TABLE 2.1 (continued)
Desiccation Tolerance of Isolated Chloroplasts and of Poikilohydrous Autotrophs3
C. intrepidus, floating leaves
C. intrepidus, submersed leaves
Craterostigma (2 species)
Limosella grandiflora (corms)
Poaceae from India (10 species)
Southern African Poaceae (11 species)
Poaceae from Africa and Kenya (5 species)
Trilepis pilosa (African Inselberg)
Australian Poaceae (6 species) Australian Cyperaceae
(4 species) Southern African
Cyperaceae (4 species) Cyperaceae from Africa and Kenya (3 species) Australian Liliaceae (2 species) Borya nitida Xerophyta squarrosa Xerophyta scabrida Xerophyta (5 species) Velloziaceae from Africa and Kenya (2 species)
Degree of Desiccation Survived
18% of initial weight
0-2 (11)% rh 0%-5% rh 0%—15% rh 8% RWC Air-dry 0%—15% rh 0%—15% rh 0%-2% rh
Mature leaf tissues: 5%-30% rh
Time of Drought Survived
2 days 6-12 months Until equilibrium 10 months Until equilibrium 4.5 months Until equilibrium
4.5 months (but both species decayed at 100% rh) Leaves (several year)
3 months 2-7 months Until equilibrium Up to 1 year
Until equilibrium Until equilibrium Until equilibrium
>4 year 5 year 5 year
Markowska et al. 1994 Kappen 1966 Markowska et al. 1994 Gaff and Latz 1978 Heil 1925 Gaff 1971 Gaff 1971 Gaff 1971
Gaff and Giess 1986
Ziegler and Vieweg 1969,
Gaff 1971 Barthlott and Porembski 1996
Gaff and Bole 1986 Gaff and Ellis 1974 Gaff and Latz 1978 Hambler 1961 Gaff 1977 Gaff 1971 Gaff and Latz 1978 Gaff and Latz 1978
Gaff and Ellis 1975
Gaff and Latz 1978 Gaff and Churchill 1976 Gaff 1971
Abbreviation: RWC, relative water content; d.wt., dry weight; rh, relative humidity; until equilibrium, until equilibrium between moisture content and ambient air relative humidity.
a The list in this table is not exhaustive.
hydrophytes (c.940 spp.) are included. Among the land plants, we know nearly 90 species of pteridophytes and approximately 350 of the angiosperms (Gaff 1989, Proctor and Tuba 2002). Within the angiosperms only 10 families have to be taken into account, the Myrothamnaceae, Cactaceae, Acanthaceae, Gesneriaceae, Scrophulariaceae, and Lamiaceae (contributing in total only 35 dicotyledonous species), and the Cyperaceae, Boryaceae (sensu Lazerides 1992), Poaceae, and Velloziaceae (together 300 monocotyledonous species). Solely the latter, old and isolated family comprises 8 genera with nearly 260 species (Kubitzki 1998), all most likely desiccation tolerant, and more Velloziaceae species may be discovered in the future (Ibisch et al. 2001). Gaff (1989) suggests an early specialization of the poikilohydrous taxa within their small and often isolated genera.
Nonvascular autotrophs (cyanobacteria, algae, bryophytes, and lichens) are considered constitutively poikilohydrous because they lack the means of controlling water relations (Stocker and Holtheide 1938, Biebl 1962, Walter and Kreeb 1970). This is in contrast with vascular plants, which in general have constitutively homoiohydrous "sporophytes," and keep their hydration state within certain limits by such means of roots, conducting tissues, epidermis, cuticles, and stomata. The poikilohydrous performance of vascular plants is to be taken as an acquired ("secondary": Raven 1999) trait and is realized in phylogenetically unrelated plant species, genera, or families (Oliver et al. 2000). Because poikilohydry is constitutional in nonvascular autotrophs and rare among vascular plants, it is tempting to consider it a primitive property and to suggest that evolutionarily early terrestrial, photosyn-thetic organisms based their survival on tolerance (Raven 1999) instead of avoidance mechanisms. However, poikilohydry is not an indicator of an early evolutionary stage among vascular plants. Although several recent pteridophytes are poikilohydrous, there is no known poikilohydrous recent gymnosperm, and poikilohydry is frequent only in highly derived angiosperm families (Oliver and Bewley 1997, Oliver et al. 2000). Therefore, poikilohydrous performance by vascular plants can be interpreted evolutionarily as an adaptive response to climates and habitats with infrequent moist periods (see also Proctor and Tuba 2002).
