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Annals of Forest Science

, 75:77 | Cite as

Beneath the mistletoe: parasitized trees host a more diverse herbaceous vegetation and are more visited by rabbits

  • José A. Hódar
  • Alba Lázaro-González
  • Regino Zamora
Research Paper

Abstract

• Key message

Parasitism by mistletoe increases the cover and diversity of herbaceous vegetation under the host tree and attracts the activity of rabbits in comparison to control trees. Thus, the effects on forest community go beyond the parasitized tree.

• Context

Mistletoes are a diverse group of aerial hemiparasitic plants and are considered keystone species in forest ecosystems around the world. They produce nutrient-enriched litter, which exerts a substantial effect on soil-nutrient concentration, and the enriched nutrient patch alters the vegetation at the site as well as the associated fauna.

• Aims

Our goal is to ascertain whether mistletoe (Viscum album) parasitism of pine forest of a Mediterranean mountain favors herbaceous vegetation and attracts mammalian herbivores.

• Methods

We recorded in Sierra de Baza (SE Spain) the composition of the herbaceous vegetation under pines with and without mistletoe parasitism, and estimated the rabbit activity at the same sites by collecting their excrements.

• Results

An effect on herbaceous vegetation, especially in grasses belonging to the family Poaceae, was reflected in a notable increase in soil cover, species richness, and species diversity beneath parasitized pines with respect to unparasitized ones. As a consequence, parasitized pines attract the activity of rabbits, as shown by a fivefold quantity of excrement with respect to control ones.

• Conclusion

Parasitism by mistletoe, by creating patches of greater nutrient availability under the host canopy, extends its effects beyond the host tree to other members of the forest community, such as herbaceous plants and associated herbivorous animals, which in turn contribute to environmental heterogeneity with their activity.

Keywords

Fertility island Herbaceous plant diversity Herbivore occupancy Mistletoe litterfall Nutrient concentration Pine woodlands Poaceae Rabbit 

Notes

Acknowledgments

The Andalusian Environmental Council, Junta de Andalucía, and the Direction of the Sierra de Baza Natural Park provided permission for field work. Ramón Ruiz-Puche helped us while field sampling and lab sample processing. David Nesbitt looked over the English version of the manuscript. Two anonymous referees greatly contributed to improve an early version of this manuscript.

Funding

The study was supported by project CLAVINOVA CGL2011-29910 from the Spanish Ministry of Science and Innovation (MICINN) and FPI predoctoral grant from MCYT to ALG.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Supplementary material

13595_2018_761_MOESM1_ESM.docx (33 kb)
ESM 1 (DOCX 32 kb)

