ESA CENTENNIAL PAPER

Advances in restoration ecology:

rising to the challenges of the coming decades
MICHAEL P. PERRING,1,2,  RACHEL J. STANDISH,1,3 JODI N. PRICE,1 MICHAEL D. CRAIG,1,3 TODD E. ERICKSON,1,4
KATINKA X. RUTHROF,3 ANDREW S. WHITELEY,5 LEONIE E. VALENTINE,1 AND RICHARD J. HOBBS1
1
School of Plant Biology, The University of Western Australia, 35 Stirling Highway,
Crawley, Western Australia 6009 Australia
2
Forest & Nature Lab, Ghent University, BE-9090, Gontrode-Melle, Belgium
3
School of Veterinary and Life Sciences, Murdoch University, 90 South Street, Murdoch, Western Australia 6150 Australia
4
Kings Park and Botanic Garden, Fraser Avenue, Kings Park, Western Australia 6005 Australia
5
School of Earth and Environment, The University of Western Australia, 35 Stirling Highway,
Crawley, Western Australia 6009 Australia

Citation: Perring, M. P., R. J. Standish, J. N. Price, M. D. Craig, T. E. Erickson, K. X. Ruthrof, A. S. Whiteley, L. E.

Valentine, and R. J. Hobbs. 2015. Advances in restoration ecology: rising to the challenges of the coming decades.
Ecosphere 6(8):131. http://dx.doi.org/10.1890/ES15-00121.1

Abstract. Simultaneous environmental changes challenge biodiversity persistence and human well-
being. The science and practice of restoration ecology, in collaboration with other disciplines, can contribute
to overcoming these challenges. This endeavor requires a solid conceptual foundation based in empirical
research which confronts, tests and influences theoretical developments. We review conceptual
developments in restoration ecology over the last 30 years. We frame our review in the context of
changing restoration goals which reflect increased societal awareness of the scale of environmental
degradation and the recognition that inter-disciplinary approaches are needed to tackle environmental
problems. Restoration ecology now encompasses facilitative interactions and network dynamics, trophic
cascades, and above- and belowground linkages. It operates in a non-equilibrium, alternative states
framework, at the landscape scale, and in response to changing environmental, economic and social
conditions. Progress has been marked by conceptual advances in the fields of trait-environment
relationships, community assembly, and understanding the links between biodiversity and ecosystem
functioning. Conceptual and practical advances have been enhanced by applying evolving technologies,
including treatments to increase seed germination and overcome recruitment bottlenecks, high throughput
DNA sequencing to elucidate soil community structure and function, and advances in satellite technology
and GPS tracking to monitor habitat use. The synthesis of these technologies with systematic reviews of
context dependencies in restoration success, model based analyses and consideration of complex socio-
ecological systems will allow generalizations to inform evidence based interventions. Ongoing challenges
include setting realistic, socially acceptable goals for restoration under changing environmental conditions,
and prioritizing actions in an increasingly space-competitive world. Ethical questions also surround the use
of genetically modified material, translocations, taxon substitutions, and de-extinction, in restoration
ecology. Addressing these issues, as the Ecological Society of America looks to its next century, will require
current and future generations of researchers and practitioners, including economists, engineers,
philosophers, landscape architects, social scientists and restoration ecologists, to work together with
communities and governments to rise to the environmental challenges of the coming decades.

Key words: Anthropocene; community assembly; ecosystem function; ecosystem services; ESA Centennial Paper; faunal
restoration; global change; landscape scale; novel ecosystems; resilience; socio-ecological systems; traits; trophic networks.

Received 1 March 2015; revised 7 May 2015; accepted 13 May 2015; published 7 August 2015. Corresponding Editor: D.
P. C. Peters.

v www.esajournals.org 1 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

Copyright: Ó 2015 Perring et al. This is an open-access article distributed under the terms of the Creative Commons
Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the
original author and source are credited. http://creativecommons.org/licenses/by/3.0/
Editors’ Note: This paper was commissioned by the members of the Ecosphere Editorial Board to commemorate the ESA
Centennial celebration.
  E-mail: michael.perring@uwa.edu.au

