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Early Vessel Evolution and the Diverisification American Journal of Botany 97(1): 80–93. 2010. E ARLY VESSEL EVOLUTION AND THE DIVERISIFICATION OF WOOD FUNCTION: INSIGHTS FROM MALAGASY CANELLALES 1 Patrick J. Hudson 2 , Jacqueline Razanatsoa 3 , and Taylor S. Feild 2,4 2 Department of Ecology and Evolutionary Biology, University of Tennessee, Knoxville, Tennessee 37919 USA; and 3 Herbier du Parc Botanique et Zoologique de Tsimbazaza, Rue Fernand, Kasanga, Tsimbazaza, Antananarivo 101, Madagascar Xylem vessels have long been proposed as a key innovation for the ecological diversifi cation of angiosperms by providing a breakthrough in hydraulic effi ciency to support high rates of photosynthesis and growth. However, recent studies demonstrated that angiosperm woods with structurally “ primitive ” vessels did not have greater whole stem hydraulic capacities as compared to vesselless angiosperms. As an alternative to the hydraulic superiority hypothesis, the heteroxylly hypothesis proposes that subtle hydraulic effi ciencies of primitive vessels over tracheids enabled new directions of functional specialization in the wood. However, the functional properties of early heteroxyllous wood remain unknown. We selected the two species of Canellales from Madagascar to test the heteroxylly hypothesis because Canellaceae (represented by Cinnamosma madagascariensis ) produces wood with vessels of an ancestral form, while Winteraceae, the sister clade (represented by Takhtajania perrieri) is vesselless. We found that heteroxy- lly correlated with increased wood functional diversity related predominantly to biomechanical specialization. However, vessels were not associated with greater stem hydraulic effi ciency or increased shoot hydraulic capacity. Our results support the heteroxylly hypothesis and highlight the importance integrating a broader ecological context to understand the evolution of vessels. Key words: Canellales; heteroxylly; hydraulic conductivity; shade tolerance; xylem evolution; vessel development. The early evolution and rise to ecological dominance by How and when angiosperms evolved their emblematic high fl owering plants (angiosperms) during the Mesozoic (130 to 65 rates of photosynthesis and growth remain enigmatic. However, million years ago) marked a profound change in the water- and the prerequisite that high CO2 uptake requires high transpira- carbon-use capacity of global vegetation ( Bond, 1989 ; Becker, tion means that understanding how the water conducting pipe- 2000 ; Feild and Arens, 2005, 2007 ; Boyce et al., 2009 ; Feild et line diversifi ed during early angiosperm evolution represented al., 2009a ). Specifi cally, the vast majority of ecologically im- a critical factor that enabled the evolution of angiosperm hyper- portant angiosperms today function at rates of leaf CO2 and productivity ( Sperry, 2003 ; Pammenter et al., 2004 ; Sperry transpiration that are considerably greater than all other known et al., 2006 ; Brodribb et al., 2007 ; Feild et al., 2009a ). In this living and extinct land plant clades ( Bond, 1989 ; Brodribb and vein, xylem vessels have been viewed as an important feature Feild, 2000 ; Pammenter et al., 2004 ; Brodribb et al., 2007 ; of the vascular network that helped spark the rapid ecological Boyce et al., 2009 ). The high productivity and transpiration that sweep of angiosperms across the planet during the Cretaceous angiosperm leaves can supply has (1) founded diverse biotas ( Bailey, 1944 ; Carlquist, 1975 ; Doyle and Donoghue, 1986 ; that directly or indirectly require angiosperm productivity, (2) Bond, 1989 ; Crane and Lidgard, 1989 ; Baas and Wheeler, 1996 ; may have entrained increased rates of forest turnover, and (3) Lupia et al., 1999; Sperry, 2003 ; Pammenter et al., 2004 ; Bro- irreversibly changed rates of global biogeochemical cycles dribb et al., 2005 ; Feild and Arens, 2005 ; McElwain et al., through increased nitrogen use and weathering ( Knoll and 2005 ). Vessels, by virtue of their larger conduit sizes, furnish a James, 1987 ; Volk, 1989 ; Grimaldi, 1999 ; Moreau et al., 2006 ; greater capacity to conduct water than tracheids — their evolu- Crepet, 2008 ). tionary antecedents ( Brodribb and Feild, 2000 ; Sperry, 2003 ; Sperry et al., 2006 ). In addition, increases in the effi ciency of the xylem by vessels may enable the same hydraulic fl ow for a 1 Manuscript received 8 May 2009; revision accepted 25 September 2009. given amount of transpiring leaf area supported, but with less We thank the Malagasy government agencies (ANGAP, the Direction investment in wood ( Sperry, 2003 ; Brodribb et al., 2005 ; Feild des Eaux et Foret) and PBZT for granting permission for fi eld research. We are indebted to L. Andriamehefarivo, C. Birkinshire, and the staff of the and Arens, 2007 ). Thus, vessels