BULLETIN DE L'INSTITUT ROYAL DES SCIE 1CES NATURELLES DE BELGIQUE ENTOMOLOGIE. 70: 13-31 . 2000 E TOMOLOGIE. 70: , 13-31,2000 BULLETIN VA I-l ET KONINKLIJK BELGISCH I STITUUT VOOR NATUURWETENSCHAPPEN

Flight muscle developtnent and dispersal in the life cycle of carabid beetles: patterns and processes

by Konjev DESENDER

Abstract

Seasonal patterns of flight muscle development are documented fo r 27 carabid species, collected from di fferent habi tats. The phenology or timing of their life cycle is compared to the presence o f a functional flight apparatus during complete year cycles. The majori ty of the investigated ground beetles have never been stud ied before in this respect. In most species there is a distinct seasonal pattern of flight muscle functionality. Some species, with similar life cycle timing and/ or s imilar habitat requirements, show the same pattern of flight muscle development. Inter- and intraspecific variability in maximal propor­tions o f beetles with functi onal flight muscles indicates flight muscle dimorphism. The reproductive state of females (obta ined through dis­sect ion of the ovaries) is used to test the generality of an "oogenesis­flight syndrome" (trade-off between dispersal and reproduction), the null hypothesis being that functional fl ight musculature and ripe ova­ries occur independently. Observed signi fican t deviations towards a higher proportion of beetles with fi.mctional fl ight muscles in unripe as compared to ripe females indicate such a syndrome in most of the species studied. It is especially true for species emerging during late spring before their summer-autumn reproduction. The proportion of ripe females w ith functional flight muscles d iffers between species and can be used as a measure for a less deterministic version of an "oogenesis-flight" syndrome. A complex of fac tors must play a ro le in the expression of flight muscle development. Integration of all results suggests habitat choice, evolu tion of life cycle timing and other life history traits as ultimate factors responsible for the observed patterns of flight muscle functionali ty. Flight muscle development in ground beetles therefore seems to be part of a suite of coadapted traits.

Key wonls: Carabidae, dispersal power, life cycle, flight muscle development, oogenesis-flight syndrome, reproduction, w ing dimor­phism, adaptations, sui te of coadapted tra its

Resume

Les pro til s sa isonniers du developpement des muscles a lai res sont reportes pour 27 especes de Carabidae, reco ltees dans des habitats d iffe rents. Durant des cycles annuels complets, Ia phenologie ou Ia periode du cycle vital est comparee pour chaque espece i1 Ia presence d ' un appare il devol fonctionnel. La majorite des especes de Carabidae concernees n ' a j amais ete etudiee SOLIS eel angle avant ce travai l. Chez Ia plupart des especes, il y a un cycle saisonnier de Ia fonctionnali te des muscles ala ires. Certaines especes qui ont un cycle de vie et/ou des ex igences environnementales s imila ires demontrent le meme profil sa isonnier au niveau des muscles devol. Si l' on considi:re Ia periode du cycle de vie otl le developpement des musc les de vol est le plus important, on constate une variabilite inter- et in traspecifique, ce qui suggere un dimorphisme de muscles a lai res. L 'eta! reproducti f des femelles (obtenu apres d issection des ovaires) est utilise pour tester Ia presence d ' un " oogenesis-fl ight syndrom.e" (balance entre disper­sion et reproduction), !' hypothese nulle etant qu· une musculature alaire fonctionnellc et Ia maturi te des ovaires apparaissent independamment.

Les deviations significatives observees pour une proportion plus im­portante de coleopteres avec des muscles de vols fonctionnels chez des femelles non matures en comparaison avec ce lles matures indiquent un tel syndrome chez Ia plupart des especes de Carabidae etudiees. Ceci s ' applique surtout aux especes qui emergent a Ia fin du printemps, j uste avant leur periode de reproduction en ete-automne. Le pourcentage de femelles matures avec des muscles a laires fonctionnels d iffere entre espi:ces et peut etre utilise comme une mesure d ' un "'oogenesis-flight syndrome" ma ins determin iste. L'analyse g lobale de tous les resultats suggere que les caracteristiques suivantes interviennent comme fac­teurs expliquants les profil s observes au niveau des muscles de vol: choix de !'hab itat, evolution du cycle de vie, ainsi que d'autres e ie" ments de Ia vie de l' insecte. Le developpement des muscles devol des Carabidae semble di:s lors faire partie d ' un ensemble de caracteres coadaptes.

Mots-clefs: Carabidae, pouvoir de dispersion, cycle de vie, developpe­ment des muscles ala ires, oogenesis-flight syndrome, reproduction, dimorphisme alaire, adaptations, caracti:res coadaptes

Introduction

[n many insect groups, species are known to show poly­morphisms affecting their fl ight ability. The most obvious examples are variations in wing and flight muscle devel­opment (HARRISON, 1980). Wing polymorphisms are un­der genetic and environmental control (HARRISON, 1980; ROFF, 1986).

Numerous observations indicate that in many insect species migration is limited to the post-teneral, pre-re­productive period. These observations have led to define the " oogenesis-flight syndrome" as a characteristic of insect migration (JOHNSON, 1969; for Coleoptera, see f. e. LlNDERS et a\., 1995, MUDA et a\. , 198 1, RANKIN et a\. , 1994, TADA et al. , 199 1 ). The inherent assumption is that migration (through flight dispersal by means of func­tional fl ight muscles and developed hind wi ngs) and reproduction are alternating physiological states. This view was strengthened by the fact that migration in many cases is associated with or induced by conditions promo­ting adult diapause (i.o.w. delaying reproduction), for example a shorter photoperiod, lower temperatures or poor food conditions (RANKIN et a\. , 1986). Migrating insects moreover often are physiologically comparable to cliapausing insects in their possession of hypertrophic fat bodies and immature ovaries. Studies on the physio-

14 Konjev DESENDER

logy and endocrinology of flight muscle degeneration and regeneration, in a few insect species, have suggested a control by juvenile hormone (FAIRBAIRN & Y ADLOWSKI, I 997; ZERA et al., 1997). A strong negative correlation has commonly been observed between flight muscle mass and ovarian mass of insects (ROFF, I 986), suggesting that the construction and maintenance of the flight apparatus competes with egg production for a limited internal nu­trient pool (ZERA & DENNO, 1997). The metabolic rates of flying insects can be 20-100 times that of resting animals and are among the highest known (RANKIN & BURCHSTED, 1991 ). Nevertheless, several authors ( cf. GATEHOUSE & ZHANG, 1995) have challenged the assumption that the oogenesis-flight syndrome is a general phenomenon.

