Heteroblasty in bromeliads – anatomical, morphological and physiological changes in ontogeny are not related to the change from atmospheric to tank form
Kerstin Meisner A , Uwe Winkler A and Gerhard Zotz A B C
+ Author Affiliations
- Author Affiliations
A Institut für Biologie und Umweltwissenschaften, AG Funktionelle Ökologie, Universität Oldenburg, 26111 Oldenburg, Germany.
B Smithsonian Tropical Research Institute, Apdo 08343-03092, Panama, Republic of Panama.
C Corresponding author. Email: gerhard.zotz@uni-oldenburg.de
Functional Plant Biology 40(3) 251-262 https://doi.org/10.1071/FP12201
Submitted: 6 July 2012 Accepted: 4 October 2012 Published: 23 November 2012
Abstract
Heteroblasty is defined as an abrupt change in gross morphology during ontogeny, whereas homoblastic species show no or gradual changes. For Bromeliaceae, there are conflicting reports on a very limited number of species on the functional importance of this step change compared with gradual changes (ontogenetic drift). Studying a large set of species should allow more general conclusions. Seventeen homoblastic and heteroblastic species from Panama were investigated, including the entire size range of most species. Measurements included functionally relevant anatomical (water storage tissue), morphological (stomatal and trichome densities) and physiological parameters (transpiration rates, nutrient uptake rates). Size-related variation in all parameters was common, but evidence for a step change in the studied parameters could not be detected in any of the heteroblastic species. Our results caused us to question the widely held view of the course of the ontogenetic development in heteroblastic bromeliads and their functional implications. These findings suggest that the possible functional relevance of heteroblasty in bromeliads require rethinking and future investigations should employ a comparative approach with both homoblastic and heteroblastic species and including the entire size range to account for ontogenetic drift.
Additional keywords: foliar nutrient uptake, foliar trichomes, ontogenetic drift, phosphate, potassium, stomata.
References
Adams WW Adams WW (1986a) Heterophylly and its relevance to evolution within the Tillandsioideae. Selbyana 9, 121–125.Adams WW Adams WW (1986b) Morphological changes accompanying the transition from juvenile (atmospheric) to adult (tank) forms in the Mexican epiphyte Tillandsia deppeana (Bromeliaceae). American Journal of Botany 73, 1207–1214.
| Morphological changes accompanying the transition from juvenile (atmospheric) to adult (tank) forms in the Mexican epiphyte Tillandsia deppeana (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar |
Adams WW Adams WW (1986c) Physiological consequences of changes in life form of the Mexican epiphyte Tillandsia deppeana (Bromeliaceae). Oecologia 70, 298–304.
| Physiological consequences of changes in life form of the Mexican epiphyte Tillandsia deppeana (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar |
Arruda RCO, Costa AF (2003) Foliar anatomy of five Vriesea sect. Xyphion (Bromeliaceae) species. Selbyana 24, 180–189.
Benzing DH (2000) ‘Bromeliaceae – profile of an adaptive radiation.’ (Cambridge University Press: Cambridge)
Benzing DH, Burt KM (1970) Foliar permeability among twenty species of the Bromeliaceae. Bulletin of the Torrey Botanical Club 97, 269–279.
| Foliar permeability among twenty species of the Bromeliaceae.Crossref | GoogleScholarGoogle Scholar |
Benzing DH, Renfrow A (1971) Significance of the patterns of CO2 exchange to the ecology and phylogeny of the Tillandsioideae (Bromeliaceae). Bulletin of the Torrey Botanical Club 98, 322–327.
| Significance of the patterns of CO2 exchange to the ecology and phylogeny of the Tillandsioideae (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar |
Benzing DH, Seemann J, Renfrow A (1978) The foliar epidermis in Tillandsioideae (Bromeliaceae) and its role in habitat selection. American Journal of Botany 65, 359–365.
| The foliar epidermis in Tillandsioideae (Bromeliaceae) and its role in habitat selection.Crossref | GoogleScholarGoogle Scholar |
Braga MMN (1977) Anatomía foliar de Bromeliaceae de Campina. Acta Amazonica 7, 1–73.
