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(American Journal of Botany. 2008;95:521-530.) doi: 10.3732/ajb.2007333 © 2008 Botanical Society of America, Inc. |
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Anatomy and Morphology |
2 School of Plant Science, University of Tasmania, Private Bag 55, Hobart 7001, Australia 3 Royal Botanic Gardens, Sydney, Mrs Macquaries Road, Sydney 2002, Australia 4 School of Earth and Environmental Sciences, University of Adelaide, Adelaide 5005, Australia
Received for publication 19 October 2007. Accepted for publication 23 February 2008.
ABSTRACT
Sunken, covered, and encrypted stomata have been anecdotally linked with dry climates and reduced transpiration and therefore have been used to infer dry palaeoclimates from fossils. This study assesses the evolutionary and ecological associations of such stomatal protection in a model system—the diverse southern hemisphere family Proteaceae. Analyses were based on the morphology of over 1400 Australian, South African, New Caledonian, New Zealand, and South American species, anatomy of over 300 of these species, and bioclimatic data from all 1109 Australian species. Ancestral state reconstruction revealed that five or six evolutionary transitions explain over 98% of the dry climate species in the family, with a few other, minor invasions of dry climates. Deep encryption, i.e., stomata in deep pits, in grooves, enclosed by tightly revolute margins or strongly overarched by cuticle, evolved at least 11 times in very dry environments. Other forms of stomatal protection (sunken but not closely encrypted stomata, papillae, and layers of hairs covering the stomata) also evolved repeatedly, but had no systematic association with dry climates. These data are evidence for a strong distinction in function, with deep encryption being an adaptation to aridity, whereas broad pits and covered stomata have more complex relations to climate.
Key Words: ancestral state reconstruction • bioclimatic modeling • palaeoclimate • papillae • phyloclimatic analysis • Proteaceae • sclerophylly • stomatal encryption • water relations • xeromorphy
Leaves can have a wide range of anatomical and morphological structures that partially isolate stomata from the turbulent atmosphere (Figs. 1–8). Traditionally, such stomatal protection has been considered as an adaptation to dry climates (e.g., Raven et al., 2005
), with the suggestion that they increase the effective boundary layer, decreasing stomatal conductance and thereby reducing stomatal transpiration (e.g., Hill, 1998; Roth-Nebelsick, 2007). These features are of particular interest to palaeobotanists because they have often been used to infer dry climates (e.g., Hill, 1998). However, the evidence for any association between stomatal protection and dry climates is largely anecdotal.
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) because decreases in conductance result in lower carbon dioxide concentration in the substomatal cavity. As a result, the gradient in carbon dioxide concentration from the leaf to the external atmosphere increases more than the corresponding gradient in water vapor. However, this does not necessarily imply that stomatal protection is an advantage in dry climates because plants can adjust water use efficiency by altering the degree of stomatal opening.
One possible way of determining if stomatal protection is linked with aridity would be to test for an evolutionary association with dry climates in an evolutionary model system. The extant and extinct species of Proteaceae, a southern hemisphere family of evergreen trees and shrubs, are especially suitable for investigating the evolution of xeromorphy and scleromorphy (Johnson and Briggs, 1975; Carpenter et al., 1994; Groom and Lamont, 1997; Hill, 1998; Jordan et al., 1998, 2005), for several reasons.
The great taxonomic (80 genera and 
1750 species; Weston and Barker, 2006), ecological and anatomical diversity of Proteaceae means that it is possible to tease apart the evolution of xeromorphy and scleromorphy (as argued by Hill, 1998). Although most species occur on nutrient poor soils, the family extends to deserts, tropical rainforests, mediterranean climates, wet temperate habitats, and alpine areas (Johnson and Briggs, 1975). In particular, proteaceous species of open vegetation occur in climates ranging from very wet to very dry, so that the repeated evolutionary transitions between closed forest and open vegetation are only weakly related to climate (Jordan et al., 2005).
The leaves of Proteaceae have very diverse anatomy (Venkata Rao, 1971; Carpenter, 1994; Catling and Gates, 19951998; Jordan et al., 2005), including a wide variety of forms of stomatal protection (Figs. 1–8). Many anatomical features have evolved repeatedly in the family, making it possible to test for evolutionary convergence in leaf anatomy (Jordan et al., 2005).
