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Species, hybrid and genotype effects on leaf litter curling, and their extended consequences for spiders and soil moisture dynamics

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Abstract

Background and aims

Subtle morphological traits, such as leaf litter curling, may have unexpected legacy effects on ecosystems. We tested the hypotheses that litter curling is influenced by plant species, hybridization and genotype, and has extended consequences for associated organisms and soil processes.

Methods

A novel litter curling index (LCI) was used to characterize the curling of leaf litter from 11 plant species (including shrubs, trees and a forb) in natural field sites and of two Populus species (P. fremontii James, P. angustifolia S. Watson), their F1 hybrids and replicated P. angustifolia genotypes from a common garden. Surveys of dominant, litter-dwelling spiders (Agelenidae), and a soil drying experiment, were used to test the potential extended ecological consequences of litter curling.

Results

Five results emerged. (1) LCI ranged 15-fold among plant species in natural sites. (2) LCI nearly doubled from P. fremontii to P. angustifolia, while average LCI for F1 hybrids was intermediate (although not statistically different from P. fremontii). (3) LCI exhibited broad-sense heritability (H2 = 0.42) among P. angustifolia genotypes. (4) Abundance of spider webs was positively associated with increasing litter curl across the Populus hybrid system (R2 = 0.35). (5) After 57 days of drying, flat litter contained 1.4 times higher moisture than curled litter, which translated to wetter soil beneath flat litter.

Conclusion

Litter curling has a genetic basis, which has legacy effects on other trophic levels and soil moisture dynamics that may shape the ecology and evolution of complex communities.

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Data availability

Data generated for this study are available in the Dryad Digital Repository at doi:https://doi.org/10.5061/dryad.2jm63xsth.

References

  • Babl E, Alexandera HD, Siegerta CM, Willis JL (2020) Could canopy, bark, and leaf litter traits of encroaching non-oak species influence future flammability of upland oak forests? For Ecol Manage 458:117731. https://doi.org/10.1016/j.foreco.2019.117731

    Article  Google Scholar 

  • Barbour RC, Baker SC, O’Reilly-Wapstra JM, Harvest TM, Potts BM (2009) A footprint of tree‐genetics on the biota of the forest floor. Oikos 118:1917–1923. https://doi.org/10.1111/j.1600-0706.2009.17609.x

    Article  Google Scholar 

  • Bosco JM, Riechert SE, O’Meara BC (2017) The ontogeny of personality traits in the desert funnel-web spider, Agelenopsis lisa (Araneae: Agelenidae). Ethology 123:648–658

    Google Scholar 

  • Brygadyrenko VV (2014) Influence of soil moisture on litter invertebrate community structure of pine forests of the steppe zone of Ukraine. Folia Oecol 41:8–16

    Google Scholar 

  • Bultman TL, Uetz GW (1982) Abundance and community structure of forest floor spiders following litter manipulation. Oecologia 55:34–41

    PubMed  Google Scholar 

  • Bultman TL, Uetz GW (1984) Effect of structure and nutritional quality of litter on abundances of litter-dwelling arthropods. Amer Mid Nat 111:165–172

    Google Scholar 

  • Burton JE, Cawson JG, Filkov AI, Penman TD (2021) Leaf traits predict global patterns in the structure and flammability of forest litter beds. J of Ecol 109:1344–1355. https://doi.org/10.1111/1365-2745.13561

    Article  CAS  Google Scholar 

  • Butenschoen O, Scheu S, Eisenhauer N (2011) Interactive effects of warming, soil humidity and plant diversity on litter decomposition and microbial activity. Soil Biol Biochem 43:1902–1907

    CAS  Google Scholar 

  • Classen AT, Overby ST, Hart SC, Koch GW, Whitham TG (2007) Season mediates herbivore effects on litter and soil microbial abundance and activity in a semi-arid woodland. Plant Soil 295:217–227

    CAS  Google Scholar 

  • Compson ZG, Hungate BA, Whitham TG, Meneses N, Busby P, Wojtowicz T, Ford A, Adams KJ, Marks JC (2016) Plant genotype influences aquatic-terrestrial ecosystem linkages through timing and composition of insect emergence. Ecosphere 7:e01331. https://doi.org/10.1002/ecs2.1331

    Article  Google Scholar 

  • Crutsinger GM, Rodriguez-Cabal MA, Roddy AB, Peay KG, Bastow JL, Kidder AG, Dawson TE, Fine PV, Rudgers JA (2014) Genetic variation within a dominant shrub structures green and brown community assemblages. Ecology 95:387–398. https://doi.org/10.1890/13-0316.1