Ground beetles are well-known for their varying de­gree of hind wing development. Some species are con­stantly winged, others show a wing polymorphism or wing dimorphism and some species always possess re­duced wings. Carabid beetles consequently exhibit a large amount of variation in their respective dispersal power. Wing development is largely under direct genetic control in the few ground beetle species studied so far (cf. Au­KEMA, 1986; DESENDER, 1989a; LINDROTH, 1946). About three-quarters or as much as 280 carabid species from Belgium are known to be constantly macropterous or full­winged. Nevertheless wing development and, as a con­sequence, flight capacity are extremely variable between winged species too, as has been shown on the basis of a biometric approach (DEN BOER et al., 1980; DESENDER et a!., 1986; DESENDER, 1989b ). Many winged ground beet­les moreover not necessarily possess functiona l flight muscles. Below a certain value of relative wing size, functiona l flight muscles apparently are only rarely ob­served (DEN BOER et a!., 1980; DESENDER, 1989b ).

Genetic studies on flight muscle development have not yet been performed in ground beetles, with one excep­tion: NELEMANS ( 1987) showed that there is no simple genetic basis for flight muscle development in Nebria brevicollis. However, genetic studies on other beetles (two species of Scarabaeidae; T ADA et a!., 1993, I 994, 1995) have demonstrated genetic flight muscle dimor­phism, besides environmental control of flight muscle development. Seasonal changes in the proportions of carabid beetles with functiona l flight musculature for a given species could suggest phenotypic plasticity and point to environmental conditions possibly influencing flight muscle development. Some studies have shown that proportions of beetles with flight capability differ be­tween species. Seasonal aspects, however, usually were not included. Such data could nevertheless suggest whether there is some kind of dimorphism or polymorph­ism in the determination of flight muscle functionali ty.

The current knowledge on seasonal variation in flight muscle development as compared to adult life cycle of ground beetles is limited to some five species only. Amara plebeja, reproduci ng during spring and hiberna­ting as adult, showed a strict "oogenesis-flight" syn­drome: migration occurs during autumn (post-teneral), but also during spring (after hibernation and before Te-

''

production) and is related to habitat change (TIETZE, 1963; VAN HuiZEN, 1977). Flying females were always unripe. According to DEN BOER eta!. ( 1980) some species (Amara.familiaris, Anisodactylus binotatus, Calathus ro­tundicollis and Nebria brevicollis) deviate more or less from an "oogenesis-flight" syndrome. In Nebria brevi­col/is developing flight muscles were found in immature beetles (i.e. in spring) more than in reproducing beetles (in autumn), while at least some flight activity was ob­served during autumn too (N ELEMANS, 1987). MATALIN ( 1994, 1997) and ZHANG et a!. ( 1997) studied Harpalus rujipes and came to the conclusion that flight was more prevalent in (but not limited to) young beetles before reproduction. MEIJER ( 1974) suggested variation in flight behaviour of the small Bembidion varium (always posses­sing functional flight muscles): in spring relatively more unripe females were recorded flying as compared to reproducing ones.

Clearly, there is a considerable lack of empirical data on most carabid beetles in this respect. To this end, we have dissected large numbers of ground beetles collected during complete year cycles in a multitude of habitats and belonging to 27 different species (20 constantly macro­pterous, seven wing dimorphic or polymorphic). These species can be roughly divided into spring breeders (adult hibernators) on the one hand and summer-autumn bree­ders (larval or larval/adult hibernators) on the other hand.

In this paper, we will first look at seasonal patterns of flight muscle development by comparing the phenology or timing of the life cycle in each species to the relative occurrence of a functional flight apparatus. Secondly, the reproductive state of females (obtained through dissec­tion of the ovaries) will be used to test the generality of an "oogenesis-flight syndrome", the null hypothesis being that functional flight musculature and ripe ovaries occur independently. A significant deviation towards a higher proportion of beetles with functional flight mus­cles in unripe females as compared to ripe females would be an indication for such a syndrome. The percentage of ripe females with functional flight muscles can be used as a measure for a less deterministic version of an " oo­genesis-flight" syndrome. Results for species with dif­ferent life cycle timing will finally be compared in an attempt to give ultimate explanations or underlying evo­lutionary processes responsible for the observed variabi­lity and timing of the presence of functional flight mus­culature.

Material and Methods

Two groups of indirect flight muscles, situated in the metathorax of beetles, are essential for flight activity (Fig. I) . The medio-dorsal longitudinal muscles (Fig. I B) bulge the metatergum outwards when contrac­ting and provoke the downward stroke of the wings. The latera l dorso-ventral muscles (Fig. I A) have an antago­nistic effect and fl atten the metatergum, in this way provoking the upward stroke of the wings.

Figs. 1-2 - Functional (Fig. I) and degenerated indirect flight muscles (Fig. 2; muscle fibres replaced by adi­pose tissue) in the metathorax of Pogonus chal­ceus; I A: lateral dorso-ventral muscles, I 8: me­dio-dorsal longitudinal muscles

Diss.ection of carabid beetles reveals that these muscles can be reduced to different degrees or even totally be replaced by adipose tissue (Fig. 2). Intra-specific differ­ences in the state of flight musculature are not necessarily restricted to different individuals, but may, in certain species, occur during the lifetime of even a single beetle. In such a case flight musculature can differentiate, be resorbed or autolysed and then regenerate.

We dissected the meta thorax from about I 0.000 field­collected beetles belonging to 27 different carabid species (nomenclature according to DESENDER et al. , 1995), oc­cutTing in different habitats in Belgium, in order to define the state of their flight muscles. From 13 species, a high number of individuals could be checked: in these cases monthly fractions of beetles with functional flight mus­cles were plotted with their respective 95% confidence limits (WONNACOTT & WONNACOTT, 1977). Jn the re­maining species only the obtained fractions were plotted. The timing of the life cycle was also illustrated for each species. Based on data from the same sampling sites (nearly always from pitfall year cycle series, interpolated per month), frequency distributions were given for adult and teneral (newly emerged) beetles (in some cases also for larvae; in one case based on seasonal occurrence of mean number of ripe eggs in females). Data from seven wing dimorphic or wing polymorphic species are in­cluded: here, proportions of beetles with functional fl ight muscles were calculated based on macropterous indivi­duals only. For two high-density populations of Bembi­dion properans (a wing dimorphic species), the monthly proportion of observed macropterous beetles was also calculated and plotted in order to look for possible sea­sonal changes in these fractions too.

