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Influence of the direct and indirect effects of habitat fragmentation, via microclimate change, on animal locomotion

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Abstract

Context

Intensive use of agricultural land often modifies the landscape by dividing continuous natural habitat into smaller and more isolated patches. While the effects of habitat fragmentation on species abundance and diversity have been widely studied, little is known about how fragmentation impacts the function of organisms that do persist in the modified environment. Understanding these effects is complicated by the fact that fragmentation can affect organisms directly but also indirectly, by altering the patch microclimatic conditions.

Objectives

We tested the hypothesis that fragmentation-induced microclimate change might be an important mechanism driving changes in animal locomotion in an agricultural landscape.

Methods

We used satellite image analysis, behavioral assays, and patch analyses, to disentangling the direct and indirect effects of fragmentation on the locomotor behavior of a darkling beetle, Zophosis punctata (Tenebrionidae), in the Southern Judea Lowlands in Israel.

Results

We found that fragmentation in an agricultural ecosystem may lead to changes in the thermal conditions of natural habitat patches. Importantly, such fragmentation-related increases in patch temperature played an important role in explaining variation in beetle locomotion across an agricultural landscape. Specifically, beetles from highly fragmented landscapes, which included warmer habitat patches, showed high locomotor intermittence -frequent pausing events during locomotion.

Conclusions

This study shows that the potential consequences of habitat fragmentation on organism function are likely to be underestimated when fragmentation-related microclimate change is ignored. Intermittent locomotion, as opposed to steady locomotion, may provide physiological and fitness benefits in fragmented landscapes, like mitigating performance limitations imposed by extreme thermal conditions.

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Data availability

Data are shared privately for-peer review in a figshare repository https://figshare.com/s/ab2abfef546ca0f10848. If paper is accepted for publication, data will be permanently archived in this same repository.

References

  • Aiken LS, West, SG (1991) Multiple regression: testing and interpreting interactions. Sage Publications, Incorporated, Newbury Park

  • Alexander RMN (2005) Models and the scaling of energy costs for locomotion. J Exp Biol 208:1645–1652

    Article  PubMed  Google Scholar 

  • Allsopp PG (1980) The biology of false wireworms and their adults (soil-inhabiting Tenebrionidae) (Coleoptera): a review. Bull Entomol Res 70:343–379

    Article  Google Scholar 

  • Angilletta MJ, Steury TD, Sears MW (2004) Temperature, growth rate, and body size in ectotherms: fitting pieces of a life-history puzzle. Integr Comp Biol 44:498–509

    Article  PubMed  Google Scholar 

  • Arroyo-Rodríguez V, Saldaña-Vázquez RA, Fahrig L, Santos BA (2017) Does forest fragmentation cause an increase in forest temperature? Ecol Res 32:81–88

    Article  Google Scholar 

  • Baguette M, Legrand D, Fréville H et al (2012) Evolutionary ecology of dispersal in fragmented landscape. In: Clobert J, Baguette M, Benton TGBJ (eds) Dispersal ecology and evolution. Oxford University Press, Oxford, pp 381–391

    Google Scholar 

  • Bender DJ, Tischendorf L, Fahrig L (2003) Using patch isolation metrics to predict animal movement in binary landscapes. Landsc Ecol 181(18):17–39

    Article  Google Scholar 

  • Bergerot B, Merckx T, Van Dyck H, Baguette M (2012) Habitat fragmentation impacts mobility in a common and widespread woodland butterfly: do sexes respond differently? BMC Ecol 12:5

    Article  PubMed  PubMed Central  Google Scholar 

  • Bivand RS, Pebesma E, Gómez-Rubio V (2013) Applied spatial data analysis with R, 2nd edn. Springer, New York

    Book  Google Scholar 

  • Boyle MJW, Bishop TR, Luke SH et al (2021) Localised climate change defines ant communities in human-modified tropical landscapes. Funct Ecol 35:1094–1108

    Article  CAS  Google Scholar 

  • Castro AV, Porrini DP, Cicchino AC, Scharf I (2014) Annual activity density of groundbeetles (Coleoptera: Carabidae) of a Celtis ehrenbergiana (Rosales: Celtidaceae) Forest of Buenos Aires Province, Argentina. J Insect Sci. https://doi.org/10.1093/jisesa/ieu114

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen J, Saunders SC, Crow TR et al (1999) Microclimate in forest ecosystem and landscape ecology: variations in local climate can be used to monitor and compare the effects of different management regimes. Bioscience 49:288–297

