Habitat fragmentation impacts mobility in a common and widespread woodland butterfly: do sexes respond differently?

Annals of Occupational and Environmental Medicine

Benjamin Bergerot¹  Thomas Merckx³  Hans Van Dyck⁴  Michel Baguette² 

[1] hepia Geneva, University of Applied Sciences Western Switzerland, Technology, Architecture and Landscape, Centre de Lullier, Route de Presinge 150, Jussy, CH-1254, Switzerland

[2] CNRS, USR 2936, Station d’ Ecologie Expérimentale du CNRS, Moulis, 09200, France

[3] Theoretical Ecology and Biodiversity Change Lab, Centro de Biologia Ambiental, Faculdade de Ciências, Universidade de Lisboa, Campo Grande, Lisboa,, 1749-016, Portugal

[4] Biodiversity Research Centre, Earth and Life Institute, Université catholique de Louvain (UCL), Croix du Sud 4 bte, Louvain-la-Neuve, L7.07.04, B-1348, Belgium

关键词: Dispersal benefit;    Dispersal cost;    Permeability;    Edge effect;    Mean daily distances;   

Others  :  1086058
DOI  :  10.1186/1472-6785-12-5

 received in 2012-01-19, accepted in 2012-04-18,  发布年份 2012

【 摘 要 】

Background

Theory predicts a nonlinear response of dispersal evolution to habitat fragmentation. First, dispersal will be favoured in line with both decreasing area of habitat patches and increasing inter-patch distances. Next, once these inter-patch distances exceed a critical threshold, dispersal will be counter-selected, unless essential resources no longer co-occur in compact patches but are differently scattered; colonization of empty habitat patches or rescue of declining populations are then increasingly overruled by dispersal costs like mortality risks and loss of time and energy. However, to date, most empirical studies mainly document an increase of dispersal associated with habitat fragmentation. We analyzed dispersal kernels for males and females of the common, widespread woodland butterfly Pararge aegeria in highly fragmented landscape, and for males in landscapes that differed in their degree of habitat fragmentation.

Results

The male and female probabilities of moving were considerably lower in the highly fragmented landscapes compared to the male probability of moving in fragmented agricultural and deciduous oak woodland landscapes. We also investigated whether, and to what extent, daily dispersal distance in the highly fragmented landscape was influenced by a set of landscape variables for both males and females, including distance to the nearest woodland, area of the nearest woodland, patch area and abundance of individuals in the patch. We found that daily movement distance decreased with increasing distance to the nearest woodland in both males and females. Daily distances flown by males were related to the area of the woodland capture site, whereas no such effect was observed for females.

Conclusion

Overall, mobility was strongly reduced in the highly fragmented landscape, and varied considerably among landscapes with different spatial resource distributions. We interpret the results relative to different cost-benefit ratios of movements in fragmented landscapes.

【 授权许可】

   
2012 Bergerot et al.; licensee BioMed Central Ltd.

【 图 表 】

Figure 1 .

Figure 2 .

Figure 3 .

Figure 4 .

Figure 5 .

