Embryonic development and the systematics of the tettigoniidae (Orthoptera: Saltatoria)

Int. J. Insect Morphol. & Embryol. 1 (3): 267-287. 1972. Pergamon Press. Printed in Great Britain.

EMBRYONIC DEVELOPMENT AND THE SYSTEMATICS OF THE TETTIGONIIDAE (ORTHOPTERA: SALTATORIA) A. C. WARNE Department of Physiology and Environmental Studies, University of Nottingham School of Agriculture, Sutton Bonington, Loughborough, Leicestershire, England

(Accepted 22 May 1972) Abstract--The embryonic development of 56 species of Tettigoniidae was studied and the 4 basic patterns of development which were found are described in detail. Differences are to be found in the location of the embryonic primordium and the subsequent movements of the embryo. Representatives of the 10 subfamilies which were studied showed the developmental pattern to remain constant and thus the subfamilies may be grouped according to their developmental patterns, indicating some previously uncertain relationships. A generalised system of numbering is proposed for embryonic stages of all the Orthoptera-Saltatoria. Using this system the development of embryos of the Tettigoniidae is compared with that of embryos of other families of the Saltatoria. For the important period of physiological development between anatrepsis and catatrepsis the term mesentrepses is proposed. Index deseriptnrs (in addition to those in title): Mesentrepses. INTRODUCTION THE ONLY account that has been published on the embryology of the Tettigoniidae is that by Wheeler in 1893. This account, however, concentrated particularly on the development of organs, the embryonic membranes, and the formation of the embryonic primordium. By only comparing Xiphidium ensiferum with Orchelimum vulgate, both of which belong to the Conocephalinae, the great diversity that exists in the embryonic developmental patterns of the Tettigoniidae was not observed. By contrast the embryology of the related groups, the Gryllidae and Acrididae, has been studied in detail, and a comparison of the development of the eggs of these 2 families with those of the Tettigoniidae is given in the last part of this paper. The Tettigoniidae combine the useful features of both the eggs of the Gryllidae and the Acrididae, making them ideal for observation of embryonic development. They are as large as the eggs of the Acrididae and in many cases very much larger, and they have a chorion that may be rendered transparent, like that of the Gryllidae by immersion in certain organic solvents without harm to the embryo. M A T E R I A L S AND METHODS Adult Tettigoniidae were collected in England, France, Spain and Andorra in 1966-71 by the author and Dr. J. C. Hartley. Some species were sent from abroad and 2 species were obtained after being accidentally imported with bananas. 267

268

A.C. WARNE

The adult insects were kept in a heated greenhouse in cages containing a medium suitable for oviposition, and with as large and as varied a food supply as possible. Many species lay eggs into slightly damp cotton wool or polyurethane foam. Species that normally lay eggs in the soil were provided with dishes of sieved sand from which the eggs could be easily removed. The food requirements of the Tettigoniidae are very variable. Many are carnivorous and will eat dead locusts and tinned dog meat, some are predatory and will only feed on live insects, but the majority are omnivorous and take a small amount of animal food and much plant material. Many species feed on grass seeds as well as the foliage of many common broad-leaved weeds, apple and carrot. The eggs were collected, washed and dried and then kept on moist cotton wool in Petri dishes or specimen tubes. These were examined regularly to observe development and check the development of mould. The eggs of the Tettigoniidae are large and in many species the air layer of the chorion may be displaced with certain organic liquids, of which xylene is the most useful (Hartley, 1971) to render the chorion transparent, so that the embryo may be observed. Xylene does not harm the embryos even when the eggs are immersed for several hours. In many species the chorion is pale and reflected light may be used, in others where it is thicker or darker strong transmitted light must be used. Drawings of living embryos in the eggs were made where possible, using a stereomicroscope with a built-in drawing tube. Early stages of development were difficult to see, so for these fixed and stained preparations were used. Embryos at early stages of development were killed by puncturing the chorion with a needle in a fixative; later stages in development were killed by dipping in boiling water followed by puncturing. Puncturing eggs with a needle before killing resulted in some of the contents of the egg being expelled and the arrangement of the limbs being upset. Fixation was in Bouin's or Pampel's fluid; eggs fixed in Bouin were washed in 70% alcohol saturated with lithium carbonate to remove the picric acid. TABLE 1. PROPOSEDCLASSIFICATIONOF THE TETTIGONIIDAEBASEDON THESHAPEOFTHEHEADANDTHETRACHEALAPPARATUS(ZEUNER,1936) I

Bradyporoidea

Pseudophylloidea

Tettigonioidea

Concephaloidea Phaneropteroidea

Ephippigerinae Pycnogastrinae Bradyporinae 1 HetrodinaeDeracanthinae ?Acridoxeninae L Rammeinae (Exinct) ( Pterophyllinae Pseudophyllinae I ?Meconeminae Mecopodinae t Tettigoniinae Phyllophorinae Decticinae Saginae I Salomoninae Copiphorinae Conocephalinae Listeroscleinae L Tympanophorinae -- Phaneropterinae

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Embryos were stained with 0.2% alum carmine. Where overstaining occurred the surplus was removed with acid alcohol. Eggs were dehydrated, cleared and mounted in Canada balsam. Fully developed embryos were killed for more detailed morphological examination but were not always stained or cleared. In this paper the name Tettigoniidae is used to include all the subfamilies shown in Table 1, which shows a classification proposed by Zeuner (1936). The specific names in this account follow Chopard (1951) for European species. The names of African species were provided by the British Museum (Natural History). A list of the Tettigoniidae studied follows: Tettigoniidae studied Phaneropterinae: Barbitistes fischeri (Yersin) Leptophyes punctatissima (Bosc) Orphania scutata Brunner Phaneroptera falcata (Poda) P. quadripunctata Brunner Tylopsis lilifolia (Fabricius) Sp? Meconeminae: Meconema thalassinum (De Geer) Conocephalinae: Conocephalus conocephalus (Linne) C. discolor Thunberg C. dorsalis (Latreille) Phlesirtes merumontanus (Sjostedt) Copiphorinae: Homorocoryphus nitidulus nitidulus Scopoli H. nitidulus vicinus Walker Tettigoniinae: Tettigonia cantans (Fuessly) T. viridissima Linne Decticinae: Anonconotus alpinus (Yersin) Antaxius capelli Cazurro A. chopardi Morales Agacino A. hispanicus Bolivar A. pedestris (Fabricius) Decticus albifrons (Fabricius) D. verrucivorus (Linne) Metrioptera abbreviata (Serville) M. bicolor (Phillipi) M. brachyptera (Linne) M. roeseli (Hagenbach) M. saussuriana (Frey-Gessner) M. sepium (Yersin)