    Article  Google Scholar 

  • Chown SL, Pistorius P, Scholtz CH (2011) Morphological correlates of flightlessness in southern African Scarabaeinae (Coleoptera:Scarabaeidae): testing a condition of the water-conservation hypothesis. Can J Zool 76:1123–1133

    Article  Google Scholar 

  • Davis ALV, Chown SL, Scholtz CH (1999) Discontinuous gas-exchange cycles in Scarabaeus dung beetles (Coleoptera: Scarabaeidae): mass-scaling and temperature dependence. Physiol Biochem Zool 72:555–565

    Article  CAS  PubMed  Google Scholar 

  • De Heij SE, Benaragama D, Willenborg CJ (2022) Carabid activity-density and community composition, and their impact on seed predation in pulse crops. Agric Ecosyst Environ 326:107807

    Article  Google Scholar 

  • Ewers RM, Banks-Leite C (2013) Fragmentation impairs the microclimate buffering effect of tropical forests. PLoS ONE 8:e58093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ferrante L, Baccaro FB, Ferreira EB et al (2017) The matrix effect: how agricultural matrices shape forest fragment structure and amphibian composition. J Biogeogr 44:1911–1922

    Article  Google Scholar 

  • Ferraz G, Nichols JD, Hines JE et al (2007) A large-scale deforestation experiment: effects of patch area and isolation on Amazon birds. Science (80–) 315:238–241

    Article  CAS  Google Scholar 

  • Full RJ, Zuccarello DA, Tullis A (1990) Effect of variation in form on the cost of terrestrial locomotion. J Exp Biol 150:233–246

    Article  CAS  PubMed  Google Scholar 

  • Gavish Y, Ziv Y, Rosenzweig ML (2012) Decoupling fragmentation from habitat loss for spiders in patchy agricultural landscapes. Conserv Biol 26:150–159

    Article  PubMed  Google Scholar 

  • Giladi I, Ziv Y, May F, Jeltsch F (2011) Scale-dependent determinants of plant species richness in a semi-arid fragmented agro-ecosystem. J Veg Sci 22:983–996

    Article  Google Scholar 

  • Goosem M (2001) Effects of tropical rainforest roads on small mammals: inhibition of crossing movements. Wildl Res 28:351–364

    Article  Google Scholar 

  • Haddad NM, Brudvig LA, Clobert J et al (2015) Habitat fragmentation and its lasting impact on Earth’s ecosystems. Sci Adv 1:e1500052

    Article  PubMed  PubMed Central  Google Scholar 

  • Hargis CD, Bissonette JA, David JL (1998) The behavior of landscape metrics commonly used in the study of habitat fragmentation. Landsc Ecol 13:167–186

    Article  Google Scholar 

  • Harper KA, Macdonald SE, Burton PJ et al (2005) Edge influence on forest structure and composition in fragmented landscapes. Conserv Biol 19:768–782

    Article  Google Scholar 

  • Hill JK, Thomas CD, Blakeley DS (1999) Evolution of flight morphology in a butterfly that has recently expanded its geographic range. Oecologia. https://doi.org/10.1007/s004420050918

    Article  PubMed  Google Scholar 

  • Holben BN (1986) Characteristics of maximum-value composite images from temporal AVHRR data. Int J Remote Sens 7:1417–1434

    Article  Google Scholar 

  • Jensen JR (2009) Remote sensing of the environment: an Earth resource perspective, 2nd edn. Pearson Education India, New Delhi

    Google Scholar 

  • Klepsatel P, Gáliková M (2022) Developmental temperature affects thermal dependence of locomotor activity in Drosophila. J Therm Biol 103:103153

    Article  CAS  PubMed  Google Scholar 

  • Kramer DL, McLaughlin RL (2001) The behavioral ecology of intermittent locomotion. Am Zool 41:137–153

    Google Scholar 

  • Lachenicht MW, Clusella-Trullas S, Boardman L et al (2010) Effects of acclimation temperature on thermal tolerance, locomotion performance and respiratory metabolism in Acheta domesticus L. (Orthoptera: Gryllidae). J Insect Physiol 56:822–830

    Article  CAS  PubMed  Google Scholar 

  • Latimer CE, Zuckerberg B (2017) Forest fragmentation alters winter microclimates and microrefugia in human-modified landscapes. Ecography (cop). https://doi.org/10.1111/ecog.02551

    Article  Google Scholar 

  • Lausch A, Herzog F (2002) Applicability of landscape metrics for the monitoring of landscape change: issues of scale, resolution and interpretability. Ecol Indic 2:3–15

