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Baltic J. Coleopterol. 7(1) 2007ISSN 1407 - 8619

INTRODUCTION

Urban Grasslands

Urban environments typically contain a widevariety of semi-natural grassland habitats. Thesevary from intensely managed lawns and amenitygrasslands, through periodically cut habitats,

Morphological responses to disturbance in wing-polymorphiccarabid species (Coleoptera: Carabidae) of managed urbangrasslands

Stephen Venn

Venn S. 2007. Morphological responses to disturbance in wing-polymorphic carabid species(Coleoptera: Carabidae) of managed urban grasslands. Baltic J. Coleopterol., 7 (1): 51 - 59.

A disturbance gradient comprising three intensities of management of grasslands in urbanparks is used to study the responses of carabid beetles to disturbance. The three levels ofdisturbance are: mown, intermediate and meadow. GLM is used to analyze the response oftwo morphological traits to disturbance: body size, macroptery and wing length ofbrachypterous individuals. The proportion of macropterous individuals was greater in thepopulations of both disturbed and intermediate sites. Also wing-length of brachypterousindividuals was longer in the disturbed and intermediate treatments. For body size, there wasno change in mean body size for females, though males were larger in the disturbed andintermediate treatments. These males were similarly sized with females, whereas in the undis-turbed treatment, there was strong sexual dimorphism for this trait. I conclude that distur-bance results in changes that are important for population dynamics. There is a need forfurther study of species traits that are affected by disturbance, rather than just species assem-blage effects.

Key words: Benign neglect, brachypterous, dispersal, disturbance, Lamarck, lawn,macropterous, semi-natural grasslands, sexual dimorphism, Wing-dimorphic, wing-polymor-phic, urban

Stephen Venn. Department of Biological and Environmental Sciences, Faculty of Biosciences,P.O. Box. 65 (Viikinkaari 1), 00014 University of Helsinki, Finland; e-mail:stephen.venn@helsinki.fi

such as roadside verges, to unmanagedgrasslands. Lawns in urban parks are amongstthe most intensely managed grasslands, gener-ally being mown using tractor-drawn machineryon an approximately 2-week interval. Whilst thelong history of this form of management has re-sulted in some species developing behaviourpatterns to help them exploit the resultant lawnhabitat, particularly birds of the thrush family

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(Turdus spp) and starling (Sturnus vulgaris), ithas also been criticized on ecological groundsfor preventing plant species from completing theirreproductive cycles. Thus the flora of lawns isdominated by species that colonize vegetativelyand those which manage to flower and set seedvery rapidly, such as white clover Trifoliumrepens.

Whilst the establishment and management oflawns has been traditionally favoured for rea-sons of ease and economy (Kendle & Forbes1997), and a number of popular recreational ac-tivities require lawns, many municipalities areconsidering the adoption of alternative grass-land management strategies. The potential eco-nomical and ecological benefits resulting fromtransferring to less intensive grassland manage-ment regimes are the main incentive for thischange. The term benign-neglect has been ap-plied to the termination of such habitat manage-ment regimes (Haila et al. 1989). For grasslands,however, the adoption of a less intensive man-agement regime is generally preferable to thecomplete cessation of management. Mowingonce or twice per year produces conditions fa-vourable for many forbs and nectar-feeding in-sects, whereas cessation of management oftenresults in a habitat that is both aesthetically andecologically of poor quality.

Habitat management, such as mowing, representsa disturbance regime for at least some taxa (Grime1979). In the case of mowing a lawn, the impacton different taxa will vary according to their mo-bility and scale of perception. For bird species ofthe lawn ecosystem, it is highly unlikely thatmowing represents a disturbance, though forplant species, mowing represents a stress thatimpairs the growth of dominant species but im-proves growing conditions for shorter forbs inparticular. For epigaeic arthropod assemblages,the disturbance of mowing is likely to representa periodically repeated disturbance.

As well as representing a disturbance regime,mowing also maintains favourable habitat con-ditions for many sensitive taxa. This has beenshown particularly well for nectar-feeding in-

sects, such as the butterfly species Melitaeacinxtia (Hanski et al. 1995). For the less mobileepigaeic fauna, however, the influence of mow-ing is not clear. The primary objective of thisstudy is to consider the influence of mowing andits cessation on the carabid assemblage of urbangrasslands. The reason for this is to consider theinfluence of changes in management regime onbiodiversity.

