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Journal of Vegetation Science 17: 543-547, 2006 © IAVS; Opulus Press Uppsala. FORUM - Biodiversity and ecosystem functioning: It is time for dispersal experiments - 543 FORUM Biodiversity and ecosystem functioning: It is time for dispersal experiments Zobel, Martin*; Öpik, Maarja1,2; Moora, Mari3 & Pärtel, Meelis4 Institute of Botany and Ecology, University of Tartu, 40 Lai St., Tartu 51005, Estonia; address: Scottish Crop Research Institute, Errol Road, Invergowrie, DD2 5DA Dundee, UK 1E-mail [email protected]; 3E-mail [email protected]; 4E-mail [email protected] *Corresponding author; E-mail [email protected] 2Present Abstract The experimental study of the relationship between biodiversity and ecosystem function has mainly addressed the effect of species and number of functional groups. In theory, this approach has mainly focused on how extinction affects function, whereas dispersal limitation of ecosystem function has been rarely discussed. A handful of seed introduction experiments, as well as numerous observations of the effects of long-distance dispersal of alien species, indicate that ecosystem function may be strongly determined by dispersal limitation at the local, regional and/or global scales. We suggest that it is time to replace biodiversity manipulation experiments, based on random draw of species, with those addressing realistic scenarios of either extinction or dispersal. Experiments disentangling the dispersal limitation of ecosystem function should have to take into account the probability of arrival. The latter is defined as the probability that a propagule of a particular species will arrive at a particular community. Arrival probability depends on the dispersal ability and the number of propagules of a species, the distance a species needs to travel, and the permeability of the matrix landscape. Current databases, in particular those in northwestern and central Europe now enable robust estimation of arrival probability in plant communities. We suggest a general hypothesis claiming that dispersal limitation according to arrival probability will have ecosystem-level effects different from those arising due to random arrival. This hypothesis may be rendered more region-, landscape- or ecosystem-specific by estimating arrival probabilities for different background conditions. Keywords: Arrival probability; Ecosystem function; Diaspore; Invasion; Propagule; Seed; Species diversity; Species pool. Introduction There is an increasing consensus that biodiversity significantly influences ecosystem function (Hooper et al. 2005; Srivastava & Vellend 2005), including stocks of energy and materials (e.g. biomass), fluxes of energy or materials (e.g. productivity, decomposition), and the stability of rates or stocks over time (Pacala & Kinzig 2002). The relationship between biodiversity and ecosystem function implies that a reduction in biological diversity (variety of species, genotypes, etc.) will cause a reduction in ecosystem-level processes. Synthetic experimental communities, exhibiting different levels of species diversity and functional group diversity, have been the most widely used object to investigate the relationship between biodiversity and ecosystem function. In very general terms, research on biodiversityecosystem function has so far focused mainly on how extinction affects ecosystem function (Loreau et al. 2001; Schmid & Hector 2004; Srivastava & Vellend 2005). Although the role of arrival sequence (Grime 1998) or recruitment limitation in gaps (Symstad & Tilman 2001) in determining ecosystem function has been discussed, and the arrival sequence has been shown to influence species composition (Ejrnæs et al. 2006), the setup of experiments with synthetic communities has not incorporated natural processes like dispersal limitation. At the same time, we know that the species composition and diversity of natural plant communities may be significantly dispersal-limited (Tilman 1997; Stampfli & Zeiter 1999; Zobel et al. 2000; Foster 2001; Foster & Dickson 2004; Lord & Lee 2001; Xiong et al. 2003). Since species functional characteristics strongly influence ecosystem function (Grime 2001; Garnier et al. 2004; Lavorel & Garnier 2002; Diaz et