Bucher M (2007) Functional biology of plant phosphate uptake at root and mycorrhiza interfaces. New Phytologist 173, 11–26.
| Functional biology of plant phosphate uptake at root and mycorrhiza interfaces.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXht1antrs%3D&md5=1ac4940facb6bbbcac8d1c9ca06e3454CAS |
de Souza GM, Estelita MEM, Wanderley MGL (2005) Anatomia foliar de espécies brasileiras de Aechmea subg. Chevaliera (Gaudich. ex Beer) Baker, Bromelioideae-Bromeliaceae. Revista Brasileira de Botânica 28, 603–613.
| Anatomia foliar de espécies brasileiras de Aechmea subg. Chevaliera (Gaudich. ex Beer) Baker, Bromelioideae-Bromeliaceae.Crossref | GoogleScholarGoogle Scholar |
Epstein E, Hagen CE (1952) A kinetic study of the absorption of alkali cations by barley roots. Plant Physiology 27, 457–474.
| A kinetic study of the absorption of alkali cations by barley roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaG38XmtFCnsg%3D%3D&md5=21d724821612738b243ab54ec1b8cfa0CAS |
Evans GC (1972) ‘The quantitative analysis of plant growth.’ (University of California Press: Berkeley, CA)
Freschi L, Takahashi CA, Cambui CA, Semprebom TR, Cruz AB, Mioto PT, Versieux LD, Calvente A, Latansio-Aidar SR, Aidar MPM, Mercier H (2010) Specific leaf areas of the tank bromeliad Guzmania monostachia perform distinct functions in response to water shortage. Journal of Plant Physiology 167, 526–533.
| Specific leaf areas of the tank bromeliad Guzmania monostachia perform distinct functions in response to water shortage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlt1Krsro%3D&md5=bbfa3260cffef84b32a77f6d3e3a5292CAS |
Givnish TJ, Barfuss MHJ, Ee BV, Riina R, Schulte K, Horres R, Gonsiska PA, Jabaily RS, Crayn DM, Smith JAC, Winter K, Brown GK, Evans TM, Holst BK, Luther H, Till W, Zizka G, Berry PE, Sytsma KJ (2011) Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: Insights from an eight-locus plastid phylogeny. American Journal of Botany 98, 872–895.
| Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: Insights from an eight-locus plastid phylogeny.Crossref | GoogleScholarGoogle Scholar |
Goebel K (1900) ‘Organography of plants. Part 1.’ (Clarendon Press: Oxford)
Jackson ML (1958) ‘Soil chemical analysis.’ (Prentice Hall: Englewood Cliffs, NJ)
Jones CS (2001) The functional correlates of heteroblastic variation in leaves: changes in form and ecophysiology with whole plant ontogeny. Boletín de la Sociedad Argentina de Botánica 36, 171–184.
Lieske R (1914) Die Heterophyllie epiphytischer, rosettenbildender Bromeliaceen. Jahrbuch wissenschaftlicher Botanik 53, 502–510.
Meisner K, Zotz G (2011) Three morphs, one species. Journal of the Bromeliad Society 61, 104–111.
Meisner K, Zotz G (2012) Heteroblasty in bromeliads – its frequency in a local flora and the timing of the transition from atmospheric to tank form in the field. International Journal of Plant Sciences 173, 780–788.
| Heteroblasty in bromeliads – its frequency in a local flora and the timing of the transition from atmospheric to tank form in the field.Crossref | GoogleScholarGoogle Scholar |
Mez C (1904) Physiologische Bromeliaceen-Studien I. Die Wasser-Ökonomie der extrem atmosphärischen Tillandsien. Jahrbuch wissenschaftlicher Botanik 40, 158–229.
Morren E (1873) Exposition de Liège. Belgique Horticole 23, 137–138.
Ohrui T, Nobira H, Sakata Y, Taji T, Yamamoto C, Nishida K, Yamakawa T, Sasuga Y, Yaguchi Y, Takenaga H, Tanaka S (2007) Foliar trichome- and aquaporin-aided water uptake in a drought-resistant epiphyte Tillandsia ionantha Planchon. Planta 227, 47–56.
| Foliar trichome- and aquaporin-aided water uptake in a drought-resistant epiphyte Tillandsia ionantha Planchon.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhtlyku73L&md5=6a45a9b4ab65582ae2f4f0c5c404e0c7CAS |
Pierce S (2007) The jeweled armour of Tillandsia – multifaceted or elongated trichomes provide photoprotection. Aliso 23, 44–52.
Pierce S, Maxwell K, Griffiths H, Winter K (2001) Hydrophobic trichome layers and epicuticular wax powders in Bromeliaceae. American Journal of Botany 88, 1371–1389.
| Hydrophobic trichome layers and epicuticular wax powders in Bromeliaceae.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3Mngt1amtg%3D%3D&md5=391f4bb3f0f7847de8e8b82ba124056eCAS |
Poirier Y, Bucher M (2002) Phosphate transport and homeostasis in Arabidopsis. The Arabidopsis Book 1. Available at http://www.bioone.org/doi/abs/10.1199/tab.0024 [Verified 1 November 2012]
R Development Core Team (2010) ‘R: A language and environment for statistical computing.’ (R Foundation for Statistical Computing: Vienna, Austria)
Reinert F, Meirelles ST (1993) Water acquisition strategy shifts in the heterophyllous saxicolous bromeliad, Vriesea geniculata (Wawra) Wawra. Selbyana 14, 80–88.