The term resurrection has been commonly used for some species and, in general, matches the capability of poikilohydrous plants to quickly reactivate after falling into a period of anabiosis caused by dehydration. It is very appropriate for spikemosses (Selaginella) and certain bryophytes and lichens that curl strongly with water loss and unfold conspicuously upon rehydration. Similar performance can be observed in the dead remnants of plants in deserts and steppes. In addition, in fact, the annual homoiohydrous species Anastatica hierochuntica was called a resurrection plant by some investigators (Wellburn and Wellburn 1976) because of the dramatic change between a curled and shriveled stage in the dry season and the spreading of the dead branches in the rainy season to release the seeds. Consequently, resurrection, in a broad, intuitive sense, could also be applied to certain homoiohydrous desert perennials (e.g., Aloe, Mesembryanthemaceae, and certain cacti). On the other hand, the shape and appearance of some constitutively poikilohydrous autotrophs, such as terrestrial unicellular algae and crustose lichens, do not visibly change. To add to the confusion, water loss can be dramatic in some homoiohydrous desert plants, whereas it can be minor in constitutively poikilohydrous plants such as Hymenophyllum tunbridgense or bryophytes and lichens from moist environments. Therefore, the resurrection phenomenon (visible changes in shape and aspect with hydration) is only part of the poikilohydrous performance and it is not exhibited to the same extent by all poikilohydrous autotrophs.
Ferns are dual because they produce constitutively poikilohydrous gametophytes and a cormophytic sporophyte with the full anatomy of a homoiohydrous plant. Knowledge about gametophytes is scant. They are usually found in humid, sheltered habitats where hygric and mesic bryophytes also grow. Previous literature reports on extremely desiccation-tolerant prothallia of the North American Camptosorus rhizophyllus, and of Asplenium platyneuron and Ceterach officinarum (= Asplenium ceterach) (Walter and Kreeb 1970). The desiccation tolerance of prothallia of some European fern species varied with species and season (Kappen 1965). They usually overwinter, and their ability to survive low temperatures and freezing is based on increased desiccation tolerance. Prothallia of rock-colonizing species (Asplenium species, Polypodium vulgare) could withstand 36 h drying in 40% relative humidity; some species were partly damaged but could regenerate from surviving tissue. Prothallia of other ferns from European forests were more sensitive to desiccation (Table 2.1).
The poikilohydrous nature of a terrestrial vascular plant is frequently defined by the combination of a passive response to ambient water relations and a tolerance to desiccation (Gaff 1989), but the emphasis on the different functional aspects involved and the actual limits of poikilohydry are matters of debate. Some poikilohydrous species cannot even tolerate a water loss greater than 80% of their maximal water content (Gaff and Loveys 1984), and others can be shown to gain their tolerance only by a preconditioning procedure. Boundaries between poikilohydrous and homoiohydrous plants can be rather blurry, especially if we include examples of xerophytes that can survive extremely low water potentials (Kappen et al. 1972). Surviving at very low relative humidities is not a useful indicator because a limit of 0%-10% relative humidity excludes many nonvascular plants that are undoubtedly poikilohydrous. Considering the photosynthetic performance and low tolerance to desiccation of certain forest lichens (Green et al. 1991) and the fact that, in particular, endohydric bryophytes depend on moist environments, Green and Lange (1994) concluded that the passive response to ambient moisture conditions of poikilohydrous autotrophs varies in a species- and environment-specific manner.
