Printer Friendly

Heteroblasty--a review.

Introduction

The shoot system of higher plants grows by adding new modules or metamers at the shoot apex, which normally consist of an intemode, a leaf or leaves, and vegetative or floral buds. Three more or less discrete temporal phases are frequently distinguished during postembryonic development: a juvenile vegetative phase, an adult vegetative phase, and a reproductive phase (Poethig, 2003). While only defined by the capacity to produce reproductive organs, more or less simultaneous changes in vegetative features such as differences in leaf shape and size, leaf arrangement, internode elongation, or the capacity for adventitious root production are frequently used as proxies to identify these phases.

Thus, plants do not merely increase in size (biomass, height, volume) during ontogeny by adding metamers, but these metamers almost universally show a certain degree of variation, in part simply because an increase in size necessitates correlated changes in shape and geometry (Niklas, 1994). This size-related variation is relatively subtle and gradual in the majority of cases, but there are also species with quite dramatic and abrupt changes. More than a century ago, Goebel (1889) described these species as "heteroblastic" to be distinguished from "homoblastic" taxa, in which changes are negligible or gradual. Classic examples of heteroblastic development (Fig. 1) are found among phyllodineous Acacia species (Kaplan, 1980), European ivy (Hedera helix, Goebel, 1913), aroid vines (Lee & Richards, 1991), Ulex europaeus (a leafless shrub with a leaf-beating "juvenile" stage), or tree species with a "divaricate" initial stage, i.e. small-leaved woody shrubs that have closely interlaced branches, which are quite distinctive for the flora of New Zealand (Cockayne, 1912). Remarkably, the morphological differences between forms can be so stunning as to fool scientists into describing them as different species (Lecomte & Webb, 1981).

Since Goebel's original publication, a considerable amount of research has been dedicated to the subject, addressing a range of questions such as the proximate mechanisms behind these abrupt changes (Kerstetter & Poethig, 1998), their evolutionary implications (Tomlinson, 1970; Li & Johnston, 2000), and also their functional and ecological consequences (Jones, 2001). The older literature, mostly dealing with morphological and anatomical, but also physiological aspects of heteroblasty, was reviewed in detailed and extensive earlier reviews, e.g. by Troll, 1939, Ashby, 1948, Schaffalitzky de Muckadell, 1959, or Allsopp, 1965, while more recent reviews clearly reflect the advance of molecular techniques (Kerstetter & Poethig, 1998). There are also a considerable number of studies trying to demonstrate an extant adaptive function of these ontogenetic changes, although to date most results are negative or inconclusive (Winn, 1999; Darrow et al., 2001, 2002; Gamage & Jesson, 2007).

[FIGURE 1 OMITTED]

However, no comprehensive recent review on heteroblasty is available. Such a review seems important not least because of a growing inconsistency in terminology in the literature, e.g. when it comes to the use of the terms heteroblastic vs. homoblastic species or heteroblasty vs. heterophylly. Although Jones (1999) has discussed major conceptual and terminological issues in an excellent essay, subsequent studies have paid little attention to her suggestions. The current review thus deals explicitly with the existing terminological ambiguity and reviews major biological aspects of heteroblasty in the hope to provide a stimulating basis for future research.

Particular emphasis is put on the functional implications of heteroblasty, starting with the assumption that it is indeed adaptive ('all juvenile characteristics will be shown to be adaptive in certain environments'; Barber, 1965). To demonstrate that heteroblastic changes are indeed functionally important under current ecological conditions, we face a prominent problem, since different processes are likely to co-occur during ontogeny. Apart from heteroblasty, which describes a step change in vegetative features, there are gradual ontogenetic changes associated with changes in size ('ontogenetic drift'; Evans, 1972) as well as a phase change from juvenile to adult (= reproductive) associated with maturing and possible functional physiological changes of vegetative organs. To complicate matters further, processes can be modified by phenotypic plasticity as a response to the prevailing ambient conditions within each stage or phase (Wright & McConnaughay, 2002). Unless studies distinguish between these possibilities differences may easily be ascribed to the wrong process. For example, a recent study with Eucalyptus occidentalis shows quite clearly that a sudden vegetative change in leaf anatomy and function and the phase change from juvenile to reproductive phase are developmentally uncoupled, i.e. these are two independent developmental processes which are under separate genetic control (Jaya et al., 2010).

Terminology

The term "heteroblastic" (condition: 'heteroblasty') [from Greek blastos, shoot] was originally introduced by Goebel to describe a form of plant development, in which substantial differences between earlier ("Jugendform" = juvenile form) and later stages ("Folgeform", subsequent form) are observed as opposed to the "homoblastic" type of development with small and gradual changes (Goebel, 1898, 1913). He explicitly stated that changes could affect the entire shoot ("Gestaltung" = morph) as well as its physiology. His concept was not restricted to leaves, but also included, e.g., differences in the capacity to produce adventitious roots. Moreover, he already identified an inherent problem of his concept, the fact that there was no sharp separation between these two developmental trajectories, but his examples of heteroblasty all show a fairly abrupt and conspicuous change between stages. Although mostly applied to vegetative morphology, the concept can also be applied to reproductive features (Lord, 1979).

Unfortunately, during the last decades the usage of the term "heteroblasty" has changed considerably, and it has become customary to describe even slight changes in leaf size and/or leaf shape during ontogeny as heteroblastic (e.g. Greyson et al., 1982; Hunter et al., 2006; Hall, 2007). However, a certain degree of ontogenetic variation in (leaf) form is probably universal in plants (Wright & McConnaughay, 2002), in part simply as a structural consequence of changes in the size of the apical meristem (SAM). Thus, if heteroblasty is used for any minor change, the distinction between homo- and heteroblasty becomes virtually meaningless.

Other modifications of Goebel's original concept seem more appropriate. For example, Philipson (1964) introduced the term "habit-heteroblastic" for cases with an abrupt (!) break in plant habit as found in a number of divaricating shrubs, which develop into a tree with a single trunk and are particularly prominent in the flora of New Zealand. A further important refinement was proposed by Ray (1990) in his treatise of climbing aroids. This author distinguished isomorphic, allomorphic and metamorphic shoot developments. The first represents a lack of ontogenetic changes in size or shape of a vegetative metamer (isomorphy), the second gradual changes in size and/or shape of varying degrees (allomorphy), and the last an abrupt change in form (metamorphosis). The major advance achieved with this scheme is the possibility of a quantitative distinction between homoblastic and heteroblastic species, morphologically or physiologically, which overcomes the vagueness of Goebel's definition (see below). In this paper, we include Philipson's and Ray's refinements, but otherwise use "heteroblasty" similar to Goebel's original definition as a "rather sudden and substantial change in form of individual metamers or plant habit during ontogeny". However, acknowledging the fact that a similar trial by Jones (1999) to disentangle decades of terminological confusion has not been very successful, we may rather take the risk of creating additional jargon and propose the term "metamorphic heteroblasty" to distinguish true heteroblasty unambiguously from allomorphy.

Similarly inconsistent is the use of the term "heterophylly" in the current literature. Heterophylly is sometimes defined extremely broadly as "variation in the size and shape of leaves produced along the axis of an individual plant" (Winn, 1999). Following this definition, all plants would be heterophyllous. Worse, heteroblasty and heterophylly are quite frequently confused, although the terms are clearly distinct conceptually (Lloyd, 1984): either one has been used as umbrella term of the other (e.g. Winn, 1999; Keller, 2004; Roberts, 2007). However, heterophylly refers exclusively to concurrent variation in leaf form within a single plant (= sensu lato) or, alternatively, to environmentally induced switches between either of two (or more) possible leaf morphologies (sensu stricto, Pigliucci, 2001), with typical examples among amphibious plants (Arber, 1919). The use of heterophylly should be confined to such cases and is then simply a special case of "phenotypic plasticity" (Alpert & Simms, 2002). In contrast, heteroblasty is not confined to leaves, although admittedly many studies on heteroblasty focus on differences in leaf form and size. Differences may also be found in phyllotaxy, intemode length, anthocyanin pigmentation, rooting ability, or wood structure (Goebel, 1898; Rumball, 1963; Frydman & Wareing, 1973).

In contrast to heterophylly, heteroblastic development can only be modified, but is not driven, by environmental stimuli. Particularly remarkable creations in the literature are terms like "environmentally induced heteroblasty" or "ontogenetic heterophylly". An additional advantage of this narrow definition of heteroblasty is a clear distinction from "ontogenetic drift", i.e. a gradual ontogenetic change in phenotypic traits associated with changes in plant size (Evans, 1972). Growth not only leads to an increase in plant parts such as leaves, stem and roots, but often to a quite predictable change in the proportional distribution ofbiomass among these parts. For example, the root to shoot ratio is initially very high in most plants, but drops rapidly during subsequent growth. Similarly, structural changes in leaf anatomy during growth in a rosette plant may be primarily related to mechanical functions: when leaf length increases from 1 to 100 cm during ontogeny in a large tank bromeliad such as Werauhia sanguinolenta (Zotz et al., 2004), increasingly stiff tissues are essential to avoid buckling under the leaves' own weight, since the deflection of a leaf is proportional to the cube of its length (Niklas, 1999). Without attention to ontogenetic drift, a study with a heteroblastic species comparing "small" plants with "early" morphology with "large" plants of "late" morphology cannot separate the effects of size and heteroblastic change. For example, in a study with the epiphytic bromeliad, Werauhia sanguinolenta, we could show that a large proportion of the anatomical and physiological differences between small atmospherics (with linear leaves with dense trichome cover) and large tanks (with broad leaves featuring overlapping leaf bases forming a water-holding reservoir) were due to size and not at all associated with the conspicuous change in leaf form and plant habit (Zotz et al., 2004).

There is yet another terminological problem in the literature, since most studies conflate heteroblastic development and the phase change from non-reproductive (juvenile) to reproductive status (adult) (Jones, 1999). Although a change in morphological characteristics may indeed coincide with the onset of maturity, this is unlikely in some cases and at least unclear in most other cases (Poethig, 1990; Wiltshire et al., 1994; Jones, 1999). For a few taxa, e.g. Eucalyptus occidental& or the E. risdonii--tenuiramis complex, there is even good evidence that the two processes are developmentally uncoupled (Wiltshire et al., 1998; Jaya et al., 2010). The different timing of these processes is particularly obvious when the abrupt change occurs at seedling size like in Acacia (Gardner et al., 2008) or heteroblastic bromeliads (Zotz, 2004), i.e. many years before minimum reproductive size is attained, but also in other cases, e.g., when large Eucalyptus trees are said to reproduce with a "juvenile" crown (Williams & Woinarski, 1997). At least two problems arise. First, this frequently used practice mixes two conceptually distinct processes. As already argued by Jones (1999) replacing the currently used terms "juvenile" and "adult" by "early" and "later forms" is not completely unambiguous either, but arguably such a change would be highly preferable over the current practice, which almost inevitably confuses potentially independent ontogenetic processes. In this review, juvenile and adult are put into quotation marks unless specifically referring to reproductive status (compare Jones, 2001). Secondly, when functional aspects are studied, the same argument applies as the one developed above for ontogenetic drift. Since physiological processes frequently change with reproductive status of a plant (Lambers et al., 2008), studies ignoring the reproductive status of a plant may erroneously ascribe differences between early and late forms of a species to heteroblastic changes instead of reproductive status.

A Quantitative Definition of Heteroblasty

A quantitative approach is a crucial step in advancing our understanding of the ecological and evolutionary importance of heteroblasty, which is also tree for other sources of ontogenetic variation such as phenotypic plasticity (Valladares et al., 2006). Moreover, a quantitative definition of heteroblasty should allow us to avoid much of the current terminological confusion. Clearly, in spite of the complex nature of heteroblasty, the chosen quantitative trait(s) should be simple and readily measurable to allow comparisons among a larger number of species. Ray's (1990) system, originally proposed for heteroblastic vines, allows a clear distinction between homoblastic and heteroblastic species. Figure 2 illustrates a straightforward application of this scheme to a number of epiphytic bromeliads, using the leaf index (compare Tsukaya, 2002) as a readily measurable trait. Following Goebel's original definition, only the "metamorphic" species Vriesea heliconioides and Guzmania lingulata would qualify as heteroblastic species, while the other four species included in this comparison with no or subtle and gradual changes are homoblastic. This approach does not consider cotyledons, which would otherwise lead to an inflation of "heteroblastic" species. This exclusion is clearly justified not only from a practical point of view--cotyledons are not derived from SAM and are thus no true leaves.

[FIGURE 2 OMITTED]

Other Uses of the Term "Heteroblasty" in the Botanical Literature

The term "heteroblasty" is used here in the context of ontogenetic changes in form and function, but it has at least four additional meanings in the botanical literature. First, orchid pseudobulbs (i.e. swollen or thickened stems) are called "heteroblastic", when they are comprised of a single node as compared to "homoblastic", when comprised of two or more nodes (Pridgeon et al., 1999). Second, spores from unilocular sporangia of some algae may have quite different fates and develop either into gametophytes or into sporophytes, which has been called heteroblasty by Muller (1966). This variation is largely independent of abiotic conditions (Lockhart, 1979). Third, there is an analogous phenomenon among seeds, where different germination patterns are observed within seeds of the same mother plant to identical germination conditions, which has also been called "heteroblastic" (Evenari, 1963; Datta et al., 1970; Fenner, 2000). Finally, the tern1 is used when embryogeny is indirect and the offspring is dissimilar to the parent, producing the adult form as an outgrowth, as in Chara (Jackson, 1905).

Functional Significance

Goebel (1898) was the first to propose that heteroblasty is indeed adaptive and functional under current ecological conditions, a view implicitly or explicitly shared by most subsequent researchers. Heteroblasty can be seen as one possible "strategy" used by plants to cope with heterogeneous environmental conditions similar to, e.g., phenotypic plasticity (which includes heterophylly) or polymorphism (Lloyd, 1984). It is a basic assumption that heteroblasty should only evolve when there is a highly predictable difference in the abiotic or biotic conditions of "juveniles" and larger conspecifics.

Heteroblastic species include both relatively short-lived and long-lived taxa, and ecological context is likewise diverse. Not surprisingly then, we can hardly expect a single cause behind this phenomenon, which justifies the diverse and partly contradictory hypotheses put forward in the literature regarding its possible function. Moreover, since heteroblasty can be manifest in a number of different ways (e.g. habit heteroblasty, morphological changes, topic response) in phylogenetically distant plant lineages, we should expect at least some cases of heteroblasty to be functionally "neutral". Such a non-adaptive explanation is the more likely the shorter the duration of the "juvenile" phase, e.g. when many Acacia species retain the ancestral compound habit in the first few plastochrons. Conversely, the longer a particular phase lasts the less likely it seems that it is not under selection under current ecological conditions.

Light and Carbon Gain

In forests, the light conditions experienced by trees, vines and lianas during ontogeny may vary substantially from deepest shade in the understory during the "juvenile" state to full sun light after reaching the forest canopy. While in the majority of plants phenotypic plasticity allows an adaptive response to such predictable changes in abiotic conditions (Valladares & Niinemets, 2008), heteroblasty may be an alternative possibility. For example, Day (1998) suggested that heteroblasty found in many tree species in New Zealand has evolved in response to such changes in light intensity. However, the evidence she presented was only indirect, e.g. morphological and anatomical resemblance of "juvenile" leaves to shade leaves (Cameron, 1970; Gould, 1993; Day et al., 1997). The only direct experimental test of this notion, with "juveniles" of 4 homoblastic and heteroblastic species pairs, failed to detect an advantage of heteroblastic species (Gamage & Jesson, 2007). Unfortunately, adult forms were not included in this experiment. Hence, it is not ruled out that heteroblasty is as adaptive a response as phenotypic plasticity to varying light conditions during ontogeny.

Some climbing aroids, e.g. Monstera sp. or Syngonium sp., are among the most conspicuous examples of heteroblastic changes in morphology among plants (Ray, 1990; Lee & Richards, 1991). Possible functional significance is usually assumed to be related to the factor light, with important differences to tree species due to their growth habit. While tree saplings invest in own stem and branches, "juveniles" of climbing plants depend on structural support from other plants for further access to the canopy. Contact can be achieved by skototropism, i.e. growth towards the shade (Strong & Ray, 1975). Once a trunk is reached, there is a switch to positively phototropic growth. This phenomenon is little studied, but suggests a change in tropic response during ontogeny in addition to any morphological variation. In Syngonium, plants may go through several cycles of rosettes and prostate, skototropic shoots until a trunk is encountered (Ray, 1987), highlighting the search function of "juvenile" morphology.

