Intraspecific variability in the context of ecological ... - Science Direct

Vol. 1/2, pp. 221–237 © Gustav Fischer Verlag, 1998

Perspectives in Plant Ecology, Evolution and Systematics

Intraspecific variability in the context of ecological restoration projects Jelte van Andel Laboratory of Plant Ecology, University of Groningen, P.O. Box 14, 9750 AA Haren, The Netherlands; email: [email protected]

Abstract Population differentiation within species is a common phenomenon. The question raised in this review is whether such variability should be recognized while making a choice for populations as sources for the (re)introduction of species into former or novel environments. To estimate the ecological importance of population differentiation in the context of restoration projects, I reviewed literature in which the results from (reciprocal) sowing and transplant experiments are reported. This survey reveals that survival of the transplants (one of the earliest recognizable fitness components) is almost entirely site-dependent, while the fitness of surviving plants (measured in terms of growth and fecundity) is frequently higher for native plant populations as compared to alien populations of a species. Phenological timing is sensitive to selection and rather difficult to recover in an adequate way. As far as fitness reduction is concerned, it can be stated that this is a minor effect in comparison to the complete lack of a species from the restoration site; however, the credits and debits of quantity vs. quality of the members of a population cannot yet be estimated scientifically. Comparative experiments in restoration projects would help in solving this problem. The suitability of environmental conditions for the species and the accessibility of the dispersal units to the restoration site are actually thought to be the major constraints. Key words: intraspecific variation, reciprocal transplants, restoration ecology, site and population effects

Introduction Restoration ecology Restoration ecology has emerged as a distinct discipline during the last decade, representing the scientific background for a new development in nature conservation. Restoration of degraded sites, either degenerated seminatural ecosystems or sites temporarily used for agriculture or industrial activities, calls for the application of appropriate theory and knowledge. Current theories, however, have not been developed with such applications in view and may, therefore, be inappropriate. An example may illustrate this. If, for socio-political reasons, an agricultural site is

abandoned, and authorities in charge of nature conservation are required to restore the site to a particular type of seminatural grassland, several problems may arise: 1. Are current theory and knowledge about dispersal capabilities of seeds and about seedbank dynamics adequate to predict which plant species will become established at the site? To cope with this question the concept of regional, local and community species pools has been developed; for reviews, see for example Zobel (1997) and Zobel et al. (1998).

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2. Do current theory and knowledge of plant species responses to environmental factors (pH, nutritional status, hydrological regimes, pollutants) suffice to estimate the chances for germination and establishment of plant species at the site in question, assuming their propagules are available? For example, can Ellenberg’s indicator values (Ellenberg et al. 1991), which have been largely derived from observations in well developed (semi)natural communities, be used to predict potential vegetation development at an empty and degraded site? For such a purpose comparative experiments are indispensable, including reintroduction experiments (Sarrazin & Barbault 1996). 3. Do current theory and knowledge of population differentiation and evolutionary processes give a clue about the way in which seed sources can be artificially utilized in restoration management? This is the most critical part of any choice of reference systems: should intraspecific variation be taken into consideration? To answer this and similar questions, debates about nominalistic or biological or evolutionary species concepts (Mayr 1988) are not very helpful, though they may be of high scientific interest. Rather we have to answer the question of the way in which man is taking an active part in plant evolution once particular restoration practices are adopted (Brown 1994). This question is the subject of the present review.

The dilemma Population differentiation is a generally recognized phenomenon (Bradshaw 1984). Since the famous publications of Turesson (1922, 1925) and Clausen et al. (1939, 1940), and later reviews on genecology by HeslopHarrison (1964) and Langlet (1971), the importance of such differentiation has been clear. Taken literally, it could be argued that the notion of restoration implies to reverse the process of evolution that has produced local differentiation, though nobody would argue for such an approach to reference systems. Rather, we should let knowledge of history guide our path to the future. While ecologists can apply their theoretical understanding to restoring communities and species, geneticists are supposed to help in solving the problem of how to restore genotypes. The im-

portance of this distinction can be elucidated by referring to two comments from the provocative paper of Brown (1994). Quoting Lande (1988), Brown states that there is little evidence that lack of genetic variation has hindered restoration projects or caused the failure of a reintroduced population (though he recognizes that there is much room for additional experimentation and model validation). Later, however, he suggests that transplantation of individuals among distinct subpopulations may not only endanger the success of the introduced individuals but may compromise the variability of the entire population as maladaptive genes are introduced into the new population. In fact, these two statements are not contradictory, because for the first survival would be the appropriate measure of fitness, while for the second fitness measures such as growth and fecundity are required. The question thus arises as to whether restoration aims only at the survival of established plants, or at maintaining a particular level of fitness of the surviving plants as well. Which choice do nature managers have as long as scientific information is so confusing? How can we mimic nature in the case of intentional dispersal of propagules? Is it sufficient to trust the classical axiom that ‘every species is everywhere, waiting for selection by the environment’? In The Netherlands this idea, expressed in terms of ‘Beijerinck’s law’, is still taught in schools and adopted by nature managers. Or should we accept the evidence that most dispersal of seeds and fruits is over short distances, even though they may have apparently dispersal promoting traits (e.g. Hodkinson & Thompson 1997; Poschlod & Bonn 1998)? While recognizing intraspecific variability as a result of evolutionary processes, there are two extreme options in restoration projects. The first is to create another founder population from a neighbouring population of any species which we want to establish at the restoration site. Alternatively, we can introduce seeds from a large number of populations of the particular species wanted, which together represent the entire within-species variation, and wait for habitat selection. Pegtel (1998) explores the problem of how to make a choice for seed sources with a focus on biogeographically central and marginal populations of rare vascular plant species. In this paper I focus on relatively small-scale differentiation among popula-

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tions, because the majority of propagules do not travel large distances (Poschlod & Bonn 1998). I do not consider the question of which mechanism has been responsible for population differentiation, but only – given a certain differentiation – the extent to which this is ecologically relevant in restoration projects.

