Pugnaire F.I. Valladares F. Functional Plant Ecology
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Longton, R.E., 1974. Microclimate and biomass in communities of the Bryum association on Ross
Island, continental Antarctica. Bryologist 77: 109–127.
Longton, R.E., 1988a. The biology of polar bryophytes and lichens. Cambridge University Press,
Cambridge.
Longton, R.E., 1988b. Adaptations and strategies of polar bryophytes. Botanical journal of the Linnean
Society. Linnean Society of London 98: 253–268.
Longton, R.E. and M.W. Holdgate, 1967. Temperature relations of antarctic vegetation. Philosophical
Transactions of the Royal Society, London B. 252: 237–250.
Lovelock, C.E., C.B. Osmond, and R.D. Seppelt, 1995a. Photoinhibition in the antarctic moss Grimmia
antarctici Card. when exposed to cycles of freezing and thawing. Plant Cell and Environment 18:
1395–1402.
Lovelock, C.E., A.G. Jackson, D.R. Melick, and R.D. Seppelt, 1995b. Reversible photoinhibition in
antarctic moss during freezing and thawing. Plant Physiology 109: 955–961.
Lud, D., T. Moerdijk, W. Van der Poll, A.G.J. Buma, and A.H.L. Huiskes, 2002. DNA damage and
photosynthesis in Antarctic and Arctic Sanionia uncinata (Hedw.) Loeske. under ambient and
enhanced levels of UV-B radiation. Plant Cell and Environment 25: 1579–1589.
Lud, D., M. Schlensog, B. Schroeter, and A.H.L. Huiskes, 2003. The influence of UV-B radiation on
light-dependent photosynthetic performance in Sanionia uncinata (Hedw.) Loeske in Antarctica.
Polar Biology, 26: 225–232.
Lyons, W.B., A. Foutain, P. Doran, J.C. Priscu, K. Neumann, and K.A. Welch, 2000. Importance of
landscape position and legacy: the evolution of the lakes in Taylor Valley, Antarcica. Freshwater
Biology 43: 355–367.
Marshall, W.A., 1996. Aerial dispersal of lichen soredia in the maritime Antarctic. New Phytologist 134:
523–530.
Matsuda, T., 1968. Ecological study of the moss community and microorganisms in the vicinity of
Syowa Station, Antarctica. Japanese Antarctic Research Expedition Science Reports. E29: 1–58.
Melick, D.R. and R.D. Seppelt, 1992. Loss of soluble carbohydrates and changes in freezing point of
antarctic bryophytes after leaching and repeated freeze–thaw cycles. Antarctic Science 4: 399–404.
Montiel, P., A. Smith, and D. Keiler, 1999. Photosynthetic responses of selected Antarctic plants to
solar radiation in the southern maritime Antarctic. Polar Research 18: 229–235.
Newsham, K., D. Hodgson, and A. Murray et al., 2002. Response of two Antarctic bryophytes to
stratospheric ozone depletion. Global Change Biology 8: 1–12.
Nienow, J.A., C.P. McKay, and E.I. Friedmann, 1988. The cryptoendolithic microbial environment in
the Ross Desert of Antarctica. Mathematical models of the thermal regime. Microbial Ecology
16: 253–270.
Noakes, T.D. and R.E. Longton, 1989. Studies on water relations in mosses from the cold—Antarctic.
In: R.B. Heywood, ed. University Research in Antarctica. Antarctic Special Topic. British
Antarctic Survey, Cambridge, pp. 103–116.
Nolan, L., I.D. Hogg M.I. Stevens, and M. Haase, 2006. Fine scale distribution of mtDNA haplotypes
for the springtail Gomphocephalus hodgsoni (Collembola) corresponds to an ancient shoreline in
Taylor Valley, continental Antarctica. Polar Biology 29: 813–819.
Ochyra, R., 1998. The moss flora of King George Island, Antarctica. Polish Academy of Sciences,
Cracow, Poland pp. 279.
Okitsu, S., S. Imura, and E. Ayukawa, 2004. Micro-relief distribution of major mosses in ice-free areas
along the So
ˆ
ya Coast, The Syowa Station area, East Antarctica. Polar Bioscience 17: 69–82.
Olech, M., 1990. Preliminary studies on ornithocoprophilous lichens of the arctic and Antarctic regions.
NIPR Symposium on Polar Biology 3: 218–223.