Finally, the evolutionary radiation of Proteaceae straddles the transition of Australia from a well-watered region in the Late Cretaceous and Paleogene into a mainly arid continent by the Late Neogene (e.g., Frakes, 1999). A detailed macro- and microfossil record shows that the family was present in the Late Cretaceous (Dettmann and Jarzen, 1998) and was very diverse by the Paleogene, when a range of both extinct and modern genera was present (e.g., Carpenter et al., 1994; Macphail et al., 1994; Carpenter and Jordan, 1997; Jordan et al., 1998).
This paper combines bioclimatic, anatomical, and phylogenetic data for living proteaceous species to reconstruct the evolution of the family into dry climates and to assess the relation of this evolution with each form of stomatal protection.
MATERIALS AND METHODS
The phylogeny and classification
This work uses a supertree derived from available molecular phylogenies (Weston and Barker, 2006). Many genera were each represented in this supertree by only one species, and multiple species of some of these genera were incorporated into the current analyses with the assumption that these genera were monophyletic (see Jordan et al., 2005). The phylogeny of Banksia of Mast and Givnish (2002) was also reanalyzed in the same way as the generic supertree because that study did not quantify climatic relationships. Platanaceae are treated as the sole outgroup because the only other family in the order Proteales, Nelumbonaceae, is aquatic and herbaceous. The two basal clades of extant Platanaceae (Platanus kerrii, an evergreen, tropical rainforest species from Indochina, and the remainder, which are deciduous species of Eurasia and North America) were scored separately.
Characters and data sources
Presence/absence characters were scored for species for climatic variables and forms of stomatal protection. The climatic characters were scored for all Australian species of Proteaceae, except poorly documented ones (1109 species in total). Published descriptions (Cookson and Duigan, 1950; Virot, 1968; Hô, 1992; McCarthy, 1995; Wilson, 1999; Goldblatt and Mann, 2000; Makinson 2000) and observations of herbarium collections were used to score macroscopic forms of protection for the 1109 Australian species, 332 South African species, 42 New Caledonian species, 10 South American species, and two New Zealand species of the family. Anatomical data were derived from cross sectional anatomy of over 300 species described by Weston (1983, 1994), Catling and Gates (1995, 1998) and Jordan et al. (2005), and from cuticle preparations of over 500 species (Carpenter, 1994; Jordan et al., 1998; Carpenter et al., 2005).
Climatic variables
Moisture indices of the dry and warm seasons (DSM and WSM) were calculated, based on the moisture index generated by the climatic prediction program BIOCLIM (Houlder et al., 2003). Moisture index is a synthetic estimate of the water content of relatively well-drained soils (sandy loam). The index reflects the estimated average water content of soils through a season, with 0 indicating zero soil water and 1 indicating saturated soils. It is assumed to be a good indicator of the drivers of plant water stress (vapor pressure deficit and soil moisture availability) because it is an integrated measure of the long-term balance between evaporation and transpiration, allowing for loss of excess water. The index was calculated for each point record in a data set assembled from Floyd (1990), Forster et al. (1991), the Australian Virtual Herbarium (http://www.rbg.vic.gov.au/cgi-bin/avhpublic/avhxml.cgi) and personal records. Following Jordan et al. (2005), DSM and WSM were calculated as the lower quartile for each species of the driest and warmest three consecutive months, respectively. The lower quartile was chosen so that DSM and WSM would reflect the dry end of the species’ ranges. DSM and WSM are therefore assumed to reflect tolerance of dry environments.
DSM and WSM were coded into presence/absence characters for ancestral state analyses. Separate characters were created for a range of thresholds (0.2, 0.3, 0.4, 0.5, and 0.6) in both DSM and WSM to help detect the presence of gradual evolutionary transitions and transitions at different levels of aridity in different lineages.
The moisture index could not be estimated for extra-Australian taxa, including the outgroup (Platanaceae). However, WSM was assumed to exceed 0.6 for Platanus kerrii, given the high summer rainfall in most of Indochina, apart from the east coast of Vietnam (Muller, 1982). WSM is scored as unknown for the rest of the Platanaceae (the sister group of P. kerrii), although it is likely that most of the species occur naturally in wet climates (e.g., Nixon and Poole, 2003). Even those species of Platanus that occur naturally in dry climates tend to be riparian (e.g., P. racemosa from California [Hickman, 1993] and P. wrightii from Arizona [Kearney and Peebles, 1961]). DSM was scored as unknown for both groups.