    Article  PubMed  Google Scholar 

  • Crutsinger GM, Sanders NJ, Classen AT (2009) Comparing intra- and inter-specific effects on litter decomposition in an old-field ecosystem. Basic Appl Biol 10:535–543

    Google Scholar 

  • Deutsch ES, Bork EW, Willms WD (2010) Soil moisture and plant growth responses to litter and defoliation impacts in Parkland grasslands. Agric Ecosyst Environ 135:1–9. https://doi.org/10.1016/j.agee.2009.08.002

    Article  Google Scholar 

  • Driebe EM, Whitham TG (2000) Cottonwood hybridization affects tannin and nitrogen content of leaf litter and alters decomposition. Oecologia 123:99–107

    PubMed  CAS  Google Scholar 

  • Drost DR, Puranik S, Novaes E, Novaes CRDB, Dervinis C, Gailing O, Kirst M (2015) Genetical genomics of Populus leaf shape variation. BMC Plant Biol 15:1–10

    CAS  Google Scholar 

  • Engber E, Varner J (2012) Patterns of flammability of the California oaks: the role of leaf traits. Can J For Res 42:1965–1975

    Google Scholar 

  • Fischer DG, Classen AT, Chapman SK, Gehring CA, Grady KC, Schweitzer JA, Whitham TG (2014) Marschner Review: can plant genes mediate plant and soil responses to climate change? Plant Soil 379:1–19

    CAS  Google Scholar 

  • Fischer DG, Hart SC, Rehill BJ, Lindroth RL, Keim P, Whitham TG (2006) Do high-tannin leaves require more roots? Oecologia 149:668–675

    PubMed  CAS  Google Scholar 

  • Fischer DG, Hart SC, Whitham TG, Martinsen GD, Keim P (2004) Ecosystem implications of genetic variation in water-use of a dominant riparian tree. Oecologia 139:288–297

    PubMed  CAS  Google Scholar 

  • Gehring CA, Mueller RC, Whitham TG (2006) Environmental and genetic effects on the formation of ectomycorrhizal and arbuscular mycorrhizal associations in cottonwoods. Oecologia 149:158–164

    PubMed  Google Scholar 

  • Gómez JE, Lohmiller J, Joern A (2016) Importance of vegetation structure to the assembly of an aerial web-building spider community in north american open grassland. J Arachnol 44:28–35

    Google Scholar 

  • Heatwole H (1961) Analysis of the forest floor habitat with a structural classification of the litter layer or L layer. Ecol Mono 31:267–283

    Google Scholar 

  • Higgins RW, Chen Y, Douglas AV (1999) Interannual variability of the Northern American warm season precipitation regime. J Clim 12:653–680

    Google Scholar 

  • Hobbie SE (1992) Effects of plant species on nutrient cycling. Trends Ecol Evol 7:336–339

    PubMed  CAS  Google Scholar 

  • Ivask M, Kuu A, Truu M, Truu J (2006) The effect of soil type and soil moisture on earthworm communities. Agraarteadus 17:3–33

    Google Scholar 

  • Kane JM, Kreye JK, Barajas-Ramirez, Varner JM (2021) Litter trait driven dampening of flammability following deciduous forest community shifts in eastern North America. For Ecol Manage 489:119100. https://doi.org/10.1016/j.foreco.2021.119100

    Article  Google Scholar 

  • Katte J, Diaz S, Lavorel S, Prentice IC et al (2011) TRY – a global database of plant traits. Glob Chang Biol 17:2905–2935. https://doi.org/10.1111/j.1365-2486.2011.02451.x

    Article  Google Scholar 

  • Kreye JK, Varner JM, Hiers JK, Mola J (2013) Toward a mechanism for eastern north american forest meseophication: differential litter drying across 17 species. Ecol Appl 23:1976–1986

    PubMed  Google Scholar 

  • Kuznetsova A, Brockhoff PB, Christensen RHB (2017) lmerTest package: tests in linear mixed effects models. J Stat Softw 82:1–26

    Google Scholar 

  • Lamit LJ, Holeski LM, Flores-Rentería L, Whitham TG, Gehring CA (2016) Tree genotype and litter chemistry linked to ectomycorrhizal fungal communities: ecological and evolutionary implications. Fungal Ecol 24:124–134

    Google Scholar 

  • Lamit LJ, Wojtowicz T, Kovacs Z, Wooley SC, Zinkgraf M, Whitham TG, Lindroth RL, Gehring CA (2011) Hybridization among foundation tree species influences the structure of associated understory plant communities. Botany 89:165–174