For the current paper we distinguished beetles with well-developed flight muscles from all states of fli ght

Flight muscle development in carabid beetles '' 15

muscle reduction, i.o.w. individuals with a non-functional flight apparatus. When avai lable, replicate year samples from different sites were studied. The ovaries of about 3000 females belonging to the same 27 species (except Amara tibialis and Clivina.fossor) were dissected in order to define their reproductive state as compared to flight muscle functionality. The null hypothesis (functional flight muscles and ripe ovaries occur independently) was tested by means of a G-test of independence (SOKAL & ROHLF, 1981 ).

Results

I. Seasonal variation of flight muscle jimctionality in spring-reproducing ground beetles (adult hibernators)

Fig. 3 (A-Q) summarises data obtained for I 0 carabid species, reproducing mainly during spring. Amara aenea was studied in 6 populations (Fig. 3, G-L), Agonum muelleri (Fig. 3, M-N) and Pterostichus versicolor (Fig. 3, P-Q) in 2 populations. The remaining species were studied in a single population year cycle (Fig. 3, A-F, 0). These l 0 species show their reproductive activ­ity (expressed as numbers caught per month in pitfa ll traps) mainly during spring, resulting in larvae develop­ing during summer and the emergence of the new beetle generation during autumn (teneral beetles, indicated by black columns). Table I summarises the results for fe­males from the same spring-reproducing species, along with G-test results and sample sizes.

The percentage of beetles with functional flight mus­cles shows no clear pattern of seasonal variation in Amara .familiaris (Fig. 3 A) and Asaphidion curtum (Fig. 3 B). Both are characterised by well-developed hind wings (DESENDER, 1989b). At any time during the adult life cycle of Amarajamiliaris about 25 to 50% of the indivi­duals show functiona lity of the fl ight apparatus (cf. DEN BoER et al., 1980). This carabid is known to occur in rather ephemeral habitats, for example on open, recently created, sandy sites (our sampling site was a recent motorway verge on sandy soil). Asaphidion curtum is particularly common in light forest and forest clearings. The continuous possession (at least in a number of in­dividuals) of a functional flight apparatus in these species thus can be interpreted as an adaptation to unpredictable changes in their habitat. There is no statistical deviation from independence between reproductive state and fl ight muscle functionali ty (Table I), i.o. w. we do not observe a significant oogenesis-flight syndrome.

Most other spring breeders, on the other hand, show a significant oogenesis-flight syndrome (Table I), although somewhat less deterministic. Tn each species we observe at least some reproducing females with functional fl ight muscles, but the reproductive period overlaps only partly with the period of functional fligh t muscles. Anisodacty­lus binotatus and Acupalpus jlavicollis individuals all possess flight muscles during early spring (at the onset

16

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Konj ev DESENDER

Amara familiaris road verge on sand A

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Asaphidion curium B woodland

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8 9 18 II 12

D

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F

2 3 4 5 6 7 8 9 19 II 12

Fig. 3 (A-Q) - Phenology of the li fe cycle in spring breedi ng ground beetles (upper fi gure; black co lu mns: tenera l beetles), compared to the seasonal occurrence of monthl y proportions of beetl es with functiona l fl ight muscles (lower fi gure; with 95% c.i . for large samp les,?: months withou t data, arrows indica te zero-va lues based on large sample sizes) . A: Amara .fCnnifiaris (recent motorway verge on sandy soil ), 8: Asaphidion curium (woodland site), C: Acupa fpusjlavico ffis (humid grass land), D: Anisodaclylus binotalus (humid poor gras land), E: Amara tibialis (dune grass land) , F: Agonum dorsafe (cu lti vated fi elds and dry pasture).

Flight muscle development ·in carabid beetles I I 17

79 Amara aenea G H 2SB H H

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Fig. 3 (continued) - G-L: Amara aenea (G: pasture, 1-1 : dry poor grassland , l: relic dune grassland, J: recent motorway verge on sandy soil , K-L: lawns in city of Ghent).

18 Konj ev DESENDER ''

Agonum muelleri 118

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Fig. 3 (co nti nued) - M-N: Agonum muelleri (M: grassland on motorway verge, N : pasture) , 0: Harpalus a/]inis (dry pasture); P-Q: Pterostichus versicolor (dry poo r grass lands).

I I

Flight muscle development in carabid beetles 19

Table I - The oogenesis-fl ight syndrome in ground beetles: flight muscle development and reproductive state of ovaries in females of the investigated ground beetles; n = number of dissected females; R = ovaries with ripe eggs, 0 = ovaries immature or only with corpora lutea (spent, after egg-laying), + = functional fl ight muscles, - = degenerated flight muscles; G-test-statistic: test of independence after comparing [number with flight muscles and unripe or spent ovaries to the total with unripe or spent ovaries] with [number with flight muscles and ripe ovaries to the tota l with ripe ovaries]; number of specimens with or without fl ight muscles within some species not comparable (indicated with an asterisk); data only used to test independence between the occurrence of reproduction and functional flight musculature; species ordered in three groups as in results (spring breeders, autumn breeders and dimorphic/polymorphic species) and in a lphabetic order within each group.

Species n 0+ 0-

Acupalpus f lavicollis 33 19 6 Agonum dOJ··sale * 11 8 6 16 Agonum. muelleri * 78 19 12 Amara aenea 324 24 59 Amara familiaris 48 7 7 Amara tibialis -Anisodactylus binotatus 14 9 Asaphidion curtum 11 7 8 18 Harpalus ajji.nis 33 9 5 Pterostichus versicolor 92 26 28

Amara biji-ons 26 3 Harpalus attenuatus 96 19 I I Harpalus rubripes * 31 10 4 Harpalus rujipes * 30 3 18 Hwpalus rujipalpis * 15 10 I Hcupalus tardus * 45 5 1 Leist us fitlvibarbis * 22 5 7 Leistus nifomarginatus 106 14 4 Nebria brevicollis 349 9 99 Trechus quadristriatus * 95 34 4

Bembidion properans * 219 28 II Bradycellus harpalinus 130 12 9 Calathus rotundicollis 63 2 7 Clivina fossor -Pogonus chalceus 407 4 87 Pterostichus minor 59 I 18 Pterostichus vernalis * 390 21 108

of their reproductive period) (Fig. 3, C-D). Later on, this percentage decreases. These carabids also possess well­developed hind wings (D ESENDER, 1989b). Both species can be found in moderately to very humid sites, which regularly inundate during winter. The remaining species to some degree show two periods a year with a more elevated fraction of beetles with functional flight muscles (Amara tibialis and Harpalus ~[finis show one such per­iod, but the number of individuals studied was low in these species). In nearly all species the periods with a higher incidence of functional fl ight musculature are clearly complementary to the reproductive period (Fig. 3, E-Q). Without exception, these carabids li ve in open habi tat types, ranging from dune grasslands (Amara

R+ R- G-test significance

5 3 0.53 n.s. II 85 3.1 7 n.s. 9 38 14.55 p<0.001 27 214 13.2 1 p<0.001 18 16 0.03 n.s.

