Eye morphology re¯ects habitat demands in three closelyrelated ground beetle species (Coleoptera: Carabidae)

Thomas Bauer1, Konjev Desender2, Thomas Morwinsky1 and Oliver Betz1

1 Zoologisches Institut der UniversitaÈt Kiel, D-24098 Kiel, Germany2 K.B.I.N., Entomology Department, Vautierstraat, 29, B-1040 Brussels, Belgium

(Accepted 7 January 1998)

Abstract

Asaphidion ¯avipes, A. curtum, and A. stierlini, which are similar in shape and size, were compared for

morphological measurements of the head and eyes. The species not only differ in body size but also in the

relative length of their antenna, the surface area of their compound eyes, the number and density of their

ommatidia, and the structure of their visual space. These differences can be interpreted functionally and

correlate well with features of the various habitats in which the species are found.

Key words: Carabidae, compound eyes, Asaphidion

INTRODUCTION

Morphological characteristics of the compound eyere¯ect features of the life style of insect species (Wehner,1981), and are thus well suited for predicting thesefeatures (Bauer & Kredler, 1993). Diurnal visualhunters have large laterally protruding eyes with a largebinocular overlap of the visual ®elds. In nocturnalinsects, which detect prey chemically and by mechanicalcues, the eyes are much smaller with fewer ommatidia.Among closely related species, e.g. those of the samegenus, differences in eye morphology may be small; theyexist, however, if there are differences in the habitatchoice (Bauer, 1985; Morwinsky & Bauer, 1997).

In this paper, we investigate three species of theAsaphidion ¯avipes group (Carabidae): A. ¯avipes (L.1761), A. curtum (Heyden, 1870), and A. stierlini(Heyden, 1880). These species show great similarities insize and body shape and are thus dif®cult to discrimi-nate. In the past, specimens of A. curtum and A. stierliniwere often classi®ed under A. ¯avipes. A revision ofvarious collections has only recently revealed that A.curtum in particular has often mistakenly been identi®edas A. ¯avipes (Focarile, 1964; Lohse, 1983; Jorum &Mahler, 1985; Hartmann, 1985; Speight, Martinez &Luff, 1986; Desender, 1990; Ljungberg, 1991; Muilwijk& Heijerman, 1991; Heijerman & Muilwijk, 1992) andseems to be much more common in middle Europe thanpreviously assumed.

Intensive pitfall trapping in the major terrestrialhabitats occurring in Belgium (mainly performed duringthe two most recent decades; total data set of more than300 000 carabid beetles from about 500 samplingstations; all beetles identi®ed or checked by the second

author) revealed that these Asaphidion species show apronounced and species-speci®c habitat preference (seeTable 1).

Asaphidion ¯avipes, the most common of the threespecies, is active on open areas in gardens and ®elds andits wings are more reduced than those of the otherspecies. A. curtum is mostly restricted to open woodlandsites (e.g. poplar plantations) and is active there in areaswith little vegetation or litter. A. stierlini, the rarestspecies, is found near the coast in open dune habitats,where it ¯ies during the day. Inland, it prefers open siteswith a hot microclimate (e.g. railway embankments).Thus, we suggest that A. stierlini is adapted to the mostopen habitats with the highest light intensity, whereasA. curtum is a species of more shady places, and A.¯avipes is intermediate between these two.

In this paper, we test the hypothesis that thesesupposed differences in the habitat demands are re-¯ected by differences in the morphology, especially oftheir compound eyes.

MATERIALS AND METHODS

The beetles were collected in Belgium: A. ¯avipes on®elds and pastures near Gent, A. curtum in the forest ofZonien near Brussels, and A. stierlini on coastal dunesnear the French border. They were ®xed in formalin.For all measurements, 12 specimens of each species (6females and 6 males) were used. The length measure-ments were made with a binocular microscope (M8,Wild, Switzerland) equipped with a drawing apparatus.

To determine the number of ommatidia and the sizeof the cornea, the beetles were brie¯y softened in hot

J. Zool., Lond. (1998) 245, 467±472 # 1998 The Zoological Society of London Printed in the United Kingdom

potash lye. The cornea of each eye was removed, spreadon a microscope slide and photographed. The numberof ommatidia was counted from the photographs andthe area of each cornea determined planimetrically andconverted to its actual size.

