- Email: [email protected]
Australian micro stilt plants
TREE vol. 4, no. 2, February 1989
AustralianMicroStilt Plants The diminutive ‘micro stilt plant’ life form, recently recognized in a range of taxa throughout many ecosystems of SW Australia, has been reported rarely, if at all, in other locations in or outside Australasia. The growth form itself, its phenology, and the morphological variation that its member species collectively express, present a fascinating example of convergent evolution in response to the exacting edaphic and climatic conditions of an extreme mediterranean-type environment. The stilt habit in which the mature shoot system of a plant is partly or wholly raised and supported above ground by aerial prop roots is familiar to botanists worldwide. Aborescent monocotyledons screwpines such as (Pandanaceae)’ and Lepidocaryoid or lriarteoid palms (Palmae) or dicotyledonous trees such as strangler figs (Ficus spp.) and certain mangrove+ are well-known examples. The highly distinctive nature of the stilt plant growth form has been widely recognizedd, and its functional significance alluded to in relation to the obvious supporting function of prop roots in exposed, eroded or seasonally flooded habitats. Recently a unique sub-set of stilt plants has been described5 for ecosystems in SW Australia. The species concerned are diminutive microchamaephytes, mostly under IO cm in height and with their shoot system elevated 1-2 cm above the soil surface by a set of stiff roots. This review concentrates on the taxonomy, morphogenesis and ecology of this unusual group of species. To avoid confusion with the macrophytic stilt species mentioned above, they will be referred to as ‘micro’ stilt plants. Distribution and taxonomyof micro stilt plants Micro stilt plants are found commonly in a wide variety of habitats in the heathlands and open woodlands of the mediterranean-type ecosystems (kwongan) of SW Australia. This growth form has been recorded in nine genera from three families of monocotyledons
John S. Pate and two families of dicotyledons (Table 1); most come from the genus Stylidium, which has at least 70 stilt species. Only one of the plant genera concerned (Drosera) is cosmopolitan; of the remaining eight, four are endemic to SW Australia, and the others have all or the great majority of their stiltforming species located on the western side of the continent. An exception to this rule is Romnalda grallata (Xanthorrhoeaceae), an understorey species of swampy margins of rain forest in Queensland. The stems of this species are almost entirely supported above ground by stilt-like root&; but with a mature shoot height of 30-40 ems, this species is larger than most micro stilt plants encountered in SW Australia. All but one of the genera listed in Table 1 contain non-stilt partner species with a wide variety of growth forms and life histories. For example, the genera lohnsonia, Stawellia, Conostylis, Anarthria and Hensmania have hemicryptophytic or chamaephytic (see Box I) nonstilt species represented in SW Australia, mostly of greater size than corresponding stilt forms. Laxmannia has a hemicryptophytic form in E Australia, and certain species of Borya (e.g. B. nitida and f3. sobulata) exhibit ecological races ranging from non-stilt chamaephytes with no evidence of aerial roots, through intermediate morphologies with stems pafib touching the substrate, to genuine stilt form!?. Drosera and Stybdium within SW provide examples Australia of all listed growth and life form categories - Drosera with most of its examples as stem-tuberous geophytes or non-stilt chamaephytes (see Refs 7 and 81, Stylidium with most prolific speciation as chamaephytes and therophytes5.
1989. Elsever
Science
Publishers
Table 1. Micro stilt plants currently known for SWAustralia (based pdmarity on the species surveyof Ref. 5) Family
Genus
Liliaceae
Borya Hensmania lohnsonia Laxmannia Stawellia
2 I 2 8 I
Haemodoraceae
Conostylis
5
Restionaceae
Anarthria
I
Droseraceae
Drosera
5
Stylidiaceae
Stylidiom
70+
Developmentof stilt habit and morphological variation behveen species
Establishment of micro stilt plants from seed is at first not noticeably different from that of other plant species (Fig. 11, but the seedling soon develops one or john Pate is at the Botany Dept, The University of more aerial roots from its shoot Western Australia, Nedlands, Western Australia and, with eventual senescence and 6009. decay of the original hypocotyl and 0
radicle, this aerial root system assumes sole supportive and absorptive function. Ultimately each plant acquires a complex morphology, involving seasonal additions of vegetative and reproductive shoot parts and associated stilt roots in a manner highly characteristic of the species in question. Micro stilt species differ from one another in relation to a number of morphological features (see Figs 2 and 3). All monocotyledonous species and micro stilt forms of Drosera possess essentially uniform (monomorphic) shoots with regularly spaced leaves and axillary inflorescences. Sheathing leaf bases, ligules or stipules protect the stem, and more than one adventitious root usually develops on each season’s extension of the shoot. In Stylidium both monomorphic and dimorphic shoot morphologies are encountered (Fig. 31, the latter exhibiting short shoots bearing closely spaced leaves and long shoots with widely spaced leaves. The short shoots are axillary, typically form at the end of a growing season, and extend into long shoots of the following year. Each long shoot normally develops a terminal inflorescence at the end of the season (Figs I and 3). Further variation relates to branching pattern and shoot disposition (Fig. 3). Overall habit is determined essentially by branching pattern, whether shoot growth is erect, ascending or procumbent, and whether each
Ltd (lJKl0169-5347/89/$02.00
Known no. of micro stilt spp.
