Abstract
Mistletoe infection between conspecific and interspecific hosts can be restricted by seed dispersal, host-mistletoe compatibility and abiotic factors, yet no studies have linked mistletoe infection patterns and pollination together for understanding mistletoe distribution at a local scale. Psittacanthus calyculatus (Loranthaceae) is a hemiparasitic plant with a broad host range across its geographic distribution. The potential for local host adaptation has been shown using cross-inoculation experiments, in which plants of mistletoe seeds collected from a given host are more likely to survive when they are inoculated on conspecific host trees compared with those inoculated on other host provenances. Here we evaluate host adaptation by describing the local patterns of infection (prevalence and intensity) of P. calyculatus mistletoes on three native host tree species (Alnus acuminata, Quercus crassipes, Salix bonplandiana) and one introduced species (Populus alba) and carried out cross-pollination experiments to examine how pollination affects infection patterns of different host species. Mistletoe infection prevalence (proportion of infection) and infection intensity (mean number of mistletoes per tree) were in general disproportional with respect to the availability of native host tree species but higher to that of non-native host tree species. Cross-pollination experiments showed higher mating success on the native host tree species, suggesting higher local adaptation to specially Q. crassipes. The observed spatial distribution of host tree species and mistletoe infection along with the non-random mating could contribute to local genetic structuring of mistletoe populations.
Similar content being viewed by others
References
Akaike H (1981) Likelihood of a model and information criteria. J Econom 16:3–14
Amico GC, Nickrent DL (2009) Population structure and phylogeography of the mistletoes Tristerix corymbosus and T. aphyllus (Loranthaceae) using chloroplast DNA sequence variation. Am J Bot 96:1571–1580
Amico GC, Vidal-Russell R, Nickrent DL (2012) Phylogenetic relationships and ecological speciation in the mistletoe Tristerix (Loranthaceae): the influence of pollinators, dispersers, and hosts. Am J Bot 94:558–567
Anderson RM, May RM (1978) Regulation and stability of host–parasite population interactions: I. Regulatory processes. J Anim Ecol 47:219–247
Anderson RM, May RM (1982) Coevolution of hosts and parasites. Parasitology 85:411–426
Arce-Acosta I, Suzan-Azpiri H, Garcia Rubio O (2016) Biotic actors associated with the spatial distribution of the mistletoe Psittacanthus calyculatus in a tropical deciduous forest of central Mexico. Bot Sci 94:89–96
Arruda R, Carvalho LN, Del-Claro K (2006) Host specificity of a Brazilian mistletoe, Struthanthus aff. polyanthus (Loranthaceae), in cerrado tropical savanna. Flora 201:127–134
Aukema JE (2004) Distribution and dispersal of desert mistletoe is scale-dependent, hierarchically nested. Ecography 27:137–144
Aukema JE, Martínez del Rio C (2002a) Variation in mistletoe seed deposition: effects of intra-and interspecific host characteristics. Ecography 25:139–144
Aukema JE, Martínez del Rio C (2002b) Where does a fruit-eating bird deposit mistletoe seeds? Seed deposition patterns and an experiment. Ecology 83:3489–3496
Azpeitia F, Lara C (2006) Reproductive biology and pollination of the parasitic plant Psittacanthus calyculatus (Loranthaceae) in Central Mexico. J Torrey Bot Soc 133:429–438
Bennetts RE, White GC, Hawksworth FG et al (1996) The influence of dwarf mistletoe on bird communities in Colorado ponderosa pine forests. Ecol Appl 6:899–909
Bush GL (1969) Sympatric host race formation and speciation in frugivorous flies of the genus Rhagoletis (Diptera, Tephritidae). Evolution 23:237–251
Calder DM (1983) Mistletoe in focus: an introduction. In: Calder DM, Bernhardt P (eds) The biology of mistletoes. Academic Press, Sydney, pp 1–17
Carlo TA, Morales JM (2008) Inequalities in fruit-removal and seed dispersal: consequences of bird behaviour, neighbourhood density and landscape aggregation. J Ecol 96:609–618
Clay K, Dement D, Rejmanek M (1985) Experimental evidence for host races in mistletoe (Phoradendron tomentosum). Am J Bot 72:1225–1231
Cocoletzi E, Angeles G, Ceccantini G et al (2016) Bidirectional anatomical effects in a mistletoe-host relationship: Psittacanthus schiedeanus mistletoe and its hosts Liquidambar styraciflua and Quercus germana. Am J Bot 103:986–997
