Contrasting arthropod communities associated with dwarf mistletoes Arceuthobium globosum and A. vaginatum and their host Pinus hartwegii

Abstract

Arthropod communities and epiphytic plants associated with tree canopies have been widely studied and have revealed a great diversity of organisms; however, the community hosted by parasitic plants, such as dwarf mistletoes, remains poorly known. In the coniferous forests of North America, dwarf mistletoe infection (Arceuthobium spp.) significantly damages the health of the forest, causing large financial losses for the forest industry, but it also positively affects diversity, especially of mammals and birds. This study examined the attributes of the arthropod communities associated with two species of dwarf mistletoe [Arceuthobium globosum Hawksw. & Wiens and A. vaginatum (Humb. & Bonpl. ex Willd.) J. Presl] and their host Pinus hartwegii Lindl. In 2010, in five sites located in Zoquiapan (Central Mexico), we collected plant tissue from the three species bimonthly. Arthropods were separated from the plant tissue and identified to the finest level possible. We collected 32,059 individuals, for which 51 morphospecies were identified, belonging to 15 taxonomic orders; the most abundant orders for the three plants were Prostigmata, Thysanoptera and Homoptera. The community associated with P. hartwegii had the highest value of diversity (H′ = 1.47; A. globosum, H′ = 0.64; A. vaginatum, H′ = 0.68) and species richness (S = 40; A. globosum, S = 30; A. vaginatum, S = 35); while abundance was significantly higher for the mistletoes (A. globosum, n = 407 individuals/sample; A. vaginatum, n = 536 individuals/sample; P. hartwegii, n = 134 individuals/sample). Species richness, abundance and diversity were significantly different for the three studied plants, as well for sampling month and the interaction of these two factors (except for diversity). The results suggest that the canopy of P. hartwegii is an important element in the ecosystem, providing a mosaic of resources and conditions to the associated fauna. We also propose that mistletoes are key species within the forest canopy, as they greatly influence the establishment of diverse organisms, particularly arthropods.

Keywords

Arceuthobium spp. / Pinus hartwegii / Arthropod community / Thrips / Mites / Hemiparasitic plants

References

[1] Agren J, Danell K, Elmqvist T, Ericson L, Hjältén J. Geber MA, Dawson TE, Delph LF. Sexual domorphism and biotic interactions. Gender and sexual dimorphism in flowering plants, 1999, New York: Springer 217 246

[2] Anderson SJ, Braby MF. Invertebrate diversity associated with tropical mistletoe in a suburban landscape from northern Australia. North Territ Nat, 2009, 21: 2-23.

[3] Arriaga L, Espinoza JM, Aguilar C, Martínez E, Gómez L, Loa E. Regiones terrestres prioritarias de México, 2002, Mexico City: Comisión Nacional para el Conocimiento y Uso de la Biodiversidad.

[4] Basset Y. Local communities of arboreal herbivores in Papua New Guinea predictors of insect variables. Ecology, 1996, 77: 1906-1919.

[5] Basset Y, Arthington J. The arthropod community of an Australian rainforest tree: abundance of component taxa. Aust J Ecol, 1992, 17: 89-98.

[6] Borror DJ, Johnson NF, Triplehorn CA. An introduction to the study of insects, 1989, Philadelphia: Saunders College.

[7] Burns AE, Cunningham SA, Watson DM. Arthropod assemblages in tree canopies: a comparison of orders on box mistletoe (Amyema miquelii) and its host eucalypts. Aust J Entomol, 2011, 50: 221-230.

[8] Castaño-Meneses G, Palacios-Vargas JL, Cutz-Pool L. Feeding habits of Collembola and their ecological niche. Anales del Instituto de Biología, Serie Zoología, 2004, 75: 135-142.

[9] Connor EF, McCoy E. The statistics and biology of the species-area relationship. Am Nat, 1979, 113: 791-833.

[10] de Rzedowski GC, Rzedowski J, and contributors (2001) Flora fanerogámica del Valle de México. Instituto de Ecología, A. C. and Comisión Nacional para el Conocimiento y Uso de la Biodiversidad. Pátzcuaro

[11] Fitzjarrald DR, Moore KE. Lowman MD, Nadkarni NM. Physical mechanism of heat and mass exchange between forest and the atmosphere. Forest canopies, 1995, San Diego: Academic Press 45 72

[12] Goulet H, Huber J. Hymenoptera of the world: an identification guide to families, 1993, Ontario: Research Branch Agriculture.

[13] Grimble DG, Beckworth RC. Temporal changes inpresence of late instar Mitoura spinetorum (Lycaenidae) in eastern Oregon. J Lepid Soc, 1993, 47: 329-330.

[14] Hawksworth FG. Calder M, Bernhardt P. Mistletoes as forest parasites. The biology of mistletoes, 1983, New York: Academic Press 320 329

[15] Hawksworth FG, Wiens D. Dwarf mistletoes: biology, pathology and systematics. Agriculture Handbook 709, 1996, Washington, DC: U.S.D.A. Forest Service.

