Plant Conservation in the Anthropocene: Definitely Not Win–Win But Maybe Not

Lose–Lose?
S Volis, Chinese Academy of Sciences, Kunming, China
© 2018 Elsevier Inc. All rights reserved.

Introduction

The stakes for conservation have never been higher than in the new geological epoch, Anthropocene, dominated by rapid and
profound human modifications of the Earth leading to increasingly uncertain environmental future. Rates of landscape modifica-
tion, habitat fragmentation, and species extinctions are unprecedented, and few, if any, ecosystems remain beyond the human
activity impact. The combined effects of changing climate, species loss, and ecosystems’ degradation at times exceed the ability of
ecosystems to maintain their structure and function. Creatures that we know are struggling hard to survive in the Anthropocene
environment where their habitats are destroyed and their food webs collapsed. This century may well be the fin de sicle in terms of
global biodiversity. Will the nonhuman creatures in the Anthropocene be just weeds, rats and cockroaches or also at least some of
the plants and animals that our generation has luck of witnessing before they are gone?
Witnessing rapid loss of biodiversity despite all the conservation efforts in the new Anthropocene conditions, should we accept
the changes passively or keep anyway trying to revert the altered habitats to historical conditions? Knowledge of historical
conditions is essential in restoration because the latter requires reference states, but historical records either nonexist or are
fragmentary and ambiguous. Nowadays, the global climate change, a shift from static to dynamic view of ecological communities,
the ambiguities of the past, and uncertainties of the future make use of historical reference increasingly problematic and impractical.
This crisis of reference baselines is to a large extent responsible for a dichotomy of two global views of nature conservation future,
the forward-looking and backward-looking ones. The first wing of conservation community, so-called new environmentalists or
new conservationists, declares the whole baseline concept obsolete in the emerging Anthropocene, and suggests to abandon history,
focusing not on the past but the future. The second wing is trying to refine or redefine the reference concept often placing the
baseline in deep, distant past, adopting so-called rewilding or resurrection ecology (Alagona et al., 2012). The forward-looking view
proposes to drop the term “restoration ecology” with its historical focus as inappropriate and replace it by terms emphasizing the
new focus on intervention and creation of communities having no historic analogs, such as “intervention ecology,” “reconciliation
ecology,” “win–win ecology,” and “futuristic restoration” (Choi, 2004; Allison, 2007; Choi, 2007; Halle, 2007; Choi et al., 2008;
Hobbs et al., 2011) with the goals of the latter becoming just repairing or reinstating the key ecosystem services. This is done through
creation of “novel ecosystems” (Hobbs et al., 2013) that may contain new combinations of species either as a result of deliberate or
inadvertent introduction, anthropogenic disturbance, change in land use, pollution, or rapid climate change. The concept of the
“novel ecosystem” goes back to the paper of Chapin and Starfield (1997) describing Arctic tundra transitioning to boreal grassland
steppe under altered climate and fire regime. This term has since been applied to a wide variety of ecosystems, for example, mixed
exotic-native tropical forests establishing on abandoned pasture and cropland (Lugo and Helmer, 2004), a grassland developed on
abandoned gravel pit (Seastedt et al., 2008) or ecosystems in urban context with altered abiotic conditions and many exotic species
(Kowarik, 2011). All these ecosystems have one thing in common—they have no analogs in the past ecosystems, and this kind of
ecosystems is expected to dominate in the Anthropocene. While many conservationists consider this an ecological disaster, the “new
conservationists” see this change optimistically, as an opportunity to build “a new, more positive, and forward-looking
environmentalism” (Marris et al., 2011) that will secure ecosystem goods and services rather than species from extinction. The
latter movement tries to shift the emphasis from preserving biodiversity per se to creation and management “of those natural
systems that benefit the widest number of people, especially the poor” (Kareiva and Marvier, 2007; Kareiva et al., 2011). Clear, that
the new concept has no sentiments for preserving species not fulfilling an important functional role in such “natural systems.”
Although the advocates of the novel ecosystem concept state that it does not abandon the conservation of historic habitats and
endangered species as central goals of natural area management (Kueffer et al., 2013), people whose activities interfere with
traditional nature conservation perceive these novel ecosystems exactly that way.
Thus, one of the two extreme views of conservation and restoration treats ecosystems as static and looks backward for a reference,
while another one celebrates completely transformed landscapes and looks forward for ecological novelty. Is there a third way
compromising backward and forward views with an ultimate goal of preserving biodiversity? A third way accepting important role
of historical knowledge in conservation and restoration but which “seeks neither to recreate an imagined past nor to abandon
history entirely” (Alagona et al., 2012)? In this article I will try to provide such a view based on the ideas presented in Volis (2016a,b,
c). In this concept, interventions, assisted colonization, and experimentation are important components, but they have nothing to
do with benefiting local human population ecosystem services. Similarly, in this concept, apparent inadequacy of the current
conservation methodology (low effectiveness of threatened species legislation and protection in nature reserves, low success in plant
reintroductions) is critically evaluated but not for downplaying the role of protected areas at the expense of botanical gardens and
germplasm banks. This model adopts an idea of creating partly novel, that is, having species compositions that differ from historical
analogs ecosystems, but not as a Trojan horse for traditional conservation. Just the contrary, this idea is adopted as an opportunity
for conceptually new conservation of threatened species and their habitats which always was the focus of traditional conservation.