4s
TREE vol. 4, no. 2, February
season’s shoot extensions are short or long. Certain micro stilt plants exhibit a tuft- or cushion-like form, erect compact others possess shoots, yet others a lax stoloniferous habit (Fig. 3). Progressive outward senescence of stoloniferous species may lead to clones being established (e.g. in Anthria polyphylla and certain species of Sty/i&urn, Conostylis and Laxmanda). In some cases (e.g. Styhdium repens) a clone may spread
a metre or more in diameter and consist of a dozen or more independent individuals at its periphery. Variations between species in leaf morphology include a range of different shapes, deciduous or non-deciduous habits, succulent or xeromorphic leaf textures, and absence or presence of seasonal dimorphy in leaf size and longevity5. Patterns of root production are species-specific, some species producing only one, others two or more aerial roots on each new shoot segment. Figures 2 and 3 provide examples of some of the more commonly found combinations of attributes, and collectively illustrate the prolific morphological diversity within the growth form.
AR(I) b’b _,
42)
Fig. 1. Early growth and subsequent seasonal development of a typical micro stilt plant. la) First-season seedling shortly after germination. C, cotyledons; R, primary root developed from radicle. fb) Early in the second (winter) growing season: an adventitious stilt root, AR( I ), is &v&ping from the current season’s shoot, Sf I ). fc) Condition during summer dormancy at the end of the second growing season. fd) Early in the third growing season: primary root now dead, a second set of stilt roots, ARf2), is forming on new shoot extensions S(2). (e) End of the fourth growing season, showing further generation of shoot extensions, S(3), and stilt roots, ARf3), and inflorescences (F) terminating the current season’s growth.
46
1989
Seasonalgrowth, reproduction and habitat requirements Because of their small size and paucity of storage reserves, the growth, flowering and seed production of micro stilt plants is tightly constrained by climatic influences within their habitats. Seasonal increments in plant dry matter commence with the onset of autumn rains, and continue through winter and spring. Growth ceases in early summer and net losses in dry weight are observed during the severe drought and heat typically experienced by SW Australian habitats through high summer to the first rains of the following autumn. Fastest rates of dry matter production occur in late spring when temperatures are still rising to an optimum, yet while soil moisture is still sufficient to maintain nearmaximal rates of transpiration and photosynthesis. This is the time when stilt plants typically produce flowers and seeds. Production of stilt roots is restricted to early winter - the only period of assured cool wet weather when root primordia are unlikely to become severely desiccated before reaching the soil surface. After penetrating the soil each new root branches and extends rapidly to depths of up to 30-50 cm. Its aerial portion becomes heavily lignified before the onset of summer. Each successive set of stilt roots persists into a second growing season, and remains physiologically active at least until the following generation of roots has acquired the capacity to absorb water and nutrients. Micro stilt plants are especially vulnerable to fire and susceptible to competition from overshadowing vegetation. They therefore tend to be most common in open habitats such as beds of gravel and fringes to rocky outcrops, seasonally inundated areas in which fire damage is unlikely, and, more generally, in open spaces in early post-fire successions of woodland or heathland. Since they establish almost exclusively in the season immediately after a fire, populations consist of similarly sized siblings whose identical age can be readily confirmed by counts of seasonal shoot increments and associated generations of stilt roots (see Fig. I I. Indeed, the micro stilt plants of an ecosystem provide a convenient
TREE vol. 4, no. 2, February
1989
means of checking the post+fire age of a particular stand of vegetation, while also providing ideal experimental material for progressively monitoring growth and phenological development in a particular habitat (see Ref. 5). Evolutionarysignificanceof the micro stilt habit The micro stilt habit may be considered as an evolutionary avenue by which diminutive, woody perennial species have become adapted to the severe drought and high surface-soil temperatures experienced during summer in open habitats of the SW Australian sandplains. This hypothesis implies that the aestivating shoot is particularly vulnerable to heat damage and that measurable benefit to a species in terms of relief from heat stress does indeed accrue from elevating a shoot 2 cm or so above the soil surface. Figure 4 depicts a typical set of temperature profiles below, at and above the surface of a light grey sand substrate during a still, sunny day in January, when micro stilt plants and other larger species in the habitat appeared to be under severe water stress. Ambient air temperatures 20 cm above the site were in the range 35-38°C over the period 10.00-l 6.00 h, compared with 46-48°C at soil surface. The zone 2-4 cm above soil surface, where shoots of the micro stilt plants in the habitat were mostly located, recorded 3642°C over the same period, suggesting a &IO”C benefit to the shoot of the plant during day time through possession of the stilt habit. Two simple experiments were carried out to test the respective tolerance limits of root and shoot to high temperatures, each conducted in separate seasons on the genera Stylidium (three species), Laxmannia (two species), Conostylis (two and lohnsonia (one species) species). The habitats concerned were white, grey or yellow sands exhibiting maximum surface temperatures in high summer within the range 45-52°C. In one experiment comparisons were made of the effect on plant growth and survival of artificially placing habitat sand around plants (ten of each species) to a level that maintained the lowest living part of
Fig. 2. Three species of S W Australian micro stilt plants, illustrating the extent of differences in morphology between representatives of different genera. (a) Drosera drummondii (Droseraceae), (b) Stykdium cygnorum (Stylidiaceaef. (cl lohnsonia pobescens Ililiaceae). Arrowheads indicate soil level in natural habitat.
the shoot precisely at soil level. Such partial burying consistently sponsored high (40-100%) mortality when plants were treated over summer (December to March), compared with less than 10% pro-
portional death in equivalent populations of control untreated plants retaining their natural stilt habit throughout the same period. By contrast, when similar treatments were carried out in the cool
Laxmannia
Stylidium scandens
Stvlidium bulbiferum
Fig. 3. Examples showing Redrawn with modifications
the range of morphological from Ref. 5.
variation
among
S W Australian
micro
stilt plants.
