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Anatomy and Morphology |
2 School of Plant Science, University of Tasmania, Locked Bag 55, Hobart 7001, Australia; 3 Royal Botanic Gardens, Sydney, Mrs Macquaries Rd, Sydney 2002, Australia
Received for publication May 27, 2004. Accepted for publication January 25, 2005.
ABSTRACT
Species of the major Southern Hemisphere family, Proteaceae, have many scleromorphic anatomical structures in their leaves. Many of these structures (very thick cuticles and five anatomically distinct structures beneath the epidermis) are associated with the leaf surface exposed to direct light. These structures increase the path through which solar radiation must pass before reaching the mesophyll. In this study, such structures are proposed to protect the mesophyll from excess solar radiation, including photosynthetically active, ultraviolet, and possibly infrared radiation. Scleromorphic structures of the upper leaf surface and nonscleromorphic photoprotective structures (dense trichomes and papillae of the upper surface) occur almost exclusively in open vegetation. Open vegetation species of Proteaceae occur in oligotrophic and/or cold and/or dry places, where protection from light in excess of photosynthetic capacity and damage from ultraviolet light should be most important. Data from 123 species and a supertree constructed from available molecular phylogenies are used to show that the proposed photoprotective structures evolved many times within Proteaceae. In tests of correlated evolution, the proposed photoprotective structures are significantly associated with open vegetation, but not with dry habitats.
Key Words: anatomy • cuticle • photoprotection • Proteaceae • scleromorphy • sclerophylly • ultraviolet • xeromorphy
The strong fossil record and ecological, morphological, and anatomical diversity of the major Southern Hemisphere family, Proteaceae, have led to it being used as a model for understanding the evolution and function of scleromorphic leaf structures (Groom and Lamont, 1997
; Hill, 1998
; Jordan et al., 1998
; Mast and Givnish, 2002
). The family includes 79 genera and over 1700 species (Douglas, 1995
). Its center of diversity is Australia, with secondary centers in the Cape Province of South Africa, New Caledonia, Southeast Asia, and South America, and some species in Central America, Madagascar and New Zealand (Weston and Crisp, 1996
). Most species grow on nutrient poor soils, but range from the arid zone, to closed tropical rainforests, to Mediterranean climates, to alpine areas. They range from large-leaved trees to subshrubs, although most species are scleromorphic shrubs. The family has diverse leaf morphology (Johnson and Briggs, 1975
) and anatomy (Carpenter, 1994
; Catling and Gates, 1995
, 1998
). The family has a rich fossil record (Hill et al., 1995
). Fossil pollen show that the family was diverse by the Late Cretaceous, with major groups within the family present by this time (Dettmann and Jarzen, 1998
). Leaf macrofossils from the Palaeogene vary widely in leaf form (Carpenter and Jordan, 1997
; Hill, 1998
; Jordan et al., 1998
).
As discussed by Hill (1998)
, confused use of the terms xeromorphy, sclerophylly, and scleromorphy has impeded understanding of the evolution of scleromorphy. Scleromorphy refers to hardness or toughness, especially of leaves. Accordingly, we assume for the present work that heavily lignified tissues and very thick cuticles are scleromorphic anatomical structures. Scleromorphy is sometimes considered to be related to dry environments, especially temperate, dry summer climates. However, low nutrients appear to have been more important than aridity in the evolution of scleromorphy in many southern hemisphere groups (see Hill, 1998
). Thus, the centers of diversity of scleromorphic Proteaceae have very nutrient-poor soils, but include both wet and dry environments (Johnson and Briggs, 1975
). Also, diverse scleromorphic proteaceous fossil leaves occurred in the Paleogene long before the drying of Australia (Carpenter et al., 1994
; Carpenter and Jordan, 1997
; Jordan et al., 1998
). Hill (1998)
argued that truly xeromorphic fossils appeared later, when climates became drier. Similarly, phylogenetic reconstructions and fossil evidence suggest that Northern Hemisphere scleromorphs predate Mediterranean climates (Verdú et al., 2003
).
Two models explain the evolution of scleromorphy in response to low nutrient environments. An early model proposed that photosynthate that cannot be used metabolically because of phosphate limitation is accumulated as nonfunctional sclerenchyma or cuticle (Loveless, 1962
). This model would predict nonspecific distribution of sclerenchyma in leaves, perhaps concentrated near the site of production, the mesophyll. Alternatively, scleromorphy may protect long-lived leaves in low productivity environments from many kinds of damage and stress (Turner, 1994
). Importantly, this model predicts scleromorphy not only in low nutrient environments, but also in dry and cold ones. It also predicts that scleromorphic structures should be arranged in ways that maximize leaf protection. Although most related research has focused on physical damage, especially herbivory, Turner (1994)
did consider protection from excess solar radiation.