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390 Plant Conservation in the Anthropocene: Definitely Not Win–Win But Maybe Not Lose–Lose?

For preserving biodiversity in Anthropocene, I consider really important only restoration driven by conservation objectives such
as rescuing threatened species and their habitats regardless of benefiting “the widest number of people, especially the poor”. This
kind of ecological restoration called conservation-oriented restoration (Volis, 2016b,c) explicitly deals with threatened species.
Large-scale restoration and assisted colonization are complementary crucial aspects of conservation-oriented restoration allowing a
large number of species and habitats to recover. Another crucial point is close integration of in situ and ex situ conservation with the
latter providing material for in situ actions. Below is a detailed description of this concept.

Usage of Threatened Plant Species in Restoration

Although some species can be at risk because they are inherently adapted to low abundance, proportion of such species among the
currently rare species appears to be small (Rabinowitz et al., 1986), and most of the currently rare species are formerly common but
nowadays threatened “anthropogenic rarities” (Fiedler and Laven, 1996). If a species became rare as a result of fragmentation and
destruction of its habitat by a man, not only number of its populations but also its former range most probably was larger than
today with not necessarily existing records of the latter. Existence of many such species as well as a difficulty in predicting where and
for which species the rapid climate changes will make current ranges unsuitable justifies a conservation approach in which
threatened plant species are introduced not only into locations where they grow or grew in the recent past but also into as many
as possible apparently suitable locations within their potential distribution range. As the number of potentially suitable locations
can be close to zero if only pristine ecosystems are considered as suitable, a solution is to use partly degraded habitats.
Hobbs et al. (2013) distinguished historical ecosystems, which remain within their historical range of variability, hybrid
ecosystems, where the changes are reversible, and novel ecosystems, where the changes are irreversible. Only hybrid ecosystems
(beside historical ones) that did not approach the irreversibility threshold can be a home for the threatened species. For the latter
they must undergo conservation-oriented restoration involving introduction of threatened and nonthreatened but functionally
important species. In these areas, spontaneous recovery of a degraded system might occur naturally when threats are identified and
removed (e.g., prohibition of grazing and logging), but, as a rule, a successional change will be too slow or not to a desired state
without crucial interventions (e.g., thinning or plant/animal introductions) (Benayas et al., 2008). Partly degraded habitats often
have species richness as high as pristine ones but differ to some degree in community structure and composition. Restoration of
these habitats requires enrichment with late-successional species and absent functional groups, for example, species with diverse
flower and fruit types that support diverse pollinator and frugivorous fauna. Instead of using common and widespread species,
restoration can utilize functionally equivalent threatened species that became rare due to disappearance and fragmentation of once
existing habitats. Suitable for this purpose threatened species are those having viable population demographic structure, that is,
relatively high abundance of juveniles relative to adults, presence of all life cycle stages and size categories, and good natural
regeneration. The latter is especially important criterion, and at least some threatened species satisfy this requirement (e.g., see Volis,
2016c). In some cases regeneration problems are apparent and viable population demographic structure can become evident after
removal of the direct anthropogenic effects (e.g., collecting or seeds, seedlings or adults, grazing or planting profitable crops in the
understory).
The reasons of limited (if any) usage of threatened species in ecological restoration include lack of a protocol of the species’
propagation by seeds or cuttings, which is necessary for obtaining large number of outplants, and lack of knowledge about outplant
size and time for planting, which is vital for successful establishment. Increased investments in acquiring the necessary knowledge
and protocol developments will result in comparable to the common species cost per seedling. The latter is crucial for convincing
restoration practitioners to incorporate threatened species into their plans.
A suitability of a given threatened species for habitat restoration, that is, for introduction not only inside but also outside its
current range, can be assessed by modeling its potential niche under both current and future climatic conditions (Fig. 1). After the
modeled suitable species ranges are superimposed, the species assemblages can be defined for any spatial scale (Fig. 1).
Establishing viable, with recruitment, populations from the outplants in conservation projects proved to be an exception rather
than a rule (Godefroid et al., 2011; Dalrymple et al., 2012). The numerous reproduction failures in these projects led to recognizing
the importance of replicating introduced populations over time and space, with reintroductions not necessarily having higher
chances of establishment than relocations (Dalrymple et al., 2012). Given high variability in seedling survival over spatial scales
ranging from very small to very large with reasons poorly understood, introduction trials involving threatened species must be
conducted at multiple sites over large spatial scale.
Threatened species are usually sporadic or subdominant and almost never dominant species. Majority of them are slowly
growing plants, often dependent on specialized pollinator vectors and animal dispersers. Such species are highly vulnerable to
chance local extinction and disappear the first in a fragmented and altered landscape. This results in distortion of species
composition in favor of abundant dominant and subdominant species. As species richness and dominance are inversely related,
thinning of the dominant species and replacement by the threatened species can be a way to preserve both high species diversity and
the threatened species. This option of replacement planting can be especially relevant for those endangered species that were either
outcompeted by aggressive fast growing and dispersal-efficient dominant species or could not recolonize their favorable habitats
after the latter were logged or cleared.
From a very few studies using threatened plant species in active restoration (Morgan, 1999; Cordell et al., 2008; Millet et al.,
2013; Schneider et al., 2014), a major conclusion is that threatened plant species show similar prospects of establishment in
comparison with nonthreatened species in restoration projects. For example, in a study of Millet et al. (2013), from 12 native tree
 Plant Conservation in the Anthropocene: Definitely Not Win–Win But Maybe Not Lose–Lose? 391