47
TREE vol. 4, no. 2, February
1989
“C
ABOVE -GROUND 50 I TEMFEf
1
SOIL SURFACE
plasts themselves to tolerate prolonged high temperatures must also be paramount in survival of the species.
Relationshipsbetween the micro stilt habit and other life growth forms \, AMBlENi AIR---*‘* The micro stilt habit may be (+20cm 1 7 viewed as one of three principal \ avenues through which hemicryptophytic or chamaephytic species might respond to selection pressures militating strongly against the location of small exposed plant organs at or close to hot dry soil surfaces. il i8 lb 2b 7 8 12 Ij 14 15 1e ii 9 10 11 The first alternative strategy to the stilt habit would be the adop“C tion of a geophytic habit, in which BELOW- GROUNO the cool moist months of autumn to 5o TEMPERATURE late spring are used for aboveSOIL SURFACE ground vegetative growth and reproduction and the drought of summer avoided by dying back to an underground bulb, corm or tuber. Geophytes are relatively common elements of the herbaceous component of kwongan floras (see Refs 7 and 9). Their perennating organs are normally buried 8 cm or more below the surface, thereby giving a considerable advantage in terms of lower temperatures (see Fig. 4) and 251 avoidance of water stress’. However, geophytic species inhabiting shallow lenses of soil fringing rocky 20s outcrops must locate their aestivat1 ing organs only a centimetre or so 2l 18 19 20 14 15 18 17 11 12 13 7 8 9 lo below the soil surface. In such cases TIME OF DAY (I+) the tubers become highly desicFig. 4. Daily changes in temperature at, below and above soil surface in a typical micro stilt locality on cated in summer and may even a hot dry summer’s day. Ambient air temperatures were measured 20 cm above the soil surface. assume seed-like structure and Reproduced with modifications from Ref. 5 composition’O. The second alternative is for a proportion of the species to assume an ephemeral wet growing seasons (April to a significant treated plants did survive into the habit, establishing from seed with September) no significant effect the first rains of autumn, completnext season attested to the remarkwas observed from raising the level able capacity of the stilt root to ing its growth cycle by late spring of the soil around plants. or early summer, and surviving the survive prolonged heat stress. The second experiment involved rest of the summer solely as dorUnusual anatomical characterisapplication at the beginning of mant seed. Plants of this kind are summer of a 3 mm layer of pow- tics of the roots of micro stilt plants cortex of surprisingly rare elements of SW dered charcoal around the base of include a multi-layered thick-walled sclerenchyma, and in Australian vegetation (see Ref. 91, sets of ten plants of each species. whether in terms of numbers of some species, possession of intemThis treatment did not significantly species or as proportions of bioaffect the elevated position of the ally located fintraxylary) phloem5. mass. This life form does howThese features are likely to contribshoot, but, by offering a highly absorptive surface, raised surface ute to avoidance of desiccation, but ever become dominant in the year following fire, when temperatures around the base of since most stilt roots are of very immediately large perennial vegsmall (l-3 mm) diameter and are competing the stilt roots by up to 20°C above that experienced by adjacent un- exposed to sunlight for most of the etation has been wholly or partly day, central conducting tissues will destroyed and availability of water treated soil surfaces. This treatment caused death of up to 60% of quickly reach temperatures almost and nutrients are transiently suffi‘fire weed’ the plants, compared with &lo% in as high as at the soil surface. There- cient for ephemeral controls. Nevertheless, the fact that fore the ability of the root protospecies to develop adequate bio48 r”--’
TREE vol. 4, no. 2, February
1989
mass for effective reproduction by seed”. As mentioned above, species exhibiting micro stilt, ephemeral or geophytic traits exist congeneritally in several instances within the SW Australian flora. It would be interesting to discover whether parallel examples exist within or outside the Australian continent, and, if micro stilt plants prove to be
=
unique, to determine
why they are
so rarely encountered son with other life forms.