Spain England, France France France France France, Spain Brazil England, France Kenya England, France England, Belgium Kenya France, Spain Uganda France England, France France Spain Andorra, France Andorra France France, Spain Andorra, France France France, Spain England, France France France France

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Pholidoptera ehabrieri (Charpentier) P. femorata (Fieber) P. griseoaptera (De Geer) Platycleis affinis (Fieber) P. albopunctata (Goeze) P. (albopunctata) denticulata (Panzer) P. falx (Fabricius) P. intermedia (Serville) P. sabulosa Azam P. tessellata Charpentier Thyreonotus corsicus (Rambur) Yersinella raymondi (Yersin)

France France England, France France France, Andorra England France France France, Spain France, Spain Spain France, Spain

Ephippigerinae: Ephippiger cruciger (Fieber) E. cunii Bolivar E. ephippiger (Fiebig) E. provencalis (Yersin) E. terrestris (Yersin) Ephippigerida sp. (areolaria type) Platystolus obvius (Navas) Steropleurus catalaunicus Bolivar S. perezi Bolivar Uromenus rugosicollis (Serville)

France France, Spain, Andorra France France France Spain Spain Spain Spain France

Hetrodinae: Acanthoplus sp.

Africa, Botswana

Pseudophyllinae: Jamaicana flava (Caudell) .1. subguttata Walker

? Jamaica (via bananas) ? Jamaica (via bananas)

Saginae: Clonia ? sp. 1 Clonia ? sp. 2 Saga pedo (Pallas)

Botswana Botswana France

OBSERVATIONS

Numbering the Stages of Embryonic Development For numbering the stages of development of embryos of the Tettigoniidae, a system is proposed here, and it is hoped that it will be universal for the Orthoptera-Saltatoria. This system is a modification of that used by Chapman and Witham (1968) for the embryos of Acrididae. Development can be considered in 2 ways: either as a process in which there are a number of phases of activity, or as a series of growth stages where each stage is morphologically distinct. By numbering stages 1-26 rather than numbering them as subdivisions of the phases employed by Chapman and Witham the continuity of growth is retained.

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The phases o f activity are n u m b e r e d 0 - V I I , where Phase 0 is a p r e - e m b r y o n i c p h a s e when the b l a s t o d e r m is laid down. Phases I - V I I are where the g r o w t h a n d m o v e m e n t o f the e m b r y o is characteristic. Phases I I - I V together f o r m w h a t is often called blastokinesis, a l t h o u g h this t e r m is often t a k e n as being s y n o n y m o u s with catatrepsis. It is suggested t h a t Phase I I I should be called Mesentrepses as it is between anatrepsis a n d catatrepsis. This i m p o r t a n t phase o f e m b r y o n i c d e v e l o p m e n t was originally called d i a p a u s e by W h e e l e r in his w o r k on Xiphidium, b u t now this term means something entirely different. A synopsis o f the d e v e l o p m e n t o f the Tettigoniidae showing the division into phases o f activity a n d m o r p h o l o g i c a l stages is given in Table 2. TABLE 2.

SYNOPSIS OF THE EMBRYONIC DEVELOPMENT OF THE

Phase 0

Blastoderm formation Embryonic primordium: formation and differentiation

II

Anatrepsis

III

Mesentrepses

IV

Catapresis

V

Envelopment (dorsal closure)

VI

Completion

VII VIII

Prehatching Hatching

Tettigoniidae

Stage 1. 2. 3. 4.

No blastoderm Blastoderm covers half the yolk Blastoderm covers the whole yolk Embryonic primordium roughly circular

5. Embryonic primordium pear-shaped 6. Differentiation into protocephalic and protocormic regions 7. Gnathal and thoracic segmentation appears 8. Abdominal segmentation begins, limb buds tiny 9. Thoracic appendages become larger than Gnathal appendages 10. Abdomen completely segmented, proctodaeum just visible 11. Appendages begin segmentation, legs point outwards 12. Appendages become directed into the mid-line 13. Embryo broadens to almost the width of the yolk (cylindrical eggs only) 14. Embryo at posterior end of yolk, head slightly bent gack 15. Head bent back at right angles to the 16. Head and thorax bent round end of yolk, legs begin to hang free 17. Tip of abdomen only remains bent back under the yolk 18. Embryo less than half the length of the yolk 19. Embryo half the length of the yolk dorsal closure begun 20. Embryo three quarters the length of the tolk 21. Embryo almost the whole length of the yolk, only a small plug of yolk protrudes behind the head 22. Dorsal closure complete: posterior femurs short 23. Posterior femurs medium 24. Posterior femurs long 25. Spines and mandibles darken 26. Hatching

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Comparison of the development of embryos of Homorocoryphus n. vicinus (Copiphorinae), Leptophyes punctatissima (Phaneropterinae), Meconema thalassinum (Meconeminae) and Pholidoptera griseoaptera ( Decticinae) From over 50 species of Tettigoniidae that have been studied 4 contrasting patterns of development have been found. These patterns are exemplified by Homorocoryphus ii. vicinus, Leptophyes punctatissima, Meconema thalassinum and Pholidoptera griseoapter. Homorocoryphus has a long, thin, cylindrical egg, tapering gently to the anterior pole and rounded at the posterior. The embryonic primordium develops in a mid-ventral position. The egg of Pholidoptera is almost cylindrical with a slight lateral compression. It is blunter than the egg of Homorocoryphus, and the embryonic primordium develops at the posterior pole. Meconema has a much smaller egg than Pholidoptera but similar in shape. The embryonic primordium develops at the posterior pole. Leptophyes lays a laterally flattened, oval egg, in which the embryonic primordium develops at the posterior pole. Later in development the embryo of Leptophyes develops, not on the dorsal surface, but slightly to one side of it, so that embryos may be found either to the right or the left of the mid-line. Development has been studied in detail from the time of the formation of the embryonic primordium, which is the first clearly stainable stage. Earlier stages of blastoderm formation have not been examined. Leptophyes, Meconema, and Pholidoptera have been studied from the stage where the embryonic primordium is oear-shaped and the protocephalic and protocormic components are just defined. Homorocoryphus embryos were rarely found before the first traces of segmentation had become visible. As the embryonic primordium begins to elongate and become segmented, anatrepsis begins (Phase II Stage 7). This is a backward movement which in Leptophyes, Meconema,