Deep encryption
Deep encryption was defined as the presence of an external aperture that is separated from the stomatal aperture by at least twice the width of the aperture of the crypt, pit, or groove. Four forms of deep encryption were recognized in Proteaceae:
100 µm in diameter, and the cavities were often 300 µm in diameter and contained 40–100 stomata.
Other forms of stomatal protection
Papillose pits were defined to include stomata that were sunken below the epidermis and partially covered by large papillae (Figs. 7, 8; see also Jordan et al., 1998). The stomata were typically sunken by 25–40 µm, with apertures 25–40 µm wide.
Some other species had stomata slightly sunken (<20 µm) below the leaf surface (e.g., Lomatia dentata, Grevillea hilliana) or had somewhat papillose surfaces (e.g., Lambertia echinata, Hakea petiolaris), but these did not form a discrete, clearly defined class and had no consistent pattern with climate. They are not considered further.
Dense hairs covering the stomatal regions were defined as the presence of a dense layer of hairs obscuring the stomata in fully developed leaves. This definition included species with hairs at the apertures of pits, grooves, or closely revolute margins (Figs. 1, 2, 5). Many other species had immature leaves with hairs that were lost at maturity.
Analyses
Statistical evolutionary comparative methods could not be used. Because many of the key features occur in isolated species in large clades (e.g., Grevillea/Hakea with 500 species), unbiased evolutionary comparative analyses would require species-level phylogenies. However, such phylogenies are lacking, except several clades of Banksia in which anatomical variation was insufficient to allow the application of statistical methods. This paper therefore uses ancestral state reconstruction and bioclimatic analyses of the traits.
For Grevillea, logistic regressions were used to test for association of WSM and DSM with tightly revolute margins and dense hairs covering the stomatal regions. Similar analyses tested the association of DSM and WSM with dense hairs covering the stomatal regions. While these analyses did not allow for phylogenetic effects, they provided evidence of nonrandom associations between climates and traits.
Character state changes were reconstructed with Fitch optimization of ancestral states, implemented in the program Mesquite version 1.12 (Maddison and Maddison, 2006), assuming both soft and hard polytomies. Soft polytomies generate the minimum possible number of evolutionary changes required to explain the distribution of a character on a given tree. They are inconsistent with techniques of tree construction based on parsimony (Coddington and Scharff, 1996), but are valid in the current analyses because the characters being reconstructed were not used in creating the phylogeny. Hard polytomies can generate multiple evolutionary events at polytomies, even though these apparent multiple events may be artefactual because the species having the derived state may form a clade.
RESULTS
Climatic relations of the family
The bioclimatic distribution of Australian Proteaceae was strongly skewed toward dry climates, with 75% of species having a DSM (dry season moisture index) less than 0.2 and 68% having a WSM (warm season moisture index) less than 0.2 (Fig. 9A). The distributions were not unimodal, with a low point between 0.2 and 0.3 in both the DSM and WSM. The phylogenetic reconstructions of WSM (thresholds 0.3–0.6) and DSM (thresholds 0.2–0.3) were all similar, suggesting that they reflected a stable signal. For all these traits, the ancestral state in the family was reconstructed as "wet" (Fig. 10). In each case, many genera were polymorphic, suggesting further evolution into and/or out of dry climates. For DSMs with thresholds >0.2, the ancestral state was ambiguous, although this may have been partly due to the lack of scores for the outgroup, but the reconstructions were poorly resolved and anomalously classified many genera of wet tropical rainforest as "dry." As a result, it is assumed that the reconstructions based on WSM best reflect the transition into dry climates in Proteaceae.
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] and in Lambertia ericifolia) (Figs. 11, 12). One ambiguous case is B. ericifolia, which occurs in moderately dry climates (DSM 0.4 and WSM 0.5). In addition, the more than 100 species of Grevillea with tightly revolute margins are likely to be the result of repeated evolution in dry climates. This large genus lacks an explicitly reconstructed phylogeny, but tightly revolute leaved species occur in 19 of Makinson’s (2000) 33 informal groups and were strongly overrepresented in dry climates: 91% of the tightly revolute-margined species have DSM and WSM <0.2 (Fig. 9D). However, tightly revolute margins were associated once with non-arid climates (in the subalpine-alpine species, Orites revoluta, which has DSM and WSM >0.8).
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), but the strong association of Hakea species with dry climates (Fig. 9C) implies that the encryption in Hakea either evolved in a dry climate or has been a very successful trait in such climates.