in compariand growth
References I Halle, F., Oldeman, R.A.A. and Tomlinson, P.B. ( 1978) Tropical Trees and Forests. Springer-Vedag 2 Dransfield, 1. ( I9781 in Tropical Trees as LivingSystems (Tomlinson, P.B. and Zimmermann, M.H., edsf, Cambridge University Press 3 jenik, 1. ( 1978) in Tropical Treesas Living Systems (Tomlinson, P.B. and Zimmermann, M.H., eds), Cambridge University Press 4 Raunkiaer, C. (I 934) Life Form and Terrestrial f/ant Geography, Clarenden Press 5 Pate, j.S., Weber. G.and Dixon, K.W. (19841 in Kwongan: Plant Life of the Sandplain (Pate,f.S. and Beard,l.S., eds), pp. 12g-145,
University of Western Australia Press 6 Henderson, R.J.F. (1981) KewBull. 37, 229-235 7 Pate, J.S.and Dixon, K.W. (I 982) Tubemus, Comous and Bulbous P/ants, University of Western Australia Press 8 Marchant, N.G., Aston, H.I. and George, A.S. ( 1982) Droseraceae: Flora Australia Vol. 29, Australian Government Publishing Service 9 Pate, f.S., Dixon, K.W. and Orshan, G. f 1984) in Kwongan: Plant Life of the Sandplain fPate,j.S.and Beard,f.S.,edsl, pp.84-100, University of Western Australia Press IO Dixon, K.W., Pate, IS. and Kuo, I. II9831 Aust.I.Bot.31,85-103 I I Pate, IS., Casson, N., Rullo, 1. and Kuo, I. I 1985) Aust. J. P/ant Physiol. 12,64 l-65 I
Letters to the Editor Patternsin Food Webs A third class of theories, totally ignored along with these patterns by Lawton and Warren, go much of the way toward explaining the three patterns, as well as most of Lawton and Warren’s ten (namely: 1, 2,3, 5,7,9, 10). These theories view food web structure as the outcome of a process of assembly by sequentially arriving species, with the process constrained by energy*,s, by the requirement that predators be ‘mild specialists’ in that they tend to consume prey that are ecologically similar in a certain well defined sense (Sugihara, op. cit.; Ref. 2), or by a global version of the local LotkaVolterra dynamics discussed by Lawton and Warren (Ref. 10; J.A. Drake, PhD thesis, Purdue University, 1985). The energetic and mild specialist versions of assembly account for pattern 11 (Sugihara, op. cit.; Refs 2 and 1 I), while pattern 13 seems difficult to explain in any other way than by invoking energetic constraints7. (Indeed, this pattern was investigated specifically as an ‘acid test’ for the influence of energy in food web structure.) Pattern 12 suggests a simple tendency for predators to be specialized either on plants or on animals for their major food sources (keeping in mind how food web data have generally been arrived at). It hardly calls for explanation; rather, it explains the rarity of omnivory seen ectotherms tending to have interby some in terms of an elementary mediate production efficiencies5s6. constraint. Pattern 12 Within observed food webs, at a biological sharpens and supersedes Lawton given ‘trophic height’ and for a given pattern 5. Much has body size, a higher proportion of and Warren’s invertebrate ectotherms than of been made, in the paper by Law-ton of the vertebrate ectotherms than of en- and Warren and elsewhere, of local ‘dynamic’ Lotkadotherms ‘support a consumer’ in ability Volterra models to account for patthe sense of lying in the shortest path linking that consumer to basal tern 5 - but these models do not explain pattern 12 (Ref. 12). species’.
In a recent TREE commentary, Lawton and Warren’ review ‘static’ and ‘dynamic’ explanations for ten empirical patterns in food web structure. Curiously, they omit any mention of three further empirical patterns, which are at least as well founded as those in their list of ten, and which, as far as I am aware, have not been accounted for by either of the reviewed explanations. They are as follows. (11) Food webs are ‘rigid circuit’ more often than expected by chance (G. Sugihara, PhD thesis, Princeton University, 1982; Ref. 2). This property expresses the topology of the packing of niches in niche space. For a rigid circuit food web, niches are packed in such a way as to leave no ‘holes’ in niche space. (12) There is a simple pattern in the distribution of omnivore links within observed food webs, namely a deficit of predators that feed on both plants and animals relative to predators that feed on animals at different ‘trophic levels’. This deficit alone is more than sufficient to account for the overall ‘rarity’ of omnivores relative fpPimm’s null models3 (pattern 5 of Lawton and Warrem4. (13) Invertebrate ectotherms tend to be about an order of magnitude more efficient at energy conversion than endotherms, with vertebrate
It needs to be said as well that Lawton and Warren’s discussion of the tree hole data of Pimm and Kitching13 is misleading. It is indeed reasonable to infer from these data that ‘frequent disturbances would make it impossible for high ranking carnivores to persist in the system’. This happens to coincide with the local dynamics prediction14 that food chains should be shorter in more variable environments, but to offer it as support for that prediction is fallacious, for the following reason. The local dynamic models discussed by Lawton and Warren (which they call simply ‘dynamic’, thereby obfuscating an important distinction) deal with the phase space dynamics in an infinitesimal neighbourhood of an equilibrium of a system with a fixed number of species. As Lawton and Warren correctly report, the PimmKitching result is that ‘species feeding higher in the food chains.. . recolonized more slowly after an experimental disturbance’ (the emphasis on ‘recolonized’ is mine). The dynamics of recolonization, during which the very dimension of the system phase space changes, is not the local neighbourhood dynamics of the ‘dynamic’ models treated by Lawton and Kitching, it is the dynamics of assembly I have sketched in the preceding two paragraphs. Far from supporting the local dynamics viewpoint, the tree hole data show that environmental variability sometimes that viewpoint renders irrelevant. I heartily join in Lawton and Warren’s applause for the ‘growing interest