Legends to Figures1-6 FIGS. 1-6. The scale shown against the first egg of each species is the same for all eggs of that species illustrated. Right side of Figs. 1-5 is ventral. FIG. 1.

Homoroeoryphusn. vieinusII 7a-II 8 II 7a 1I 7a II 7b II 7b II 8 II 8

ventral view ~ lateral view .j Gnathal and thoracic segmentation appears lateral view ~ ventral view j Beginning of anatrepsis lateral view ventral view Anatrepsis, abdominal segmentation begins.

I5 I6 II 7 11 7

Pholidopteragriseoaptera I 5-11 8 dorsal v i e w Embryonic primordium pear shaped lateral v i e w Differentiation into protocephalic and protocormic regions dorsal view "~ lateral view .~ Gnathal and thoracic segmentation appears

Iili 88

dorsallateral viewView ~ Anatrepsis, abdominal segmentation begins.

I5 I6 II 7 11 8

Leptophyespunctatissima I 5-11 8 (all lateral views) Embryonic primordium pear shaped Differentiation into protocephalic and protocormic regions Gnathal and thoracic segmentation appears Abdominal segmentation begins.

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and Pholidoptera is very short and on the surface of the yolk. In Homorocoryphus, however, anatrepsis involves the germ band moving through the yolk from the ventral to the dorsal side. Initially the head of the embryo points anteriorly, but after moving tail first in an arc through the yolk, the germ band rests with its head pointing posteriorly. During anatrepsis the germ band of Homorocoryphus grows considerably, doubling in length and becoming segmented. The appendages appear and begin to differentiate, so that at the conclusion of this phase the cephalic, gnathal, thoracic and abdominal regions of the embryo can be clearly seen. The germ bands of Leptophyes, Meconema and Pholidoptera begin segmentation at anatrepsis, but because this is such a brief phase, completion of segmentation and development of the appendages occur later.

11.7a

11.7b

11.7a

J

11.7b

11.8!

11.8

11.8

11.8

Homorocoryphus n vicinus

1,5

1.6

11.7

Pholidoptera

1.5 Fig.1

1.6

11.7

griseoaptera

11,7

Leptophyes punctatissima

11.8

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Anatrepsis is followed by a phase during which the segmented germ band remains stationary and undergoes considerable growth and differentiation; this phase is here called Mesentrepses. At this phase the germ band of Meconema sinks into the yolk and undergoes considerable growth, whereas the germ bands of the other 3 species remain on the surface of the yolk and show less relative growth. During mesentrepses the tip of the abdomen curls forward, and the limb buds change in alignment, become segmented and change from pointing out at right angles to the body to pointing towards the mid line and slightly backwards. In Homorocoryphus the realignment of the limb buds precedes the curling forward of the tip of the abdomen (Fig. 2, III, 10-12), whereas in Pholidoptera the 2 changes occur at about the same line (Fig. 2, III, 11 and 12). Clear signs of appendage

!:i}

) 11.9

HI,tO

II1.10

III.-'11

Homorocoryphus

II1.11

III. 11:

IlL 12

III. 12

tit.12

n. vicinus

III. 12

IV. 14

IV, 14

P h o l i d o p t er a g r i s e o a p t e r a

I|. 9 Fi9,2

111.10 Leptophyes

III. 11 punctatissima

III. 12

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segmentation do not occur until later in Homorocoryphus and Pholidoptera. In Leptophyes the tip of the abdomen becomes curled forward first, followed by the segmentation of the appendages and lastly by the realignment of the limb buds (Fig. 2, III, 10-12). During these changes the embryo becomes broader so that just before catatrepsis the heads of both Homorocoryphus and Pholidoptera are almost as wide as the yolk. At mesentrepses Meconema differs considerably from the other 3 species by its greater relative growth and its immersion in the yolk, making accurate observation of living embryos difficult. The tip of the abdomen of Meconema does not curl forward as much as in the other species, which have very much longer narrower germ bands. In Meconema the hind limbs reach almost to the end of the abdomen, whose tip bends forward at right angles to the rest of the body. Immersed in the yolk with usually only a small patch at the base of the antennae showing the embryo of Meconema grows until it almost reaches both ends of the egg (Fig. 6, III, 13). In the other 3 species the embryo at this stage of development is less than half the length of the egg, Pholidoptera and Leptophyes being within the posterior half of the egg. Some water uptake precedes catatrepsis; eggs of Homorocoryphus, Meconema and Pholidoptera take up water so that a clear fluid-filled space forms at the posterior end of the egg (Fig. 3, III, 13 and IV, 14). Leptophyes takes up water similarly and a clear margin forms between the egg shell and the yolk. Although water uptake continues in Homorocoryphus n. vicinus, which does not diapause, in the other species the main period of water uptake is after diapause, and only sufficient water is taken up before catatrepsis to form the clear space at the posterior end of the egg. The embryo of Homorocoryphus moves down the yolk from its mid-dorsal position to the posterior pole as water uptake begins. The embryo of Pholidoptera is already at the posterior pole; but in Meconema the embryo moves slightly towards the posterior pole and the anterior end of the embryo comes to the dorsal surface of the yolk. In Leptophyes the embryo becomes positioned on the dorsal surface of the yolk. Catatrepsis is similar in all 4 species. After reaching the posterior pole of the egg the embryo moves round the pole FIc. 2.

