Seedling maturation drives spatial variability in demographic dynamics of an invader with multiple introductions: insights from an LTRE analysis

Abstract

Multiple introductions are hypothesized to facilitate the success of invasive plant species, because they can result in novel genotypes through intraspecific hybridization potentially increasing the ability to adapt to the novel environment. In this study, we address the question of how the demography of an invader with multiple introductions and intraspecific hybridization varies across sites. This was done by modeling the population dynamics of Brazilian pepper, Schinus terebinthifolia Raddi (Anacardiaceae), a shrub native to Brazil, Paraguay and Argentina that has invaded the global subtropics and was introduced to Florida on two separate occasions. This species exhibits variability in growth form such that vertical and lateral growth are not strongly associated. Our demographic field work took place at six sites spanning the introduced range in Florida and differing in introduction history. For each site we constructed integral projection models where the probabilities of survival, growth and reproduction were modeled as functions of two different metrics of size, the continuous variables diameter and height, metrics of vertical and lateral growth, respectively. We performed a Life Table Response Experiment analysis to decompose the effects of variation among sites in vital rates on the population dynamics of S. terebinthifolia. We found that spatial variation in population dynamics was driven primarily by site-level differences in the maturation of seedlings into reproductive adults. The survival and growth of the largest individuals had the highest elasticity, suggesting that management actions capable of decreasing these vital rates would have the greatest effect on reducing the population growth rate.

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References

  1. Bates D, Maechler M (2017) Matrix: sparse and dense matrix classes and methods, R package version 1.2-1. https://CRAN.R-project.org/package=Matrix

  2. Buckley YM, Briese DT, Rees M (2003) Demography and management of the invasive plant species Hypericum perforatum II. Construction and use of an individual-based model to predict population dynamics and the effects of management strategies. J Appl Ecol 40:494–507

    Article  Google Scholar 

  3. Caswell H (2001) Matrix population models. Sinauer, Sunderland

    Google Scholar 

  4. Claridge K, Franklin SB (2002) Compensation and plasticity in an invasive plant species. Biol Invasions 4:339–347

    Article  Google Scholar 

  5. Cuda J, Ferriter A, Manrique V, Medal J (2006) Interagency Brazilian peppertree (Schinus terebinthifolius) management plan for Florida, recommendations from the Brazilian peppertree task force. Florida Exotic Pest Plant Council. Technical report, South Florida WAter Management District, West Palm Beach, FL

  6. Culley T, Hardiman NA (2009) The role of intraspecific hybridization in the evolution of invasiveness: a case study of the ornamental pear tree Pyrus calleryana. Biol Invasions 11:1107–1119

    Article  Google Scholar 

  7. Dauer J, Jongejans E (2013) Elucidating the population dynamics of Japanese Knotweed using integral projection models. PLoS ONE 8:e75181

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. DeWalt SJ (2006) Population dynamics and potential for biological control of an exotic invasive shrub in Hawaiian rainforests. Biol Invasions 8:1145–1158

    Article  Google Scholar 

  9. Easterling M, Ellner S, Dixon P (2000) Size-specific sensitivity: applying a new structured population model. Ecology 81:694–708

    Article  Google Scholar 

  10. Elderd BD, Miller TEX (2016) Quantifying demographic uncertainty: Bayesian methods for integral projection models. Ecol Monogr 86:125–144

    Google Scholar 

  11. Ellner SP, Rees M (2006) Integral projection models for species with complex demography. Am Nat 167:410–428

    PubMed  Article  Google Scholar 

  12. Erickson KD (2017) Spatiotemporal variation in frugivore assemblages and population dynamics of an invasive shrub, Schinus terebinthifolius. Ph.D. thesis, University of Miami

  13. Erickson KD, Pratt PD, Rayamajhi MB, Horvitz CC (2017) Introduction history influences aboveground biomass allocation in Brazilian Peppertree (Schinus terebinthifolius). Invasive Plant Sci Manag 10:247–253

    Article  Google Scholar 

  14. Ewel J, Ojima D, Karl D, DeBusk W (1982) Schinus in successional ecosystems of Everglades National Park. Technical report T-676, Everglades National Park, South Florida Research Center

  15. Florida Automated Weather Network (2019) https://fawn.ifas.ufl.edu/. Accessed 19 June 2019

  16. Franco M, Silvertown J (2004) A comparative demography of plants based upon elasticities of vital rates. Ecology 85:531–538