INTRODUCTION context of the plurality of restoration motivations

and goals that characterize the current era. We
We are in an unprecedented era of simulta- explicitly consider conceptual ecological devel-
neous global environmental changes, many opments pertinent to restoration since A. D.
unperceived at the founding of the Ecological Bradshaw’s (1983) Presidential Address to the
Society of America (ESA) one hundred years ago British Ecological Society in 1982, when he stated:
(Steffen et al. 2011, Barnosky et al. 2012, Steffen et ‘‘The acid test of our understanding is not whether we
al. 2015). Significant challenges facing humanity can take ecosystems to bits on paper, however
include global biodiversity loss, anthropogenic scientifically, but whether we can put them together
pollution and associated climate change, land in practice and make them work’’. We explore how
allocation, energy generation and coping with a conceptual developments are being applied to
growing global human population (Vitousek et restoration practice and how ecological knowl-
al. 1997, Steffen et al. 2005). However, there are edge is faring against the ‘acid test’.
inspiring messages that suggest global environ- We were motivated to provide this review in
mental change and associated challenges can be acknowledgement of the ESA’s Centenary and
tackled (DeFries et al. 2012). One long-term, given the fact that restoration ecology has
potentially cost-effective, and optimistic solution become an important discipline within the broad
is the science of restoration ecology and its corpus of ecological knowledge since Bradshaw’s
applied practice of ecological restoration (Dob- address. We aim to build on earlier reviews (e.g.,
son et al. 1997, Nelleman and Corcoran 2010, Young et al. 2005, Brudvig 2011, Suding 2011)
Suding et al. 2015). and present evidence for a coherent conceptual
The restoration of ecosystems that have been framework that represents the development and
damaged, degraded or destroyed, through es- contemporary state of restoration ecology (see
tablishing or re-introducing flora and fauna also Figs. 1 and 2). This framework synthesizes
(SERI 2004), provides options to mitigate envi- the development and incorporation of important
ronmental degradation, especially at large scales ecological concepts in restoration ecology, as it
(Menz et al. 2013). Ecological restoration has the moved beyond traditional foci of plant commu-
potential to improve air quality, reverse forest nities and single functional goals within a patch
clearance and desertification, slow biodiversity (Young 2000). Contemporary practice considers
loss, enhance urban environments and perhaps organisms beyond plant communities and mul-
improve human livelihoods and humanity’s tiple functional, as well as compositional, goals.
relationships within nature. These examples It applies concepts with a landscape scale,
highlight the opportunity for restoration ecology anthro-ecological perspective that is required to
to develop the tools that will allow people to rise address environmental issues in the current and
to the environmental challenges of the coming future human-influenced biosphere (Ellis 2015).
decades, finding solutions that meet both social Ecological restoration provides an ideal setting
and environmental goals, particularly when for hypothesis generation and testing in ecology
coupled with other disciplines. However, rising (Jordan et al. 1987 in Young et al. 2005, Laughlin
to these challenges will require clear articulation 2014) but the full potential of this opportunity
of restoration goals (Hobbs and Norton 1996) has yet to be realized. Our review highlights the
and solid ecological foundations upon which to need for practical tests of the concepts we present
build restoration practice. while discussing the challenges associated with
Here, we elucidate the conceptual foundations this call. We further highlight how conceptual
upon which to build restoration practice, in the and practical developments may be aided by

v www.esajournals.org 2 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

Fig. 1. Framing conceptual and technological advances in restoration. (a) The development of restoration
ecology: Restoration traditionally focused either on a functional goal (e.g., reinstating soil processes,
productivity) or, in conservation settings, achieving desired (plant) species composition that was assumed to
lead to desired (ecosystem) function, with an ecological worldview that tended to think in terms of equilibrium in
an unchanging environment. Over time, non-equilibrium dynamics, simultaneous environmental changes, and
widespread persistent degradation of the global environment including the presence of thresholds in ecosystem
dynamics became more apparent. This necessitated a rethinking of restoration goals and has led to a plurality of
motivations and goals for contemporary restoration across scales. (b) Contemporary restoration ecology:
Contemporary restoration ecology sits at the nexus between ecological and social systems and is therefore
influenced by changes within each of these dimensions and interactions between them. Contemporary
restoration uses trait frameworks and new understanding of trophic networks to achieve dynamic, process-based
functional and compositional goals in an era of socio-environmental change. Increasingly, restoration aims to
deliver functions such as ecosystem services and resilience, across scales, and has taken far greater account of the
human dimension, in terms of our capacity to achieve goals and what form these goals should take. Table 1 and
the main text use this framing of contemporary restoration ecology to review conceptual and technological
advances that will allow ecological restoration to rise to the environmental challenges of the coming decades.