Homorocoryphus n. vicinusII 9-111 12 II 9 III 10 III 10 III 11 1II 12 1II 12

lateral view ventral view '[. lateral view .f ventral view dorsal view ~ lateral view

III 11 II1 11 III 12 111 12 IV 14 IV 14

lateral view lateral view lateral view dorsal view lateral view dorsal view f

II 9 1II 10 III 11 III 12

Leptophyespunctatissima II 9-111 12 (all lateral views) Thoracic appendages become larger than gnathal Abdomen almost fully segmented Tip of abdomen curls forward Thoracic appendages still pointing outwards.

Late anatrepsis, thoracic appendages larger than Gnathal Anatrepsis complete, mesentrepsis begins. Abdomen segmented. Thoracic appendages point towards the mid-line Tip of adbomen curls forward.

Pholidoptera griseoaptera III l I-IV 14 Mesentrepses, thoracic appendages point outwards, tip ofabdomen curls forward Mesentrepses, appendages point towards the mid-line Catatrepsis begins, head bends back round posterior pole of yolk.

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of the yolk and forward along the ventral side. The appendages are freed just as the head begins to move up the ventral side of the yolk, and then hang free into the fluid-filled space. At the end of catatrepsis, the embryo is on the ventral side of the egg with the tip of the abdomen straightened out and enclosing the posterior end of the yolk mass (Fig. 4, V, 18). After catatrepsis, the embryo grows forward and the sides of the body grow up, so that the yolk becomes enclosed (Fig. 4, V, 19 and 20). During this phase of development the embryo pulses fairly vigorously, especially in the region of the dorsal closure where the heart is forming. The body wall is thin and colourless during envelopment and for a short time afterwards the enclosed yolk is clearly visible. The appendages develop further; the maxillary palps and antennae lengthen and the tarsal segments become marked by constrictions.

111.13

IV. 14

IV, 15

IV. 16

IV. 16

IV, 17

Homorocor yphus n.vicinus

IV.15

IV.15

IV. 15

IV,15-16

IV. 16

IV.16-17

Pholidoptera griseoaptera

111,13

Fig.3

IV. 14

IV.15

Leptophyes punctatissima

IV. 16

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After dorsal closure, the embryo fills the egg; in Leptophyes, Meconema and Pholidoptera there is a further increase in size as water is taken up. Homorocoryphus, which takes up water earlier in development has already reached its maximum size by this stage. Pigment and developing tissues now mask the yellow colour of the yolk. Growth of the limbs occurs and the posterior femurs double in length and take their characteristic shape. The antennae lengthen considerably until, having reached the posterior end of the egg, they double back and extend to the base of the hind legs. Pigmentation of the eyes takes place rapidly in Homorocoryphus and in Leptophyes, Meconema and Pholidoptera, in which eye pigmentation begins just before catatrepsis, the eyes become completely darkened. The embryonic cuticle is laid down very soon after the embryo fills the egg, it is very wrinkled to allow for expansion when water uptake occurs. Just before hatching the cuticle of the first instar larva is laid down underneath the embryonic cuticle. The spines, bristles and mandibles darken just before hatching. In Pholidoptera and Leptophyes diapause occurs during Phase VI between stages 23 and 24, in Meconema during Phase I I I at stage 13 and is absent in Homorocoryphus n. vicinus although it occurs during Phase H I at stage 12-13 in Homorocoryphus n. nitidulus. After diapause water is taken up to the extent that an egg may increase its weight by 100 per cent. DISCUSSION

Comparison of development in the Tettigoniidae As already mentioned 56 species of Tettigoniidae have been studied and 4 contrasting patterns of development have been found. The species here used to exemplify these patterns all belong to different subfamilies. Homorocoryphus belongs to the Copiphorinae, Leptophyes to the Phaneropterinae, Meconema to the Meconeminae and Pholidoptera to the Decticinae. The 56 species studied fall into 10 subfamilies and within each subfamily the major pattern of development has been found to be the same. Grouping the subfamilies according to their mode of development reveals some possible affinities. FIG. 3.

Homorocoryphus n. vicinus III 13-IV 17 III 13 IV 14

lateral view lateral view

IV IV IV IV

15 16 16 17

lateral lateral lateral lateral

IV IV IV IV IV IV

Pholidopteragriseoaptera IV 15-IV 16-17 15 dorsal view ~ 15 ventral view Head of embryo bent round posterior pole of yolk 15 lateral view .J 15-16 lateral view Eyes begin to show distinct pigmentation 16 lateral view Head begins to move up ventral side of yolk 16-17 lateral view Limbs become free, head and thorax move up ventral side of yolk.

III 13 IV 14 IV 15 IV 16

view view view view

Mesentrepses embryo considerably broader Catatrepsis begins, embryo moves to posterior end of egg and head bends back Head bent back at right angles to rest of body Head and thorax bent round posterior pole of yolk Limbs become free Head and thorax move up ventral side of yolk.

Leptophyes punctatissima III 13-IV 16 Mesentrepses--embryo broadens considerably Catatrepsis begins, embryo on dorsal edge of yolk Embryo begins to move round posterior pole of yolk Limbs become free.

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Homorocoryphus was the only genus of the Copiphorinae available, but the 3 species of the Conocephalinae studied show great similarity. The eggs of these species are very similar in appearance, and development of the embryo follows the same pattern. Xiphidium ensiferum (Scudder) and Orchelimum vulgate (Harris), whose embryology was studied by Wheeler (1893), are also members of the Conocephalinae and their development seems to be identical with that of Homorocoryphus and Conocephalus. The development of Jamaicana, the only representative of the largest subfamily of the Tettigoniidae--the Pseudophyllinae--is similar in most respects to Homorocoryphus. The egg bears no resemblance to the eggs of the Copiphorinae or Conocephalinae, being large