Common environment experiments The taxonomic species concept can be applied for ecological purposes only through experiments. For this purpose Turesson (1922) used common garden experiments, Hall (1932) and Clausen et al. (1940, 1948) reintroduced the reciprocal transplant experiments, using cloned materials to compare the fitnesses of populations. Though the use of cloned plants is to be preferred for genetic reasons, the option of using seeds or seedlings as transplant units is closer to natural processes in the case of annual plants. To tackle the question I would like to answer in this review, viz to what extent such variation is relevant in restoration projects, I selected from the literature those papers that apply reciprocal transplantation techniques to compare the survival and fitness of native and alien populations. In this type of experiments all transplant sites have proven to be a suitable habitat for the species. The common garden experiment is not useful for the present purpose, because proof of habitat suitability is missing; in a common garden all populations are alien and detection of genetic variation does not address directly questions about the potential adaptive nature of such variation (Rice & Mack 1991). Only if a common natural site is chosen for comparison of transplants, has the adaptive value been taken into consideration. Population differentiation due to climatic contrasts is outside the scope of restoration projects, even if the contrasting populations occur at relatively short distances, such as is the case for Dryas octopetala from a snowfree fell field and a snowbank in an area in Alaska (McGraw 1987), and for central and marginal populations of Ranunculus lingua in Scandinavia (Johansson 1994).

Reciprocal transplant experiments Before starting our survey, it is important to recognize that the studies mentioned have

been performed to demonstrate local adaptation through differentiation, whereas our problem concerns whether such differentiation should be recognized in restoration projects. In general, the pattern of differentiation depends on the outcome of the interplay between directional selection (tending to enhance differences) and migration (tending to reduce differences); in plants, because of their essentially sedentary nature, migration can be easily overruled by selection (Bradshaw 1984). According to Bradshaw (1984) the crucial question is not whether differences between populations are adaptive, but whether the differences we find in different populations enable each to survive better in its own original environment than the other populations. This would be direct evidence of adaptation, rather than interpreting as adaptive some characteristics that may be present for historical reasons. For comparisons of material from different environments a reciprocal transplant design is adequate. For the purpose of the present paper, I will use the extant information to discuss the consequences of transplantations to restoration sites.

Seeds and seedlings The use of seeds as population sources is usual for annuals, but it has also been applied for perennials, because the germination and early establishment are the primary parameters to test the existence of safe sites (Harper 1977; Urbanska 1997). I distinguish here two aspects of plant responses: (1) fitness components such as survival and fecundity, (2) phenology, e.g. timing of germination and flowering.

Fitness components Differences in fitness components between populations of a species can in many cases be due to phenotypic plasticity. In such cases, transplantation does not involve, as far as current knowledge can reveal, any risk of the transport of maladaptive genes. For example, caryopses from three populations of the winter annual grass, Catapodium rigidum were sown in six sites, representing a range of climatic variation and of substrates in the United Kingdom (Clark 1980). There were significant differences between sites but not between populations in the number of cary-

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opses produced and in yield. Soil factors largely determined differences in yield between the various sites. However, growthroom experiments also revealed genetically based differences between the populations. There was no evidence, either from the transplant or from the growth-room experiment, that each of the C. rigidum populations was best adapted to its site of origin. Another example of the high phenotypic plasticity of a winter annual grass is the case of Phleum arenarium in response to, e.g. nutrients, in the coastal dunes of The Netherlands (Ernst 1981, 1983). Similarly, Cheplick’s (1988) reciprocal transplant study of the annual cleistogamous peanutgrass Amphicarpum purshii in the New Jersey Pine Barrens revealed that the effects of the site on shoot dry weight and production of aerial spikelets, subterranean spikelets, and seeds (produced on the same individual) were generally much more significant than the effects of population origin. In general, phenotypic plasticity responds to both artificial and natural selection (Scheiner 1993), so it would be interesting to know whether the populations differ in genetically based plasticity. Ecotypic differentiation may be considered to contrast with phenotypic plasticity. Pegtel (1976) investigated Sonchus arvensis, a rosette-forming perennial, and distinguished between a coastal type, taxonomically designated as S. arvensis var. maritimus, and an arable type, designated as S. arvensis var. arvensis. Prior to transplantation, plants were raised from achenes, hardened for a fortnight, and transplanted to three sites in the coastal area of The Netherlands: an outer dune site (native site of the coastal type), a less nutrient-poor inner dune site, and a ploughed and fertilized site potentially suitable for the arable type. The arable type was not capable of establishing and growing at the outer dune site. Both varieties survived well on both the inner dune site and the arable site. Dry shoot weights indicated that both varieties reacted in a similar manner on the inner dune and arable sites, which implies that, provided that the plants survive (which depends on the origin of the population), performance is mainly site-specific. In many studies, it is not clear whether ecotypic differentiation has been recognized. I will, therefore, use the more general term population differentiation. Schemske (1984) investigated two populations of Impatiens