in gathering
more
and
better
data on food webs, and in manipulating webs experimentally’. As our data base becomes more sophisticated, 49
AustralianMicroStilt Plants The diminutive ‘micro stilt plant’ life form, recently recognized in a range of taxa throughout many ecosystems of SW Australia, has been reported rarely, if at all, in other locations in or outside Australasia. The growth form itself, its phenology, and the morphological variation that its member species collectively express, present a fascinating example of convergent evolution in response to the exacting edaphic and climatic conditions of an extreme mediterranean-type environment. The stilt habit in which the mature shoot system of a plant is partly or wholly raised and supported above ground by aerial prop roots is familiar to botanists worldwide. Aborescent monocotyledons screwpines such as (Pandanaceae)’ and Lepidocaryoid or lriarteoid palms (Palmae) or dicotyledonous trees such as strangler figs (Ficus spp.) and certain mangrove+ are well-known examples. The highly distinctive nature of the stilt plant growth form has been widely recognizedd, and its functional significance alluded to in relation to the obvious supporting function of prop roots in exposed, eroded or seasonally flooded habitats. Recently a unique sub-set of stilt plants has been described5 for ecosystems in SW Australia. The species concerned are diminutive microchamaephytes, mostly under IO cm in height and with their shoot system elevated 1-2 cm above the soil surface by a set of stiff roots. This review concentrates on the taxonomy, morphogenesis and ecology of this unusual group of species. To avoid confusion with the macrophytic stilt species mentioned above, they will be referred to as ‘micro’ stilt plants. Distribution and taxonomyof micro stilt plants Micro stilt plants are found commonly in a wide variety of habitats in the heathlands and open woodlands of the mediterranean-type ecosystems (kwongan) of SW Australia. This growth form has been recorded in nine genera from three families of monocotyledons
John S. Pate and two families of dicotyledons (Table 1); most come from the genus Stylidium, which has at least 70 stilt species. Only one of the plant genera concerned (Drosera) is cosmopolitan; of the remaining eight, four are endemic to SW Australia, and the others have all or the great majority of their stiltforming species located on the western side of the continent. An exception to this rule is Romnalda grallata (Xanthorrhoeaceae), an understorey species of swampy margins of rain forest in Queensland. The stems of this species are almost entirely supported above ground by stilt-like root&; but with a mature shoot height of 30-40 ems, this species is larger than most micro stilt plants encountered in SW Australia. All but one of the genera listed in Table 1 contain non-stilt partner species with a wide variety of growth forms and life histories. For example, the genera lohnsonia, Stawellia, Conostylis, Anarthria and Hensmania have hemicryptophytic or chamaephytic (see Box I) nonstilt species represented in SW Australia, mostly of greater size than corresponding stilt forms. Laxmannia has a hemicryptophytic form in E Australia, and certain species of Borya (e.g. B. nitida and f3. sobulata) exhibit ecological races ranging from non-stilt chamaephytes with no evidence of aerial roots, through intermediate morphologies with stems pafib touching the substrate, to genuine stilt form!?. Drosera and Stybdium within SW provide examples Australia of all listed growth and life form categories - Drosera with most of its examples as stem-tuberous geophytes or non-stilt chamaephytes (see Refs 7 and 81, Stylidium with most prolific speciation as chamaephytes and therophytes5.
1989. Elsever
Science
Publishers
Table 1. Micro stilt plants currently known for SWAustralia (based pdmarity on the species surveyof Ref. 5) Family
Genus
Liliaceae
Borya Hensmania lohnsonia Laxmannia Stawellia
2 I 2 8 I
Haemodoraceae
Conostylis
5
Restionaceae
Anarthria
I
Droseraceae
Drosera
5
Stylidiaceae
Stylidiom
70+
Developmentof stilt habit and morphological variation behveen species
Establishment of micro stilt plants from seed is at first not noticeably different from that of other plant species (Fig. 11, but the seedling soon develops one or john Pate is at the Botany Dept, The University of more aerial roots from its shoot Western Australia, Nedlands, Western Australia and, with eventual senescence and 6009. decay of the original hypocotyl and 0
radicle, this aerial root system assumes sole supportive and absorptive function. Ultimately each plant acquires a complex morphology, involving seasonal additions of vegetative and reproductive shoot parts and associated stilt roots in a manner highly characteristic of the species in question. Micro stilt species differ from one another in relation to a number of morphological features (see Figs 2 and 3). All monocotyledonous species and micro stilt forms of Drosera possess essentially uniform (monomorphic) shoots with regularly spaced leaves and axillary inflorescences. Sheathing leaf bases, ligules or stipules protect the stem, and more than one adventitious root usually develops on each season’s extension of the shoot. In Stylidium both monomorphic and dimorphic shoot morphologies are encountered (Fig. 31, the latter exhibiting short shoots bearing closely spaced leaves and long shoots with widely spaced leaves. The short shoots are axillary, typically form at the end of a growing season, and extend into long shoots of the following year. Each long shoot normally develops a terminal inflorescence at the end of the season (Figs I and 3). Further variation relates to branching pattern and shoot disposition (Fig. 3). Overall habit is determined essentially by branching pattern, whether shoot growth is erect, ascending or procumbent, and whether each
Ltd (lJKl0169-5347/89/$02.00
Known no. of micro stilt spp.
