Climatic gradients and forest composition shape bat communities in Eastern Mediterranean pine plantations

Abstract

Biotic and abiotic factors can act as filters for determining the species composition of biological communities. We aimed to identify abiotic factors driving the assembly of bat communities in Eastern Mediterranean pine plantations along a north–south climatic gradient, as they are crucial forest habitats for the assessment and conservation of these communities. We expected that bat communities are predominantly shaped by environmental filtering. We conducted acoustic sampling in 35 pine plantations in Israel and analyzed recordings for species identification. We used the ESLTP analysis, an extension of the three-table ordination (RLQ analysis), to explore relationships between environmental characteristics, species occurrences, and functional traits of species while accounting for phylogenetic relationships between species and spatial distribution of the communities. Communities showed phylogenetic and trait clustering. Climatic conditions and forest vegetation composition shaped communities of bats, affecting the distribution of traits related to foraging behaviors, vegetation clutter, and the ability of bats to maneuver in it. Maneuverable species were associated with the northern Mediterranean climatic zone, with a scarce cover of drought-tolerant small shrubs and grassland. Fast flyers were associated with the center-south semi-arid area, with abundant drought-tolerant small shrubs and grassland. These forces might have a predominant role in the assembly of these communities, presumably due to the stressful climatic conditions of the study area. The ESLTP approach can be extended to other taxa and environments to predict species responses to disturbance and environmental changes and give insights into environmental management.

Keywords

assembly rules / bats / environmental filtering / Mediterranean ecosystem / pine forest

References

[1] Ackerly DD,Cornwell WK (2007). A trait-based approach to community assembly: Partitioning of species trait values into within-and among-community components. Ecology Letters 10,135–145.

[2] Adams RA,Hayes MA (2021). The importance of water availability to bats: Climate warming and increasing global aridity. In: Lim BK,Fenton MB,Brigham RM,Mistry S,Kurta A,Gillam EH, eds. 50 Years of Bat Research. Springer,New York, pp. 105–120.

[3] Adams RA,Pedersen SC (2013). Bat Evolution, Ecology, and Conservation. Springer,New York.

[4] Agnarsson I,Zambrana-Torrelio CM,Flores-Saldana NP,May-Collado LJ (2011). A time-calibrated species-level phylogeny of bats (Chiroptera, Mammalia). PLoS Currents 3,RRN1212.

[5] Aldridge HD,Rautenbach IL (1987). Morphology, echolocation, and resource partitioning in insectivorous bats. The Journal of Animal Ecology 56,763–778.

[6] Allegrini C,Korine C,Krasnov BR (2022). Insectivorous bats in Eastern Mediterranean planted pine forests—Effects of forest structure on foraging activity, diversity, and implications for management practices. Forests 13,1411.

[7] Amichai E,Levin E,Kronfeld-Schor N,Roll U,Yom-Tov Y (2013). Natural history, physiology, and energetic strategies of Asellia tridens (Chiroptera). Mammalian Biology 78,94–103.

[8] Avila-Flores R,Medellin RA (2004). Ecological, taxonomic, and physiological correlates of cave use by mexican bats. Journal of Mammalogy 85,675–687.

[9] Barak Y,Yomtov Y (1991). The mating system of Pipistrellus kuhlii (Microchiroptera) in Israel. Mammalia 55,285–292.

[10] Batalha MA,Silva IA,Cianciaruso MV,França H,de Carvalho GH (2011). Phylogeny, traits, environment, and space in cerrado plant communities at Emas National Park (Brazil). Flora—Morphology, Distribution, Functional Ecology of Plants 206,949–956.

[11] Becker NI,Encarnação JA,Tschapka M,Kalko EKV (2012). Energetics and life-history of bats in comparison to small mammals. Ecological Research 28,249–258.

[12] Ben-Hamo M,Munoz-Garcia A,Williams JB,Korine C,Pinshow B (2013). Waking to drink: Rates of evaporative water loss determine arousal frequency in hibernating bats. Journal of Experimental Biology 216,573–577.

[13] Bloch CP,Stevens RD,Willig MR (2011). Body size and resource competition in New World bats: A test of spatial scaling laws. Ecography 34,460–468.

