Download Biodiversity and ecosystem functioning: It is time for dispersal

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.