pallida, a selfing annual herb of deciduous forests. Seedlings were collected from field sites in Allerton Park (Central Illinois, USA) and grown in a shaded glasshouse for population differentiation studies. For the reciprocal transplant experiments in a riparian forest and a prairie grove seeds were used which were the F2-progeny of one individual from each of the glasshouse-grown families. Highly significant population differentiation was observed at both localities (growth-room experiment), but reciprocal transplant experiments indicated local adaptation only at the prairie grove location. The author stated that the processes leading to the genetic subdivision of these highly inbred populations vary considerably between localities, probably due to selfing followed by drift in small neighbourhoods as well as local natural selection. Another reciprocal transplant study in the field, using seedlings from one population of Impatiens pallida and three populations of I. capensis in Mont St. Hilaire (Québec, Canada), was performed by Schoen et al. (1986). All four sites were located in wet areas in beech-maple forest and separated from one another by 0.5 to 1 km. Survival and fruit production were studied in designs where the neighbouring transplant individual was of the same species or of the opposite species. The within-species (I. capensis with conspecific neighbours) reciprocal transplant series revealed that differences in survivorship and fruit production by cleistogamous flowers were attributable primarily to the effect of conspecific neighbours. Plants surrounded by neighbours from the site of origin produced significantly more fruit from chasmogamous flowers as compared with plants surrounded by neighbours from the alien site. In the between-species reciprocal transplant series, the fitness parameters measured were site-dependent. Van Groenendael (1985) described a comparison between two populations of the perennial rosette-forming Plantago lanceolata, reciprocally sown in dry and wet home sites in coastal dune grassland in The Netherlands. Seeds from both populations survived better in the dry site, and seeds from the dry site did better in both habitats. The interaction between site and origin, which suggests local adaptation, was significant only after taking into account the effects of size and depth of burial. In a parallel experiment, using shoots propagated vegetatively from


leaves, each site was planted with 10 genotypes, each represented by 20 shoots. Strong site effects dominated the first few months. After the first year, an interaction became significant, again with the strongest contrast in survival being for the plants from the wet site. In an earlier study on Plantago lanceolata in Durham County (Northern Carolina), Fowler & Antonovics (1981) had shown within-population differentiation resulting from smallscale environmental heterogeneity, e.g. density effects on transplants. Seedling performance of progeny families of Phyteuma nigrum from three differentsized populations was studied by Boerrigter (1995) by comparing their performance after transplanting 8-weeks old, pregrown seedlings into two sites differing in habitat quality. Both site and population effects were significant for survival in the first growing season. There was no sign of a population x site interaction, either for survival or for performance of surviving plants. Site effects accounted for a larger proportion of the total variation in performance, represented by the number of leaves and the diameter of the thickened root (wintering organ), than the population effect, and this was also the case for survival. Pooled over all populations, plants performed better at the higher-quality meadow site than at the lower-quality road verge site, and pooled over the two sites progeny from the largest populations (native at the meadow site) performed best. The picture that emerged was that both survival and performance of surviving individuals were determined to a large extent by site effects, and that both site and population effects are important for the surviving individuals. Local adaptation could not be demonstrated due to a lack of population x site interactions. Dijk & Grootjans (1998) report on the experimental introduction of juvenile plantlets of four marsh orchid species of the genus Dactylorrhiza along a productivity gradient which included their home sites. They interpreted the survival after one year of the introduced plantlets as related to the ecology of adult plants in the field. Survival was to a minor extent determined by the fresh weight of the seedlings at the start of the experiment. Interspecific differences in survival became apparent within the plots, where species survived significantly better in the plots closest to their home sites. Apparently, the relatively finely tuned optimum environment for juvenile

orchids is almost similar to that of adult plants. This result emphasizes once more that site conditions are the first priority in restoration if introductions are to have any chance of success.

Phenological timing Ter Borg (1972, 1985) investigated two populations of the annual species Rhinanthus serotinus (now called R. angustifolius), a vernal population growing in a hay meadow, and an autumnal population in an extensively grazed pasture. The reciprocal sowing experiment showed that, despite good seedling establishment, the introduced alien ecotypes hardly ever succeeded in establishing populations. Usually the plants did not even produce seeds. Apparently, flowering time of the aestivals was adapted to the constant mowing regime, and autumnals cannot cope with such a regime. Only if mowing was postponed to late summer could the autumnals perform fairly well in aestival habitats. For the vernal population the autumnal habitat may not have been sufficiently stable and uniform. Using a one-season reciprocal transplant design, Lotz & Blom (1986) demonstrated that plants of Plantago major from a riverbank population flowered earlier than plants from a seashore meadow. In a later paper, Lotz (1990) published the results from a 2-year experiment in The Netherlands, but using five populations belonging to two subspecies. Seedlings were grown from bulk samples of seeds grown from each of the five populations, prior to transplantation into the field sites. Again, plant survival appeared to depend largely on the location of transplantation. The age at first flowering differed between sites and populations of origin. Three different selection regimes were demonstrated: plants had the highest fitness if they had flowered early and were large, flowered early and were small, or flowered late and were large. He concluded that the betweenpopulation differences in age and size at first reproduction corresponded generally with the different selection regimes before and after initiation of flowering, as became apparent from the selection differentials of several traits. Rice & Mack (1991) investigated survival and reproduction of the annual grass Bromus tectorum (cheatgrass), where it had invaded the arid Intermountain West region of North

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America. Seeds collected from seven sites were sown at all sites in each of three years of the experiment. The sites represented an environmental gradient from arid steppe to mesic subalpine forest. Patterns of survival and emergence were strongly influenced by the local environment. In contrast, relative differences in flowering time among seed sources were stable across sites and years, populations from the arid steppe being the earliest to flower. Using net reproductive rate as an integrative index of fitness, local adaptation could only be detected in the environmentally most extreme habitats which were the driest and most saline desert steppe site and the coolest, most mesic forest site. As to annuals in general, Mahn (1989) distinguished three types of tactics associated with adaptation to anthropogenically altered environments which constrain the period of growth and seed production: (1) germinate earlier, (2) reproduce earlier, and (3) maintain a shorter life cycle in general. Reciprocal transplant experiments with pregrown seedlings in eastern Germany revealed evidence for each of these tactics. The first was shown by ecotypic differentiation in the winter annual Veronica hederifolia. Subspecies lucorum occurs in woodland. Subspecies hederifolia is a plant of agro-ecosystems and showed an earlier start to growth. A similar adaptation was found for Sinapis arvensis ssp. orientalis. In Lapsana communis the second tactic was developed, with a shorter reproductive period in a field population as compared to a woodland population. The third tactic was established in populations of the summer annual Polygonum lapathifolium from agro-ecosystems; as compared to ruderal populations these plants had a shorter period of vegetative growth. Selection on time of emergence and seedling performance within a population of the perennial rosette forming Lychnis flos-cuculi was investigated by Biere (1991b, 1996). He used seeds from a full 8x8 dialled cross of eight genotypes from one field population, resulting in 64 progeny families including eight families of selfed progeny. Relative growth rates (RGR) varied significantly among progeny families, both in nutrient-rich and in nutrient-poor conditions (Fig. 1a). Differences in RGR among families were due to variation in both the rate of biomass production per unit leaf area (NAR), and the investment in leaf area per unit plant weight (LAR), two