4s
TREE vol. 4, no. 2, February
season’s shoot extensions are short or long. Certain micro stilt plants exhibit a tuft- or cushion-like form, erect compact others possess shoots, yet others a lax stoloniferous habit (Fig. 3). Progressive outward senescence of stoloniferous species may lead to clones being established (e.g. in Anthria polyphylla and certain species of Sty/i&urn, Conostylis and Laxmanda). In some cases (e.g. Styhdium repens) a clone may spread
a metre or more in diameter and consist of a dozen or more independent individuals at its periphery. Variations between species in leaf morphology include a range of different shapes, deciduous or non-deciduous habits, succulent or xeromorphic leaf textures, and absence or presence of seasonal dimorphy in leaf size and longevity5. Patterns of root production are species-specific, some species producing only one, others two or more aerial roots on each new shoot segment. Figures 2 and 3 provide examples of some of the more commonly found combinations of attributes, and collectively illustrate the prolific morphological diversity within the growth form.
AR(I) b’b _,
42)
Fig. 1. Early growth and subsequent seasonal development of a typical micro stilt plant. la) First-season seedling shortly after germination. C, cotyledons; R, primary root developed from radicle. fb) Early in the second (winter) growing season: an adventitious stilt root, AR( I ), is &v&ping from the current season’s shoot, Sf I ). fc) Condition during summer dormancy at the end of the second growing season. fd) Early in the third growing season: primary root now dead, a second set of stilt roots, ARf2), is forming on new shoot extensions S(2). (e) End of the fourth growing season, showing further generation of shoot extensions, S(3), and stilt roots, ARf3), and inflorescences (F) terminating the current season’s growth.
46
1989
Seasonalgrowth, reproduction and habitat requirements Because of their small size and paucity of storage reserves, the growth, flowering and seed production of micro stilt plants is tightly constrained by climatic influences within their habitats. Seasonal increments in plant dry matter commence with the onset of autumn rains, and continue through winter and spring. Growth ceases in early summer and net losses in dry weight are observed during the severe drought and heat typically experienced by SW Australian habitats through high summer to the first rains of the following autumn. Fastest rates of dry matter production occur in late spring when temperatures are still rising to an optimum, yet while soil moisture is still sufficient to maintain nearmaximal rates of transpiration and photosynthesis. This is the time when stilt plants typically produce flowers and seeds. Production of stilt roots is restricted to early winter - the only period of assured cool wet weather when root primordia are unlikely to become severely desiccated before reaching the soil surface. After penetrating the soil each new root branches and extends rapidly to depths of up to 30-50 cm. Its aerial portion becomes heavily lignified before the onset of summer. Each successive set of stilt roots persists into a second growing season, and remains physiologically active at least until the following generation of roots has acquired the capacity to absorb water and nutrients. Micro stilt plants are especially vulnerable to fire and susceptible to competition from overshadowing vegetation. They therefore tend to be most common in open habitats such as beds of gravel and fringes to rocky outcrops, seasonally inundated areas in which fire damage is unlikely, and, more generally, in open spaces in early post-fire successions of woodland or heathland. Since they establish almost exclusively in the season immediately after a fire, populations consist of similarly sized siblings whose identical age can be readily confirmed by counts of seasonal shoot increments and associated generations of stilt roots (see Fig. I I. Indeed, the micro stilt plants of an ecosystem provide a convenient
TREE vol. 4, no. 2, February
1989
means of checking the post+fire age of a particular stand of vegetation, while also providing ideal experimental material for progressively monitoring growth and phenological development in a particular habitat (see Ref. 5). Evolutionarysignificanceof the micro stilt habit The micro stilt habit may be considered as an evolutionary avenue by which diminutive, woody perennial species have become adapted to the severe drought and high surface-soil temperatures experienced during summer in open habitats of the SW Australian sandplains. This hypothesis implies that the aestivating shoot is particularly vulnerable to heat damage and that measurable benefit to a species in terms of relief from heat stress does indeed accrue from elevating a shoot 2 cm or so above the soil surface. Figure 4 depicts a typical set of temperature profiles below, at and above the surface of a light grey sand substrate during a still, sunny day in January, when micro stilt plants and other larger species in the habitat appeared to be under severe water stress. Ambient air temperatures 20 cm above the site were in the range 35-38°C over the period 10.00-l 6.00 h, compared with 46-48°C at soil surface. The zone 2-4 cm above soil surface, where shoots of the micro stilt plants in the habitat were mostly located, recorded 3642°C over the same period, suggesting a &IO”C benefit to the shoot of the plant during day time through possession of the stilt habit. Two simple experiments were carried out to test the respective tolerance limits of root and shoot to high temperatures, each conducted in separate seasons on the genera Stylidium (three species), Laxmannia (two species), Conostylis (two and lohnsonia (one species) species). The habitats concerned were white, grey or yellow sands exhibiting maximum surface temperatures in high summer within the range 45-52°C. In one experiment comparisons were made of the effect on plant growth and survival of artificially placing habitat sand around plants (ten of each species) to a level that maintained the lowest living part of
Fig. 2. Three species of S W Australian micro stilt plants, illustrating the extent of differences in morphology between representatives of different genera. (a) Drosera drummondii (Droseraceae), (b) Stykdium cygnorum (Stylidiaceaef. (cl lohnsonia pobescens Ililiaceae). Arrowheads indicate soil level in natural habitat.
the shoot precisely at soil level. Such partial burying consistently sponsored high (40-100%) mortality when plants were treated over summer (December to March), compared with less than 10% pro-
portional death in equivalent populations of control untreated plants retaining their natural stilt habit throughout the same period. By contrast, when similar treatments were carried out in the cool
Laxmannia
Stylidium scandens
Stvlidium bulbiferum
Fig. 3. Examples showing Redrawn with modifications
the range of morphological from Ref. 5.
variation
among
S W Australian
micro
stilt plants.