[14] Burgar JM,Stokes VL,Craig MD (2017). Habitat features act as unidirectional and dynamic filters to bat use of production landscapes. Biological Conservation 209,280–288.

[15] Cadotte MW,Tucker CM (2017). Should environmental filtering be abandoned? Trends in Ecology & Evolution 32,429–437.

[16] Capaverde UD,Pereira LGdA,Tavares VdC,Magnusson WE,Baccaro FB,Bobrowiec PED (2018). Subtle changes in elevation shift bat-assemblage structure in Central Amazonia. Biotropica 50,674–683.

[17] Cavender-Bares J,Ackerly DD,Baum DA,Bazzaz FA (2004). Phylogenetic overdispersion in Floridian oak communities. American Naturalist 163,823–843.

[18] Culina A,Garroway CJ (2019). Bats use social information within and across species. The Journal of Animal Ecology 88,1444–1446.

[19] Dale MR,Fortin MJ (2014). Spatial Analysis: A Guide for Ecologists. Cambridge University Press,Cambridge.

[20] Dambros C,Zuquim G,Moulatlet GM et al. (2020). The role of environmental filtering, geographic distance and dispersal barriers in shaping the turnover of plant and animal species in Amazonia. Biodiversity and Conservation 29,3609–3634.

[21] Denzinger A,Schnitzler H-U (2013). Bat guilds, a concept to classify the highly diverse foraging and echolocation behaviors of microchiropteran bats. Frontiers in Physiology 4,164.

[22] Dolédec S,Chessel D,Ter Braak CJF,Champely S (1996). Matching species traits to environmental variables: A new three-table ordination method. Environmental and Ecological Statistics 3,143–166.

[23] Dray S,Pélissier R,Couteron P et al. (2012). Community ecology in the age of multivariate multiscale spatial analysis. Ecological Monographs 82,257–275.

[24] Dray S,Choler P,Dolédec S et al. (2014). Combining the fourth-corner and the RLQ methods for assessing trait responses to environmental variation. Ecology 95,14–21.

[25] Duchamp JE,Swihart RK (2008). Shifts in bat community structure related to evolved traits and features of human-altered landscapes. Landscape Ecology 23,849–860.

[26] Fenton MB,Bogdanowicz W (2002). Relationships between external morphology and foraging behaviour: Bats in the genus Myotis. Canadian Journal of Zoology 80,1004–1013.

[27] Fick SE,Hijmans RJ (2017). WorldClim 2: new 1-km spatial resolution climate surfaces for global land areas. International Journal of Climatology 37,4302–4315.

[28] Frampton GK,Van Den Brink PJ,Gould PJ (2000). Effects of spring drought and irrigation on farmland arthropods in southern Britain. Journal of Applied Ecology 37,865–883.

[29] Franco-Belussi L,Provete DB,de Oliveira C (2017). Environmental correlates of internal coloration in frogs vary throughout space and lineages. Ecology & Evolution 7,9222–9233.

[30] Frank TM,Gabbert WC,Chaves-Campos J,LaVal RK (2019). Impact of artificial lights on foraging of insectivorous bats in a Costa Rican cloud forest. Journal of Tropical Ecology 35,8–17.

[31] Gearhart C,Adams AM,Pinshow B,Korine C (2020). Evaporative water loss in Kuhl’s pipistrelles declines along an environmental gradient, from mesic to hyperarid. Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology 240,110587.

[32] Goldreich Y (2012). The Climate of Israel: Observation, Research and Application. Springer Science & Business Media,New York.

[33] Hanspach J,Fischer J,Ikin K,Stott J,Law BS (2012). Using trait-based filtering as a predictive framework for conservation: A case study of bats on farms in southeastern Australia. Journal of Applied Ecology 49,842–850.

[34] Hardy OJ,Senterre B (2007). Characterising the phylogenetic structure of communities by an additive partitioning of phylogenetic diversity. Journal of Ecology 95,493–506.

[35] Harris I,Jones PD,Osborn TJ,Lister DH (2014). Updated high-resolution grids of monthly climatic observations—the CRU TS3.10 Dataset. International Journal of Climatology 34,623–642.

[36] Huelsenbeck JP,Ronquist FJB (2001). MRBAYES: Bayesian Inference of Phylogenetic Trees 17,754–755.

