 5). The fl i g h t experiments discussed in the previous section showed that the insects were able to f l y at this age; they were unable to f l y previously. Reduction in the >ize of the nuclei is seen for a further two days, and the closely packed fibres show basiphilia in the eight day old adult (Figure 26). Insects sectioned two months after the moult into the adult stage show the dorso-longitudinal muscles composed of acidophilic fibres. These are very close together and have very small and indistinct nuclei which do not prodtrude from the fibre surface (Figure 27). In a l l f i f t h instar and adult sections, the fibre nuclei were investigated in order to check for chromatin clumping, an effective test for nuclei maturation (Finnegan, 1961). However, the sections cut proved to be too thick and the nuclei too small for any conclusion to be drawn. It is obvious that the nuclei become smaller and the colour much more dense as the fibres age; this may be due to the maturation of the nuclei. 30 Figure 2 5 Adult plus three days, cross section of the mesothorax, 400x. The fibres of the dorso-longitudinal muscle are now almost fully-formed, as the adult is able to f l y . The fibres at the adult stage are very acidophilic. Figure 2 6 Adult plus eight days, cross section of the mesothorax, 400x. Fibre enlargement has ceased by this stage. Figure 2 7 Adult plus two months, cross section of mesothorax, 400x. The fibre shape is seen to be hexagonal in most cases? this is the most efficient shape for packed bodies. N - Nucleus T - Trachea D. Metathoracic muscle development In the metathorax, seven fully-formed fibres are seen in the f i r s t instar, s e r i a l l y homologous to the dorso-logitudinal muscles found at this stage in the more anterior thoracic segments. These fibres merely enlarge during the next three instars. At the beginning of the f i f t h instar, the fibres can be seen splitting or cleaving longitudinally; each fibre producing two new fibres. At this time, no change in staining properties of the fibres can be seen. By the adult stage, there has been a ten-fold increase in fibre number in the dorso-longitudinal muscles. The fibres are much smaller on the average than before, the cross sectional area of the entire muscle has increased only some five and a half times. E. Comparative studies on Leptocoris The sections of the Coreid, Leptocoris trivittatus, show that the development of the dorso-longitudinal muscles in the mesothorax of this insect of a group closely related to Oncopeltus is very similar to the development in Oncopeltus, except for a delay of approximately one half instar: the i n i t i a l dorso-longitudinal muscles of the mesothorax disappear by the second instar, but the myoblasts did not appear until the third instar. The fibre bundles in the late third and early fourth instars of Leptocoris are smaller than their counterparts in Oncopeltus. although the bugs are similar in size. Sections of the late adult (the age of the Leptocoris adults being unknown) were similar in overall muscle shape, fibre size, and fibre shape to the sections of old Oncopeltus adults, but the fibres were slightly, more widely spaced in Leptocoris. 32 DISCUSSION A. Relative importance of the two pairs of wings and their thoracic segments. Flight requires propulsion, l i f t , and s t a b i l i t y . The two former factors are mainly the functions of the wings and their musculature; s t a b i l i t y is a function of the shape of the wings and the body. The experiments with Oncopeltus fasciatus show that with the hind-wings removed, the insect can s t i l l provide the propulsion for fl i g h t ; with the fore-wings removed, propulsion is not possible. It would seem therefore that the mesothorax and the fore-wings are more important than the metathorax and the hind-wings for propulsion. From the results i t is evident that the hind-wings are necessary for adequate fl i g h t and i t i s shown that they provide much of the l i f t . Insects lacking hind-wings were unable to maintain horizontal f l i g h t and quickly descended to the ground; they would probably not be able to take off from the ground, as the l i f t force provided by the fore-wings alone is less than the weight of the insect. Thus, the hind-wings are important in that they provide the extra surface necessary to increase the l i f t to a value greater than the insect's weight. For this extra surface area to be effective, the two pairs of wings must be coupled together, presenting a single surface