Fig. 1 Stages of conservation-oriented restoration with major issues and appropriate methodology for their solving. At the site prioritization stage four quadrates
denote candidate sites with border line width corresponding to the priority rank. As a result of ecological niche modeling for the three species which extant
populations are denoted by colored circles, the small-scale planting sites are defined (grid cells in gray).

species used for conversion of a postlogged plantation in Vietnam into secondary forest, 11 were threatened. Although natural
regeneration was not assessed in their study, which precludes calling it a complete success, there was high survival (above 70%) of
all the species but one four years after planting.

Prioritization of Sites for Restoration

Ecological restoration applied to degraded natural environments has obvious limitations. Even with the most intensive and
expensive restoration methods currently available, and allowing long periods for succession and growth, many ecological attributes
of primary habitats are impossible to restore in degraded environments (Shoo et al., 2016). This has clear implications for
prioritizing areas for restoration. Novel ecosystems, where the changes are irreversible, are useless for conservation-oriented
restoration. In contrast, hybrid ecosystems, where the changes are reversible, can be the targets for restoration, but not all hybrid
ecosystems will have the same conservation value. Clearly, the priority should be given to the least altered habitats, which still need
interventions to restore altered structure and some missing ecological functions but have a reasonable chance of approaching a
primary habitat. But other features, both intrinsic and extrinsic, are also important for ranking the candidate restoration sites by
conservation value. The former are presence of threatened species and their regeneration, and the latter are the total forest cover
remaining in the landscape and richness of the regional species pool. I propose the following ranking (Volis, 2016c):

(1) Hybrid systems in which highly endangered plant species still have populations and these populations exhibit natural
regeneration.
(2) Hybrid systems in which highly endangered plant species still have populations but natural regeneration in these populations
has not been observed or is depressed.
(3) Hybrid systems which are least degraded among other similar systems, and which can potentially support establishment of
endangered species currently not growing there.
(4) Hybrid systems of varying degree of disturbance that have a low probability of supporting establishment of endangered species
but have a good chance of approaching (after restoration) historical habitats by species structure and composition.
(5) Hybrid systems of varying degree of disturbance that are important for establishing connectivity between patches of fragmented
habitat and maintaining the regional species pool.
Restoration interventions should boost the naturally occurring succession and change the species composition toward higher
species richness and increased proportion of threatened and rare species. Lack of convergence of the species composition in the
restored habitat with that of the nearest undisturbed one should not be seen as a failure of the restoration project, as shown later.

