Life History of Tristerix aphyllus

One of the most unusual of all genera and species of Loranthaceae is Tristerix aphyllus. The mistletoe parasitizes two species of cactus, Echinopsis (=Trichocereus) chilensis and Eulychnia acida. The mistletoe seed germinates, forms a radicle whose tip differentiates into an haustorium that attaches to the host epidermis. Tissues of the haustorium then enter the host and grown into an internal endophyte which is the highly reduced vegetative stage of the mistletoe. The inflorescence of the parasite is produced by adventitious buds formed on the endophyte which then grow outward through the tissues of the cactus host. In some cases the inflorescence axes bear small leaves, yet in other cases these leaves are absent. Tristerix aphyllushas been reported to be a nonphotosynthetic holoparasite (Kraus et al. 1995), however, the presence of green tissues in seedling radicles (see photos below) suggest that chlorophyll is present.  Moreover, the Nickrent lab has generated sequences of several chloroplast genes indicating a chloroplast genome (plastome) is present and functional.

Habit Photographs

  1. Photo. Fray Jorge National Forest, Chile showing many Echinopsis chilensis cactus plants infected with Tristerix aphyllus. January 2003. Photo by G Amico.
  2. Photo. Same as above - close-up of inflorescences. Photo by John W. Reynolds.
  3. Photo. The mistletoe and the host (Echinopsis chilensis) in flower. Chile. Photo by G. Glatzel.
  4. Photo Mistletoe parasitic on Echinopsis chilensis, along road heading into the Andean foothills, east of Santiago Chile. The stem of the parasite actually grows underneath the outer cortex of the cactus - a good way to avoid the heat! Photo by John W. Reynolds.
  5. Photo. Same as above - closer view of inflorescences. Photo by John W. Reynolds.
  6. Photo. Cactus (Echinopsis chilensis) with plants. Fray Jorge National Park, Chile. Photo by G. Amico.
  7. Photo. Flowering plants on cactus. Near the Yerba Loca National Park, Chile. Photo by G. Amico.
  8. Photo. Cactus with flowering plants. Near the Yerba Loca National Park, Chile. Photo by G. Amico.
  9. Photo Mistletoe on Echinopsis chilensis with Guillermo Amico. In Fray Jorge National Forest, Chile. January 2003. Photo by Mariano Rodriguez Cabal.
  10. Photo.  Mistletoe emerging from cactus host.  Valle Nevado, metropolitan region (ca1500 m).  Photo by Serge Aubert, 9 Jan. 2003.
  11. Photo. Close-up of flowers. In Fray Jorge National Forest, Chile. January 2003. Photo by G. Amico.
  12. Photo. Another close-up of the flowers. Chile. Photo by G. Glatzel.
  13. Photo. Echinopsis chilensis with a yellow form of Tristerix aphyllus. Reserva Nacional Las Chinchillas, Chile. Photo by Wilfredo Gonzáles Lozada.
  14. Photo. Closer view of the flowers of the yellow form. Reserva Nacional Las Chinchillas, Chile. Photo by Wilfredo Gonzáles Lozada.
  15. Photo. Living (top) and dead (bottom) Tristerix aphyllus parasitic on the cactus, Echinopsis chilensis. Near Santiago, Chile. May 1991. See Mauseth et al. (1984, 1985). Photo by J. Mauseth.
  16. Photo. Inflorescence showing the prolific branching as it departs from its cactus host, Echinopsis chilensis. Near Santiago, Chile. January 1983. See Mauseth et al. (1984, 1985). Photo by J. Mauseth.
  17. Photo. Fruiting plants. Fray Jorge National Park, Chile. Photo by G. Amico.
  18. Photo. Mistletoe with flowers and fruits. Chile. Photo by G. Glatzel.
  19. Photo. Mature fruits containing viviparous embryos with elongated, twisted cotyledonary petioles. Reserva Nacional Las Chinchillas, Chile. Photo by Wilfredo Gonzáles Lozada.
  20. Photo. Another view of fruits, showing green and red embryos within. Reserva Nacional Las Chinchillas, Chile. Photo by Wilfredo Gonzáles Lozada.
  21. Photo. Fruit with pericarp split open revealing the viscid seed and viviparous embryo. Reserva Nacional Las Chinchillas, Chile. Photo by Wilfredo Gonzáles Lozada.
  22. Photo. Seed with pericarp removed. The radicle with a light-colored haustorial disk is visible at the tip. January 1983. See Mauseth et al. (1984, 1985). Photo by J. Mauseth.
  23. Photo. The seed disperser of Tristerix aphyllus, Mimus thenca in Fray Jorge National Forest, Chile. October 2003. Photo by Mariano Rodriguez Cabal
  24. Photo. Close-up of germinating seeds on cactus. Fray Jorge National Park, Chile. Photo by G. Amico.
  25. Photo. Seedling, attached to host needle, with extremely elongated, fused cotyledonary petioles "reaching" for host tissue. Reserva Nacional Las Chinchillas, Chile. Photo by Wilfredo Gonzáles Lozada. See Delrio et al. (1995) for a discussion of the relationship between cactus spine length and mistletoe seedling length.
  26. Photo. Seedling with tape measure showing that the fused cotyledonary petioles are ca. 10 cm long. Reserva Nacional Las Chinchillas, Chile. Photo by Wilfredo Gonzáles Lozada.
  27. Photo.  Seedlings of T. corymbosus showing the cotyledonary petioles that are fused at their tip (inside the seed), as in T. aphyllus and apparently other members of the genus, but are not fused outside the seed. In T. aphyllus, these petioles are fused into one structure that elongates tremendously.  The epicotyl never forms in T. aphyllus and the radicle occurs on a very short hypocotyl.  In T. corymbosus, the epicotyl is functional such that after host attachment and primary haustorial growth, the aerial shoots of the mistletoe develop from the epicotyl.
  28. Photo. Seedling attaching to host tissue with a primary haustorium. After successful attachment, the cotyledonary petioles wither and development of the parasite endophyte occurs entirely within the host tissue. Thus, the stems and inflorescences are not formed from the epicotyl but endogenously from the endophyte. Reserva Nacional Las Chinchillas, Chile. Photo by Wilfredo Gonzáles Lozada.
  29. Photo. Echinopsis chilensis areole with a young floral branch of the mistletoe emerging from its center. Near Santiago, Chile. October 1984. See Mauseth et al. (1984, 1985). Photo by J. Mauseth.
  30. Photo. A crack in the epidermis of Echinopsis chilensis with numerous floral buds of Tristerix emerging. See Mauseth et al. (1984, 1985). Photo by J. Mauseth.
  31. Photo. Mistletoe inflorescence emerging from Echinopsis chilensis. Note the small leaves (bracts) subtending some of the axes.
  32. Photo. Cross-section through the cactus stem shown the haustorial strand of the mistletoe penetrating through the cortex. Chile. Photo by G. Glatzel.