Although "juvenile" forms are assumed to be "adapted to the extreme shade conditions to which the plants are exposed in nature" (Lee & Richards, 1991), there is little quantitative evidence to back up this statement. To our knowledge there is a single physiological study with Hedera helix which shows that "juvenile" foliage resembles shade leaves, while leaves from adult plants resemble sun leaves in a common garden experiment (Bauer & Bauer, 1980). Other evidence is at odds with the notion of improved light capture efficiency by "juvenile" leaves. The "shingle leaves" produced by many "juvenile" vines (e.g. Monstera, but also various dicotyledonous climbers; Lee & Richards, 1991), which grow closely attached to tree trunks, intercept much less radiation then horizontally exposed leaves, which leads to a reduction of potential carbon gain of almost 50% (Oberbauer & Noudali, 1998). Alternative explanations for the "adaptive value" of this leaf type still await experimental scrutiny. Since ontogenetic development usually coincides with changes in abiotic conditions, only experimental work will allow us to differentiate between intrinsic and extrinsic reasons for the observed changes. Unfortunately, such studies are also rare for vines, although a large number of suggestions for such experiments were made by Lee & Richards (1991) almost 20 years ago. One of the few exceptions is a study by Lee (1988), although he investigated the response of homoblastic species to varying light quality.

Differences in photosynthetic capacity between early and late leaf forms show no consistent trend in heteroblastic woody species, early forms may show higher (Kubien et al., 2007), similar (Hansen & Steig, 1993) or lower (Bauer & Bauer, 1980) rates of net photosynthesis. On the other hand, the compound leaves of "juvenile" acacias have a consistently higher rate of photosynthesis per unit of photosynthetic investment, which arguably maximises growth during the seedling phase, while the phyllodes of later stages are physiologically superior under water stress and high irradiance (Brodribb & Hill, 1993; Hansen & Steig, 1993; Hansen, 1996; Yu & Li, 2007, Pasquet-Kok et al., 2010). This suggests an ontogenetic strategy shift.

Nutrients

Goebel already suggested a causal relationship between nutrient supply and heteroblasty, a notion that was also supported by others (e.g. Allsopp, 1965). However, the link between differences in nutrient supply and variation in plant morphology and physiology is a rather general one (Lambers et al., 2008), and no longer discussed as the proximal cause of the ontogenetic changes dealt with in this review. On the other hand, many cases of heteroblasty may have substantial consequences for the nutrient economy of such a plant. For example, the transition from atmospheric juvenile to tank form in epiphytic bromeliads should improve the supply of essential nutrients substantially from "pulse supply" in atmospheric forms to "continuous supply" (sensu Benzing, 1990) in plants with impounding structures. In an analogous way, the humus-collecting fronds of larger Platycerium or Drynaria individuals allow these canopy-dwelling ferns to obtain more nutrients, while juveniles only feature green fronds (Goebel, 1913). Here, a similar argument can be used as for heteroblastic bromeliads, i.e. that small 'juvenile" fronds are very inefficient in capturing debris, which does not permit to pay back the structural investment, thus selecting for an alternative strategy. Finally, heteroblasty is also observed in a few carnivorous plant species, a mode of existence also associated with nutrient-poor situations. In contrast to epiphytic plants, carnivorous leaves are only developed during the early phase in these species, e.g. the tropical woody liana Triphyophyllum peltatum, where young plants produce a series of lanceolate leaves which alternate with a few glandular filiform carnivorous leaves (Green et al., 1979). Barthlott et al. (1987) reasoned that nutrient supply is probably improved and may be crucial for successful establishment.

Water Relations

Heteroblasty is quite common among tillandsioids in the family Bromeliaceae (Fig. 1, Benzing, 2000). In these plants, there is a conspicuous and abrupt shift from "juveniles" with the morphological characteristics of atmospherics (i.e. plants possessing non-impounding rosettes of small, linear leaves, which are densely covered with foliar trichomes) to larger conspecifics with tanks (i.e. featuring broad leaves, which overlap basally forming water-filled chambers). All these characteristics are related to plant water relations, which are known to be of most critical importance in the epiphytic habitat (Zotz & Hietz, 2001). Noteworthy, there are species with the atmospheric habit throughout their lifetime, which are typically found in more arid (micro-)environments, e.g. in drier forests or in the outer canopy of moister forests such as Tillandsia recurvata or T. flexuosa, which from early on led researchers to believe that the early atmospheric stage is primarily an adaptation to drought (Schulz, 1930). This interpretation agreed with the results of experimental work with heteroblastic Tillandsia deppeana (Adams & Martin, 1986a, b), and those of a quantitative assessment of tank water relations in two other, homoblastic species (Zotz & Thomas, 1999): the efficiency of tanks to bridge rainless periods decreases in smaller plants, suggesting that the observed morphological change represents a strategy shift from drought-tolerant "juvenile" to drought-avoiding tank form. However, the already mentioned study with another heterohlastic species (Werauhia sanguinolenta) suggested that a simple comparison of small atmospheric and large tanks confounds the effects of heteroblasty with those of ontogenetic drift (Fig. 3, Schmidt & Zotz, 2001; Zotz et al., 2004).

Future studies should not only avoid the previously used typological approach in the study of heteroblasty, but also consider alternative hypotheses. The exclusive focus on water stress as the only selective factor ignores that many heteroblastic bromeliad species occur in the understory of moist and wet forests, compare, e.g., Vriesea heliconioides, Werauhia lutheri, or Guzmania musaica. In these situations, light may be similarly or even more limiting than water supply, which suggests that heteroblasty in such species may primarily reduce self-shading in "juveniles".

[FIGURE 3 OMITTED]

Water stress has also been invoked as selective factor in heteroblasty of ground-rooted heteroblastic species in New Zealand (McGlone & Webb, 1981). A direct test, however, did not support this hypothesis: using pressure-volume curves, Darrow et al. (2002) found no consistent differences in plant water relations parameters between early and late stage of heteroblastic species. Noteworthy, this study was one of the few in which a homoblastic species was included to control for ontogenetic drift.

Herbivory

A possible function of heteroblasty in the defence against herbivores and pathogens has been invoked repeatedly (e.g. Greenwood & Atkinson, 1977; Givnish et al., 1994). A few studies are available which compared secondary compounds between "juvenile" and "adult" leaves of a number of heteroblastic species (e.g. Li et al., 1995; Hansen et al., 2004; Gras et al., 2005), but they failed to demonstrate major differences. Direct bioassays, on the other hand, repeatedly revealed significant effects of different leaf types of a given species on the performance of herbivorous insects (Karban & Thaler, 1999; Brennan et al., 2001). However, care should be taken to ascribe different effects of early and later leaves of a species to heteroblasty itself, since ontogenetic changes in leaf structure and leaf chemical composition are quite common in plants in general (Boege & Marquis, 2005) and the findings may thus well be due to ontogenetic drift (see discussion on the function of heteroblasty in bromeliads). Much attention has been given recently to a proposed co-evolution of herbivorous birds and heteroblastic plant species on some oceanic islands (Wood et al., 2008; Burns & Dawson, 2009; Fadzly et al., 2009). This suggestion seems particularly attractive because the proposed causal agents for the peculiar morphology of divaricate shrubs, i.e. New Zealand's Moa, Madagascar's elephant birds, or Polynesia's flightless geese (Bond et al., 2004; Bond & Silander, 2007), are now all extinct, and thus the case has a whiff of mystery ("Moas ghost", Diamond, 1990). Not surprisingly, the issue is hotly debated (McGlone & Clarkson, 1993; Howell et al., 2002).

Other Proximate Explanations

Ontogenetic changes in leaf form may be functionally related to the climbing habit. For example, in Triphyophyllum peltatum the leaves of older and larger plants, which are climbing into the forest canopy, are not only different in shape compared to those of smaller, self-supporting conspecifics, but feature a tip with two distinctive hooks with an obvious function in this liana (McPherson, 2008).

Darrow et al. (2001) suggested that tree seedlings and sapling were subjected to more frequent incidents of frost close to the ground. However, an experimental test with several hetero- and homoblastic species yielded no consistent support for this notion. There are a range of additional suggestions put forward in the literature (e.g. direct action of strong wind), which are discussed by McGlone & Clarkson (1993) and Howell et al. (2002).

Does Heteroblasty have an Adaptive Value Under Current Conditions?

The previous five sections reviewed the literature in regard to possible adaptive functions of heteroblastic changes under current ecological conditions. Clearly, unambiguous evidence for extant function is scarce, which does not mean, however, that the adaptionist approach failed (Gould & Lewontin, 1979). We argue that the search for function is appropriate, although a single functional explanation for all cases of heteroblasty is unlikely. As suggested above, even in a closely related group of plants such as the Tillandsioideae, heteroblasty may have completely different functional implications, e.g. for species in the understory or at exposed growing sites. Thus, an excellent understanding of natural history is needed to develop appropriate hypotheses for different groups of heteroblastic species. Since experiments frequently do not control for ontogenetic drift, crucial experiments are still to be conducted before we can accept the notion that heteroblasty may be neutral under current ecological conditions.

Molecular Control of Leaf Development--of Genes and Hormones

Excellent compilations of the morphological changes for a large number of heteroblastic species are available in the older literature (Goebel, 1898; Diels, 1906; Allsopp, 1965). In these early publications one already finds suggestions for the proximal physiological causes of heteroblastic changes. For example, Goebel (1913) hypothesized that carbohydrate deficiency results in the production of juvenile leaves, while others favoured the notion that low levels of nutrient supply were responsible for their formation (e.g. Allsopp, 1965). Since the findings of other studies were clearly at odds with these scenarios (e.g. Njoku, 1957), these earlier notions are rarely considered any more as a general explanation. There were also reports about a correlation of ontogenetic phase and genome DNA content in Hedera helix (Kessler & Reches, 1977), but subsequent studies suggest that the claim was based on artefacts caused by methodological problems (Greilhuber, 1998). In contrast, the involvement of particular plant hormones in heteroblastic changes, which was also demonstrated rather early for gibberellic acid (GA, Robbins, 1957), is well established: the application of GA may lead to a reversal from "adult" to "juvenile" morphology, although this artificial" rejuvenation" (Doorenbos, 1954) has only been demonstrated for a few taxa such as Hedera helix or Acacia melanoxylon (Robbins, 1957; Borchert, 1965). Not surprisingly, other hormones are involved as well (e.g. Rogler & Hackett, 1975).

Modern approaches try to understand the link between gene expression, hormonal action, and morphogenesis. However, none of the species routinely used to study the genetic framework of morphological changes is heteroblastic in the strict sense. The eudicot model plants Arabidopsis thaliana (thale cress) and Antirrhinum majus (snapdragon), but also the monocot Zea mays (corn) are mainly popular because of the availability of rich sources of mutants affected by developmental control genes. All three progress from juvenile to reproductive phase without major morphological changes except for internode elongation in the case of A. thaliana, and minor and gradual changes in leaf morphology.

Is there a Model Plant for the Study of the Genetics of Heteroblasty?

Studying the induction of heteroblasty and the regulatory cascades involved in the morphological changes associated with heteroblasty requires an organism that undergoes the ontogenetic changes described in the previous paragraphs. However, finding an organism that can serve as a genetic model system for the study of heteroblasty is rather difficult in practical terms. Ideally, genetic model organisms have a short generation time, a small genome, are amenable to genetic transformation, and can be easily grown in large amounts. Moreover, for the useful model systems, sufficient genome or transcriptome sequence information is available and a mutant collection has been set up. Unfortunately, most heteroblastic plant species are quite the opposite of a perfect model organism: many are woody species, such as eucalypts and acacias with a generation time of many years, and their genomes are largely uncharacterized. The same is true for many heteroblastic forbs, e.g. epiphytic bromeliads.

Eucalyptus grandis (flooded gum or rose gum) is a species that displays characteristics of heteroblasty as abrupt change from juvenile (ovate) to adult leaf morphology (lanceolate) (Boland et al., 1984). Moreover, E. grandis is of major economic value as it is one of the most widely grown hardwood trees in the tropics and subtropics. Its genome is currently being sequenced, several EST sequencing projects are under way and a substantial number of quantitative trait loci (QTL) have been mapped onto the genome (Grattapaglia & Kirst, 2008; Novaes et al., 2008; Rengel et al., 2009), and a transformation and regeneration protocol has been established (Tournier et al., 2003). The already established resources and tools for molecular biologists allow the use of E. grandis as a possible model organism for heteroblasty.

The well-characterized model plant Arabidopsis thaliana traverses with rather moderate morphological changes from a juvenile life phase characterized by rosette leaves and very short internodes to the reproductive phase. In this phase, leaf shape changes into the cauline form, internodes stretch, and the shoot apical meristem converts into an inflorescence meristem giving rise to inflorescences instead of leaves. Work with A. thaliana may thus help to analyze more abrupt and dramatic changes in morphology, assuming similar molecular regulation in other species. Several aspects of phyllotaxy and leaf development such as size determinants, polarity, and lobe formation have been studied in detail. These key aspects of the molecular principles of leaf development in A. thaliana and other well-studied species such as Zea mays allow at least a few general conclusions about the development in heteroblastic species.

Control of Leaf Morphogenesis--Evidence from Homoblastic Species

Phyllotaxy and Leaf Initiation

It is well established that the regular patterns in leaf initiation (phyllotaxy) are due to localized maxima of the plant hormone auxin in the SAM (Reinhardt et al., 2003). These auxin gradients are established by the action of PINFORMEDI (PIN1), a polar auxin efflux carrier localized in the cell wall of cells constituting the outer layer of the SAM. PIN1 localization at the SAM periphery allows auxin to accumulate and to promote leaf primordium formation. The new primordium subsequently acts as auxin sink, which yields a patterning mechanism for the proliferating SAM and defines the mode of phyllotaxy. Interestingly, auxin mutants in A. thaliana do not show phyllotactic changes suggesting that additional signalling cascades are involved in phyllotaxy.

A remarkable maize mutant, aberrant phyllotaxy1 (abph1) displays a decussate phyllotactic pattern (leaves are paired at 180[degrees] and the following leaf pair develops at a 90[degrees] angle) while wild type maize develops as distichous (alternating leaf initiation) plants. ABPH1 encodes a cytokinin-inducible response regulator and the abph1 mutant is impaired in the crosstalk between the two hormones auxin and cytokinin shedding light on the importance of cytokinin in addition to auxin in the regulation of phyllotactic patterning (Giulini et al., 2004; Lee et al., 2009). We hypothesize that a sudden change in the phyllotaxy, which is quite conspicuous, e.g., in heteroblastic Eucalyptus species (Fig. 1), could be simply achieved by modulating the crosstalk between cytokinin and auxin. Conversion from distichous to decussate phyllotaxy could thus result from differential regulation of homologs of the ABPH1 gene in heteroblastic species. Clearly, this hypothesis requires a general conservation of the molecular mechanism underlying phyllotactic patterning in angiosperms, an evolutionary aspect of plant development that has received little attention so far.

Control of Leaf Size--When to Stop Growing

While final size of leaves within most plant species is quite uniform, many heteroblastic species, e.g. the well studied Pseudopanax crassifolius (Clearwater & Gould, 1994), produce leaves that differ substantially in size and shape during different stages of individual development (Fig. 1). Again, understanding changes in the molecular control of rather subtle morphological changes during life phase changes of genetic model plants could be a first step to unravel the genetic processes that shape heteroblastic taxa.

Phytohormones of various classes influence organ growth in plants, e.g. plants insensitive to ethylene produce larger organs. Conversely, mutants in genes involved in auxin or brassinosteroid perception and biosynthesis are dwarfed. While auxins and brassinosteroids stimulate cell proliferation as well as cell expansion, cytokinins promote only cell proliferation but not expansion (Guzman & Ecker, 1990; Haubrick & Assmann, 2006; Sakakibara, 2006; Teale et al., 2006). Extensive cross-talk occurs between these plant hormones, for example auxin, cytokinins and brassinosteroids increase the expression of ethylene biosynthesis genes (Lin et al., 2009).