IV, 17

IV. 17

V.19

V. 19

V. 20

V. 20

Homorocoryphus n. vicinus

IV.17

V, 18

V.19

V. 21

V,19

V. 21

Pholidoptera griseoaptera

V.18

Fig.4

V.19

V.20

Lept ophyes punctatissima

V. 21

Embryonic Development and the Systematics of the Tettigoniidae

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and thick shelled and having a complex anterior respiratory structure. The development is similar to that of Homorocoryphus in that the earliest stages of development are ventral and the embryos pass through the yolk at anatrepsis. The embryonic primordium, however, develops nearer the posterior end and in all stages prior to catatrepsis the embryo remains within the posterior half of the egg. After anatrepsis, limb realignment takes place before the tip of the abdomen curls forward, as in Homorocoryphus. The Decticinae, as exemplified here by Phoh'doptera, is a very diverse subfamily and it is not possible to find a species that is entirely typical. The shape of the eggs varies considerably. For example, short broad eggs are laid by Decticus, slightly laterally flattened eggs by Pholidoptera, small thin tapered eggs by Yersinella and eggs that are not tapered and are almost square ended by Metrioptera roeseli. The egg of Yersinella is similar in shape to the egg of Conocephalus. The eggs also vary in pigmentation and in the structure of the chorion. Despite these differences, development in all the species studied is the same as in Pholidoptera. Similar developmental patterns have also been found in the genus Tettigonia (subfamily Tettigoniinae). The developmental pattern in eggs of Saga pedo (subfamily Saginae) is basically the same as is found in the Decticinae, the embryonic primordium being formed on the posterior end of the egg. The fully developed embryo differs little from those of the Decticinae. The eyes are a little more prominent and at the posterior end of the abdomen the rudiments of the ovipositor valves are clearly indicated by small bumps. The Ephippigerinae are much more uniform in the shape of their eggs and nearly all are slightly laterally compressed when laid, like those of Pholidoptera. Ephippiger terrestris lays eggs which, although larger than those of Homorocoryphus, are similar in being long and narrow. However, the embryo develops in the same manner as Pholidoptera, as do the rest of the Ephippigerinae examined which have shorter broader eggs. The development of the Hetrodinae has been found to be similar to that of the Ephippigerinae in the only species studied, Acanthoplus sp.

Fro. 4

Homorocoryphus n. vicinusIV 17-V 20 IV 17 IV 17 IV 19 IV 19 IV 20 IV 20

ventral view ~ Catatrepsis almost complete, only tip of abdomen remains on dorsal lateral view f side of yolk ventral view ~ lateral view Embryo occupies over ½ length of egg, dorsal closure begins ventral view ~ Embryo occupies over ¼ length of egg. lateral view f

IV 17 VI8 VI9 V19 V21 V 21

Pholidopteragriseoaptera IV 17-V 21 ventral view Only tip of abdomen remains on dorsal side yolk lateral view Tip of abdomen "hooked" onto posterior pole of yolk ventral view ~ lateral view Embryo occupies ½ length of egg, dorsal closure begins ventral view ~. Embryo occupies almost whole of egg, small plug of yolk protrudes lateral view f behind the head.

VI8 V 19 V 20 V 21

Leptophyespunctatissima V 18-V 21 Catatrepsis complete Dorsal closure begins, embryo occupies ½ length of egg Embryo occupies ¼ length of egg Embryo occupies almost whole egg, small plug of yolk protrudes behind head.

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All the species of the Phaneropterinae studied had oval eggs that were strongly compressed laterally, like that of Leptophyes, and in which the embryos all developed in exactly the same manner. The development of Leptophyes may be regarded as a variation of that of Pholidoptera, the principal difference being caused by the lateral compression of the egg. It would be interesting to compare this with the development of Steirodon validum, the egg of which was illustrated by Cappe de Baillon (1922) and appears to be more rectangular than oval and much less compressed. Meconema was the only species of the Meconeminae studied and because this species is so unlike all the others studied it would be of great interest to compare it with the related genera Canariola and Cyrtaspis. / f

Vl. 22

VI. 22

Vl.23

VI.23

VI.24

VI.24

Homorocoryphus n.vicinus

VI.22

VI.22

VI.23

VL23

VI,24

VI.24

Pholidoptera griseoaptera

VI.22 Fig.5

VI.23

VI.24

L eptophyes punctatissima

ii

VII.25

Embryonic Development and the Systematics of the Tettigoniidae

281

As the result of grouping the 10 subfamilies studied according to their pattern of embryonic development 4 major groups are formed: the Decticinae, Ephippigerinae, Hetrodinae, Saginae and Tettigoniinae: the Copiphorinae, Conocephalinae and Pseudophillinae: the Phaneropterinae: and the Meconeminae. Egg.shape and size have no effect on the mode of development except perhaps in the case of the Phaneropterinae, and the pattern of development of a tettigoniid embryo is related solely to its phylogenetic position. If this grouping is justified then some important conclusions may be drawn. The classification of the Tettigoniidae prior to the work of Zeuner (1936) consisted of the division of the family into a large number of subfamilies with little attempt to relate them. Zeuner grouped the subfamilies after studying the shape of the head and the prothoracic tracheal apparatus; 5 groups were distinguished on this basis (Table 1). The Bradyporoids were clearly shown as the most primitive and the Pseudophylloids were also separated from the rest of the Tettigoniidae through being less advanced in some respects. The Tettigonioids and Conocephaloids, he suggested, may be related and may have originated from a common ancestor. The Phaneropteroids are a homogenous group and are somewhat isolated from the rest of the Tettigoniidae. Embryonic development within the subfamily groups appears to be similar although representatives of only 10 out of about 20 subfamilies were studied. The linking of these groups according to their mode of development, however, suggests very different relationships from those proposed by Zeuner. The Bradyporoid group is said to be one of the most primitive in many respects, but the similarity in development between this group and the Tettigonioids suggests that they are derived from the same stock. The Phaneropteroids although some of their characters indicate that they are not closely related to the other groups, could have developed from the same stock as the Bradyporoid-Tettigonioid ancestor. There is, however, no evidence for any connection between the Conocephaloids and Tettigonioids, but strong evidence for a link between the Conocephaloids and the Pseudophylloids.