Craig TP, Horner JD, Itami JK (2001) Genetics, experience, and host-plant preference in Eurosta solidaginis: implications for host shifts and speciation. Evolution 55:773–782
Criscione CD, Poulin R, Blouin MS (2005) Molecular ecology of parasites: elucidating ecological and microevolutionary processes. Mol Ecol 14:2247–2257
Díaz Infante S, Lara C, Arizmendi MC et al (2016) Reproductive ecology and isolation of Psittacanthus calyculatus and P. auriculatus mistletoes (Loranthaceae). Peer J 4:e2491
Donohue K (1995) The spatial demography of mistletoe parasitism on a Yemeni Acacia. Int J Plant Sci 156:816–823
Dzerefos CM, Witkowski ETF, Shackleton CM (2003) Host-preference and density of woodrose-forming mistletoes (Loranthaceae) on savanna vegetation, South Africa. Plant Ecol 167:163–177
Fadini RF (2011) Non-overlap of hosts used by three congeneric and sympatric loranthaceous mistletoe species in an Amazonian savanna: host generalization to extreme specialization. Acta Bot Bras 25:337–345
Glazner JT, Devlin B, Ellstrand NC (1988) Biochemical and morphological evidence for host race evolution in desert mistletoe, Phoradendron californicum (Viscaceae). Plant Syst Evol 161:13–21
Hines WGS, Hines ROH (1979) The Eberhardt statistic and the detection of nonrandomness of spatial point distributions. Biometrika 66:73–79
Jaenike J (1996) Population-level consequences of parasite aggregation. Oikos 76:155–160
Jermy T (1984) Evolution of insect/host plant relationships. Am Nat 124:609–630
Jerome CA, Ford BA (2002a) Comparative population structure and genetic diversity of Arceuthobium americanum (Viscaceae) and its Pinus host species: insight into host–parasite evolution in parasitic angiosperms. Mol Ecol 11:407–420
Jerome CA, Ford BA (2002b) The discovery of three genetic races of the dwarf mistletoe Arceuthobium americanum (Viscaceae) provides insight into the evolution of parasitic angiosperms. Mol Ecol 11:387–405
Kavanagh P, Burns K (2012) Mistletoe macroecology: spatial patterns in species diversity and host use across Australia. Biol J Linn Soc 106:459–468
Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Colorado
Knerer G, Atwood CE (1972) Evolutionary trends in the subsocial sawflies belonging to the Neodiprion abietis complex (Hymenoptera: Tenthredinoidea). Am Zool 12:407–418
Kuijt J (2009) Monograph of Psittacanthus (Loranthaceae). Systematic Botany Monographs, vol 86. American Society of Plant Taxonomists, pp 361
Laird NM, Ware JH (1982) Random-effects models for longitudinal data. Biometrics 3:963–974
Lamont BB (1983) Germination of mistletoes. In: Calder M, Bernhardt P (eds) The biology of mistletoes. Academic Press, Sydney, pp 129–143
Lara C, Pérez G, Ornelas JF (2009) Provenance, guts, and fate: field and experimental evidence in a host-mistletoe-bird system. Ecoscience 16:399–407
Lemaitre AB, Troncoso AJ, Niemeyer HM (2012) Host preference of a temperate mistletoe: disproportional infection on three co-occurring host species influenced by differential success. Aust Ecol 37:339–345
Linhart YB, Malville Ellwood L, Karron JD et al (2003) Genetic differentiation in the dwarf mistletoes Arceuthobium vaginatum and Arceuthobium americanum on their principal and secondary hosts. Int J Plant Sci 164:61–69
Lira-Noriega A, Toro-Núñez O, Oaks JR et al (2015) The roles of history and ecology in chloroplast phylogeographic patterns of the bird-dispersed plant parasite Phoradendron californicum (Viscaceae) in the Sonoran Desert. Am J Bot 102:149–164
López de Buen L, Ornelas JF (1999) Frugivorous birds, host selection and the mistletoe Psittacanthus schiedeanus, in central Veracruz, Mexico. J Trop Ecol 15:329–340
López de Buen LL, Ornelas JF (2002) Host compatibility of the cloud forest mistletoe Psittacanthus schiedeanus (Loranthaceae) in central Veracruz, Mexico. Am J Bot 89:95–102
López de Buen LL, Ornelas JF, García-Franco JG (2002) Mistletoe infection of trees located at fragmented forest edges in the cloud forests of central Veracruz, Mexico. For Ecol Manag 164:293–302
Magalhães S, Forbes MR, Skoracka A et al (2007) Host race formation in the Acari. Exp Appl Acarol 42:225–238
Manly BFJ, Miller P, Cook LM (1972) Analysis of a selective predation experiment. Am Nat 106:719–736
Martínez del Rio C, Silva A, Medel R et al (1996) Seed dispersers as disease vectors: bird transmission of mistletoe seeds to plant hosts. Ecology 77:912–921