Most leaves grow first by cell proliferation and then by cell elongation once the leaf axes are established. Over the past few years, the genetic framework of leaf size control has been partially revealed when several genes involved in this process were identified (Krizek, 2009). However, most of these genes influence the timing rather than the rate of proliferation suggesting that the transition from proliferation to expansion is the crucial point in organ-size control (Anastasiou et al., 2007). The transcription factor AINTEGUMENTA (ANT) is one of the major genes promoting growth by maintaining cells in a proliferating state and is linked to auxin action, but additional genes contribute as well. Mutants in these growth-promoting genes exhibit smaller organs, jagged organ shape, or smaller narrower leaves (Mizukami & Fischer, 2000; Dinneny et al., 2004). The transition from proliferative to expansive growth is characterized by a wave of cell-cycle arrest starting from the distal and moving towards the proximal part of the leaf. TCP (TEOSINTE BRANCHED1/ CYCLOIDEA/PDF) genes most likely control this process while another set of genes induces cell cycle arrest in progenitors of stomata and vascular tissue (Nath et al., 2003; White, 2006).

A wealth of genes seems to control the size of leaves in A. thaliana including genes required for cell cycle maintenance, genes encoding transcription factors, a gene encoding a mobile signal, as well as genes involved in phytohormone signalling (Krizek, 2009). Most of the genes known to regulate leaf size do not interact genetically suggesting that leaf size is dependent upon the concerted and well-balanced action of many pathways rather than on a single master switch inducing or repressing further growth. Similarly complex regulation of leaf size might be implemented in other plants as well. Heteroblastic plants developing leaves of substantially different size during their life time may thus draw from a rather large pool of pathways to regulate the final size of their leaves. Since different species probably regulate the same process in a different way, the rather detailed understanding of the molecular control of leaf size in A. thaliana yields only limited insights into analogous processes in heteroblastic species.

Regulation of Leaf Shape

Leaf shape changes dramatically in some heteroblastic species. The perforated leaf blades of the "adult" foliage of many Monstera species (Fig. 1) result from developmentally regulated programmed cell death (PCD), which is a rather exceptional way of achieving complex leaf shape in the plant kingdom (Gunawardena et al., 2005), and thus deviates from most other cases of heteroblastic changes in leaf shape, a classic example being Hedera helix that produces lobed leaves as "juvenile" and entire leaves as "adult". The "normal", PCD independent molecular determinants of leaf shape, in particular leaf dissection, have been analyzed in A. thaliana and other, phylogenetically distant, plants with diverse modes of leaf margin dissection, leaflet specification, and leaflet development. Compound leaves generally maintain meristematic regions at their margins which enable organogenesis of leaflets.

The organogenic activity at the leaf margins is preserved by two different pathways in seed plants which possibly reflects multiple independent origins of compound leaves. While in Pisum sativum (pea) the transcription factor UNIFOLIATA (UN1) is required for organogenic regions at leaf margins, plants such as Solanum lycopersicum (tomato) and Cardamine hirsuta employ class 1 homeodomain transcription factors to achieve activity of these organogenic regions (Hay & Tsiantis, 2006; Champagne et al., 2007). However, a universally conserved molecular framework required for leaf dissection and leaflet formation seems to emerge from the analysis of S. lycopersicum, P. sativum, C. hirsuta, and Aquilegia, an early branching eudicot. It seems that the NAM/CUC3 genes are required for leaf dissection and leaflet formation in compound leaves in all the above mentioned species as they pattern the interleaflet boundary (Blein et al., 2008). As the phylogenetic range of the plants shown to employ the NAM/CUC3-1ike genes for specifying interleaflet boundary extends from early branching eudicots to rosids and asterids, it can be assumed that heteroblastic taxa that develop simple and dissected leaves during their lifetime (e.g. Hedera) might use the same switch to turn on their leaf dissection program, by simply activating the NAM/CUC3 pathway in the very early stages of leaf development. This regulatory potential could be achieved during evolution if the promoter of the NAM/CUC3-1ike genes in heteroblastic species acquired a regulatory element active in a specific life phase only. When inactive, this would lead to simple leaves and when active e. g. in the "adult" phase of a heteroblastic species, dissected leaves would be generated by the action of NAM/CUC3-1ike genes.

Evolutionary Implications

Goebel (1913) already noted that heteroblastic changes may shed light on evolutionary relationships among species. A classic example are phyllodineous Acacia species, where the compound leaves of juveniles are seen as an evolutionary legacy of an ancient, leaf-bearing progenitor (Kaplan, 1980; Gardner et al., 2008). Many other and less well-known examples exist, e.g. among some fern groups (Kato & Setoguchi, 1999) or in the Maloideae (Phipps et al., 1991). Inclusion of "juvenile" forms is also useful in chemotaxonomy (Li et al., 1995). In many other cases, the resemblance of "adults" of closely related species with the early forms of heteroblastic species is interpreted as indications of neoteny. This is the case for atmospheric species in the tillandsioids (Tomlinson, 1970), aroid vines such as Monstera tuberculata, which produces only saucer-shaped leaves throughout their life time (Lee & Richards, 1991), life-long carnivorous plants as descendents of species, in which carnivory was originally restricted to the early stages of ontogeny as in a few extant species (Barthlott et al., 1987), or divaricate shrubs that may have arisen from heteroblastic trees after losing the original adult state (Day, 1998). Alternatively, heteroblastic species may be the result of hybridization events. Godley (1985) proposed that at least some heteroblastic species may have arisen in this manner, one example being heteroblastic Pittosporum turneri as the hybrid between a divaricating shrub (P. divaricatum) and a non-divaricating tree (P. colensoi). A recent study using both molecular and morphological methods provided some support for this notion, but overall the results were inconclusive (Carrodus, 2009).

Our understanding of the evolution of heteroblasty would certainly benefit substantially from a consensus of a quantitative definition of heteroblasty. This would enable us to make broad-scale correlative analyses of heteroblasty, ecological conditions, and phylogenetic relatedness. Crayn et al.'s (2004) work is a good example for the power of this type of analysis. They compared the occurrence of crassulacean acid metabolism (CAM) and epiphytism among bromeliads in a phylogenetic context. They were able to show that both CAM and epiphytism have evolved multiple times within the family, and that both arose independently. The analogous question, i.e. how often heteroblasty has evolved within this family and whether there is a connection with the transition from terrestrial life style to epiphytism cannot be addressed at the moment. Even in smaller taxa, our understanding of the evolution of heteroblasty is quite limited. An analysis of the phylogeny of the 12 species in the small genus Pseudopanax did not yield sufficient resolution to reconstruct the evolution of heteroblasty in this genus (Petrie & Shepherd, 2009).

Similarly important for evolutionary considerations would be a better understanding of the molecular mechanisms causing heteroblastic changes. As heteroblasty has evolved many times independently in the plant kingdom it is parsimonious to assume that already existing regulatory networks have been adopted and modified, rather than supposing the de-novo generation of developmental programs. Candidate genes for changing the mode of phyllotaxy, the size or the shape of leaves could be identified and used to manipulate morphogenesis in genetic model plants. Possibly, life-phase dependent control of networks directing differential modes of developmental programs could play a major role for the evolution of heteroblasty. For the animal kingdom, such an adoption of pre-existing control elements and layering of new elements onto already existing ones to create new developmental patterns has been just recently demonstrated (Wemer et al., 2010)

Even plant species with subtle morphological changes between life phases traverse through at least two different developmental programs, the vegetative and reproductive phase. The shoot apical meristem active during vegetative development acquires inflorescence and, later, floral meristem fate. In Arabidopsis, these meristem identity shifts are induced by the differential expression of only a handful of genes, such as LEAFY conferring inflorescence meristem identity and APETALA 1 required for floral meristem identity (Sablowski, 2007). In heteroblastic species, a similarly simple genetic switch may be sufficient for transition between vegetative stages.

Strategy shifts, e.g. from "pulse-supplied" juveniles in epiphytic bromeliads to "continuously supplied" later stages (sensu Benzing, 2000) lend themselves to quantitative modelling exercises in the framework of life history theory: quite a few studies have dealt with the question of the optimal size and/or age for metamorphosis in animals (Hentschel, 1999; Rudolf & Rodel, 2007). The same logic could be applied to heteroblastic plants: for example, when is the optimal time for a small bromeliad to switch to tank form? Can the transitional stage, which may last for several months (Zotz, 2004) be considered a life history bottleneck? Plasticity in the timing of heteroblastic changes could also be exploited in experiments because the timing of the change from "juvenile" to "adult" form normally shows considerable variation. This approach was used by Burns (2005) in a study with heteroblastic Senecio lautus. He hypothesized that heteroblasty was related to shade and high winds in this species, and indeed, the juvenile-adult transition was slowed in shaded conditions. Care must be taken, however, to distinguish between changes in the timing of a switch between leaf types and the response of individual leaves (Jones, 1995).

Outlook

Heteroblastic species offer fascinating research opportunities for the study of general ecological and evolutionary questions concerning developmental regulations, plant adaptation and speciation. Unfortunately, the terminology of ontogenetic changes in plants has developed in a very inconsistent way in the last decades, which quite likely reflects a similar confusion of concepts. For further progress in the field it seems essential to clearly distinguish the step changes observed in heteroblastic species from both (gradual) ontogenetic changes in form and function that are associated with increases in size (i.e. ontogenetic drift and allometric changes) and those associated with a (similarly abrupt) phase change. Conceptual clarity is a prerequisite for an increased understanding of the developmental, functional, and evolutionary dimensions of a phenomenon that has attracted scientific attention for more than a century. Currently, we are not even able to provide a rough estimate of the number of heteroblastic plants in the plant kingdom, in contrast to other "peculiar" groups such as carnivorous plants, parasitic plants, or plants with crassulacean acid metabolism. We hope that this review will help to change this situation.

Appendix I

A diverse body of literature that deals with heteroblasty has accumulated over the last 100 or so years. Unfortunately, the older literature is hardly covered in data bases such as WOS, in part because quite a few contributions were made in monographs, in dissertations, or in journals, which are not indexed. Other studies are not readily accessible due to terminological confusion. To assist in future research we have done an extensive literature search and compiled the following list of research articles, books and book chapters that deal with heteroblasty. Also included is a selection of general textbooks, which provide different definitions of "heteroblasty", "heterophylly" and/or "phase change".

Abedon, B. G., R. D. Hatfield, & W. F. Tracy. 2006. Cell wall composition in juvenile and adult leaves of maize (Zea mays L.). Journal of Agricultural and Food Chemistry 54: 3896-3900.

Adams III, W. W., & C. E. Martin. 1986. Heterophylly and its relevance to evolution within the Tillandsioideae. Selbyana 9: 121-125.

--. 1986. 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.

--. 1986. Physiological consequences of changes in life form of the Mexican epiphyte Tillandsia deppeana (Bromeliaceae). Oecologia 70: 298-304.

Allsopp, A. 1952. Experimental and analytical studies of Pteridophytes 17. The effect of various physiologically active substances on the development of Marsilea in sterile culture. Annals of Botany 16: 165-185.

--. 1953. Experimental and analytical studies of Pteridophytes 19. Investigations on Marsilea. 2. Induced reversion to juvenile stages. Annals of Botany 17: 37-55.

--. 1953. Experimental and analytical studies of Pteridophytes 21. Investigations on Marsilea. 3. The effect of various sugars on development and morphology. Annals of Botany 17: 447-463.

--. 1954. Experimental and analytical studies of pteridophytes. 24. Investigations on Marsilea. 4. Anatomical effects of changes in sugar concentration. Annals of Botany 18: 449-461.

--. 1954. Juvenile stages of plants and the nutritional status of the shoot apex. Nature 173: 1032-1035.

--. 1964. Shoot morphogenesis. Annual Review of Plant Physiology 15: 225-254.

--. 1965. Heteroblastic development in cormophytes. Pp. 1172-122l. In: Ruhland, W., (ed.) Handbuch der Pflanzenphysiologie XV/1. Springer-Verlag, Heidelberg.

--. 1965. Land and water forms: physiological aspects. Pp. 1236-1255. In: Ruhland, W., (ed.) Handbuch der Pflanzenphysiologie XV/1. Springer-Verlag, Heidelberg.

Andergassen, S., & H. Bauer. 2002. Frost hardiness in the juvenile and adult life phase of ivy Hedera helix L. Plant Ecology 161: 207-213.

Andersson, S. 1989. Variation in heteroblastic succession among populations of Crepis tectorum. Nordic Journal of Botany 8: 565-573.

--. 1991. Geographical variation and genetic analysis of leaf shape in Crepis tectorum (Asteraceae). Plant Systematics and Evolution 178: 247-258.

--. 1993. Morphometric differentiation, patterns of interfertility, and the genetic basis of character evolution in Crepis tectorum (Asteraceae). Plant Systematics and Evolution 184: 27-40.

--. 1995. Differences in the genetic basis of leaf dissection between two populations of Crepis tectorum (Asteraceae). Heredity 75: 62-69.

Asai, K., N. Satoh, H. Sasaki, H. Satoh, & Y. Nagato. 2002. A rice heterochronic mutant, moril, is defective in the juvenile-adult phase change. Development 129: 265-273.

Ashby, E. 1948. Studies in the morphogenesis of leaves 2. The area, cell size and cell number of leaves of Ipomoea in relation to their position on the shoot. New Phytologist 47: 177-195.

--. 1948. Studies in the morphogenesis of leaves. 1. An essay on leaf shape. New Phytologist 47: 153-176.

--. 1950. Studies in the morphogenesis of leaves. VI. Some effects of length of day upon leaf shape in Ipomoea caerulea. New Phytologist 49: 375-387.

--, & E. Wangermann. 1950. Studies in the morphogenesis of leaves. IV. Further observations on area, cell size and cell number of leaves of Ipomoea in relation to their position on the shoot. New Phytologist 49: 23-35.

Atkinson, I. A. E., & R. M. Greenwood. 1989. Relationships between moas and plants. New Zealand Journal of Ecology 12: 67-96.

Barber, H. N. 1965. Selection in natural populations. Heredity 20: 551-572.

Barghi, N., & R. Gorenflot. 1989. A comparative study of the heteroblastic development in some species of Glycvrrhiza genus and Astragalus glycyphyllos. Annales Des Sciences Naturelles-Botanique Et Biologie Vegetale 10: 63-75.

Barton, K. E. 2007. Early ontogenetic patterns in chemical defense in Plantago (Plantaginaceae): genetic variation and trade-offs. American Journal of Botany 94: 56-66.

Battaglia, M., & J. B. Reid. 1993. Ontogenic variation in frost-resistance of Eucalyptus delegatenis Baker, R.T. Australian Journal of Botany 41: 137-141.

Bauer, H., & U. Bauer. 1980. Photosynthesis in leaves of juvenile and adult phase of ivy (Hedera helix). Physiologia Plantarum 49: 366-372.

--, & W. Thoni. 1988. Photosynthetic light acclimation in fully developed leaves of the juvenile and adult life phases of Hedera helix. Physiologia Plantarum 73: 31-37.

Beadle, C. L., D. E. McLeod, C. R. A. Turnbull, D. A. Ratkowsky, & R. McLeod. 1989. Juvenile/total foliage ratios in Eucalyptus nitens and the growth of stands and individual trees. Trees 3: 117-124.

Bell, A. D., & A. Bryan. 2008. Plant form: an illustrated guide to flowering plant morphology. Portland, Oregon, Timber Press.

Benzing, D. H., & K. M. Burt. 1970. Foliar permeability among twenty species of the Bromeliaceae. Bulletin of the Torrey Botanical Club 97: 269-279.

Berardini, T. Z., K. Bollman, H. Sun, & R. S. Poethig. 200l. Regulation of vegetative phase change in Arabidopsis thaliana by cyclophilin 40. Science 291: 2405-2407.

Bharathan, G., & N. R. Sinha. 2001. The regulation of compound leaf development. Plant Physiology 127: 1533-1538.