Reference—A Dynamic View

Adopting the idea that many ecosystems will inevitably have species combinations different from those in historic or prehistoric
times should not lead us to either focusing on natural systems benefiting the widest number of people or welcoming exotic and
invasive species as parts of novel ecosystems. Knowledge of historical past, that is, ecological changes overtime rather than a single
392 Plant Conservation in the Anthropocene: Definitely Not Win–Win But Maybe Not Lose–Lose?

baseline state, can serve a solid ground for restoration approach “where the past may inform but not determine the ecosystems of
the future” (Alagona et al., 2012). In other words, the past may be unachievable as a model for the future, but it is invaluable for
working out a model that can be achieved. Although advocates of novel ecosystems perceive the historical reference an anachronistic
or obsolete, we should not disqualify historical knowledge from restoration and conservation projects. Just the opposite, instead of
abandoning search for and usage of the references we need to reinforce the latter. A reinforcement can come from recognizing not a
single but multiple alternative stable states for an ecosystem (Balaguer et al., 2014), intensive utilization of plaeoclimatic and fossil
data, environmental niche modeling, and species ranges realignment (Birks, 1996; Millar, 1998; Davies and Watson, 2007; Brewer
and Menzel, 2009; Butterfield et al., 2016; Natlandsmyr and Hjelle, 2016). A broad view of reference conditions equates them to the
historical range of variability in ecosystem composition, structure, and function. There are several reasons for considering alternative
potential reference states in conservation-oriented restoration. First, existence of alternative states is predicted by assembly rules
theory of theoretical community ecology, in which environmental conditions determine the types of available niches which the
functional groups can fill, while species compositions within functional groups are determined by different historical order of
species arrival. Second, extant populations of the threatened species are usually located in small in size remnants of a natural habitat
representing only a subset of the habitat original variation in terms of environment, community composition, and successional
stage. Third, palaeobotanic data suggest the dynamic nature of many vegetation communities during centuries and millennia.
Finally, the rapid climate change can make even primary species habitats unsuitable in the near future.
For these reasons, ecological restoration, and especially conservation-oriented restoration, in the Anthropocene apparently will
focus more on environmental (soil, hydrology, topography) and ecosystem (vegetation community, plant functional types,
nitrogen cycling) aspects of a target landscape rather than on the ecosystem memory and species identities within particular
environments. On the other hand, the above reasons justify introduction of the threatened species as a part of different species
assemblages into locations outside their known historical range. There is a restoration approach with a similar narrative which was
introduced two decades ago. A realignment approach (Millar, 1998) states that compositions, structures, and distributions of plant
communities were constantly shifting over long timeframes, with historic ranges of the species contracting and expanding in a
response to changing regional and global conditions. Therefore, rather than emphasizing historic ranges and past conditions, this,
and similar “prestoration” (Butterfield et al., 2016) approaches propose to realign restored ecosystems to present and expected
future conditions based on knowledge of the species prehistory and biological requirements. An example is a conservation
assessment of Monterey Pine (Pinus radiata), as described in Millar and Brubaker (2006). Pinus radiata is currently represented by
only five small, human-disturbed and declining populations in California and Mexico. Conservation of this species initially focused
on rehabilitation of extant populations. However, palaeoclimatic data revealed that the species range shifted many times in
response to climatic changes during Quaternary. The known past distribution range of Monterey pine included coastal northern
California 600 km from the closest current native population. In this region, Monterey pine has been used for landscaping and
naturalized widely, spreading into parks and nature reserves. Based on palaeecological knowledge, Millar (1998) proposed a
realignment restoration strategy for this species to except and encourage it to persist in areas on the north coast of California where it
has naturalized, instead of removing it as an exotic. These locations can be considered “neonative” sites for this species because they
overlap with the historic range of Monterey pine under similar to the current climates, and because they resemble floristic
communities found in Monterey pine fossil assemblages.
In view of the above, a restoration project should target alternative states as reference ecosystems through adaptive learning, as a
replicated over space experiment which outcomes are critically evaluated and used to inform the next introductions. As a result,
optimal, that is, leading to the highest success intervention actions can be worked out. A criterion of success in restoration project
having conservation goals is a long-term persistence of the target population of a threatened species, that is, its viable demographic
structure evident in the presence of new generations in addition to the founders. The variation among reference sites in local
population demography can be important for understanding restoration failures; thus, more than one reference site should be used
for estimating restoration success.