Øvstedal, D.O. and R.I.L. Smith, 2001. Lichens of Antarctica and South Georgia. A guide to their
identification and ecology. Cambridge University Press, Cambridge.
Pannewitz, S., T.G.A. Green, C. Scheidegger, M. Schlensog, and B. Schroeter, 2003a. Activity pattern of
the moss Hennediella heimii (Hedw.) Zand. in the Dry Valleys, Southern Victoria Land,
Antarctica during the mid-austral summer. Polar Biology 26: 545–551.
Pannewitz, S., M. Schlensog, T.G.A. Green, S. Sancho, and B. Schroeter, 2003b. Are lichens active
under snow in continental Antarctica? Oecologia 135: 30–38.
Francisco Pugnaire/Functional Plant Ecology 7488_C013 Final Proof page 430 16.4.2007 2:34pm Compositor Name: BMani
430 Functional Plant Ecology
Pannewitz, S., T.G.A. Green, K. Masek, M. Schlensog, R.D. Seppelt, L.G. Sancho, R. Tuerk, and
B. Schroeter, 2005. Photosynthetic responses of three common mosses from continental
Antarctica. Antarctic Science 17: 341–352.
Peat, H.J., A. Clarke, and P. Convey, 2007. Diversity and biogeography of the Antarctic flora. Journal
of Biogeography 34: 132–146.
Pickard, J., 1986. Antarctic oases, Davis station and the Vestfold Hills. In J. Pickard, ed. Antarctic
Oasis; Terrestrial Environments and History of the Vestfold Hills. Academic Press Australia,
Sydney, pp. 1–19.
Poelt, J., 1987. Das Gesetz der relativen Standortkonstnz bei den Flechten. Botanische Jahrbuecher der
Systematik 108: 363–371.
Post, A., 1990. Photoprotective pigment as an adaptive strategy in the Antarctic moss Ceratodon
purpureus. Polar Biology 10: 241–245.
Post, A. and M. Vesk, 1992. Photosynthesis, pigments, and chloroplast ultrastructure of an
antarctic liverwort from sun-exposed and shaded sites. Canadian Journal of Botany 70:
2259–2264.
Post, A., E. Adamson, and H. Adamson, 1990. Photoinhibition and recovery of photosynthesis in
antarctic bryophytes under field conditions. Current Research in Photosynthesis 4: 635–638.
Proctor, M.C.F., 2000. Physiological ecology. In: A.J. Shaw and B. Goffninet, eds. Bryophyte Biology.
Cambridge University Press, Cambridge, pp. 225–247.
Rastorfer, J.R., 1970. Effects of light intensity and temperatre on photosynthesis and respiration of two
east Antarctic mosses, Bryum argenteum and Bryum antarcticum. Bryologist 73: 544–556.
Rastorfer, J.R., 1972. Comparative physiology of four west antarctic mosses. In: G.A. Llano, ed.
Antarctic Terrestrial Biology. Antarctic Research Series Vol. 20. American Geophysical
Union, Washington, pp. 143–161.
Rikkinen, J., 1995. What’s behind the pretty colours? A study on the photobiology of lichens.
Bryobrothera 4: 1–239.
Robinson, S.A., J. Wasley, M. Popp, and C.E. Lovelock, 2000. Desiccation tolerance of three moss
species from continental Antarctica. Australian Journal of Plant Physiology 27: 379–388.
Robinson, S.A., J. Wasley, and A.K. Tobin, 2003. Living on the edge—plants and global change in
continental and maritime Antarctica. Global Change Biology 9: 1681–1717.
Robinson, S.A., J.D. Turnbull, and C.E. Lovelock, 2005. Impact of changes in natural ultraviolet
radiation on pigment composition, physiological and morphological characteristics of the
Antarctic moss, Grimmia antarctici. Global Change Biology 11: 476–489.
Ruhland, C. and T. Day, 2001. Size and longevity of seed banks in Antarctica and the influence of
ultraviolet-B radiation on survivorship, growth and pigment concentration of Colobanthus
quitensis seedlings. Environmental and Experimental Biology 45: 143–154.
Sancho, L.G. and A. Pintado, 2004. Evidence of high annual growth rate for lichens in the maritime
Antarctic. Polar Biology 27: 312–319.
Sancho, L.G., A. Pintado, F. Valladares, B. Schroeter, and Schlensog, M., 1997. Photosynthetic
performance of cosmopolitan lichens in the maritime Antarctic. Bibliotheca Lichenologica 67:
197–210.
