Community Ecology of Absent Species: Hidden and Dark Diversity Meelis Partel€
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Journal of Vegetation Science && (2014) SPECIAL FEATURE: VEGETATION PATTERNS AND THEIR UNDERLYING PROCESSES Community ecology of absent species: hidden and dark diversity Meelis Partel€ Keywords Abstract Absent species; Community composition; Dark diversity; DNA; Ecological community; Missing Community ecologists have so far focused mainly on species identified at a species; Species diversity; Species pool; site. I suggest that we can understand better patterns and their underlying Species richness processes in ecological communities if we also examine those species absent from the sampled community. However, there are various types of absences, Received 19 September 2013 which all harbour different information. Hidden diversity comprises species Accepted 22 January 2014 that are absent from our sight: dormant or locally very rare species over- Co-ordinating Editor: Rein Kalamees looked by traditional sampling. Fortunately, modern DNA-based techniques can help us to find hidden species when analysing environmental samples. Partel,€ M. ([email protected]): Institute of Depending on habitat type and sampling scale, a large number of co-existing Ecology and Earth Sciences, University of species might be hidden. Dark diversity comprises absent species that consti- Tartu, Lai 40, Tartu, 51005, Estonia tute the habitat-specific species pool. Dark diversity can be determined based on data on species distribution, dispersal potential and ecological require- ments. If we know both observed and dark diversity, we can estimate com- munity completeness and infer those processes that determine which species in the species pool actually co-exist locally. In addition, most species in the world do not actually belong to the habitat-specific species pool of the com- munity: their ecological requirements differ or their distribution area is else- where. Such other absent species are usually not directly relevant to a particular community. However, knowing ecologically suitable species from other regions can give early warning of possible future invasion of alien spe- cies (alien dark diversity). To conclude, species presences have meaning only if there are absences (and vice versa). Methods to detect absent species are rapidly developing and will soon form a standard toolbox for community ecology. allow community ecologists and conservation practitioners Introduction to better understand community patterns and their under- An ultimate goal of community ecology is to understand lying processes. why different sites host different species (Vellend 2010). Species absent from a particular community sample pro- Studies of ecological communities have concentrated pri- vide valuable information. Without absences, all samples marily on observations of species found in local sites. Spe- host the same species and the table can be represented as a cies identified in a set of ecological communities are simple species list. There is no reason why species absences typically listed in species 9 sample tables. If species compo- cannot be used instead of presences; it is simply a matter of sition varies among samples, these tables also feature tradition that we count presences in a species 9 sample absences. In fact, absences are usually more frequent than table. Ultimately the maximum number of absences in a presences in such tables. Scientists generally focus on spe- species 9 sample table is the total global flora or fauna. cies presences to examine variation in species diversity and For example, there are currently 283 556 accepted names community composition. Present species are also segre- of vascular plant species (www.theplantlist.org, accessed gated into groups of different functional types, alien or Dec 2013). An Estonian wooded meadow holds the world threatened species, etc. Here I outline the importance of record for the number of vascular plant species within a species absences and suggest how various types of absences 10 9 10 cm plot: 25 rooted species (Kull & Zobel 1991; Journal of Vegetation Science Doi: 10.1111/jvs.12169 © 2014 International Association for Vegetation Science 1 Community ecology of absent species M. P€artel Wilson et al. 2012). The very same plot also holds the Twenty years ago, Eddy van der Maarel and Martin world record for the lowest number of species absences at Sykes proposed the Carousel Model (van der Maarel & that scale, ‘just’ 283 531 (i.e. 283 556–25) absent species. Sykes 1993) after examining 10 9 10 cm permanent Why are these species absent? This question is by no plots in dry calcareous grasslands in Sweden. They noticed means as trivial as it might seem. Some absent species are high small-scale species mobility: each subsequent year found adjacent to the 10 9 10 cm plot. Several species revealed the appearance and disappearance of several spe- common to wooded meadows in the region are absent cies in all permanent plots. This was especially surprising both in the plot and its close vicinity. Moreover, most spe- since most species were