Wing morphology in carabids

Carabid beetles are one of a number of insecttaxa in which wing morphology can vary consid-erably within the same species. Thus differentindividuals within the same population of thesame species can have radically different disper-sal ability. Species that exhibit two or more wingmorphs, generally with a flight capable full-winged(macropterous) form and a reduced winged(brachypterous) form that is incapable of flight,have been referred to as dimorphic, which im-plies that there are simply two morphs:macropterous and brachypterous. However, inmany instances, wing length appears to be a con-tinuous variable, so I consider the term polymor-phic to be more appropriate than dimorphic. Inaddition to wing morphology, there is also varia-tion in development of the flight muscle, withsome macropterous individuals being incapableof flight due to undeveloped flight muscles(Desender, Lindroth 1992). Lindroth (1992) alsoreports observations of individuals with reducedwings that attempt to fly, that clearly possessfunctional flight muscles. In the present study,flight muscles are not examined and wing mor-phology is the only measured indicator of po-tential flight ability.

Lindroth also observed that the proportions ofmacropterous and brachypterous individuals inpopulations of wing-polymorphic carabids couldvary considerably between populations from thesame geographical region. He used such wingmorphology data to hypothesize on the coloni-zation routes of carabid species in the Palaearcticregion subsequent to the Würmian glacial pe-riod (Lindroth 1971?), and he also acknowledgedthat “environmental factors are likely to influ-

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Morphological responses to disturbance in wing-polymorphic carabid species (Coleoptera: Carabidae)...

ence the distribution of different wing morphs inpopulations” (Lindroth 1992).

Both Lindroth (1992) and den Boer (1971) con-sidered that the proportion of macropterous in-dividuals in a population was indicative of theage and stability of the population. A stable andlong established population should contain al-most exclusively brachypterous individuals, asdispersal ability is not advantageous in thesecircumstances. By means of breeding experi-ments, Lindroth (1949) has shown that forPterostichus anthracinus, macroptery is deter-mined by a recessive gene, with macropterousindividuals being homozygous recessive. If weassume, as Lindroth (1992) and den Boer did,that macropterous species are adapted for colo-nization, then a newly founded population willbe composed of macropterous individuals andtheir progeny. In reality it is likely that somecolonizers might be brachypterous individuals,as species that are entirely brachypterous arealso capable of dispersal and colonization of newhabitats. Clearly though, individuals that havefunctional wings in addition to strong legs arebetter adapted to disperse. Indeed if newlyfounded populations are composed entirely ofhomozygous recessive macropterous species,then that population will remain macropterousunless there is an inoculation of brachypterousindividuals. The only other possibility for devel-opment to a wing-polymorphic population is ifbrachypterous individuals are produced as theresult of a mutation. Thus in a newly foundedpopulation of a wing polymorphic species, thepopulation should either 1) remain macropterous(homozygous recessive) or 2) acquire thebrachyptery gene and produce a gradually in-creasing proportion of brachypterous individu-als and eventually develope a brachypterouspopulation with a small number of macropterousindividuals. Being better adapted for dispersal, aproportion of these macropterous individuals willemigrate, further reducing the proportion ofmacropterous individuals in the population. Thisfraction of emigrating individuals should increaseas the population size approaches its carryingcapacity, as competition for resources increasesthe incentive to disperse. Thus an old, stable

population is likely to be composed of almostentirely brachypterous individuals and corre-spondingly a less stable population should con-tain more macropterous individuals.

A number of more recent studies using carabidshave suggested that when disturbance increases,the numbers of specialist, large bodied andpoorly dispersing species decrease in abundance,whilst generalist, small bodied effectivedispersers increase (Rushton et al. 1989, Blakeet al. 1994, Niemelä et al. 2000 & Grandchamp etal. 2002).

In this study I compare the wing morphologyratios of wing-polymorphic species under threetreatment regimes, 1) lawn - mown at c. 2 weeklyintervals, 2) intermediate - mown at two weeklyintervals until the previous season and thereaf-ter not managed, 3) meadow - unmanaged for>10 years. Assuming that mowing constitutes adisturbance for epigaeic carabid populations ofthese habitats, I consider that this design repre-sents a disturbance gradient with treatment (1)lawn as intensive disturbance, treatment (3)meadow as undisturbed and treatment (2) as in-termediate. Treatment 3 should thus represent astable population, treatment 1 an unstable popu-lation and treatment 2 an intermediate popula-tion. My hypothesis is that there should be ahigher proportion of macropterous individualsin the lawn treatment, a small proportion in themeadow treatment and intermediate in the inter-mediate treatment. I will also compare the winglengths of brachypterous specimens to see if thereis any change in wing length along the distur-bance gradient.