Bitter, G. 1897. Vergleichend-morphologische Untersuchungen fiber die Blattformen der Ranunculaceae und Umbelliferen. Flora 83: 223-303.

Bollman, K. M., M. J. Aukerman, M. Y. Park, C. Hunter, T. Z. Berardini, & R. S. Poethig. 2003. HASTY, the Arabidopsis ortholog of exportin 5/MSN5, regulates phase change and morphogenesis. Development 130: 1493-1504.

Bond, W. J., W. G. Lee, & J. M. Craine. 2004. Plant structural defences against browsing birds: a legacy of New Zealand's extinct tunas. Oikos 104: 500-508.

--, & J. A. Silander. 2007. Springs and wire plants: anachronistic defences against Madagascar's extinct elephant birds. Proceedings of the Royal Society B: Biological Sciences 274: 1985-1992.

Borchert, R. 1964. Zur Heterophyllie yon Acacia melanoxylon: Naturliche und kunstlich hervorgerufene Ruckschlage von der Folge- zur Jugendform. Beitrage zur Biologie der Pflanzen 40: 265-285.

--, 1965. Gibberellic acid and rejuvenation of apical meristems in Acacia melanoxylon. Naturwissenschaften 52: 65-66.

Bordonneau, M. 1987. Relationship between nuclear ultrastructure and heteroblastic development in Marsilea vestita. Cytobios 51: 135-143.

Boyarina, N. 2010. Late Gzhelian pteridosperms with callipterid foliage of the Donets Basin, Ukraine. Acta Palaeontologica Polonica 55: 343-359.

Brand, M. H., & R. D. Lineberger. 1992. In vitro rejuvenation of Betula (Betulaceae): biochemical evaluation. American Journal of Botany 79: 626-635.

--. 1992. In vitro rejuvenation of Betula (Betulaceae): morphological evaluation. American Journal of Botany 79: 618-625.

Brennan, E. B., & S. A. Weinbaum. 2001. Stylet penetration and survival of three psyllid species on adult leaves and 'waxy' and 'de-waxed' juvenile leaves of Eucalyptus globulus. Entomologia Experimentalis Et Applicata 100: 355-363.

--, --., J. A. Rosenheim, & R. Karban. 2001. Heteroblasty in Eucalyptus globulus (Myricales: Myricaceae) affects ovipositonal and settling preferences of Ctenarytaina eucalypti and C. spatulata (Homoptera : Psyllidae). Environmental Entomology 30: 1144-1149.

Bright, K. L., & M. D. Rausher. 2008. Natural selection on a leaf-shape polymorphism in the ivyleaf morning glory (Ipomoea hederacea). Evolution 62: 1978-1990.

Brink, R. A. 1962. Phase change in higher plants and somatic cell heredity. Quarterly Review of Biology 37: 1-22.

Brodribb, T., & R. S. Hill. 1993. A physiological comparison of leaves and phyllodes in Acacia melanoxylon. Australian Journal of Botany 41: 293-305.

Bruck, D. K., & D. R. Kaplan. 1980. Heterophyllic development in Muehlenbeckia (Polygonaceae). American Journal of Botany 67: 337-346.

Burns, K. C. 2005. Plastic heteroblasty in beach groundsel (Senecio lautus). New Zealand Journal of Botany 43: 665-672.

--, & S. Beaumont. 2009. Scale-dependent trait correlations in a temperate tree community. Austral Ecology 34: 670-677.

--, & J. W. Dawson. 2006. A morphological comparison of leaf heteroblasty between New Caledonia and New Zealand. New Zealand Journal of Botany 44: 387-396.

--, --. 2009. Heteroblasty on Chatham Island: A comparison with New Zealand and New Caledonia. New Zealand Journal of Ecology 33: 156-163.

Cameron, R. J. 1970. Light intensity and growth of Eucalyptus seedlings. 1. Ontogenetic variation in E. fastigata. Australian Journal of Botany 18: 29-43.

Carrodus, S. K. 2009. Identification and the role of hybridisation in New Zealand Pittosporum. Master thesis, Hamilton, New Zealand, The University of Waikato: 161 pages.

Cassells, A. C., & P. B. Gahan. 2006. Dictionary of plant tissue culture. New York, Food Products Press, an Imprint of the Haworth Press Inc.

Cevahir, G., S. Yentur, M. Yazgan, M. Unal, & N. Yilmazer. 2004. Peroxidase activity in relation to anthocyanin and chlorophyll content in juvenile and adult leaves of "mini-star" Gazania splendens. Pakistan Journal of Botany 36: 603-609.

Chalmers, P. 1992. The adaptive significance of juvenile versus adult leaves in Eucalyptus globulus ssp. globulus. Unpublished Honours Thesis, Hobart, University of Tasmania.

Christianson, M. L., & J. A. Jernstedt. 2009. Reproductive short-shoots of Ginkgo biloba: A quantitative analysis of the disposition of axillary structures. American Journal of Botany 96: 1957-1966.

Chua, Y. L., S. Channeliere, E. Mott, & J. C. Gray. 2005. The bromodomain protein GTE6 controls leaf development in Arabidopsis by histone acetylation at ASYMMETRIC LEAVES1. Genes & Development 19: 2245-2254.

Clair-Maczulajtys, D., & G. Bory. 1986. Stucture et fonction des cataphylles d'Ailanthus gladulosa au cours du developpement heteroblastique. Phytomorphology 36: 367-381.

Clearwater, M. J., & K. S. Gould. 1994. Comparative leaf development of juvenile and adult Pseudopanax crassifolius. Canadian Journal of Botany 72: 658-670.

--, --. 1995. Leaf orientation and light interceptions by juvenile Pseudopanax crassifolius (Cunn.) C. Koch in a partially shaded forest environment. Oecologia 104: 363-371.

Clemens, J., R. E. Henriod, D. G. Bailey, & P. E. Jameson. 1999. Vegetative phase change in Metrosideros: Shoot and root restriction. Plant Growth Regulation 28: 207-214.

Climent, J., M. R. Chambel, R. Lopez, S. Mutke, R. Alia, & L. Gil. 2006. Population divergence for heteroblasty in the Canary Island pine (Pinus canariensis, Pinaceae). American Journal of Botany 93: 840-848.

--, F. C. E. Silva, M. R. Chambel, M. Pardos, & M. H. Almeida. 2009. Freezing injury in primary and secondary needles of Mediterranean pine species of contrasting ecological niches. Annals of Forest Science 66.

Cockayne, L. 1905. On the significance of spines in Discaria toumatou, Raoul. (Rhamnaceae). New Phytologist 4: 79-85.

--. 1912. Observations concerning evolution, derived from ecological studies in New Zealand. Transactions of the New Zealand Institute (1911) 44: 1-50.

Couderc, H. 1979. Etude des stades de jeunesse chez plusieurs especes du genre Anthyllis. Bulletin De La Societe Botanique De France-Actualites Botaniques 126: 93-98.

Couderc, M. 1979. Quelques aspects du developpement heteroblastique dans le genre Crupina DC. Bulletin De La Societe Botanique De France-Actualites Botaniques 126: 117-123.

Cushman, J. A. 1902. Studies of localized stages of growth in some common New England plants. The American Naturalist 36: 865-885.

--. 1903. Studies of localized stages in some plants of the Botanic Gardens of Harvard University. The American Naturalist 37: 243-259.

--. 1904. Localized stages in common roadside plants. The American Naturalist 38: 819-832.

Damerval, C. 1983. Study on the heteroblastic development in certain species of Medicago. Canadian Journal of Botany 61: 2212-2223.

Damerval, C., & M. Chakass. 1985. The heteroblastic development in 8 annual species of Medicago. Bulletin De La Societe Botanique De France-Actualites Botaniques 132: 19-27.

Darrow, H. E., P. Bannister, D. J. Burritt, & P. E. Jameson. 2001. The frost resistance of juvenile and adult forms of some heteroblastic New Zealand plants. New Zealand Journal of Botany 39: 355-363.

--, --, --, --. 2002. Are juvenile forms of New Zealand heteroblastic trees more resistant to water loss than their mature counterparts? New Zealand Journal of Botany 40: 313-325.

--, --, --, --. 2004. Are juvenile forms of New Zealand heteroblastic trees more resistant to water loss than their mature counterparts? (vol 40, pg 313, 2002). New Zealand Journal of Botany 42: 719.

Datta, S. C., M. Evenari, & Gutterma. Y. 1970. Heteroblasty of Aegilops ovata L. Israel Journal of Botany 19: 463-483.

Day, J. S. 1998. Light conditions and the evolution of heteroblasty (and the divaricate form) in New Zealand. New Zealand Journal of Ecology 22: 43-54.

--, & K. S. Gould. 1997. Vegetative architecture of Elaeocarpus hookerianus. Periodic growth patterns in divaricating juveniles. Annals of Botany 79: 607-616.

--, --, & P. E. Jameson. 1997. Vegetative architecture of Elaeocarpus hookerianus. Transition from juvenile to adult. Annals of Botany 79: 617-624.

Dempewolf, H., & Loren H. Rieseberg. 2007. Adaptive evolution: The legacy of past giants. Current Biology 17: R773-R774.

Dengler, N. G. 1994. The influence of light on leaf development. Pp. 100-136. In: Iqbal, M., (ed.) Growth patterns in vascular plants. Dioscorides Press, Portland, Oregon, Portland, Oregon.

Deschamp, P. A., & T. J. Cooke. 1984. Causal mechanisms of leaf dimorphism in the aquatic angiosperm Callitriche heterophylla. American Journal of Botany 71: 319-329.

Diamond, J. 1990. Biological effects of ghosts. Nature 345: 769-770.

Dickinson, T. A., & J. B. Phipps. 1984. Studies in Crataegus (Rosaceae, Maloideae). IX. Short-shoot leaf heteroblasty in Crataegus crus-galli sensu lato. Canadian Journal of Botany-Revue Canadienne De Botanique 62: 1775-1780.

Diels, L. 1906. Jugendformen und Blutenreife im Pflanzenreich. Berlin, Borntraeger.

Diggle, P. K. 1999. Heteroblasty and the evolution of flowering phenologies. International Journal of Plant Sciences 160: S123-S134.

--, 2002. A developmental morphologist's perspective on plasticity. Evolutionary Ecology 16: 267-283.

Doorenbos, J. 1954. Rejuventation of Hedera helix in graft combinations. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series C 57: 99-102.

--, 1965. Juvenile and adult phases in woody plants. Pp. 1222-1235. In: Ruhland, W., (ed.) Handbuch der Pflanzenphysiologie XV/1. Springer-Verlag, Heidelberg.

Dutkowski, G. W., B. M. Potts, D. R. Williams, P. D. Kube, & C. McArthur. 2001. Geographic genetic variation in Central Victorian Eucalyptus nitens. Developing the Eucalypt of the Future, Valdivia, Chile.

Ebbers, M. J. H., I. R. Wallis, S. Dury, R. Floyd, & W. J. Foley. 2002. Spectrometric prediction of secondary metabolites and nitrogen in fresh Eucalyptus foliage: towards remote sensing of the nutritional quality of foliage for leaf-eating marsupials. Australian Journal of Botany 50: 761-768.

Eckenwalder, J. E. 1980. Foliar heteromorphism in Populus (Salicaceae), a source of confusion in the taxonomy of tertiary leaf remains. Systematic Botany 5: 366-383.

Edwards, P. S. J., & A. Allsopp. 1956. The effects of changes in the inorganic nitrogen supply on the growth and development of Marsilea in aseptic culture. Journal of Experimental Botany 7: 194-202.

Fadzly, N., C. Jack, H. M. Schaefer, & K. C. Burns. 2009. Ontogenetic colour changes in an insular tree species: signalling to extinct browsing birds? New Phytologist 184: 495-501.

--, & K. C. Burns. 2010. Hiding from the ghost of herbivory past: evidence for crypsis in an insular tree species. International Journal of Plant Sciences 171: 828--833.

Farnsworth, E. J., & A. M. Ellison. 1996. Sun-shade adaptability of the red mangrove, Rhizophora mangle (Rhizophoraceae): Changes through ontogeny at several levels of biological organization. American Journal of Botany 83: 1131-1143.

Farrell, T. P., & D. H. Ashton. 1978. Population studies on Acacia melanoxylon. 1. Variation in seed and vegetative characteristics. Australian Journal of Botany 26: 365-379.

Fink, W. L. 1988. Phylogenetic analysis and the detection of ontogenetic patterns. Pp. 71-91. In: McKinney, M. L., (ed.) Heterochrony in Evolution. Plenum Press, New York.

Forster, M. A. 2008. The ecology of heteroblasty in Acacia.PhD thesis. Evolution and Ecology Research Centre, School of Biological, Earth and Environmental Sciences. Sydney, University of New South Wales: 212 pages.

--., & S. P. Bonser. 2009. Heteroblastic development and shade-avoidance in response to blue and red light signals in Acacia implexa. Photochemistry and Photobiology 85: 1375-1383.

--, --. 2009. Heteroblastic development and the optimal partitioning of traits among contrasting environments in Acacia implexa. Annals of Botany 103: 95-105.

Franck, D. H. 1976. Comparative morphology and early leaf histogenesis of adult and juvenile leaves of Darlingtonia californica and their bearing on concept of heterophylly. Botanical Gazette 137: 20-34.

Frank, H., & O. Rennet. 1956. Uber Verjungung bei Hedera helix L. Planta 47: 105-114.

Friedmann, F., & T. Cadet. 1976. Observations sur l'heterophyllie dans les iles Mascareignes. Adansonia 15: 423-440.

Frydman, V. M., & P. F. Wareing. 1973. Phase-change in Hedera helix L. 1. Gibberellin-like substances in two growth phases. Journal of Experimental Botany 24: 1131-1138.

--, --, 1973. Phase-change in Hedera helix L. 2. Possible role of roots as a source of shoot gibberellin-like substances. Journal of Experimental Botany 24: 1139-1148.

--, --, 1974. Phase-change in Hedera helix L. 3. Effects of gibberellins, abscisic-acid and growth retardants on juvenile and adult ivy. Journal of Experimental Botany 25: 420-429.

Furlani, J. 1914. Zur Heterophyllie von Hedera helix L. Osterreichische Botanische Zeitschrift 64: 153-169.

Gamage, H. K., & L. Jesson. 2007. Leaf heteroblasty is not an adaptation to shade: seedling anatomical and physiological responses to light. New Zealand Journal of Ecology 31: 245-254.

Gardner, S., A. Drinnan, E. Newbigin, & P. Ladiges. 2008. Leaf ontogeny and morphology in Acacia Mill. (Mimosaceae). Muelleria 26: 43-50.

Gaudet, J. J., & R. K. Malenky. 1967. Changes in shoot apex during early development of fern Marsilea vestita. Nature 213: 945-946.

Gaume, L., & B. Di Giusto. 2009. Adaptive significance and ontogenetic variability of the waxy zone in Nepenthes rafflesiana. Annals of Botany 104: 1281-1291.

Gerrath, J. M., & C. R. Lacroix. 1997. Heteroblastic sequence and leaf development in Leea guineensis. International Journal of Plant Sciences 158: 747-756.

Givnish, T. J, & G. J. Vermeij. 1976. Sizes and shapes of liane leaves. American Naturalist 110: 743-778.

--, K. J. Sytsma, J. F. Smith, & W. J. Hahn. 1994. Thorn-Like Prickles and Heterophylly in Cyanea-Adaptations to Extinct Avian Browsers on Hawaii. Proceedings of the National Academy of Sciences of the United States of America 91: 2810-2814.

Godley, E. J. 1985. Paths to maturity. New Zealand Journal of Botany 23: 687-706.

Goebel, K. 1889. Ueber die Jugendzustande der Pflanzen. Flora 72: 1-44.

--. 1896. Uber die Jugendformen yon Pflanzen und deren kunstliche Wiederhervorrufung. Sitzungsberichte der Bayerischen Akademie der Wissenschaften zu Munchen, Mathematisch-Physikalische Klasse 26: 447-497.

--. 1898. Organography of plants, part 1. Oxford, Clarendon Press.

--. 1913. Organographie der Pflanzen. 1. Teil: Allgemeine Organographie. Jena, Gustav Fischer.