Schlensog, M., B. Schroeter, L.G. Sancho, A. Pintado, and L. Kappen, 1997a. Photosynthetic perform-
ance of the cyanobacterial lichen Leptogium puberulum in the maritime Antarctic Biology of the
Royal Society Espan
˜
ola de Historia Natural. Seccio
´
n biolo
´
gica 93: 107–113.
Schlensog, M., B. Schroeter, L.G. Sancho, A. Pintado, and L. Kappen, 1997b. Effect of strong
irradiance on photosynthetic performance of the melt-water dependent cyanobacterial
lichen Leptogium puberulum (Collemataceae) Hue from the maritime Antarctic. Bibliotheca
Lichenenologica 67:235–246.
Schlensog, M., B. Schroeter, S. Pannewitz, and T.G.A. Green, 2003. Adaptations of mosses and lichens
to irradiance stress in maritime and continental Antarctic habitats. In: Huiskes, Gieskes,
Rozema, Schorno, van der Vries and W. Wolff, eds. Antarctic Biology in a Global Context.
Backhuys, Leiden, 352 pp.
Schlensog, M., S. Pannewitz, T.G.A. Green, and B. Schroeter, 2004. Metabolic recovery of continental
antarctic cryptogams after winter. Polar Biology 27: 399–408.
Francisco Pugnaire/Functional Plant Ecology 7488_C013 Final Proof page 431 16.4.2007 2:34pm Compositor Name: BMani
Plant Life in Antarctica 431
Schroeter, B., 1991. Untersuchungen zu Prima
¨
rproduction und Wasshaushalt von Flechten der maritimen
Antarktis unter besonderer Beru
¨
cksichtigung von Usnea antarctica Du Rietz. Dissertation
Universitaet Kiel, pp. 1–148.
Schroeter, B., 1994. In situ photosynthetic differentiation of the green algal and the cyanobacterial
photobiont in the crustose lichen Placopsis contortuplicata. Oecologia 98: 212–220.
Schroeter, B., 1997. Grundlagen der Stoffproduktion von Kryptogamen unter besonderer Beru
¨
cksichtigung
der Flechten—eine Synopse—Habilitationsschrift der mathematisch—Naturwissenschaftlichen
Fakulta
¨
t der Christian—Albrechts—Universita
¨
t zu Kiel, pp. 130.
Schroeter, B. and C. Scheidegger, 1995. Water relations in lichens at subzero temperatures: Structural
changes and carbon dioxide exchange in the lichen Umbilicaria aprina from continental Antarc-
tica. New Phytologist 131: 273–285.
Schroeter, B., L. Kappen, and C. Moldaenke, 1991. Continuous in situ recording of the photosynthetic
activity of Antarctic lichens–established methods and a new approach. Lichenologist 23:
253–265.
Schroeter, B., T.G.A. Green, R.D. Seppelt, and L. Kappen, 1992. Monitoring photosynthetic activity of
crustose lichens using a PAM–2000 fluorescence system. Oecologia 92: 457–462.
Schroeter, B., T.G.A. Green, L. Kappen, and R.D. Seppelt, 1994. Carbon dioxide exchange at subzero
temperatures. Field measurements on Umbilicaria aprina in Antarctica. Cryptogamic Botany
4: 233–241.
Schroeter, B., A. Olech, L. Kappen, and W. Heitland, 1995. Ecophysiological investigations of Usnea
antarctica in the maritime Antarctic. I. Annual microclimatic conditions and potential primary
production. Antarctic Science 7: 251–260.
Schroeter, B., L. Kappen, and F. Schulz, 1997a. Long–term measurements of microclimate conditions in
the fruticose lichen Usnea aurantiaco-atra in the maritime Antarctic. In: J. Cacho, and D. Serrat,
eds. Actas del V Simposio de Estudios Antarcticos (1993). CICYT, Madrid, pp. 63–69.
Schroeter, B., F. Schulz, and L. Kappen, 1997b. Hydration-related spatial and temporal variation of
photosynthetic activity in antarctic lichens. In: B. Battaglia, J. Valencia, and D.W.H. Walton,
eds. Antarctic Communities. Species, Structure and Survival. Cambridge University Press,
Cambridge, pp. 221–225.
Schroeter, B., L. Kappen, T.G.A. Green, and R.D. Seppelt, 1997c. Lichens and the antarctic environ-
ment: effects of temperature and water availability on photosynthesis. In: W.B. Lyons,
C. Howard-Williams, and I. Hawes, eds. Ecosystem Processes in Antarctic Ice-free Landscapes.
Balkema, Rotterdam, Brookfield, pp. 103–118.