MATERIALS AND METHODS

Study sites

Five urban parks in the city of Helsinki were usedfor this study. Each site contained (1) an area ofgrassland that had been managed intensively(mown lawn) for many years previously (intensedisturbance), (2) an area of formerly mown grass-land that had been unmanaged for c. 10 years

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previously (unmanaged/minimal disturbance)and (3) an area of formerly mown grassland thathad been mown until one year prior to the onsetof this study but was subsequently leftunmanaged (intermediate disturbance), exceptfor the site Hertakannas Crematorium Park, inwhich there was no meadow treatment.

Study design

Sampling was performed using 140 plastic pit-fall traps of 67mm diameter. Traps were placed10 m apart in transects of 10 per treatment andcontained propylene glycol (50% aqueous) as apreservative. Lids of 10 cm2 were placed overthe traps to prevent inundation. The traps wereset on 7/5/2003, emptied monthly and maintaineduntil 16/9/2003. The trapped carabid beetles wereidentified to species using Lindroth (1985, 1986).

Analyses

GLMWing morph was analyzed by means of general-ized linear model (GLM) using the negative bi-nomial distribution, as has been recommendedfor taxa with an aggregated distribution (Niemeläet al.1992). The tested factors are macropterousvs. brachypterous for all carabid species andwing length of brachypterous individuals ofwing polymorphic species, and with gender as acategorical variable. A randomized block designwas employed, though it was incomplete due tothe absence of one treatment from one site. Ahierarchical design of trap nested in site wasused. The statistical package R 1.7.1 was usedfor the statistical analyses.

RESULTS

The total catch consisted of 1902 carabid bee-tles, belonging to 40 species. The most abun-dant species were Bembidion properans (28.9%of total catch), Pterostichus melanarius (14.1%)and Harpalus rufipes (9.46%).

DISCUSSION

My previous paper on this study (Venn & Rokala2005) considered the effects of disturbance, inthis case mowing, on beetle size and flight at thespecies level. This was accomplished by catego-rizing species into five size classes and as flightcapable, flightless or wing dimorphic. That studyshowed that, in accordance with Gray˙s hypoth-esis that larger sized species should be predomi-nant when disturbance is less intense, the small-est size class was more numerous in the mostdisturbed treatments and the largest size classwas most numerous in the least disturbed treat-ments (Gray 1989). Also the proportion of flight-less species decreased with increasing distur-bance and the proportion of flight capable (pio-neer) species increases, in accordance with Gray˙shypothesis, that the proportion of flight capablepioneer species should increase with increasingdisturbance. Furthermore individuals of dimor-phic species increased strongly with increasingdisturbance, in keeping with the suggestion thatwing dimorphism is an adaptation to overcomedispersal barriers.

In the present study, I have tested the same hy-potheses but at the individual level, using thefactors body size, wing morphology and lengthof wing fragments of individuals with reducedwings, in place of species values derived fromthe literature. This enables me to test the actualvariation of wing morphology and body sizewithin species. The results show that mean bodysize is unaffected by disturbance for femalesthough male body size was considerably smallerin the undisturbed treatment (Fig. 1). This resultis the opposite to the prediction of Gray˙s hy-pothesis, whereby body size should decreasewith increasing disturbance.

For wing morphology the results were in keepingwith Gray˙s hypothesis. The proportion ofmacropterous individuals was much less in theundisturbed meadow treatment (Fig. 2). For fe-males the mean value was much smaller than formales, though the amount of variation was alsomuch greater. Measurement of the wing fragments

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Fig. 1 Male body size is smaller at the meadow (unmanaged) sites than on both of the other treat-ments. There is no significant difference in female body size between the treatments, though thevariation is markedly less in the meadow population, suggesting greater stability

of brachypterous individuals showed further-more that the wings were smaller for individualsfrom the least disturbed treatment (Fig. 3). Thisis also in keeping with Gray˙s hypothesis, thatflight ability should be more developed in indi-viduals from more disturbed treatments. In thiscase males showed the greater difference in wingsize between more and less disturbed treatments(Fig. 3).

For all three of these analyses there was no dis-cernable difference between the most disturbed(lawn) treatment and intermediate (mown untilprevious season).