The papers published by James Mauseth and collaborators (cited below) greatly increased our knowledge of the anatomy of the infection process. I thank Jim for allowing access to his original color slides for scanning, some of which were published (in black and white) in the original journal articles.

Anatomy Photographs

  1. Photo. Longitudinal section of elongating radicle-haustorium of Tristerix aphyllus. Multiseriate trichomes occur over the surface except on the haustorial disk. See Mauseth et al. (1984, 1985). Photo by J. Mauseth.
  2. Photo. Haustorium attached to Eulychnia acida (Cactaceae). The haustorium has removed the cuticle and epidermis of the host and two collapsed zones are visible. September 1984. See Mauseth et al. (1984, 1985). Photo by J. Mauseth.
  3. Photo. Transstomatal penetration of Eulychnia acida by the haustorium of Tristerix aphyllus. The haustorium is on the top and the host cuticle and epidermis below, then a thick hypodermis, and at the extreme bottom host parenchymatous cortex. The parasite filament has broken at the level of the stoma. See Mauseth et al. (1985) Fig. 19. Photo by J. Mauseth.
  4. Photo. Hyphalike filament of the Tristerix endophyte. The parasite has large, red-staining nuclei compared with the host. See Mauseth et al. (1984). Photo by J. Mauseth.
  5. Photo. Vascular bundle of the cactus Echinopsis chilensis with endophyte cells of the mistletoe (cells scattered in central region with large, dark-staining nuclei. See Mauseth et al. (1984). Photo by J. Mauseth.
  6. Photo. A mature strand of Tristerix aphyllus growing in the phloem of a vascular bundle of the cactus Echinopsis chilensis. A collapsed zone is just beginning to form on the left side. The parasite cells have large, dark-staining nuclei. There are numerous small strands and filaments of the parasite mixed in the host phloem and cortex. See Mauseth et al. (1984). Photo by J. Mauseth.
  7. Photo. Endogenous bud forming under the epidermis of Echinopsis chilensis. A lysigenous space has formed between the parasite meristematic cells (below) and the host cells above. See Mauseth et al. (1985). Photo by J. Mauseth.
  8. Photo. Magnification of the phloem of Echinopsis chilensis infected with Tristerix aphyllus. The parasite cells have large, dark-staining nuclei. Many of the host seive plates are stained darker blue. See Mauseth et al. (1984). Photo by J. Mauseth.
  9. Photo. Echinopsis chilensis vascular bundle in which several filaments of the mistletoe endophyte have begun to develop into large strands. Note the strand (to the right) that is approaching one of the axial strands. See Mauseth et al. (1984). Photo by J. Mauseth.
  10. Photo. Early stage in the formation of the endophyte filament of the mistletoe growing within the cortex of Trichocereus chilensis. The parasite cells have large, dark-staining nuclei. See Mauseth et al. (1984). Photo by J. Mauseth.