The Proteaceae show a remarkable range of specialized scleromorphic leaf anatomical structures (Dillon, 2002
). These include structures associated with the vascular bundles, leaf margins, and mesophyll. However, most are associated with the leaf surface exposed to radiation, usually the adaxial surface (Figs. 1–5). These include cuticles up to 35 µm thick and five anatomically distinct kinds of lignified layers between the epidermis and the mesophyll. These structures presumably attenuate the solar radiation that reaches the mesophyll because they increase the amount of tissue and number of surfaces that radiation must pass though. Furthermore, comparable structures of the lower leaf surface are rare, and species with thick upper cuticles have thinner abaxial cuticles (Dillon, 2002
). This raises the hypothesis that the adaxial scleromorphic structures act to reduce solar radiation.
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; Adams et al., 2002
). Most research on excess radiation has focused on biochemical photoprotection. However, self-shading reduces radiation and can act as fixed photoprotection. For example, Kern et al. (2004)
showed that architectural self-shading significantly reduced excess light with little effect on maximum photosynthesis under high light conditions in Nothofagus cunninghamii. Reflectance and absorption by trichomes or glaucous surfaces are well known to attenuate light (e.g., Ehleringer and Björkman, 1978
). However, there is less evidence for anatomical self-shading. Thick cuticles and hypodermes, which may absorb radiation before it reaches the mesophyll, are common in tropical, montane environments (Grubb, 1977
). Within Proteaceae, Jordan et al. (1998)
proposed that the multiseriate, sclerified hypodermis of Orites milliganii evolved as protection against excess light. The evolutionary patterns of scleromorphic and other potentially photoprotective structures within Proteaceae are therefore reconstructed in the present work, and the hypothesis that scleromorphic structures of the upper leaf surface are more strongly associated with open vegetation than with dry environments is tested using comparative methods. Open vegetation is used as an indicator of low productivity, high light environments, where photoprotection is most likely to be needed.
MATERIALS AND METHODS
Anatomical data
Anatomical data from cross-sections and clearings of fully expanded adult sun leaves were collected from 123 species (see Data Supplement 1 accompanying the online version of this article). Species of all the major clades and 61 of the 79 genera identified by Douglas (1995)
were sampled. This included species from throughout the geographic range of the family except Southeast Asia and Madagascar, although most were Australian. The species cover a very wide range of habitats, including all combinations of cold or warm, wet or dry, low or relatively high nutrients.
Multiple specimens were available for 35 species (see Data Supplement 1 accompanying the online version of this article). These represented within species contrasts, either between field-grown and cultivated plants, or between exposed montane habitats and sheltered lowland habitats. All character states used in this study were represented in this subsample (several times for most states). Each of these species was invariant with regard to these character states. The samples of 31 of the remaining species were field-grown specimens, and 58 were from botanic gardens (see Data Supplement 1 accompanying the online version of this article).
Transverse sections 20–25 µm thick were cut approximately half way along the leaves with a freeze microtome, stained with a 0.5% aqueous solution of toluidine blue for approximately 2 minutes, drained, rinsed with water, then stained for approximately 15 minutes in a saturated solution of Sudan III in ethanol, drained, rinsed with water, mounted on microscope slides in phenol glycerine jelly and heated to eliminate the staining of cellulose. This provided differential staining of lignin and cuticle. For examining hypodermal structures, small areas of leaf were cleared by digesting in dilute hydrogen peroxide, and then stained with toluidine blue.
For each species, three environmental variables (characters 1–3) and eight characters (characters 4–11) reflecting specific leaf structures and four composite characters (characters 12–15) reflecting categories of structures were scored (Table 1; see also Data Supplement 1 accompanying the online version of this article). The characters were all binary. Most of the characters are intrinsically binary, but a few (notably thick cuticles and the two aridity characters) could also be treated as continuous traits. Reducing these last characters to binary makes all analyses comparable.
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, Johnson and Briggs (1975)
, Vogts (1982)
, Poole and Adams (1986)
, Zegers and Garcia (1994)
, McCarthy (1995)
, Zegers (1995)
, and Wilson (1999
, 2000
).