These results thus support the hypothesis thatincreased levels of disturbance result in in-creased investment in flight ability. The similar-ity in the results for the most disturbed treatment(lawn) and intermediate (undisturbed for one sea-son) suggest that there is a delay of more thanone year before any reduction in this adaptationto disturbance. It would be interesting to repeatthe study in subsequent seasons in the samesites, to see whether there is evidence of a sub-sequent reduction in macroptery and wing sizewith time in subsequent seasons after the cessa-tion of mowing and, if so, how rapidly this change

Morphological responses to disturbance in wing-polymorphic carabid species (Coleoptera: Carabidae)...

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then spreads through the population. The mor-phology of individuals from the undisturbedmeadow treatment should be regarded as thenormal situation, and that of the other two treat-ments as the response to disturbance. Thus theseresults seem to also indicate that another affectof increasing disturbance is reduced sexual di-morphism in these traits, as there is considerablevariation between the results for males and fe-males for all three of the measured traits in the

meadow treatment, and very little such variationfrom the two disturbed treatments.

These results appear to show that, for males inparticular, there is a shift towards macroptery andlarger body size as disturbance increases, pre-sumably because smaller sized andbrachypterous individuals are lost from the popu-lation. For the larger females, their body size isalready sufficiently large to enable persistence

Fig. 2 Less macropterous individuals in meadow (unmanaged) populations, particularly females. Inthis case, the variation is greatest in the meadow treatment.

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in a disturbed site, though disturbance results ina considerable reduction in the proportion ofbrachypterous individuals.

The increase in length of wing fragments ofbrachypterous individuals with increasing dis-turbance seems at first puzzling, as it is difficultto conceive of a longer non-functional wing con-ferring any kind of advantage to individuals inpersisting in a disturbed site. This could sug-gest that there is continuous variation betweenbrachyptery and macroptery, with increasingmean wing fragment length leading towards theproduction of macropterous individuals. How-ever, such an explanation seems to be Lamarck-

ian and to defy explanation in terms of naturalselection.

I conclude that whilst disturbance effects oncommunity composition are well documented formany taxa in a variety of disturbed habitats, thisstudy shows that there are also complex effectson population dynamics, and traits affecting fit-ness. This suggests that, changes in speciescomposition of communities is inadequate forassessing the ecological impacts of disturbance.There is clearly a need for the developement ofother indicators for assessing the ecological im-pacts of disturbance. Genetic studies to eluci-date the mechanisms behind the phenotypic re-

Fig. 3 Wing rudiments are smaller in individuals from meadow populations, particularly in males.

Morphological responses to disturbance in wing-polymorphic carabid species (Coleoptera: Carabidae)...

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sponses observed in this study are also neces-sary, as there are many issues that are not re-solvable on the basis of phenotype data.

ACKNOWLEDGEMENTS

I wish to thank the Finnish Biologist˙s SocietyVanamo for providing funding for this study, Pro-fessor Jari Niemelä for support and guidance, KatiRokala for assistance with the fieldwork and iden-tification and Dr. Bob O˙Hara for significant as-sistance with the analyses.

LITERATURE

Blake, S., Foster, G.N., Eyre, M. D. & Luff, M. L.1994: Effects of habitat type and grasslandmanagement practices on the body size dis-tribution of carabid beetles. Pedobiologia38: 502-512.

Den Boer, P.J. 1971: On the dispersal power ofcarabid beetles and its possible significanceIn: Dispersal and dispersal power ofcarabid beetles (ed. Den Boer, P.J.) Miscel-laneous papers 8, LH Wageningen, The Neth-erlands 119-137

Connell, J.H. 1978: Diversity in tropical rainfor-ests and coral reefs. Science 199: 1302-1310.

Grandchamp, A., Niemelä, J. & Kotze, J. 2002: theeffects of trampling on assemblages ofground beetles (Coleoptera, Carabidae) inurban forests in Helsinki, Finland. UrbanEcosystems 4: 321-332.

Gray, J.S. 1989: Effects of environmental stresson species rich assemblages. BiologicalJournal of the Linnean Society 37: 19-32.

Grime, J.P. 1979: Plant strategies and vegetationprocesses John Kiley, Chichester UK

Haila, Y., Halme, E. & Somerma, P. 1988:Kaupunkiviheriöiden ekologisen

monipuolisuuden arviointi.Pääkaupunkiseudulla suoritetunkaupunkiekologisen tutkimuksenväliraportti. [engl. Evaluating the ecologi-cal diversity of urban green space, in Finn-ish] Helsinki municipality publications C1988:8. YTV-SAD. 39 p.