technological advancement (see also Table 1). We ical concepts we discuss apply to marine areas as
mainly focus on terrestrial ecosystems and well and can inform marine restoration programs
examples. However, environmental changes in into the future and those that are already
the marine biosphere (Halpern et al. 2008) also underway (e.g., Elliott et al. 2007, Bastyan and
demand restorative action. Many of the ecolog- Cambridge 2008, Campbell et al. 2014).

v www.esajournals.org 3 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

Fig. 2. Achieving functional and compositional goals among flora, fauna and soil. Recent conceptual advances
highlight the interactions between flora, fauna and soil in restoration ecology. Developments in plant
establishment (technological advances in brown) and soil resource supply have been complemented by a focus
on fauna from the outset of projects, the potential for aboveground-belowground linkages to influence
restoration success and the use of trait-environment frameworks to integrate across ecosystem properties to
achieve restoration success. Although in this schematic the circles are of equal size, it is neither the case that all
restorative actions are influenced by each sphere equally, nor do they occur on the same spatial and temporal
scales. For instance, it is not possible to restore some soil properties over short time frames at large scales. The star
denotes the intersection of all three spheres, and, while it is not always necessary to aim for the star (i.e.,
manipulate soil, flora and fauna) in restoration, we argue that it is important to consider each sphere and their
interactions at the outset and plan restoration accordingly. Example ecological concepts that pertain to the star
are outlined at the base of the figure and explored further in the main text.

We conclude by presenting important chal- holders, is to reach this potential.

lenges and opportunities that remain for resto-
ration ecology, especially the necessity to develop RESTORATION MOTIVATIONS AND GOALS
mechanisms to test the conceptual ideas present-
ed at the required scale. Robust testing will The practice of ecological restoration has
identify context dependency and the appropri- varied motivations (Wiens and Hobbs 2015).
ateness of various concepts in different restora- Some projects are undertaken primarily to
tion efforts. Our overarching goal is to show how address environmental problems (e.g., environ-
concepts in restoration ecology have the potential mental plantings for carbon sequestration; reveg-
to allow ecological restoration to rise to the etation to tackle loss of productive capacity
challenges of the coming decades. The challenge through salinity or soil erosion) while others are
for restoration ecologists, in conjunction with motivated by legislative requirements for repa-
practitioners, colleagues from disciplines such as ration following development or mining (e.g.,
landscape architecture and economics, and stake- Carrick et al. 2015). Other projects are focused on

v www.esajournals.org 4 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

Table 1. Ecological concepts with direct application to restoration practice. (a) Concepts with an established
history of application in restoration (see also Young et al. 2005); (b) concepts being incorporated into
restoration practice; and (c) concepts with potential that have yet to be fully realized. Recent advances in
concepts are listed in the third column and examples of technological advances that have facilitated the
practical application of concepts appear in the far column. Technological advances that have facilitated global
networks of experiments and widespread exchange of information and ideas have in turn contributed to
advances of many of the concepts listed. A major challenge is working out context dependency—i.e., under
what circumstances can the different ecological insights be best utilized to achieve restoration goals. Another
challenge is identifying emerging ecological concepts that may influence restoration success (e.g., the
importance of chemical ecological cues Dixson et al. 2014).

Ecological theory/concept Examples of practice Conceptual advances Technological advances