Goodin, J. R. 1965. Anatomical changes associated with juvenile-to-mature growth phase transition in Hedera. Nature 208: 504-505.

--, & Stoutemy.Vt. 1961. Effect of temperature and potassium gibberellate on phases of growth of algerian ivy. Nature 192: 677-678.

Gorenflot, R. 1979. Homoblastie et heteroblastie chez les Plantains. Bulletin De La Societe Botanique De France-Actualites Botaniques 126: 111-116.

Gould, K. S. 1993. Leaf heteroblasty in Pseudopanax crassifolius: Functional significance of leaf morphology and anatomy. Annals of Botany 71: 61-70.

Gras, E. K., J. Read, C. T. Mach, G. D. Sanson, & F. J. Clissold. 2005. Herbivore damage, resource richness and putative defences in juvenile versus adult Eucalyptus leaves. Australian Journal of Botany 53: 33-44.

Greenwood, M. S. 1984. Phase-change in loblolly pine: Shoot development as a function of age. Physiologia Plantarum 61: 518-522.

Greenwood, R. M., & I. A. E. Atkinson. 1977. Evolution of divaricating plants in New Zealand in relation to moa browsing. Proceedings of the New Zealand 24: 21-33.

Gregory-Wodzicki, K. M. 2000. Relationships between leaf morphology and climate, Bolivia: implications for estimating paleoclimate from fossil floras. Paleobiology 26: 668-688.

Greilhuber, J. 1998. Intraspecific variation in genome size: A critical reassessment. Annals of Botany 82: 27-35.

Greyson, R. I., D. B. Walden, & W. J. Smith. 1982. Leaf and stem heteroblasty in Zea. Botanical Gazette 143: 73-78.

Groom, P. K., B. B. Lamont, & L. Kupsky. 1994. Contrasting morphology and ecophysiology of coocurring broad and terete leaves in Hakea trifurcata (Proteaceae). Australian Journal of Botany 42: 605-605.

Guern, M., & J.-P. Briane. 1979. Polyploidie et developpement heteroblastique chez l'Hippocrepis comosa L. Bulletin De La Societe Botanique De France-Actualites Botaniques 126: 125-132.

Guerrant, E. O., jr. 1988. Heterochrony in plants the intersection of evolution, ecology and ontogeny. Pp. 111-133. In: McKinney, M. L., (ed.) Heterochrony in evolution: a multidisciplinary approach. Plenum Press, New York.

Gunawardena, A. H. L. A. N., K. Sault, P. Donnelly, J. S. Greenwood, & N. G. Dengler. 2005. Programmed cell death and leaf morphogenesis in Monstera obliqua (Araceae). Planta 221: 607-618.

Ha, C. M., G. T. Kim, B. C. Kim, J. H. Jun, M. S. Soh, Y. Ueno, Y. Machida, H. Tsukaya, & H. G. Nam. 2003. The BLADE-ON-PETIOLE I gene controls leaf pattern formation through the modulation of meristematic activity in Arabidopsis. Development 130: 161-172.

Hackett, W. P. 1976. Control of phase change in woody plants ISHS Acta Horticulturae 56: 143-154.

--. 1985. Juvenility, maturation and rejuvenation in woody plants. Horticultural Reviews 7: 109-155.

Hall, B. K. 2007. Keywords and concepts in evolutionary developmental biology. New Delhi, Discovery Publishing House.

Hansen, D., & E. Steig. 1993. Comparison of water-use efficiency and internal leaf carbon-dioxide concentration in juvenile leaves and phyllodes of Acacia koa (Leguminosae) from Hawaii, estimated by 2 methods. American Journal of Botany 80: 1121-1125.

Hansen, D. H. 1986. Water relations of compound leaves and phyllodes in Acacia koa var. latifolia. Plant Cell and Environment 9: 439-445.

--. 1996. Establishment and persistence characteristics in juvenile leaves and phyllodes of Acacia koa (Leguminosae) in Hawaii. International Journal of Plant Sciences 157: 123-128.

Hansen, I., L. Brimer, & P. Molgaard. 2004. Herbivore-deterring secondary compounds in heterophyllous woody species of the Mascarene Islands. Perspectives in Plant Ecology Evolution and Systematics 6: 187-203.

Heenan, P. B. 1997. Heteroblasty in Carmichaelia, Chordospartium, Corallospartium, and Notospartium (Fabaceae Galegeae) from New Zealand. New Zealand Journal of Botany 35: 243-249.

Hentsehel, B. T. 1999. Complex life cycles in a variable environment: Predicting when the timing of metamorphosis shifts from resource dependent to developmentally fixed. American Naturalist 154: 549-558.

Hietz, P., & W. Wanek. 2003. Size-dependent variation of carbon and nitrogen isotope abundances in epiphytic bromeliads. Plant Biology 5: 137-142.

Hill, J. P., & E. M. Lord. 1990. A method for determining plastochron indexes during heteroblastic shoot growth. American Journal of Botany 77: 1491-1497.

Hooker, J. D. 1853. Introductory essay to the New Zealand flora. Reeve.

Horrell, B. A., P. E. Jameson, & P. Bannister. 1989. Growth promotion of Ivy (Hedera helix L) by paclobutrazol. Plant Growth Regulation 8: 309-314.

--, --, --. 1989. Response of juvenile Pseudopanax crassifolius to gibberellic acid and paclobutrazol. New Zealand Journal of Botany 27: 591-594.

--, --, --. 1990. Growth regulation and phase change in some New Zealand heteroblastic plants. New Zealand Journal of Botany 28: 187-193.

--, --, --. 1990. Responses of Ivy (Hedera helix L.) to combinations of gibberellic acid, paclobutrazol and abscisic acid. Plant Growth Regulation 9: 107-117.

Hou, G. C., & J. P. Hill. 2002. Heteroblastic root development in Ceratopteris richardii (Parkeriaceae). International Journal of Plant Sciences 163: 341-351.

Howell, C. J., D. Kelly, & M. H. Turnbull. 2002. Moa ghosts exorcised? New Zealand's divaricate shrubs avoid photoinhibition. Functional Ecology 16: 232-240.

Jackson, B. D. 1905. A Glossary of botanic Terms, with their Derivation and Accent, Duckworth & Co.

James, A. C., & S. H. Mantell. 1994. Characterization of developmental phases of the woody perennial shrub, Solanum aviculare Forst. New Phytologist 127: 591-600.

James, S. A., & D. T. Bell. 2000. Influence of light availability on leaf structure and growth of two Eucalyptus globulus ssp globulus provenances. Tree Physiology 20: 1007-1018.

--, --. 2001. Leaf morphological and anatomical characteristics of heteroblastic Eucalyptus globulus ssp. globulus (Myrtaceae). Australian Journal of Botany 49: 259-269.

--, W. K. Smith, & T. C. Vogelmann. 1999. Ontogenetic differences in mesophyll structure and chlorophyll distribution in Eucalyptus globulus ssp. globulus (Myrtaceae). American Journal of Botany 86: 198-207.

Jay, M., & M. Coudere. 1985. Ontogeny and regulation of flavonoid biosynthesis in Crupina crupinastrum Vis. Bulletin De La Societe Botanique De France-Actualites Botaniques 132: 89-95.

Jaya, E., J. Clemens, J. C. Song, H. B. Zhang, & P. E. Jameson. 2010. Quantitative expression analysis of meristem identity genes in Eucalyptus occidentalis: AP1 is an expression marker for flowering. Tree Physiology 30: 304-312.

--, D. S. Kubien, P. E. Jameson, & J. Clemens. 2010. Vegetative phase change and photosynthesis in Eucalyptus occidentalis: architectural simplification prolongs juvenile traits. Tree Physiology 30: 393--403.

Jefferies, R. L. 1984. The phenotype: its development, physiological constraints, and environmental signals. Pp. 347-358. In: Dirzo, R., & J. Sarukhan, (eds.), Perspectives on plant population ecology Sinauer Associates Inc., Sunderland, Massachuetts.

Jones, C. S. 1992. Comparative ontogeny of a wild Cucurbit and its derived cultivar. Evolution 46: 1827-1847.

--. 1993. Heterochrony and heteroblastic leaf development in two subspecies of Cucurbita argyrosperma (Cucurbitaceae). American Journal of Botany 80: 778-795.

--. 1995. Does shade prolong juvenile development? A morphological Analysis of Leaf Shape changes in Cucurbita argyrosperma Subsp. Sororia (Cucurbitaceae). American Journal of Botany 82: 346-359.

--. 1999. An essay on juvenility, phase change, and heteroblasty in seed plants. International Journal of Plant Sciences 160: S105-S111.

--. 2001. The functional correlates of heteroblastic variation in leaves: changes in form and ecophysiology with whole plant ontogeny. Boletin de la Sociedad Argentina de Botanica 36: 171-184.

--, & M. A. Watson. 2001. Heteroblasty and preformation in mayapple, Podophyllum peltatum (Berberidaceae): Developmental flexibility and morphological constraint. American Journal of Botany 88: 1340-1358.

Jordan, G. J., B. M. Potts, P. Chalmers, & R. J. E. Wiltshire. 2000. Quantitative genetic evidence that the timing of vegetative phase change in Eucalyptus globulus ssp globulus is an adaptive trait. Australian Journal of Botany 48: 561-567.

--, --, & R. J. E. Wiltshire. 1999. Strong, independent, quantitative genetic control of the timing of vegetative phase change and first flowering in Eucalyptus globulus ssp globulus (Tasmanian Blue Gum). Heredity 83: 179-187.

Kaplan, D. R. 1980. Heteroblastic leaf development in Acacia Morphological and morphogenetic implications. La Cellule 73: 135-203.

Karban, R., & J. S. Thaler. 1999. Plant phase change and resistance to herbivory. Ecology 80: 510-517.

Kaskey, J. B., & D. R. Tindall. 1979. Physiological aspects of growth and heteroblastic development of Nasturtium officinale under natural conditions. Aquatic Botany 7: 209-229.

Kato, M., & K. Iwatsuki. 1985. Juvenile leaves and leaf ramification in Phanerosorus major (Matoniaceae). Acta Phytotaxonomica et Geobotanica 36: 139-147.

--, & H. Setoguchi. 1999. An rbcL-based phylogeny and heteroblastic leaf morphology of Matoniaceae. Systematic Botany 23: 391-400.

Kelly, D. 1994. Towards a numerical definition for divaricate (interlaced small-leaved) shrubs. New Zealand Journal of Botany 32: 509-518.

--, & M. R. Ogle. 1990. A test of the climate hypothesis for divaricate plants. New Zealand Journal of Ecology 13: 51-61.

Kerp, J. H. F. 1988. Aspects of Permian paleobotany and palynology. 10. The west European and central European species of the genus Autunia Krasser Emend Kerp (Peltaspermaceae) and the form-genus Rhachiphyllum Kerp (Callipterid Foliage). Review of Palaeobotany and Palynology 54: 249-360.

Kerstetter, R. A., & R. S. Poethig. 1998. The specification of leaf identity during shoot development. Annual Review of Cell and Developmental Biology 14: 373-398.

Kessler, B., & S. Reches. 1977. Structural and functional changes of chromosomal DNA during aging and phase change in plants. Chromosomes Today 6: 237-246.

Konig, C., I. Ebert, & J. Greilhuber. 1987. A DNA cytophotometric and chromosome banding study in Hedera helix (Araliaceae), with reference to differential DNA replication associated with juvenile-adult phase change. Genome 29: 498-503.

Krenke, N. P. 1940. Theory of cyclic ageing and rejuvenescence of plants, Moscow.

Krings, M., S. D. Klavins, T. N. Taylor, E. L. Taylor, R. Serbet, & H. Kerp. 2006. Frond architecture of Odontopteris brardii (Pteridospermopsida, ?Medullosales): new evidence from the Upper Pennsylvanian of Missouri, USA. Journal of the Torrey Botanical Society 133: 33-45.

Kubien, D. S., E. Jaya, & J. Clemens. 2007. Differences in the structure and gas exchange physiology of juvenile and adult leaves in Metrosideros excelsa. International Journal of Plant Sciences 168: 563-570.

Kunze, H. 1986. Studies on leaf metamorphosis. Beitrage zur Biologie der Pflanzen 61: 49-77.

Lambert, C., R. Buis, & M.-T. L'Hardy-Halos. 1995. Le phenomene d'heteroblastie chez les vegetaux: Comment l'expliquer? Acta Biotheoretica 43: 67-80.

Lawrence, R., B. M. Potts, & T. G. Whitham. 2003. Relative importance of plant ontogeny, host genetic variation, and leaf age for a common herbivore. Ecology 84: 1171-1178.

Lawson, E. J. R., & R. S. Poethig. 1995. Shoot development in plants: time for a change. Trends in Genetics 11: 263-268.

Le Hir, R., N. Leduc, E. Jeannette, J.-D. Viemont, & S. Pelleschi-Travier. 2005. Variations in sucrose and ABA concentrations are concomitant with heteroblastic leaf shape changes in a rhythmically growing species (Quercus robur). Tree Physiology 26: 229-238.

Lecomte, J. R., & C. J. Webb. 1981. Aciphylla townsonii--a juvenile form of Aciphylla hookeri (Umbelliferae). New Zealand Journal of Botany 19: 187-191.

Lee, D. W., & T. M. Collins. 2001. Phylogenetic and ontogenetic influences on the distribution of anthocyanins and betacyanins in leaves of tropical plants. International Journal of Plant Sciences 162: 1141-1153.

Lee, D. W., & J. H. Richards. 1991. Heteroblastic development in vines. Pp. 205-243. In: Putz, F. E., & H. A. Mooney, (eds.), The Biology of Vines. Cambridge University Press, Cambridge.

Leroy, C., & P. Heuret. 2008. Modelling changes in leaf shape prior to phyllode acquisition in Acacia mangium Willd. seedlings. Comptes Rendus Biologies 331: 127-136.

Li, H., J. L. Madden, & B. M. Potts. 1995. Variation in volatile leaf oils of the Tasmanian Eucalyptus Species. 1. Subgenus Monocalyptus. Biochemical Systematics and Ecology 23: 299-318.

--, --, --. 1996. Variation in volatile leaf oils of the Tasmanian Eucalyptus species. 2. Subgenus Symphyomyrtus. Biochemical Systematics and Ecology 24: 547-569.

--, --, --. 1997. Variation in leaf waxes of the Tasmanian Eucalyptus species. 1. Subgenus Symphyomyrtus. Biochemical Systematics and Ecology 25: 631-657.

Li, P., & M. O. Johnston. 2000. Heterochrony in plant evolutionary studies through the twentieth century. Botanical Review 66: 57-88.

Lieske, R. 1914. Die Heterophyllie epiphytischer, rosettenbildender Bromeliaceen. Jahrbuch wissenschaftlicher Botanik 53: 502-510.

Lloyd, D. G. 1984. Variation strategies of plants in heterogeneous environments. Biological Journal of the Linnean Society 21: 357-385.

Lockhart, J. C. 1979. Factors determining various forms in Cladosiphon zosterae (Phaeophyceae). American Journal of Botany 66: 836-844.

Loiseaux, S. 1968. Sur les phenomenes d'heteroblastie et de dimorphisme chez les Pheophycees. Revue Generale de Botanique 75: 229-244.

Lord, E. 1979. Development of cleistogamous and chasmogamous flowers in Lamium amplexicaule (Labiatae)--Example of heteroblastic inflorescence development. Botanical Gazette 140: 39-50.

Matos, J. A., & D. C. Rudolph (1984). Aspects of the life history of Tillandsia deppeana. 1982 World Bromeliad Conference, Corpus Christi, TX, USA, Mission Press. Pp. 71-75.

Maury, G. 1979. Interet systematique et phylogenique des caracteres juveniles (germination, embryon mur, plantules) chez les ipterocarpacees. Bulletin De La Societe Botanique De France-Actualites Botaniques 126: 13-21.

McGlone, M. S., & B. D. Clarkson. 1993. Ghost stories: Moa, plant defences and evolution in New Zealand. Tuatara 32: 1-21.

--, & C. J. Webb. 1981. Selective forces influencing the evolution of divaricating plants. New Zealand Journal of Ecology 4: 20-28.