area. It was observed, on the insect whose hooking mechanism failed, that the hind-wings would not flap unless they were coupled to the fore-wings. Thus, one is led to believe that the 33 power for f l i g h t movement of the wings usually comes from the mesothorax, and is transmitted to the hind-wings through the fore-wings and the coupling mechanism. The hind-wings were observed to vibrate when uncoupled, and so the metathoracic musculature is capable of bringing about hind-wing movement, but in the flying insect, the actual operation of the wings is evidently mesothorax controlled. Thus, the two pairs of wings are capable of independent movement, but in normal f l i g h t they must remain coupled to provide a l l the essential components for continuous forward locomotion. A similar situation i s seen in the Lepidoptera and the Hymenoptera. The two pairs of wings in these groups are also joined by hooking mechanisms, and the power for f l i g h t comes from the mesothorax. For adequate l i f t and propulsion, both pairs of wings are necessary, but they are both controlled by the mesothoracic musculature, acting through the hook mechanism and through the metathoracic muscles in some cases (Chadwick, 1953; Pringle, 1968). The muscles in the mesothorax also differ from those in the metathorax in these groups; the mesothoracic muscles are much larger and of a different physiological type than the metathoracic muscles (Pipa, 1955; Pringle, 1957). Observations on the indirect f l i g h t muscles of the eight day old adult Oncopeltus revealed similar morphological differences. The indirect f l i g h t muscles in the mesothorax are much larger than the corresponding muscles in the metathorax, both in cross sectional area and in length. The fibres in the mesothoracic muscles are more numerous, and appear to be less mature than 34 the metathoracic fibres; theyi-are rounder, are more widely spaced, have larger and more prominant nuclei, and are less eosinophilic than the fibres seen in the metathoracic indirect f l i g h t muscle. The metathoracic fibres are closely packed and hexagonal in shape, a sign of mature muscle (Thompson, 1961); the smaller and less prominant nuclei seen in these fibres are also a sign of mature muscle. Such mature muscle was seen in the mesothorax of much older adults. The reason for the differences in the maturity of the muscles in the mesothorax and the metathorax at the time the insect is capable of sustained f l i g h t are not obvious on examination of the adult instar alone. The post-embryonic development of these muscles was therefore investigated for an explanation. B. Morphology and development This study of the post-embryonic development in Oncopeltus showed that significant changes take place in the thoracic musculature. The mesothorax undergoes a much greater change than does the prothorax or the metathorax. The dorso-longitudinal muscle in the prothorax merely increases in size during larval l i f e . The homologous muscle in the mesothorax exhibits a development similar to that seen in the indirect f l i g h t muscles in Holometabolous insects (Tiegs, 1955). The dorso-longitudinal muscles in the metathorax and the dorso-ventral muscles in the mesothorax enlarge during larval development by the processes of fibre growth and fibre cleavage. In the post-embryonic development of the mesothoracic dorso-longitudinal muscles of Oncopeltus fasciatus, two phases 35 of development can be recognized; the f i r s t phase involves the disappearance of the fu l ly - formed, funct iona l l a r v a l muscle, and the second phase the development from myoblasts of f ibres with the f i n a l funct ion of f l i g h t . Such muscle metamorphosis has not been reported previous ly i n an Exopterygote insect , although i t i s commonly seen i n the Endopterygota. In th i s study on the mesothoracic muscles i n the f i r s t and second ins tars of Oncopeltus i t has not been possible to invest igate the muscle disappearance i n d e t a i l . However, we may note that the muscles of the f i r s t i n s t a r do disappear at the time of the moult to the second i n s t a r , so a hormonal component could be present. I t i s not known i f there i s any nervous system component involved, and i n Oncopeltus no phagocytic haemocytes have been seen. However, i n Cenocorixa  b i f i d a (Hung.) (Hemiptera) where a s i m i l a r muscle degeneration i s seen at the end of the f i r s t nymphal i n s t a r , Scudder (unpub.) has found evidence of phagocytic haemocytes present at