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Can Leaf Litter from Genetically Modified Trees Affect Aquatic Ecosystems?

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Abstract

In addition to potential benefits, biotechnology in silviculture may also be associated with environmental considerations, including effects on organisms associated with the living tree and on ecosystems and processes dependent on tree residue. We examined whether genetic modification of lignin characteristics (CAD and COMT) in Populus sp. affected leaf litter quality, the decomposition of leaf litter, and the assemblages of aquatic insects colonizing the litter in three natural streams. The decomposition of leaf litter from one of the genetically modified (GM) lines (CAD) was affected in ways that were comparable over streams and harvest dates. After 84 days in streams, CAD-litter had lost approximately 6.1% less mass than the non-GM litter. Genetic modification also affected the concentration of phenolics and carbon in the litter but this only partially explained the decomposition differences, suggesting that other factors were also involved. Insect community analyses comparing GM and non-GM litter showed no significant differences, and the two GM litters showed differences only in the 84-day litterbags. The total abundance and species richness of insects were also similar on GM and non-GM litter. The results presented here suggest that genetic modifications in trees can influence litter quality and thus have a potential to generate effects that can cross ecosystem boundaries and influence ecosystem processes not directly associated with the tree. Overall, the realized ecological effects of the GM tree varieties used here were nevertheless shown to be relatively small.

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References

  • Adler E. 1977. Lignin chemistry—past, present and future. Wood Sci Technol 11:169–218.

    Article  CAS  Google Scholar 

  • Aerts R. 1997. Climate, leaf litter chemistry and leaf litter decomposition in terrestrial ecosystems: a triangular relationship. Oikos 79:439–49.

    Article  Google Scholar 

  • Anderson MJ. 2001. A new method for non-parametric multivariate analysis of variance. Austral Ecol 26:32–46.

    Article  Google Scholar 

  • Baucher M, Chabbert B, Pilate G, VanDoorsselaere J, Tollier MT, PetitConil M, Cornu D, Monties B, VanMontagu M, Inze D, Jouanin L, Boerjan W. 1996. Red xylem and higher lignin extractability by down-regulating a cinnamyl alcohol dehydrogenase in poplar. Plant Physiol 112:1479–90.

    PubMed  CAS  Google Scholar 

  • Brodeur-Campbell SE, Vucetich JA, Richter DL, Waite TA, Rosemier JN, Tsai CJ. 2006. Insect herbivory on low-lignin transgenic aspen. Environ Entomol 35:1696–701.

    Article  CAS  Google Scholar 

  • Clarke KR. 1993. Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–43.

    Article  Google Scholar 

  • Clarke KR, Gorley RN. 2001. Primer v5: user manual/tutorial. Plymouth: Primer-E Ltd.

    Google Scholar 

  • Cummins KW, Klug MJ. 1979. Feeding ecology of stream invertebrates. Annu Rev Ecol Syst 10:147–72.

    Article  Google Scholar 

  • Cummins KW, Wilzbach MA, Gates DM, Perry JB, Taliferro WB. 1989. Shredders and riparian vegetation. Bioscience 39:24–30.

    Article  Google Scholar 

  • Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang LJ. 2002. The phenylpropanoid pathway and plant defence—a genomics perspective. Mol Plant Pathol 3:371–90.

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Field JG, Clarke KR, Warwick RM. 1982. A practical strategy for analyzing multispecies distribution patterns. Mar Ecol Prog Ser 8:37–52.

    Article  Google Scholar 

  • Findlay S, Carreiro M, Krischik V, Jones CG. 1996. Effects of damage to living plants on leaf litter quality. Ecol Appl 6:269–75.

    Article  Google Scholar 

  • Giller PS, Malmqvist B. 1998. The biology of streams and rivers. Oxford: Oxford University Press.

    Google Scholar 

  • Griffiths NA, Tank JL, Royer TV, Rosi-Marshall EJ, Whiles MR, Chambers CP, Frauendorf TC, Evans-White MA. 2009. Rapid decomposition of maize detritus in agricultural headwater streams. Ecol Appl 19:133–42.