To determine the interommatidial angles and to re-construct the binocular visual ®eld, living beetles weremounted on a goniometer by means of Plasticine. Thehead was centred under a binocular microscopeequipped with coaxial illumination (Wild M 650). Todetermine the horizontal plane, the eyes were viewed ina symmetrical position parallel to the labrum andclypeus (= reference plane: 08). The head was thenturned about the transverse axis and the size-change ofthe principal pseudopupil observed. Its maximum sizeindicated the position of the frontally directed acutezone. In the Asaphidion species this value was about 43±458 above the reference plane. The optical axis of theommatidia was determined by using the deep pseudo-pupil, which could be seen as a small black spot withinthe principal pseudopupil in bright coaxial light (cf.Stavenga, 1979). Starting with the eyes in a symmetricalposition, the head was turned in the horizontal plane insteps of 38 to the right and to the left. After each turn,the ommatidia between the inner margin of the eyes andthe position of the deep pseudopupil were counted,focusing ®rst on the level of the pseudopupil and then

on the corneal surface. This procedure was repeated 3times for each beetle and ®nally the mean values from 3specimens of each species were pooled. The optical axesof the ommatidia were drawn on the contour of ahistological section of the head through the same plane.

Statistical analysis was undertaken by means of SPSSfor windows (SPSS Inc., Chicago). For comparing thevarious means of the species a single classi®cationanalysis of variance (ANOVA) followed by a Student±Newman±Keuls test was carried out.

RESULTS

Table 2 summarizes the measurements of 12 individualsof each species. A. ¯avipes is the largest and A. curtumthe smallest; the body length difference between A.¯avipes and the two others is signi®cant. For a com-parison of body proportions all other parameters arerelated to body length (Fig. 1): A. stierlini has signi®-cantly shorter antennae than the two other species. Thehead of A. curtum is broader than that of the other twospecies. All three species differ signi®cantly in theirrelative number of ommatidia, the largest number occur-ring in A. stierlini and the lowest in A. ¯avipes. The eyesurface is largest in A. curtum and similar in the twoother species. The number of ommatidia per mm2

surface area differs signi®cantly in all three species and islargest in A. stierlini and lowest in A. curtum. A. curtumhas the relatively longest metatrochanter and A. stierlinithe shortest. Measurements of the optical axes revealedthat in all three species the acute zones with the smallestinterommatidial angles are directed frontally. Thesmallest interommatidial angles are approx. 2.68 in A.¯avipes and A. stierlini and 2.88 in A. curtum. Thereconstruction of the binocular visual space (Fig. 2)revealed structural differences that are discussed below.

Comparing the means of measurements of malesand females we found signi®cant differences in A. stier-lini. The males of this species have more ommatidia(H number of ommatidia/mm body length: males, 6.862;females, 6.347; P<0.005); the density of ommatidia islarger (males, 600.75/mm2; females, 517.62; P<0.05);their antennae are longer (males, 0.445/mm body length;females, 0.432; P<0.005), and their metatrochanters areshorter (males, 0,111/mm body length; females, 0.115;P<0.05). In the other two species some of these differ-

T. Bauer ET AL.468

Table 1. Occurrence of the Asaphidion species in differenthabitats (number of individuals caught in pitfall traps indifferent sampled habitats)

Species

Sampled habitat type A. curtum A. ¯avipes A. stierlini

Deciduous forest 787Dune woodland 10 4Meadow forests 6 20Marshland 6Humid grassland 1 8Riparian habitats 9Dry grassland 2 85 1Cultivated ®elds, ruderal

habitats 657 4Heathland 4Railway embankments 16 16Coastal dunes 2 108Saltmarshes 1

Table 2. Parameters of the beetles. Cases that are marked by different superscript letters are different at the 5% level (one-wayStudent±Newman±Keuls test). Means of 12 specimens per species are given

A. curtum A. stierlini A. ¯avipes

X sd X sd X sd

Body length (mm) 4.05b 0.25 4.10b 0.29 4.32a 0.15Length of antenna (mm) 1.89b 0.09 1.80c 0.11 2.03a 0.06Head width (mm) 1.18ab 0.06 1.15b 0.06 1.22a 0.03Number of ommatidia 615.04b 52.07 733.71a 90.54 631.71b 68.72Surface area of eyes (mm2) 1.49a 0.19 1.33a 0.25 1.39a 0.24Length of metatrochanter (mm) 0.48ab 0.04 0.47b 0.04 0.50a 0.01

ences between the sexes were similar, but not signi®cant,probably due to the small samples (six males and sixfemales per species).