Mathiasen RL, Hawksworth FG, Edminster CB (1990) Effects of dwarf mistletoe on growth and mortality of Douglas-fir in the Southwest. Great Basin Nat 50:173–179
Mathiasen RL, Nickrent DL, Shaw DC et al (2008) Mistletoes: pathology, systematics, ecology, and management. Plant Dis 92:988–1006
May DS (1971) The role of population differentiation in experimental infection of Prosopis by Phoradendron. Am J Bot 58:921–931
May RM, Anderson RM (1978) Regulation and stability of host-parasite population interactions: II. Destabilizing processes. J Anim Ecol 47:249–267
McCoy KD, Boulinier T, Tirard C et al (2003) Host-dependent genetic structure of parasite populations: differential dispersal of seabird tick host races. Evolution 57:288–296
Medel R, Botto-Mahan C, Smith-Ramírez C et al (2002) Historia natural cuantitativa de una relación parásito-hospedero: el sistema Tristerix-cactáceas en Chile semiárido. Rev Chilena Hist Nat 75:127–140
Monteiro RF, Martins RP, Yamamoto K (1992) Host specificity and seed dispersal of Psittacanthus robustus (Loranthaceae) in south-east Brazil. J Trop Ecol 8:307–314
Morales JM, Carlo TA (2006) The effects of plant distribution and frugivore density on the scale and shape of dispersal kernels. Ecology 87:1489–1496
Nickrent DL, Butler TL (1990) Allozymic relationships of Arceuthobium campylopodum and allies in California. Biochem Syst Ecol 18:253–265
Nickrent DL, Butler TL (1991) Genetic relationships in Arceuthobium monticola and A. siskiyouense (Viscaceae): new dwarf mistletoe species from California and Oregon. Biochem Syst Ecol 19:305–313
Nickrent DL, Stell AL (1990) Electrophoretic evidence for genetic differentiation in two host races of hemlock dwarf mistletoe (Arceuthobium tsugense). Biochem Syst Ecol 18:267–280
Nickrent DL, Duff RJ, Colwell AE et al (1998) Molecular phylogenetic and evolutionary studies of parasitic plants. In: Soltis DE, Soltis PS, Doyle JJ (eds) Molecular systematics of plants II. Springer, New York, pp 211–241
Norton DA, Carpenter MA (1998) Mistletoes as parasites: host specificity and speciation. Trends Ecol Evol 13:101–105
Norton DA, de Lange PJ (1999) Host specificity in parasitic mistletoes (Loranthaceae) in New Zealand. Funct Ecol 13:552–559
Norton DA, Hobbs RJ, Atkins L (1995) Fragmentation, disturbance, and plant distribution: mistletoes in woodland remnants in the Western Australian wheatbelt. Conserv Biol 9:426–438
Norton DA, Ladley J, Sparrow AD (2002) Host provenance effects on germination and establishment of two New Zealand mistletoes (Loranthaceae). Funct Ecol 16:657–663
Okubamichael DY, Griffiths ME, Ward D (2014) Reciprocal transplant experiment suggests host specificity of the mistletoe Agelanthus natalitius in South Africa. J Trop Ecol 30:153–163
Ornelas JF, Ordano M, de-Nova AJ et al (2007) Phylogenetic analysis of interspecific variation in nectar of hummingbird-visited plants. J Evol Biol 20:1904–1917
Ornelas JF, Gándara E, Vásquez-Aguilar AA et al (2016) A mistletoe tale: postglacial invasion of Psittacanthus schiedeanus (Loranthaceae) to Mesoamerican cloud forests revealed by molecular data and species distribution modeling. BMC Evol Biol 16:78
Overton JM (1994) Dispersal and infection in mistletoe metapopulations. J Ecol 82:711–723
Overton JM (1997) Host specialization and partial reproductive isolation in desert mistletoe (Phoradendron californicum). SW Nat 42:201–209
Perkins SL (2001) Phylogeography of Caribbean lizard malaria: tracing the history of vector-borne parasites. J Evol Biol 14:34–45
Phillips PA, Barnes MM (1975) Host race formation among sympatric apple, walnut, and plum populations of the codling moth, Laspeyresia pomonella. Ann Entomol Soc Am 68:1053–1060
Pinheiro J, Bates D (2006) Mixed-effects models in S and S-PLUS. Springer, New York, p 527
Poulin R (2007) Evolutionary ecology of parasites, 2nd edn. Princeton University Press, Princeton
Press MC, Phoenix GK (2005) Impacts of parasitic plants on natural communities. New Phytol 166:737–751
Price PW (1980) Evolutionary biology of parasites. Princeton University Press, Princeton
R Core Development Team (2014) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, http://WWW.r-project.org/)
Ramírez MM, Ornelas JF (2009) Germination of Psittacanthus schiedeanus (mistletoe) seeds after passage through the gut of Cedar Waxwings and Grey Silky-flycatchers. J Torrey Bot Soc 136:322–331