The conflict between ecologically based and physiologically or morphologically based criteria cannot be easily solved. However, a compromise can be reached by distinguishing between stenopoikilohydrous (narrow range of water contents) and eurypoikilohydrous (broad range of water contents) autotrophs. This distinction is especially useful for nonvas-cular, that is, for constitutively poikilohydrous autotrophs. For instance, microfungi that spend all their active lifetime within a narrow range of air humidity are stenopoikilohydrous. As xeric species they grow in equilibrium with relative humidities as low as 60% (Pitt and Christian 1968, Zimmermann and Butin 1973). Aquatic algae and cyanobacteria are also typically stenopoikilohydrous. The so-called hygric and mesic bryophytes and filmy ferns that are not able to survive drying to less than 60% water content or less than 95% relative humidity also belong to the stenopoikilohydrous type. The same is the case with some wet forest lichens that have low desiccation tolerance (Green et al. 1991). A stenopoikilohydrous performance is also apparent in those ephemeral bryophytes that germinate after heavy rain and then quickly develop gametophytes and sporogons. Some examples with this drought evasion strategy are the genera Riella, Riccia, and species of Sphaerocarpales, Pottiaceae, and Bryobatramiaceae. These annual shuttle species are characteristic of seepage areas and pond margins where the soil remains wet for a few weeks (Volk 1984). The many vascular plant species growing permanently submersed in water have also a stenopoikilohydrous life style (see Raven 1999).
All nonvascular and vascular species that are extremely tolerant to desiccation and typically perform as resurrection plants (Gaff 1972, 1977, Proctor 1990) belong to the eurypoikilohydrous group. Because many of these species grow in dry or desert environments, poikilohydry was often associated with xerophytism (Hickel 1967, Patterson 1964, Gaff 1977). However, seasonal changes in the tolerance to desiccation can confound this distinction between stenopoikilohydrous and eurypoikilohydrous organisms. These changes have been found in bryophytes (Dilks and Proctor 1976b) and ferns (Kappen 1964) and are very likely to occur in angiosperms. As suggested by Kappen (1964), such plants may be considered as temporarily poikilohydrous. Hence, the number of eurypoikilohydrous bryophyte species cannot be fixed until temporal changes of desiccation tolerance are better studied in mesic species (Proctor 1990, Davey 1997, Proctor and Tuba 2002). Most of the available information and, consequently, most of what follows, involves eurypoikilohydrous auto-trophs. The different groups of poikilohydrous autotrophs that can be identified according to the range of water contents experienced in nature or tolerated are summarized later.
Ecology and Distribution of Poikilohydrous Autotrophs
Nowhere else in the world are poikilohydrous autotrophs more conspicuous than in arid and climatically extreme regions (e.g., Namib desert, Antarctica). It is somewhat paradoxical that precisely in habitats with extreme water deficits the dominant organisms are the least protected against water loss. Additionally, the poikilohydrous angiosperms show in general no typical features against water loss, but they can compete well with extremely specialized taxa of homoiohydrous plants. However, again the distinction between stenopoikilohydrous and eurypoikilohydrous plants becomes important, because stenopoikilohydrous autotrophs can be very abundant in moist habitats (e.g., cloud forests: Gradstein 2006). In the moist and misty climate of San Miguel, Azores, even Sphagnum species are able to grow as epiphytes on small trees. However, eurypoikilohydrous autotrophs, which are capable of enduring prolonged drought and extreme temperatures, represent the most interesting group because they have more specifically exploited the ecological advantages of their opportunistic strategy. The remainder of this chapter presents examples of poikilohydrous autotrophs living under very limiting ecological conditions in many different regions of the Earth.
In temperate climates, poikilohydrous autotrophs are mainly represented by aerophytic algae, bryophytes, and lichens. Depending on their habitat, bryophytes can be eurypoikilo-hydrous or stenopoikilohydrous. Among the temperate vascular plants, poikilohydrous performance is realized in some mainly rock-colonizing fern genera such as Asplenium, Ceterach, Cheilanthes, Hymenophyllum, Notholaena, and Polypodium and the phanerogamous genera Haberlea and Ramonda.