[16] Hawksworth FG, Wiens D, Geils BW. Geils BW, Cibrián-Tovar J, Moody B. Arceuthobium in North America. Mistletoes of North American conifers, 2002, Ogden: U.S.D.A. Forest Service 29 56

[17] Keifer HH (1952) Eriophyid studies. XIX. Bulletin 41. State of California, Department of Agriculture, Sacramento, CA, pp 65–74

[18] Kennett CE. Some species of Typhlodromus from dwarf mistletoes in North America (Acarina-Phytoseidae). Pan Pac Entomol, 1963, 39: 247-252.

[19] Krebs CJ. Ecological methodology, 1999, Menlo Park: Addison-Wesley Educational Publication.

[20] Kuijt J. Dwarf mistletoes. Bot Rev, 1955, 10: 569-619.

[21] Langellotto GA, Denno RF. Responses of invertebrate natural enemies to complex-structures habitats: a meta-analytical synthesis. Oecologia, 2004, 139: 1-10.

[22] Larsen EM, Rodrick E, Milner R. Management recommendations for Washington’s priority species, vol 1: invertebrates, 1995, Olympia: Washington Department of Fish and Wildlife.

[23] Lawton JH. Plant architecture and the diversity of phytophagous insects. Annu Rev Entomol, 1983, 28: 23-39.

[24] Legendre L, Legendre P. Numerical ecology, 1998, Amsterdam: Elsevier.

[25] Letourneau DK, Dyer LA. Density patterns of Piper ant-plants and associated arthropods: top-predator trophic cascades in a terrestrial system. Biotropica, 1998, 30: 162-169.

[26] Lomolino MV. Ecology´s most general, yet protean pattern: the species-area realationship. J Biogeogr, 2000, 27: 17-26.

[27] López-Gómez V, Cano-Santana Z. Best host-plant attribute for species-area relationship, and effects of the shade, conspecific distance and plant phenophase in an arthropod community within the grass Muhlenbergia robusta. Entomol Sci, 2010, 13: 174-182.

[28] Maraun M, Scheu S. The structure of oribatid mite communities (Acari, Oribatida): patterns, mechanisms and implications for future research. Ecography, 2000, 23: 374-383.

[29] March WA, Watson D. Parasites boost productivity: effects of mistletoe on litterfall dynamics in a temperate Australian forest. Oecologia, 2007, 154: 339-347.

[30] Mathiasen RL, Nickrent DL, Shaw DC, Watson DM. Mistletoes. Pathology, systematic, ecology and management. Plant Dis, 2008, 92: 988-1006.

[31] Mittelbach GG, Steiner CF, Scheiner SM, Gross KL, Reynolds HL, Waide RB, Willig MR, Dodson SI, Gough L. What is the observed relationship between species richness and productivity?. Ecology, 2001, 82: 2381-2396.

[32] Mooney KA. The life history of Dasypyga alternosquamella Ragonot (Pyralidae) feeding on the Southwestern dwarf mistletoe (Arceuthobium vaginatum) in Colorado. J Lepid Soc, 2001, 55: 140-143.

[33] Moran VC, Southwood TRE. The guild composition of arthropods communities in trees. J Anim Ecol, 1982, 51: 289-306.

[34] Morecroft MT, Taylor P, Oliver HR. Air and soil microclimates of deciduous woodland compared to an open. Agric For Meteorol, 1985, 90: 141-156.

[35] Morse JG, Hoddle MS. Invasion biology thrips. Annu Rev Entomol, 2006, 51: 67-89.

[36] Ndagurwa GT, Dube JS, Mlambo D. The influence of mistletoes on nutrient cycling in a semi-arid savanna, southwest Zimbabwe. Plant Ecol, 2014, 215: 15-26.

[37] Obieta C, Sarukhán J. Estructura y composición la vegetación herbácea de un bosque uniespecífico de Pinus hartwegii. I. Estructura y composicion florística. Boletín de la Sociedad Botánica de México, 1981, 41: 75-125.

[38] Penfield FB, Stevens RE, Hawksworth FG. Pollination ecology of three Rocky Mountain dwarf mistletoe. For Sci, 1976, 22: 473-484.

[39] Polis GA, Anderson WB, Holt RD. Toward an integration of landscape and food web ecology: the dynamics of spatially subsidized food webs. Annu Rev Ecol Syst, 1997, 28: 289-316.

[40] Post DM, Conners ME, Goldberg DS. Prey preference by a top predator and the stability of linked food chains. Ecology, 2000, 81: 8-14.

[41] Power ME, Tilman D, Estes JA, Menge B, Bond W, Mills LS, Daily G, Castilla JC, Lubchenco J, Paine RT. Challenges in the quest for keystones. Bioscience, 1996, 46: 609-620.