basic components of RGR (Fig. 1b). Variation in LAR among families was mainly governed by differences in the amount of leaf area per unit leaf weight (SLA). Each of the RGR-components showed a significant plastic response to differences in the level of nutrient supply. To test whether inherent differences in growth parameters are associated with fitness components under field conditions, sixteen seeds of each family were sown in four sites (A–D; Fig. 2) including the native site C, in a hayfield along a natural gradient of soil fertility in a brook valley in The Netherlands. Rank correlations between growth parameters and survivorship were generally not significant. Likewise, correlations between growth parameters and plant size in the field were generally not significant, although their direction tended to vary with soil fertility. From a glasshouse experiment, using the same families, Biere (1991a) concluded that selec-

Fig. 1. (A). Mean RGR values of families of outcrossed progeny families of Lychnis flos-cuculi, ranked in ascending order for nutrient-rich (closed circles) and nutrient-poor (open circles) conditions. Horizontal bars indicate groups of families that differ significantly in RGR. Vertical bars indicate 95% confidence limits. (B). Path coefficients between RGR and its components in two nutrient conditions for outcrossed progeny families of Lychnis flos-cuculi. After Biere (1991c); cf. also Biere (1996).


Fig. 2. Cross section of the Drentsche Aa brook valley basin and the location of the study sites used for transplant studies of Lychnis flos-cuculi; site C is the site of the source population; sites A to D represent a gradient of increasing productivity. After Biere (1991b,c).

tion shortly after emergence mainly favours particular maternal genotypes, indicating no particular advantage of sexual reproduction, while selection later in the life cycle may act upon zygotic genotypes. He found consistent differences among maternal genotypes in the degree of variation in the time to germination, suggesting that selection could operate to favour polymorphic or uniform behaviour. In contrast to the glasshouse results, maternal effects on plant size in the field appeared to persist until the end of the growing season, possibly partly carried over from differences in germination time, whereas the genotype of the zygote explained only a small proportion of the variation in plant size that was dependent on the site of growth (Biere 1991c). In the field, however, other interesting patterns

were shown, which could not be predicted from the laboratory experiments (see Table 1). The percentage of emergence was significantly highest in the home site, as well as the survivorship. The average performance of progeny from selfed plants was substantially reduced compared to that of individuals from outcrossed parents. In outcrossed progeny, early emerging seedlings had significantly higher survivorship than later emerging seedlings, and significant directional selection for early emergence was observed, independent of sites episodes, in contrast to selection intensity which varied among sites (even within sites) and episodes. No family x environment interaction was present for germination time. Directional selection is probably slow due to contrasting effects of paternal and maternal

Table 1. Effects of site on time and percentage of seedling emergence, survivorship after three episodes of selection, and plant size of outcrossed families of Lychnis flos-cuculi, sown into four sites including the home site C (see Fig. 2). After Biere (1991b). Site

Seedling emergence Survivorship (%) –––––––––––––––––––– –––––––––––––––––––––––––––––––––––––––– Time* % May 87 June 87 Oct 87 Overall June 87 Oct 87 June 88

Size (mg) ––––––––––––––––––– Oct 87 June 88

A B C D

19.7a 19.9a 19.0a 21.4b

0.3a 8.7b 11.5c 8.1b

*Days after 1 May 1987.

80.6b 82.6bc 86.8c 68.8a

74.6a 96.9c 97.9c 89.1b

3.5a 28.8c 46.2d 12.9b

0.0a 31.6b 71.6c 72.5c

0.0a 8.8b 32.4c 8.3b

– 48.6a 58.9b 120.7b

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genotype on emergence time and its low heritability, and to family x environment interactions. On a phenotypic level, effects of emergence time on survival and plant size of seedlings were significant. However, differences in survivorship and plant size among progeny groups diminished with time; differences had levelled off in the second year (Biere 1991b).

Clonal perennials Tillering plants In order to investigate physiological differentiation in Agrostis tenuis, Bradshaw (1960) transplanted samples of sixty tillers of a number of populations into five experimental plots established in various natural habitats within a relatively narrow environmental range (10–2500 ft altitude) in the Aberystwyth region of Wales. Two populations were also grown on lead- and zinc-contaminated soil. The tillers, pregrown in soil from the experimental sites, were planted into cleared, cultivated and fenced plots in each of the contrasting habitats. Observations were then carried out for a number of years. Bradshaw concluded that the population differentiation shown in the transplant experiment, including both morphological and physiological differentiation, was of a magnitude and pattern analogous to that earlier found in morphological studies in a uniform environment. There are populations with widely different attributes within the relatively small geographic region studied; some attributes are highly differentiated, others only little. Remarkable differentiation was established amongst populations resistant to lead and zinc. These transplant experiments have shown population differentiation, rather than local adaptation. Rapson & Wilson (1988) studied Agrostis capillaris (= A. tenuis) in New Zealand, where the species is an exotic. Using tillers derived from five ecologically wide-ranging populations in a reciprocal transplant design, they found no strong evidence for genetic adaptation to local site conditions. Davies & Snaydon (1976) published the results from reciprocal transplants of three pairs of contrasting populations of Anthoxanthum odoratum, collected from the Park Grass Experiment at Rothamsted (England). Approximately 25 plants, taken at random from each of six plots, were grown in boxes and then planted in a garden bed for cloning