47
TREE vol. 4, no. 2, February
1989
“C
ABOVE -GROUND 50 I TEMFEf
1
SOIL SURFACE
plasts themselves to tolerate prolonged high temperatures must also be paramount in survival of the species.
Relationshipsbetween the micro stilt habit and other life growth forms \, AMBlENi AIR---*‘* The micro stilt habit may be (+20cm 1 7 viewed as one of three principal \ avenues through which hemicryptophytic or chamaephytic species might respond to selection pressures militating strongly against the location of small exposed plant organs at or close to hot dry soil surfaces. il i8 lb 2b 7 8 12 Ij 14 15 1e ii 9 10 11 The first alternative strategy to the stilt habit would be the adop“C tion of a geophytic habit, in which BELOW- GROUNO the cool moist months of autumn to 5o TEMPERATURE late spring are used for aboveSOIL SURFACE ground vegetative growth and reproduction and the drought of summer avoided by dying back to an underground bulb, corm or tuber. Geophytes are relatively common elements of the herbaceous component of kwongan floras (see Refs 7 and 9). Their perennating organs are normally buried 8 cm or more below the surface, thereby giving a considerable advantage in terms of lower temperatures (see Fig. 4) and 251 avoidance of water stress’. However, geophytic species inhabiting shallow lenses of soil fringing rocky 20s outcrops must locate their aestivat1 ing organs only a centimetre or so 2l 18 19 20 14 15 18 17 11 12 13 7 8 9 lo below the soil surface. In such cases TIME OF DAY (I+) the tubers become highly desicFig. 4. Daily changes in temperature at, below and above soil surface in a typical micro stilt locality on cated in summer and may even a hot dry summer’s day. Ambient air temperatures were measured 20 cm above the soil surface. assume seed-like structure and Reproduced with modifications from Ref. 5 composition’O. The second alternative is for a proportion of the species to assume an ephemeral wet growing seasons (April to a significant treated plants did survive into the habit, establishing from seed with September) no significant effect the first rains of autumn, completnext season attested to the remarkwas observed from raising the level able capacity of the stilt root to ing its growth cycle by late spring of the soil around plants. or early summer, and surviving the survive prolonged heat stress. The second experiment involved rest of the summer solely as dorUnusual anatomical characterisapplication at the beginning of mant seed. Plants of this kind are summer of a 3 mm layer of pow- tics of the roots of micro stilt plants cortex of surprisingly rare elements of SW dered charcoal around the base of include a multi-layered thick-walled sclerenchyma, and in Australian vegetation (see Ref. 91, sets of ten plants of each species. whether in terms of numbers of some species, possession of intemThis treatment did not significantly species or as proportions of bioaffect the elevated position of the ally located fintraxylary) phloem5. mass. This life form does howThese features are likely to contribshoot, but, by offering a highly absorptive surface, raised surface ute to avoidance of desiccation, but ever become dominant in the year following fire, when temperatures around the base of since most stilt roots are of very immediately large perennial vegsmall (l-3 mm) diameter and are competing the stilt roots by up to 20°C above that experienced by adjacent un- exposed to sunlight for most of the etation has been wholly or partly day, central conducting tissues will destroyed and availability of water treated soil surfaces. This treatment caused death of up to 60% of quickly reach temperatures almost and nutrients are transiently suffi‘fire weed’ the plants, compared with &lo% in as high as at the soil surface. There- cient for ephemeral controls. Nevertheless, the fact that fore the ability of the root protospecies to develop adequate bio48 r”--’
TREE vol. 4, no. 2, February
1989
mass for effective reproduction by seed”. As mentioned above, species exhibiting micro stilt, ephemeral or geophytic traits exist congeneritally in several instances within the SW Australian flora. It would be interesting to discover whether parallel examples exist within or outside the Australian continent, and, if micro stilt plants prove to be
=
unique, to determine
why they are
so rarely encountered son with other life forms.