a) Established in practice
Competition/plant Weed control; nutrient stripping Importance of facilitation/ GIS to map weed invasion;
strategy theory and reduction parasitism; stoichiometric unmanned aerial vehicles to
theory aid mapping
Succession Interventions informed by initial Assembly rules; tests of ‘‘field of Digital processing of historical
floristics or relay models dreams’’ hypothesis aerial photographs; satellite
imagery/NDVI; digital
multispectral imagery to
detect changes in greenness
Recruitment Seed addition Ecology of ontogeny (Young et Optimum seed processing and
limitation al. 2005); chain of seed use: pre-treatments; seed coats and
restoration seed bank (Merritt extruded pellets for native
and Dixon 2011) and systems seeding
approach (James et al. 2013);
seeds and seedling traits
Herbivory/ Fencing; pest control Integrated pest management Seed coating, bait development,
predation infra-red cameras
Niche concept Ground preparation; Plant-soil feedback; ecosystem Tools to measure the niche, e.g.,
mycorrhizal inoculation; engineers electrical resistivity
assisted migration and tomography for fine-scale
translocations measures of soil water;
modelling capabilities, e.g.,
cellular automata models
Disturbance Prescribed burning; grazing; Temporal and spatial scales of Simulation modelling to predict
taxon substitution disturbance regimes outcomes of management
interventions; de-extinction
b) Increasingly incorporated into practice
Ecotypes/genetic Seed collection based on genetic Role of genetic diversity in Seed banking, e.g., cryo-
diversity provenance with assumption ecosystem services preservation
that local provenance is best
practice; assisted migration
Facilitation/ Nurse planting; mycorrhizal Mycorrhizal networks; Analytical models to understand
mutualism inoculation phylogenetic relatedness interactive effects (e.g.,
structural equation modelling)
Island Reserve design (several small Meta-population and meta- Machinery to re-vegetate at
biogeography reserves or single large community theory; landscape scale; radio collars to track
reserve); planting buffers and ecology; land sharing concept movement of fauna; satellite-
corridors to improve GPS technology and micro-
connectivity collars
Biodiversity– Interventions to restore Trait based approaches; High throughput next
ecosystem particular functions/ecosystem response-effect framework generation DNA sequencing
function services; planting species to and functional gene mapping
attract keystone pollinators
and seed dispersers
c) Yet to be fully realized
Alternative stable Interventions to overcome State and transition models; State and transition simulation
states/thresholds abiotic/biotic thresholds novel ecosystem framework models; Bayesian approaches
for management
Trophic dynamics Improve practices to facilitate Improvements in understanding Use of stable isotopes to
faunal return, e.g., decaying of trophic networks and role determine trophic interactions
log piles, tree hollows of fauna in ecosystem and food web structure
processes
Resilience Notable as a concept that Network theory; links to Machinery with ability to detect
explicitly includes people functional diversity, scale, thresholds, i.e., small changes
thresholds and connectivity; in environmental attributes
socio-ecological systems that result in large changes in
state variable

v www.esajournals.org 5 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

reinstating locally important ecosystems or spe- growing appreciation of non-equilibrium dynam-

cies and/or involving local communities in ics, alternative ecosystem states, and thresholds
conservation and reconnecting people with na- and barriers with concomitant acknowledgement
ture. This range of projects can be implemented of the major interventions sometimes required to
from small-scales by individuals or community reverse these state changes (Whisenant 1999,
groups (e.g., Thomas 2009), to large-scales by Hobbs and Harris 2001). Thus, environmental
government agencies and programs (e.g., Yin changes prompted a conversation about the
and Yin 2010). Ultimately, project directors may degree of intervention required to meet tradi-
wish to engage people with nature, to restore tional restoration goals, and also a debate about
nature for its own sake and/or to benefit human the restoration goals themselves, that continues
wellbeing. Restoration offers the potential to to this day. Most recently, this took the form of a
incorporate different motivations and this is call for ecological restoration to be based on four
reflected in the plurality of restoration goals. principles which inform appropriate goals for
The switch from single to multiple goals parallels restoration: increasing ecological integrity, sus-
changing concepts of the relationship(s) among tainability, taking account of the past and future,
conservation, nature and people over the last and benefitting and engaging society (Suding et
century (Mace 2014). al. 2015).
Developing clear goals for restoration facili- It has been recently argued that systems are
tates shared understanding and allows progress likely to change to such an extent that alterations
to be monitored (Hobbs and Norton 1996). are no longer reversible or even desirable given
Arguably, this articulation has increased in that historical compositional references could
importance since Bradshaw’s address (December lead to ossification of systems (Harris et al.
1982). At that time, the predominant ecological 2006). This may either be due to the extent or
worldview was of deterministic systems ap- severity of changes, or because they render
proaching some kind of equilibrium in essential- restorative action impractical or beyond available
ly unchanging environmental conditions. The resources. Such ‘‘novel ecosystems’’ can then be
goal for many restorationists was hastening a considered as candidates for some other type of
return to the pre-disturbance equilibrium state. management that focuses on the benefits these
In essence, there was a clear goal for restoration, systems can provide (e.g., particular ecosystem
not open to debate except perhaps with regards services or faunal conservation) (Hobbs et al.
to methodology. Success was generally measured 2006, Hobbs et al. 2009, Hobbs et al. 2013). The
against static compositional targets that were idea of novel ecosystems is considered by some
assumed to relate to a properly functioning authors as an accurate depiction and necessary
ecosystem, usually a managed or unmanaged consideration of the current and future reality
reference state (Ruiz-Jaen and Aide 2005). Reha- facing many ecosystem managers (Kowarik 2011,
bilitation of some systems incorporated explicit Belnap et al. 2012, Doley and Audet 2013, Perring
functional targets, for example soil stabilization et al. 2013). However, it has also been criticized
at former mine sites. as a dangerous and baseless idea that runs the
In the ensuing decades, awareness grew of risk of lowering restoration standards and
simultaneous and rapid environmental changes, diminishing the restoration enterprise (Wood-
including climate change and global biodiversity worth 2013, Murcia et al. 2014). These commen-
decline. These abiotic and biotic environmental tators suggest recognizing the existence of novel
changes, which sometimes led to rapid ecosys- ecosystems threatens the progress made in
tem change with apparent hysteresis (e.g., Sud- restoration to date, whereas others suggest that
ing et al. 2004, Groffman et al. 2006, Suding and incorporating alternative approaches to deal with
Hobbs 2009, Samhouri et al. 2010), necessitated a radically altered ecosystems enlarges the range of
radical rethink of classical restoration goals (e.g., goals available for restoration and could make
Harris et al. 2006). Changes called into question for more efficient use of scarce management
aims of restoring to some historic species resources (Hobbs et al. 2014). This debate
composition or to within the historic range of remains ongoing, and the ideas are being
variability (Swetnam et al. 1999). There was a expanded and refined (Morse et al. 2014; Larson,