Schwarz, A.M.J., T.G.A. Green, and R.D. Seppelt, 1992. Terrestrial vegetation at Canada Glacier,
Southern Victoria Land, Antarctica. Polar Biology 12: 397–404.
Senchina, D.S., 2005. A historical survey of botanical exploration in Antarctica. Huntia 12: 31–69.
Seppelt, R.D., 1995. Phytogeography of continental antarctic lichens. Lichenologist 27: 417–431.
Seppelt, R.D. and D.H. Ashton, 1978. Studies on the ecology of the vegetation of Mawson Station
Antarctica. Australian Journal of Ecology 3: 373–388.
Seppelt, R.D. and H. Kanda, 1986. Morphological variation and taxonomic interpretation in the moss
genus Bryum in Antarctica. Member of the National Institute of Polar Research 37: 27–42.
Seppelt, R.D. and T.G.A. Green, 1998. A bryophyte flora for Southern Victoria Land, Antarctica.
New Zealand Journal of Botany 36: 617–635.
Smith, R.I.L., 1984. Terrestrial plant biology of the sub-Antarctic and Antarctic. In: R.M. Laws, ed.
Antarctic Ecology. Academic Press, London, pp. 61–162.
Smith, R.I.L., 1993. The role of bryophyte propagule banks in primary succession: case-study of an
antarctic fellfield soil. In: J. Miles and D.W.H. Walton, eds. Primary Succession on Land.
Oxford, Blackwells, pp. 55–78.
Smith, R.I.L., 1994. Vascular plants as bioindicators of regional warming in Antarctica. Oecologia 99:
322–328.
Smith, R.I.L. 1996. Terrestrial and freshwater biotic components of the western Antarctic Peninsula. In:
R.M. Koss, E. Hofmann, and L.B. Quetin, eds. Foundations for Ecological Research West of
the Antarctic Peninsula. Antarctic Research Series, Volume 70, pp. 15–59. American
Geophysical Union, Washington.
Francisco Pugnaire/Functional Plant Ecology 7488_C013 Final Proof page 432 16.4.2007 2:34pm Compositor Name: BMani
432 Functional Plant Ecology
Smith, R.I.L., 1999. Biological and environmental characteristics of three cosmopolitan mosses dominant
in continental Antarctica. Journal of Vegetation Science 10: 231–242.
Smith, R.I.L., 2000. Plants of extreme habitats in Antactica. Bibliotheca Lichenologica 75: 405–419.
Smith, R.I.L. and D.O. O
¨
vstedal, 1991. The lichen genus Stereocaulon in Antarctica and South Georgia.
Polar Biology 11: 91–112.
Smith, V.R., 1993. Effect of nutrients on CO
2
assimilaton by mosses on a sub-antarctic island. New
Phytologist 123: 693–697.
So
¨
chting, U. and M. Olech, 1995. The lichens genus Caloplaca in polar regions. Lichenologist 27: 463–471.
Stenroos, S., 1993. Taxonomy and distribution of the lichen family Cladoniaceae in the Antarctic and
peri–Antarctic regions. Cryptogamic Botany 3: 310–344.
Stevens, M.I. and I.D. Hogg, 2003. Long-term isolation and recent expansion from glacial refugia
revealed for the endemic springtail Gomphiocephalus hodgsoni from Victoria Land, Antarctica.
Molecular Ecology 12: 2357–2369.
Stevens, M.I., P. Greenslade, I.D. Hogg, and P. Sunnucks, 2006. Southern hemisphere springtails: Could
they have survived glaciation of Antarctica. Molecular Biology and Evolution 23: 874–882.
Tarnawski, M., D. Melick, D. Roser, E. Adamson, H. Adamson, and R. Seppelt, 1992. In situ carbon
dioxide levels in cushion and turf forms of Grimmia antarctici at Casey Station, east Antarctica.
Journal of Bryology 17: 241–249.
Tuerk, R., T.G.A. Green, L.G. Sancho, and R. Seppelt, 2004. Unexpectedly high number of lichen
species at 848 S, Southern Victoria Land: Flattening the biodiversity cline. SCAR Open Science
Conference, Bremen, Germany, 25–31 July.
Vestal, J.R., 1988. Primary production of cryptoendolithic microbiota from the Antarctic desert.
Polarforschung 58: 193–198.