References

  1. Archibold OW (1995) Ecology of world vegetation. Chapman & Hall, LondonCrossRefGoogle Scholar
  2. Blanca G, Morales C (1991) Flora del Parque Natural de la Sierra de Baza. Universidad de Granada, GranadaGoogle Scholar
  3. Blanca G, Cabezudo B, Cueto M, Salazar C, Morales-Torres C (eds) (2011) Flora vascular de andalucía oriental. Universidades de Almería, GranadaGoogle Scholar
  4. Bokdam J (2001) Effects of browsing and grazing on cyclic succession in nutrient-limited ecosystems. J Veg Sci 12:875–886CrossRefGoogle Scholar
  5. Bowie M, Ward D (2004) Water and nutrient status of the mistletoe Plicosepalus acaciae parasitic on isolated Negev Desert populations of Acacia raddiana differing in level of mortality. J Arid Environ 56:487–508CrossRefGoogle Scholar
  6. Braun-Blanquet J (1979) Fitosociología: bases para el estudio de las comunidades vegetales. Blume, MadridGoogle Scholar
  7. Bremer LL, Farley KA (2010) Does plantation forestry restore biodiversity or create green deserts? A synthesis of the effects of land-use transitions on plant species richness. Biodivers Conserv 19:3893–3915CrossRefGoogle Scholar
  8. Chirino E, Bonet A, Bellot J, Sánchez JR (2006) Effects of 30-year-old Aleppo pine plantations on runoff, soil erosion, and plant diversity in a semi-arid landscape in south eastern Spain. Catena 65:19–29CrossRefGoogle Scholar
  9. CMAOT, Consejería de Medio Ambiente y Ordenación del Territorio (2016) Memoria de actividades cinegéticas de la temporada 2015–2016. Instituto Andaluz de Caza y Pesca Continental, AndalucíaGoogle Scholar
  10. Dellafiore CM, Gallego-Fernández JB, Muñoz-Vallés S (2010) The rabbit (Oryctolagus cuniculus) as a seed disperser in a coastal dune system. Plant Ecol 206:251–261CrossRefGoogle Scholar
  11. Ehleringer JR, Marshall JD (1995) Water relations. In: Press MC, Graves JD (eds) Parasitic plants. Chapman and Hall, London, pp 125–140Google Scholar
  12. Ferreira LMM, Celaya R, Benavides R, Jáuregui BM, García U, Santos AS, García RR, Rodrigues MAM, Osoro K (2013) Foraging behaviour of domestic herbivore species grazing on heathlands associated with improved pasture areas. Livest Sci 155:373–383CrossRefGoogle Scholar
  13. Fisher JP, Phoenix GK, Childs DZ, Press MC, Smith SW, Pilkington MG, Cameron DD (2013) Parasitic plant litter input: a novel indirect mechanism influencing plant community structure. New Phytol 198:222–231CrossRefPubMedGoogle Scholar
  14. Garin I, Aldezábal A, García-González R, Aihartza JR (2001) Composición y calidad de la dieta del ciervo (Cervus elaphus L.) en el norte de la península ibérica. Anim Biodivers Conserv 24:53–63Google Scholar
  15. Gómez-Aparicio L, Zavala MA, Bonet FJ, Zamora R (2009) Are pine plantations valid tools for restoring Mediterranean forests? An assessment along abiotic and biotic gradients. Ecol Appl 19:2124–2141CrossRefPubMedGoogle Scholar
  16. González-González G, González-Doncel I (1999) Algunos residuos forestales y madereros en la alimentación del ganado. Invest Agrar-Sist R Sist R 1:349–373Google Scholar
  17. Grünzweig JM, Körner C (2003) Differential phosphorus and nitrogen effects drive species and community responses to elevated CO2 in semi-arid grassland. Funct Ecol 17:766–777CrossRefGoogle Scholar
  18. Herrero A, Rigling A, Zamora R (2013) Varying climate sensitivity at the dry distribution edge of Pinus sylvestris and P. nigra. For Ecol Manag 308:50–61CrossRefGoogle Scholar
  19. Hódar JA, Palo RT (1997) Feeding by vertebrate herbivores in a chemically heterogeneous environment. Écoscience 4:304–310CrossRefGoogle Scholar
  20. Hódar JA, Lázaro-González A, Zamora R (2018) Beneath the mistletoe: parasitized trees host a more diverse herbaceous vegetation and are more visited by rabbits (Version v1) [Dataset]. Zenodo.  https://doi.org/10.5281/zenodo.1311757
  21. Huang W, Zhou G, Deng X, Liu J, Duan H, Zhang D, Chu G, Liu S (2015) Nitrogen and phosphorus productivities of five subtropical tree species in response to elevated CO2 and N addition. Eur J For Res 134:845–856CrossRefGoogle Scholar