Deep pits were reconstructed by Mast and Givnish (2002) as having evolved twice in Banksia and lost twice, once to be replaced by tightly revolute margins (B. splendida) and once to be replaced by stomata in shallow depressions (B. coccinea). All these are reconstructed as being associated with dry habitats (Fig. 12).
Other forms of stomatal protection
Papillose pits evolved nine or ten times, generally in individual species that vary greatly in climatic association (Fig. 13). The Australian species with these structures included four wet (DSM and WSM >0.8) and two dry climate taxa (DSM and WSM <0.3) (Fig. 9E). These structures also occur in Leucadendron pubescens (Cape flora of South Africa), Kermadecia pronyensis (tropical rainforest, New Caledonia), and in Embothrium coccineum and Lomatia ferruginea (cool temperate rainforest, Chile and Argentina).
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The large polytomies within genera increase the ambiguity of some of the ancestral state reconstructions. For example, the reconstruction showed reversions to wet climates in the Proteeae + Leucadendreae clade (e.g., in wet grassland species of Protea, species of the wet heaths in eastern Australia in Isopogon and in species of the wettest parts of the Cape Floristic Region). However, species level phylogenies could reveal an alternative pattern of multiple invasions of dry habitats. Similar situations apply within the Hakea-Grevillea, Xylomelum-Lambertia, and Persoonia-Acidonia clades. However, with the possible exception of Hakea, none of these permutations affects any of the relations of form with climate discussed in this paper.
DISCUSSION
The data presented here indicate that most of the diversity of Proteaceae in dry climates is the result of a small number of major transitions and that the four forms of deep encryption found in the family each subsequently evolved more than once in members of the resulting dry climate clades. We take this as evidence that deep encryption is an adaptation to aridity. In contrast, other forms of stomatal protection (hairs, open pits, sunken stomata without encryption) have no obvious relation to dry climate and indeed seem to have a weak association with wet climates. The distinction between deep encryption and other forms of protection lies in deeply encrypted stomata having narrow external apertures that are distant from the stomatal complex.
Evolution of Proteaceae into dry climates
The reconstructions imply that Proteaceae evolved in wet climates, with only 7–10 transitions into dry climates (Table 2). However, five or six of these transitions explain 98% of dry climate Australian species (as defined as having WSM <0.3; Table 2). These reconstructions (based on climatic data for Australian species) are supported by the fact that they make plausible predictions for the climatic habitats of virtually all non-Australian Proteaceae (Table 3). Thus, they predict wet climates for rainforest and wet heath groups and dry climates for dry heaths and dry forest taxa. Brabejum stellatifolium may be an exception. It was predicted as wet, but grows in the summer dry Cape Floristic Region (Goldblatt and Mann, 2000). However, its riparian habitat (Goldblatt and Mann, 2000) may indicate a requirement for wet microsites. Also, the Protea + Faurea clade was predicted as dry, which is consistent with the distribution of most species in the summer dry Cape Floristic region. However, some Protea and most species of Faurea occur in summer wet regions further north in Africa. This inconsistency in habitat may be due to a reversion to wet climates, but it is also possible that the true ancestral state of the clade was wet, with subsequent invasion of dry climates. These anomalies may be clarified by species-level phylogenies and bioclimatic analysis.
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) and therefore predate the aridification of Australia (Frakes, 1999). The ancestral state of "dry" in these clades may be due to biased reconstructions resulting from extinction and/or poor phylogenetic resolution (e.g., Hardy, 2006). Thus, the recent ancestor of each of these clades could well have been "wet," but systematic extinction of wet climate lineages may have resulted in a reconstruction of "dry." In support of this alternative reconstruction is abundant evidence of the extinction of apparently wet climate Proteaceae, but little or no evidence of extinction of dry climate taxa (e.g., Hill et al., 1995; Jordan et al., 1998) although this evidence is slightly ambiguous because dry climate taxa tend to be poorly represented in fossil assemblages. Also, each of these lineages includes both wet and dry climate taxa, and reconstructions may change with improved phylogenetic resolution, as described for the Protea + Faurea clade. Notwithstanding these biases, the high abundance of dry climate taxa in these few major clades compared with the numerous clades containing only wet climate taxa suggests that these clades have features that allow evolution into dry climates. The presence of preadaptations for aridity is consistent with Mast and Givnish’s (2002) argument that the bundle sheath extensions in Banksieae were preadaptations for the deep pits in Banksia.