al. 2004), the differential arrival of species may influence ecosystem properties even if the arrival of species is a random 544 Zobel, M. et al. process. But some species typically arrive earlier, and plant traits that enhance dispersal may be non-randomly associated with other functional traits (Leishman & Westoby 1992; Díaz & Cabido 1997; Díaz et al. 2004; Grime 2001). In this context, a more general question arises: to what extent is ecosystem function limited by dispersal? In landscapes under human influence, ecosystems become increasingly fragmented, and the dispersal of many species is inhibited (Fahrig 2003; Honnay et al. 2005; Helm et al. 2006). At the same time, the dispersal of other species is enhanced by human activities and a ‘McDonaldization’ of the biosphere (Lövei 1997) takes place – a limited set of species become common and abundant over several continents. The interrelationship between dispersal and ecosystem function is evidently a topic that deserves further discussion. Examples of relevant questions are how much do we know about dispersal limitation of diversity, what are the hypotheses about the role of dispersal limitation as a determinant of ecosystem function, and what kind of research is needed to approach this topic. Without intending to answer these questions, our contribution aims to discuss the dispersal limitation of ecosystem function, and the possible design of experimental studies addressing the nature of this relationship. What do we know? In many cases, the community species pool represents a subsample of the local or regional species pool due to dispersal limitation (Zobel 1997; Pärtel et al. 2000). The experimental introduction of the missing members of the regional pool into a local community may identify the intensity of dispersal limitation for each particular stand. In addition to the change in local diversity, the introduction of propagules may also change an ecosystem’s functioning. According to our knowledge, there are still only a handful of experimental studies showing that plant dispersal at the landscape scale may shape the functional properties of ecosystems like above-ground primary productivity. For example, Wilsey & Polley (2003) demonstrated that sowing 20 native prairie species in subhumid grasslands decreased aboveground productivity, primarily because of a decrease in the share of highly productive C4 grasses in the community. Although all of the sown species belonged to the regional species pool, the distribution of most of them was strongly fragmented due to either habitat loss or habitat change. On the other hand, Foster et al. (2004) demonstrated that FORUM the experimental sowing of species from the regional species pool into an abandoned hay field was accompanied by increases in biodiversity and local plant production across the natural productivity gradient. In this case, the diversity of the available propagule pool constrained ecosystem productivity by determining the availability of key species, and by governing opportunities for functional compensation within the community. The experiments described above show that dispersal limitation at the landscape level has the potential to induce moderate alterations in the functional parameters of a local ecosystem. Observations of the effects of introductions of alien species illustrate the effect of dispersal limitation at the biogeographic scale. The most dramatic examples of the effects of species crossing of former dispersal barriers probably come from oceanic islands in general and the Hawaiian Islands in particular. These islands have the highest level of endemism of any floristic and faunistic region in the world, whilst native ecosystems have developed in conditions of the absence of several ecologically important groups, such as ants, rodents, mammalian carnivores and ungulate herbivores, throughout history (Loope & Mueller-Dombois 1989). The introduction of alien species can be considered to be ‘natural experiments’ showing how crucial dispersal limitation at the biogeographical scale can be in determining ecosystem function, including nutrient cycling and decomposition (Mack & D'Antonio 2003; Asner & Vitousek 2005; Rothstein et al. 2004), and flammability (Freifelder et al. 1998; Mack et al. 