Ramírez MM, Ornelas JF (2012) Cross-infection experiments of Psittacanthus schiedeanus: effects of host provenance, gut passage and host fate on mistletoe seedling survival. Plant Dis 96:780–787
Reid N (1989) Dispersal of mistletoes by honeyeaters and flowerpeckers: components of seed dispersal quality. Ecology 70:137–145
Reid N, Smith MS, Zhao Gui Y et al (1995) Ecology and population biology of mistletoes. In: Lowman MD, Nadkarni NM (eds) Forest canopies. Academic Press, San Diego, pp 285–310
Rieseberg LH, Wendel J (2004) Plant speciation—rise of the poor cousins. New Phytol 161:1–21
Rieseberg LH, Willis JH (2007) Plant speciation. Science 317:910–914
Rist L, Uma Shaanker R, Ghazoul J (2011) The spatial distribution of mistletoe in a southern Indian tropical forest at multiple scales. Biotropica 43:50–57
Rödl T, Ward D (2002) Host recognition in a desert mistletoe: early stages of development are influenced by substrate and host origin. Funct Ecol 16:128–134
Roura-Pascual N, Brotons L, García D et al (2012) Local and landscape-scale biotic correlates of mistletoe distribution in Mediterranean pine forests. For Syst 21:179–188
Roxburgh L, Nicolson SW (2005) Patterns of host use in two African mistletoes: the importance of mistletoe–host compatibility and avian disperser behaviour. Funct Ecol 19:865–873
Sargent S (1990) Neighborhood effects on fruit removal by birds: a field experiment with Viburnum dentatum (Caprifoliaceae). Ecology 71:1289–1298
Sargent S (1995) Seed fate in a tropical mistletoe: the importance of host twig size. Funct Ecol 9:197–204
Shaw DJ, Grenfell BT, Dobson AP (1998) Patterns of macroparasite aggregation in wildlife host populations. Parasitology 117:597–610
Stiles FG, Freeman CE (1993) Patterns in floral nectar characteristics of some bird-visited plant species from Costa Rica. Biotropica 25:191–205
Sumida A, Miyaura T, Torii H (2013) Relationships of tree height and diameter at breast height revisited: analyses of stem growth using 20-year data of an even-aged Chamaecyparis obtusa stand. Tree Physiol 33:106–118
Teodoro GS, van den Berg E, Santos MDCN et al (2010) How does a Psittacanthus robustus Mart. population structure relate to a Vochysia thyrsoidea Pohl. host population? Flora 205:797–801
Troncoso AJ, Cabezas NJ, Faúndez EH et al (2010) Host-mediated volatile polymorphism in a parasitic plant influences its attractiveness to pollinators. Oecologia 162:413–425
Ward SA (1992) Assessing functional explanations of host-specificity. Am Nat 139:883–891
Yan Z, Reid N (1995) Mistletoe (Amyema miquelii and A. pendulum) seedling establishment on eucalypt hosts in eastern Australia. J Appl Ecol 32:778–784
Yule KM, Koop JAH, Alexandre NM et al (2016) Population structure of a vector-borne plant parasite. Mol Ecol 25:3332–3343
Zuber D, Widmer A (2009) Phylogeography and host race differentiation in the European mistletoe (Viscum album L.). Mol Ecol 18:1946–1962
Zuria I, Castellanos I, Gates JE (2014) The influence of mistletoes on birds in an agricultural landscape of central Mexico. Acta Oecol 61:51–56
Acknowledgments
We thank S. Díaz-Infante, H. Martínez-Roldan, S. Rodríguez-Mendieta, and the municipal and community authorities of Tetlatlahuca (San Andrés Coamilpa, Santa Agueda and Santa Cruz) for field assistance and logistic support, and R. Guevara for statistical advice. We are indebted to Antonio González-Rodríguez, Eduardo Ruiz-Sanchez and three anonymous reviewers for comments on previous versions of the manuscript. Permission to conduct our fieldwork was granted by the Mexican government (INE, SEMARNAT, SGPA/DGGFS/712/1299/12). This project was funded by research funds (20030/10563) from the Departamento de Biología Evolutiva, Instituto de Ecología, A.C. (INECOL), and from a competitive grant (155686) from the Consejo Nacional de Ciencia y Tecnología (CONACyT) awarded to J.F.O. M.J.P.C. was supported by a doctoral scholarship from CONACyT (365006/248109). This work constitutes partial fulfilment of MJPC’s doctorate at INECOL.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pérez-Crespo, M.J., Lara, C. & Ornelas, J.F. Uncorrelated mistletoe infection patterns and mating success with local host specialization in Psittacanthus calyculatus (Loranthaceae). Evol Ecol 30, 1061–1080 (2016). https://doi.org/10.1007/s10682-016-9866-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10682-016-9866-z