[37] Jamieson MA,Trowbridge AM,Raffa KF,Lindroth RL (2012). Consequences of climate warming and altered precipitation patterns for plant-insect and multitrophic interactions. Plant Physiology 160,1719–1727.

[38] Kalka MB,Smith AR,Kalko EK (2008). Bats limit arthropods and herbivory in a tropical forest. Science 320,71–71.

[39] Keddy P (1999). Wetland restoration: The potential for assembly rules in the service of conservation. Wetlands 19,716–732.

[40] Kirk MA,Rahel FJ,Laughlin DC (2022). Environmental filters of freshwater fish community assembly along elevation and latitudinal gradients. Global Ecology and Biogeography 31,470–485.

[41] Krasnov BR,Shenbrot GI,Khokhlova IS,Stanko M,Morand S,Mouillot D (2015). Assembly rules of ectoparasite communities across scales: Combining patterns of abiotic factors, host composition, geographic space, phylogeny and traits. Ecography 38,184–197.

[42] Kunz TH,Braun de Torrez E,Bauer D,Lobova T,Fleming TH (2011). Ecosystem services provided by bats. Annals of the New York Academy of Sciences 1223,1–38.

[43] Levin SA (2012). The Princeton Guide to Ecology. Princeton University Press,Princeton.

[44] MacArthur R,Levins R (1967). Limiting similarity convergence and divergence of coexisting species. American Naturalist 101,377.

[45] Maddison W,Maddison D (2021). Mesquite: A modular system for evolutionary analysis. Version 3.70. Available from URL: http://www.mesquiteproject.org

[46] Marciente R,Bobrowiec PE,Magnusson WE (2015). Ground-vegetation clutter affects phyllostomid bat assemblage structure in lowland amazonian forest. PLoS ONE 10,e0129560.

[47] McCracken GF,Westbrook JK,Brown VA,Eldridge M,Federico P,Kunz TH (2012). Bats track and exploit changes in insect pest populations. PLoS ONE 7,e43839.

[48] McGill BJ,Enquist BJ,Weiher E,Westoby M (2006). Rebuilding community ecology from functional traits. Trends in Ecology 21,178–185.

[49] Mello MAR,Felix GM,Pinheiro RBP et al. (2019). Insights into the assembly rules of a continent-wide multilayer network. Nature Ecology & Evolution 3,1525–1532.

[50] Mendelssohn H,Yom-Tov Y (1999). Mammalia of Israel. Israel Academy of Sciences and Humanities,Jerusalem.

[51] Meyer CFJ,Kalko EKV (2008). Bat assemblages on Neotropical land-bridge islands: Nested subsets and null model analyses of species co-occurrence patterns. Diversity and Distributions 14,644–654.

[52] Muller J,Brandl R,Buchner J et al. (2013). From ground to above canopy-Bat activity in mature forests is driven by vegetation density and height. Forest Ecology and Management 306,179–184.

[53] Nekola JC,White PS (1999). The distance decay of similarity in biogeography and ecology. Journal of Biogeography 26,867–878.

[54] Norberg UM,Rayner JM (1987). Ecological morphology and flight in bats (Mammalia; Chiroptera): Wing adaptations, flight performance, foraging strategy and echolocation. Philosophical Transactions of The Royal Society B Biological Sciences 316,335–427.

[55] Osem Y,Fogel T,Moshe Y,Ashkenazi M,Brant S (2017). Understory structure and function following release from cattle grazing and overstory thinning in Mediterranean conifer plantations. Annals of Forest Science 74,22.

[56] Patrick LE,Stevens RD (2016). Phylogenetic community structure of North American desert bats: Influence of environment at multiple spatial and taxonomic scales. The Journal of Animal Ecology 85,1118–1130.

[57] Pavoine S (2020). adiv: An r package to analyse biodiversity in ecology. Methods in Ecology and Evolution 11,1106–1112.

[58] Pavoine S,Baguette M,Bonsall MB (2010). Decomposition of trait diversity among the nodes of a phylogenetic tree. Ecological Monographs 80,485–507.

[59] Pavoine S,Bonsall MB (2011). Measuring biodiversity to explain community assembly: A unified approach. Biological Reviews 86,792–812.