2001; Cabin et al. 2002). A frame for further studies The examples described above lead us to hypothesize that ecosystem function is dispersal-limited. In order to make this hypothesis more specific, we shall introduce concept of arrival probability. This term, which has been used earlier in a more specific context to characterize the outcome of particular dispersal events (e.g. Jackson 1981; Alcantara & Rey 2003), can be defined as the probability that a propagule of a particular species will arrive in a particular community. Arrival probability is thus a parameter integrating characteristics of a particular species and a local target community. We may express arrival probability with the help of a general equation: arrival probability = f (dispersal probability, distance from source, landscape permeability) FORUM - Biodiversity and ecosystem functioning: It is time for dispersal experiments - Dispersal probability as a specific characteristic is determined by the interaction of two factors: the number of dispersal units (propagules), and the dispersal ability of a single propagule (Willson & Traveset 2000; Eriksson 2000). Dispersal ability (Eriksson 2000), also expressed as dispersal curve (Greene & Calogeropoulos 2002) or dispersal potential (Tackenberg et al. 2003), is the ability of a propagule of a particular species to move in space. In addition, arrival probability depends on two more parameters – the distance a propagule has to disperse, and the properties of landscape(s) across which a propagule has to disperse – its permeability (Jules & Shahani 2003; Haynes & Cronin 2003) or resistance to movement (Ricketts 2001). In summary, the larger the number of propagules of particular species and the better their dispersal ability, the closer the propagule source to the target community and the easier the migration across particular landscape(s), the higher the arrival probability in a particular target community. Having this concept in mind, one may develop general hypotheses regarding the ecosystem-function consequences of dispersal limitation at different scales. For example, the primary hypothesis could be the following: dispersal limitation according to arrival probability will have ecosystem-level effects different from those arising due to random arrival. This hypothesis may be further rendered more region-, landscape- or ecosystem-specific by estimating arrival probabilities for different background conditions (Pärtel 2006). Also, one may hypothesise that dispersal limitation acts only at the level of functional groups, and not on the level of species. The hypotheses suggested above may be put to test using biodiversity-manipulation experiments. When the focus is on the recovery of the ecosystem in formerly disturbed habitats, the use of synthetic communities may be justified. Another option is to manipulate natural plant communities. Removal experiments have been suggested for addressing the effect of local extinctions on ecosystem function (Díaz et al. 2003). In contrast, propagule addition experiments (Zobel & Kalamees 2005) may represent appropriate tools when the recovery of ecosystem from former extinction, or the effect of alien species, is addressed. Both propagule introduction and design of synthetic communities have to mimic not only a random sample from a species pool, but probable sequences of species arrival. Species-poor communities will consist of species with high arrival probability, while communities with high richness will gradually come to include species whose arrival is relatively improbable. 545 Experiments may address the diaspore limitation at different spatial scales. They may mimic dispersal limitation within a community, local or regional species pool (sensu Zobel 1997). In such cases, the colonisation of free sites after disturbance, or recolonization after local extinction, may be addressed. Alternatively, one may also address the dispersal limitation at a biogeographic scale and the possible effect of the dispersal of those species that do not have a long evolutionary history of coexistence with local species. For example, Petryna et al. (2002) introduced propagules of invasive species into differently managed grassland ecosystems. One may extend this design and add