【 参考文献 】

• [1]Clobert J, Danchin E: Dhont AA, Nichols JD (Eds): Dispersal. New York: Oxford University Press; 2001.
• [2]Ricketts TH: The matrix matters: Effective isolation in fragmented landscapes. Am Nat 2001, 158:87-99.
• [3]Hanski I (Eds): Metapopulation ecology. New York: Oxford University Press; 1999.
• [4]Spear SF, Balkenhol N, Fortin MJ, McRae BH, Scribner K: Use of resistance surfaces for landscape genetic studies: considerations for parameterization and analysis. Mol Ecol 2010, 19:3576-3591.
• [5]Bonte D, Van Dyck H, Bullock JM, Coulon A, Delgado M, Gibbs M, Delgado M, Lehouck V, Matthysen E, Mustin K, Saastamoinen M, Schtickzelle, N., Stevens VM, Vandewoestijne S, Baguette M, Barton K, Benton TG, Chaput-Bardy A, Clobert J, Dytham C, Hovestadt T, Meier CM, Palmer SC, Turlure C, Travis JM: Costs of dispersal. Biol Rev 2012. in press
• [6]Shreeve TG, Dennis RLH: Landscape scale conservation: resources, behaviour, the matrix and opportunities. J Insect Conserv 2010, 15:179-188.
• [7]Schtickzelle N, Mennechez G, Baguette M: Dispersal depression with habitat fragmentation in the bog fritillary butterfly. Ecology 2006, 87:1057-1065.
• [8]Stevens VM, Pavoine S, Baguette M: Variation within and between closely related species uncovers high intra-specific variability in dispersal. PLoS One 2010, 5:e11123.
• [9]Stevens VM, Verkenne C, Vandewoestijne S, Wesselingh RA, Baguette M: Gene flow and functional connectivity in the natterjack toad. Mol Ecol 2006, 15:2333-2344.
• [10]Van Dyck H, Baguette M: Dispersal behaviour in fragmented landscapes: Routine or special movements? Basic Appl Ecol 2005, 6:535-545.
• [11]Ohsaki N: Comparative population studies of three Pieris butterflies, Pieris rapae, Pieris melete and Pieris napi, living in the same area .2. Utilization of patchy habitats by adults through migratory and non-migratory movements. Res Popul Ecol 1980, 22:163-183.
• [12]Baguette M, Van Dyck H: Landscape connectivity and animal behavior: functional grain as a key determinant for dispersal. Landsc Ecol 2007, 22:1117-1129.
• [13]Merckx T, Van Dyck H, Karlsson B, Leimar O: The evolution of movements and behaviour at boundaries in different landscapes. Proc R Soc B 2003, 270:1815-1821.
• [14]Merckx T, Van Dyck H: Habitat fragmentation affects habitat-finding ability of the speckled wood butterfly, Pararge aegeria L. Anim Behav 2007, 74:1029-1037.
• [15]Stevens VM, Turlure C, Baguette M: A meta-analysis of dispersal in butterflies. Biol Rev 2010, 85:625-642.
• [16]Snep RPH, Opdam PFM, Baveco JM, WallisDeVries MF, Timmermans W, Kwak RGM, Kuypers V: How peri-urban areas can strengthen animal populations within cities: A modeling approach. Biol Conserv 2006, 127:345-355.
• [17]Thomas CD: Dispersal and extinction in fragmented landscapes. Proc R Soc B 2000, 267:139-145.
• [18]Hughes CL, Hill JK, Dytham C: Evolutionary trade-offs between reproduction and dispersal in populations at expanding range boundaries. Proc R Soc B 2003, 270:147-150.
• [19]Hughes CL, Dytham C, Hill JK: Modelling and analysing evolution of dispersal in populations at expanding range boundaries. Ecol Entomol 2007, 32:437-445.
• [20]Van Dyck H, Van Strien AJ, Maes D, Van Swaay CAM: Declines in common, widespread butterflies in a landscape under intense human use. Conserv Biol 2009, 23:957-965.
• [21]Hanski I, Heino M: Metapopulation-level adaptation of insect host plant preference and extinction-colonization dynamics in heterogeneous landscapes. Theor Popul Biol 2003, 64:281-290.
• [22]Ovaskainen O, Hanski I: From individual behavior to metapopulation dynamics: Unifying the patchy population and classic metapopulation models. Am Nat 2004, 164:364-377.
• [23]Rabasa SG, Gutierrez D, Escudero A: Relative importance of host plant patch geometry and habitat quality on the patterns of occupancy, extinction and density of the monophagous butterfly Iolana iolas. Oecologia 2008, 156:491-503.
• [24]Dover J, Settele J: The influences of landscape structure on butterfly distribution and movement: a review. J Insect Conserv 2009, 13:3-27.
• [25]Gaston KJ, Blackburn TM, Greenwood JJD, Gregory RD, Quinn RM, Lawton JH: Abundance-occupancy relationships. J Appl Ecol 2000, 37:39-59.