Vincent, W.F., 1988. Microbial systems of Antarctica. Cambridge University Press, Cambridge.
Walker, F.J., 1985. The lichen genus Usnea subgenus Neuropogon. Bulletin of the British Museum
Botany Series 13: 1–130.
Wasley, J., S.A. Robinson, C.E. Lovelock, and M. Popp, 2006. Climate change manipulations show
Antarctic flora is more strongly affected by elevated nutrients than water. Global Change
Biology, 12: 1800–1812.
Waterhouse, E.J., ed., 2001. Ross Sea Region: A state of the environment report for the Ross Sea
Region of Antarctica. New Zealand Antarctic Institute, Christchurch.
Wierzchos, J. and C. Ascaso, 2001. Life, decay and fossilisation of endolithic microorganisms from the
Ross Desert, Antarctica. Polar Biology 24: 863–868.
Wierzchos, J. and C. Ascaso, 2002. Microbial fossil record of rocks from the Ross Desert, Antarctica:
implications in the search for past life on Mars. International Journal of Astrobiology 1: 51–59.
Wierzchos, J., C. Ascaso, L. Garcia Sancho, and A. Green, 2003. Iron-rich diagenetic minerals are
biomarkers of microbial activity in Antarctic rocks. Geomicrobiology Journal 20: 15–24.
Wierzchos, J., L. Garcia-Sancho, and C. Ascaso, 2005. Biomineralization of endolithic microbes in
rocks from the McMurdo Dry Valleys of Antarctica: Implications for microbial fossil formation
and their detection. Environmental Microbiology 7: 566–575.
Wierzchos, J., C. Ascaso, F.J. Ager, I. Garcı
´
a-Orellana, A. Carmona-Luque, and M.A
´
. Respaldiza,
2006. Identifying elements in rocks from the Dry Valleys desert (Antarctica) by ion beam
proton induced X-ray emission. Nuclear Instruments and Methods in Physics Research B 249:
571–574.
Wilson, M.E., 1990. Morphology and photosynthetic physiology of Grimmia antarctici from wet and
dry habitats. Polar Biology 10: 337–341.
Wise, K.A.J. and J.L. Gressit, 1965. Far southern animals and plants. Nature 207: 101–102.
Francisco Pugnaire/Functional Plant Ecology 7488_C013 Final Proof page 433 16.4.2007 2:34pm Compositor Name: BMani
Plant Life in Antarctica 433
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14
Facilitation in Plant
Communities
Ragan M. Callaway and Francisco I. Pugnaire
CONTENTS
Introduction ....................................................................................................................... 435
Mechanisms........................................................................................................................ 436
Shade .............................................................................................................................. 436
Soil Moisture .................................................................................................................. 438
Soil Nutrients.................................................................................................................. 439
Soil Oxygenation ............................................................................................................439
Protection from Herbivores ............................................................................................ 440
Pollination ...................................................................................................................... 441
Mycorrhizae and Root Grafts ........................................................................................ 441
Interactions between Facilitation and Interference ............................................................ 442
Are Benefactor Species Interchangeable? ........................................................................... 447
Positive Interactions and Community Theory.................................................................... 448
Conclusion.......................................................................................................................... 449
References .......................................................................................................................... 450
INTRODUCTION
Until the last decade, the importance of positive relationships among plant species have been
underestimated in community ecology, perhaps based on broader perspectives on the indi-
vidualistic nature of communities (Callaway 1997). However, rapidly accumulating evidence
for common and strong facilitative effects in communities (Callaway 1995, Bruno et al. 2003)
have led to reconsideration of formal community theory and the rejection of strict individu-
alistic theory by some ecologists (Lortie et al. 2004).
Traditional models for plant interactions have emphasized competition, assuming that
plants must compete for always-limiting resources, such as water, nutrients, light, space, or
pollinators, and try to overthrow each other when in proximity. However, a large amount of
experimental evidence for interspecific positive interactions has accumulated, suggesting that
old conceptual models for the forces that structure communities are inadequate. The fact that
different species of plants may benefit each other when growing together has attracted the
interest of ecologists, and the number of papers reporting, or somehow involved with, positive
interactions has grown considerably in the recent years.
Neighboring plant species may compete with one another for resources, but they may also
provide benefits for neighbors such as shade, higher nutrient levels, more available moisture,
soil oxygenation, protection from herbivores, a more favorable soil microflora, shared
resources via mycorrhizae, and increased pollinator visits (Callaway 1995), resulting in
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435
interactions that can be cumulatively positive for at least one of the species involved.