3 2 4.20 p<0.05 30 61 0.04 n.s. 8 11 1.60 n.s. 9 29 5.84 p<0.05

1 22 17.23 p<0.001 66 51. 13 p<O.OOI

2 15 12.31 p<0.00 1 9 1.42 n.s.

2 2 2.76 n.s. 39 34.23 p<O.OOI 10 5.39 p<0.05 88 75.44 p<O.OOI

1 240 15.83 p<0.001 21 36 28.72 p<O.OO I

44 136 30.77 p<O.OOI I 108 44.47 p<O.OOI

54 10.39 p<O.O I

16 300 0.07 n.s. 40 2.07 n.s.

15 246 10.68 p<0.005

tibialis), poor grasslands (Pterostichus versicolor) to pas­tures and cultivated fie lds (Agonum dm·sale, Agonum muelleri, Amara aenea, Harpalus ajjinis). Some of these species are known to hibernate in edges of fields, hedges or woodland edges. The obtained patterns therefore can be interpreted in terms of habitat change performed by beetles, though not necessarily in many individuals by means of fl ight dispersal.

Species studied from multiple populations show com­parable patterns. The different populations of Amara aenea, for example, show a clear alternation of the period of reproduction and periods with a higher proportion of individuals with functional fl ight muscles. The maximal proportion of beetles with functiona l flight muscles how-

20 Konjev DESENDER

ever shows a large interpopulation variability. These differences can nevertheless at least pa1tly be interpreted when comparing the sampling site characteristics. High percentages of beetl es wi th functiona l flight muscles are observed on a recently created motorway verge (Fig. 3, J) , whereas very low va lues are found in a popul ation occur­ring in a relic s ite from an old, highly deca lcified, dune grass land area (F ig. 3, I) . These results indicate that a complex of factors plays a role in the expression offlight musc le development (not only habitat characteristics, but also age of the population si nce initial colonisation, mean individual body size influenced by environmental condi­tions during ontogeny, etc.; cf. DESEN DER, 1989a).

In Agonum dorsale and Agonum muelleri (two species available in sufficiently large numbers), the number of individuals with fli ght muscles is reduced to zero during w inter. This suggests that a number of specimens must deve lop and subsequently autolyse or resorb the ir fli ght muscles at least two or three times during their lifetime. They first develop their flight musc les after emergence during autumn in order to fly in search of a convenient hibernation quarter. Then, they autolyse their musc les, followed by regeneration during early spring in order to search for a suitable reproductive site and , once again, resorption at the onset of reproduction.

Compari son of the observed maximal proportion of beetl es with flight musc les and the species-spec ific hind wing development (DESENDER, 1989b), shows that those species w ith sma llest relative w ing size (Agonum d01·sale, Amara tibialis) show very low percentages of beetles w ith fli ght muscles.

2. Seasonal variation ojjlight muscle jill1ctionality in summer-autumn-reproducing ground beetles (larval or larval/adult hibernators)

Data on I 0 spec ies are shown in Fig. 4 (A-P) . For Nebria brevicollis, Hwpalus tare/us and Harpalus attenuatus, data are g iven on respectively 4, 3 and 2 year cycle series. These spec ies can be grouped into different categories: (I) Amara bifi-·ons, a species w ith summer reproduction (short adult period), (2) species be longing to the genus Harpalus, probably with summer reproduction , some species in an annual ( larva l hibernation) to bi enni a l cyc le (larva l and adult hibernation), (3) Leistus jidvibarbis, Leistu.s· rufomarginatus and Nebria brevicollis, a ll known to emerge in spring, followed by an adult aestivation dormancy and reproduction during autumn, ( 4) Trechus quadrislriatus, with its new generat ion appea ring in sum­mer, reproducing in autumn till ea rly next spring. The number of beetles with fu nctiona l flight muscles in non­reprod uct ive as compared to reproducti ve fe males is g iven in Table I, along with the results of G-tests of independence, as we ll as sampl e s izes.

Amara biji-ons prefers dry sandy hab itats with poor vegeta ti on. Our resul ts (F ig. 4 A) show no c lea r differ­ence between the seasonal act ivity peak and the monthly proporti ons of beetl es w ith flight musc les. Nevertheless,

''

there is a significant deviation from independence between reproduction and the occurrence of fu nctional fli ght muscles, but the number of di ssected beetles is low. A similar result is obtained for Hmpalus rujipes (Fig. 4 E), but here the percentages of beetles with flight muscles are higher, while the G-test is not s ignifi ­cant (but low sample size). Hcupalus rujipes, known as a weed seed predator, prefers fi e lds with a more or less developed herb layer (its larvae mainly feeding on small plant seeds), thus possibly requiring regular (re)colonisa­tion.

The remaining Hmpalus species (F ig. 4, 8-1) show a higher proportion of beetles with functional fli ght mus­cles at the beginning of their phenology curve (co inciding w ith the appearance of the new generation), followed by a sharp dec line. Dissection of females revea ls that those w ith ripe eggs in the ovaries never possess functional fli ght muscles, demonstrating a complete (highly signifi­cant) oogenesis-flight syndrome (Table I). All these Harpalus species are more or less bound to sandy so il , usually w ith poor g rassy vegetation . Diffe rences between maximal proportions of beet les with flight muscles are re lati ve ly large between species, but somewhat less reli­able due to re lative ly low sample s izes. H01palus tare/us (F ig. 4, G-l), with low fractions of beetles w ith functional fli ght musc les, shows some variability between popula­tions. The differences between the two popul ations of Harpalus attenuatus can be in part the consequence of a possible detection problem: proportions wi th functional fli ght muscles in the dune grass land (F ig. 4, 8-C) could have been biased to lower va lues because of the very high proportion of newly emerged tenera ls in thi s sample. In such beetles flight muscle development is sometimes di fficult to describe. If such indi viduals develop post­teneral functional flight muscles, flight muscle develop­ment would need at least some days to some weeks after the beetles have emerged and a lready could have been active on the so il surface (cf. SMITH, 1964).

Leistusfulvibarbis, Leistus rufoma rginatus and Nebria brevicollis (Fig. 4, J-0), three species with a high number of di ssected specimens, show strong sim ilariti es in their patterns of seasona l flight musc le development. Again, beet les with functional fli ght musc les are large ly re­stri cted to the non-reproductive peri od, i.e. the emergence period during late spring, before the summer aesti vat ion . These species suggest the occurrence of a di st inct (s ig­nificant) oogenes is-fli ght syndrome (Table I ). Differ­ences in the fractions of beetl es with fli ght muscles can be interpreted in terms of the hab itats prefe rred by the different spec ies. Both Leistus spec ies occur in wood­lands, espec ially in moderately humid to wet s ites. Nebria brevicollis, on the other hand, is a very eLuytopic species from forests , park land and grass lands.