Role of Ex Situ Conservation: Seed Banks

Seed banks are a critical component of any project having an objective of retaining or restoring native plant diversity. In restoration,
availability of large quantities of seed and quality of these seeds is a prerequisite for a restoration project success because quality of
seeds is directly related to the germination and survival of seedlings and the genetic diversity of populations. The detailed guidelines
for collecting seeds of threatened species are given in Volis (2016a,b) with the following major points: (i) sampling should be done
repeatedly over years not to harm the population or simply because seed production is too low; (ii) seeds collected from individual
plants must be kept separately as maternal lines (families) and not as bulk collections; and (iii) it is desirable to distinguish long-
term and short-term seed collections, the first being a “strategic” source of germplasm to be used for studying species biology and
development of propagation protocols, but not for in situ actions, and the second to be used exclusively in in situ actions either
directly or after propagation. Utilization of the stored seeds for in situ conservation must take into account a possible risk of
maladaptation and outbreeding depression.
Potential maladaptation of the introduced genotypes and reduced fitness of their offspring (outbreeding depression) have
always been a concern in restoration. Introduction of maladapted nonlocal genotypes can cause a failure of a restoration project and
also negatively affect local or neighboring native locally adapted populations through gene flow. To insure that the introduced plant
 Plant Conservation in the Anthropocene: Definitely Not Win–Win But Maybe Not Lose–Lose? 393

germplasm is adapted to local environment, yet also possess sufficient diversity to adapt and respond to future biotic and abiotic
conditions, seed sourcing in restoration involves delineation of the seed transfer zones, geographic areas within which seeds can be
moved around with minimal risk of maladaptation (Kramer and Havens, 2009).
As experimental determination of seed transfer zones for each species is too costly to be a realistic option, a solution is to use
ecoregions either alone (Johnson et al., 2010; Miller et al., 2011) or in a combination with relevant climatic parameters (Bower
et al., 2014) as a proxy. The latter proxy should be adjusted using a species-specific information (dispersal ability, breeding structure,
and history of the populations’ isolation).
Efficiency of existing seed banks for conservation of threatened species is low for several reasons. First, seed bank managers often
are reluctant to collect threatened species having small and sparsely distributed in remote places populations due to high cost of
collecting. The seed collections of threatened species often represent low number of populations and accessions and are seldom
used for in situ actions. Living collections in Botanical Gardens, potentially useful as seed sources, often lack information on place of
origin or possess a risk of spontaneous hybridization making them unsuitable for in situ actions.
Several improvements are needed in seed bank concept and management. In order to make seed banks useful for conservation-
oriented restoration and their managers willing to collect seeds of species which pose a collecting challenge it is necessary to
establish conservation seed banks, that is, germplasm storages of threatened and rare species. These seed banks should be designed
to store, handle, and use large number of seeds per species rather than just large number of species, they must have an emphasis on
collecting and storage of maximum species genetic variation, and the collected seeds be fully available for in situ actions. The idea of
collecting and storing only species to be used in in situ actions is utilized in restoration seed banks, facilities to collect, store, and
propagate germplasm to be used in restoration projects (Merritt and Dixon, 2011). Experience of existing restoration seed banks
should be learned and adopted for specific needs of conservation seed banks.
A requirement of large quantities of seeds in restoration projects, on one hand, and space limitations of the traditional seed
banks, high cost of storing nonorthodox seeds and negative impacts of seed harvesting on local population dynamics, on the other
hand, call for an intermediate stage of seed propagation. The quasi in situ concept (Volis and Blecher, 2010; Volis, 2016a) provides
detailed guidelines to choice of material, planting, and management of the living collections, with plants maintained in these
collections be a reliable source of seeds for restoration projects (see later).

Role of Ex Situ Conservation: Living Collections in Botanical Gardens

The major depositories for living plants representing threatened species traditionally are botanical gardens and arboreta. These
collections’ aim is to serve a germplasm backup in a case of in situ conservation failure, preserve the species genetic diversity, and
help propagating germplasm for in situ actions (Prance, 1997; Maunder et al., 2001; IPGRI, 2004; Guerrant et al., 2004). However,
role of botanical gardens and arboreta in conservation should not be overestimated due to numerous limitations in their utility for
maintaining sufficiently large and genetically diverse living collections. Some of the problems are associated with poor genetic or
demographic management, for example, mislabeling, representation of species by only a few individuals, and lack of information
on accession sampling locality. When the number of stored accessions per species is low or they are inadequately documented or
mixed, these collections are extremely vulnerable to the processes of genetic erosion, artificial selection, and infestation by
pathogens. Physical proximity of plants having different origin can lead to spontaneous hybridization with produced offspring
lacking genetic integrity and having maladaptive gene combinations. To prevent or at least reduce these effects, sampled individuals
must be maintained separately or through controlled breeding and pedigree design. This introduces two major weaknesses of
botanic garden and arboreta ex situ collections—their low capacity and high cost of maintenance. As a result, in overwhelming
majority of the cases, the garden living collections are far from what is needed to represent the species genetic diversity (e.g., 10–50
individual plants from five natural populations). The above problems and weaknesses of living collections in gardens and arboreta
call for reevaluation of their specific tasks. The goals of serving a germplasm depository properly preserving the species genetic
diversity and providing material for in situ actions appear to be too ambitious for these collections given their limited space and
financial resources. Instead, their role should be limited largely to botanical research, development of seed germination, cutting and
tissue culture propagation techniques, and education. The above conservation goals can be achieved only by a strategy that is
specifically designed to integrate ex situ and in situ conservation components and is less space limited and much cheaper.