McLellan, T. 1993. The roles of heterochrony and heteroblasty in the diversification of leaf shapes in Begonia dregei (Begoniaceae). American Journal of Botany 80: 796-804.

Medina, E. 1974. Dark C[O.sub.2] fixation, habitat preference and evolution within the Bromeliaceae. Evolution 28: 677-686.

Mehri, H., & C. J. 2002. Processus de croissance et d'organogenese chez le pommier cv Golden Delicious. Biotechnologie, Agronomie, Societe et Environnement 6: 39-49.

Melville, R. 1976. Neoteny, evolution and the New Zealand Parsonia hybrids (Apocynaceae). Botanical Journal of the Linnean Society 72: 171-189.

Merrill, E. K. 1986. Heteroblastic seedlings of green ash. I. Predictability of leaf form and primordial length. Canadian Journal of Botany 64: 2645-2649.

--. 1986. Heteroblastic seedlings of green ash. II. Early development of simple and compound leaves. Canadian Journal of Botany 64: 2650-2661.

--. 1986. Heteroblastic seedlings of green ash. III. Cell-division activity and marginal meristems. Canadian Journal of Botany 64: 2662-2668.

Mez, C. 1904. Physiologische Bromeliaceen-Studien I. Die Wasser-Okonomie der extrem atmospharischen Tillandsien. Jahrbuch wissenschaftlicher Botanik 40: 158-229.

Minorsky, P. V. 2003. The hot and the classic. Plant Physiology 133: 1671-1672.

Miriti, M. N. 2006. Ontogenetic shift from facilitation to competition in a desert shrub. Journal of Ecology 94: 973-979.

Mitchell, N. D. 1980. A study of the nutritive value of juvenile and adult leaves of Pseudopanax crassifolius. New Zealand Journal of Ecology 3: 159.

Montaldi, R., O. H. Caso, & I. J. Lewin. 1963. Algunos factores que afectan la morfologia de las hojas en una planta de desarrollo heteroblastico. Revista de Investigaciones agricolas (Buenos Aires) 17: 321-340.

Monteuuis, O., F. C. Baurens, D. K. S. Goh, M. Quimado, S. Doulbeau, & J. L. Verdeil. 2009. DNA methylation in Acacia mangium in vitro and ex-vitro buds, in relation to their within-shoot position, age and leaf morphology of the shoots. Silvae Genetica 58: 287-292.

Moose, S. P., & P. H. Sisco. 1996. Glossy 15, an APETALA2-like gene from maize that regulates leaf epidermal cell identity. Genes & Development 10: 3018-3027.

Moran, R. C. 2000. Monograph of the neotropical species of Lomariopsis (Lomariopsidaceae). Brittonia 52: 55-111.

--, & J. E. Watkins jr. 2004. Lomariopsis X farrarii: a new hybrid fern between L. japurensis and L. vestita (Lomariopsidaceae) from Costa Rica. Brittonia 56: 205-209.

Moreno-Alias, I., L. Leon, R. de la Rosa, & H. F. Rapoport. 2009. Morphological and anatomical evaluation of adult and juvenile leaves of olive plants. Trees-Structure and Function 23: 181-187.

Morren, E. 1873. Exposition de Liege. Belgique Horticole 23: 137-138.

Mueller, R. J. 1982. Shoot ontogeny and the comparative development of the heteroblastic leaf series in Lygodium japonicum (Thunb) Sw. Botanical Gazette 143: 424-438.

Mundhra, A., & N. D. Paria. 2009. Heteroblastic expression in leaves of Phyllanthus urinaria Linn. Researcher 1: 14-16.

Newton, A. E. 2007. Branching architecture in pleurocarpous mosses. Pp. 287-307. In: Newton, A. E., (ed.) Pleurocarpous mosses--Systematics and Evolution. CRC Press, Boca Raton.

Nillesen, G. A., & W. H. K. Karstens. 1955. Remarks on the morphology and anatomy of the dimorphous leaves of Marcgravia umbellata Jacq. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series C 58: 554-566.

Njoku, E. 1956. Studies in the morphogenesis of leaves XI. The effect of light intensity on leaf shape in Ipomea caerulea. New Phytologist 55: 91-110.

--. 1957. The effect of mineral nutrition and temperature on leaf shape in Ipomoea caerulea. New Phytologist 56: 154-171.

--. 1958. Effect of gibberellic acid on leaf form. Nature 182: 1097-1098.

Oberbauer, S. F., & M. Noudali. 1998. Potential carbon gain of shingle leaves in juveniles of the vine Monstera tennis (Araceae) in Costa Rica. American Journal of Botany 85: 850-854.

Obermayer, R., & J. Greilhuber. 2000. Genome size in Hedera helix L.--a clarification. Caryologia 53: 1-4.

Orkwiszewski, J. A. J., & R. S. Poethig. 2000. Phase identity of the maize leaf is determined after leaf initiation. Proceedings of the National Academy of Sciences of the United States of America 97: 10631-10636.

Pardos, M., R. Calama, & J. Climent. 2009. Difference in cuticular transpiration and sclerophylly in juvenile and adult pine needles relates to the species-specific rates of development. Trees-Structure and Function 23: 50l-508.

Pasquet-Kok, J., C. Creese, & L. Sack. 2010. Turning over a new 'leaf': multiple functional significances of leaves versus phyllodes in Hawaiian Acacia koa. Plant, Cell & Environment 33: 2084-2100.

Passecker, F. 1977. Theorie der ontogenetischen Evolution und Alterung holziger Gewachse. Bodenkultur 28: 277-294.

Petrie, L. R., & L. D. Shepherd. 2009. Reconstructing the species phylogeny of Pseudopanax (Araliaceae), a genus of hybridising trees. Molecular Phylogenetics and Evolution 52: 774-783.

Philipson, W. R. 1964. Habit in relation to age in New Zealand trees. The Journal of the Indian Botanical Society 42: 167-179.

Phipps, J. B., K. R. Robertson, J. R. Rohrer, & P. G. Smith. 1991. Origins and evolution of subfam. Maloideae (Rosaceae). Systematic Botany 16: 303-332.

Poethig, R. S. 1990. Phase change and the regulation of shoot morphogenesis in plants. Science 250: 924-930.

--. 1997. Leaf morphogenesis in flowering plants. Plant Cell 9: 1077-1087.

--. 2003. Phase change and the regulation of developmental timing in plants. Science 301: 334-336.

Polito, V. S., & V. Alliata. 1981. Growth of calluses derived from shoot apical meristems of adult and juvenile english ivy (Hedera helix L.). Plant Science Letters 22: 387-393.

Pollock, M. L., W. G. Lee, S. Walker, & G. Forrester. 2007. Ratite and ungulate preferences for woody New Zealand plants: influence of chemical and physical traits. New Zealand Journal of Ecology 31: 68-78.

Proenca, S. L., & M. d. G. Sajo. 2004. Estrutura foliar de especies de Aechmea Ruiz & Pav. (Bromeliaceae) do Estado de Sao Paulo, Brasil. Acta Botanica Brasilica 18: 319-331.

Pryer, K. M., & D. J. Hearn. 2009. Evolution of leaf form in marsileaceous ferns: evidence for heterochrony. Evolution 63: 498-513.

Rattenbury, J. A. 1962. Cyclic hybridization as a survival mechanism in New Zealand forest flora. Evolution 16: 348-363.

Ray, T. S. 1990. Metamorphosis in the Araceae. American Journal of Botany 77: 1599-1609.

Reinert, F., & S. T. Meirelles. 1993. Water acquisition strategy shifts in the heterophyllous saxicolous bromeliad, Vriesea geniculata (Wawra) Wawra. Selbyana 14: 80-88.

Richards, J. H. 1983. Heteroblastic development in the water hyacinth Eichhornia crassipes Solms. Botanical Gazette 144: 247-259.

Robbelen, G. 1957. Uber Heterophyllie bei Arabidopsis thaliana (L.) Heyn. Berichte der Deutschen Botanischen Gesellschaft 70: 39-44.

Robbins, W. J. 1957. Gibberellic acid and the reversal of adult Hedera to a juvenile state. American Journal of Botany 44: 743-746.

--. 1960. Further observations on juvenile and adult Hedera. American Journal of Botany 47: 485-491.

--., & A. Hervey. 1969. Culture of callus of Hedera canariensis, Willd. Proceedings of the National Academy of Sciences of the United States of America 63: 300-301.

Roberts, K. 2007. Handbook of plant science, Volume 1, John Wiley & Sons. Rogler, C. E., & W. P. Hackett. 1975. Phase-change in Hedera helix--Induction of mature to juvenile phase-change by Gibberellin-[A.sub.3]. Physiologia Plantarum 34: 141-147.

--, --. 1975. Phase-change in Hedera helix--Stabilization of mature form with abscisic acid and growth retardants. Physiologia Plantarum 34: 148-152.

Rothwell, G. W., & S. Warner. 1984. Cordaixylon dumusum n.sp. (Cordaitales). 1. Vegetative structures. Botanical Gazette 145: 275-291.

Rouhan, G., J. G. Hanks, D. McClelland, & R. C. Moran. 2007. Preliminary phylogenetic analysis of the fern genus Lomariopsis (Lomariopsidaceae). Brittonia 59: 115-128.

Rumball, W. 1963. Wood structure in relation to heteroblastism. Phytomorphology 13: 206-214.

Sandquist, D. R., W. S. E Schuster, L. A. Donovan, S. L. Phillips, & J. R. Ehleringer. 1993. Differences in carbon-isotope discrimination between seedlings and adults of Southwestern Desert perennial plants. Southwestern Naturalist 38: 212-217.

Scatena, V. L., S. Segecin, & A. I. Coan. 2006. Seed morphology and post-seminal development of Tillandsia L. (Bromeliaceae) from the "Campos Gerais", Parana, Southern Brazil Brazilian Archives of Biology and Technology 49: 945-951.

Schaffalitzky de Muckadell, M. 1954. Juvenile Stages in Woody Plants. Physiologia Plantarum 7: 782-796.

--. 1959. Investigations on aging of apical meristems in woody plants and its significance in silviculture. Det Forstlige Forsogsvaesen i Danmark 25: 310-455.

Schaffner, K. H., & W. Nagl. 1979. Differential DNA-replication involved in transition from juvenile to adult phase in Hedera helix (Araliaceae). Plant Systematics and Evolution Suppl. 2:105-110.

Schmidt, G., & G. Zotz. 2001. Ecophysiological consequences of differences in plant size--in situ carbon gain and water relations of the epiphytic bromeliad, Vriesea sanguinolenta. Plant, Cell and Environment 24: 101-112.

--, --. 2002. Inherently slow growth in two Caribbean epiphytic species: A demographic approach. Journal of Vegetation Science 13: 527-534.

Schulz, E. 1930. Beitrage zur physiologischen und phylogenetischen Anatomie der vegetativen Organe der Bromeliaceen. Botanisches Archiv 29: 122-209.

Sefton, C. A., K. D. Montagu, B. J. Atwell, & J. P. Conroy. 2002. Anatomical variation in juvenile eucalypt leaves accounts for differences in specific leaf area and C[O.sub.2] assimilation rates. Australian Journal of Botany 50: 301-310.

Shull, G. H. 1905. Stages in the development of Sium cicutaefolium. Carnegie Institution of Washington 30: 1-28.

Sinnott, E. W. 1960. Plant Morphogenesis. New York, McGraw-Hill Press. Sismilich, M., R. E. Henriod, P. E. Jameson, & J. Clemens. 2003. Changes in carbon isotope composition during vegetative phase change in a woody perennial plant. Plant Growth Regulation 39: 33-40.

Sparks, P. D., & S. N. Postlethwait. 1967. Comparative morphogenesis of dimorphic leaves of Cyamopsis tetragonoloba. American Journal of Botany 54: 281-285.

Stein, O. L., & E. B. Fosket. 1969. Comparative developmental anatomy of shoots juvenile and adult Hedera helix. American Journal of Botany 56: 546-551.

--, & C. M. Johnson. 1987. Comparison of shoot dynamics and early leaf ontogeny in 2 species of Saraca (Leguminosae). American Journal of Botany 74: 1492-1500.

Stephens, S. 1944. The genetic organization of leaf-shape development in the genus Gossypium. Journal of Genetics 46: 28-51.

--. 1945. Canalization of gene action in the Gossypium leaf-shape system and its bearing on certain evolutionary mechanisms. Journal of Genetics 46: 345-357.

--. 1945. A genetic survey of leaf shape in new world cottons--A problem in critical identification of alleles. Journal of Genetics 46: 313-330.

--. 1945. The modifier concept. A developmental analysis of leaf-shape 'modification' in new world cottons. Journal of Genetics 46: 331-344.

Stevens, L. G., & J. Hilton. 2009. Ontogeny and ecology of the filicalean fern Oligocarpia gothanii (Gleicheniaceae) from the Middle Permian of China. American Journal of Botany 96: 475-486.

Stoneman, G. L. 1994. Ecology and physiology of establishment of eucalypt seedlings from seed: a review. Australian Forestry 57: 11-29.

Stoutemyer, V. T., & O. K. Britt. 1961. Effect of temperature and grafting on vegetative growth phases of algerian ivy. Nature 189: 854-855.

--. 1963. Tissue cultures of juvenile and adult specimens of ivy. Nature 199: 397-98.

Strable, J., L. Borsuk, D. Nettleton, P. S. Schnable, & E. E. Irish. 2008. Microarray analysis of vegetative phase change in maize The Plant Journal 56: 1045-1057.

Sylvester, A. W., V. Parker-Clark, & G. A. Murray. 2001. Leaf shape and anatomy as indicators of phase change in the grasses: Comparison of maize, rice, and bluegrass. American Journal of Botany 88: 2157-2167.

Tanaka-Oda, A., T. Kenzo, S. Kashimura, I. Ninomiya, L. H. Wang, K. Yoshikawa, & K. Fukuda. 2010. Physiological and morphological differences in the heterophylly of Sabina vulgaris Ant. in the semi-arid environment of Mu Us Desert, Inner Mongolia, China. Journal of Arid Environments 74: 43-48.

Tomlinson, P. B. 1969. Anatomy of the monocotyledons. III. Commelinales--Zingiberales. Oxford, Oxford University Press.

--. 1970. Monocotyledons--towards an understanding of their morphology and anatomy. Advances in Botanical Research 3: 207-292.

--. 1979. Juvenilite des plantes ligneuses en Nouvelle-Zelande. Bulletin De La Societe Botanique De France-Actualites Botaniques 126: 151-154.

--. 1979. Juvenilite et neotenie chez les Monocotyledones. Bulletin De La Societe Botanique De France-Actualites Botaniques 126: 227-232.

Trippi, V. S. 1963. Studies on ontogeny and senility in plants. VI. Reversion in Acacia melanoxylon and morphogenetic changes in Gaillardia pulchella. Phyton 20: 172-174.

Troll, W. 1939. Vergleichende Morphologie der hoeheren Pflanzen. 1: Vegetationsorgane. 2. Teil. Berlin, Borntraeger.

Tsialtas, J. T., & N. Maslaris. 2007. Leaf shape and its relationship with leaf area index in a sugar beet (Beta vulgaris L.) cultivar. Photosynthetica 45: 527-532.

Tsukaya, H. 2002. The leaf index: Heteroblasty, natural variation, and the genetic control of polar processes of leaf expansion. Plant and Cell Physiology 43: 372-378.

--. 2008. Controlling size in multicellular organs: Focus on the leaf. PLoS Biology 6: e174.

--, K. Shoda, G. T. Kim, & H. Uchimiya. 2000. Heteroblasty in Arabidopsis thaliana (L.) Heynh. Planta 210: 536-542.

Usami, T., G. Horiguchi, S. Yano, & H. Tsukaya. 2009. The more and smaller cells mutants of Arabidopsis thaliana identify novel roles for SQUAMOSA PROMOTER BINDING PROTEIN-LIKE genes in the control of heteroblasty. Development 136: 955-964.

Vassal, J. 1972. Application of ontogenic and seminologic research to the morphology taxonomy and phylogeny of the genus Acacia. Bulletin De La Societe d'Histoire Naturelle de Toulouse 108: 125-247.