Richardson BA, Rogers C, Richardson MJ (2000) Nutrients, diversity and community structure of two phytotelm systems in a lower montane forest, Puerto Rico. Ecological Entomology 25, 348–356.
| Nutrients, diversity and community structure of two phytotelm systems in a lower montane forest, Puerto Rico.Crossref | GoogleScholarGoogle Scholar |
Schmidt G, Zotz G (2001) Ecophysiological consequences of differences in plant size – in situ carbon gain and water relations of the epiphytic bromeliad, Vriesea sanguinolenta. Plant, Cell & Environment 24, 101–111.
| Ecophysiological consequences of differences in plant size – in situ carbon gain and water relations of the epiphytic bromeliad, Vriesea sanguinolenta.Crossref | GoogleScholarGoogle Scholar |
Schulz E (1930) Beiträge zur physiologischen und phylogenetischen Anatomie der vegetativen Organe der Bromeliaceen. Botanisches Archiv 29, 122–209.
Szczerba MW, Britto DT, Kronzucker HJ (2009) K+ transport in plants: physiology and molecular biology. Journal of Plant Physiology 166, 447–466.
| K+ transport in plants: physiology and molecular biology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltVeqt70%3D&md5=af1ee33ce4394d54ec7e541b964dd7afCAS |
The Plant List (2010) The Plant List. Version 1. Available at http://www.theplantlist.org/ [Verified 1 November 2012]
Tomlinson PB (1969) ‘Anatomy of the monocotyledons. III. Commelinales – Zingiberales.’ (Oxford University Press: Oxford)
Versieux LM, Elbl PM, Wanderley MDGL, de Menezes NL (2010) Alcantarea (Bromeliaceae) leaf anatomical characterization and its systematic implications. Nordic Journal of Botany 28, 385–397.
| Alcantarea (Bromeliaceae) leaf anatomical characterization and its systematic implications.Crossref | GoogleScholarGoogle Scholar |
Winkler U, Zotz G (2010) ‘And then there were three’: highly efficient uptake of potassium by foliar trichomes of epiphytic bromeliads. Annals of Botany 106, 421–427.
| ‘And then there were three’: highly efficient uptake of potassium by foliar trichomes of epiphytic bromeliads.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVGru7%2FL&md5=58a0870069aa51cc5061e45a32330b23CAS |
Zotz G, Thomas V (1999) How much water is in the tank? Model calculations for two epiphytic bromeliads. Annals of Botany 83, 183–192.
| How much water is in the tank? Model calculations for two epiphytic bromeliads.Crossref | GoogleScholarGoogle Scholar |
Zotz G, Tyree MT, Patiño S (1997) Hydraulic architecture and water relations of a flood-tolerant tropical tree, Annona glabra. Tree Physiology 17, 359–365.
| Hydraulic architecture and water relations of a flood-tolerant tropical tree, Annona glabra.Crossref | GoogleScholarGoogle Scholar |
Zotz G, Hietz P, Schmidt G (2001) Small plants, large plants – the importance of plant size for the physiological ecology of vascular epiphytes. Journal of Experimental Botany 52, 2051–2056.
| Small plants, large plants – the importance of plant size for the physiological ecology of vascular epiphytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXns1Wkt7Y%3D&md5=d8370176a1175c4b46ea7cf2c297114fCAS |
Zotz G, Reichling P, Valladares F (2002) A simulation study on the importance of size-related changes in leaf morphology and physiology for carbon gain of an epiphytic bromeliad. Annals of Botany 90, 437–443.
| A simulation study on the importance of size-related changes in leaf morphology and physiology for carbon gain of an epiphytic bromeliad.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XovFWnsbs%3D&md5=440df05968a9598dc1c187a326e821b3CAS |
Zotz G, Enslin A, Hartung W, Ziegler H (2004) Physiological and anatomical changes during the early ontogeny of the heteroblastic bromeliad, Vriesea sanguinolenta, do not concur with the morphological change from atmospheric to tank form. Plant, Cell & Environment 27, 1341–1350.
| Physiological and anatomical changes during the early ontogeny of the heteroblastic bromeliad, Vriesea sanguinolenta, do not concur with the morphological change from atmospheric to tank form.Crossref | GoogleScholarGoogle Scholar |
Zotz G, Wilhelm K, Becker A (2011) Heteroblasty – a review. Botanical Review 77, 109–151.
| Heteroblasty – a review.Crossref | GoogleScholarGoogle Scholar |