Integration of Ex Situ and In Situ

In restoration projects involving threatened species the material can either come directly from the natural populations as seeds,
seedlings, or adult plants or through obtaining outplants from seeds or vegetatively in nurseries. Acquiring sufficient quantity of
seeds, bulbs, root cuttings, or saplings from natural populations of threatened species is rarely possible even under multiple visits
and can negatively affect their viability. Thus, propagation in specialized nurseries does not seem to have an alternative. However,
germinating the seeds collected in natural populations and stored in gene banks, and growing them to the stage of seedlings or
saplings in nurseries, does not solve a problem of having sufficient number of seeds. The seeds produced by plants in botanical
gardens and arboreta can have numerous problems identified above, and their quantities will be far from those required. A solution
is seed production in living collections which will be of needed capacity and which design will prevent both inbreeding and
394 Plant Conservation in the Anthropocene: Definitely Not Win–Win But Maybe Not Lose–Lose?

Fig. 2 Role of quasi in situ living collections in conservation-oriented restoration. A quasi in situ collection (gray rectangle) is established in a protected location
having the same environmental conditions with the extant species populations (circles in red). Seeds that resulted from spontaneous or assisted cross-pollination
within a quasi in situ site are used to produce the outplants for restoration.

outbreeding depression, as an intermediate step followed by propagation in nurseries. Quasi in situ approach (Volis and Blecher,
2010) suits this purpose. To overcome the space and logistic limitations of garden living collections this concept proposes creation
of living collections of required capacity in sites having legal protection status and natural or seminatural conditions. Natural
populations from which the individuals maintained in the collection originated, and the quasi in situ site must share the same
climatic zone and biotic/abiotic environment (Fig. 2). Sampling within a particular environmental type must include several
(ideally all) geographically isolated populations with a representative number of genetically different individuals per population.
The areas suitable for creation of living collections can be even the least valuable and degraded to some degree parts of
archeological, memorial, cultural, and other, not only natural, protected areas, as well as buffer zones in nature reserves.
An optimal design is planting different genotypes separately at a distance from each other allowing their subsequent identification.
This can be important for identification of superior in terms of survival and seed production genotypes, maintaining collection
genetic variation, and controlled pollination, if necessary.
Plants, grown in this collection, can be expected to be locally adapted and represent properly the species genetic variation, that is,
contain adapted and genetically different individuals. As all plants in the collection originate from the same environment, there will
be no maladapted genes to participate in recombination and segregation, and cross-pollination of these plants should not lead to
breakdown of coadapted gene complexes or dilution of local adaptation. Therefore, the offspring of cross-pollination occurring in
the collection suit well in situ actions and, on the other hand, can be produced and collected in large quantities needed for
conservation-oriented restoration to be successful.
Use of seeds in in situ conservation actions is known to be ineffective as compared with seedlings or saplings because of high
seed mortality and low establishment. This necessitates a properly organized production of large quantities of the outplants. For this
purpose, specialized nurseries are the best option, but in some cases “in situ seedling banks” (Pritchard et al., 2014) can be useful.
In this method seeds are sown and seedlings are maintained in the forest understory. For those species having low requirements for
successful germination and high seed germination rate this method it easy to apply in a wide range of forests: natural, degraded, or
planted forests including monoculture tree plantations.
The introduced population, according to the latest population genetics guidelines (Frankham et al., 2014), ideally should be at
least 100 families and around 10 000 individuals. For many critically endangered species this number of families can be
unachievable due to the small number of reproducing adults in extant populations, but the required number of individuals
(5000–10 000) derived from all available mother plants is achievable after properly done propagation. For a species introduced
into multiple sites within a spatial matrix allowing efficient seed and pollen dispersal, a mosaic of these locations can be considered
a single metapopulation to which the recommended number of introduced individuals applies.