--. 1979. The interest of leaf ontogeny for taxonomy and phylogeny in the genus Acacia. Bulletin De La Societe Botanique De France-Actualites Botaniques 126: 55-65.

Vaughan, R. E., & P. O. Wiehe. 1939. Studies on the vegetation of Mauritius II. The effect of environment on certain features of leaf structure. Journal of Ecology 27: 263-281.

Velikova, V., F. Loreto, F. Brilli, D. Stefanov, & I. Yordanov. 2008. Characterization of juvenile and adult leaves of Eucalyptus globulus showing distinct heteroblastic development: photosynthesis and volatile isoprenoids. Plant Biology 10: 55-64.

Wagner, W. H., Jr. 1952. Juvenile leaves of Two Polypodies. American Fern Journal 42: 81-85.

--. 1957. Heteroblastic leaf morphology in juvenile plants of Dicranopteris linearis (Gleicheniaceae). Phytomorphology 7: 1-6.

Wallerstein, I., & W. P. Hackett. 1989. The effects of pulse and continuous treatments with gibberellic and triiodobenzoic acid on the growth and rejuvenation of mature-phase Hedera helix plants. Israel Journal of Botany 38: 217-227.

Waiters, G. A., & D. P. Bartholomew. 1984. Acacia koa leaves and phyllodes: gas exchange, morphological, anatomical and biochemical characteristics Botanical Gazette 145: 351-357.

Wardlaw, C. W. 1968. Morphogenesis in Plants--A Contemporary Study. London, Methuen.

Wardle, D. A. 1963. Evolution and distribution of the New Zealand flora, as affected by quaternary climates New Zealand Journal of Botany 1: 3-17.

Williams, D. R., B. M. Potts, & P. J. Smethurst. 2004. Phosphorus fertiliser can induce earlier vegetative phase change in Eucalyptus nitens. Australian Journal of Botany 52: 281-284.

Wiltshire, R. J. E., I. C. Murfet, & J. B. Reid. 1994. The genetic control of heterochrony--evidence from developmental mutants of Pisum sativum L. Journal of Evolutionary Biology 7: 447-465.

--, B. M. Potts, & J. B. Reid. 1998. Genetic control of reproductive and vegetative phase change in the Eucalyptus risdonii E. tenuiramis complex. Australian Journal of Botany 46: 45-63.

Winkler, M., K. Hulber, & P. Hietz. 2005. Effect of canopy position on germination and seedling survival of epiphytic bromeliads in a Mexican humid montane forest. Annals of Botany 95: 1039-1047.

Winn, A. A. 1996. The contributions of programmed developmental change and phenotypic plasticity to within-individual variation in leaf traits in Dicerandra linearifolia. Journal of Evolutionary Biology 9: 737-752.

--. 1999. The functional significance and fitness consequences of heterophylly. International Journal of Plant Sciences 160: Sl13-S121.

Withers, J. R. 1979. Studies on the status of unburnt Eucalyptus woodland at Ocean Grove, Victoria. IV. The effect of shading on seedling establishment. Australian Journal of Botany 27: 47-66.

Wood, J. R., N. J. Rawlence, G. M. Rogers, J. J. Austin, T. H. Worthy, & A. Cooper. 2008. Coprolite deposits reveal the diet and ecology of the extinct New Zealand megaherbivore moa (Aves, Dinornithiformes). Quaternary Science Reviews 27: 2593-2602.

Wulff, R. D. 1985. Effect of seed size on heteroblastic development in seedlings of Desmodium paniculatum. American Journal of Botany 72: 1684-1686.

Yagi, T. 2009. Ontogenetic strategy shift in sapling architecture of Fagus crenata in the dense understorey vegetation of canopy gaps created by selective cutting. Canadian Journal of Forest Research 39: 1186-1196.

Young, J. P., N. G. Dengler, P. M. Donnelly, & T. A. Dickinson. 1990. Heterophylly in Ranunculus flabellaris--the effect of abscisic acid on leaf ultrastructure. Annals of Botany 65: 603-615.

--, --, & R. F. Horton. 1987. Heterophylly in Ranunculus flabellaris--the effect of abscisic-acid on leaf anatomy. Annals of Botany 60: 117-125.

Yu, H., & J. T. Li. 2007. Physiological comparisons of true leaves and phyllodes in Acacia mangium seedlings. Photosynthetica 45: 312-316.

Zimmermann, R. H., W. P. Hackett, & R. P. Pharis. 1985. Hormonal aspects of phase change and precocious flowering. Pp. 79-115. In: Pharis, R. P., & D. M. Reid, (eds.), Hormonal Regulation of Development III Role of Environmental Factors. Springer, Berlin.

Zotz, G. 2004. Growth and survival of the early stages of the heteroblastic bromeliad, Vriesea sanguinolenta. Ecotropica 10: 51-57.

--, A. Enslin, W. Hartung, & H. Ziegler. 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 and Environment 27: 1341-1350.

Acknowledgements Of tremendous help in procuring the literature for this review were Herta Sauerbrey (Oldenburg, Germany) and Angel Aguirre (STRI, Panama). Financial support of the Deutsche Forschungsgemeinschaft (GZ ZO 94/4-1) for our current studies on heteroblasty in bromeliads is acknowledged. The Deutsche Forschungsgemeinschaft also funds ongoing research in AB's laboratory (BE 2547/7-2 and/8-1). Critical comments on an earlier draft by Dirk Albach, Oldenburg, are appreciated.

Literature Cited

Adams, W. W. & C. E. Martin. 1986a. 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.

-- & --. 1986b. Physiological consequences of changes in life form of the Mexican epiphyte Tillandsia deppeana (Bromeliaceae). Oecologia 70: 298-304.

Allsopp, A. 1965. Heteroblastic development in cormophytes. Pp. 1172-1221. In: Ruhland, W., (ed.) Handbuch der Pflanzenphysiologie XV/1. Springer-Verlag, Heidelberg.

Alpert, P. & E. L. Simms. 2002. The relative advantages of plasticity and fixity in different environments: when is it good for a plant to adjust? Evolutionary Ecology 16: 285-297.

Anastasiou, E., S. Kenz, M. Gerstung, D. MacLean, J. Timmer, C. Fleck & M. Lenhard. 2007. Control of plant organ size by KLUH/CYP78A5-dependent intercellular signaling. Developmental cell 13: 843-56.

Arber, A. 1919. On heterophylly in water plants American Naturalist 53: 272-278.

Ashby, E. 1948. Studies in the morphogenesis of leaves. 1. An essay on leaf shape. New Phytologist 47: 153-176.

Barber, H. N. 1965. Selection in natural populations. Heredity 20: 551-572.

Barthlott, W., S. Porembski, R. Seine & I. Theisen. 1987. The Curious World of Carnivorous Plants: A Comprehensive Guide to Their Biology and Cultivation. Portland, Oregon, Timber Press.

Bauer, H. & U. Bauer. 1980. Photosynthesis in leaves of juvenile and adult phase of ivy (Hedera helix). Physiologia Plantarum 49: 366-372.

Benzing, D. H. 1990. Vascular epiphytes. General biology and related biota. Cambridge, Cambridge University Press.

--. 2000. Bromeliaceae--Profile of an adaptive radiation. Cambridge, Cambridge University Press.

Blein, T., A. Pulido, A. Vialette-Guiraud, K. Nikovics, H. Morin, A. Hay, I. E. Johansen, M. Tsiantis, & P. Laufs. 2008. A conserved molecular framework for compound leaf development. Science 322: 1835-1839.

Boege, K. & R. J. Marquis. 2005. Facing herbivory as you grow up: the ontogeny of resistance in plants. Trends in Ecology & Evolution 20: 441-448.

Boland, D. J., M. I. H. Brooker, G. M. Chippendale, N. Hall, B. P. M. Hyland, R. D. Johnston, D. A. Kleinig & J. D. Turner. 1984. Forest trees of Australia. Melbourne, CSIRO.

Bond, W. J., W. G. Lee & J. M. Craine. 2004. Plant structural defences against browsing birds: a legacy of New Zealand's extinct moas. Oikos 104: 500-508.

-- & J. A. Silander. 2007. Springs and wire plants: anachronistic defences against Madagascar's extinct elephant birds. Proceedings of the Royal Society B-Biological Sciences 274: 1985-1992.

Borchert, R. 1965. Gibberellic acid and rejuvenation of apical meristems in Acacia melanoxylon. Naturwissenschaflen 52: 65-66.

Brennan, E. B., S. A. Weinbaum, J. A. Rosenheim & R. Karban. 2001. Heteroblasty in Eucalyptus globulus (Myricales: Myricaceae) affects ovipositonal and settling preferences of Ctenarytaina eucalypti and C. spatulata (Homoptera : Psyllidae). Environmental Entomology 30: 1144-1149.

Brodribb, T. & R. S. Hill. 1993. A physiological comparison of leaves and phyllodes in Acacia melanoxylon. Australian Journal of Botany 41: 293-305.

Burns, K. C. 2005. Plastic heteroblasty in beach groundsel (Senecio lautus). New Zealand Journal of Botany 43: 665-672.

-- & J. W. Dawson. 2009. Heteroblasty on Chatham Island: A comparison with New Zealand and New Caledonia. New Zealand Journal of Ecology 33: 156-163.

Cameron, R. J. 1970. Light intensity and growth of Ettcalyptus seedlings. 1. Ontogenetic variation in E. fastigata. Australian Journal of Botany 18: 29-43.

Carrodus, S. K. (2009). Identification and the role of hybridisation in New Zealand Pittosporum. MSc thesis. Hamilton, New Zealand, The University of Waikato: 161 p.

Champagne, C. E., T. E. Goliber, M. F. Wojciechowski, R. W. Mei, B. T. Townsley, K. Wang, M. M. Paz, R. Geeta & N. R. Sinha. 2007. Compoud leaf development and evolution in the legumes. Plant Cell 19: 3369-78.

Clearwater, M. J. & K. S. Gould, 1994. Comparative leaf development of juvenile and adult Pseudopanax crassifolius. Canadian Journal of Botany 72: 658-670.

Cockayne, L. 1912. Observations concerning evolution, derived from ecological studies in New Zealand. Transactions of the New Zealand Institute (1911) 44: 1-50.

Crayn, D. M., K. Winter & J. A. C. Smith, 2004. Multiple origins of crassulacean acid metabolism and the epiphytic habit in the Neotropical family Bromeliaceae. Proceedings of the National Academy of Sciences of the United States of America 101: 3703-3708.

Darrow, H. E., P. Bannister, D. J. Burritt & P. E. Jameson. 2001. The frost resistance of juvenile and adult forms of some heteroblastic New Zealand plants. New Zealand Journal of Botany 39: 355-363.

--, --, --, --. 2002. Are juvenile forms of New Zealand heteroblastic trees more resistant to water loss than their mature counterparts? New Zealand Journal of Botany 40: 313-325.

Datta, S. C., M. Evenari & Gutterma.Y. 1970. Heteroblasty of Aegilops ovata L. Israel Journal of Botany 19: 463-483.

Day, J. S. 1998. Light conditions and the evolution of heteroblasty (and the divaricate form) in New Zealand, New Zealand Journal of Ecology 22: 43-54.

--, K. S. Gould & P. E. Jameson. 1997. Vegetative architecture of Elaeocarpus hookerianus. Transition from juvenile to adult. Annals of Botany 79: 617-624.

Diamond, J. 1990. Biological effects of ghosts. Nature 345: 769-770.

Diels, L. 1906. Jugendformen und Blutenreife im Pflanzenreich. Berlin, Borntraeger.

Dinneny, J. R., R. Yadegari, R. L. Fischer, M. F. Yanofsky & D. Weigel. 2004. The role of JAGGED in shaping lateral organs. Development 131 : 1101-10.

Doorenbos, J. 1954. Rejuventation of Hedera helix in graft combinations. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, Series C 57: 99-102.

Evans, G. C. 1972. The quantitative analysis of plant growth. Berkeley, CA, University of California Press.

Evenari, M. 1963. Zur Keimungsokologie zweier Wustenpflanzen. Mitteilungen der floristischsoziologischen Arbeitsgemeinschaft, Neue Folge 10: 70-81.

Fadzly, N., C. Jack, H. M. Schaefer & K. C. Burns. 2009. Ontogenetic colour changes in an insular tree species: signalling to extinct browsing birds? New Phytologist 184: 495-501.

Fenner, M., Ed. (2000). Seeds. The Ecology of Regeneration in Plant Communities. Wallingford, UK, CABI Publishing.

Frydman, V. M. & P. F. Wareing. 1973. Phase-change in Hedera helix L. 1. Gibberellin-like substances in two growth phases. Journal of Experimental Botany 24: 1131-1138.

Gamage, H. K. & L. Jesson. 2007. Leaf heteroblasty is not an adaptation to shade: seedling anatomical and physiological responses to light. New Zealand Journal of Ecology 31: 245-254.

Gardner, S., A. Drinnan, E. Newbigin & P. Ladiges. 2008. Leaf ontogeny and morphology in Acacia Mill. (Mimosaceae). Muelleria 26: 43-50.

Giulini, A., J. Wang & D. Jackson. 2004. Control of phyllotaxy by the cytokinin-inducible response regulator homologue ABPHYL1. Nature 430: 1031-4.

Givnish, T. J., K. J. Sytsma, J. F. Smith & W. J. Hahn. 1994. Thorn-Like Prickles and Heterophylly in Cyanea--Adaptations to Extinct Avian Browsers on Hawaii. Proceedings of the National Academy of Sciences of the United States of America 91: 2810-2814.

Godley, E. J. 1985. Paths to maturity. New Zealand Journal of Botany 23: 687-706.

Goebel, K. 1889. Ueber die Jugendzustande der Pflanzen. Flora 72: 1-44.

--. 1898. Organography of plants, part 1. Oxford, Clarendon Press.

--. 1913. Organographie der Pflanzen. 1. Teil: Allgemeine Organographie. Jena, Gustav Fischer.

Gould, K. S. 1993. Leaf heteroblasty in Pseudopanax crassifolius: Functional significance of leaf morphology and anatomy. Annals of Botany 71: 61-70.

Gould, S. J. & R. C. Lewontin. 1979. The sprandrels of San Marco and the Panglossian paradigm: a critique of the adaptionist programme. Proceedings of the Royal Society of London 205: 581-598.

Gras, E. K., J. Read, C. T. Mach, G. D. Sanson & F. J. Clissold. 2005. Herbivore damage, resource richness and putative defences in juvenile versus adult Eucalyptus leaves. Australian Journal of Botany 53: 33-44.

Grattapaglia, D. & M. Kirst. 2008. Eucalyptus applied genomics: from gene sequences to breeding tools. New Phytologist 179: 911-29.

Green, S., T. L. Green & Y. Heslop-Harrison. 1979. Seasonal heterophylly and leaf gland features in Triphyophyllum (Dioncophyllaceae), a new carnivorous plant genus. Botanical Journal of the Linnean Society 78: 99-116.

Greenwood, R. M. & I. A. E. Atkinson. 1977. Evolution of divaricating plants in New Zealand in relation to moa browsing. Proceedings of the New Zealand 24: 21-33.

Greilhuber, J. 1998. Intraspecific variation in genome size: A critical reassessment. Annals of Botany 82: 27-35.

Greyson, R. I., D. B. Walden & W. J. Smith. 1982. Leaf and stem heteroblasty in Zea. Botanical Gazette 143: 73-78.

Gunawardena, A. H. L. A. N., K. Sault, P. Donnelly, J. S. Greenwood & N. G. Dengler. 2005. Programmed cell death and leaf morphogenesis in Monstera obliqua (Araceae). Planta 221: 607-618.

Guzman, P. & J. R. Ecker. 1990. Exploiting the triple response of Arabidopsis to identify ethylene-related mutants. Plant Cell 2: 513-23.

Hall, B. K. 2007. Keywords and concepts in evolutionary developmental biology. New Delhi, Discovery Publishing House.

Hansen, D. 1996. Establishment and persistence characteristics in juvenile leaves and phyllodes of Acacia koa (Leguminosae) in Hawaii. International Journal of Plant Sciences 157: 123-128.