    Article  Google Scholar 

  17. Gaskin JF (2017) The role of hybridization in facilitating tree invasion. AoB Plants 9:plw079

    Google Scholar 

  18. Geiger J, Pratt P, Wheeler G, Williams D (2011) Hybrid vigor for the invasive exotic Brazilian peppertree (Schinus terebinthifolius Raddi, Anacardiaceae) in Florida. Int J Plant Sci 171:655–663

    Article  Google Scholar 

  19. Genz A, Bretz F, Miwa T, Mi X, Leisch F, Scheipl F, Hothorn T (2018) mvtnorm: multivariate normal and t distributions, r package version 1.0-8. https://CRAN.R-project.org/package=mvtnorm

  20. Goldstein EA, Butler F, Lawton C (2015) Frontier population dynamics of an invasive squirrel species: do introduced populations function differently than those in the native range? Biol Invasions 17:1181–1197

    Article  Google Scholar 

  21. Govindarajulu P, Altwegg R, Anholt BR (2005) Matrix model investigation of invasive species control: bullfrogs on Vanvouver Island. Ecol Appl 15:2161–2170

    Article  Google Scholar 

  22. Grotkopp E, Rejmanék M (2007) High seedling relative growth rate and specific leaf area are traits of invasive species: phylogenetically independent contrasts of woody angiosperms. Am J Bot 94:525–532

    Article  Google Scholar 

  23. Havens K, Jolls CL, Knight TM, Vitt P (2019) Risks and rewards: assessing the effectiveness and safety of classical invasive plant biocontrol by arthropods. Bioscience 69:247–258

    Article  Google Scholar 

  24. Horton JL, Neufeld HS (1998) Photosynthetic responses of Microstegium vimineum (Trin.) A. Camus, a shade-tolerant C\(_4\) grass, to variable light environments. Oecologia 114:11–19

    CAS  PubMed  Article  Google Scholar 

  25. Horvitz CC, Denslow JS, Johnson T, Gaoue O, Uowolo A (2018) Unexplained variability among spatial replicates in transient elasticity: implications for evolutionary ecology and management of invasive species. Popul Ecol 60:61–75

    Article  Google Scholar 

  26. Hyatt LA, Araki S (2006) Comparative population dynamics of an invading species in its native and novel ranges. Biol Invasions 8:261–275

    Article  Google Scholar 

  27. Jongejans E, Shea K, Skarpaas O, Kelly D (2008) Dispersal and demography contributions to population spread of Carduus nutans in its native and invaded ranges. J Ecol 96:687–697

    Article  Google Scholar 

  28. Jongejans E, Shea K, Skarpaas O, Kelly D, Ellner S (2011) Importance of individual and environmental variation for invasive species spread: a spatial integral projection model. Ecology 92:86–97

    PubMed  Article  Google Scholar 

  29. Kolbe JJ, Gor RE, Rodriguez Schettino L, Chamizo Lara A, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431:177–181

    CAS  PubMed  Article  Google Scholar 

  30. Koop AL, Horvitz CC (2005) Projection matrix analysis of the demography of an invasive, nonnative shrub Ardisia ellpitica. Ecology 86:2661–2672

    Article  Google Scholar 

  31. Lewis MA (2000) Spread rate for a nonlinear stochastic invasion. J Math Biol 5:430–454

    Article  Google Scholar 

  32. Morton J (1978) Brazilian pepper-its impact on people, animals and the environment. Econ Bot 32:353–359

    CAS  Article  Google Scholar 

  33. Mukherjee A, Williams D, Wheeler G, Cuda J, Pal S, Overholt W (2012) Brazilian peppertree (Schinus terebinthifolius) in Florida and South America: evidence of a possible niche shift driven by hybridization. Biol Invasions 14:1415–1430

    Article  Google Scholar 

  34. Parker IM (2000) Invasion dynamics of Cytissus scoparius: a matrix model approach. Ecol Appl 10:726–743

    Article  Google Scholar 

  35. Pergl J, Pyšek Perglová P, Dietz H (2006) Population age structure and reproductive behavior of the monocarpic perennial Heracleum mantegassianum (Apiaceae) in its native and invaded distribution ranges. Am J Bot 93:1018–1028

    PubMed  Article  Google Scholar 

  36. Pimentel D, Zuniga R, Morrison D (2005) Update on the environmental and economic costs associated with alien-invasive species in the United States. Ecol Econ 52:273–288