VI VI VI VI VI VI

22 22 23 23 24 24

FIG. 5. Homorocoryphus n. vicinus VI 22-VI 24 lateral view ~_ Dorsal closure complete, body wall still fairly transparent ventral view . f Posterior femurs short lateral view ~ Pigmentation and developing tissues mask colour of yolk. Posterior ventral view f femurs medium length lateral view ~ ventral view Embryo fully formed, posterior femurs full length.

VI VI VI VI VI VI

22 22 23 23 24 24

lateral view ventral view lateral view ventral view lateral view ventral view

VI VI VI VI

22 23 24 25

Leptophyespunctatissima VI 22-VII 25 Dorsal closure complete, posterior femurs short Body wall still fairly transparent. Posterior femurs medium length Pigmentation and developing tissues mask colour of yolk. Posterior femurs full length Pre-hatching spines and bristles of 1st instar cuticle darkened.

~ f ~. f ~

Pholidoptera griseoaptera VI 22-VI 24 Dorsal closure complete, body wall still fairly transparent. Posterior femurs short Pigmentation and developing tissues mask colour of yolk. Posterior femurs medium length Embryo fully formed, posterior femurs full length.

282

A.C. WARNE

IILll

F i g .6

III.1Z

111.13

Meconema

IV.14

IV.15

IV,17

thalassinum.

FI6. 6. Meconema thalassinum III 1l-IV 17 Upper row dorsal except 1V 17 which is ventral. Lower row lateral. Right side is dorsal. Ili 11 Mesentrepses, embryo completely immersed in yolk. Tip of abdomen only slightly curled forward. 11I 12 Labrum and base of antennae visible on surface of yolk. III 13 Embryo undergoes considerable growth occupying almost whole egg. 1V 14 Catatrepsis begins, embryo moves towards posterior pole, head emerges from yolk. IV 15 Head and thorax bend round posterior end of yolk, abdomen still immersed, limbs not free. IV 16 Catatrepsis almost complete, embryo fully emerged from yolk.

M e c o n e m a shows such a different pattern of development to the other m e m b e r s of the Tettigoniidae that it must be placed separately rather t h a n tentatively with the Tettigonioids as in Z e u n e r ' s arrangement. Table 3 shows a regrouping of the subfamilies based on their e m b r y o n i c development.

Embryonic Developmentand the Systematicsof the Tettigoniidae

283

TABLE 3. G R O U P I N G OF THE SUBFAMILIES OF THE TETTIGONIIDAE BASED ON THEIR EMBRYONIC DEVELOPMENTAL PATTERNS

Meconemoidea Phaneropteroidea

-- Meconeminae -- Phaneropterinae ~ Ephippigerinae Bradyporoidea Hetrodinae ~ Tettigoniinae Tettigonioidea Decticinae Saginae Pseudophylloidea -- Pseudophyllinae ~ Copiphorinae Conocephaloidea Conocephalinae

(Phlesirtes merumontaeus)

Phlesirtes merumontanus, a Kenyan species, is dubiously classified as a member of the Decticinae (Uvarov 1923). However, observations of its embryology show that it develops in the same manner as the Conocephalinae and this is further supported by the shell structure, which is clearly conocephaline (Hartley, 1964 and personal communication, 1969). Thus the taxonomic position of this species is indicated by the study of its embryology. Comparison of embryonic development in the Tettigoniidae with that of other Saltatoria Accounts of the embryology of several species of Saltatoria have been published, mostly concerning species of economic importance, particularly locusts and allied species. The Gryllidae and Tettigoniidae have been neglected and only accounts of Oecanthus niveus (Ayers, 1883), Gryllotalpa gryllotalpa (Korotneff, 1884), Xiphidium ensiferum (Wheeler, 1893), Tachycines asynamorus (Krause, 1938), Teleogryllus commodus (Brookes, 1952) and Gryllus assimilis (Rakshpal, 1962) give any detail of the embryology of these two families. In these accounts, various numbering systems have been used. The system outlined earlier is now proposed as suitable for all Saltatoria. Table 4 compares other numbering systems and further comparison can be found in Chapman and Witham (1968). The use of a double notation allows flexibility so that exceptional cases may be numbered according to the same scheme. For example, an exceptional species may develop morphologically to a particular stage yet may be in a different phase of activity. Using appropriate phase and stage numbers the exception can be clearly shown. Comparison of the Tettigoniidae, Gryllidae and Acrididae has been complicated by problems of interpretation of the orientation of the eggs and embryos. In the Tettigoniidae the micropyles are clearly placed ventrally towards the posterior end. In the Gryllidae the micropyles are much more variable; they may be found round the middle of the egg or as in Acheta in a mid-ventral position, but are very small and difficult to see. In Acheta they are not suitable for use for orientation as they can only be detected by microscopic examination of flattened egg shells. In Tachycines the micropyles are on the posterior pole and in Oecanthus Ayers indicates them as being on the anterior end of the egg. In the Acrididae the micropyles are larger and in a distinct ring round the posterior end. Consequently egg shape has been used for orientation; in Acheta, however, curvature is not a prominent feature and is lost as soon as water absorption takes place. In accounts of the development of Gryllus assimilis and Teleogryllus commodus the dorsal surface of the egg is described as convex and the ventral surface as concave. This differs from Homorocoryphus, where

284

A.C. WARNE

the dorsal side is concave and the ventral convex. In accounts of the embryology of the Gryllidae and Acrididae the embryo appears to develop upside down compared with the Tettigoniidae, but for present purposes of comparison the orientation is assumed to be the same as in the Tettigoniidae. TABLE 4.