perennial. Species moved around cies absent from the 10 9 10 cm plot inhabit other conti- like children on a merry-go-round. This high small-scale nents, other biogeographic regions or simply other mobility was originally attributed to the short life span of habitats, e.g. wetlands or seashores. Consequently, by dis- plant individuals and frequent regeneration from the seed tinguishing relevant types of absences, we can make the bank. However, community recruitment from seeds observed diversity – recorded presences – much more use- depends on favourable local conditions and can be highly ful. For simplicity, I shall neglect species abundances, but it stochastic (Eriksson & Froborg€ 1996). More recent is theoretically possible to account for this as well, e.g. research has stressed the importance of the below-ground when working with the effective number of species (Hill bud bank (Klimesova & Klimes 2007). Some plant species 1973). Here I present an overview of different types of can stay dormant below ground, sometimes for several absences representing hidden diversity and dark diversity, years (Reintal et al. 2010). In temperate grasslands, often as well as an overview of other absent species that might more than 75% of plant biomass is below ground in com- ‘stalk’ our study sites. plex symbiosis with other trophic levels (Jackson et al. 1997; Steinaker & Wilson 2005; Mokany et al. 2006). This means that a plant community might be more of a below- Hidden diversity ground phenomenon than often realized. How many We can expect that some species from our sampled area plant species actually co-exist in soil? Do above-ground (or volume) remain unobserved. I call this set of species plant community patterns reflect those below ground? hidden diversity, because these species are not in fact These aspects of vegetation science have been badly absent from the sample, but merely absent from observa- neglected because, until recently, plant roots and rhi- tion. At larger spatial scales, it is also likely that some rare zomes of different species were mostly indistinguishable. species remain overlooked (Gaston et al. 1997). Several Current DNA-based methods have started to shed light on methods, however, are available to estimate if sampling is this phenomenon (Partel€ et al. 2012). We have used the sufficient, e.g. species accumulation curves based on sam- next-generation sequencing to identify plant species in ples or individuals, rarefaction curves with resampling, temperate grasslands in 10 9 10 9 10 cm volume below Jackknife and Chao estimates which incorporate multiple the soil surface, the horizon where most roots in grass- subsamples (Gotelli & Colwell 2001; Cao et al. 2007). lands are located (Hiiesalu et al. 2012). We found that These methods can estimate how many species have been small-scale plant species richness below ground is up to overlooked but do not inform us of the identity of hidden twice that above ground. When we examined the whole diversity. Current developments in environmental DNA 2-ha grassland (cumulative data from several samples), metabarcoding have hinted that such methods might be there were still a number of species found only below sensitive enough to detect some rare species missed by tra- ground. All these species belonged to the local species pool ditional sampling (Taberlet et al. 2012; Ji et al. 2013; Zhan and were recorded in the study site in previous years. At et al. 2013). The potential and limitations of new DNA- the sampling time, however, they were present only in based methods await further testing. the soil. In addition, there are different species co-exis- When the sampling area is small, it is likely that all indi- tence patterns above and below the ground: more biotic viduals are counted and all species are observed above assembly rules were detected above ground, whereas the ground at any given time. At the same time, some species below ground part was largely determined abiotically in the community simply cannot be recorded by traditional (Price et al. 2012). Even relationships with other commu- visual inspection. This is readily apparent for mobile organ- nity properties such as productivity, heterogeneity or dis- isms; members of an ecological community might be turbance regime might differ between above- and below- absent temporarily (e.g. foraging for food). Sessile plants, ground realms (Partel€ et al. 2012). For example, if the however, can also be temporarily absent above ground. above-ground richness decreases with increasing soil fer- Species can be dormant, e.g. existing at the time of sam- tility, the number of species only found below ground pling as vegetative rhizomes or roots in the soil, or as part increases; hence, the total richness is independent of soil of the active seed bank. fertility (Hiiesalu et al. 2012). Journal of Vegetation Science 2 Doi: 10.1111/jvs.12169 © 2014 International Association for Vegetation Science M. P€artel Community ecology of absent species The recent knowledge of hidden diversity provides a ful- from astrophysics, where dark matter is the term for the ler picture of co-existing species.