purposes. One hundred ramets, each of two tillers, were collected at random from each population; 50 of these were transplanted into the native plot of the population and the other 50 into the plot of the contrasting paired population. Plant survival and number of tillers were measured over a period of 18 months. The largest coefficients of selection occurred on plots characterized by large annual yield and tall vegetation in summer. These plots received heavy applications of fertilizer and lime. The lowest selection coefficient occurred on plots with small annual yield and short vegetation. Populations collected from plots with tall vegetation were taller and more tolerant of low light conditions than populations from plots with short vegetation. In most cases, plants survived longer and produced more tillers and more dry matter when transplanted into their native plots than when transplanted into ecologically contrasting plots. The average half-life of plants transplanted into contrasting plots was eight months, that of plants in their native plots was estimated at about two years. The authors concluded that selection pressures acting upon A. odoratum in the mosaic of environments that occur on the Park Grass Experiment are large and sufficient to account for morphological and physiological differences that had been observed between closely adjacent populations on the plots. Similarly, Grant & Anthonovics (1978) showed substantial phenetic differentiation (with respect to a series of morphological traits as well as biomass partitioning and seed size) between an ecologically central (old field) population and an ecologically marginal (adjacent woodland) population of Anthoxanthum odoratum in North Carolina, despite gene flow between the two populations. The ecologically marginal population had a higher turnover rate and life expectancy was shorter than the ecologically central population, while in the central population the age distribution was strongly skewed in favour of older individuals. The paper, however, describes no test by reciprocal transplants. Platenkamp (1990) reported the results from a reciprocal transplant experiment with clonal replicates of A. odoratum populations from a relatively wet (mesic) and a relatively dry (xeric) site in a northern Californian grassland. He followed the survival, reproductive output and growth of the transplants for three growing seasons. Variations


in survival of second or third generation clonal descendants were determined entirely by the environment and showed no betweenpopulation genetic differences. Variation in annual reproductive output was mainly under genetic control in the first year (xeric populations flowered earlier and realized a higher reproductive output), but was almost completely environmentally determined in the second and third years. Population differentiation in Agrostis stolonifera was shown experimentally by Aston & Bradshaw (1966). Twenty populations from maritime habitats in Wales were cultivated as spaced plants, and stolon length was recorded after a nine week growing period, partly with replication of individual genotypes. The authors concluded that high coeffcients of selection are operating in the natural habitats of A. stolonifera, which are sufficient to initiate the differentiation of the populations and to maintain it against considerable gene flow. These studies leave no room for doubt about the existence of genetic population differentiation. The question now is whether such differentiation can be proven to be of ecological significance, by applying reciprocal transplant techniques. Kik (1987) sampled 50 tillers from each of three populations of A. stolonifera in The Netherlands, an inland meadow, a polder (former salt marsh), and a sand dune population. These were grown in a glasshouse for cloning purposes. Isozyme analysis revealed that the sampled inland meadow population comprised 14 genotypes, the polder population 35 genotypes, and the sand dune population 37 genotypes. These genotypes were analysed in a glasshouse experiment for their relative growth rates, and in a reciprocal transplant design for their local adaptation as measured by survival and growth characteristics (Kik et al. 1991). Relative growth rates of each of the cloned genotypes were tested at low and high nitrogen supply (Fig. 3), thus revealing information on genetic variability and plasticity. The inland meadow population showed the lowest genetic variation and the highest plasticity in reponse to nitrogen, while the polder population showed highest genetic variation and also a significant genotype x nitrogen level interaction. Though these results could be interpreted in terms of local adaptation, no correlations between RGR and survival of genotypes within the populations

were found in transplant experiments in the field; this implies that genotype differences in RGR do not necessarily indicate an adaptation to any habitat, even at the home site (see also van Andel & Biere 1990). Two weeks prior to the actual transplant, each genotype was subdivided into single tillers in the glasshouse and, after a short period of pregrowth to initiate the formation of new tillers, the tillers were transplanted into the four field sites from which the genotypes originated. Each genotype was represented in each site by a single tiller. Survival, growth, and fecundity was censused for two years. The analysis of life-history traits among populations, including the rate of survival (Fig. 4), showed that they were determined by transplant site (environmental) factors to a much greater extent than by population (genetical) factors. Indications of a genetical component were found as well. Overall, survival of the polder population (a colonizing population which showed intermediate and variable values for a number of vegetative growth components and produced the highest number of inflorescences) tended to be highest.

Fig. 3. Mean RGR values of genotypes from three populations of Agrostis stolonifera grown at two nitrogen levels over six weeks. Single genotypes are connected with a solid line. After Kik et al. (1991).

Survival (%)

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Fig. 4. Site-specific surviorship in three populations of Agrostis stolonifera (meadow: open circle, polder: closed circle, sand dune: triangle). Means and standard errors are shown. Native populations are indicated by a bold line. After Kik et al. (1991).