    Google Scholar 

  • Lenth RV (2020) emmeans: Estimated Marginal Means, aka Least-Squares Means. R package version 1.5.3. https://CRAN.R-project.org/package=emmeans

  • LeRoy CJ, Marks JC (2006) Litter quality, stream characteristics and litter diversity influence decomposition rates and macroinvertebrates. Fresh Biol 51:605–617

    Google Scholar 

  • LeRoy CJ, Whitham TG, Wooley SC, Marks JC (2007) Within-species variation in foliar chemistry influences leaf-litter decomposition in a Utah river. J N Am Benthol Soc 26:426–438

    Google Scholar 

  • Levings SC, Windsor DM (1984) Litter moisture content as a determinant of litter arthropod distribution and abundance during the dry season on Barro Colorado Island, Panama. Biotropica 16:125–131

    Google Scholar 

  • Liu R, Navon Y, Steinberger Y, Sternberg M (2020) Effects of rainfall manipulations versus a natural aridity gradient on plant litter arthropods in desert and Mediterranean ecosystems. Appl Soil Ecol 156:103716. https://doi.org/10.1016/j.apsoil.2020.103716

    Article  Google Scholar 

  • Lojewski NR, Fischer DG, Bailey JK, Schweitzer JA, Whitham TG, Hart SC (2009) Genetic basis of aboveground productivity in two native Populus species and their hybrids. Tree Physiol 29:1133–1142

    PubMed  Google Scholar 

  • Lojewski NR, Fischer DG, Bailey JK, Schweitzer JA, Whitham TG, Hart SC (2012) Genetic components to belowground carbon fluxes in a riparian forest ecosystem: a common garden approach. New Phytol 195:631–639

    PubMed  CAS  Google Scholar 

  • Madritch MD, Hunter MD (2005) Phenotypic variation in oak litter influences short- and long-term nutrient cycling through litter chemistry. Soil Biol and Biochem 37:319–327

    CAS  Google Scholar 

  • Marcos MS, Bertiller MB, Cisneros HS, Olivera NL (2016) Nitrification and ammonia-oxidizing bacteria shift in response to soil moisture and plant litter quality in arid soils from the Patagonian Monte. Pedobiologia 59:1–10. https://doi.org/10.1016/j.pedobi.2015.11.002

    Article  Google Scholar 

  • Martinsen GD, Whitham TG, Turek RJ, Keim P (2001) Hybrid populations selectively filter gene introgression between species. Evolution 55:1325–1335

    PubMed  CAS  Google Scholar 

  • McNett BJ, Rypstra AL (2000) Habitat selection in a large orb-weaving spider: vegetational complexity determines site selection and distribution. Ecol Ent 25:423–432

    Google Scholar 

  • Moyano FE, Manzoni S, Chenu C (2013) Responses of soil heterotrophic respiration to moisture availability: an exploration of processes and models. Soil Biol Biochem 59:72–85. https://doi.org/10.1016/j.soilbio.2013.01.002

    Article  CAS  Google Scholar 

  • R Core Team (2020) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL https://www.R-project.org/

  • Rasband WS (2014) ImageJ, U. S. National Institutes of Health, Bethesda. http://imagej.nih.gov/ij/, 1997–2014

  • Reese Naesborg R, Lau MK, Michalet R, Williams CB, Whitham TG (2022) Tree genotypes affect rock lichens and understory plants: examples of trophic-independent interactions. Ecology 103:e03589. https://doi.org/10.1002/ecy.3589

  • Riechert SE (1976) Web-site selection in the desert spider Agelenopsis aperta. Oikos 27:311–315

    Google Scholar 

  • Riechert SE, Roeloffs R, Echternacht AC (1986) The ecology of the cooperative spider Agelena consociata in equatorial Africa (Araneae, Agelenidae). J Arachnol 14:175–191

    Google Scholar 

  • Rojas A (2011) Sheet-web construction by Melpomene sp. (Araneae: Agelenidae). J Arachnol 39:189–193

    Google Scholar 

  • Schweitzer JA, Bailey JK, Fischer DG, LeRoy CJ, Lonsdorf EV, Whitham TG, Hart SC (2008) Plant-soil microorganism interactions: heritable relationship between plant genotype and associated soil microorganisms. Ecology 89:773–781. https://doi.org/10.1890/07-0337.1