• [26]Honnay O, Jacquemyn H: Susceptibility of common and rare plant species to the genetic consequences of habitat fragmentation. Conserv Biol 2007, 21:823-831.
• [27]Hill JK, Collingham YC, Thomas CD, Blakeley DS, Fox R, Moss D, Huntley B: Impacts of landscape structure on butterfly range expansion. Ecol Lett 2001, 4:313-321.
• [28]Hill JK, Thomas CD, Fox R, Telfer MG, Willis SG, Asher J, Huntley B: Responses of butterflies to twentieth century climate warming: implications for future ranges. Proc R Soc B 2002, 269:2163-2171.
• [29]Vandewoestijne S, Van Dyck H: Population genetic differences along a latitudinal cline between original and recently colonized habitat in a butterfly. PLoS One 2010, 5(11):e13810.
• [30]Bergerot B, Fontaine B, Renard M, Cadi A, Julliard R: Preferences for exotic flowers do not promote urban life in butterflies. Landsc Urban Plan 2010, 96:98-107.
• [31]Chardon JP, Adriaensen F, Matthysen E: Incorporating landscape element into a connectivity measure: a case study for the Speckled wood butterfly (Pararge aegeria L.). Landsc Ecol 2003, 18:561-573.
• [32]Shreeve TG: Habitat selection, mate location, and microclimatic constraints on the activity of the speckled wood butterfly Pararge aegeria. Oikos 1984, 42:371-377.
• [33]Schweiger O, Dormann CF, Bailey D, Frenzel M: Occurrence pattern of Pararge aegeria (Lepidoptera : Nymphalidae) with respect to local habitat suitability, climate and landscape structure. Landsc Ecol 2006, 21:989-1001.
• [34]Karlsson B, Van Dyck H: Does habitat fragmentation affect temperature-related life-history traits? A laboratory test with a woodland butterfly. Proc R Soc B 2005, 272:1257-1263.
• [35]Merckx T, Van Dyck H: Mate location behaviour of the butterfly Pararge aegeria in woodland and fragmented landscapes. Anim Behav 2005, 70:411-416.
• [36]Gibbs M, Van Dyck H: Butterfly flight activity affects reproductive performance and longevity relative to landscape structure. Oecologia 2010, 163:341-350.
• [37]Hill JK, Hughes CL, Dytham C, Searle JB: Genetic diversity in butterflies: interactive effects of habitat fragmentation and climate-driven range expansion. Biol Lett 2006, 2:152-154.
• [38]Parmesan C, Ryrholm N, Stefanescu C, Hill JK, Thomas CD, Descimon H, Huntleyk B, Kaila L, Kullberg J, Tammaru T, Tennent WJ, Thomas JA, Warren M: Poleward shifts in geographical ranges of butterfly species associated with regional warming. Nature 1999, 399:579-583.
• [39]Kemp DJ, Wiklund C, Van Dyck H: Contest behaviour in the speckled wood butterfly (Pararge aegeria): seasonal phenotypic plasticity and the functional significance of flight performance. Behav Ecol Sociobiol 2006, 59:403-411.
• [40]Merckx T, Van Dyck H: Landscape structure and phenotypic plasticity in flight morphology in the butterfly Pararge aegeria. Oikos 2006, 113:226-232.
• [41]Petit S, Moilanen A, Hanski I, Baguette M: Metapopulation dynamics of the bog fritillary butterfly: movements between habitat patches. Oikos 2001, 92:491-500.
• [42]Schultz CB, Crone EE: Edge-mediated dispersal behavior in a prairie butterfly. Ecology 2001, 82:1879-1892.
• [43]Berwaerts K, Van Dyck H, Aerts P: Does flight morphology relate to flight performance? An experimental test with the butterfly Pararge aegeria. Funct Ecol 2002, 16:484-491.
• [44]Wickman PO, Wiklund C: Territorial defense and its seasonal decline in the speckled wood butterfly (Pararge aegeria). Anim Behav 1983, 31:1206-1216.
• [45]Vande Velde L, Turlure C, Van Dyck H: Body temperature and territory selection by males of the speckled wood butterfly (Pararge aegeria): what makes a forest sunlit patch a rendezvous site? Ecol Entomol 2011, 36:161-169.
• [46]Bergman M, Wiklund C: Differences in mate location behaviours between residents and nonresidents in a territorial butterfly. Anim Behav 2009, 78:1161-1167.
• [47]Van Dyck H, Matthysen E: Thermoregulatory differences between phenotypes in the speckled wood butterfly: hot perchers and cold patrollers? Oecologia 1998, 114:326-334.
• [48]Kuussaari M, Nieminen M, Hanski I: An experimental study of migration in the Glanville fritillary butterfly Melitaea cinxia. J Anim Ecol 1996, 65:791-801.