Several reciprocal transplant experiments have revealed phenotypically plastic responses. Santelman (1991) investigated factors influencing the distribution pattern of Carex exilis, which is considered an indicator of minerotrophic conditions in midcontinental bogs and fens, along the Atlantic coast of North America. Reciprocal-transplant gardens were established at four peatlands in Minnesota and Nova Scotia. Twenty plants from each field site were split into quarters, which were transplanted into the four sites, including the native site. They were left for two years and then harvested. For most of the growth variables measured, the effect of transplant site was more significant than the site of origin. Plants from all populations studied could complete their life cycle in coastal bogs, coastal fens and midcontinental fens, but not in midcontinental bogs. There were no signs of ecotypic differentiation. Another case of phenotypic plasticity was shown by Thompson et al. (1991), who investigated population variation in Spartina anglica in relation to vegetation succession. Ten clones were collected from each of the pioneer, coalesced sward and mature zones of the Dee estuary salt marsh (Cheshire, UK). These clones were grown for six months in a heated glasshouse prior to transplantation into the field sites. The clonal replicates exhibited a large amount of environmentally determined variation (phenotypic plasticity) for fitness characteristics such as survival, tiller number,

biomass, rhizome bud production. Furthermore, there was significant variation between and within these populations in their response to environmental heterogeneity, which provides strong evidence for the existence of inherent differences in plasticity in relation to successional status. A third case of phenotypic plasticity refers to the coastal dune slack plant Scirpus americanus in Cape Henlopen State Park in Delaware. Seliskar (1990) reciprocally transplanted clumps of plants from two sites differing in waterlogging and sand accretion, to determine the role of heredity in plant height along environmental gradients represented by areas of lower and higher elevation. Again, environmental factors rather than hereditary traits were more important in accounting for the differences in plant morphology expressed in the field. A similar conclusion followed from the results of Wang & Redman (1996), who transplanted tillers and seedlings of Hordeum jubatum from three sites with contrasting salinity regimes in Saskatchewan (Canada) and measured survival, growth and fecundity within the year of transplantation. Fecundity was, however, greatest when the populations were grown at their site of origin.

Rosette-forming plants Snaydon was the first to involve competition experiments in some kind of a transplant design, not so much to investigate competitive


abilities in itself but to enhance potential site effects by including a biotic component. In a study on Trifolium repens, Snaydon (1962) used populations from highly calcareous to markedly acid soil in Great Britain. He sampled 25–30 plants from each of five populations and grew them for at least three months on potting compost before they were used as sources for the experiments, thus minimizing carry-over effects. Four rooted cuttings were planted per pot (four from one population or 2 × 2 from two contrasting populations) and grown in an unheated glasshouse on soils from three different sites (pH 8.9, 5.5 and 4.6, respectively). Particularly striking was the difference between the acid and calcareous population types in susceptibility to chlorosis on the calcareous soil (‘lime-induced chlorosis’). Populations from contrasting soil types differed in their competitive growth on the contrasting soil types, especially under conditions of interpopulation competition. The calcareous population samples grew better than the acid population samples, both relatively and absolutely, on the chalk soil. The acid population samples grew relatively better than the calcareous population samples on the acidic soil as compared with growth on chalk soil. In no case, however, did acidic population samples yield absolutely more

than the calcareous population samples. Snaydon concluded, therefore, that it may be questioned whether the acidic populations ever outyield the calcareous populations even on acid soil. Competitive abilities of ‘biotypes’ of Trifolium repens, sampled from sites within a field of permanent grassland in Wales, were investigated by Turkington & Harper (1979) using a reciprocal transplant design. Cuttings were taken from three different clones in each of four sites in the experimental field, the sites being locally dominated by respectively Lolium perenne, Holcus lanatus, Cynosurus cristatus and Agrostis tenuis. These cuttings were rooted and propagated under glasshouse conditions, and after three months further subdivided and grown for one month prior to transplantation in pots containing soil from the field sites. The rooted shoots were then transplanted into plots in the field swards, either leaving the existing sward intact, or after destruction of the vegetation but leaving the soil intact. In addition, rooted shoots were planted in sown grass swards of the four species. This way, they could compare the effect of abiotic factors alone and the combined effect of abiotic and biotic factors (Table 2). In general, each clover ‘type’ performed best when grown in the site from

Table 2. Yields (g) of phytometers of Trifolium repens ‘types’ sampled from four sites in the experimental field and transplanted back into all combinations of ‘type’ and site; the performances of ‘type’ transplanted back into their original sites are shown in bold on the principal diagonal of each matrix; all values are the mean of three replicates. After Turkington & Harper (1979). Clover ‘type’

(a) Denuded plots T. repens (Lolium) T. repens (Holcus) T. repens (Cynosurus) T. repens (Agrostis) (b) Control vegetated plots T. repens (Lolium) T. repens (Holcus) T. repens (Cynosurus) T. repens (Agrostis) (c) Sown grass plots T. repens (Lolium) T. repens (Holcus) T. repens (Cynosurus) T. repens (Agrostis)