From the arctic region, no poikilohydrous vascular plants are known, and most parts of Antarctica are inhabited solely by algae, bryophytes, lichens, and fungi, which are mainly eurypoikilohydrous. In the polar regions and in hot, extremely arid deserts, nonvascular autotrophs may be restricted to clefts and rock fissures or even grow inside the rock as endolithic organisms or hypolithic on the underside of more or less translucent rock particles and stones (Friedmann and Galun 1974, Scott 1982, Danin 1983, Kappen 1988, 1993b, Nienow and Friedmann 1993).
In subtropical regions bryophytes, algae, and lichens are well known as crust-forming elements on open soils (Belnap and Lange 2001). The coastal Namib desert, with extremely scattered rainfall, consists of wide areas where no vascular plants can be found, but a large cover of mainly lichens forms a prominent vegetation. In rocky places of the Near East, southern Africa, arid northwest North America, coastal southwest North America, and the South American westcoast, lichens and bryophytes coexist with xeromorphic or succulent plants. They also occupy rock surfaces and places where vascular plants do not find enough soil, or they grow as epiphytes on shrubs and cacti. Under such extreme conditions, lichens and bryophytes share the habitat with poikilohydrous vascular plants as for instance Borya nitida on temporarily wet granitic outcrops (Figure 2.1) with shallow soil cover in southern and western Australia (Gaff and Churchill 1976).
In Africa, subfruticose poikilohydrous plants such as Lindernia crassifolia and Lindernia acicularis grow in sheltered rock niches (Fischer 1992). The same is true for the fruticose poikilohydrous species, Myrothamnus flabellifolius, occurring in southern Africa and Madagascar from Namibia (Child 1960, Puff 1978, Sherwin et al. 1998), which is frequently associated with other resurrection plants (e.g., Pellaea viridis, Pellaea calomelanos). In the wet season, these plants benefit from run off water that floods the shallow ground (Child 1960). Particularly remarkable are poikilohydrous aquatic Lindernia species (L. linearifolia,
L. monrio, L. conferta) and Chamaegigas (Lindernia) intrepidus (Heil 1925, Hickel 1967, Gaff and Giess 1986, Heilmeier et al. 2005), which grow in small temporarily water-filled basins of granitic outcrops in Africa (Angola, Zaire, Zimbabwe, South Africa, Namibia). Many of the poikilohydrous grass species (less than 20 cm high) and sedges (30-50 cm high) are pioneering perennial plants colonizing shallow soil pans in southern Africa (Gaff and Ellis 1974). In Kenya and West Africa, the resurrection grasses, sedges, and Vellociaceae (in Africa 30 species, Ibisch et al. 2001) are confined to rocky areas, except Sporobolus fimbriatus and Sporobolus pellucidatus. Eragrostis invalida is the tallest poikilohydrous grass species known with a foliage up to 60 cm (Gaff 1986). Vellozia schnitzleinia is a primary mat former following algae and lichens on shallow soils of African inselbergs, persisting during the dry season with brown, purple-tinged rolled leaves that turn green in the wet season (Owoseye and Sandford 1972).
The resurrection flora of North America is represented mainly by pteridophytes. Most of the poikilohydrous fern species so far known are preferentially found in rock cervices, gullies, or sheltered in shady rocky habitats (Nobel 1978, Gildner and Larson 1992). By contrast, the most famous resurrection plant Selaginella lepidophylla colonizes open plains in Texas (Eickmeier 1979, 1983). In Middle and South America, 220 species of the Velloziaceae form the dominant part of the poikilohydrous flora. They grow in various habitats and even in alpine regions. The endemic Vellozia andina seems to be an opportunistic species as it takes benefit from degraded formerly forested sites (Ibisch et al. 2001). Fire resistance is typical of many Velloziaceae species (Kubitzki 1998). Gaff (1987) has enumerated 12 fern species for South America. Pleopeltis mexicana and Trichomanes bucinatum may also be candidates (Hietz and Briones 1998). One of the most remarkable poikilohydrous vascular plants could be Blossfeldia liliputana, a tiny cactus that grows in shaded rock crevices of the eastern Andean chain (Bolivia to northern Argentine) at altitudes between 1200 and 2000 m (Barthlott and Porembski 1996). This plant is unable to maintain growth and shape during periods of drought, and it persists in the dry state (18% of initial weight) for 12-14 months, looking like a piece of paper. When water is again available, it can rehydrate and resume CO2 assimilation within 2 weeks; it is the only known example of a succulent poikilohydrous plant.