• [49]Mennechez G, Petit S, Schtickzelle N, Baguette M: Modelling mortality and dispersal: consequences of parameter generalisation on metapopulation dynamics. Oikos 2004, 106:243-252.
• [50]Wagner HH, Wildi O, Ewald KC: Additive partitioning of plant species diversity in an agricultural mosaic landscape. Landsc Ecol 2000, 15:219-227.
• [51]Shreeve TG: Egg-laying by the speckled wood butterfly (Pararge aegeria): the role of female behavior, host plant abundance and temperature. Ecol Entomol 1986, 11:229-236.
• [52]Baker RR: In The dilemma: when and how to go or to stay, The biology of butterlies. Edited by Vane-Wrigth RI, Ackery PR. London: Academic; 1984:279-296.
• [53]Ries L, Debinski DM: Butterflies responses to habitat edges in the highly fragmented prairies of Central Iowa. J Anim Ecol 2001, 70:840-852.
• [54]Rutowski RL: Postural changes accompany perch location changes in male butterflies (Asterocampa leilia) engaged in visual mate searching. Ethology 2000, 106:453-466.
• [55]Van Dyck H, Matthysen E, Dhondt AA: The effect of wing colour on male behavioural strategies in the speckled wood butterfly. Anim Behav 1997, 53:39-51.
• [56]Pellegroms B, Van Dongen S, Van Dyck H, Lens L: Larval food stress differentially affects flight morphology in male and female speckled woods (Pararge aegeria). Ecol Entomol 2009, 34:387-393.
• [57]Gotthard K, Nylin S, Wiklund C: Mating system evolution in response to search costs in the speckled wood butterfly, Pararge aegeria. Behav Ecol Sociobiol 1999, 45:424-429.
• [58]Hill JK, Thomas CD, Lewis OT: Effects of habitat patch size and isolation on dispersal by Hesperia comma butterflies: Implications for metapopulation structure. J Anim Ecol 1996, 65:725-735.
• [59]Clobert J, Le Galliard JF, Cote J, Meylan S, Massot M: Informed dispersal, heterogeneity in animal dispersal syndromes and the dynamics of spatially structured populations. Ecol Lett 2009, 12:197-209.
• [60]Thomas CD, Hanski I: Butterfly metapopulations. Edited by Hanski I, Gilpin M. San Diego: Academic; 1997:359-386.
• [61]Hovestadt T, Messner S, Poethke HJ: Evolution of reduced dispersal mortality and ‘fat-tailed’ dispersal kernels in autocorrelated landscapes. Proc R Soc Lond B 2001, 268:385-391.
• [62]Heinz SK, Strand E: Adaptive patch searching strategies in fragmented landscapes. Evol Ecol 2006, 20:113-130.
• [63]Barton KA, Phillips BL, Morales JM, Travis JMJ: The evolution of an 'intelligent' dispersal strategy: biased, correlated random walks in patchy landscapes. Oikos 2009, 118:309-319.
• [64]Roff DA: The evolution of flightlessness in insects. Ecol Monogr 1990, 60:389-421.
• [65]Langellotto GA, Denno RF: Benefits of dispersal in patchy environments: mate location by males of a wing-dimorphic insect. Ecology 2001, 82:1870-1878.
• [66]Hill KJ, Dytham C, Hughes CL: Evolutionary changes in expanding butterfly populations. Edited by Fellowes MDE, Holloway GJ, Rolff J. Oxon: CABI publishing; 2005:519-533.
• [67]Schtickzelle N, Baguette M: Behavioural responses to habitat patch boundaries restrict dispersal and generate emigration-patch area relationships in fragmented landscapes. J Anim Ecol 2003, 72:533-545.
• [68]Berwaerts K, Van Dyck H: Take-off performance under optimal and suboptimal thermal conditions in the butterfly Pararge aegeria. Oecologia 2004, 141:536-545.
• [69]Dover J, Sparks T: A review of the ecology of butterflies in British hedgerows. J Environ Manage 2000, 60:51-63.
• [70]Berwaerts K, Aerts P, Van Dyck H: On the sex-specific mechanisms of butterfly flight: flight performance relative to flight morphology, wing kinematics, and sex in Pararge aegeria. Biol J Linn Soc 2006, 89:675-687.
• [71]Baguette M, Schtickzelle N: Negative relationship between dispersal distance and demography in butterfly metapopulations. Ecology 2006, 87:648-654.
• [72]MacKenzie DI, Nichols JD, Lachman GB, Droege S, Royle JA, Langtimm CA: Estimating site occupancy rates when detection probabilities are less than one. Ecology 2002, 83:2248-2255.
• [73]Akaike H: A new look at the statistical-model identification. Curr Contents Eng Technol Appl Sci 1981, 51:22-22.