in compariand growth
References I Halle, F., Oldeman, R.A.A. and Tomlinson, P.B. ( 1978) Tropical Trees and Forests. Springer-Vedag 2 Dransfield, 1. ( I9781 in Tropical Trees as LivingSystems (Tomlinson, P.B. and Zimmermann, M.H., edsf, Cambridge University Press 3 jenik, 1. ( 1978) in Tropical Treesas Living Systems (Tomlinson, P.B. and Zimmermann, M.H., eds), Cambridge University Press 4 Raunkiaer, C. (I 934) Life Form and Terrestrial f/ant Geography, Clarenden Press 5 Pate, j.S., Weber. G.and Dixon, K.W. (19841 in Kwongan: Plant Life of the Sandplain (Pate,f.S. and Beard,l.S., eds), pp. 12g-145,
University of Western Australia Press 6 Henderson, R.J.F. (1981) KewBull. 37, 229-235 7 Pate, J.S.and Dixon, K.W. (I 982) Tubemus, Comous and Bulbous P/ants, University of Western Australia Press 8 Marchant, N.G., Aston, H.I. and George, A.S. ( 1982) Droseraceae: Flora Australia Vol. 29, Australian Government Publishing Service 9 Pate, f.S., Dixon, K.W. and Orshan, G. f 1984) in Kwongan: Plant Life of the Sandplain fPate,j.S.and Beard,f.S.,edsl, pp.84-100, University of Western Australia Press IO Dixon, K.W., Pate, IS. and Kuo, I. II9831 Aust.I.Bot.31,85-103 I I Pate, IS., Casson, N., Rullo, 1. and Kuo, I. I 1985) Aust. J. P/ant Physiol. 12,64 l-65 I
Letters to the Editor Patternsin Food Webs A third class of theories, totally ignored along with these patterns by Lawton and Warren, go much of the way toward explaining the three patterns, as well as most of Lawton and Warren’s ten (namely: 1, 2,3, 5,7,9, 10). These theories view food web structure as the outcome of a process of assembly by sequentially arriving species, with the process constrained by energy*,s, by the requirement that predators be ‘mild specialists’ in that they tend to consume prey that are ecologically similar in a certain well defined sense (Sugihara, op. cit.; Ref. 2), or by a global version of the local LotkaVolterra dynamics discussed by Lawton and Warren (Ref. 10; J.A. Drake, PhD thesis, Purdue University, 1985). The energetic and mild specialist versions of assembly account for pattern 11 (Sugihara, op. cit.; Refs 2 and 1 I), while pattern 13 seems difficult to explain in any other way than by invoking energetic constraints7. (Indeed, this pattern was investigated specifically as an ‘acid test’ for the influence of energy in food web structure.) Pattern 12 suggests a simple tendency for predators to be specialized either on plants or on animals for their major food sources (keeping in mind how food web data have generally been arrived at). It hardly calls for explanation; rather, it explains the rarity of omnivory seen ectotherms tending to have interby some in terms of an elementary mediate production efficiencies5s6. constraint. Pattern 12 Within observed food webs, at a biological sharpens and supersedes Lawton given ‘trophic height’ and for a given pattern 5. Much has body size, a higher proportion of and Warren’s invertebrate ectotherms than of been made, in the paper by Law-ton of the vertebrate ectotherms than of en- and Warren and elsewhere, of local ‘dynamic’ Lotkadotherms ‘support a consumer’ in ability Volterra models to account for patthe sense of lying in the shortest path linking that consumer to basal tern 5 - but these models do not explain pattern 12 (Ref. 12). species’.
In a recent TREE commentary, Lawton and Warren’ review ‘static’ and ‘dynamic’ explanations for ten empirical patterns in food web structure. Curiously, they omit any mention of three further empirical patterns, which are at least as well founded as those in their list of ten, and which, as far as I am aware, have not been accounted for by either of the reviewed explanations. They are as follows. (11) Food webs are ‘rigid circuit’ more often than expected by chance (G. Sugihara, PhD thesis, Princeton University, 1982; Ref. 2). This property expresses the topology of the packing of niches in niche space. For a rigid circuit food web, niches are packed in such a way as to leave no ‘holes’ in niche space. (12) There is a simple pattern in the distribution of omnivore links within observed food webs, namely a deficit of predators that feed on both plants and animals relative to predators that feed on animals at different ‘trophic levels’. This deficit alone is more than sufficient to account for the overall ‘rarity’ of omnivores relative fpPimm’s null models3 (pattern 5 of Lawton and Warrem4. (13) Invertebrate ectotherms tend to be about an order of magnitude more efficient at energy conversion than endotherms, with vertebrate
It needs to be said as well that Lawton and Warren’s discussion of the tree hole data of Pimm and Kitching13 is misleading. It is indeed reasonable to infer from these data that ‘frequent disturbances would make it impossible for high ranking carnivores to persist in the system’. This happens to coincide with the local dynamics prediction14 that food chains should be shorter in more variable environments, but to offer it as support for that prediction is fallacious, for the following reason. The local dynamic models discussed by Lawton and Warren (which they call simply ‘dynamic’, thereby obfuscating an important distinction) deal with the phase space dynamics in an infinitesimal neighbourhood of an equilibrium of a system with a fixed number of species. As Lawton and Warren correctly report, the PimmKitching result is that ‘species feeding higher in the food chains.. . recolonized more slowly after an experimental disturbance’ (the emphasis on ‘recolonized’ is mine). The dynamics of recolonization, during which the very dimension of the system phase space changes, is not the local neighbourhood dynamics of the ‘dynamic’ models treated by Lawton and Kitching, it is the dynamics of assembly I have sketched in the preceding two paragraphs. Far from supporting the local dynamics viewpoint, the tree hole data show that environmental variability sometimes that viewpoint renders irrelevant. I heartily join in Lawton and Warren’s applause for the ‘growing interest
in gathering
more
and
better
data on food webs, and in manipulating webs experimentally’. As our data base becomes more sophisticated, 49