DISCUSSION

The three species of the A. ¯avipes group have large

protruding eyes that are typical for visual huntersamong ground beetles. Laterally protruding compoundeyes favour peripheral vision and may be associatedwith an array of ommatidia improving resolution in thefrontal visual ®eld (e.g. Burkhardt & de la Motte, 1983).However, they may also hinder the movements of abeetle between plants and soil structures. Thus, pro-truding eyes are characteristic of surface-dwelling

469Eye morphology and habitat demands in Asaphidion

1.50

1.20

0.90

0.60

0.30

0.00

(a)

0.60 0.61 0.62 0.63 0.64 0.65Log body length (mm)

Log

head

wid

th (

mm

) *

10

A.c.A.s.

A.f.

0.40

0.35

0.30

0.25

0.20

(b)

0.60 0.61 0.62 0.63 0.64 0.65Log body length (mm)

Log

leng

th o

f ant

enna

(m

m)

A.c.

A.s.

A.f.

1.60

1.50

1.40

1.30

1.20

(c)

0.60 0.61 0.62 0.63 0.64 0.65Log body length (mm)

A.c.

A.s.

A.f.

1.50

0.90

0.30

0.60

0.00

(d)

0.60 0.61 0.62 0.63 0.64 0.65Log body length (mm)

A.c.

A.s.A.f.

Log

num

ber

of o

mm

atid

ia 1.20

Log

ey

e su

rfac

e (m

m)

* 10

0.30

0.26

0.22

0.18

0.14

(e)

0.60 0.61 0.62 0.63 0.64 0.65Log body length (mm)

A.c. A.s.

A.f.

Log

(leng

th o

f met

atro

chan

ter

+1)

(m

m)

0.10

Fig. 1. Measurements of (a) head width, (b) antenna length, (c) number of ommatidia, (d) eye surface and (e) metatrochanter

length of the beetles with respect to body length (means of 12 specimens per species). Bars: standard deviation. A.c. = Asaphidion

curtum, A.s. = A. stierlini, A.f. = A. ¯avipes.

species. All species of the genus Asaphidion belong tothis type. A. pallipes (Duftschmid, 1812) and A. cara-boides (Schrank, 1781), which can be easilydiscriminated from species of the A. ¯avipes group bysize and body shape, also possess this type of eye.Correspondingly, they have the same hunting behaviour(Bauer, 1985). They turn towards moving prey objects,approach in short jerks and attack with a fast lungefrom close distance (for details of this behaviour seeBauer & Kredler, 1993).

Normally, eye features like surface area and numberof ommatidia are enlarged isometrically with increasingbody size in Carabidae, while the interommatidialangles of the acute zones decrease (Bauer & Kredler,1993). This may be partly because the relevant bio-logical dimensions grow with increasing body size.Precise detection of movements of small objects, prey orenemies, needs a ®ner `grain' of the optical raster if theseobjects move in larger distances. However, A. caraboidesand A. pallipes, which are larger than A. ¯avipes, have amuch coarser optical raster. Correspondingly they areless successful in hunting fast prey animals on the soilsurface, which was shown experimentally usingCollembola as prey (cf. Bauer, 1985). It was thusconcluded that the smallest species of the three is moreadapted to visual hunting on the soil surface than theother two.

The morphological differences between the speciesconcerned here are much smaller. However, despite

their very similar size and body shape, differences doexist.

Length of antenna

The relative length of antennae is the same in A. ¯avipesand A. curtum, but A. stierlini has shorter antennae anddiffers signi®cantly from the other species in thisrespect (cf. Fig. 1). The antennae are generally shorterin visual than in tactile hunters (Bauer & Kredler,1993), probably because palpating for prey is lessimportant for them. This may also be true for A.stierlini in its open habitat, when compared with thetwo other species.

Eye measurements

The relative head width and the relative surface area ofthe eyes is largest in A. curtum and this species differssigni®cantly from the other two. The relative number ofommatidia is largest in A. stierlini and smallest in A.¯avipes, all three species differing signi®cantly for thisparameter. The density of ommatidia (number/mm2

surface area) is again largest in A. stierlini and lowest inA. curtum and all three species differ signi®cantly. Thesemeasures are interdependent and thus have to be con-sidered together.

T. Bauer ET AL.470

A. curtum A. flavipes A. stierlini

1 mm

Fig. 2. Structure of the horizontal visual ®elds of the three species. Black: diamond shapes are overlap regions on the midline,

the extent of which can be used as a measure of acuity in depth and width; grey: ®eld of the ®rst visual cones with incomplete

binocular overlap.