    Article  Google Scholar 

  37. R Core Team (2018) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria, https://www.R-project.org/

  38. Raghu S, Osunkoya O, Pichancourt J (2014) Historical demography of Lantana camara L. reveals clues about the influence of land use and weather in the management of this widespread invasive species. Basic Appl Ecol 15:565–572

    Article  Google Scholar 

  39. Rejmánek M, Richardson DM (1996) What attributes make some plant species more invasive? Ecology 77:1655–1661

    Article  Google Scholar 

  40. Spector T, Putz FE (2006) Biomechanical plasticity facilitates invasion of maritime forests in the southern USA by Brazilian pepper (Schinus terebinthifolius). Biol Invasions 8:255–260

    Article  Google Scholar 

  41. Stebbins GL (1950) The role of hybridization in evolution. Proc Am Philos Soc 103:231–251

    Google Scholar 

  42. Stevens J, Beckage B (2010) Fire effects on demography of the invasive shrub Brazilian pepper (Schinus terebinthifolius) in Florida pine savannas. Nat Areas J 30:53–63

    Article  Google Scholar 

  43. Swope SM, Satterthwaite WH (2012) Variable effects of a generalist parasitoid on a biocontrol seed predator and its target weed. Ecol Appl 2012:20–34

    Article  Google Scholar 

  44. Thomson DM (2017) Do source-sink dynamics promote the spread of an invasive grass into a novel habitat? Ecology 88:3126–3134

    Article  Google Scholar 

  45. Tobe J, Craddock Burks K, Cantrell R, Garland M, Sweeley M, Hall D, Wallace P, Anglin G, Nelson G, Cooper J, Bickner D, Gilbert K, Aymond N, Greenwood K, Raymond N (1998) Florida wetland plants: an identification manual. Florida Department of Environmental Protection, Florida

    Google Scholar 

  46. USDA NRCS Web Soil Survey (2019) https://websoilsurvey.nrcs.usda.gov. Accessed 30 July 2019

  47. van Kleef H, Jongejans E (2014) Identifying drivers of pumpkinseed invasiveness using population models. Aquat Invasions 9:315–326

    Article  Google Scholar 

  48. Williams D, Overholt W, Cuda J, Hughes C (2005) Chloroplast and microsatellite DNA diversities reveal the introduction history of Brazilian peppertree (Schinus terebinthifolius) in Florida. Mol Ecol 14:3643–3656

    CAS  PubMed  Article  Google Scholar 

  49. Williams D, Muchugu E, Overholt W, Cuda J (2007) Colonization patterns of the invasive Brazilian peppertree, Schinus terebinthifolius, in Florida. Heredity 98:284–293

    CAS  PubMed  Article  Google Scholar 

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Acknowledgements

We wish to thank L. Kasarjian for field assistance and logistical assistance in accessing the demography study plots. We would also like to thank J. Geiger, E. Mattison, J. Ledi, R. Moscat, L. Witek, K. Sealey, B. Zhang, D. Weidemann, N. Martinez, S. Baguidy, R. Little, A. Villat, D. Farag and V. Vargas for field assistance. We are also grateful for collaborators who helped facilitate site access: D. Hall of the USDA’s US Horticulture Research Laboratory in Fort Pierce, J. Aspiolea and T. Smith at Charlotte Harbor Preserve State Park, C. Stylianos of the South Florida Water Management District, H. Cooley from Everglades National Park, and C. Olson and H. Joergens from Lee County Conservation 20/20. Thanks to the National Park Service (Permits BICY-00061 and EVER-00335) and Florida Department of Environmental Protection (Permit 01211514) for permitting this project. This work was supported in part by a forEverglades Scholarship (Everglades Foundation) as well as a Kushlan award from the Department of Biology (University of Miami). K. D. Erickson was supported by funding from the James W. McLamore Fellowship (University of Miami).

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Erickson, K.D., Pratt, P.D., Rayamajhi, M.B. et al. Seedling maturation drives spatial variability in demographic dynamics of an invader with multiple introductions: insights from an LTRE analysis. Biol Invasions 22, 2185–2203 (2020). https://doi.org/10.1007/s10530-020-02249-x

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Keywords

  • Brazilian pepper
  • Integral projection models
  • Life table response experiment
  • Population dynamics
  • Schinus terebinthifolia
  • Spatial variation
  • Plasticity in growth form
  • Multiple size metrics