Sites dominated by Lolium perenne

Holcus lanatus

Cynosurus cristatus

Agrostis tenuis

169.6 106.0 146.1 92.9

90.0 125.4 102.3 112.0

103.0 109.4 140.0 138.5

77.4 116.5 61.9 107.5

0.51 0.30 0.50 0.57 64.8 25.4 30.2 39.7

0.05 0.35 0.08 1.15 18.3 32.3 22.3 32.7

0.53 0.34 0.87 1.29 27.1 29.0 68.4 38.9

0.24 0.94 0.20 1.83 49.1 27.5 43.2 71.9

232 J. van Andel

which it had originally been sampled (field sites), or in association with the grass species that dominated the site (artificially sown swards). The authors suggest that the most likely explanation of the experimental results is that micro-evolution of T. repens had occurred in response to the differing selection pressures exerted by the different species of grass (see also Turkington & Aarssen 1984). They can be considered, therefore, as ‘biotically-adapted strains’. Another clonal plant species, Ranunculus repens, was investigated by Lovett Doust (1981), who transplanted and replanted ramets directly from the field back to field sites, including plots in undisturbed grassland and woodland areas in Wales. Lovett Doust preferred this field-to-field method, because differences between populations would have been accentuated rather than minimized by pregrowing cultures in the glasshouse. Transplanted and replanted ramets were monitored for leaf demography. Ramets from the woodland population grew significantly faster when replanted in the woodland than when transplanted to the grassland; they produced a higher number of leaves and daughter ramets. In several respects plants from the grassland performed better in grassland than when transplanted into the woodland site; for example, they maintained a higher average birth rate of leaves and produced more daughter ramets. However, in other respects they performed almost as well in the alien woodland site as in their own native grassland. Plants of woodland origin transplanted to grassland had much shorter internodes than had woodland plants growing undisturbed, or replanted in woodland. Grassland plants transplanted to woodland showed increased internode length compared with grassland plants left undisturbed or replanted in grassland, but the internodes were not as long as those of the woodland plants in woodland. Leaf birth rates were generally increased by the transplant treatment, but the pattern of change in leaf birth rate in plants replanted in their native site followed that of undisturbed plants in each site. Apparently, transplanting in this study brought about a phenotypic shift in transplants in the direction of the native plants. Reciprocal transplant experiments were applied by van Tienderen & van der Toorn (1991) to study genetic differentiation and adaptation to local conditions in populations

of Plantago lanceolata at three different grassland sites in The Netherlands. Differences in components of seed yield, plant size, growth habit and timing of flowering were studied in populations from a dry hayfield, a wet hayfield, and a pasture grazed by cattle. In addition to experiments with seedlings to detect differences at the juvenile stage, they transplanted cloned material and monitored it for four years. Root cuttings were grown in the glasshouse on a potting soil/sand mixture for three months and then subdivided and pregrown for six weeks. Small cuttings were transplanted from 19 clones per population. Juvenile mortality may be severe, but it is generally not selective or only to a small extent. However, at both hayfields significant differences were found in the survival of the adult plants from the three populations. Local adaptation as measured by seed yield was pronounced, with very low yields from plants transplanted to an alien site. Several morphological traits differed among the three populations, of which the onset of flowering was considered to be adaptive. Hayfield plants flowered earlier than pasture plants, and plants from the early-mown hayfield flowered earlier than plants from the other hayfield. This suggests genetic differentiation. Biere (1995) produced over 50 clonal replicates from each of 24 genotypes from one population of Lychnis flos-cuculi in The Netherlands. Side rosettes, rooted prior to transplantation, were transplanted to four sites (Fig, 2, sites A–D) including the native site C, which together represented the productivity range of grasslands in which the species naturally occurs. At each site, three plots with four replicates of each of the 24 genotypes were planted. Survival, plant size and morphology, reproduction and allocation patterns were measured after the growing season and in the next year after wintering. Heterogeneity in both survivorship and fecundity was observed among sites. Although phenotypic plasticity explained the largest part of this variation, significant genetic variation was present as well. Autumn rosette size appeared to be a good predictor of both winter survival and fruit production in the next year. The intensity of fecundity selection on plant size was generally higher than the intensity of mortality selection. Mortality selection was closely associated with local survival schedules. Patterns of fecundity could not be


inferred from patterns of fruit production in the more productive sites. Highest reproduction and survival did not occur in the ‘home’ site of the clones in which the species was most abundant, but in a less productive part of the Calthion community (site B).

Evaluation in view of restoration ecology The problem to be solved A major goal of conservation biology is to prevent the extinction of species by human activities. One method currently being used to lower the risk of extinction is the intentional reintroduction of plant and animal species. In the Introduction I raised the question of the extent to which the currently observed population differentiation, resulting from microevolutionary processes, should be taken into account in restoration planning. According to Primack (1996) successful reintroduction mimics the natural processes of dispersal and establishment. So, where species are introduced just beyond their actual range but within the original biogeographical area, this can be considered an attempt to restore a former natural dispersal pattern. Moreover, the majority of species involved in intentional reintroduction are rare species which would generally not have the typical characteristics of a weedy species. On the other hand, Montalvo et al. (1997) state that use of proper genetic variants is becoming a more common concern in restoration planning, which implies the need to assess whether the use of single or multiple sources of seeds is the best strategy for initiating populations in novel environments. According to these authors, this may be especially valid for rare species in which genetic variance is supposed to be very low within a single source population. Pegtel (1998), focusing on recovery of rare vascular plants, argued that translocation of plants between central and marginal habitats is only acceptable if we apply our knowledge of the species’ biology and ecology. In particular, we need to take account of geographic history, breeding system, genetic variability, chromosome number, competitive interactions, life history, demography and habitat requirements. I suggested that the best information we can apply to help solving the dilemma – how

to make a choice for seed sources in restoration projects if ecological and genetic knowledge are insufficient – comes from transplant studies. However, before discussing the value of such experiments, we have to consider a methodological problem. Van Tienderen & van der Toorn (1991) recognized that it is difficult to deduce from the present composition of a population the processes that have taken place in the past to produce such a population. Their arguments have even more force when we attempt to predict future adaptations or understand failures from a reconstruction of past micro-evolutionary processes. According to Loveless & Hamrick (1984), selection factors vary in time and space in ways that cannot be directly anticipated by a plant population, and this local and idiosyncratic selection cannot be used to predict the genetic variation within and among populations. However, having recognized this problem we have to live with it. It is a problem inherent to restoration ecology in general, and also appears, for example, with regard to reference ecosystems. In the end we have to rely on ‘best professional judgement’ based on comparative observations.