    Article  PubMed  Google Scholar 

  • Haapala A, Muotka T, Markkola A. 2001. Breakdown and macroinvertebrate and fungal colonization of alder, birch, and willow leaves in a boreal forest stream. J N Am Benthol Soc 20:395–407.

    Article  Google Scholar 

  • Halpin C, Thain SC, Tilston EL, Guiney E, Lapierre C, Hopkins DW. 2007. Ecological impacts of trees with modified lignin. Tree Genet Genomes 3:101–10.

    Article  Google Scholar 

  • Hattenschwiler S, Tiunov AV, Scheu S. 2005. Biodiversity and litter decomposition interrestrial ecosystems. Annu Rev Ecol Evol Syst 36:191–218.

    Article  Google Scholar 

  • Hjältén J, Lindau A, Wennström A, Blomberg P, Witzell J, Hurry V, Ericson L. 2007. Unintentional changes of defence traits in GM trees can influence plant–herbivore interactions. Basic Appl Ecol 8:434–43.

    Article  Google Scholar 

  • Hoenicka H, Fladung M. 2006. Biosafety in Populus spp and other forest trees: from non-native species to taxa derived from traditional breeding and genetic engineering. Trees Struct Funct 20:131–44.

    Google Scholar 

  • Julkunen-Tiitto R, Sorsa S. 2001. Testing the effects of drying methods on willow flavonoids, tannins, and salicylates. J Chem Ecol 27:779–89.

    Article  PubMed  CAS  Google Scholar 

  • Kominoski JS, Pringle CM, Ball BA, Bradford MA, Coleman DC, Hall DB, Hunter MD. 2007. Nonadditive effects of leaf litter species diversity on breakdown dynamics in a detritus-based stream. Ecology 88:1167–76.

    Article  PubMed  CAS  Google Scholar 

  • Lapierre C, Pollet B, Petit-Conil M, Toval G, Romero J, Pilate G, Leple JC, Boerjan W, Ferret V, De Nadai V, Jouanin L. 1999. Structural alterations of lignins in transgenic poplars with depressed cinnamyl alcohol dehydrogenase or caffeic acid O-methyltransferase activity have an opposite impact on the efficiency of industrial kraft pulping. Plant Physiol 119:153–63.

    Article  PubMed  CAS  Google Scholar 

  • Lecerf A, Chauvet E. 2008. Intraspecific variability in leaf traits strongly affects alder leaf decomposition in a stream. Basic Appl Ecol 9:598–605.

    Article  Google Scholar 

  • Lecerf A, Risnoveanu G, Popescu C, Gessner MO, Chauvet E. 2007. Decomposition of diverse litter mixtures in streams. Ecology 88:219–27.

    Article  PubMed  Google Scholar 

  • LeRoy CJ, Marks JC. 2006. Litter quality, stream characteristics and litter diversity influence decomposition rates and macroinvertebrates. Freshw Biol 51:605–17.

    Article  Google Scholar 

  • LeRoy CJ, Whitham TG, Keim P, Marks JC. 2006. Plant genes link forests and streams. Ecology 87:255–61.

    Article  PubMed  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 26:426–38.

    Article  Google Scholar 

  • Lewis NG, Yamamoto E. 1990. Lignin—occurence, biogenesis and biodegradation. Annu Rev Plant Physiol Plant Mol Biol 41:455–96.

    Article  PubMed  CAS  Google Scholar 

  • Madritch M, Donaldson JR, Lindroth RL. 2006. Genetic identity of Populus tremuloides litter influences decomposition and nutrient release in a mixed forest stand. Ecosystems 9:528–37.

    Article  CAS  Google Scholar 

  • Mathews JH, Campbell MM. 2000. The advantages and disadvantages of the application of genetic engineering to forest trees: a discussion. Forestry 73:371–80.

    Article  Google Scholar 

  • McArdle BH, Anderson MJ. 2001. Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82:290–7.

    Article  Google Scholar 

  • Melillo JM, Aber JF, Muratore JF. 1982. Nitrogen and lignin control of hardwood leaf litter decomposition dynamics. Ecology 63:621–6.

    Article  CAS  Google Scholar 

  • Mulder C, Lotz LAP. 2009. Biotechnology, environmental forcing, and unintended trophic cascades. Arthropod Plant Interact 3:131–9.