A. curtum A. ¯avipes A. stierlini

Visual hunters generally have c. 50% more ommatidia(mean >200 ommatidia/mm body length) than tactilehunters (mean <100/mm body length), although largedifferences have been observed within these groups (cf.Bauer & Kredler, 1993). For visual hunters, high opticalresolution is crucial for detecting and gauging theposition of moving objects, either enemies or prey. Foreyes of a similar size and shape we can predict that themore ommatidia per surface area unit, the smaller theinterommatidial angles and the better the optical reso-lution. This is especially true for the frontal eye parts,where small moving objects are imaged by a turntowards them after they have been detected. However,species that hunt in dim light need larger lenses toachieve suf®cient contrast sensitivity than those thathunt in bright sunlight (for details see Wehner, 1981).Thus, in dim-light species, the number of ommatidiashould be lower at a given eye size or the surface area ofthe eyes should be larger. This could explain why A.curtum has the largest eye surface and the lowestnumber of ommatidia per surface area unit and A.stierlini has the most ommatidia with the highest densityper surface area unit. A. curtum moves on the forest¯oor, i.e. in dim light, and is probably well hidden bysoil structures. A. stierlini is active in open habitatsunder better light conditions. In this environment, thespecies is probably also more threatened by predators,which may detect the beetles from some distance andthus, in turn have also to be recognized from a greaterdistance. Therefore, many ommatidia per surface areaunit, i.e. a better optical resolution, is not only possiblebecause of favourable light conditions but also neces-sary because survival in bright light requires thedetection of moving objects over large distances.

Structure of the visual space

In compound eyes the ommatidium constitutes the basicsampling station and spatial resolution is exclusivelydetermined by the divergence angles between the opticalaxes of adjacent ommatidia (Wehner, 1981). Thus theextent of the diamond-shaped overlap regions in thebinocular visual ®eld (cf. Fig. 2) can be used as ameasure of acuity in depth and width (Burkhardt,Darnhofer-Demar & Fischer, 1973). Generally, thisacuity, especially acuity in depth, decreases dramaticallywith increasing distance from the head.

The structure of the binocular ®eld of vision seems tobe rather similar in the three species (Fig. 2). Their acutezones consist of ommatidia with angles of approx. 2.6±2.88 and are directed frontally. However, the differencesin head size and number of ommatidia per surface areaunit lead to differences in the structure of the visualspace. The number of all binocular overlap regions inthe horizontal plane is 400 in A. ¯avipes and A. stierliniand 324 in A. curtum, the number of overlap regions onthe midline (black in Fig. 2) is 8 in A. curtum, 9 in A.¯avipes and 10 in A. stierlini. According to Burkhardt etal. (1973) binocular distance estimation on the midline

is possible to the point of incomplete overlap of thecones, representing the visual ®elds of correspondingommatidia, in the two eyes (E ? in Burkhardt et al.,1973). The distance of this point from the front edge ofthe eyes is 8.4 mm in A. curtum, 9.18 mm in A. ¯avipesand 15.1 mm in A. stierlini indicating that binoculardistance estimation in A. stierlini is possible at greaterdistances than in the other two.

Length of the metatrochanter

The metatrochanter contains a special muscle thatrotates the femur and thus lifts the body when it ispushed forward (Evans, 1977). Species that propel them-selves through the litter when searching for preygenerally have much larger metatrochanters (relativelength >0.11) than surface runners (relative length<0.09) and are called `wedge pushers' (Forsythe, 1981).In the three Asaphidion species, these values are above0.11, indicating that all three belong to the `wedgepusher' type. This is inconsistent with their behaviourand their large eyes. Species of Notiophilus or Elaphrus,other large-eyed visual hunters, have typical surface-runner legs with short trochanters. In comparison withthese old carabid genera, Asaphidion is probably a youngbranch of the genus Bembidion (Maddison, 1993). In thisspecies-rich genus, intensive adaptive radiation has gen-erated not only many tactile hunters but also some visualhunting species that are morphologically less conspic-uous than Asaphidion and that have still the largetrochanters of their `wedge pushing' ancestors (Mor-winsky & Bauer, 1997). We consider that this is also truefor Asaphidion. There are, however small differencesbetween the three. The metatrochanter is smallest in theopen habitat species A. stierlini, which differs signi®-cantly from the other two. We regard this as anindication that, among the three species, A. stierlini issomewhat more adapted to running on the soil surface.

Differences between the sexes

Intersexual differences in A. stierlini may be explained ina similar way to the differences between the threespecies. As in most insects, in Carabidae the malesrather than the females actively search for sexual part-ners. In visual hunting species the males use their eyes tosearch for females and are thus forced to move about onthe soil in the light more than females do. The selectivepressure on the enhancement of optical resolutionleading to an increase in the number and density ofommatidia may thus be stronger for males than forfemales, particularly in an open-land species like A.stierlini. Larger samples of other species have to beexamined to determine whether these intersexual differ-ences occur in general in visual hunting species.