    Article  PubMed  Google Scholar 

  • Schweitzer JA, Bailey JK, Rehill BJ, Martinsen GD, Hart SC, Lindroth RL, Keim P, Whitham TG (2004) Genetically based trait in a dominant tree affects ecosystem processes. Ecol Lett 7:127–134

    Google Scholar 

  • Stevenson BG, Dindal DL (1982) Effect of leaf shape on forest litter Collembola: community organization and microhabitat selection of two species. J Ga Entomol Soc 17:363–369

    Google Scholar 

  • Stevenson BG, Dindal DL (1982) Effect of leaf shape on forest litter spiders: community organization and microhabitat selection of immature enoplognatha ovata (clerck) (Theridiidae). J Arachnol 10:165–178

    Google Scholar 

  • Treseder KK, Vitousek PM (2001) Potential ecosystem-level effects of genetic variation among populations of Metersideros polymorpha form a soil fertility gradient in Hawaii. Oecologia 126:266–275

    PubMed  Google Scholar 

  • Uetz GW (1975) Temporal and spatial variation in species diversity of wandering spiders (Araneae) in deciduous forest litter. Environ Entomol 4:719–724

    Google Scholar 

  • Veihmeyer FJ, Hendrickson AH (1950) Soil moisture in relation to plant growth. Annu Rev Plant Physiol 1:285–304

    Google Scholar 

  • Whitham TG, Allan GJ, Cooper HF, Shuster SM (2020) Intraspecific genetic variation and species interactions contribute to community evolution. Annu Rev Ecol Evol Syst 51:587–612. https://doi.org/10.1146/Annurev-Ecolsys-011720-123655

    Article  Google Scholar 

  • Wojtowicz T, Compson ZG, Lamit LJ, Whithm TG, Gehring CA (2014) Plant genetic identity of foundation tree species and their hybrids affect a litter-dwelling generalist predator. Oecologia 176:799–810. https://doi.org/10.1007/s00442-014-2998-3

    Article  PubMed  Google Scholar 

  • Zytynska SE, Fay MF, Penney D, Preziosi RF (2011) Genetic variation in a tropical tree species influences the associated epiphytic plant and invertebrate communities in a complex forest ecosys- tem. Philos Trans R Soc B 366:1329–1336

    Google Scholar 

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Acknowledgements

We thank the Ogden Nature Center for field housing and a site for the common garden, and we thank M. Bowker, M. Lau, P. Patterson, B. Harrop, C. Brocious, the Gehring Lab and the Cottonwood Ecology Group for input and technical assistance. D.A. Frank and three anonymous reviewers provided valuable feedback on the manuscript.

Funding

Research was supported by the following National Science Foundation funding: a Frontiers in Integrative Biological Research grant (DEB-0425908), MRI support for the Southwest Experimental Garden Array (DBI-1126840), and Integrative Graduate Education and Research Traineeships to L. J. Lamit and Z. G. Compson. Additional support was provided by Achievement Rewards for College Scientists scholarships.

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Author notes

  1. Todd Wojtowicz

    Present address: U.S. Geological Survey, Northern Rocky Mountain Science Center, Bozeman, MT, 59715, USA

Authors and Affiliations

  1. Department of Biological Sciences, Northern Arizona University, Flagstaff, AZ, 86011-5640, USA

    Todd Wojtowicz, Thomas G. Whitham & Catherine A. Gehring

  2. Department of Biology, Syracuse University, Syracuse, NY, 13244, USA

    Louis J. Lamit

  3. Department of Biological Sciences, Advanced Environmental Research Institute, University of North Texas, Denton, TX, 76203-5017, USA

    Zacchaeus G. Compson

  4. Center for Adaptable Western Landscapes, Northern Arizona University, Flagstaff, AZ, 86011, USA

    Thomas G. Whitham & Catherine A. Gehring

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  1. Todd Wojtowicz
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Contributions

TW and ZC envisioned the study and developed methods. TW, ZC and LJL conducted the fieldwork and/or data collection. LJL analyzed the data. TGW established the common garden. TGW, CAG and LJL provided input into experimental design and interpretation of results. TW, LJL and TGW wrote the manuscript with significant input from other authors.

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Correspondence to Louis J. Lamit.

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Todd Wojtowicz and Louis J. Lamit contributed equally as co-first authors on this research.

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Wojtowicz, T., Lamit, L.J., Compson, Z.G. et al. Species, hybrid and genotype effects on leaf litter curling, and their extended consequences for spiders and soil moisture dynamics. Plant Soil 492, 641–653 (2023). https://doi.org/10.1007/s11104-023-06206-0

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