Positive interactions, or facilitation, occur when one plant species enhances the survival,
growth, or fitness of another, and have been demonstrated in virtually all biome types
(DeAngelis et al. 1986, Hunter and Aarssen 1988, Bertness and Callaway 1994, Callaway
1995, Callaway and Walker 1997, Tirado and Pugnaire 2005) though they have been regarded
in the past as interesting anecdotal curiosities rather than principles fundamentally important
to communities (Bertness and Callaway 1994).
Facilitation affects plant community structure and diversity in very different ways than
competition. Competitive interactions limit coexistence among species, and competition-
based theory focuses on how species avoid competitive exclusion (Lotka 1932, Gause 1934,
Hardin 1990, Hutchinson 1961). Coexistence in a world dominated by competition has been
attributed to niche partitioning (Parrish and Bazzaz 1976, Cody 1986), variation in the
physical environment and subtle differences in competitive advantages, disturbance that
continuously provides competition-free microhabitat and alters competitive hierarchies
(McNaughton 1985), heterogeneity in the ratios of limiting resources that alter competitive
hierarchies (Tilman 1976, 1985, 1988), the development of local and species-specific resource
depletion zones that, under certain conditions, do not strongly affect the resources available
to neighbors (Huston and DeAngelis 1994, Grace 1995), and spatial structures that suggest
niche facilitation (Van der Maarel et al. 1995). In contrast to the suite of theories that attempt
to explain species coexistence despite competition for the few resources that are shared by all
plants, positive interactions may directly promote coexistence and increase community diver-
sity (Kikvidze et al. 2005, Michalet et al. 2006).
MECHANISMS
S
HADE
The benefits of shade include maintenance of plant tissues below lethal or near-lethal
temperatures, decreasing respiration costs, lowering transpirational demands by decreasing
the vapor pressure difference between leaves and air, reduction of ultraviolet irradiation,
and increased soil moisture due to lower evaporative demand. These benefits may, but do
not have to, come at the cost of reduced energy for photosynthesis. For the cost of shade to
exceed its benefit, shade must be below the photosynthetic saturation point of the benefi-
ciary species. If not, the beneficiary can get a free lunch because it cannot use any
photosynthetically active radiation (PAR) above the saturation point anyway. Many species
reach their maximum photosynthetic rates at PAR levels far below the general natural
maximum (2000 mmol m
2
s
1
). These species may benefit from the effects of taller
neighbors on leaf temperature and transpirational loss without any cost of decreased carbon
gain. For example, Arnica cordifolia is a perennial herb that is commonly found in the
understory of conifer forests in the northern Rocky Mountains. Young and Smith (1983)
found that a 30% decrease in light on the forest floor during cloudy days in the Medicine
Bow Mountains of Wyoming resulted in a 37% increase in carbon gain for Arnica and an
84% reduction in transpiration. They found that the photosynthetic rates of Arnica
remained near saturation even on cloudy days because of its low PAR saturation point,
thus Arnica gained from the lower transpiration rates associated with decreased light levels
without a carbon cost.
Milena Holmgren and colleagues (1997) took these potential cost-benefit trade-offs into
account by modeling the relative importance of shade from a nurse plant as a facilitative effect
or a competitive effect depending on the synergy between shade and moisture in a plant’s
environment. Assuming that plant growth is a relatively simple product of light and moisture,
and that soil moisture is affected by canopies to a greater degree in xeric environments than in
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436 Functional Plant Ecology
mesic environments, they argued that plant growth increases as light increases. However, in
xeric environments increasing light is correlated with rapidly decreasing soil moisture, and
plant growth decreases at higher light intensities. This sets the stage for shade-derived facilita-
tion in water-limited environments and decreased likelihood for such facilitation in mesic
environments.
Indeed, the importance of shade has been emphasized in deserts where many species of
cacti and other succulents may depend on nurse plants when they are young because seedlings
have low surface-to-volume ratios and dissipate heat inefficiently, and exposure of these
seedlings to exceptionally hot temperatures on the desert floor may be fatal (Figure 14.1).
