The Botanical Review

, Volume 78, Issue 4, pp 463–489 | Cite as

Leaf Development, Metamorphic Heteroblasty and Heterophylly in Berberis s. l. (Berberidaceae)

  • Natalia Pabón-MoraEmail author
  • Favio González


Shoot development of temperate and tropical members of Berberis s. l. was examined in order to assess: (1) the homology of the spines along the long shoots and the foliage leaves that form on the short shoots; (2) the occurrence of heterophylly and/or heteroblasty in the genus; and (3) the structural correspondence between cataphylls, spines, and foliage leaves. The 1-5-armed spines have been interpreted as modified compound leaves lacking stipules, as a modified lamina (central spine) with stipules (lateral spines), or less often, as transformed branches, or as epidermal outgrowths. On the other hand, the foliage leaves of the short shoots have been interpreted as leaflets of palmately compound leaves. Our results indicate that there are three distinct leaf types per node: (1) Leaves modified in spines spirally arranged in long shoots; (2) foliage, expanded leaves densely arranged in short shoots; and (3) cataphylls protecting axillary buds. The spines are leaf homologs with a clear distinction between the leaf base with stipules, and a laminar portion modified into the 1-5-armed spine; the lateral spines are not stipules as they arise from the marginal meristem of the laminar portion, and not from the leaf base. The foliage leaves also have stipules flanking the leaf base. Both spiny leaves and foliage leaves develop an articulation between the base and the laminar portion. Cataphylls of the short shoots of Berberis s. str. and those of the reproductive short shoots of Mahonia correspond to the entire leaf base, but those of the renewal (vegetative) shoots of Mahonia are spiny and have an odd vestigial pinnately compound lamina. Heterochrony due to ontogenetic truncation caused by the formation of the terminal inflorescence at the apex of the short shoots could be responsible for the lack of petiole/lamina differentiation in the foliage leaves. The spiny long-shoot/foliose short-shoot system of branching in Berberis s. str. appears to be genetically and phylogenetically fixed and not environment-dependent. This represents a clear example of metamorphic heteroblasty sensu Zotz et al. (Botanical Review 77:109–151, 2011) with further occurrence of heterophylly along the short shoots.


Berberidaceae Berberis Heterochrony Heterophylly Leaf Development Long Shoots Mahonia Metamorphic Heteroblasty Short Shoots 



We thank D. W. Stevenson (The New York Botanical Garden) for inviting us to participate in the present issue of Botanical Review. We thank Barbara Ambrose for comments on the manuscript. We thank the Facultad de Ciencias, Universidad Nacional de Colombia, Bogotá, and the staff of the Structural Laboratory, The New York Botanical Garden, for logistic support. We also thank J. Hennig, D. Basile, and M. Baxter (Lehmann College, City University of New York), for access to living collections and microscopy facilities.

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© The New York Botanical Garden 2012

Authors and Affiliations

  1. 1.The New York Botanical GardenBronxUSA
  2. 2.Instituto de Ciencias NaturalesUniversidad Nacional de ColombiaBogotáColombia
  3. 3.Instituto de BiologíaUniversidad de AntioquiaMedellínColombia

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