    Article  Google Scholar 

  • Lázaro A, Fuster F, Alomar D, Totland Ø (2020) Disentangling direct and indirect effects of habitat fragmentation on wild plants’ pollinator visits and seed production. Ecol Appl 30:e02099

    Article  PubMed  Google Scholar 

  • Lefcheck JS (2016) piecewiseSEM: piecewise structural equation modelling in r for ecology, evolution, and systematics. Methods Ecol Evol 7:573–579

    Article  Google Scholar 

  • Lehmann FO, Schützner P (2010) The respiratory basis of locomotion in Drosophila. J Insect Physiol 56:543–550

    Article  CAS  PubMed  Google Scholar 

  • Leitão AB, Miller J, Ahern J, McGarigal K (2006) Measuring landscapes: a planner’s handbook. Island Press, Washington DC

    Google Scholar 

  • May F, Giladi I, Ristow M et al (2013) Plant functional traits and community assembly along interacting gradients of productivity and fragmentation. Perspect Plant Ecol Evol Syst 15:304–318

    Article  Google Scholar 

  • McAdam AG, Kramer DL (1998) Vigilance as a benefit of intermittent locomotion in small mammals. Anim Behav 55:109–117

  • McGarigal K, Marks BJ (1995) FRAGSTATS: spatial pattern analysis program for quantifying landscape structure. USDA Forest Service General Technical Report PNW-351, Corvallis

  • McGarigal K, Cushman SA, Neel MC, Ene E (2002) FRAGSTATS: spatial pattern analysis program for categorical maps. In: Analysis. https://www.umass.edu/landeco/research/fragstats/fragstats.html. Accessed 18 Oct 2021

  • Mendenhall CD, Karp DS, Meyer CFJ et al (2014) Predicting biodiversity change and averting collapse in agricultural landscapes. Nature 509:213–217

    Article  CAS  PubMed  Google Scholar 

  • Merckx T, Van Dyck H, Karlsson B, Leimar O (2003) The evolution of movements and behaviour at boundaries in different landscapes: a common arena experiment with butterflies. Proc R Soc B Biol Sci 270:1815–1821

    Article  Google Scholar 

  • Mesquita RCG, Delamônica P, Laurance WF (1999) Effect of surrounding vegetation on edge-related tree mortality in Amazonian forest fragments. Biol Conserv 91:129–134

    Article  Google Scholar 

  • Morales JM (2002) Behavior at habitat boundaries can produce leptokurtic movement distributions. Am Nat 160:531–538

    Article  PubMed  Google Scholar 

  • Murcia C (1995) Edge effects in fragmented forests: implications for conservation. Trends Ecol Evol 10:58–62

    Article  CAS  PubMed  Google Scholar 

  • Paladino FV (1985) Temperature effects on locomotion and activity bioenergetics of amphibians, reptiles, and birds. Integr Comp Biol 25:965–972

    Google Scholar 

  • Pallarés S, Verberk WCEP, Bilton DT (2021) Plasticity of thermal performance curves in a narrow range endemic water beetle. J Therm Biol 102:103113

    Article  PubMed  Google Scholar 

  • Parastatidis D, Mitraka Z, Chrysoulakis N, Abrams M (2017) Online global land surface temperature estimation from landsat. Remote Sens 9:1208

    Article  Google Scholar 

  • Pennisi E (2000) In nature, animals that stop and start win the race. Science (80–) 288:83–85

    Article  CAS  Google Scholar 

  • Petraitis PS, Dunham AE, Niewiarowski PH (1996) Inferring multiple causality: the limitations of path analysis. Funct Ecol 10:421

    Article  Google Scholar 

  • Potts JR, Hillen T, Lewis MA (2016) The “edge effect” phenomenon: deriving population abundance patterns from individual animal movement decisions. Theor Ecol 9:233–247

    Article  Google Scholar 

  • Püttker T, Crouzeilles R, Almeida-Gomes M et al (2020) Indirect effects of habitat loss via habitat fragmentation: a cross-taxa analysis of forest-dependent species. Biol Conserv 241:108368

    Article  Google Scholar 

  • Robinson NP, Allred BW, Jones MO et al (2017) A dynamic landsat derived normalized difference vegetation index (NDVI) product for the conterminous United States. Remote Sens 9:863

    Article  Google Scholar 

  • Rodriguez A, Zhang H, Klaminder J et al (2017) ToxId: an efficient algorithm to solve occlusions when tracking multiple animals. Sci Rep 7:14774