Evidence from transplant experiments Transplant studies have shown, in general, that different fitness components have specific responses to local selection. Survival is a highly discriminative fitness component (yes/ no), while fitness components represented by growth and fecundity parameters can vary by degree. For this reason, I emphasize the distinction between the two. Survival of seedlings or pregrown plants depends mainly or almost entirely on environmental site factors. Site-dependent survival appears to be most extreme if climatic races or well-recognized ecotypes are involved in the transplant studies (e.g. Clausen et al. 1948), but it remains the dominant effect in within-region studies as well. So, from this point of view, there seems no need to consider the source population as an important concern in restoration projects. A certain species either does or does not become established, whatever the source population. The site is waiting for selection. However, we do need to consider the quality of the genotypes, in addition to the number of surviving phenotypes.

234 J. van Andel

If we exclude those cases where fitness differences could be explained by phenotypic-plastic responses to different environments (and recognizing that plasticity itself is the result of evolutionary processes; Scheiner 1993), the fitness of the surviving plants depends generally both on site factors and on the source population. In many cases, the survivors from native plant populations showed a higher fitness than surviving transplants of the same species from an alien population. Rarely did the mechanisms of local adaptation become apparent, and much is left unknown as far as site factors are concerned. In addition to abiotic factors, biotic interactions can play an important part, including processes such as competition, facilitation, mutualism, and herbivory. In my survey of the literature I have taken pains to describe the methods applied by the various authors. I am convinced that the specific results depend on whether, for example, plants have been pregrown in a common environment before being transplanted to the experimental field site or have been transplanted directly from one field site to another. However it is impossible to judge which could be the effect of one or another method, because the transplant studies have not been designed in a comparative way. An important difference, at least from a genetical point of view, but also in view of restoration success in restoration projects, is the choice for the introduction of seeds vs. the introduction of pregrown plants. Again, I cannot draw conclusions from the transplant experiments, because each author has applied only one preferred method, but without doubt there are big differences in survival. In summary, various pieces of evidence suggest that considerable differences in adaptation can be found, especially when assessed under natural conditions. Despite chance effects, whether or not alien material performs well or badly in a particular site depends on the degree of ecological and therefore evolutionary difference between the source and the planting site. The degree of evolutionary difference is likely to be greatest where the ecological factors have operated with severity over a long period; this is most most likely where there are soil and climate differences. Although differentiation is of the utmost interest genetically and ecologically, the practical question we face is whether the potentially reduced fitness of surviving trans-

plants be considered important in restoration planning.

Implications for restoration management To discuss the question raised in the Introduction – how to make a choice between using one source population when establishing a new population vs. using as many source populations as possible – I distinguish two risks: (1) the risk of introducing material with too little genetic variability (is there any lower limit?), and (2) the risk of introducing unwanted genotypes (is there any upper limit?). How can we reduce the risk of complete failure? The introduction of material of low genetic variability may have a low chance of success, which is not recommendable for practical reasons. As soon as restoration managers have an interest in the quality of the species to be restored, fitness components other than survival come into play. As we have seen, reduced fitness of plants from alien populations is common. The question arises, is there a lowest level of fitness of the population members for maintaining a sustainable population? A few preliminary remarks may be useful with regard to concerns about the fitness level that is required: (1) founder populations are not unnatural, (2) adaptive radiation, counteracting reduction in variability, is a common phenomenon, and (3) reduced fitness as compared to the optimum is still much higher than zero fitness, i.e. the case when the species is not present at all. Indeed, quality loss due to reduced fitness could be considered less important than the absence of a species at a restoration site. Yet, if suitably adapted populations can be recognized, it is desirable to use them (see McNeilly 1987). According to Loveless & Hamrick (1984), who studied causes of interpopulation diversity, and Linhart & Grant (1996) who reviewed small-scale differentiation among populations in response to environmental heterogeneity, life history and breeding systems are considered to represent primary constraints in the set of characters that are exposed to natural selection. As a large array of both life histories and breeding systems is represented among plant species in a community, generalizations useful for restoration at the community level are hard to make.


Breeding systems may vary even within plant species. From transplant experiments we have seen the adaptive value of the phenological timing from germination to seed set, which is apparently not easily recoverable. As the phenology of flowering directly affects fecundity, population differentiation in phenological timing may be considered an important constraint for restoration success. There is, however, an easier solution to reduce the risk of failure. Recognizing that population/site specificity is frequently found, a mixed source is always safer since it will ensure an adequate range of variability on which selection can act. This holds even more strongly if we take into account the ever changing environmental conditions during the course of restoration. Transplant experiments have shown that the introduction of seeds or plants from one population to another site (if it represents another potential habitat) can reveal a reduced fitness (even to zero), but they have never shown harmful results. If we really aim to mimic natural processes, we should accept Primack’s (1996) recommendation to carry out reintroduction efforts over several years, until a good year for colonization is encountered by chance. This approach may at the same time reduce the risk of low genetic variation. However, I would also like to define some upper limits. Zobel et al. (1998) confine their attention with regard to the target community in a restoration site to the regional species pool at most. Similarly, Hodder & Bullock (1997) reviewed translocations of native species within the United Kingdom, with a focus on the implications for biodiversity. A general conclusion is that, as long as restoration managers operate within a geographical region (cf. Primack 1996), they remain close to the natural dispersal potential of a species. This implies that it is not useful to transplant climatic or edaphic ecotypes. It is also not generally recommendable to take the risk of failure by introducing plant material from only one population, thus mimicking the establishment of a founder. It must be admitted, the question of how man affects evolutionary processes when taking an active part in population recovery, is poorly understood. From a scientific point of view this problem remains an interesting challenge, both in population ecology and in population genetics. I conclude that our current scientific information on the ecological

relevance of population differentiation, as deduced from transplant experiments, leaves much room for a trial and error approach in restoration projects. However, such an approach can at the same time be used to obtain more adequate experimental data.

Acknowledgements The author is indebted to Dick Pegtel, Roel Strykstra, Ab Grootjans, Rick Looijen and two anonymous referees for commenting upon an earlier draft of the manuscript.

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