Restoration: Choice of Material, Planting Design, and Plant–Animal Interactions

The major issues for decision-making in habitat restoration, when the restoration site is chosen and reference conditions deter-
mined, are the number and identity of the species to be introduced, planting design, and addressing plant–animal interactions
(Fig. 1). Conservation-oriented restoration should maximize as much as possible the number of species introduced, focusing first of
all on threatened species and giving them preference. These species should be on a top of the candidate species lists, and their
functional type matters only with respect to whether they will have a reasonable chance to establish viable populations in a given
environment. The nonthreatened candidate species should be carefully chosen from regional species pool as a source of the species
that might successfully colonize a restored site. The best candidates would be those species cooccurring with the top-priority
threatened species and having important roles in the ecosystem functioning, especially in those functions that had been lost during
ecosystem degradation (e.g., in primary production, nutrient cycling, canopy structure, seed dispersal, pollination services).
Restoration of species-rich communities such as subtropical and tropical forests must focus on the ecosystem functional diversity,
 Plant Conservation in the Anthropocene: Definitely Not Win–Win But Maybe Not Lose–Lose? 395

for example, diverse flower traits that support diverse pollinator fauna, and diverse fruit types providing food for variety of
frugivorous animals.
The appropriate for conservation-oriented restoration planting design is one emphasizing experimentation with species assem-
blages composition and replicating these experimental assemblages over space. The resulting mosaic of habitat patches having
somewhat different species composition and abundances can provide more opportunities for establishment of introduced
threatened species by offering these species wider range of microhabitats, different neighboring vegetation, and animal interactions.
This design can also benefit remaining natural populations of threatened species with regeneration problems by improving
connectivity among them and restoring the ecological processes needed for successful regeneration such as pollination and seed
dispersal by animals. In addition, augmentation of the latter populations should be practiced whenever possible. Supplementing
them with planted conspecifics can boost regeneration and lead to the population growth and expansion.
Introduced seedlings or saplings must be planted at a distance from each other and, when relevant, from the adult conspecifics,
preventing negative density effects of host-specific natural enemies such as soil pathogens and insects. At the same time, planting
design should also consider a positive density dependence in population growth rate at low densities, known as Allee effect, caused
by various genetic, demographic, and ecological factors. For example, low seed production is a common phenomenon in small and
fragmented populations of species that require animal pollination because pollinators usually forage more in dense patches in order
to reduce the interpatch travel time. As a result, plants growing at low densities may experience reproductive decline or failure due to
difficulties in attracting pollinators. The mechanisms underlying Allee effects, genetic, pollinator-mediated, or environment-
facilitative, suggest that population persistence is positively related to population size and plant density. The above considerations
must serve as the basis for decisions about sufficiently large number and appropriate density of planted individuals.
Restoration cannot succeed if it does not consider reestablishment of the integrity of disrupted interactions crucial for ecosystem
functioning (seed dispersal, pollination, nutrient cycling, and food webs) (Montoya et al., 2008). The latter may require introducing
or controlling a suite of interacting species such as soil biota, herbivores, seed predators, frugivorous vertebrates, or even top
predators, and sometimes environmental modifications needed for vertebrates such as availability of perches or structural
complexity of the vegetation.
Pollination processes are among the most important plant–animal interactions, and their reestablishment can be achieved only
by satisfying the pollinators’ needs essential for the completion of their life cycle either within the restoration site or within the
pollinators’ foraging distance. For example, for solitary bees these needs include availability of nest sites, and for butterflies—
availability of both nectar resources and larval host plants. Expected colonization of the restored sites by pollinators from the
neighboring less-degraded habitats should take into account that wide-ranging generalists such as bumblebees and bees may
succeed as colonizers, while nonflying or restricted-range specialists, for example, cursorial mammals, lizards, and many inverte-
brates will stand little chance of colonizing these sites by themselves. Thus, restoration plans must be based on good knowledge of
degree of specialization, colonization capability, and minimum habitat area requirements of the crucial pollinator groups. The
ecosystems with highly specialized pollinator associations (as many species-rich plant communities are) present the greatest
challenges for restoration and will require detailed knowledge of the ecological requirements for both plants and their pollinators.
On the other hand, because pollinators contribute critical to the ecosystems functions, the exact identities of these species are less
important than their functional role. Thus, if the crucial native pollinators are extinct or are very rare, substitution by functionally
equivalent species is an option to consider.
Functioning of many ecosystems is impossible to restore without considering another plant–animal mutualism such as
frugivory. Disappearance of large fruit-eating birds and animals as a result of rainforest clearing and fragmentation, bushmeat
harvest, and poaching has a strong effect on seedling banks by favoring seeds dispersed by bats, small birds, and wind, which
reduces recruitment in species dependent on large frugivores. For this reason habitat restoration plans must include restoring once
existed but disrupted plant–animal interactions by protecting, attracting, or reintroducing frugivore populations. Usually, when one
frugivore group disappears, its loss cannot be compensated by another group because of a low overlap between diets of different
groups of large frugivores (Kitamura et al., 2002). Even frugivores having similar diets differ in dispersal methods, distances they
travel and microhabitats into which they disperse seeds. For example, gibbons disperse seeds via defecation, while macaques
disperse seeds via their cheek pouches (Kitamura et al., 2002), and small passerine birds disperse most seeds over short distances
and into covered microhabitats, while mammals and medium-sized birds disperse seeds over long distances and mostly into open
microhabitats (Jordano et al., 2007).
When the fruit–frugivore interactions for a given community are poorly known, a priority for conservation and reintroduction in
the majority of the cases should be the large-bodied, large-gaped, and wide ranging frugivorous taxa because the latter have the
largest impact on ecosystem functioning but are the most vulnerable to hunting (McConkey et al., 2012).
Practical recommendations, for the areas where functionally important animals (e.g., seed dispersers or grazers) have become
extinct, are to reintroduce these species from other regions, or, when this is not feasible, to use functionally equivalent at the
community level substitutes from the local or regional fauna (McConkey et al., 2012). These animals can be threatened by
themselves, and thus introduction or reintroduction of endangered animals which can perform a functionally important role in a
restored ecosystem can simultaneously serve several important goals: to improve a conservation status of the introduced animal
species, restore the degraded environment, and enhance populations of the threatened local plant species. For example, introduc-
tion of endangered giant tortoises (Geochelone nigra hoodensis) to one of the Galápagos Islands had a positive impact on an arboreal
cactus Opuntia megasperma, which is itself endangered and a keystone resource for many animals on the island (Gibbs et al., 2008).
396 Plant Conservation in the Anthropocene: Definitely Not Win–Win But Maybe Not Lose–Lose?