For example, saguaro seedlings are sheltered and facilitated by many different species of
perennial plants, but predominantly by Cercidium microphyllum (Niering et al. 1963, Turner
et al. 1966, 1969, Steenberg and Lowe 1969, 1977). Young Ferrocactus acanthodes cacti may
experience 118C decrease in maximum stem surface temperatures in the shade of nurse plants
(Nobel 1984). Valiente-Banuet and Ezcurra (1991) compared the relative importance of
protection from predation and shade in the nurse plant relationship between Neobuxbaumia
tetetzo, a columnar cactus, and Mimosa luisana in the Viscaino Desert and the Gran Desierto
de Altar in Mexico. They found that cages improved survival, but that long-term survival was
restricted to shade treatments. In a perennial community in the Chihuahua Desert, Silvertown
and Wilson (1994) found more positive associations between species than expected for a
random assemblage, and concluded that community structure relied on species whose estab-
lishment was dependent on conditions provided by other species. This is also evident in a wide
variety of communities, from deserts to tropical savannas to high mountains (Tirado and
Pugnaire 2005).
Facilitative shade effects are not restricted to deserts. For example, herbaceous species in
California oak savannas also show strong preferences to either understory or open micro-
habitats. Parker and Muller (1982) demonstrated higher shade tolerance of Bromus diandrus
and Pholistoma auritum, two species apparently facilitated by Quercus agrifolia (an evergreen
oak), than that of Avena fatua, a species common in the open. In laboratory experiments,
B. diandrus had a higher relative growth rate at low light than A. fatua (Mahall et al. 1981).
Maran
˜
o
´
n and Bartolome (1993) conducted experiments in which whole soil blocks were
FIGURE 14.1 Young saguaro cactus under the canopy of a paloverde tree in the Sonoran Desert, USA.
Much older saguaros can be seen in the open, beyond the tree canopy. (Photo by Alfonso Valiente-Banuet.)
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Facilitation in Plant Communities 437
transplanted between the understory of coast live oak, adjacent open grassland, and artificial
shade treatments. They found that herbaceous species typically found in open habitats in
California oak savannas were limited by canopy shade. In some cases, the overstory oaks
themselves require shade from nurse plants when they are young. Callaway (1992) tested the
facilitative effects of shade and seedling predation on the survival of Quercus douglasii
(a winter-deciduous oak) seedlings using unshaded and shaded cages. Unshaded cages
reduced mortality rates, but eventually all unshaded seedlings died, whereas 35% of shaded
and caged seedlings survived for 1 year.
Gradients of both radiation reaching the soil and soil temperature provided by canopies
may allow different species to coexist in the more heterogeneous understory environment.
Moro et al. (1997) demonstrated how several herbaceous species positioned themselves
differently under the canopy of Retama sphaerocarpa, a leguminous shrub, in response to
several gradients including irradiance and temperature. Radiation at soil level in a central
position under the canopy was 60% of that outside, and temperature difference reached 78C
between both the positions.
Shade may also have indirect facilitative effects. Shade provided by salt-tolerant species
in salt marshes appears to reduce evaporation from subcanopy soils and consequently
maintain lower soil salinities than in those soils exposed to direct insolation (Bertness and
Hacker 1994, Callaway 1994). Bertness (1991) and Bertness and Shumway (1993) experimen-
tally manipulated soil salinity in the upper zones of a New England salt marsh and found that
Distichlis spicata, a salt-tolerant colonizer of saline bare patches, facilitated the growth of
Juncus gerardi when soil salinities were high. When soil salinities were artificially reduced by
watering, growth of Juncus was not improved by Distichlis. Similarly, Bertness and Hacker
(1994), Bertness and Yeh (1994), and Hacker and Bertness (1996) found that shade provided
by marsh elder shrubs (Iva frutescens) decreased soil salinity and facilitated the growth and
survival of J. gerardi.
SOIL MOISTURE
The water relations of one species may be enhanced by the presence of another species.
Joffre and Rambal (1993) measured a significant delay in soil water loss under Quercus
rotundifolia and Quercus suber in Spanish savannas relative to soils in open areas between
the trees. They argued that increased soil moisture was accountable for large differences in
species composition under trees and in the open. Generally, moisture conditions in the
understory are enhanced by overstory plants (Petranka and McPherson 1979, Maranga
1984, Vetaas 1992), but sometimes the reverse is true. Pugnaire et al. (1996a) found that R.
sphaerocarpa shrubs in southern Spain had higher water potentials when Marrubium
vulgare occupied the understory than that when the understory was bare ground. This
effect was observed in spring but not in summer, suggesting that the presence of a dense
understory helped to retain rainfall water in the soil mound that accumulated under
the shrub.