From a plant-geographical perspective, inselberg regions in Africa, Madagascar, tropical South America, and Western Australia have the largest diversity of poikilohydrous vascular plants in the World. Porembski and Barthlott (2000) state that 90% of the known vascular poikilohydrous plant species occur on tropical inselbergs. The presence of almost all known genera with poikilohydrous plants could be recorded from such sites. Despite the existence of similar potential habitats for poikilohydrous vascular plants in Australia, species are less numerous there than in southern Africa. Lazarides (1992) suggested that this biogeographical difference between Australia and southern Africa is due to the fact that the Australian arid flora has been exposed to alternating arid and pluvial cycles for a shorter geological period of time than the arid flora of southern Africa. The former has experienced these alternations since the Tertiary, whereas the latter has been exposed to dry-wet cycles since the Cretaceous. Ferns, represented by a relatively large number of species , and most of the poikilohydrous grasses found in Australia  grow in xeric rocky sites (Lazarides 1992). We have very few records about poikilohydrous vascular plants from Asia, although such a type of plant must exist there as well. Gaff and Bole (1986) recorded 10 poikilohydrous Poaceae (genera Eragrostidella, Oropetium, Tripogon) for India. The Gesneriaceae Boea hygrometrica, closely related to the Australian Boea hygroscopica, is a poikilohydrous representative in China (see Yang et al. 2003).
Most of the resurrection plants are confined to lowland and up to 2000 m a. s. l. However, a few Velloziaceae species such as Xerophyta splendens reach altitudes of 2800 m in Malawi (Porembski 1996) and Barbaceniopsis boliviensis reach 2900 m in the Andes (Ibisch et al. 2001), the latter staying in anabiosis with reddish-brown leaves for half a year. In such high altitudes, they are exposed to frost periods.
Does Poikilohydry Rely on Specific Morphological Features?
Poikilohydrous performance cannot be typified by any one given set of morphological and anatomical features because of the heterogeneity of this functional group of photosynthetic organisms. Poikilohydry can be found in autotrophs ranging from those with the most primitive unicellular or thallose organization to those with the most highly derived vascular anatomy. In angiosperms, desiccation tolerance is, in general, inversely related to anatomical complexity. It seems that plants can operate either by avoidance or tolerance mechanisms at all levels of organization if they are adapted to temporarily dry habitats. Gaff (1977) called resurrection plants "true xerophytic'' just because they live in xeric environments. However, poikilohydrous angiosperms do not necessarily have xeromorphic traits. Xeromorphic features such as small and leathery leaves are typical for Myrothamnus; xeromorphic narrow or needle-like leaves for many Velloziaceae, Cyperaceae, and the genus Borya (see Figure 2.1); and massive sclerenchymatic elements, for example, several Velloziaceae and Borya (Gaff and Churchill 1976, Lazarides 1992, Kubitzki 1998). Hairs on leaves (e.g., Velloziaceae, Gesneriaceae) are mostly small, and scales (e.g., Ceterach) or succulence (Blossfeldia) are the exception rather than the rule in poikilohydrous vascular plants. Xeromorphic structures would also counteract the potential of rehydration during the wet period. However, curling and uncurling of leaves, frequently enabled by contraction mechanism, is a widespread phenomenon in poikilohydrous vascular plants.