Trechus quadristriatus (Fig. 4 P) , a common speci es on certain types of culti vated fields , is an exa mple of an autumn breeder emerging during summer (Jul y-August) and reproduc ing from autumn till ea rl y nex t spring. Once aga in , immature beetl es from the new generation show a much more e levated proportion (nearly I 00%) of indiv i-

I I

Flight muscle development in carabid beet les 21

38 Harpalus attenuatus 8 " u poor grassland

" B 28 E

R

811 Amara bifrons .----" 68 poor grassland A u

" B 48 E R 38

c A 18 u 6 H T

188

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28 A ? ?? ? ? ? ? ...,.,..,.? ?? ; 18 E

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H H. aftenuatus

u dune grassland c " B 28

188

H Q8 u 88

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,--H. rubripes

t-- poor grassland D E E 118 R R Sfil

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188

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T 188

T 188

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28 A ? ? ? ? G 18 ? ? ? ? E

" 311 T

28 A ? ? ? ? ? ? 6 18 ? ? E

2 3 4 s e 7 8 9 18 11 12 II 2 s 4 5 II 8 g 18 II 12

Fig. 4 (A-P) - Phenology of the li fe cycle in summer-autumn breeding ground beetles (upper fi gure; black columns: teneral beetles), compared to the seasonal occurrence of monthly proportions of beetles with functional flight muscles (lower figure; with 95% c.i. fo r large amples,?: months without data, arrow · indicate zero-values ba eel on large sample sizes). A: Amara biji·ons (poor grassland on sanely soil), 8 -C: Hmpalus a/tenua/1/s (8: poor grass land on motorway verge on sandy soil ; C: dune .grassland), D: !-lcnpalus rubripes (poor grassland), E: Harpalus rt(/ ipes (poor grassland), F: Hmpalus ru{tpalpis (poor grassland on motorway verge on sanely soil ).

22

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29 A 6 Ill E

Konjev DESENDER

r--

G - r-- Harpalus tardus

dry grassland

.--- ..__

r- n

? ?? ? ? ? 2 ' 4 s 8 8 g 19 II 12

H H. tardus dune grassland

?? ? ? ? ? 2 3 4 5 7 e 18 II 12

H. tardus poor grassland

? ? ? ? ? ? ? 2 3 4 s 8 8 9 Ill II 12

N 78 u 89

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Leistus fulvibarbis humid valley forest

I'

3 4 S 8 7 8 9 18 II 12

L. rufomarginatus woodland K

instar I

II

Ill

2 3 4 S 8 7 8 g Ill II 12

Fig. 4 (continued) - 0- K: 0 -I: f-!cupalus tare/us (0 : dry grass land , H: dune grass land , 1: poor grass land), J: Leistusjitlvibarbis (humid vall ey fo rest) , K: Leis/us rufomcug inatus (woodland site; phenology of the three larva l instars added).

Flight muscle development in carabid beetles 23 ' '

ee Nebria brevicollis L 89

68 II 78 N. brevicollis N instar I u 48

" • grassland + scrub II 31 8 u E 519

" 28 R 48 B 18 E c 38 R • A S8 u 28 0 ;

f' 48 H II

38 II T L 188 A 28 118 R

II 88 v A p 78 E

218 E • R 519 c c A 1lil

Ill E 48 u 111 II 38 6 T H 58 A 28 T 6 18 ? ? ? ? ? ? E

It 2 3 4 5 e 7 8 II 18 11 12 u 168

" 11188 148 N. brevicollis II II 138 0 E u 128 pasture R " 1111

B ... c E .. A

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p 71 118 E • • R

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~ ~ ~ R

58 c T 28 E 411 A

6 18 ? ? II 38 T E A 28

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2 3 4 6 e 7 8 II 11 11 12

N. brevicol/is 4.11 Trechus quadristriatus p It • II 3.5 u

li8 deciduous forest u cultivated fields " " 3.8 8 B E 411 E 2.5

R R 2.8 38 c c 1.5 A 28 A u u t.ll 6 18 & H

H 8.5 T 188 T •• 118

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E 411

t ~ ~ E ... II 38 It 31 T

28 T A ? ? ? ? ? ? ? A 28 6 Ill ; .. E E

2 3 4 5 II 7 8 9 18 It 12 2 3 4 5 II 7 II 9 .. II 12

Fig. 4 (continued) - L-P: L-0: Nebria brevicollis (L: beech forest; phenology of the three larval instars added; M: deciduous forest; N: grassland with scrub; 0 : pasture), P: Trechus quadristriatus (cultivated fi e lds).

24 Konjev DESENDER

duals with functional fli ght muscles as compared to beet­les at a later stage of their life cycle. The flight period of this species is indeed restricted to a short period between July and September. Dispersal by flight is probably an adaptation to the temporary characteristics of the repro­duction habitat (e.g. due to crop rotation, ploughing and other management practices). Although several fem ales have ripe ovaries and at the same time functional fli ght muscles, a significant oogenesis-flight syndrome is ob­served (Table I).

3. Seasonal variation of wing morph .fi'equencies and flight muscle jimctionality in wing dimorphic and polymorphic ground beetles

Data on seven wing dimorphic or polymorphic carabid species are summarised in Fig. 5 (A-H) and in Table I (dissected females). Three populations were studied of the wing dimorphic Bembidion properans, two popula­tions of the wing dimorphic Bradycellus hwpalinus, one population of the wing dimorphic Clivina fossor and Calathus rotundicollis, and one population of the wing polymorphic Pogonus chalceus, Pterostichus minor and Pterostichus vernalis. Most of these species are reprodu­cing during spring (adult hibernators), with the exception of Calathus rotundicollis (summer reproduction; larva l hibernator) and Bradycel/us hcupa/inus (reproduction during autumn till next spring).

Bembidion properans (Fig. 5 A-C) does not show much diffe rences between observed wing morph frequen­cies per month (two populations) as opposed to the clear seasonal changes in functional flight muscle frequencies in all populations studied. The results suggest the occur­rence of an oogenesis-flight syndrome during spring (see also Table I) , while only very few beetles with functional fli ght musc les are observed during autumn.