propagules of introduced alien or naturalised aliens species, or even propagules of species that are likely to be introduced. Is it realistic to estimate arrival probability? The core element of planning the experiments described above is the relevant estimation of arrival probabilities. There is accumulating information about the traits determining arrival probabilities of plant species in target communities, especially for certain regions with well-studied floras like northwestern or central Europe. Seeds are the main dispersal propagules for vascular plants and seed production is a key element of estimating dispersal probability. In cases where there is no data available on seed production, one may use empirical evidence that within similar growth forms, log seed mass is linearly related to log seed number (Aarssen & Jordan 2001; Henery & Westoby 2001). Thus, when seed size is known, one can estimate the number of seeds produced annually (Westoby et al. 2002; Moles & Westoby 2004). Dispersal potential is enhanced considerably by the presence of the so-called dispersal syndromes, i.e. traits associated with dispersal by animals (zoochory), wind (anemochory) or water (hydrochory) (Ozinga et al. 2004). Dispersal syndrome may be deduced from seed morphology (Howe & Smallwood 1982) and used as a proxy of dispersal ability. Data about seed mass and dispersal syndrome for European vascular plant species may be derived from diverse databases (Seed Information Database: http://www. rbgkew.org.uk/data/sid, BiolFlor: http://www.ufz.de/biolflor/index.jsp, and Ecological Flora of the British Isles: http://www.york.ac.uk/ res/ecoflora/cfm/ecofl/). More complete information about seed production and dispersal potential of northwest European plant species will soon be available in the Leda database (Knevel et al. 2005). Background data about ecological requirements (Ellenberg et al. 1991; Klotz et al. 2002; Dahl 1998) and distribution 546 Zobel, M. et al. maps of plant species (Suominen 1999), as well as about the distribution of main habitat types in Europe (Davies & Moss 1999) provide information for realistic estimation of arrival probabilities at least within that continent. In summary, we suggest that it is high time for the incorporation of dispersal limitation issues into biodiversity-ecosystem function manipulative experiments, based on realistic estimates of arrival probabilities of species. Besides addressing relationships between biodiversity and ecosystem function, such experiments may contribute to the understanding of assembly rules of biological communities. In addition, this approach may not only provide new knowledge on an important theoretical topic, but also serve as a basis for a deeper understanding of the need for biodiversity conservation and restoration. Acknowledgements. This work was financed by EU FP6 project ALARM (GOCE-CT-2003-506675), Estonian Science Foundation (Grant No. 6614) and the University of Tartu (TBGBO0553). We would like to thank S. Díaz, D. Ackerly and three anonymous referees for constructive comments on the earlier versions of the manuscript. References Aarssen, L.W. & Jordan, C.Y. 2001. Between-species patterns of covariation in plant size, seed size and fecundity in monocarpic herbs. Ecoscience 8: 471-477. Alcantara, J.M. & Rey, P.J. 2003. Conflicting selection pressures on seed size: evolutionary ecology of fruit size in a bird dispersed tree, Olea europaea. J. Evol. Biol. 16: 1168-1176. Asner, G.P. & Vitousek, P.M. 2005. Remote analysis of biological invasion and biogeochemical change. Proc. Nat. Acad. Sci. USA 102: 4383-4386. Cabin, R.J., Weller, S.G., Lorence, D.H., Cordell, S., Hadway, L.J., Montgomery, R., Goo, D. & Urakami, A. 2002. Effects of light, alien grass, and native species additions on Hawaiian dry forest restoration. Ecol. Appl. 12: 15951610. Dahl, E. 1998. The phytogeography of Northern Europe. Cambridge University Press, Cambridge, UK. Davies, C. E. & Moss, D. 1999. EUNIS Habitat Classification, November 1999. European Environmental Agency. Díaz, S. & Cabido, M. 1997. Plant functional types and ecosystem function in relation to global change. J. Veg. Sci. 8: 463-474. Díaz, S., Symstad, A., Chapin III, F.S., Wardle, D.A. & Huenneke, L.F. 2003. Functional diversity revealed by removal experiment. Trends Ecol. Evol. 18: 140-146. Díaz, S., Hodgson, J.G., Thompson, K., Cabido, M., Cornelissen, J.H.C. et al. 2004. The plant traits that drive ecosystems: Evidence from three continents. J. Veg. Sci. FORUM 15: 295-304. Ejrnæs, R., Bruun, H.H. & Graae, B.J. 2006. Community assembly in experimental grassland: suitable environment or timely arrival? Ecology 87: 1225-1233. Ellenberg, H., Weber, H.E., Düll, R., Wirth, V., Werner, W. & Paulißen, D. 1991. Zeigerwerte von Pflanzen in Mitteleuropa. Scripta Geobot. 