Protection of the Restored Habitat

A site for conservation-oriented restoration must have an appropriate legal protection status that will, on one hand, prevent
unauthorized anthropogenic disturbance during or after restoration and, on the other hand, make possible pre- and postplanting
management interventions that may be needed, for example, weeding, burning, supplemental watering, or fencing. Plant micro-
reserves (Laguna et al., 2004) suit well conservation-oriented restoration because they not only protect the designated area which
can be of any size but also permit interventions, which are forbidden in strictly protected areas having protected categories Ia and Ib
(Dudley, 2008). Active protection must be accompanied by the long-term monitoring of the population demography to make sure
that the new population really became established, both for the outplants and for subsequent generations of plants. Besides,
monitoring of introduced and comparison with extant populations can help to optimize the management of introduced popula-
tions. For example, demographic comparisons of the rare Centaurea corymbosa showed that reintroduced populations had higher
survival but lower fecundity than natural populations, with a management recommendation to increase plant density to improve
mate availability for self-incompatible flowering individuals (Colas et al., 2008).

Concluding Remarks

This paper presents the concept of conservation-oriented restoration as a solution to numerous conservation challenges of the
Anthropocene. The concept includes the following crucial elements:
(i) assisted colonization of threatened species into as many as possible locations with conditions suitable in the near and more
distant future
(ii) highest priority for restoration to the least degraded areas that have extant populations of the threatened species
(iii) targeting alternative states as reference ecosystems through adaptive learning, as a replicated over space experiment which
outcomes are critically evaluated and used to inform the next introductions
(iv) establishing conservation seed banks, that is, germplasm storages of threatened and rare species designed to store, handle, and
use large number of seeds per species rather than just large number of species, with the collected seeds be fully available for
in situ actions
(v) obtaining sufficient number of outplants through seed production in living quasi in situ collections, and then seedling
production in specialized nurseries
(vi) planting design based on experimentation with species assemblages composition and replicating these experimental assem-
blages over space
(vii) reestablishment of the integrity of disrupted interactions crucial for ecosystem functioning (seed dispersal, pollination,
nutrient cycling, and food webs)
(viii) legal status of the restored site preventing unauthorized anthropogenic disturbance but permitting pre- and postplanting
management interventions

Although this strategy was conceived as an approach to conservation of threatened plant species and their habitats that can be
applied worldwide, it definitely has limits and may not apply in many circumstances. These limits will be recognized, and more
concrete guidelines will be worked out from the results of the studies implementing this strategy.

Acknowledgments

No grant supported this study. I am grateful to Mark Richardson for constructive comments on an earlier version of the manuscript.

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Further Reading

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Schneider T, Ashton MS, Montagnini F, and Milan PP (2014) Growth performance of sixty tree species in smallholder reforestation trials on Leyte, Philippines. New Forests 45: 83–96.