Deep encryption
The four different forms of deep encryption evolved a minimum of 11 times in very dry climates (and probably many times more in Grevillea), once in moderately dry conditions (Banksia ericifolia), and once in moderately well-watered subalpine areas (Orites revouta). However, the association of revolute margins with wet habitats in some species and the loss of deep encryption in B. coccinea indicate that the association of such encryption with dry climates is not absolute. These inferences are unlikely to have been significantly biased by systematic extinction because many of the events are related to single species.
Other stomatal protection
Most (six of nine) of the times that papillose pits evolved in Proteaceae were clearly associated with wet climates (Fig. 13). Any structure that increases the roughness of a surface should enhance the hydrophobic character of leaf waxes, and leaf papillae have been shown to reduce the wettability of waxy stomatal surfaces (Wagner et al., 2003) and therefore may decrease the occlusion of stomata by water drops or make leaf surfaces less amenable to fungal overgrowth (as suggested by Hill [1998] among others). However, these structures also evolved three times in mediterranean climates.
Dense hairs over the stomatal region evolved at least seven times in wet climates, but it is difficult to determine how often they evolved in dry climates because of the lack of good phylogenies of a number of large genera. However, the incidence of these structures is not biased toward dry climates either overall (Fig. 9F) or within the genera that are polymorphic for both hairs and climate (Table 1). Furthermore, all the dry climate taxa involved except Lambertia and Grevillea have amphistomatic leaves, and the hairs may have evolved for protection from excess radiation, including avoidance of overheating (e.g., Jordan et al., 2005). Hill (1998) argued that hairs covering the stomata may sometimes be xeromorphic, but in other cases prevent waterlogging or fungal/epiphytic overgrowth of stomata. As with papillae, the increased leaf surface roughness created by hairs should enhance the hydrophobic nature of surfaces. For example, hairs are associated with decreased leaf wettability in Patagonian species (Brewer and Nuñez, 2007).
The evolution of encryption
These results imply that forms of deep encryption are derived features closely tied to dry climates, whereas other forms of stomatal protection (both papillose pits and dense coverings of hairs) were not consistently associated with aridity. This lack of association is consistent with Roth-Nebelsick’s (2007) models that suggest that encryption involving narrow external apertures should have greater impact on conductance than broader apertures. The fossil record of Proteaceae is also consistent with this hypothesis, with deep encryption only occurring in relatively recent fossils, well after the aridification of Australia. Fossils with individual crypts and tightly revolute margins occur in the Early Pleistocene of Tasmania (Jordan, 1995). Deep pits and longitudinal grooves are not recorded in the fossil record, although relatively deep pits occur in fossil Banksia by the early Neogene (Hill, 1998). In contrast, other forms of stomatal protection occur in the Paleogene, when climates are considered to have been very wet (Hill, 1998; Jordan et al., 1998; Carpenter et al., 2004).
Overall, these result imply that the presence of hairs or papillae should not be used to infer dry climates from fossil leaves or to infer adaptation to aridity in living species. In contrast, deep encryption would appear to be good evidence for adaptation to xeric environments, and therefore the presence of such anatomy in fossil leaves could provide evidence of past aridity.
FOOTNOTES
1 The authors thank G. Sankowsky, M. Bradford, A. Leigh, D. Rathbone, R. Elick, and staff at the Royal Sydney, Mt Annan, Mt Tomah, and Royal Tasmanian Botanic Gardens for assistance with collecting specimens. A Hansjorg Eichler student award to R.A.D. from the Australian Systematic Botany Society award assisted this work. 
5 Author for correspondence (greg.jordan{at}utas.edu.au)
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  R. J. Carpenter, G. J. Jordan, D. E. Lee, and R. S. Hill Leaf fossils of Banksia (Proteaceae) from New Zealand: An Australian abroad Am. J. Botany, February 1, 2010; 97(2): 288 - 297. [Abstract] [Full Text] [PDF]
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 A. Roth-Nebelsick, F. Hassiotou, and E. J. Veneklaas Stomatal Crypts Have Small Effects on Transpiration: A Numerical Model Analysis Plant Physiology, December 1, 2009; 151(4): 2018 - 2027. [Abstract] [Full Text] [PDF]
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2= 86.9 and 60.8, respectively; P<< 0.001). (E) Species with papillose pits. (F) Species with hairs covering the stomatal region. Numbers of species without hairs covering the stomata are also given. Logistic regression showed no association between presence/absence of such hairs in Australian species and either DSM or WSM (likelihood ratio test, 