v www.esajournals.org 6 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

in press) and interpreted in the context of case is one aspect that has changed little since
studies across a wide range of ecosystems Bradshaw’s address in 1982, and also refers to
(Zedler et al. 2012, Graham et al. 2014, Trueman the idea that applied and fundamental sciences
et al. 2014). are arrayed on the same continuum and should
The greater awareness of complexity and influence each other (Lawton 1996, Hobbs and
contingency in ecology led to suggestions that Harris 2001). It allows us to ask: how are
references and endpoints should be viewed as ecological concepts faring against the ‘acid test’?
dynamic (Norgaard et al. 2009, Hiers et al. 2012) In other words, are advances in ecological
or even that ecosystems could be allowed to concepts aiding the setting and achievement of
develop without being directed at a particular ecological restoration goals? In the ensuing
endpoint (Hughes et al. 2012). Hence, there has sections, we will explore these questions by
been a growing call for future-focused goals that discussing how established and emerging eco-
are dynamic, process-based and functional but logical concepts, together with technological
that still account for historical knowledge, a so- advances, have been influencing the science of
called ‘‘Restoration v2.0’’ (Higgs et al. 2014), restoration ecology and practice of ecological
goals that align with anticipative management restoration since Bradshaw’s address over 30
(e.g., Rogers et al. 2015). Ultimately, desired years ago. Firstly we discuss concepts that aid
attributes of restored ecosystems will likely need achievement of compositional goals, then func-
to take far greater account of environmental tional goals, at the patch scale. We then outline
change (e.g., Shackelford et al. 2013, Poff 2014). concepts and approaches that are useful at the
This dynamic focus in an era of environmental landscape scale, and finally explore the human
change has led to many policy documents and dimension to ecological restoration. We illustrate
management agencies aiming to achieve a goal of our review with site-specific examples and
‘resilient’ ecosystems through restoration. The technological advances. However, explicit tests
concept has its roots in ecology, where the of many ecological (and socio-economic) ideas
original definition is the capacity of an ecosystem remain absent in a restoration framework, and
to absorb change and disturbance and still knowing the relative importance of different
maintain the same relationships between popu- processes in different locations is an ongoing
lations or state variables (Holling 1973). Thus, challenge that restoration ecologists need to
one can see its conceptual appeal for managing address.
dynamic ecosystems in the face of global
changes. However, it is fair to say that the RESTORING SPECIES COMPOSITION REQUIRES
concept of resilience remains difficult to quantify MORE THAN JUST PLANTS
especially in a restoration context (Brand and Jax
2007, Standish et al. 2014). Emerging research on Restoration is often seen as a largely plant-
the contribution of functional diversity to resil- focused enterprise (Young 2000). Indeed, at the
ience offers a promising way forward to oper- time of Bradshaw’s presidential address, al-
ationalizing the concept (e.g., Laliberté et al. though acknowledging the importance of fauna
2010). From a restoration perspective, it is in organic matter decomposition and pollination,
important to note that highly degraded states he stated: ‘‘From the point of view of the reconstruc-
may be very resilient to change, hence requiring tion of a properly functioning ecosystem they
large management inputs to return to a more [animals] play little part since it is the first trophic
desirable condition (Standish et al. 2014). level which is so crucial to any ecosystem’’. In this
Clearly stated goals, as developmental trajec- section, we first present conceptual ecological
tories or as compositional or functional end- advances and some technological advances that
points, increase ecological understanding have aided the establishment of plants in
through assessment of the appropriateness, ecosystems, usually to achieve compositional
achievability and the relative progress of the targets. We then highlight, in turn, recent
system towards stated goals (Zedler 2007, Hobbs evidence detailing the vital part that soil resource
et al. 2009). The idea of measuring ecological supply, soil biota (especially fungi ), plant-soil
progress against well-defined restoration success feedbacks and fauna play from the outset in