[60] Pavoine S,Vela E,Gachet S,de Belair G,Bonsall MB (2011). Linking patterns in phylogeny, traits, abiotic variables and space: A novel approach to linking environmental filtering and plant community assembly. Journal of Ecology 99,165–175.

[61] Posada D (2008). jModelTest: Phylogenetic model averaging. Molecular Biology and Evolution 25,1253–1256.

[62] Posada D,Buckley TR (2004). Model selection and model averaging in phylogenetics: Advantages of Akaike information criterion and Bayesian approaches over likelihood ratio tests. Systematic Biology 53,793–808.

[63] R Core Team (2021). R: A Language Environment for Statistical Computing. R Foundation for Statistical Computing,Vienna, Austria.

[64] Razgour O,Korine C,Saltz D (2010). Pond characteristics as determinants of species diversity and community composition in desert bats. Animal Conservation 13,505–513.

[65] Razgour O,Persey M,Shamir U,Korine C (2018). The role of climate, water and biotic interactions in shaping biodiversity patterns in arid environments across spatial scales. Diversity and Distributions 24,1440–1452.

[66] Riedinger V,Müller J,Stadler J,Ulrich W,Brandl R (2013). Assemblages of bats are phylogenetically clustered on a regional scale. Basic and Applied Ecology 14,74–80.

[67] Rodrigues JFM,Sobral FL,Iverson JB,Diniz JAF (2019). Phylogenetic and spatial analyses suggest minimum temperature as an environmental filter for turtle communities. Journal of Biogeography 46,671–679.

[68] Ronquist F,Teslenko M,van der Mark P et al. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology 61,539–542.

[69] Russo D,Ancillotto L,Jones G (2018). Bats are still not birds in the digital era: Echolocation call variation and why it matters for bat species identification. Canadian Journal of Zoology 96,63–78.

[70] Saito VS,Cianciaruso MV,Siqueira T,Fonseca-Gessner AA,Pavoine S (2016). Phylogenies and traits provide distinct insights about the historical and contemporary assembly of aquatic insect communities. Ecology & Evolution 6,2925–2937.

[71] Saldaña-Vázquez RA,Munguía-Rosas MA (2013). Lunar phobia in bats and its ecological correlates: A meta-analysis. Mammalian Biology 78,216–219.

[72] Speakman JR (2001). The evolution of flight and echolocation in bats: Another leap in the dark. Mammal Review 31,111–130.

[73] Sternberg M,Holzapfel C,Tielbörger K et al. (2011). The use and misuse of climatic gradients for evaluating climate impact on dryland ecosystems—An example for the solution of conceptual problems. Climate Change -Geophysical Foundations and Ecological Effects 12,361–374.

[74] Stevens RD,Willig MR (2002). Geographical ecology at the community level: Perspectives on the diversity of New World bats. Ecology 83,545–560.

[75] Thioulouse J,Dray S,Dufour AB,Siberchicot A,Jombart T,Pavoine S (2018). Multivariate Analysis of Ecological Data with ade4. Springer,New York.

[76] Threlfall C,Law B,Penman T,Banks PB (2011). Ecological processes in urban landscapes: Mechanisms influencing the distribution and activity of insectivorous bats. Ecography 34,814–826.

[77] Todd VLG,Williamson LD (2019). Habitat usage of Daubenton’s bat (Myotis daubentonii), common pipistrelle (Pipistrellus pipistrellus), and soprano pipistrelle (Pipistrellus pygmaeus) in a North Wales upland river catchment. Ecology & Evolution 9,4853–4863.

[78] Violle C,Navas M-L, Vile D et al. (2007). Let the concept of trait be functional! Oikos 116,882–892.

[79] Voigt CC,Holderied MW (2012). High manoeuvring costs force narrow-winged molossid bats to forage in open space. Journal of Comparative Physiology B 182,415–424.

[80] Weiher E,Keddy P (2001). Ecological Assembly Rules: Perspectives, Advances, Retreats. Cambridge University Press,Cambridge.

[81] Yom-Tov Y,Kadmon R (1998). Analysis of the distribution of insectivorous bats in Israel. Diversity and Distributions 4,63–70.

[82] Zohary M (1966). Flora Palaestina. In: Part 1—Text, Equisetaceae to Moringaceae, The Israel Academy of Science and Humanities. Goldbergs Press,Jerusalem.

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