The two aridity measurements were based on the moisture index, which reflects the long-term balance between precipitation and evaporation. It is estimated with a cumulative model by the software, BIOCLIM (Houlder et al., 2003
). The model works by taking a starting value, then adding or subtracting water according to weekly estimates of precipitation and evaporation. This is run for one year then the data from the second year provides the estimates. The moisture index ranges between 0 (indicating zero moisture balance) and 1, which would predict consistently saturated sandy loam soils in the absence of evapotranspiration. For each Australian species, point distribution data was assembled from Floyd (1990)
, Forster et al. (1991)
, the Australian Virtual Herbarium (www.rbg.vic.gov.au/cgi-bin/avhpublic/avhxml.cgi) and personal records. Estimates of the moisture index of the driest 3 consecutive months and of the warmest 3 consecutive months were made for each record. For each species, the lower quartile of these measures was then calculated. Lower quartiles were chosen to indicate the dry end of the geographic range of each Australian species, which is assumed to reflect the species' ability to survive in dry environments. The thresholds were chosen so that approximately half the species scored zero and half scored one for each variable. This should maximize the information content of these variables.
The leaf characters all refer to the surface of the leaves most exposed to direct light. In most species, this is the adaxial surface. The structures were present on both leaf surfaces in species with terete or isobilateral leaves, but were often less well developed on the lower surface. Characters 4–8 refer to five anatomically (and presumably evolutionarily) distinct lignified hypodermal tissues. Although the Orites-type abaxial pseudohypodermis occurs in both O. milliganii (Fig. 2) and O. acicularis (Fig. 4) (Jordan et al., 1998
) it is only scored as a potentially photoprotective structure in the latter species. The abaxial surface of O. acicularis is exposed to direct light in this terete-leaved species, whereas the abaxial surface is sheltered in the bifacial-leaved O. milliganii. Characters 12 and 13 refer to external reflective features (Figs. 6 and 7). These are not considered to be specific scleromorphic features, but were included to assess their relationship with the scleromorphic structures.
The phylogeny
The phylogeny (Fig. 8) is based on a supertree based on all available molecular phylogenies. This was constructed as the strict consensus of 10 000 trees found by heuristic search with PAUP* 4.0b (Swofford, 2000
). Each character (See Data Supplement 2 accompanying the online version of this article) defined a clade with greater than 60% bootstrap support from one of the following analyses: Hoot and Douglas' (1998)
analysis of atpB and rbcL-atpB spacer data; Barker et al.'s (2002)
analysis of ITS data, Mast's (1998)
analysis of ITS and ITS1 data; Mast and Givnish's (2002)
analysis of rp116 intron and psbA/trnH spacer data; analyses of ITS and rbcL data (Peter Weston, Royal Botanic Gardens Sydney, and Nigel Barker, Rhodes University, unpublished data).
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about the monophyly of Leucadendron, Leucospermum, Serruria, Protea, and Isopogon. See Weston and Crisp (1994)
about the monophyly of Telopea, Lomatia, and Alloxylon. Orites species have the apparent synapomorphy of tepals without midribs in their distal portion (Johnson and Briggs, 1975
). Lambertia species have solitary, terminal flowers (Johnson and Briggs, 1975
). Persoonia has unusually large (15–30 µm) chromosomes, drupaceous fruits with smooth endocarps and wingless seeds and simple, entire leaves (Weston, 1994
). Hakea was assumed to be monophyletic but allowed to make Grevillea paraphyletic (Barker et al., 1999
). Strangea and Stenocarpus species formed a polytomy (Johnson and Briggs, 1975
; Douglas, 1995
).
Analyses
Character state changes were reconstructed with Fitch optimization implemented in MacClade 3.08 (Maddison and Maddison, 1999
). The illustrated reconstructions assume hard polytomies (i.e., assuming multiple speciation events when more than one branch of a polytomy has a derived state). However, reconstructions assuming soft polytomies (i.e., ones which reconstruct polytomies to give the minimum tree lengths) were also performed. Tree lengths for hard and soft polytomies represent the upper and lower bounds, respectively, of the minimum number of evolutionary changes required to explain the character distributions.
Pagel's (1994
, 1997
) program DISCRETE was used to test for correlated evolution between the three environmental variables and the four composite leaf characters and very thick cuticles. DISCRETE tests for evolutionary association between pairs of binary variables using a Markov model of evolution. This study only used "omnibus" tests, which test nonindependence in evolution of two variables. Because of the lack of resolution in parts of the phylogeny (Fig. 8), separate analyses were performed on 40 trees that were constrained to the topology in Fig. 8 but random with regard to the polytomies. DISCRETE includes branch lengths in its calculations (Pagel, 1997
). In this study the branches were made one unit long. Although this can lead to misleading results (Pagel, 1997
), it is unlikely to lead to false inferences in this present study. Analyses of trees constructed with uniform total length from base to terminals produced very similar log likelihood ratios (N = 8; r = 0.985; regression slope = 1.00; intercept = –0.27) to the corresponding trees with unit branch lengths.