These results show that morphological measurements,especially of the compound eye, are sensitive indicatorsof niche differences even among closely related species.

471Eye morphology and habitat demands in Asaphidion

The unexpected intersexual differences that were foundin A. stierlini suggest that eye measurements might alsobe suited for estimating trends of niche differentiationwithin a species.

REFERENCES

Bauer, T. (1985). Different adaptation to visual hunting in threeground beetle species of the same genus. J. Insect Physiol. 3:593±601.

Bauer, T. & Kredler, M. (1993). Morphology of the compoundeyes as an indicator of life-style in carabid beetles. Can. J. Zool.71: 799±810.

Burkhardt, D., Darnhofer-Demar, B. & Fischer, K. 1973. Zumbinokularen Entfernungssehen der Insekten. I. Die Struktur desSehraumes von Synsekten. J. comp. Physiol. 87: 165±188.

Burkhardt, D. & de la Motte, I. (1983). Selective pressures,variability, and sexual dimorphism in stalk-eyed ¯ies (Diop-sidae). Naturwissenschaften 72: 204±206.

Desender, K. (1990). Preliminary note on Asaphidion curtum(Heyden, 1870) and A. stierlini (Heyden, 1880) two Carabidbeetles new for the Belgian fauna (Coleoptera, Carabidae).Bull. Annls Soc. r. belge Ent. 126: 179±180.

Evans, M.E.G. (1977). Locomotion of the Coleoptera Adephaga,especially Carabidae. J. Zool. (Lond.) 181: 189±116.

Focarile, A. (1964). Gli Asaphidion del gruppo ¯avipes (L.) conparticolare riguardo alla fauna italiana. Mem. Soc. Entomol.Italiana 43: 97±120.

Forsythe, T.G. (1981). Running and pushing in relationship tohind leg structure in some Carabidae (Coleoptera). Coleopt.Bull. 35: 353±378.

Hartmann, M. (1985). Zur Verbreitung der Arten aus der Ver-wandtschaft des Asaphidion ¯avipes L. (Col., Carabidae).Entomol. Nachr. Ber. 29: 121±123.

Heijerman, T. & Muilwijk, J. (1992). Asaphidion stierlini, eenderde soort uit de A. ¯avipes groep in Nederland (Coleoptera:Carabidae). Ent. Ber. Amst. 52: 14±18.

Jorum, P. & Mahler, V. (1985). Asaphidion curtum (Heyden,1870)±en ny dansk lobebille (Coleoptera, Carabidae). Ent.Meddr. 53: 46±48.

Ljungberg, H. (1991). Asaphidion curtum (Heyden) en foÈr Sverigeny jordloÈpare (Coleoptera, Carabidae). Entomol. Tidskr. 112:161±162.

Lohse, G. (1983). Die Asaphidion-Arten aus der Verwandtschaftdes A. ¯avipes L. Ent. Bl. Biol. Syst. KaÈfer 79: 33±36.

Maddison, D.R. (1993). Systematics of the holarctic beetle sub-genus Bracteon and the related Bembidion (Coleoptera: Cara-bidae). Bull. Mus. Comp. Zool. 153: 143±299.

Morwinsky, T. & Bauer, T. (1997). Prediction of life style by eyemorphology in Bembidion species (Coleoptera, Carabidae).Pedobiologia 41: 472±480.

Muilwijk J. & Heijerman, T. (1991). Asaphidion curtum, eentweede soort uit de A. ¯avipes groep in Nederland (Coleoptera:Carabidae). Ent. Ber. Amst. 51: 145±152.

Speight, M., Martinez, M. & Luff, M. (1986). The Asaphidion(Col.: Carabidae) species occurring in Great Britain andIreland. Proc. Trans. Br. Ent. Nat. Hist. Soc. 19: 17±21.

Stavenga, D.G. (1979). Pseudopupils of compound eyes. In Hand-book of sensory physiology, Part 6A Comparative physiologyand evolution of vision in invertebrates: 357±440. Autrum, H(Ed.). Berlin, Heidelberg, New York: Springer.

Wehner, R. (1981). Spatial vision in arthropods. In Handbook ofsensory physiology, 7, Part 6C. Comparative physiology andevolution of vision in invertebrates: 297±616. Autrum, H. (Ed.).Berlin, Heidelberg, NewYork: Springer.

T. Bauer ET AL.472