A higher incidence of beetles with flight muscles in spring and in autumn is observed in Pterostichus vernalis and Pterostichus minor, again suggesting the occurrence of a seasonal shift in habitat (migration towards or away from an overwintering habitat, cf. DESEN DER et al. , 198 1 ). In the case of Pterostichus vernalis, however, maximal proportions of beetl es with functional fli ght muscles are quite low. Obviously these numbers are further reduced not only during reproduction but also during hibernation diapause.

Clivinajossor (only limited data and no macropterous females ava il abl e) shows a low maximal proportion of beetles with fli ght musc les, which seems to coincide with the reproducti ve period. Interestingly, thi s spec ies has a largely subterranean way of life and does not seem to perform habitat change in the pasture studied (cf. DESEN­DER, 1983 ; DESENDER & POLLET, 1985).

The saltmarsh inhabiting Pogonus chalceus does not show an oogenesis-flight syndrome, although high num­bers of beetles were investigated (Table I). Despite being low, the yea rl y peak of beetles with functional flight muscles (DESEN DER, 1985), coincides with the moment

I I

of highest number of ripe eggs carried by the females in their ovaries (Fig. 5 G).

Calathus rotundicol/is, a species from light forest and woodland edges, again seems to show an oogenesis-flight syndrome. Only at the onset of the seasonal activity cycle, at most 20% of the beetles possessed functional flight musc les.

Finally, Bradycel/us hcnpalinus shows a pronounced oogenesis-flight syndrome: functional flight muscles and possible dispersa l by fli ght are limited to the post-teneral and pre-reproductive period. Dry grassland, heathland as well as wetland are the preferred habitats of this rather eurytopic species.

Discussion

Because we did not study actual flight behaviour in ground beetles, our results give indirect evidence only fo r seasonal variation in the occurrence of dispersal by flight. Studies based on flight observations only, on the other hand, suffer from other shortcomings, because such observations are highly influenced by meteorological variation. In addition, flight observations, especially if gathered by light trapping, are much more difficult to quantify in terms of local population sizes. Data on flight musc le development (as in our study) give an idea of the maximal proportion of individuals in a population that might be able to fl y.

Proximate factors influencing the onset and duration of flight in carabid beetles predominantly act as strong in­hibitors for flight. VAN HuiZEN (1979) showed that most ground beetles show no flight acti vity below l7°C (see also 1-IONEK & PULPAN, 1983), during precipitation and at wind speed exceeding about 5 m/s. Day-active spec ies appear to require strong insolation prior to flight beha­viour. For many carabids from our regions, these imposed physiological constraints reduce the number of days per year, suitabl e for flight , to a few days to some weeks, with extreme va riation between years and sites . This has been confirmed by long term series of fli ght observations in ground beetles (e.g.: light traps: 1-IONEK & PuLPAN, 1983 ; window traps: VAN 1-I UIZEN, 1979; DEN BoER et al. , 1980) . Publi shed data on the fli ght periods in the species from our study (compiled in Table 2) largely correspond to our observed seasonal pattern of flight muscle func­tionality. Species which are known occasionally to per­form mass fli ghts also show nearly complete flight mus­cle functionality during such periods (e.g. Bradycellus hwpalinus, cf. KERSTENS, 196 1; Trechus quadristriatus, cf. LACMAN, in press).

If the species that we have investigated are grouped into spring breeders (short larval cyc le in summer, adult hibernation) and summer-autumn breeders (long larva l cycle till next spring or summer) , the latter contain more species with functional flight musc les in the post-tenera l and pre-reproductive period than the fo rmer. Such species fl y during a short time span of the year (sometimes a few days only with mass flight , cf. 1-IONEK & PUL PAN, 1983).

188

88 p 78 E ea ~ sa E 48

l : 6 18 E

N u 21111

" B E 168 R

c 188 A

~ sa H T

188 811 88

p 78 E ee ~ sa E 48

~ : A s 18 E

188

88 p 78 E ee ~ sa E 48 N 38

! 211 6 18 E -H 3611 u " 3118 ~2511 R2llll

c rsa A u 188 6 H sa T

188

88 p 78 E 88

~ 58 E 48

~ : A 6 18 E

Bembidion properans city lawn

? ?

? ? 2 s 4 5

?

? ? 2 s 4 s e

A

?

?? 8 IB II 12

B

?

? 8 II 18 II 12

II

Flight muscle development in carabid beetles 25

Hsae u

"­B

~-c2llll A u s 188 H T

188 811 811

p 7B E BB ~ sa E 48

~ : A s 18 E

N 38 u

" B E 2ll R

c A IB u 6 H T

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BB p 78 E ee ~ sa E 40

~ : A 6 Ill E

68

" u 40

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811 811

p 7B E BB ~ 58 E 411

" 38 ! 2ll 6 IB E

B. properans pasture

?? ?

2 3 4 S 8 7 8 II II II 12

Pt. minor marshland forest

? ? . . 2 s 4 5 e 1 8 9 18 11 12

Pt. vernalis pasture

2 S 4 5 8 7 8 II II II 12

c

E

Fig. 5 (A-H) - Wing dimorphic and polymorphic carabid spec ies: ca lculated percentages with functiona l fli ght musc les based on the number of mac ropterous individuals onl y, except for D, E and G; see legend Fig. 3 fo r further ex planation. A-C: Bembidion properans (A-8 : two recent lawns in the city of Ghent; uppermost fi gure represents the seasonal va ri at ion in the percentage (with 95% c. i.) of winged beetl es for thi s wing dimorphi c species, middle figure shows phenology of the li fe cycle (black columns: teneral beetles), compared to the seasonal occurrence of monthly proportions of beetles with funct ional fli ght musc les (lower fi gure; with 95% c. i. fo r large samples,?: months without data , arrows indicate zero-va lu~s based on large sample sizes).; C: pasture), D: Pterostichus minor (marshland forest) , E: Pterostichus vernalis (pasture).