References

Amico, G. C., R. Vidal-Russell and D. L. Nickrent. 2007. Phylogenetic relationships and ecological speciation in the mistletoe Tristerix (Loranthaceae): the influence of pollinators, dispersers, and hosts.  American Journal of Botany 94: 558-567.

Botto-Mahan, C., R. Medel, R. Ginocchio, and G. Montenegro. 2000. Factors affecting the circular distribution of the leafless mistletoe Tristerix aphyllus (Loranthaceae) on the cactus Echinopsis chilensis. Revista Chilena De Historia Natural 73: 525-531.

Caballero P, Ossa CG, Gonzáles WL, González-Browne C, Astorga G, Murúa MM, Medel R. 2013. Testing non-additive effects of nectar-robbing ants and hummingbird pollination on the reproductive success of a parasitic plant. Plant Ecology 214:633-640.

DelRio, C. M., M. Hourdequin, A. Silva, and R. Medel. 1995. The influence of cactus size and previous infection on bird deposition of mistletoe seeds. Australian Journal of Ecology 20: 571-576.

DelRio, C. M., A. Silva, R. Medel, and M. Hourdequin. 1996. Seed dispersers as disease vectors: Bird transmission of mistletoe seeds to plant hosts. Ecology 77: 912-921.

Gonzáles WL, Suárez LH, Guiñez R, Mede lR. 2007. Phenotypic plasticity in the holoparasitic mistletoe Tristerix aphyllus (Loranthaceae): consequences of trait variation for successful establishment. Evolutionary Ecology 21:431-444.

Gonzáles, W. L. , Suárez LH, Medel R. 2007. Outcrossing increases infection success in the holoparasitic mistletoe Tristerix aphyllus (Loranthaceae). Evolutionary Ecology 21:173-183.

Kelt DA, others. 2016. The avifauna of Bosque Fray Jorge National Park and Chile's Norte Chico. Journal of Arid Environments 126:23-36.

Kraus, R., P. Trimborn, and H. Ziegler. 1995. Tristerix aphyllus, a holoparasitic Loranthaceae. Naturwissenschaften 82: 150-151.

Lucero F, Botto-Mahan C, Medel R, Fontúrbel FE. 2014. New insights on the mistletoe Tristerix aphyllus (Loranthaceae): interaction with diurnal and nocturnal frugivorous species. Gayana Botánica. 71:270-272.

Mauseth, J. D., G. Montenegro, and A. M. Walckowiak. 1984. Studies on the holoparasite Tristerix aphyllus (Loranthaceae) infectng Trichocereus chilensis (Cactaceae). Can. J. Bot. 62: 847-857.

Mauseth, J. D., G. Montenegro, and A. M. Walckowiak. 1985. Host infection and flower formation by the parasite Tristerix aphyllus (Loranthaceae). Can. J. Bot. 63: 567-581.

Mauseth, J. D. 1990. Morphogenesis in a highly reduced plant: the endophyte of Tristerix aphyllus (Loranthaceae). Bot. Gaz. 151: 348-353.

Medel RG, Vergara E, Silva A, Serey IA. 1995. Variation of the architectural phenotype of Tristerix aphyllus in central Chile. Revista Chilena De Historia Natural 68:451-458.

Medel, R. 2000. Assessment of parasite-mediated selection in a host-parasite system in plants. Ecology 81: 1554-1564.

Medel, R. 2001. Assessment of correlational selection on tolerance and resistance traits in a host plant-parasitic plant interaction. Evolutionary Ecology 15: 37-52.

Medel, R., C. Botto-Mahan, C. Smith-Ramírez, M. A. Méndez, C. G. Ossa, L. N. Caputo, and W. L. Gonzáles. 2002. Historia natural cuantitative de una relación parásito-hospedero: el sistema Tristerix-cactáceas en Chile semiárido. Revista Chilena de Historia Natural 75: 127-140.

Medel, R., E. Vergara, A. Silva, and M. Kalin-Arroyo. 2004. Effects of vector behavior and host resistance on mistletoe aggregation. Ecology 85: 120-126.

Midgley, G. F., J. J. Midgley, W. J. Bond, and H. P. Linder. 1994. C-3 mistletoes on CAM hosts - an ecophysiological perspective on an unusual combination. South African Journal of Science 90: 482-485.

Silva, A., and C. M. delRio. 1996. Effects of the mistletoe Tristerix aphyllus (Loranthaceae) on the reproduction of its cactus host Echinopsis chilensis. Oikos 75: 437-442.

Soto-Gamboa, M., and F. Bozinovic. 2002. Fruit-disperser interaction in a mistletoe-bird system: a comparison of two mechanisms of fruits processing on seed germination. Plant Ecology 159: 171-174.

Last updated: 31-Oct-18 / dln