-- & E. Steig. 1993. Comparison of water-use efficiency and internal leaf carbon-dioxide concentration in juvenile leaves and phyllodes of Acacia koa (Leguminosae) from Hawaii, estimated by 2 methods. American Journal of Botany 80: 1121-1125.

Hansen, I., L. Brimer & P. Molgaard. 2004. Herbivore-deterring secondary compounds in heterophyllous woody species of the Mascarene Islands. Perspectives in Plant Ecology Evolution and Systematics 6: 187-203.

Haubrick, L. L. & S. M. Assmann. 2006. Brassinosteroids and plant function: some clues, more puzzles. PCE 29: 446-57.

Hay, A. & M. Tsiantis. 2006. The genetic basis for differences in leaf form between Arabidopsis thaliana and its wild relative Cardamine hirsuta. Nature genetics 38: 942-7.

Hentsehel, B. T. 1999. Complex life cycles in a variable environment: Predicting when the timing of metamorphosis shifts from resource dependent to developmentally fixed. American Naturalist 154: 549-558.

Howell, C. J., D. Kelly & M. H. Turnbull. 2002. Moa ghosts exorcised? New Zealand's divaricate shrubs avoid photoinhibition. Functional Ecology 16: 232-240.

Hunter, C., M. R. Willmann, G. Wu, M. Yoshikawa, M. de la Luz Gutierrez-Nava & R. S. Poethig. 2006. Trans-acting siRNA-mediated repression of ETTIN and ARF4 regulates heteroblasty in Arabidopsis. Development 133: 2973-2981.

Jackson, B. D. 1905. A Glossary of botanic Terms, with their Derivation and Accent, Duckworth & Co.

Jaya, E., D. S. Kubien, P. E. Jameson & J. Clemens. 2010. Vegetative phase change and photosynthesis in Eucalyptus occidentalis: architectural simplification prolongs juvenile traits. Tree Physiology 30: 393-403.

Jones, C. S. 1995. Does shade prolong juvenile development? A morphological Analysis of Leaf Shape changes in Cucurbita argyrosperma Subsp. Sororia (Cucurbitaceae). American Journal of Botany 82: 346-359.

--. 1999. An essay on juvenility, phase change, and heteroblasty in seed plants. International Journal of Plant Sciences 160: SI05-S111.

--. 2001. The functional correlates of heteroblastic variation in leaves: changes in form and ecophysiology with whole plant ontogeny. Boletin de la Sociedad Argentina de Botanica 36: 17l--184.

Kaplan, D. R. 1980. Heteroblastic leaf development in Acacia--Morphological and morphogenetic implications. La Cellule 73: 135-203.

Karban, R. & J. S. Thaler. 1999. Plant phase change and resistance to herbivory. Ecology 80: 510-517.

Kato, M. & H. Setoguchi. 1999. An rbcL-based phylogeny and heteroblastic leaf morphology of Matoniaceae. Systematic Botany 23: 391-400.

Keller, R. 2004. Identification of tropical woody plants in the absence of flowers: a field guide (2nd edition), Birkhauser.

Kerstetter, R. A. & R. S. Poethig. 1998. The specification of leaf identity during shoot development. Annual Review of Cell and Developmental Biology 14: 373-398.

Kessler, B. & S. Reches. 1977. Structural and functional changes of chromosomal DNA during aging and phase change in plants. Chromosomes Today 6: 237-246.

Krizek, B. A. 2009. Making bigger plants: key regulators of final organ size. Current opinion in plant biology 12: 17-22.

Kubien, D. S., E. Jaya & J. Clemens. 2007. Differences in the structure and gas exchange physiology of juvenile and adult leaves in Metrosideros excelsa. International Journal of Plant Sciences 168: 563-570.

Lambers, H., F. S. Chapin III & T. L. Pons. 2008. Plant Physiological Ecology. New York, Springer Verlag.

Lecomte, J. R. & C. J. Webb. 1981. Aciphylla townsonii--a juvenile form of Aciphylla hookeri (Umbelliferae). New Zealand Journal of Botany 19: 187-191.

Lee, D. W. 1988. Simulating forest shade to study the developmental ecology of tropical plants: Juvenile growth in three vines in India. Journal of Tropical Ecology 4: 281-292.

-- & J. H. Richards. 1991. Heteroblastic development in vines. Pp. 205-243. In: Putz, F. E. & H. A. Mooney, (eds.), The Biology of Vines. Cambridge University Press, Cambridge.

Lee, B. H., R. Johnston, Y. Yang, A. Gallavotti, M. Kojima, B. A. Travencolo, F. Costa Lda, H. Sakakibara & D. Jackson. 2009. Studies of aberrant phyllotaxyl mutants of maize indicate complex interactions between auxin and cytokinin signaling in the shoot apical meristem. Plant Physiology 150: 205-16.

Li, P. & M. O. Johnston. 2000. Heterochrony in plant evolutionary studies through the twentieth century. Botanical Review 66: 57-88.

Li, H., J. L. Madden & B. M. Ports. 1995. Variation in volatile leaf oils of the Tasmanian Eucalyptus Species. 1. Subgenus Monocalyptus. Biochemical Systematics and Ecology 23: 299-318.

Lin, Z., S. Zhong & D. Grierson. 2009. Recent advances in ethylene research. Journal of Experimental Botany 60: 3311-36.

Lloyd, D. G. 1984. Variation strategies of plants in heterogeneous environments. Biological Journal of the Linnean Society 21: 357-385.

Lockhart, J. C. 1979. Factors determining various forms in Cladosiphon zosterae (Phaeophyceae). American Journal of Botany 66: 836-844.

Lord, E. 1979. Development of cleistogamous and chasmogamous flowers in Lamium amplexicaule (Labiatae)--Example of heteroblastic inflorescence development. Botanical Gazette 140: 39-50.

McGlone, M. S. & B. D. Clarkson. 1993. Ghost stories: Moa, plant defences and evolution in New Zealand. Tuatara 32: 1-21.

-- & C. J. Webb. 1981. Selective forces influencing the evolution of divaricating plants. New Zealand Journal of Ecology 4: 20-28.

McPherson, S. 2008. Glistening carnivores. Poole, Dorset, England, Redfem.

Mizukami, Y. & R. L. Fischer. 2000. Plant organ size control: AINTEGUMENTA regulates growth and cell numbers during organogenesis. Proceedings of the National Academy of Sciences of the United States of America 97: 942-7.

Muller, D. G. 1966. Untersuchungen zur Entwicklungsgeschichte der Braunalge Ectocarpus siliculosus aus Neapel. Planta 68: 57-68.

Nath, U., B. C. Crawford, R. Carpenter & E. Coen. 2003. Genetic control of surface curvature. Science 299: 1404-7.

Niklas, K. J. 1994. Plant allometry: the scaling of form and process. Chicago, Chicago University Press.

--. 1999. A mechanical perspective on foliage leaf form and function. New Phytologist 143: 19-31.

Njoku, E. 1957. The effect of mineral nutrition and temperature on leaf shape in Ipomoea caerulea. New Phytologist 56: 154-171.

Novaes, E., D. R. Drost, W. G. Farmerie, G. J. Pappas, Jr., D. Grattapaglia, R. R. Sederoff & M. Kirst. 2008. High-throughput gene and SNP discovery in Eucalyptus grandis, an uncharacterized genome. BMC Genomics 9: 312.

Oberbauer, S. F. & M. Noudali. 1998. Potential carbon gain of shingle leaves in juveniles of the vine Monstera tenuis (Araceae) in Costa Rica. American Journal of Botany 85: 850-854.

Pasquet-Kok, J., C. Creese & L. Sack. 2010. Turning over a new 'leaf': multiple functional significances of leaves versus phyllodes in Hawaiian Acacia koa. Plant, Cell & Environment 33: 2084-2100.

Perrie, L. R. & L. D. Shepherd. 2009. Reconstructing the species phylogeny of Pseudopanax (Araliaceae), a genus of hybridising trees. Molecular Phylogenetics and Evolution 52: 774-783.

Philipson, W. R. 1964. Habit in relation to age in New Zealand trees. The Journal of the Indian Botanical Society 42: 167-179.

Phipps, J. B., K. R. Robertson, J. R. Rohrer & P. G. Smith. 1991. Origins and evolution of subfam. Maloideae (Rosaceae). Systematic Botany 16: 303-332.

Pigliucci, M. 2001. Phenotypic plasticity: Beyond nature and nurture. Baltimore, MD, USA, Johns Hopkins University Press.

Poethig, R. S. 1990. Phase change and the regulation of shoot morphogenesis in plants. Science 250: 924-930.

--. 2003. Phase change and the regulation of developmental timing in plants. Science 301: 334-336.

Pridgeon, A., P. J. Cribb, M. W. Chase & F. N. Rasmussen, Eds. (1999). Genera Orchidacearum. Oxford, Oxford University Press.

Ray, T. S. 1987. Cyclic heterophylly in Syngonium (Araceae). American Journal of Botany 74: 16-26.

--. 1990. Metamorphosis in the Araceae. American Journal of Botany 77: 1599-1609.

Reinhardt, D., E. R. Pesce, P. Stieger, T. Mandel, K. Baltensperger, M. Bennett, J. Traas, J. Friml & C. Kuhlemeier. 2003. Regulation of phyllotaxis by polar auxin transport. Nature 426: 255-60.

Rengel, D., H. San Clemente, F. Servant, N. Ladonce, E. Panx, P. Wincker, A. Coulonx, P. Sivadon & J. Grima-Pettenati. 2009. A new genomic resource dedicated to wood formation in Eucalyptus. BMC Plant Biology 9: 36.

Robbins, W. J. 1957. Gibberellic acid and the reversal of adult Hedera to a juvenile state. American Journal of Botany 44: 743-746.

Roberts, K. 2007. Handbook of plant science, Volume 1, John Wiley & Sons.

Rogler, C. E. & W. P. Hackett. 1975. Phase-change in Hedera helix--Stabilization of mature form with abscisic acid and growth retardants. Physiologia Plantarum 34: 148-152.

Rudolf, V. H. W. & M. O. Rodel. 2007. Phenotypic plasticity and optimal timing of metamorphosis under uncertain time constraints. Evolutionary Ecology 21: 121-142.

Rumball, W. 1963. Wood structure in relation to heteroblastism. Phytomorphology 13: 206-214.

Sablowski, R. 2007. Flowering and determinacy in Arabidopsis. Journal of Experimental Botany 58: 899-907.

Sakakibara, H. 2006. Cytokinins: activity, biosynthesis, and translocation. Annual Review of Plant Biology 57: 431-49.

Schaffalitzky de Muckadell, M. 1959. Investigations on aging of apical meristems in woody plants and its significance in silviculture. Det Forstlige Forsogsvaesen i Danmark 25: 310-455.

Schmidt, G. & G. Zotz. 2001. Ecophysiological consequences of differences in plant size--in situ carbon gain and water relations of the epiphytic bromeliad, Vriesea sanguinolenta. Plant, Cell and Environment 24: 101-112.

Schulz, E. 1930. Beitrage zur physiologischen und phylogenetischen Anatomie der vegetativen Organe der Bromeliaceen. Botanisches Archiv 29: 122-209.

Strong, D. R. & T. S. Ray. 1975. Skototropism in Monstera gigantea. Science 190: 804-806.

Teale, W. D., I. A. Paponov & K. Palme. 2006. Auxin in action: signalling, transport and the control of plant growth and development. Nature reviews. Molecular cell biology 7: 847-59.

Tomlinson, P. B. 1970. Monocotyledons--towards an understanding of their morphology and anatomy. Advances in Botanical Research 3: 207-292.

Tournier, V., S. Grat, C. Marque, W. El Kayal, R. Penchel, G. de Andrade, A. M. Boudet & C. Teulieres. 2003. An efficient procedure to stably introduce genes into an economically important pulp tree (Eucalyptus grandis x Eucalyptus urophylla). Transgenic Research 12: 403-11.

Troll, W. 1939. Vergleichende Morphologie der hoeheren Pflanzen. 1: Vegetationsorgane. 2. Teih Berlin, Borntraeger.

Tsukaya, H. 2002. The leaf index: Heteroblasty, natural variation, and the genetic control of polar processes of leaf expansion. Plant and Cell Physiology 43: 372-378.

Valladares, F. & U. Niinemets. 2008. Shade tolerance, a key plant feature of complex nature and consequences. Annual Review of Ecology and Systematics 39: 237-257.

--, D. Sanchez-Gomez & M. A. Zavala. 2006. Quantitative estimation of phenotypic plasticity: bridging the gap between the evolutionary concept and its ecological applications. Journal of Ecology 94: 1103-1116.

Werner, T., S. Koshikawa, T. M. Williams & S. B. Carroll. 2010. Generation of a novel wing colour pattern by the Wingless morphogen. Nature 464: 1143-1149.

White, D. W. 2006. PEAPOD regulates lamina size and curvature in Arabidopsis. 103: 13238-43.

Williams, J. E. & J. Woinarski. 1997. Eucalypt ecology: Individuals to Ecosystems. Cambridge, Cambridge University Press.

Wiltshire, R. J. E., I. C. Murfet & J. B. Reid. 1994. The genetic control of heterochrony--evidence from developmental mutants of Pisum sativum L. Journal of Evolutionary Biology 7: 447-465.

--, B. M. Polls & J. B. Reid. 1998. Genetic control of reproductive and vegetative phase change in the Eucalyptus risdonii E. tenuiramis complex. Australian Journal of Botany 46: 45-63.

Winn, A. A. 1999. The functional significance and fitness consequences of heterophylly. International Journal of Plant Sciences 160: S113-S121.

Wood, J. R., N. J. Rawlence, G. M. Rogers, J. J. Austin, T. H. Worthy & A. Cooper. 2008. Coprolite deposits reveal the diet and ecology of the extinct New Zealand megaherbivore moa (Aves, Dinomithiformes). Quaternary Science Reviews 27: 2593-2602.

Wright, S. D. & K. D. M. McConnaughay. 2002. Interpreting phenotypic plasticity: the importance of ontogeny. Plant Species Biology 17: 119-131.

Yu, H. & J. T. Li. 2007. Physiological comparisons of true leaves and phyllodes in Acacia mangium seedlings. Photosynthetica 45: 312-316.

Zotz, G. 2004. Growth and survival of the early stages of the heteroblastic bromeliad, Vriesea sanguinolenta. Ecotropica 10: 51-57.

-- & P. Hietz. 2001. The ecophysiology of vascular epiphytes: current knowledge, open questions. Journal of Experimental Botany 52: 2067-2078.

-- & V. Thomas. 1999. How much water is in the tank? Model calculations for two epiphytic bromeliads. Annals of Botany 83: 183-192.

--, A. Enslin, W. Hartung & H. Ziegler. 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 and Environment 27: 1341-1350.

DOI 10.1007/s12229-010-9062-8

Gerhard Zotz (1,2,4) * Kerstin Wilhelm (1) * Annette Becker (3)

(1) Institut fur Biologie und Umweltwissenschaften, AG Funktionelle Okologie, Universitat Oldenburg, Postfach 2503, 261l1 Oldenburg, Germany

(2) Smithsonian Tropical Research Institute, Apdo 08343-03092, Panama, Republic of Panama

(3) Fachbereich 02, AG Evolutionare Entwicklungsgenetik der Pflanzen, Universitat Bremen, Leobener Str., UFT, 28359 Bremen, Germany

(4) Author for Correspondence; e-mail: gerhard.zotz@uni-oldenburg.de

Published online: 7 February 2011

[c] The New York Botanical Garden 2011
COPYRIGHT 2011 New York Botanical Garden
No portion of this article can be reproduced without the express written permission from the copyright holder.
Copyright 2011 Gale, Cengage Learning. All rights reserved.

Article Details
Printer friendly Cite/link Email Feedback
Author:Zotz, Gerhard; Wilhelm, Kerstin; Becker, Annette
Publication:The Botanical Review
Article Type:Report
Geographic Code:4EUGE
Date:Jun 1, 2011
Words:18606
Previous Article:Tropical and temperate: evolutionary history of paramo flora.
Next Article:Flower senescence-strategies and some associated events.
Topics:

Terms of use | Copyright © 2018 Farlex, Inc. | Feedback | For webmasters