26 Konjev DESENDER

:2lil Clivina fossor F 14 Bradycel/us harpalinus H H

dry hayfield u grassland u 12

" " 8 8 HI E E R R II

18 c c II

A A .. u u .. ; 2 H H

T T IBB IBB liB liB

8B 8B

p 7B p 7B E 8B E 8B R R SB c SB c E 48 E 49 H sa N sa T T

:2lil A :2lil ? ? ? ? ? A

? ? ; 18 ? 6 Ill E E

2 3 .. s e 7 18 II 12 2 3 .. s II 7 8 9 18 II IZ

e Pogonus cha/ceus N

ee N 5 G u u " sattmarsh "

se 8 4 B

48 E E R 3 R

3B 0 c F 2 A :2lil

u E 8 Ill 6 H 6 T s 1118 1119

ge ge

ae se p 7B p 78 E 68 E 118 R se R se c c E ..., E 48 H 3B t N sa T T

:2lil A :2lil A 6 Ill 6 18 E E

2 3 5 8 7 g 18 II 12 z 3 s II 7 8 g 18 II IZ

88 N 78 Calathus rotundicol/is

H u

" 88 woodland 8 E 58 R

48

c sa A u :2lil 6 H 18 T

118 118 se

p 78 E liB R se c E <48

t N 3B T :2lil A ? ?? ? 6 18 E

2 3 s II 8 g 18 It 12

Fig. 5 (continued) - F: Clivinafossor (grass land), G: Pogonus chalceus (sa ltm arsh; num ber of ripe eggs per fe male plotted as ind ica tion of reproduct ive peri od), 1-1 : Calathus rolundico!lis (woodland site) , 1-J : Bradyce!lus harpa!inus (I: dry hayfie ld , J: dry poor grassland).

Flight muscle development in carabid beetles ' ' 27

Table 2. - Compilation of literature observations of flight and main annual flight period in the ground beetle species, studied in thi s paper; species ordered in three groups as in results (spring breeders, autumn breeders and dimorphic/polymorphic species) and in a lphabetic order within each group: number of records: * = low numbers, X= high numbers; number of symbols refers to the number of references with the species; data from: B ASEDOW & DICKLER, 198 1; BRI EL, 1962; BRIGGS, 1965; D EN BOER, 1971 ; D ES ENDER, l986b and unpublished data; GREENSLADE & SOUTHWOOD, 1962; H AECK,

1971 ; H ONEK & P UL P AN, 1983 ; KADAR & S ZENTKI RALY I, 1983 ; K ERSTENS, 1961 ; L ACMAN, in press; Li 1DROTH , 1945 ; M ATALI N, 1994, 1997; M EIJ ER, 1974; Y ANHERCKE et al. , 1980; V AN H UIZEN , 1979, 1980; ZHANG et al. , 1997; Z ULKA ,

1994.

Species number of records

A cupalpus jlavicollis X* Agonum dOl-sale *** Agonum muelleri *** Amara aenea XXXX** Amara familiar is XXX*** Amara tibialis * Anisodacty lus binotatus XXX* Asaphidion curtum **** Harpa!us afjinis X* Pterostichus versicolor **

Amara bifi·ons XX***** Harpalus attenuatus · ? Harpalus rubripes * Harpalus rufipes XXXXXX*** Harpalus rufipalpis X Hmpalus tardus ? Leistus jitlvibarbis ? Leistus nifomarginatus ? Nebria brevicollis * Trechus quadristriatus XXXXXX** *

Bembidion properctns ** Bradycellus harpalinus XXXXXX* * * * ':' Calathus rotundico/lis * Clivina jossor *** Pogonus chalceus ? Pterostichus minor X* Pterostichus vernalis ****

Many spring breeders, on the other hand, with a winter­diapause between emergence and reproduction, show a higher incidence of functional flight muscles before as well as after reproduction (in that case mainiy post-ten­era!). Seasonal variability in fli ght muscle development in these species co incides with two known fli ght periods per year (references, cf. Table 2) related to habitat change to and from overwintering sites and sites for reproduction. After emergence and fli ght activity, adults of many sum­mer-autumn breeders directly start reproduction. From then onwards the reproducing generation graduall y dies off. The very short flight periods in these species can also be a partl y consequence of other life history aspects. Many of these ground beetles indeed are known to be exc lusively act ive during the ni ght (DES ENDER et al. 1984;

flight period(s)

? Apri l-May, August April , September April-May, (September) April-July April-May April-May, (September) April-June May-June May, end July

July-August ? ? July ? ? ? ? May July-September

April-May July-August early August May-June ? ? May, September

THI ELE, 1977), as opposed to a lot of day-active spring species. Summer-autumn breeders like Bradycellus har­palinus, Harpalus rl!fipes and Trechus quadristriatus are caught especially flying at night (cf. HoNEK & PULPAN, 1983 ; MATA LI N, 1997; ZHANG et a!. , 1997). The high temperatures needed for fli ght further reduce the number of days with suitable conditions for fli ght in night-active species. Spring carabid beetles, on the contrary, are prob­ably less constrained for flight because of their daytime activity and indeed regularly show two flight periods a year, related to habitat change. In some cases (e.g. Bem­bidion properans) the spring peak appears to be more important than the autumn peak (following from data on fli ght muscle functionali ty as well as from literature data on flight periods). This cou ld reflect a synchronous de-

28 Konjev DESENDER

velopment of flight muscles after winter diapause in order to be able to recolonise the reproduction habitat as quickly as possible. During autumn the appearance of the new generation is much more spread, while short­ening of day length inhibits vitellogenesis and thus repro­duction (TH IELE, 1977). It is therefore possible that sui­table hibernation quarters are then more easily reached by less energy-demanding activities such as walking instead of flying (more " time" available?).

A majori ty of the carabid beetles investigated seems to exhibit a significant "oogenesis-flight" syndrome: repro­duction and reduced flight musculature are thus not in­dependent events in their life cycle, i.o.w. there is a trade­off between reproduction and functional flight muscula­ture. Reproduction as well as flight being both very energy-consuming activities, it seems plausible that re­sorption of flight muscles liberates energy (cf. ZERA &

DEN o, 1997) and/or creates space to accommodate en­larging reproductive organs ( cf. SOLBRECK, 1986; T ADA et al. , 1991 ). Flight activity during reproduction probably is hampered or even made impossible in some species because of an increased individual body weight (cf. MA­TA LI N, 1997) and consequently higher wing loading. These hypotheses should be tested experimentally. Spe­cies where some individuals will and others will never be able to develop flight muscles (genetic flight muscle dimorphism) present interesting cases for such experi­ments.

In many ground beetle species, especially spring bree­ders, we observe a proportion of mature females with functional flight muscles, indicating a less deterministic version of the oogenesis-flight syndrome. This could have important side effects for the colonisation chances of such species. When migration is re lated mainly to seasonal changes between habitats for reproduction and for hibernation, straggling individuals leaving hiberna­tion quarters will now and then end up in a site, never colonised before. Sporadic flight activity of ripe or at least inseminated females would strongly increase the chances for founding new populations. VAN HUIZEN ( 1990) came to a sim ilar conclusion after dissecting 932 beetles belonging to 62 carabid species. Unfortunately, this author did not list the species or sample sizes, but gave pooled results, difficult to evaluate.