v www.esajournals.org 7 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

achieving these compositional goals. We partic- climatic oscillations (e.g., El Nino phases) may
ularly focus on the interactions amongst these aid restoration planning to improve plant estab-
facets (Fig. 2) that can determine achievement of lishment success in combination with these
goals. technological advancements (Holmgren et al.
Plant establishment requires the identification, 2006).
and, if necessary the removal, of barriers to Soil resource supply also affects the attainment
effective plant germination and survival. It may of restoration goals by influencing community
be possible for this to occur through facilitation assembly and plant-plant dynamics. Traditional-
of dispersal/creation of gaps to promote sponta- ly, plant strategy theory (Grime 1979) and plant
neous establishment of plants (Baeten et al. 2009). competition theory (Tilman 1982) formed the
However, in other areas and particularly for basis of restoration interventions; for example,
restoration at scale, the removal of barriers the use of species with traits that allowed
necessitates the efficient collection, handling establishment and growth on toxic waste from
and use of large volumes of viable seed. The mine spoil (such as hyperaccumulators and other
development of the restoration seed bank con- stress tolerators (Kramer 2010)) or attempting to
cept, in conjunction with a systems approach, has reduce high nutrient supply levels to aid the
highlighted the connected nature of processes development of the desired community compo-
ranging from seed procurement at scale, break- sition by altering competitive interactions (e.g.,
ing of dormancy and emergence, to early Marrs 1993, Perring et al. 2009). This focus has
establishment and subsequent maturation of the been broadened to include facilitative (Brooker et
young plant at restoration sites (James et al. 2011, al. 2008) and parasitic (Pywell et al. 2004, Demey
Merritt and Dixon 2011, James et al. 2013). et al. 2015) relationships. Facilitation has proven
Without considering all components of this chain to be especially important for restoration in semi-
of seed use, there remain impediments to arid environments, for instance through planting
increasing the likelihood of plant establishment nurse plants to provide appropriate conditions
in a cost-effective and predictable manner (James for survival and growth of target species (Padilla
et al. 2013). and Pugnaire 2006, Siles et al. 2008).
Recent technological advances to aid success- Soil biota are also required to improve soil
ful revegetation (Table 1) include improved seed structure and conditions and hence restoration
handling, processing and quality assessments of success (Harris 2009). Insights from agriculture
wild collected seeds (e.g., X-ray seed viability have long suggested the use of facilitative
analysis/ex situ storage) (Crawford et al. 2007, legumes to ameliorate soil conditions (Bradshaw
Probert et al. 2007, Martyn et al. 2009), and the 1983, Wong 2003). More recent studies have
use of treatments and germination stimulants to shown mycorrhizal inoculation improves plant
overcome dormancy and promote germination survival and growth (e.g., Requena et al. 2001,
(Merritt et al. 2007, Turner et al. 2013). Further- Pineiro et al. 2013) although in some systems it
more, proven agricultural seeding technologies may be the presence of a mycorrhizal network
are being modified to suit restoration programs (Simard and Durall 2004, Teste et al. 2009, Booth
using native species (Jonson 2010). Seed enhance- and Hoeksema 2010), as opposed to the presence
ment technologies such as polymer seed coating of certain mycorrhizas alone, that facilitates
and embedding seeds in a soil matrix with successful restoration.
compounds that are known to assist in promot- Knowledge of above- and belowground link-
ing germination and plant establishment, while ages (Wardle et al. 2004, Bardgett and van der
reducing pathogen attack, are also rapidly being Putten 2014) and especially plant-soil feedbacks
developed (Turner et al. 2006, Madsen et al. 2012, (Kardol and Wardle 2010) have been utilized in
Madsen et al. 2014). In combination these restoration ecology. Plant-soil feedbacks are
technological advances have been shown to be generally used to describe the negative or
critical in establishing sufficient plants for suc- positive conditioning effects that a particular
cessful restoration in some systems (e.g., Turner plant species has on the soil community which
et al. 2006). The vagaries of climate often influences subsequent growth and recruitment of
influence recruitment and better predictions of the same or different species (van der Putten et