the terminal stages of the degeneration that are act ive i n the engulf ing of the muscle fragments. In Oncopeltus, i t has not been possible to study the o r i g i n of the myoblasts that go to form the new muscle i n the t h i r d i n s t a r . To date, no h i s t o b l a s t t i ssue that might give r i s e to these has been detected. I t i s possible that the myoblasts come from the muscle that was previous ly present; the muscles may dedi f ferent ia te rather than simply degenerate. The second phase of development of the mesothoracic dorso - long i tud ina l muscles i n Oncopeltus involves the aggregation 36 of myoblasts, the transformation of the myoblasts to form fibres, and the maturation of these fibres to fully-formed functional muscles. In the early stages of the muscle formation, the myoblasts appear to be slightly elongated cells, with the nucleus in the centre of the c e l l . The detail of fibre formation in Oncopeltus has not been studied, but two situations are possible, both having been recorded in the development of other animals: the myoblasts may each put out bipolar extensions and form one f i b r i l apiece, as occurs in vertebrates (Boyd, 1960) and some insects; or several myoblasts may form a column extending the length of the segment, the myoblasts then fusing to form a syncytial f i b r i l or sarcostyle (Tiegs, 1955). Whichever the method in Oncopeltus, the fibres when formed show the nuclei of the myoblasts migrating to the outer edge of the fibres where they are seen as protrusions on the surface of the young fibre. Maturation of the fibres occurs during the f i f t h nymphal instar and is continued into the f i r s t few days of adult l i f e ; f l i g h t occurs in the three to four day old adult. Involved in this maturation process are the processes of fibre separation, growth in cross-sectional area, rounding up, and reduction in the prominance of the nuclei. The four processes occur concurrently as seen in Figure 28, but each process commences and ceases at a different time. Fibre growth extends over the longest period of time, continuing until three days after the fi n a l moult. The insect at this age cannot f l y well; good fl i g h t of long duration does 3 7 Figure 28 Diagrammatic representation of the various processes associated with maturation of the dorso-longitudinal muscles in Oncopeltus, showing their relative durations and times of commencement and cessation FIBER SEPARATION Fl BER GROWTH ROUNDING UP REDUCTION OF NUCLEAR PROTRUSIONS 6 8 ~ r ~ 9 10 11 1 2 l 1 4 6 8 FIFTH LARVAL INSTAR MOULT ADULT 38 not occur until seven or eight days after the moult (Dingle, 1965). A similar developmental pattern has been observed in Locusta migratoria by Bucher (1965) and Vogell (1965). Further electron microscope studies by Vogell (1965) reveal that although differentiation of the fli g h t muscles as seen under the light microscope appears to cease, in L. migratoria by the third day after the last moult, an intracellular phase of duplication ensues in which the number of myofibrils in each f i b r i l doubles, the fibre size changing l i t t l e . Further, i t has been shown by German workers quoted in Bucher (1965) that the extramitochondrial enzyme development is not completed until the eighth day of adult l i f e in L. migratoria. It is thus l i k e l y that between the third and eighth day in the adult instar of Oncopeltus there is a similar doubling of the myofibrils and development of the exta-mitochondrial enzyme systems: this would account for the lack of good fl i g h t observable in this period. Fibre separation occurs from day seven of the f i f t h • instar to very shortly after the fi n a l moult in Oncopeltus. This separation probably enables the trachea to come closer to the fibres in the middle of the muscle (Rensch, 1948). The fibre separation is associated with the occurrence of a mucopolysaccharide (alcian blue positive) between the fibres. The fibres when close together i n i t i a l l y show an abundance of this substance between them. Since mucopolysaccharides bind water (Ogston, 1966), i t is suspected that in this muscle, 39 the mucopolysaccharide swells, forcing the muscle to separate. By twelve hours after the final moult into the adult stage, this substance has dispersed, and the fibres are at their maximum separation. Rounding up of the fibres appears to be a spatial phenomenon. After the fibres are separated, each fibre is no longer confined by i t s neighbours, and is able to assume a cylindrical