Haila, Y., Tonteri, T., Halme, E. & Somerma, P. 1989:Kaupunkiviheriöiden kasvillisuudenvaihtelu hyönteisten esiintymistämääräävänä tekijänä. [engl. Variability ofvegetation in urban green spaces as a factoraffecting insect distribution, in Finnish] Re-port of urban ecological research in Helsinki1987-1988. Helsinki City City Planning De-partment Master Plan Department publica-tion YB 5/1989. Helsinki municipality publi-cations C 1989:4. YTV-SAD. 51 p.

Hanski, I., Pakkala, T., Kuussaari, M. & Lei, G.1995: Metapopulation persistence of an en-dangered butterfly in a fragmented land-scape. Oikos 72: 21-28

Kendle, T. & Forbes, S. 1997: Urban Nature Con-servation: Landscape Management in theurban Countryside Spon Press, London, pp264

Lindroth, C.H. 1985: The Carabidae(Coleoptera) of Fennoscandia and Den-mark. Volume 15, part 1. ScandinavianPress.Ltd. 225 p.

Lindroth, C.H. 1986: The Carabidae(Coleoptera) of Fennoscandia and Den-mark. Volume 15, part 2. pp. 233-497.Scandinavian Press.Ltd.

Lindroth, C.H. 1992: Ground Beetles(Carabidae) of Fennoscandia. AmerindPublishing Co. Pvt. Ltd., New Delhi. 814 p.

Niemelä, J., Haila, Y., Halme, E., Pajunen, T. &Punttila, P. 1992: Small–scale heterogeneityin the spatial distribution of carabid beetles

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in the Southern Finnish taiga. Journal ofBiogeography 19: 173-181.

Niemelä, J., Kotze, J., Ashworth, A., Brandmayr,P., Desender, K., New, T., Penev, L., Samways& M., Spence, J. 2000: the search for com-mon anthropogenic impacts on biodiversity:a global network. Journal of Insect Conser-vation 4: 3-9.

Rushton, S.P., Eyre, M.D. & Luff, M.L. 1989: Ef-fect of pasture improvement and manage-ment on the ground beetle and spider com-munities of upland grasslands. Journal ofApplied Ecology 26: 489-503.

Venn, S.J., Kotze, D.J. & Niemelä, J. 2003: Urbani-zation effects on carabid diversity in borealforests. European Journal of Entomology100: 73-80.

Venn, S. & Rokala, K. (2005) Effects of grasslandmanagement strategy on the carabid faunaof urban parks in Protection of Coleopterain the Baltic Sea Region eds. Skłodowski, J.Huruk, S., Barsevskis, A. and Tarasiuk, S.Warsaw Agricultural University Press pp. 65-75

Received: 06.02.2007.Accepted: 31.05.2007.

Morphological responses to disturbance in wing-polymorphic carabid species (Coleoptera: Carabidae)...

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New book from Warsaw Agricultural University Press:

Monitoring zooindykacyjny pohuraganowych zniszczeń ekosystemówleśnych Puszczy Piskiej

Zooindicative monitoring of hurricane caused damage of forest eco-systems of Pisz Forest

Editor: J. Skłodowski

Departmet of Forest Protection and Ecology, SGGW – Warsaw Agricultural UniversityWarsaw Agricultural University Press 2007, pp. 200.

Book in Polish with extended English Summary Contents:

Introduction – Jarosław Skłodowski

Study area description – Jarosław Skłodowski

Selected indices describing the status of the envi-ronment – Jarosław Skłodowski

Dynamics of forest floor vegetation in the wind de-stroyed plots of Pisz Forest District – Marek Sławski

Forest floor dynamics in the stands destroyed byhurricane, results of the onground photographic re-cording method – Jarosław Skłodowski and JerzyBuszyniewicz

The dynamics of composit ion and structure ofepigeic-soil communities of Collembola in the standsof Pisz Forests destroyed by the hurr icane –Małgorzata Sławska and Marek Sławski

Diplopoda and Chilopoda fauna in the ecosystemsof posthurricane and control stands – Henryk Tracz

Dynamics of body length of the dung beetle‘Anoplotrupes stercorosus˙ in the hurricane de-stroyed stands and in the control stands – JarosławSkłodowski and Tadeusz Duda

The zooindication monitoring of wind-caused dam-age to the Pisz Forest based on the condition ofcarabids (Coleoptera, Carabidae) – JarosławSkłodowski

Analysis of cambio- and cambio-xylophilous bee-tles and accompanying subcortical Coleoptera faunaoccurrence in Scots pine trees at the area of Refer-ence Szast Forest - Artur Rutkiewicz

Discussion – Jarosław Skłodowskiwww.wydawnictwosggw.pl