Analyses were performed on two data sets. Associations of leaf characters with vegetation structures and the two aridity measures were tested on a data set containing only Australian species. Associations with vegetation structure were also tested on a data set containing all 123 species.
RESULTS
Hypodermes, very thick cuticles, papillae, and dense trichomes were each reconstructed as having evolved many times, regardless of whether hard or soft polytomies were assumed (Figs. 9–12). The four kinds of pseudohypodermes (not shown) have evolved less frequently. The Orites-type adaxial pseudohypodermis is unique to Orites milliganii (open vegetation). The Orites-type abaxial pseudohypodermis occurs in both O. milliganii and O. acicularis, but in O. acicularis occurs on the leaf surface exposed to direct light (open vegetation). Banksia-type pseudohypodermes evolved at the base of the Banksia clade (open vegetation) and were lost in B. spinulosa (open vegetation). Pseudohypodermes of ideosclereids evolved three (soft polytomies) or six (hard polytomies) times in open vegetation, based on their presence in Roupala pseudocordata, Hakea lissosperma, H. dactyloides, and three species of the Stenocarpus clade (Strangea linearis, Stenocarpus salignus and S. angustifolius).
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Potentially light protecting scleromorphic leaf structures evolved many times in Proteaceae and are almost exclusively restricted to species of open vegetation, which suggests strong evolutionary pressure on these structures. Lignified structures between the upper epidermis and the mesophyll evolved at least 10 times in open vegetation, three times in closed vegetation, and were lost once in open vegetation. However, the loss in open vegetation was of the Banksia-type pseudohypodermis in B. spinulosa, which has an alternative structure (a lignified hypodermis). Thick cuticles, which may also act as photoprotectants, evolved at least 12 times in open vegetation. The tests for correlated evolution show that these associations with open vegetation were significant.
The tests of association performed on composite characters are likely to underestimate the evolutionary association with open vegetation. Some species of Banksia, Synaphea, Franklandia, and Orites have more than one of these structures, and related species can have different structures (e.g., different species of Orites have thick cuticles, lignified hypodermes, or pseudohypodermes). These presumably represent independent evolutionary events, but the analyses of composite characters would infer single events. All the relevant species involved were from open vegetation, so the resulting biases would be toward underestimating the already strong associations between open vegetation and the proposed photoprotective characters. In contrast, the species involved varied with regard to the aridity measures, consistent with the lack of association between aridity and the proposed photoprotective structures of the upper leaf surface.
These results are consistent with scleromorphic structures of the leaf surface exposed to direct light having evolved as adaptations to reduce the amount of radiation reaching the mesophyll (as proposed by Jordan et al., 1998
with regard to Orites milliganii). Open vegetation species of Proteaceae occur in cold and/or dry and/or very low nutrient habitats with exposure to full sun. Photoprotection is a major factor in such environments, largely from limitations on photosynthetic capacity, so that these species would be expected to need more photoprotection than closed forest species (Ball et al., 1995
; Adams et al., 2002
). Furthermore, ultraviolet radiation levels should be high in most of the open environments, and plants in low productivity environments would be expected to have fewer resources to allocate to repairing such damage.
No environmental parameter appears to explain the incidence of apparent photoprotective structures better than vegetation structure. The open vegetation species with the apparent photoprotective structures come from very diverse environments including high and low rainfall alpine areas, seasonally very hot and dry lowland Mediterranean climates, and wet lowland subtropical areas. In particular, the weakness of the association of thick cuticles or hypodermal structures with dry climates argues against the evolution of these structures as a primary response to dry climates. However, photoprotective structures would be expected to show some association with summer aridity because of the combination of physical stress and maximum radiation in that environment. This, or autocorrelation with open vegetation, could explain the weak but significant associations of photoprotective structures with summer aridity.
Although the effects of the difference between closed and open vegetation on water relations needs further investigation, the scleromorphic structures described here are poor candidates for reducing water loss or protecting the leaves against low water potentials. In general, cuticle thickness is poorly related to resistance to diffusion of water vapor (Kerstiens, 1996
; Riederer and Schreiber, 2001
). Furthermore, the thick cuticles observed here are much thicker than those of many xerophytes. For example, most North American Cactoideae (the main group of cacti) have cuticles 5 µm thick or less (Loza-Cornejo and Terrazas, 2003
), and five of six disparate South African arid species sampled by Jordaan and Kruger (1998)
had cuticles less than 2 µm thick. The hypodermal tissues described here are unlikely to reduce water loss because these structures are all heavily pitted. Although it has often been suggested that scleromorphy increases drought tolerance by increasing the ability of leaves to tolerate low water potentials, this is poorly supported by experimental evidence (Salleo and Nardini, 2000
). In any case, the structures described here are mostly not good candidates for preventing leaf collapse, because they are only associated with the upper surface and do not provide specific vertical support of the mesophyll. Other scleromorphic structures found in the family (e.g., osteosclereids, thick mesophyll cell walls and bundle sheath extensions) could prevent collapse (Dillon, 2002
).