In North American shrub steppe, Artemisia tridentata (Great Basin sage) transports water
from deep, moist soils to dry surface soils during the night via hydraulic lift (Richards and
Caldwell 1987). Additional experiments using stable isotope analysis indicated that water
from hydraulic lift was distributed to neighboring plants, although the magnitude of water
transferred was small Caldwell (1990) and Dawson (1993), however, used similar techniques
to investigate the magnitude of hydraulic lift conducted by Acer saccharum and the effects of
the hydraulically lifted water on understory plants. He found hydraulically lifted water in all
understory plants he examined, with the proportional use of hydraulically lifted water ranging
from 3% to 60%. Plants that used large proportions of hydraulically lifted water had more
favorable water relations and growth than those that did not.
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438 Functional Plant Ecology
SOIL NUTRIENTS
Soils directly beneath the canopies of perennials are often richer in nutrients than those in
surrounding open spaces without perennial cover. Subcanopy soil enrichment may occur as a
result of nutrient pumping (sensu Richards and Caldwell 1987), as deep-rooted perennials
take up nutrients unavailable to shallowly rooted plants and deposit them on the soil surface
via litterfall and throughfall. In addition, perennial canopies may trap airborne particles that
are eventually deposited at the base of the plant (Pugnaire et al. 1996b, Whitford et al. 1997).
Nutrient enrichment may also occur indirectly via nitrogen fixation.
Enrichment of soil nutrients (and often a corresponding change in species composition
and increased productivity) has been reported under perennials in many systems throughout
the world, but these effects have been described most often in savannas and other semiarid
regions with clearly demarked understory and open microhabitat (Patten 1978, Schmida and
Whittaker 1981, Yavitt and Smith 1983, Weltzin and Coughenhour 1990, Callaway et al.
1991, Vetaas 1992, Belsky 1994). Nutrient enrichment has also been reported in more mesic
systems including alder shrublands (Goldman 1961), Patagonian shrublands (Rostagno et al.
1991), and forest-pasture ecotonehs of Central America (Kellman 1985).
Pugnaire et al. (1996a) reported a facilitative mutualism between the shrub R. sphaerocarpa
and the herb M. vulgare based on improvements in soil nutrients and water. Marrubium plants
under Retama had greater leaf-specific area, leaf mass, shoot mass, leaf area, flowers, higher
leaf nitrogen concentration, and more nitrogen per plant than those that were not near a
Retama shrub. Conversely, Retama shrubs with Marrubium underneath them had larger
cladodes, greater total biomass, nitrogen content, and higher shoot water potentials than
those without Marrubium in the understory, suggesting that facilitation could be bidirectional
rather than unidirectional.
Experimental studies of the relationship between soil enrichment via litterfall and
enhanced growth of plants or species shifts are less common. Turner et al. (1966) found that
saguaro seedlings survived better on soil collected from under paloverde trees (C. microphyllum)
than on those from under either mesquite (Prosopis juliflora) or ironwood (Olneya tesota).
Monk and Gabrielson (1985) found that addition of litter from the floor of deciduous forests in
South Carolina generally improved the overall productivity in understory plots, but the effects
of litter on individual species ranged from facilitation to interference. Soils under Q. douglasii
canopies are much more nutrient rich than those in the surrounding open grassland (Callaway
et al. 1991), and improve the growth of B. diandrus, an annual grass in the understory, in
greenhouse tests when compared with open grassland soils. Walker and Chapin (1986) demon-
strated facilitative effects of nitrogen-rich soil from under Alnus tenuifolia on Salix alaxensis
and Populus balsamifera seedlings. In a second experiment in Glacier Bay, Alaska, they found
that Alnus sinuata and Dryas drummondii, both nitrogen fixers, had strong positive effects on
the growth of Picea sitchensis (Chapin et al. 1994).
Moro et al. (1997) showed that the interaction between Retama and its understory
vegetation was strongly affected by gradients of litter accumulation and decomposition,
both of which influenced species composition. The abundance of annual herbs produced a
more favorable habitat for soil micro-organisms that increased mineralization rate, enhanced
litter decomposition, and increased nutrient dynamics under Retama shrubs. Litter has both
positive and negative effects on plant growth, as has been shown also elsewhere (Facelli 1994,
Hoffmann 1996).
SOIL OXYGENATION
Wetland emergent plants often passively transport oxygen from leaves to roots through
aerenchymous tissues to alleviate belowground oxygen limitation (Armstrong 1979). In some
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