v www.esajournals.org 8 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

al. 2013). The few plant-soil feedback experi- by studies showing the influence of top preda-
ments in a restoration context suggest that tors, such as wolves or bears, in structuring plant
restoration of a soil community may be crucial communities through their effects on herbivore
for establishing late successional plant commu- populations and behavior via antagonistic and
nities (e.g., De Deyn et al. 2003, Kardol et al. 2006, mutualistic relationships (as described eloquent-
Middleton and Bever 2012) although success is ly in Leopold’s ‘‘Thinking Like a Mountain’’;
not always observed (Kardol et al. 2009). Much Leopold 1949, Ripple and Beschta 2007, Grinath
remains to be learnt about where feedbacks are et al. 2015). Overabundance of herbivores, such
likely to affect restoration success, including how as deer, has important effects on plant commu-
closely related plants may be affected by soil nity dynamics, often, for instance, preventing
biota (Anacker et al. 2014). tree regeneration (Côté et al. 2004, Hobbs 2009).
There is increasing recognition of the impor- Removal of grazing either by fencing, culling or
tance of considering fauna from the outset in reintroduction of predators is often a prerequisite
restoration, both for their role in ecosystem for effective restoration of desired plant commu-
degradation and recovery, and for aiding the nities (Prober et al. 2011). Given that restored
reinstatement of plant communities (e.g., New- areas are often subject to heavy grazing pressure
some et al. 2015). In the past, reinstating a plant (e.g., Koch et al. 2004), it seems likely that the
community was assumed to provide ‘habitat’ for absence of top predators may result in restored
fauna: the ‘‘field of dreams’’ concept, or ‘‘build it areas developing different plant communities
and they will come’’ (Palmer et al. 1997, Sudduth than if these predators were present.
et al. 2011, Frick et al. 2014), but it is now In summary, a variety of ecological concepts
recognized that fauna can be critical for ecosys- have been applied for the achievement of
tem recovery through their role in, for example, compositional restoration goals. However, pro-
seed dispersal, pollination and/or nutrient cy- viding guidance to practitioners as to when and
cling (e.g., Tucker and Murphy 1997, Majer et al. where particular approaches may be most
2007, Lomov et al. 2010). The lack of attention to appropriate to apply remains difficult. Identify-
fauna from the outset can also lead to a lack of ing what concepts are likely to be most valuable
provision of key resources for them (e.g., tree now and in the future is clearly an avenue for
hollows or logs Vesk et al. 2008), spatial future research (see Challenges and Oppor-
mismatches between restoration and faunal tunities. . . section).
requirements, and imbalances (from the perspec-
tive of defined restoration goals) in the faunal MOVING FROM COMPOSITIONAL TO
communities that develop (Miller and Hobbs FUNCTIONAL GOALS IN A CHANGING
2007). Establishing tree islands in degraded areas ENVIRONMENT
can attract faunal components (e.g., birds) which
in turn may instigate further system changes Attention in restoration is increasingly turning
(e.g., through seed dispersal of desired species) to achievement of functional goals, beyond those
(i.e., applied nucleation Zahawi et al. [2013]). classically considered in rehabilitation projects
Technological advances in satellite technology (Montoya et al. 2012, Shackelford et al. 2013).
and GPS collars (Matthews et al. 2013) will also Functional goals, such as the delivery of ecosys-
improve our understanding of habitat use by tem services or reinstatement of trophic net-
fauna, and this will improve our ability to works, often aim for resilience to anticipated
provide suitable habitat. change. Trait-based ecology has great potential to
The addition or removal of key faunal species help achieve functional goals in the restoration of
can have complex and far-reaching effects on degraded systems and we elucidate this poten-
ecosystem composition and structure, particular- tial, across trophic levels, in this section. Restor-
ly if these species are ecosystem engineers or top ing functioning ecosystems will necessarily
order predators (Dirzo et al. 2014, Ripple et al. involve including, and understanding, the inter-
2014, Seddon et al. 2014, McCauley et al. 2015) actions between the environment and flora,
(see also functional effects in next section). The fauna and soil biota more broadly, and all the
importance of key species has been highlighted ideas require testing in a restoration framework