    Article  PubMed  PubMed Central  Google Scholar 

  • Rodriguez A, Zhang H, Klaminder J et al (2018) ToxTrac: a fast and robust software for tracking organisms. Methods Ecol Evol 9:460–464

    Article  Google Scholar 

  • Rotem G, Gavish Y, Shacham B et al (2016) Combined effects of climatic gradient and domestic livestock grazing on reptile community structure in a heterogeneous agroecosystem. Oecologia 180:231–242

    Article  PubMed  Google Scholar 

  • Rotem G, Giladi I, Bouskila A, Ziv Y (2020) Scale-dependent correlates of reptile communities in natural patches within a fragmented agroecosystem. Landsc Ecol 35:2339–2355

    Article  Google Scholar 

  • Saunders DA, Hobbs RJ, Margules CR (1991) Biological consequences of ecosystem fragmentation: a review. Conserv Biol 5:18–32

    Article  Google Scholar 

  • Saunders SC, Chen J, Crow TR, Brosofske KD (1998) Hierarchical relationships between landscape structure and temperature in a managed forest landscape. Landsc Ecol 13:381–395

    Article  Google Scholar 

  • Senior RA, Hill JK, González del Pliego P et al (2017) A pantropical analysis of the impacts of forest degradation and conversion on local temperature. Ecol Evol 7:7897–7908

    Article  PubMed  PubMed Central  Google Scholar 

  • Shipley B (2013) The AIC model selection method applied to path analytic models compared using a d-separation test. Ecology 94:560–564

    Article  PubMed  Google Scholar 

  • Shipley B (2016) Cause and correlation in biology, 2nd edn. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Slobodchikoff CN (1983) Water balance and temperature preferences, and their role in regulating activity times of tenebrionid beetles. Oikos 40:113

    Article  Google Scholar 

  • Thomas CD, Hill JK, Lewis OT (1998) Evolutionary consequences of habitat fragmentation in a localized butterfly. J Anim Ecol 67:485–497

    Article  Google Scholar 

  • Trabalon M (2022) Effects of wolf spiders’ captive environment on their locomotor and exploratory behaviours. Insects. https://doi.org/10.3390/insects13020135

    Article  PubMed  PubMed Central  Google Scholar 

  • Tuff KT, Tuff T, Davies KF (2016) A framework for integrating thermal biology into fragmentation research. Ecol Lett 19:361–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Van Dyck H, Matthysen E (1999) Habitat fragmentation and insect flight: a changing “design” in a changing landscape? Trends Ecol Evol 14:172–174

    Article  Google Scholar 

  • Vasquez RA, Ebensperger LA, Bozinovic F (2002) The influence of habitat on travel speed, intermittent locomotion, and vigilance in a diurnal rodent. Behav Ecol 13:182–187

  • Weinstein RB, Full RJ (1992) Intermittent exercise alters endurance in an eight-legged ectotherm. Am J Physiol Regul Integr Comp Physiol 262:R852–R859

    Article  CAS  Google Scholar 

  • Weinstein RB, Full RJ (1998) Performance limits of low-temperature, continuous locomotion are exceeded when locomotion is intermittent in the ghost crab. Physiol Zool 71:274–284

    Article  CAS  PubMed  Google Scholar 

  • Weinstein RB, Full RJ (1999) Intermittent locomotion increases endurance in a gecko. Physiol Biochem Zool 72:732–739

    Article  CAS  PubMed  Google Scholar 

  • Yaacobi G, Ziv Y, Rosenzweig ML (2007) Effects of interactive scale-dependent variables on beetle diversity patterns in a semi-arid agricultural landscape. Landsc Ecol 22:687–703

    Article  Google Scholar 

  • Ziv Y, Davidowitz G (2019) When landscape ecology meets physiology: effects of habitat fragmentation on resource allocation trade-offs. Front Ecol Evol 7:137

    Article  Google Scholar 

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Acknowledgements

This project was funded by NSF IOS-1656279 to GD and YZ.

Funding

This work was supported by an NSF IOS-1656279 to GD and YZ.

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Contributions

All authors conceived of the concepts and ideas. NT and GK conducted the field and lab work, with assistance from GD and YZ. NT and GK analyzed the data. NT and GK wrote the manuscript, with editorial input provided by GD and YZ.

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Correspondence to Natasha Tigreros.

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Tigreros, N., Kozhoridze, G., Davidowitz, G. et al. Influence of the direct and indirect effects of habitat fragmentation, via microclimate change, on animal locomotion. Landsc Ecol 38, 847–859 (2023). https://doi.org/10.1007/s10980-022-01588-5

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