[42] Prinzing A. Stork N, Adis J, Didham R. Spatial and temporal use of microhabitats as a key strategy for the colonization of tree bark by Entomobrya nivalis L. (Collembola, Entomobryidae). Canopy arthropods, 1997, London: Chapman and Hall 453 476

[43] Pritchard AE, Baker EW. The false spider mites (Acarina: Tenuipalpidae). University of California Publications in Entomology, Berkely, 1958, 14: 207-208.

[44] Queijeiro-Bolaños M, Cano-Santana Z, García-Guzmán G. Incidence, severity and aggregation patterns of two sympatric dwarf mistletoe species (Arceuthobium spp.) in Central Mexico. Eur J Forest Res, 2014, 113: 297-306.

[45] R Core Development Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 01 May 2016

[46] Room PM. The constitution and natural history of the fauna of the mistletoe Tapinanthus bangwensis (Engl. & K. Krause) growing on cocoa in Ghana. J Anim Ecol, 1972, 41: 519-535.

[47] Samways MJ. Insect conservation biology, 1994, London: Chapman and Hall.

[48] Schoener TW. Species area relationship within archipelagoes: model and evidence from island birds. Proc XVl Int Ornithol Congr, 1976, 6: 629-642.

[49] Schoener TW. Food webs from the small to the large: the Robert H. MacArthur Award Lecture. Ecology, 1989, 70: 1559-1589.

[50] Schoonhoven LM, van Loon JJA, Dicke M. Insect-plant biology, 2005, New York: Oxford University.

[51] Schowalter TD. Insect ecology. An ecosystem approach, 2011, Amsterdam: Elsevier Academic Press.

[52] SMN, Servicio Meteorológico Nacional (2013) Normales climatológicas de México. http://smn.cna.gob.mx/. Accessed 01 June 2013

[53] Shaw D. Lowman MD, Rinker HB. Vertical organization of canopy biota. Forest canopies, 2004, Amsterdam: Elsevier Academic Press 73 101

[54] Soberón J, Llorente J. The use of species accumulation functions for the prediction of species richness. Conserv Biol, 1993, 7: 480-488.

[55] Southwood TRE, Moran VC, Kennedy CEJ. The richness, abundance, and biomass of the arthropod communities in trees. J Anim Ecol, 1982, 51: 635-650.

[56] Stevens RE, Hawksworth FG (1970) Insects and mites associated with dwarf mistletoes. Research Paper RM-59. US Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station, Fort Collins, CO

[57] Stevens RE, Hawksworth FG (1984) Insect-dwarf mistletoe associations: an update. In: Hawksworth FG, Scharpf RF (tech. coords). Biology of dwarf mistletoes: proceedings of the symposium; General Technical ReportRM-111. US Department of Agriculture, Forest Service, Rocky Mountain Forest and Range Experiment Station, Fort Collins, CO, pp 94–101

[58] Stork NE. The composition of the arthropod fauna of Bornean lowland rain forest trees. J Trop Ecol, 1991, 7: 161-180.

[59] Stork NE, Adis J, Didham RK. Canopy arthropods, 1997, London: Chapman and Hall.

[60] Tassone RA, Majer JD. Abundance of arthropods in tree canopies of Banksia woodland on the Swan Coastal Plain. J R Soc West Aust, 1997, 80: 281-286.

[61] Tovar-Sánchez E, Cano-Santana Z, Oyama K. Canopy arthropod communities on Mexican oaks at sites with different disturbance regimes. Biol Conserv, 2003, 115: 79-87.

[62] Visser S. Fitter AH. Role of the soil invertebrates in determining the composition of soil microbial communities. Ecological Interactions in soil. Plants, microbes and animals, 1985, New York: Blackwell 279 317

[63] Watson DM. Mistletoe-A keystone resource in forest and woodland worldwide. Annu Rev Ecol Syst, 2001, 32: 219-249.

[64] Watson DM, Herring M. Mistletoe as a keystone resource: an experimental test.. Proc Biol Sci, 2012, 279: 3853-3860.

[65] Whittaker PL. The insect fauna of mistletoe (Phoradendron tomentosum, Loranthaceae) in Southern Texas. Southwest Nat, 1984, 29: 435-444.

[66] Williamson M, Gaston KJ, Lonsdale WM. The species-area relationship does not have an asymptote. J Biogeogr, 2001, 28: 827-830.

[67] Yanoviak SP, Nadkarni NM (2001) Arthropod diversity in epiphytic bryophytes of a neotropical cloud forest. In: Ganeshaiah KN, Shaanker RU, Bawa KS (eds), Tropical ecosystems: structure, diversity and human welfare. Proceedings of the international conference on tropical ecosystems, Bangalore, India, 15–18 July 2001. Oxford-IBH, pp 416–419

[68] Yanoviak SP, Nadkarni NM, Gering JC. Arthropods in epiphytes: a diversity component that is not effectively sampled by canopy fogging. Biodivers Conserv, 2003, 12: 731-741.

[69] Zar JH. Biostatistical analysis, 2010, Upper Saddle River: Prentice-Hall.