  22. Iason GR, Lennon JJ, Pakeman RJ, Thoss V, Beaton JK, Sim DA, Elston DA (2005) Does chemical composition of individual Scots pine trees determine the biodiversity of their associated ground vegetation? Ecol Lett 8:364–369CrossRefGoogle Scholar
  23. Jones CG, Lawton JH, Shachak M (1994) Organisms as ecosystem engineers. Oikos 69:373–386CrossRefGoogle Scholar
  24. Kontsiotis VJ, Bakaloudis DE, Merou T, Xofis P (2015) Trophic ecology of the European wild rabbit Oryctolagus cuniculus on the Mediterranean island of Lemnos, Greece. Ecol Res 30:683–691CrossRefGoogle Scholar
  25. Lombardi L, Fernández N, Moreno S, Villafuerte R (2003) Habitat-related differences in rabbit (Oryctolagus cuniculus) abundance, distribution, and activity. J Mammal 84:26–36CrossRefGoogle Scholar
  26. Lombardi L, Fernández N, Moreno S (2007) Habitat use and spatial behaviour in the European rabbit in three Mediterranean environments. Basic Appl Ecol 8:453–463CrossRefGoogle Scholar
  27. Malo JE, Suárez F (1995) Herbivorous mammals as seed dispersers in a Mediterranean dehesa. Oecologia 104:246–255CrossRefPubMedGoogle Scholar
  28. March WA, Watson DM (2007) Parasites boost productivity: effects of mistletoe on litterfall dynamics in a temperate Australian forest. Oecologia 154:339–347CrossRefPubMedGoogle Scholar
  29. March WA, Watson DM (2010) The contribution of mistletoes to nutrient returns: evidence for a critical role in nutrient cycling. Austral Ecol 35:713–721CrossRefGoogle Scholar
  30. Martínez T (2009) Role of various woody species in Spanish Mediterranean forest and scrubland as food resources for Spanish ibex (Capra pyrenaica Schinz) and Red Deer (Cervus elaphus L.). In: Rigueiro-Rodríguez A, McAdam J, Mosquera-Losa MR (eds) Agroforestry in Europe. Current status and future prospects. Springer, New York, pp 233–254Google Scholar
  31. Martins H, Milne JA, Rego F (2002) Seasonal and spatial variation in the diet of the wild rabbit (Oryctolagus cuniculus L.) in Portugal. J Zool 258:395–404CrossRefGoogle Scholar
  32. Mellado A (2016) Ecological interactions mediated by the European mistletoe, Viscum album subsp. austriacum, in Mediterranean forests—an integrated perspective. PhD thesis, University of Granada, GranadaGoogle Scholar
  33. Mellado A, Zamora R (2015) Spatial heterogeneity of a parasitic plant drives the seed-dispersal pattern of a zoochorous plant community in a generalist dispersal system. Funct Ecol 30:459–467CrossRefGoogle Scholar
  34. Mellado A, Morillas L, Gallardo A, Zamora R (2016) Temporal dynamic of parasite-mediated linkages between the forest canopy and soil processes and the microbial community. New Phytol 211:1382–1392CrossRefPubMedGoogle Scholar
  35. Moro MJ, Pugnaire FI, Haase P, Puigdefábregas J (1997) Effect of the canopy of Retama sphaerocarpa on its understorey in a semiarid environment. Funct Ecol 11:425–431CrossRefGoogle Scholar
  36. Mutze G, Cooke B, Lethbridge M, Jennings S (2014) A rapid survey method for estimating population density of European rabbits living in native vegetation. Rangel J 36:239–247CrossRefGoogle Scholar
  37. Muvengwi J, Ndagurwa HG, Nyenda T (2015) Enhanced soil nutrient concentrations beneath-canopy of savanna trees infected by mistletoes in a southern African savanna. J Arid Environ 116:25–28CrossRefGoogle Scholar
  38. Ndagurwa HGT, Ndarevani P, Muvengwi J, Maponga TS (2016) Mistletoes via input of nutrient-rich litter increases nutrient supply and enhance plant species composition and growth in a semi-arid savanna, Southwest Zimbabwe. Plant Ecol 217:1095–1104CrossRefGoogle Scholar
  39. Pate JS, True KC, Kuo J (1991) Partitioning of dry-matter and mineral nutrients during a reproductive cycle of the mistletoe Amyema linophyllum (Fenzl.) Tieghem parasitizing Casuarina obesa Miq. J Exp Bot 42:427–439CrossRefGoogle Scholar
  40. Pickett STA, Cadenasso ML, Jones CG (2000) Generation of heterogeneity by organisms: creation, maintenance and transformation. In: Hutchings MJ, John EA, Stewart AJA (eds) The ecological consequences of environmental heterogeneity. British Ecological Society-Blackwell, Oxford, pp 33–52Google Scholar
  41. Quested HM, Press MC, Callaghan TV, Cornelissen JHC (2002) The hemiparasitic angiosperm Bartsia alpina has the potential to accelerate decomposition in sub-arctic communities. Oecologia 130:88–95CrossRefPubMedGoogle Scholar