shape. Subsequently, when the fibres are f u l l y expanded, an angular shape is again attained as a result of space limitation. Most of the closely packed fibres are hexagonal in cross section, this being the most physically effic i e n t shape, seen often in nature (Thompson, 1961). The reduction in nucleus size and the subsequent increase in staining intensity is the last process observed; i t is not completed until after fibre growth has ceased. Presumably, no further structural proteins are required, nor further mitoses necessary. The increase in staining properties of the nuclei was taken to indicate chromatin clumping, a common occurrence in maturing nuclei. This has been described in the development of several other systems (Finnegan, 1961; Briggs and King, 1955). 40 C. Some observations on evolution a r i s i n g from the study-It has long been thought that the Hemiptera occupy a t r a n s i t i o n stage between the Endopterygota and the Expoterygota (Hinton, 1948; 1963). The reasons for this premise vary. The Hemiptera are usually considered the most advanced of the Exopterygote insects. In some cases, the insects belonging to this group are not hemimetabolous, and since t h i s t r a i t i s invaria b l y connected with the Exopterygota, they are a t y p i c a l . Some Coccidae and Aleyrodidae exhibit a pupal-like stage as the penultimate in s t a r ; t h i s stage usually c a l l e d the pseudopupa (Weber, 1934; Trehan, 1940; Makel, 1942). The pseudopupae act very s i m i l a r l y to the pupae of the Endopterygota, i n that they do not feed and they remain motionless, although they w i l l move i f disturbed. It i s generally accepted that f l y i n g insects evolved from non-flying insects, and i n d i r e c t f l i g h t muscles evolved from s i m i l a r l y positioned walking muscles. Increased metabolic demands on these walking-flying muscles resulted i n a great increase i n the size of the muscle (in an evolutionary sense), a change i n the development of the muscle through the non-f l y i n g l a r v a l stages, and eventually, a change i n the nature of the muscle i t s e l f (Smith, 1960). Primitive insects possess lamellar muscle which i s also found i n the non-flight muscles of most other insects. In the Exopterygota, the i n d i r e c t f l i g h t muscles may be either lamellar or " m i c r o - f i b r i l l a r " muscle; both types are synchronous with r e l a t i v e l y slow speeds of contraction, and are consequently r e l a t i v e l y i n e f f i c i e n t 41 (Pipa, 1955). in most Endopterygota, the indirect f l i g h t muscles are made up of f i b r i l l a r muscle, the highly specialized, asynchronous muscle with very high contraction frequencies (Boettiger, 1960). The Hemiptera possess two of these types of muscle in the indirect f l i g h t musculature; the mesothoracic fl i g h t muscles are f i b r i l l a r , while those found in the metathorax are lamellar in nature (Pipa, 1955); Govind, 1965) . In the possession of these two types of muscle, the Hemiptera appear transitional between the Exopterygota and the Endopterygota. Similarities between the Hemiptera and both the Exopterygota and the Endopterygota can also be seen in the study of the development of the indirect f l i g h t muscles. Tiegs (1955) studied several insect orders in this respect, and other orders have also been investigated (Table 6). The development of the indirect f l i g h t muscles through the larval stages of insects can occur by any combination of several methods. Fibre enlargement, fibre proliferation through cleavage, myoblast aggregation, and incorporation of free myoblasts to pre-existing rudiments are a l l readily recognizable in the developmental processes. The complexity of the processes depends on the position of the insect order in an evolutionary sense, and on the fin a l function of the muscle; whether flight, i f present, is strong or weak, prolonged or of short duration. In the Thysanura, primitive non-flying insects, a specific number of muscle fibres are present in the f i r s t instar nymph. TABLE 6 Types of development of the indirect f l i g h t muscles found' in various orders of insects Thysanura Odonata Orthoptera Homoptera Diptera Lepidoptera Ctenolepisma  longicaudata Anax Junius Acridopga reticulata (Tettigoneidae) Cyclochila  australasiae Erythroneura  ix (Cicadellidae) Perkinsiella  saccharicida (Delphacidae) Bathylus albicinctus (Cercopidae) Drosophila  melanogaster Antheraea  pernyi Fibre enlargment only Dorso-longitudinal muscles