have been pointed to as innova- Missouri Botanical Garden in Antananarivo, Madagascar, for invaluable tions that allowed early angiosperms to take advantage of fall- assistance in logistical planning and permit preparation. In the fi eld, Mr. M. ing atmospheric CO2 during their Cretaceous radiation as Ramahazaka and the porters of Befi ngotra, as well as J. Ratsimilaka and compared to vesselless plants with more costly stems ( McElwain the porters of Manatenaina, assisted in transporting equipment and in et al., 2005 ). The hypothesis that angiosperms vessels resulted locating plants. We express our gratitude to the people of the village of in increased fl ow capacity has in large part formed a conceptual Befi ngotra for their warm and gracious reception. Mr. J. Dedieu Tsilanizara cornerstone for an infl uential hypothesis that early angiosperms and his son, to whom we are most grateful, provided transportation to outcompeted most nonangiosperms during the Mesozoic ( Doyle Andapa, Befi ngotra, and Manatenina. We also acknowledge Mr. E. Mathieu and Donoghue, 1986 ; Bond, 1989 ; Becker, 2000 ; Lupia et al., for a welcome lift and information about Takhtajania . The authors thank N. 1999; Pammenter et al., 2004 ; Feild and Arens, 2005 ; McElwain Rowe, T. J. Brodribb, H. S. Feild, C. T. Feild, and D. S. Chatelet for helpful comments on the manuscript. This research was supported by a NSF grant et al., 2005 ; Lusk et al., 2007 ). (IOB-0714156). Highly effi cient vessels have been long viewed as appearing 4 Author for correspondence (e-mail: [email protected]) early during angiosperm evolution (Doyle and Donoghue, 1986; Bond, 1989; Pammenter et al., 2004; McElwain et al., 2005). doi:10.3732/ajb.0900130 Such vessels consisted of long tubes with thousands of short and 80 January 2010] Hudson et al. — Xylem function in Malagasy Canellales 81 wide elements that were interconnected by simple perforation 2008 ), the eastern tropical montane rainforests of Madagascar plates. However, extensive anatomical evidence indicates that represent the only region where the distributions of Canellaceae such vessels were rare at the base of extant angiosperm phylog- ( Cinnamosma ) and Winteraceae ( Takhtajania ) come into close eny as well as during the Cretaceous (Frost, 1930; Bailey, 1944; ecological contact ( Schatz, 2000 ; Feild et al., 2002 ). The excep- Carlquist, 1975, 2004; Wheeler and Baas, 1991; Carlquist and tional nature of the range overlap in Madagascar suggested that Schneider, 2002). Instead, vessels of many basal lineages a comparative study of Canellales from the region might pro- exhibited a range of small anatomical departures from vesselless vide insights on the ecophysiological consequences of early angiosperm tracheids. Such vessels, referred to as “ basal ves- vessel evolution. Such a suggestion was made because occur- sels ” ( Sperry et al., 2007 ), possessed incompletely lysed pit rence in the same climatic regime and biogeographic context membranes, had little differentiation between lateral pitting and may permit a clearer view of the possible ecophysiological ad- endwall pitting of vessel elements, and contained elongated sca- vantages of early vessels ( Feild et al., 2002 ). Although some lariform perforation plates. Compared to the vessels of most de- systematic anatomy has been presented on Malagasy Canellales rived angiosperm clades, basal vessels appear to be less ( Wilson, 1960 ; Carlquist, 2000 ), no comparative data exist on streamlined for water fl ow ( Bailey, 1944 ; Carlquist, 1975, 2004 ; how the functional responsibilities of the xylem relate to trache- Carlquist and Schneider, 2002 ). Supporting that hypothesis, ary element structure and ecological preference. measured hydraulic capacities of woods with basal vessels over- Our goal in the current study was to understand how early lapped with those of vesselless angiosperm woods, and these vessel evolution was integrated with overall wood function by capacities were much lower than woods of derived eudicots with comparing the growth habits, stem hydraulic and biomechani- vessels bearing simple perforation plates ( Sperry et al., 2007 ). cal structure – function relations, as well as shoot ecophysiologi- Hydraulic capacity in these comparisons was defi ned as hydrau- cal performances of two species of Canellales with and without lic conductivity ( KH ) divided by the cross-sectional area of xy- vessels. We investigated three questions: (1) Do xylem vessels lem ( KS = KH /sapwood area; Sperry et al., 2007 ). enable greater hydraulic effi ciency relative to tracheids? (2) If early vessels did not provide a leap in hydraulic effi ciency What are the functional consequences of an early experiment in over vesselless wood at the whole stem level, then what pro- heteroxylous vasculature
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