JoH NSON ( 1969) came to the conclusion that, in insects in general, processes of gonad maturation and degenera­tion/regeneration of flight muscles are coupled during morphogenesis. These processes would have been adap­tively brought into phase in di fferent ways accord ing to the species. De- and regeneration of fl ight muscles are part of a lab ile system of morphogenesis, but are still insufficiently understood (RANKI 1 et al. , 1986). Flight muscle development, because of its hidden aspect, has been studied insufficiently and the difference betvveen ontogenetic (direct) and phylogenetic (evolved) flight muscle dimorphi ·m is vague (JOHNSON, 1969). Variabi­lity in the synchronisation between egg production and a functional flight apparatus is more pronounced when both developmental pathways are reversible. JOHNSON ( 1969)

therefore concluded that the "oogenesis-flight syn­drome" in many cases is labile and controlled mainly by the environment.

If dispersal (migration) contributes to individual fitness (survival and direct or indirect reproductive output), we expect that species, emerging during summer, will show flight activity immediately before their reproduction. At that moment, climatological conditions are most suitable and females are not yet carrying the extra weight of eggs (males not yet the extra weight of very much enlarged gen ital accessory glands). In spring-breeding species this is not the case. Climatological conditions during early spring and autumn are much more regularly below thres­hold values for fl ight. This might give an explanation for the higher incidence in such species of females with ripe eggs simul taneously with functiona l flight muscles (i.e. a less deterministic oogenesis-flight syndrome).

In some of the species investigated, flight muscles are resorbed after suitable hibernation quarters have been reached, and are regenerated next early spring. This in­dicates that the mere maintenance of a functional flight apparatus (even without flight activity) involves high energy investments. Consequently, migration and dia­pause do not run strictly in parallel in such cases.

Functional fl ight muscles are expected to develop only when there is some selective advantage involved. This enables for example a rapid exchange between habitats for spring species while yielding much higher chances of survival in protected winter quarters. Extreme examples are species from habitats inundated during winter. An even stronger selection for the continuous presence of functional flight muscles is expected to occur in species from very unpredictable habi tats (i.e. a habitat that cannot continuously be inhabited during the reproductive peri­od). Such species need to be able to escape by flight at any time, for example from water floods after heavy ra in, or from tides in saltmarshes. In such situations, a strong positive selection is expected for a permanent functiona l flight apparatus. At the end of this line of reasoning are examples of species that need flight for their normal dai ly activities (e.g. prey caught during flight or escape from predators in Cicindela or tiger beetles, .. . ).

Maximal proportions of beetles with functional flight muscles in many species only reach low values, which can strongly differ between populations. This clearly indicates the complex regulation of flight muscle ex­pression. Underlying mechanisms can be both autolysis/ rebuilding processes and their regulation but also pure genetic flight muscle dimorphism. Experimental research is urgently needed for a better understanding of these processes. Regulation of autolysis and regeneration of flight muscles in the li fetime of individuals has hard ly been studied in ground beetles. An important problem in this respect is that the observed phenotypic variation not necessarily reflects the genetic variabi li ty present in a population. Experimenta l studies on the regulation of fli ght muscle functionality of carabids were performed in Nebria brevicollis (N ELEMANS, 1983 , 1987) and in Pterostichus ob/ongopunclatus (VAN SCHAICK ZI LLESEN

& BRUNSTING, 1984). Unfortunately, these two species rarely fly and therefore low fractions of individuals with flight muscles are observed in field situations. Favourable conditions during the larval ontogeny of Nebria brevicol­lis (such as sufficient food supply, short day-length) appear to enhance the expression of functional flight muscles in the resulting young adults. Results for Pterostichus oblongopunctatus lead more or less to an opposite conclusion, but the data seem less convincing. Some small experiments of BOMMARCO ( 1998) suggest that wing muscles of Pterostichus cupreus increase in size with increasing food availability. In a large scale biometric study on numerous ground beetle species (DESENDER, I 989b), we have regularly noted that in­dividuals possessing flight muscles have a larger mean body size as compared to beetles with degenerated flight muscles. This seems to be in agreement with the results of NELEMANS (1983, 1987) on Nebria brevicollis. In her experiments, beetles raised under more favourable conditions (higher food supply, sh01t day-length) not only developed flight muscles, but were also larger in size. The somewhat unexpected conclusion drawn from this observation is that under more favourable environ­mental conditions more beetles would be capable for flight. It contradicts the general idea that developing flight muscles and performing flight activity would lar­gely be an adaptive escape reaction in a deteriorating habitat ( cf. JOHNSON, 1969 for insects in general; VAN ZCHAICK ZILLESEN & BRUNSTING, 1984). Body size of beetles, on the other hand, is, at least partly, influenced by environmental conditions during ontogeny (cf. DESEN­DER, 1989a), which questions to some degree the term "adaptive".

Clearly, this study area offers a lot of new and original subjects for investigation. First, however, more empirical data are required, especially on other species and in other regions. Such field-collected data, along with those pre­sented in this paper, are a first step towards straightfor­ward experimental and physiological studies on flight muscle fu nctionality and its underlying processes. Over­al l, our results suggest that flight muscle development, like other life history traits of ground beetles (such as habitat preference, life cycle timing, body size, abun­dance, hind wing development, ... ), is part of a suite of coadapted traits (DESENDER, 1986a).

In conclusion, a majority of the ground beetle species, investigated in this study, shows seasonal variation in the number of specimens with functional flight musculature. In many cases, this variabili ty can be related to other life history traits. The complexity of the phenomenon is evident, and causes and effects in many cases are hard to distinguish, suggesting that flight muscle development is part of a suite of coadapted traits . The large interspe­cific variability in flight muscle functionality and the more or less pronounced occurrence of an oogenesis­fli ght syndrome is striking. This adds a further dimension to the already very large interspecific diversity in hind wing development of ground beetles (cf DEN BOER et al., 1980; DESENDER, 1989b). Eventually, it increases the

'I

Flight muscle development in carabid beetles 29

va lue of ground beetles as model organisms in studies on dispersal and gene flow, population genetics, ecology and evolution.

Acknowledgements

This paper would not have been possible without the continuous help, during many years, from many students and colleagues: in particular Mark Alderweireldt, Leon Baert, Jean-Pierre Mae! fait, Marc Pollet and Marc Van Kerckvoorde aided in the collection of large series of year cycle pitfall trap samples in different habitats of our country. Marc Van Kerckvoorde in addition helped by dissecting a number of series of ground beetles for their flight muscle development. P. Grootaert (RBINSc) and A. Huysseune (RUG) kindly revised previous drafts of this paper and H. Turin added useful review comments.

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Konjev DESENDER Department Entomology

Royal Belgian Institute ofNatural Sciences Vautierstr. 29 B-1000 Brussel

emai l: kdesender@kbinirsnb.be