reduced or absent in adult, direct f l i g h t muscles more important Functional nymphal muscles: fibre enlargement and cleavage. Pure f l i g h t muscle: rudimentary fibres followed by fibre enlargement and cleavage Myoblasts unite,forming a rudimentary fibre, then fibre cleavage occurs Free myoblasts in the young nymph, 5 of which become f i b r i l s , other myoblasts form alongside the f i b r i l s and are incorporated into the growing fibre Free myoblasts form fibre rudiments, fibre cleavage occurs Free myoblasts become incorporated onto pre-existing muscles, fibre cleavage occurs Tiegs, 1955 Clark, 1940 Smith, 1960 Tiegs,.1955 Tiegs, 1955 Tiegs, 1955 Tiegs, 1955 Tiegs, 1955 During pupation, larval muscles degenerate, Tiegs, 1955 adult muscles form from free myoblasts Hinton, 1959 which had adhered to the larval muscles (imaginal discs) Larval muscle degenerates in prepupa and Eigenmann, pupa stages. Thin strings of myoblasts 1965 originates from the larval muscles, divide; to separate fibres whose f i b r i l s divide repeatedly u n t i l the adult 43 The muscle enlarges throughout the development of the insect by-fibre enlargement only, with no increase in fibre number, the adult therefore having the same number as the nymph. In the Orthopteroid insects, some indirect f l i g h t muscles function as walking muscles in the nymph; others do not function until the adult stage and are present in the young nymphs as small rudiments. However, the development of both is similar. Fibre enlargement occurs f i r s t , and when the insect reaches a certain size, fibre cleavage ensues. Each fibre cleaves into two or three daughter fibres which may cleave a second time. This cleavage process soon outstrips the enlargement process, so that although the number of fibres may increase 4 or 5 times, the cross sectional area increases only about three times i t s i n i t i a l size. Usually the number of fibres found in the adult stage is attained by the beginning of the last nymphal instar. During this last instar, the muscle whose growth has merely kept pace with the growth of the numph, accelerates i t s development in preparation for the function of fl i g h t . The muscle may enlarge three or four times its diameter while the nymph enlarges by less than twice during this instar. In the insects with a complete metamorphosis, the indirect f l i g h t muscles do not appear until the pupal stage. Tiegs (1955), working on the Diptera, showed that the development in Drosophila started at the beginning of pupation, with the wing muscles arising out of free myoblasts. These myoblasts can be seen in late larvae adhering in small numbers to the outer surface of certain larval muscles, which degenerate during pupation. In the pupa, the myoblasts multiply actively and by 44 the end of the f i r s t day, the three larval dorso-longitudinal fibres have been almost completely replaced by three compact columns of myoblasts. Soon, fibre rudiments begin to appear, and the fibre is gradually b u i l t up by progressive addition of free myoblasts to the fibre column. This process is complete by the middle of the second day of pupation. In later pupae, the fibres thicken and become more widely spaced. The Hemiptera show developmental characteristics of both the Exopterygotes and the Endopterygotes. This is especially evident in Homoptera, in which each family seems to u t i l i z e a different method of f l i g h t muscle development. In Cicada, indirect f l i g h t muscles develop similarly to the Orthopteran method, with a muscle formed by fibre growth and cleavage. Other groups show Dipteran characteristics, with the muscle forming from aggregations of free myoblasts (see Table 6 ) . However, no Homoptera studied by Tiegs showed any degeneration of pre-existing fully-formed muscle prior to the development of the f l i g h t muscles. The dorso-longitudinal muscles in Oncopeltus fasciatus in this study are shown to develop in a different manner in each of the three thoracic segments; and the dorso-ventral and dorso-oblique muscles in the mesothorax develop differently from the dorso-longitudinal muscles in the same segment. In the prothroax, the dorso-longitudinal muscles develop in a manner similar to that seen in the Thysanura, a process of fibre growth with no increase in fibre number. The dorso-longitudinal muscles of the metathorax are functional throughout the l i f e of the insect, and develop by longitudinal fibre cleavage; 45 showing a close similarity with the development of Orthopteran