    Article  Google Scholar 

  • Ostrofsky ML. 1997. Relationship between chemical characteristics of autumn-shed leaves and aquatic processing rates. J N Am Benthol Soc 16:750–9.

    Article  Google Scholar 

  • Peters DJ, Constabel CP. 2002. Molecular analysis of herbivore-induced condensed tannin synthesis: cloning and expression of dihydroflavonol reductase from trembling aspen (Populus tremuloides). Plant J 32:701–12.

    Article  PubMed  CAS  Google Scholar 

  • Pilate G, Guiney E, Holt K, Petit-Conil M, Lapierre C, Leple JC, Pollet B, Mila I, Webster EA, Marstorp HG, Hopkins DW, Jouanin L, Boerjan W, Schuch W, Cornu D, Halpin C. 2002. Field and pulping performances of transgenic trees with altered lignification. Nat Biotechnol 20:607–12.

    Article  PubMed  CAS  Google Scholar 

  • Rosi-Marshall EJ, Tank JL, Royer TV, Whiles MR, Evans-White M, Chambers C, Griffiths NA, Pokelsek J, Stephen ML. 2007. Toxins in transgenic crop byproducts may affect headwater stream ecosystems. Proc Natl Acad Sci USA 104:16204–8.

    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 7:127–34.

    Article  Google Scholar 

  • Snow AA, Andow DA, Gepts P, Hallerman EM, Power A, Tiedje JM, Wolfenbarger LL. 2005. Genetically engineered organisms and the environment: current status and recommendations. Ecol Appl 15:377–404.

    Article  Google Scholar 

  • Swan CM, Palmer MA. 2004. Leaf diversity alters litter breakdown in a Piedmont stream. J N Am Benthol Soc 23:15–28.

    Article  Google Scholar 

  • Tilston EL, Halpin C, Hopkins DW. 2004. Genetic modifications to lignin biosynthesis in field-grown poplar trees have inconsistent effects on the rate of woody trunk decomposition. Soil Biol Biochem 36:1903–6.

    Article  CAS  Google Scholar 

  • van Frankenhuyzen KU, Beardmore T. 2004. Current status and environmental impact of transgenic forest trees. Can J For Res 34:1163–80.

    Article  Google Scholar 

  • Vannote RL, Minshall GW, Cummins KW, Sedell JR, Cushing CE. 1980. The river continuum concept. Can J Fish Aquat Sci 37:130–7.

    Article  Google Scholar 

  • Wallace JB, Eggert SL, Meyer JL, Webster JR. 1997. Multiple trophic levels of a forest stream linked to terrestrial litter inputs. Science 277:102–4.

    Article  CAS  Google Scholar 

  • Wang J, Ives NE, Lechowicz MJ. 1992. The relation of foliar phenology to xylem embolism in trees. Funct Ecol 6:469–75.

    Article  Google Scholar 

  • Waterman PG, Mole S. 1994. Analysis of phenolic plant metabolites. Oxford: Blackwell Scientific Publications.

    Google Scholar 

  • Yoshinaga A, Fujita M, Saiki H. 1997. Cellular distribution of guaiacyl and syringyl lignins within an annual ring in oak wood. J Jpn Wood Res Soc 43:384–90.

    CAS  Google Scholar 

Download references

Acknowledgement

This study was supported by FORMAS (grant to J. Hjältén). We are also grateful of Magnus Lindberg for skilled insect identification and of two anonymous reviewers for insightful comments on a previous version of the manuscript.

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Correspondence to E. Petter Axelsson.

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PA, JH, AW and CL designed the study. PA, JH performed the research and analyzed the data. RJT performed chemical analyses and GP provided the plant material. All authors contributed significantly to the interpretation of the data and writing of the paper.

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Axelsson, E.P., Hjältén, J., LeRoy, C.J. et al. Can Leaf Litter from Genetically Modified Trees Affect Aquatic Ecosystems?. Ecosystems 13, 1049–1059 (2010). https://doi.org/10.1007/s10021-010-9373-y

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  • DOI: https://doi.org/10.1007/s10021-010-9373-y

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