18: 1-248. Eriksson, O. 2000. Seed dispersal and colonization ability of plants – assessment and implications for conservation. Folia Geobot. 35: 115-123. Fahrig, L. 2003. Effects of habitat fragmentation on biodiversity. Annu. Rev. Ecol. Evol. Syst. 34: 487-515. Foster, B.L. 2001. Constraints on colonization and species richness along a grassland productivity gradient: the role of propagule availability. Ecol. Lett. 4: 530-535. Foster, B.L. & Dickson, T.L. 2004. Grassland diversity and productivity: the interplay of resource availability and propagule pools. Ecology 85: 1541-1547. Freifelder, R.R., Vitousek, P.M. & D'Antonio, C.M. 1998. Microclimate change and effect on fire following forestgrass conversion in seasonally dry tropical woodland. Biotropica 30: 286-297. Garnier, E., Cortez, J., Billes, G., Navas, M.-L., Roumet, C. et al. 2004. Plant functional markers capture ecosystem properties during secondary succession. Ecology 85: 26302637. Greene, D.F. & Calogeropoulos, C. 2002. Measuring and modelling seed dispersal of terrestrial plants. In: Bullock, J.M., Kenward, R.E. & Hails, R.S. (eds.) Dispersal ecology, pp. 3-23. Blackwell Publishing, Oxford, UK. Grime, J.P. 1998. Benefits of plant diversity to ecosystems: immediate, filter and founder effects. J. Ecol. 86: 902-910. Grime, J.P. 2001. Plant strategies, vegetation processes, and ecosystem properties. J.Wiley, Chichester, UK. Haynes, K. J. & Cronin, J. T. 2003. Matrix composition affects the spatial ecology of a prairie planthopper. Ecology 84: 2856-2866. Helm, A., Hanski, I. & Pärtel, M. 2006. Slow response of plant species richness to habitat loss and fragmentation. Ecol. Lett. 9: 72-77. Henery, M.L. & Westoby, M. 2001. Seed mass and seed nutrient content as predictors of seed output variation between species. Oikos 92: 479-490. Honnay, O., Jacquemyn, H., Bossuyt, B. & Hermy, M. 2005. Forest fragmentation effects on patch occupancy and population viability of herbaceous plant species. New Phytol. 166: 723-736. Hooper, D.U., Chapin III, F.S., Ewel, J.J., Hector, A., Inchausti, P. et al. 2005. Effects of biodiversity on ecosystem functioning: a consensus of current knowledge. Ecol. Monogr. 75: 3-35. Howe, H.F. & Smallwood, J. 1982. Ecology of seed dispersal. Annu. Rev. Ecol. Syst. 13: 201-228. Jackson, J.F. 1981. Seed size as a correlate of temporal and spatial patterns of seed fall in a neotropical forest. Biotropica 13: 121-130. Jules, E.S. & Shahani, P. 2003. A broader ecological context to habitat fragmentation: Why matrix habitat is more important than we thought. J. Veg. Sci. 14: 459-464. FORUM - Biodiversity and ecosystem functioning: It is time for dispersal experiments - Klotz, S., Kühn, I. & Durka, W. 2002. BIOLFLOR - Eine Datenbank mit biologisch-ökologischen Merkmalen zur Flora von Deutschland. Bundesamt für Naturschutz, Bonn, DE. Knevel, I.C., Bekker, R.M., Kunzmann, D., Stadler, M. & Thompson, K. 2005. The LEDA traitbase. Collecting and measuring standards of life-history traits of the Northwest European Flora. University of Groningen, Groningen, NL. Lavorel, S. & Garnier, E. 2002. Predicting changes in community composition and ecosystem functioning from plant traits: revisiting the Holy Grail. Funct. Ecol. 16: 545-556. Leishman, M. R. & Westoby, M. 1992. Classifying plants into groups on the basis of associations of individual traits – evidence from Australian semi-arid woodlands. J. Ecol. 80: 417-424. Loope, L.L. & Mueller-Dombois, D. 1989. Characteristics of invaded islands, with special reference to Hawaii. In: Drake, J.A., Mooney, H.A., Di Castri, F., Groves, R.H., Kruger, F.J., Rejmánek, M. & Williamson, M. (eds.) Biological invasions. A global perspective, pp. 257-280. John