There is little doubt that dense trichomes or papillae creating a glaucous surface reduce the light reaching the mesophyll. Their association with open vegetation (evolving at least 14 times in open vegetation) supports the concept that open vegetation reflects a need for photoprotection within Proteaceae. Also, their incidence suggests that external and scleromorphic structures can provide different means of fixed photoprotection. Such superficial photoprotection occurs in Bellendena montana and most species of Proteoideae and Persoonioideae, but is rare in Grevilleoideae. In contrast, scleromorphic photoprotective structures are common in Grevilleoideae, but absent from Persoonioideae and Bellendena and uncommon in Proteoideae. This inference is further supported by the fact that the associations of open vegetation with superficial and scleromorphic photoprotective structures combined are much stronger than with either superficial or scleromorphic structures alone.
One problem with fixed photoprotection is that, unlike biochemical protection, the degree of protection does not respond to short-term environmental changes. Although the trade-offs between biochemical and fixed photoprotection are not known, scleromorphic photoprotective structures may have a selective advantage in low resource environments by providing protection from other damage. Thick lignified hypodermal structures and thick cuticles should increase resistance to piercing and shearing, such as that caused by many invertebrate herbivores (e.g., Read et al., 2000
). Also, scleromorphic structures increase leaf carbon to nitrogen ratios, which may reduce herbivory (see Coley et al., 1985
; Coley, 1988
). However, protection against mechanical damage alone would not explain why these structures should be focused on the upper leaf surface. Multifunctionality may make these structures adaptive in spite of possible costs of their permanency.
The apparent evolution of lignified hypodermes in closed forest in Macadamia whelanii, Virotia leptophylla, and Eidothea zoexylocarya could be because they occur in some of the most resource limited of closed vegetation types, in which light protection may well be favored. Virotia leptophylla occurs on the notoriously depauperate ultramafic geology in New Caledonia (Virot, 1968
), and E. zoexylocarya and M. grandis occur on nutrient-poor, granitic soils (McCarthy, 1995
). Alternatively, other factors (such as herbivory) may have favored the evolution of these structures, or the structures may reflect past associations with open environments.
The scleromorphic structures described here are reconstructed as having evolved towards the tips of the phylogeny, which is consistent with evolution in response to environmental changes during the Late Cretaceous and Cenozoic. Soil depletion through laterization during this period, which was probably enhanced by Proteaceae themselves (Pate et al., 2001
), may have been critical for the evolution of scleromorphy (e.g., Hill, 1998
). Cooling and drying through the late Paleogene and Neogene (Frakes, 1999
) may also have contributed. Fossils of some of these structures are consistent in age with this climatic evolution. Early Oligocene fossils from Tasmania with Orites-type adaxial and abaxial pseudohypodermes coincide with the development of cold climates (Jordan et al., 1998
). Banksia-type pseudohypodermes occur in southern Australian Oligo-Miocene fossils (Cookson and Duigan, 1950
).
The hypothesis that many scleromorphic structures provide protection from excess radiation needs to be tested physiologically. Methods include direct measurement of light climates (Vogelmann, 1993
) and fluorescence profiles (Vogelmann and Evans, 2002
) within leaves, measurements of reflectivity, and measurements of biochemical photoprotection. Furthermore, the relationships of the scleromorphic structures to water relations need to be investigated further, including tests of the degree to which light and water stress induce increased development of the scleromorphic structures described here, and the impacts of such induced changes on photosynthesis and water relations.
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1 The authors thank Gary Sankowsky, Damien Rathbone, Andrea Leigh, Matt Bradford, and staff of the Royal Tasmanian Botanic Gardens and Royal Botanic Gardens at Mt. Annan, Mt. Tomah and Sydney for assistance with collecting. Ray Carpenter, Mike Crisp, Mark Hovenden, and Tim Brodribb commented on the manuscript. A Hansjörg Eichler award from the Australian Systematic Botany Society assisted this work. 
4 Author for reprint requests (greg.jordan{at}utas.edu.au
)
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24 distribution for –2logL