Poikilohydrous vascular plants are mainly perennials represented by various types of hemicryptophytic and chamaephytic life forms but no trees. Lignification of stems is not rare, and the two existing Myrothamnus species are true shrubs reaching approximately 1.5 m height. Within the monocotyledons, a tree-like habit is achieved either by an enhanced primary growth of the main axis or by secondary thickening, and trunks may reach up to 4 m length. Such pseudostems are realized in the genus Borya (secondary growth) and by some Cyperaceae and Velloziaceae (Gaff 1997, Kubitzki 1998, Porembski and Barthlott 2000). For instance, a sample of Vellozia kolbekii was looking with its stem (covered by roots and leaf sheaths) like a tree fern, was 3 m tall, and was estimated to be about 500 years old (Alves 1994).
As most of the phanerogamous resurrection plants do not show peculiar or uniform anatomical features, it is hard to decide whether a particular plant is poikilohydrous just from herbarium material or from short-term observations in the field (Gaff and Latz 1978). It is still uncertain, for instance, whether more members of the Lindernieae can be identified as poikilohydrous in studies such as that by Fischer (1992) and Proctor (2003). Many species that grow in shady habitats or that colonize temporarily inundated habitats exhibit a hygromorphic tendency (Volk 1984, Fischer 1992, Markowska et al. 1994). For instance, Chamaegigas intrepidus has, like other aquatic plants, aerenchyma and two types of leaves, floating and submerged. Blossfeldia liliputana, the only known poikilohydrous Cacta-ceae, combines a succulent habit with a typically hygromorphic anatomy: very thin cuticle, no thickened outer cell walls, absence of hypodermal layers, and extremely low stomatal density (Barthlott and Porembski 1996). Poikilohydrous vascular plants exhibit, in general, very low stomatal control of transpiration (Gebauer 1986, Sherwin et al. 1998, Proctor 2003). The leaves of Satureja gilliesii even have protruding stomata on the underside (Montenegro et al. 1979).
The secondarily poikilohydrous nature of aquatic vascular plants has rarely been acknowledged (Raven 1999). Most of them have reduced xylem structure and no sustaining function. Roots merely act to fix to the substratum, and nutrients are taken up by the leaves. Cuticles are thin and stomata are scattered and frequently nonfunctional (Isoetes, Litorella, Elodea, Vallisneria, Potamogetonaceae, etc). Living in streams and underwater rapids in the Tropics, the Podostemaceae are very remarkable examples with a drastic reduction of their homoiohydrous architecture. With their thallus-like shoots they resemble foliose liverworts.
Small size is recognized frequently as typical of the shape of the poikilohydrous autotrophs. Indeed, only a few vascular species are fruticose and reach more than 50 cm height. Alpert (2006) discusses whether there is a trade-off between low growth and desiccation tolerance in the sense of a disadvantage, because the plant has to invest in protection mechanisms instead of extension growth as most of the homoiohydrous plants do. Proctor and Tuba (2002) on the other hand, refer to poikilohydry as an advantage particularly for living in temporarily dry environments. High desiccation tolerance is the ultimate drought-evading mechanism. The resurrection strategy is ecologically as successful as that of homoiohydrous plants with CAM or the adaptation to live on heavy-metal soils or in raised bogs. In addition, the slow growth and small size of poikilohydrous plants is not only a function of changing water status but also of nutrient deficiency, which is obvious from most of their natural habitats. C. intrepidus, for instance, has to use urea as nitrogen source by means of free urease in the sediments of rock pools (Heilmeier et al. 2000) and free amino acids (Schiller 1998).
Living under water, the nonvascular autotrophs are able to develop a size (Macrocystis spp.: 60 m) comparable to that of tall trees, and the vascular plant species Elodea canadensis may produce up to 6 m long shoots (see Raven 1999). Endohydrous mosses such as the Dawsoniaceae and Polytrichaceae may reach a height of 1 m in the damp atmosphere of rain forests. This demonstrates that the small size of autotrophs which are eurypoikilohydrous is an adaptive trait to respond flexibly to drought events rather than remaining principally handicapped with respect to growth and productivity.
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