Wiley, Chichester, UK. Lord, L.A. & Lee, T.D. 2001. Interactions of local and regional processes: species richness in tussock sedge communities. Ecology 82: 313-318. Loreau, M., Naeem, S., Inchausti, P., Bengtsson, J., Grime, J.P. et al. 2001. Biodiversity and ecosystem functioning: current knowledge and future challenges. Science 294: 804-808. Lövei, G.L. 1997. Global change through invasions. Nature 388: 627-628. Mack, M.C. & D’Antonio, C.M. 2003. Exotic grasses alter controls over soil nitrogen dynamics in a Hawaiian woodland. Ecol. Appl. 13: 154-166. Mack, M.C., D'Antonio, C.M. & Ley, R.E. 2001. Alteration of ecosystem nitrogen dynamics by exotic plants: a case study of C4 grasses in Hawaii. Ecol. Appl. 11: 1323-1335. Moles, A.T. & Westoby, M. 2004. Seedling survival and seed size: a synthesis of the literature. J. Ecol. 92: 372-383. Ozinga, W.A., Bekker, R.M., Schaminée, J.H.J. & van Groenendael, J.M. 2004. Dispersal potential in plant communities depends on environmental conditions. J. Ecol. 92: 767-777. Pacala, S. & Kinzig, A.P. 2002. Introduction to theory and the common ecosystem model. In: Kinzig, A.P., Pacala, S. & Tilman, D. (eds.) Functional consequences of biodiversity: empirical progress and theoretical extensions, pp. 169-174. Princeton University Press, Princeton, US. Pärtel, M. 2006. Data availability for macroecology: how to get more out of regular ecological papers. Acta Oecol. 30: 97-99. Pärtel, M., Zobel, M., Liira, J. & Zobel, K. 2000. Species richness limitations in productive and oligotrophic plant communities. Oikos 90: 191-193. Petryna, L., Moora, M., Nuñes, C.O., Cantero, J.J. & Zobel, M. 2002. Are invaders disturbance-limited? Conservation of mountain grasslands in Central Argentina. Appl.Veg. Sci. 5: 195-202. Ricketts, T.H. 2001. The matrix matters: effective isolation in 547 fragmented landscapes. Am. Nat. 158: 87-99. Rothstein, D.E., Vitousek, P.M. & Simmons, B.L. 2004. An exotic tree alters decomposition and nutrient cycling in a Hawaiian montane forest. Ecosystems 7: 805-814. Schmid, B. & Hector, A. 2004. The value of biodiversity experiments. Basic Appl. Ecol. 5: 535-542. Srivastava, D.S. & Vellend, M. 2005. Biodiversity-ecosystem function research: is it relevant to conservation? Annu. Rev. Ecol. Evol. Syst. 36: 267-294. Stampfli, A. & Zeiter, M. 1999. Plant species decline due to abandonment of meadows cannot easily be reversed by mowing. A case study from the southern Alps. J. Veg. Sci. 10: 151-164. Suominen, J. 1999. The state of Atlas Florae Europaeae – past and present. Acta Bot. Fenn. 162: 1-3. Symstad, A. & Tilman, D. 2001. Diversity loss, recruitment limitation, and ecosystem functioning: lessons learned from a removal experiment. Oikos 92: 424-435. Tackenberg, O., Poschlod, P. & Bonn, S. 2003. Assessment of wind dispersal potential in plant species. Ecol. Monogr. 73: 191-205. Tilman, D. 1997. Community invasibility, recruitment limitation, and grassland biodiversity. Ecology 78: 81-92. Westoby, M., Falster, D.S., Moles, A.T., Vesk, P.A. & Wright, I.J. 2002. Plant ecological strategies: some leading dimensions of variation between species. Annu. Rev. Ecol., Evol. Syst. 33: 125-159. Willson, M. & Traveset, A. 2000. The ecology of seed dispersal. In: Fenner, M. (ed.) The ecology of regeneration in plant communities, pp. 85-110. CAB International, Wallingford, UK. Wilsey, B.J. & Polley, H.W. 2003. Effects of seed additions and grazing history on diversity and productivity of subhumid grasslands. Ecology 84: 920-931. Xiong, S., Johansson, M.E., Hughes, F.M.R., Hayes, A., Richards, K.S. & Nilsson, C. 2003. Interactive effects of soil moisture, vegetation canopy, plant litter and seed addition on plant diversity in a wetland community. J. Ecol. 91: 976-986. Zobel, M. 1997. The relative role of species pools in determining plant species richness: an alternative explanation of species coexistence? Trends Ecol. Evol. 12: 266-269. Zobel, M. & Kalamees, R. 2005. Diversity and dispersal – can the link be approached experimentally? Folia Geobot. 40: 3-12. Zobel, M., Otsus, M., Liira, J., Moora, M. & Möls, T. 2000. Is small-scale species richness limited by seed availability or microsite availability? Ecology 81: 3274-3282. Received 24 October 2005; Accepted 19 June 2006. Co-ordinating Editor: S. Díaz.