Tettigoniidae

COMPARISON

OF SCHEMES F O R C L A S S I F Y I N G E M B R Y O S OF S A L T A T O R I A

Acrididae (Chapman and Witham, 1968)

Phase Stage --

1

0-I

II

2 3 4 5 6 7 8

9 10 11 III 12 --13 14 1V 15 16 -17 18 V 19 20 -21 22 VI 23 -24 V I I - 25 V I I I - 26

0

Gryllulus,commodus

Gryllus assimilis

(Brookes, 1952) (i) (ii)

(Rakshpal, 1962)

a

b 1

--

C

a

A

1

--

b

B

2

II - - a+b a Ili b --

IV --

V --

C D E

c

F-G

a b

H-I J K

c

L

a a b

M

3-4 5-6 7 8

9 10 11 12

Vc VI Via

C

VIb O P

VII

IX

Vb

13 N

VI

VIII

1 1I llI IV V Va

a a--b b

Q R

14-14a 15 16 17-18 19-20 21-22 23

VII VIII IX IX X

Gryllotalpa is an exception; its eggs are small and round, and its embryology is consequently very different from other Saltatoria. The account of the embryology of Gryllotalpa by Korotneff (1894) is very detailed histologically and anatomically but lacks details of the embryonic movements. The embryo goes through the same phases of development as other Saltatoria but because of this lack of detail it is omitted from this account. The embryos of most Gryllidae and Acrididae start development at the posterior pole of the egg in a similar way to Meconerna and Pholidoptera, but Oecanthus develops slightly ventrally. Early growth in Gryllid embryos is forward rather than backward. The protocephalon grows forward on to the dorsal side of the yolk, while the end of the protocorm remains on the tip of the yolk. At anatrepsis these embryos go through a U-turn on to the ventral side of the yolk, rather like Homorocoryphus, except that they remain on the surface the whole time. In the Gryllidae as in Meconerna the embryo sinks into the yolk at mesentrepses but in Teleogryllus cornmodus and Gryllus assimilis the embryo revolves on its axis and later emerges from the yolk on the dorsal surface whereas the embryos of Meconema has its ventral surface towards the dorsal side of the egg throughout this period. In Oecanthus there appears to be no anatrepsis. Many authors apparently overlook

Embryonic Development and the Systematicsof the Tettigoniidae

285

anatrepsis in the Acrididae and refer to catatrepsis only. Shulov and Pener (1963) describe anatrepsis in Schistocerca gregaria as a slight movement backwards where the head may remain touching the micropylar end or move slightly away from it. This is much the same as in Leptophyes, Meconema, and Pholidoptera though even less distinct (Fig. 1, I, 6; II, 7 and 8). The tip of the abdomen does not curl forward at mesentrepses in the Acrididae, whereas embryos of the Gryllidae behave in the same way as those of the Tettigoniidae. The tip of the abdomen curls forward and appendage segmentation begins in Gryllus assimilis and Teleogryllus commodus before the reorientation of the limb buds. The limb buds of the Acrididae develop pointing backwards and only a slight change in orientation can be seen at this stage as they come to point slightly more towards the midline. During mesentrepses embryos of the Acrididae and Gryllidae broaden considerably just as do those of the Tettigoniidae; and at this stage some water is taken up. Catatrepsis and envelopment of the yolk proceed exactly as in the Tettigoniidae (Phases IV and V). At the end of completion (Phase VI) some Acrididae revolve on their longitudinal axes so that their dorsal and ventral surfaces correspond to those of the egg. In Austroicetes cruciata the embryo may develop either dorsally or ventrally, but only those that develop ventrally revolve at completion (Steele, 1941). Embryos of Melanoplus differentialis all revolve (Slifer, 1932) though this is not mentioned as occurring in Schistocerca gregaria (Shulov and Pener, 1963) or Locustana pardalina (Mathee, 1951). There are a number of small differences in the fully developed embryos, such as the shorter antennae of Acridid embryos and the very long cerci that reach across the abdominal segments in Gryllid embryos. Just before hatching the spines, bristles and mandibles of the first instar cuticle darken. Hatching differs slightly in that embryos of the Acrididae rely solely on the digestion of the white cuticle of the egg to weaken the shell, whereas the embryos of the Gryllidae and Tettigoniidae cut the shell using the sawlike hatching organ on the head of the embryo. The Gryllidae also weaken the chorion to some extent by digestion. The embryology of species of the Gryllidae and Acrididae is the same throughout each family, quite unlike the Tettigoniidae, where considerable differences exist between some of the subfamilies. Meconema might be regarded as a link between the basic TettigoinoidBradyporoid pattern and that of the Gryllidae. Certainly it forms a link between the basic Tettigoniid pattern and the Raphidophoridae where Tachycines asynamorus (Krause, 1938) develops in a similar manner to the Gryllidae although being classified close to the Tettigoniidae. In the Heteroptera a similar diversity occurs in the development of embryos (Cobben, 1968) and many similar problems of the interpretation exist. The eggs are more difficult to orientate and have been shown to change their orientation in the oviduct, their structure too is more complex and Cobben suggests that the surrounding egg system is best ignored initially on the assumption that the early germ band gives the best guarantee for purposeful first comparison. In the Tettigoniidae at present it is not possible to suggest that the superficial embryos are more advanced than immersed ones as is possible in the Heteroptera, although the only immersed species at present known, Meconema, is undoubtedly primitive. Cobben concludes from the embryonic evidence that the Heteroptera of the present day had a polyphyletic origin. This is probably also the case in the Tettigoniidae where evidence of a relationship between the four groups is lacking.