indirect f l i g h t muscles. The development of the dorso-ventral and dorso-oblique muscles of the mesothorax resembles a developmental process found in the Homoptera, as both arise from aggregations of myoblasts with no pre-existing muscle or rudiment. The development of the mesothoracic dorso-longitudinal muscles, however, resembles that seen in Endopterygota, involving a degeneration of fully-formed nymphal or larval muscles and a development of new muscle from aggregations of myoblasts. In Endopterygotes, this process does not commence until pupation, and so is restricted to only one instar in the l i f e of the insect. In Oncopeltus the process begins only two days after the nymph hatches from the egg; at the time of the f i r s t moult. Thus i t can be seen that the situation seen in Hemiptera is primitive in nature, as the development of the indirect f l i g h t muscles requires several instars for completion. Yet this type of development is only seen in Hemiptera in the entire Exopterygote group, supporting the hypothesis that the Hemiptera form, a transitional stage between the Exopterygote and the Endopterygote insects. 46 SUMMARY 1. Flight in Oncopeltus fasciatus is possible only i f the fore-wings are present. 2. The hind-wings are important in that they increase the surface area of the wings when they are hooked together; a l l the power for the hind-wings is transmitted from the mesothoracic muscles through the wing coupling apparatus. 3. Thus the mesothorax is the more important wing bearing segment, as the mesothoracic muscles provide the power for both pairs of wings. 4. The development of the dorso-longitudinal muscles in the prothorax is merely a process of fibre enlargement. There is no increase in fibre number. 5. The development of the dorso-longitudinal muscles in the metathorax involves both fibre enlargement and fibre cleavage, and these occur simultaneously. 6. The development of the dorso-longitudinal muscles in the mesothorax involves two processes, the f i r s t of these is the degeneration of previously existing muscles during the moult from the f i r s t to the second instars. 7. The second process of this development involves the aggregation of myoblasts and their subsequent formation of fibres. 8. These fibres mature during the f i f t h instar and the f i r s t 4 7 three or four days of the adult stage. Their maturation involves f i b r e separation, f i b r e enlargement, rounding up of f i b r e s , and the reduction of nuclear prominance. 9. Comparative studies with a c l o s e l y related insect show the process to be the same except for a time lag of approximately one-half an i n s t a r . 48 REFERENCES Andre, F., 1935. Notes on the biology of Oncopeltus fasciatus. Iowa State Coll. Journ. of Sci. 9: 73-87. Beck, S. D, Edwards, C. A., and Medler, J. T., 1958. Feeding and nutrition of the milkweed bug Oncopeltus fasciatus (Dall). Ann. Entomol. Soc. Am. 51; 283-288. Boettiger, E. G., 1960. Insect f l i g h t muscles and their basic physiology. Ann. Rev. Ent. 5: 1-16. Boyd, J. D., 1960. Development of striated muscle. From Structure and Function of Muscle, Vol. 1, ed. F. H. Bourne, Academic Press, N.Y. Briggs, R., and King, T. J., 1955. Specificity of nuclear function in embryonic development. Biological  Specificity and Growth, ed. E. G. Butler, Princeton U. Press. Bucher, Th., 1965. Formation of the specific structural and enzymic pattern of the insect fl i g h t muscle. Aspects of Insect Biochemistry, ed. T. W. Goodwin Academic Press, N.Y. Burton, A. J. and Sandeman, D. C, 1961. The l i f t provided by the elytra of the rhinoceros beetle Oryctes boas. S. Afr. J. Sci. 57: 107-109. Chadwick, L. E., 1953. The motion of wings".: In Insect  Physiology, ed. K. D. Roeder, Wiley, N.Y. pp. 577-615. Clark, H. W., 1940. The adult musculature of the Anisopterous dragonfly thorax (Odonata). J. Morph. 67: 523-565. Culling, C. F. A., 1963. Handbook of Histopathological  Techniques, 2nd ed. Butterworths, London. Dingle, H., 1965. The relationship between age and f l i g h t activity in the milkweed bug Oncopeltus fasciatus (Dall). J. Exp. Biol. 42: 269-283. _, 19 66. Some factors affecting f l i g h t activity in Oncopeltus fasciatus (Dall). J. Exp. Biol. 44: 335-343. Eigenmann, R., 1965. Untersuchungen uber die Entwicklung der dorsolongiudinalen Flugmuskelen von Antheraea  pernyi (Guer). Rev. Suisse Zool. 72: 789-840. Finnegan, C. V . , 19 61. A study of nuc l e i and i n t e r c e l l u l a r ground substance during the i n s i t u d i f f e r e n t i a t i o n of somites i n Taricha torosa . Journ. Emb. & Exp. Morph. 