  42. Quested HM, Press MC, Callaghan TV (2003) Litter of the hemiparasite Bartsia alpina enhances plant growth: evidence for a functional role in nutrient cycling. Oecologia 135:606–614CrossRefPubMedGoogle Scholar
  43. R Development Core Team (2017) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. URL http://www.R-project.org/ Google Scholar
  44. Rodrigáñez C (1949) Prados arbóreos. Publicaciones del Ministerio de Agricultura, Servicio de Capacitación y Propaganda, n° 3. Madrid, 190 ppGoogle Scholar
  45. Santilli F, Bagliacca M (2010) Habitat use by the European wild rabbit (Oryctolagus cuniculus) in a coastal sandy dune ecosystem of Central Italy. Hystrix 21:57–64Google Scholar
  46. Schaefer JA, Morellet N, Pépin D, Verheyden H (2008) The spatial scale of habitat selection by red deer. Can J Zool 86:1337–1345CrossRefGoogle Scholar
  47. Senft RL, Coughenour MB, Bailey DW, Rittenhouse LR, Sala OE, Swift DM (1987) Large herbivore foraging and ecological hierarchies. Bioscience 37:789–799CrossRefGoogle Scholar
  48. Somers N, D’Haese B, Bossuyt B, Lens L, Hoffmann M (2008) Food quality affects diet preference of rabbits: experimental evidence. Belg J Zool 138:170–176Google Scholar
  49. Soriguer RC (1981) Biología y dinámica de una población de conejos (Oryctolagus cuniculus L.) en Andalucía Occidental. Doñana Acta Vertebr 8:1–379Google Scholar
  50. Soriguer RC (1988) Alimentación del conejo (Oryctolagus cuniculus L. 1758) en Doñana, SO. España. Doñana Acta Vertebr 15:141–150Google Scholar
  51. Stewart AJA, John EA, Hutchings MJ (2000) The world is heterogeneous: ecological consequences of living in a patchy environment. In: Hutchings MJ, John EA, Stewart AJA (eds) The ecological consequences of environmental heterogeneity. British Ecological Society-Blackwell, Oxford, pp 1–8Google Scholar
  52. Stöcklin J, Körner C (1999) Interactive effects of elevated CO2, P availability and legume presence on calcareous grassland: results of a glasshouse experiment. Funct Ecol 13:200–209CrossRefGoogle Scholar
  53. Stöcklin J, Schweizer K, Körner C (1998) Effects of elevated CO2 and phosphorus addition on productivity and community composition of intact monoliths from calcareous grassland. Oecologia 116:50–56CrossRefPubMedGoogle Scholar
  54. Suding KN, Collins SL, Gough L, Clark C, Cleland EE, Gross KL, Milchunas DG, Pennings S (2005) Functional-and abundance-based mechanisms explain diversity loss due to N fertilization. Proc Natl Acad Sci U S A 102:4387–4392CrossRefPubMedPubMedCentralGoogle Scholar
  55. Van der Wal R, Bardgett RD, Harrison KA, Stien A (2004) Vertebrate herbivores and ecosystem control: cascading effects of faeces on tundra ecosystems. Ecography 27:242–252CrossRefGoogle Scholar
  56. Watson DM (2001) Mistletoe—a keystone resource in forests and woodlands worldwide. Annu Rev Ecol Evol Syst 32:219–249CrossRefGoogle Scholar
  57. Watson DM (2009) Parasitic plants as facilitators: more dryad than Dracula? J Ecol 97:1151–1159CrossRefGoogle Scholar
  58. Watson DM (2015) Disproportionate declines in ground-foraging insectiorous birds after mistletoe removal. PLoS One 10:e0142992CrossRefPubMedPubMedCentralGoogle Scholar
  59. Wiens JA (2000) Ecological heterogeneity: an ontogeny of concepts and approaches. In: Hutchings MJ, John EA, Stewart AJA (eds) The ecological consequences of environmental heterogeneity. British Ecological Society-Blackwell, Oxford, pp 9–31Google Scholar
  60. Willott SJ, Miller AJ, Incoll LD, Compton SG (2000) The contribution of rabbits (Oryctolagus cuniculus L.) to soil fertility in semi-arid Spain. Biol Fertil Soils 31:379–384CrossRefGoogle Scholar
  61. Xia J, Wan S (2008) Global response patterns of terrestrial plant species to nitrogen addition. New Phytol 179:428–439CrossRefPubMedGoogle Scholar
  62. Zuber D (2004) Biological flora of Central Europe: Viscum album L. Flora 199:181–203CrossRefGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Grupo de Ecología Terrestre, Departamento de Ecología, Facultad de CienciasUniversidad de GranadaGranadaSpain

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