286

A.C. WARNE CONCLUSIONS

There are 4 distinct patterns of embryonic development in the Tettigoniidae. These differ firstly in the position in which the embryonic primordium develops, posteriorly or mid-ventrally; and secondly in the movement of the embryo before catatrepsis. Firstly, during anatrepsis the germ band either moves slightly on the surface of the yolk from the posterior pole to the dorsal surface, or undergoes a considerable movement through the yolk from the mid-ventral to the mid-dorsal surface. Secondly, the embryos that originated posteriorly may, between anatrepsis and catatrepsis (here called mesentrepses), lie on the dorsal surface, lie slightly laterally, or become immersed in the yolk. Fifty-six species belonging to 10 subfamilies were examined and it was found that the pattern of development within each subfamily was the same. By grouping subfamilies with common developmental patterns some hitherto unsuspected affinities were revealed. The embryonic primordium of Copiphorinae, Conocephalinae and Pseudophillinae develops mid-ventrally and at anatrepsis movement is through the yolk. The embryonic primordium of Decticinae, Ephippigerinae, Hetrodinae, Saginae and Tettigoniinae develops posteriorly and the embryo remains on the surface of the yolk at all stages of development. The Phaneropterinae differ little from the Decticinae except that the development of a strongly laterally compressed egg has resulted in the embryos being displaced slightly to one side of the mid-line. The embryonic primordium of M e c o n e m a (Meconeminae) like that of the Decticinae originates at the posterior pole of the egg but the embryo becomes immersed later in development and grows much larger relative to the size of the egg prior to catatrepsis. The grouping of these subfamilies is compared with that of Zeuner (1936) and with the embryonic development of other members of the Orthoptera-Saltatoria. M e c o n e m a in particular has some affinities with the Raphidophoridae and perhaps the Gryllidae. One species examined, Phlesirtes m e r u m o n t a n u s , previously dubiously classified as a member of the Decticinae, was found to resemble the Copiphorine-Conocephaline group in its pattern of development. To simplify the comparison of the embryonic stages of the Tettigoniidae with those of other members of the Orthoptera-Saltatoria a system is proposed that is suitable for classifying all embryos of the Saltatoria. In this classification the name Mesentrepses is proposed for the important period of development between anatrepsis and catatrepsis. thank Professor E. J. W. Barrington for providing the facilities of the Department of Zoology of the University of Nottingham. I also thank Dr. J. C. Hartley for his guidance and his readiness to discuss problems throughout the course of this work. A number of the species used in this research were sent from abroad for which I would like to thank Dr. R. E. Roome, Dr. L. S. Otero, Mr. W. B. Broughton, Dr. B. Dumortier, Mr. C. R. Pashley, Miss E. Berger and Miss S. Faggiter. Acknowledgements--I

REFERENCES AVERS, H. 1883. On the development of Oecanthus niveus and its parasite Teleas. Mere. Boston Soc. Natur. Hist. 3: 225-81. BODENHEIMER,F. S. and A. SHULOV. 1951. Egg development and diapause in the Maroccan locust Dociostaurus maroccanus. Bull. Res. Coun. Israel. 1: 59-75. BROOKES,H. M. 1952. The morphological development of the embryo of Gryllulus commodus (Walker) (Orthoptera Gryllidae). Trans. Roy. Soc. South Australia 75: 150-9. CAPPE DE BAILLON, P. 1922. La reproduction chez les Locustiens et les Grilloniens--l. La ponte et l'eclosion chez les Locustiens. La Cellule 31: 1-245. CrtAVMAN,R. F. and F. WtTHAM.1968. The external morphogenesis of grasshopper embryos. Proc. Roy. Entomol. Soc. London (A) 43: 141-89.

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CHOPARD,L. 1951. Orthopteroides. Fauna de France 56. Le Chevalier, Paris. COBBEN, R. H. 1968. Evolutionary trends in Heteroptera. Part 1. Eggs, architecture of the shell, gross embryology and eclosion. Centre for Agricultural Publishing and Documentation, lYageningen. HARTLEY, J. C. 1964. The structure of the eggs of the British Tettigoniidae. Proc. Roy. Entomol. Soc. London (A) 39: II 1-17. HARTLEY, J. C. 1971. The respiratory system of the egg shell of Homorocoryphus nitidulus vicinus (Orthoptera Tettigoniidae)J. Exp. Biol. 55: 165-76. JHINGRAN, V. G. 1947. Early embryology of the desert locust Schistocerca gregaria (Forsk). Rec. Indian Mus. 45: 181-200. JOHANNSEN, O. A. and F. H. BUTT. 1941. Embryology o f lnsects and Myriapods. McGraw-Hill, New York. KOROTNEFE, A. 1885. Die Embryologie der Gryllotalpa. Z. wiss. Zool. 41: 570-604. KRAUSE, G. 1938. Einzellesactungen und typische Gesamtbilder der Entwicklung von Blastoderm und Keimalage im E i d e r Gew/ichshausschrecke. Tachycines asynamorus (Adelung). Z. Morphol. Oekol. Tiere 34: 1-78. KRAUSE, G. 1938. Die ausbildung der K6rpergrundgestalt im Ei der Gew~ichshausschrecke Tachycines asynamorus (Adelung). Z. Morphol. Oekol. Tiere 34: 499-564. MATTHEE. J. J. 1951. The structure and physiology of the egg of Locustana paradalina. Sci. Bull. Dept. Agr. South Africa No. 316. PENER, M. P. and A. SHULOV. 1960. The biology of Caliptamus palaestinensis (Bdhmr) with special reference to the development of its eggs. Bull. Res. Coun. Israel 93. RAKSHPAL, R. 1962. Morphogenesis and embryonic membranes of Gryllus assimilis F. (Orthoptera Gryllidae). Proc. Roy. Entomol. Soc. London (A) 37: 1-12. SALT, R. W. 1949. A key to the embryological development of Melanoplus bivittatus Say., M. mexicanus mexicanus Sauss, and M. packardii Scudder. Can. J. Res. D. 27: 233. SALZEN,E. A. 1960. The growth of the locust embryo. J. Embryol. Exp. Morphol. 8: 139-62. SHULOV,A. and M. P. PENNER. 1963. Studies on the development of eggs of the Desert Locust Schistocerca gregaria Forsk., and its interruption under particular conditions of humidity. Anti-Locust Bull. 41. SLIFER, E. H. 1932. Insect development--IV. External morphology of grasshopper embryos of known age and with known temperature history. J. Morphol. 53: 1-22. STEELE, H. V. 1941. Some observations on the embryonic development of Austroicetes cruciata Sauss (Acrididae) in the field. Trans. Roy. Soc. South Australia 64: 329-32. UVAROV, B. P. 1923. Notes on the Orthoptera in the British Museum 3. Some less known or new genera of the subfamilies Tettigoniinae and Decticinae. Trans. Roy. Entomol. Soc. London 71 : 492-537. VAN HORN, S. N. 1966. Studies on the embryogenesis of Aulochara elliotti. 1. External morphogenesis. J. Morphol. 1211:83-114. WHEELER,W. M. 1893. A contribution to insect embryology. J. Morphol. 8: 1-160. ZEUNER, F. E. 1936. The subfamilies of the Tettigoniidae (Orthoptera). Proc. Roy. Entomol. Soc. London (B) 5: 103.