9: 650-660. Govind, C. K . , 1965. An inves t iga t ion of the f l i g h t mechanism and o r i e n t a t i o n of the s t ink bug Anoplecnemis curv ipes . Master's thes i s , Un ivers i ty of Nata l , unpublished. Hinton, H. E . , 1948. On the o r i g i n and funct ion of the pupal stage. Trans. R. Ent . Soc. Lond. 99: 365-409. , 1959. O r i g i n of the i n d i r e c t f l i g h t muscles i n pr imi t ive f l i e s . Nature 183: 557-558. , 1963. The o r i g i n and funct ion of the pupal stage. Proc. R. Ent . Soc. Lond. A. 38: 77-85. Imms, A . D . , 1960. A General Textbook of Entomology, 9th' e d i t i o n , Methuen & C o . , London. Jackson, D. J . , 1956. Observations on f l y i n g and f l i g h t l e s s water beet les . J . L i n n . Soc. (Zool.) 43: 18-42. Larsen, 0 . , 1945. Der Thorax der Heteropteren: Skelett und Muskulature. Lund. Univ. A r s s k r i f t N . F . 41: 3: 1-96. Makel, M . , 1942. Metamorphose und Morphologie des Pseudococcus Mannchens mit besonderer Berucksichtigung des Skelettmuskelsysterns. Z o o l . J b . , Anat. 67: 461-512. Maynard Smith, J . , 1953. Birds as aeroplanes. New Biology 14: 64-81. Neiswander, c . R. , 1951. L i f e h i s t o r y and r e s p i r a t i o n of the milkweed bug Oncopeltus fasc iatus ( D a l l ) . Ohio Journ. S c i . 51: 27-33. Ogston, A. G . , 1966. On water b ind ing . Fed. Proc. 25: 986-989. Pipa, R. , 1955. A comparative h i s t o l o g i c a l study of the i n d i r e c t f l i g h t muscles of various insect orders . Master's thes i s . Un ivers i ty of Connecticut, Unpub. Pr ing le , J . W. S., 1957. Insect F l i g h t . Cambridge Univers i ty Press, London. _ , 1961. The funct ion of the d i r e c t muscles i n the bee. Proc. XIth Int . Congr. Ent . Vienna 1960 1: 660. 50 Pringle, J. W. S., 1968. Comparative physiology of the fl i g h t motor. Adv. in Insect Physiol. 5: 163-227. Rensch, B., 1948. Histological changes correlated with evolutionary changes of body size. Evolution 2: 218-230. Scudder, G. G. E., 1967. Notonecta borealis (Bueno & Hussey): A flightless species? Ent. Month Mag. 102: 258-259. Slater, J. A. and Hurlbutt, H. W., 1957. A comparative study of the metathoracic wing in the family Lygaeidae. Proc. Ent. Soc. Wash. 59: 67-79. Smith, D. S., 1964. The structure and development of flightless Coleoptera: , a "light and electron microscopic study of the wings, thoracic exoskeleton and rudimentary f l i g h t musculature. J. Morph. 114: 107-184. Thompson, D'A. W., 1961. On Growth and Form. Abridged ed. J. T. Bonner, University Press, Cambridge. Tiegs, O. W., 1955. Flight muscles in insects, anatomy and histology, with some observations on the structure of striated muscle in general. Phil. Trans. Roy.  Soc. 238: 221-348. Trehan, K. N., 1940. Studies on British whiteflies (Homoptera-Aleyrodidae). Trans. R. Ent. Soc. Lond. 90: 575-616. Vogell, W., 1965. Phasen der Bildung morphologischer und enzymatischer Muster des Flugmuskels der Wanderheuschrecke. Die Naturwissenschaften 52: 405-418. Weber, H., 1930. Biologie der Hemipteren. Julius Springer, Berling. , 1934. Die posterribryonale Entwicklung der Aleurodinen (Hemipteren-Homopteren). Ein Beitrag der Kenntnis der Metamorphose der Insekten. Z. Morph. Oekol. Tierre 29: 268-305. Weis-Fogh, T., 1956. Biology and physics of locust f l i g h t II: fl i g h t performance in the desert locust. Phil Trans.  Roy. Soc. Lond. 239: 459-510. 

Cite

Citation Scheme:

        

Citations by CSL (citeproc-js)

Usage Statistics

Share

Embed

Customize your widget with the following options, then copy and paste the code below into the HTML of your page to embed this item in your website.
                        
                            <div id="ubcOpenCollectionsWidgetDisplay">
                            <script id="ubcOpenCollectionsWidget"
                            src="{[{embed.src}]}"
                            data-item="{[{embed.item}]}"
                            data-collection="{[{embed.collection}]}"
                            data-metadata="{[{embed.showMetadata}]}"
                            data-width="{[{embed.width}]}"
                            async >
                            </script>
                            </div>
                        
                    
IIIF logo Our image viewer uses the IIIF 2.0 standard. To load this item in other compatible viewers, use this url:
http://iiif.library.ubc.ca/presentation/dsp.831.1-0104038/manifest

Comment

Related Items