v www.esajournals.org 9 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

(Fig. 2). to invasion, through limiting similarity. Howev-

The response-and-effect trait framework (Sud- er, a meta-analysis of experimental studies
ing et al. 2008) conceptually demonstrates how testing the effect of functional similarity on
functional trait targets can be used in restoration invasion success, only found evidence for this
goals, and this framework has been operational- in synthetic experimental assemblages, and not
ized by the development of a quantitative in more ‘natural’ removal experiments (Price and
approach for translating trait targets into plant Pärtel 2013). Hence ‘‘restoration through reas-
species assemblages that can be directly used in sembly’’ (Funk et al. 2008) may only be useful as
restoration (Laughlin 2014). In the quantitative a guiding principle when communities are built
framework, systems can be restored by selecting de novo. Importantly, trait-based predictive
plant species to suit current, or changing, models can be used in an experimental context
environmental filters (using response traits), or to test hypotheses about which traits and species
to optimize specific ecosystem processes or combinations will be most effective at achieving
functions (using effect traits) (Suding et al. 2008, the functional targets. The effectiveness of these
Laughlin 2014). The response-and-effect trait targeted trait values for achieving restoration
framework can also be used to understand success can then be monitored over time for
multi-trophic linkages in ecosystem service pro- different experimental conditions and targets can
vision (Lavorel et al. 2013). be adjusted as we learn which traits help achieve
Response traits can be used in restoration goal restoration goals (Laughlin 2014).
setting by selecting plant species with functional Effect traits may be used in restoration to set
characteristics that should enable persistence functional targets to provide specific ecosystem
under specific abiotic conditions (Suding et al. services (Montoya et al. 2012, Perring et al. 2012).
2008). For example, if a restoration practitioner is Biodiversity and ecosystem function studies have
interested in restoring a native community that established clear links between functional com-
will be resilient to predicted future occurrences of position and varied ecosystem services (Lavorel
drought, drought-adapted species can be select- and Grigulis 2012) but there are few examples in
ed—however, where drought tolerance of species a restoration context (e.g., Doherty et al. 2011).
is not known, a trait target can be set that Large-scale experiments are needed, especially in
includes suitable plant species with higher leaf woodland systems, given the grassland and
mass per area and higher wood density as these microbial focus of this research (Cardinale et al.
traits confer greater tolerance to moisture deficits 2012). Furthermore, there is still room to improve
(Laughlin 2014). There are limits to setting our fundamental understanding of the links
specific trait targets as knowledge of which traits between biodiversity and ecosystem services
drive fitness and performance along environ- (Mace et al. 2012, Balvanera et al. 2014) in
mental gradients is still developing (Webb et al. addition to its application to restoration. Re-
2010). Recent work has highlighted the need to search is required on the importance of function-
move beyond considering adult leaf and root al diversity and identity in regulating restoration
traits to also assessing seed and seedling traits outcomes, rather than just focusing on species
when considering the role of functional traits in numbers per se (see also TreeDivNet www.
restoration performance (Larson et al. 2015). treedivnet.ugent.be; and Verheyen et al., in press).
Assessment of multiple traits is likely to improve Restoring some functions for instance could
the ability of restoration practitioners to develop involve a few species with particular traits that
restoration that is more resilient to future are critical to ecosystem processes e.g., pollina-
environmental changes. tion and seed dispersal can be conducted by
In addition to choosing plant species based on ‘hub’ species (Forup et al. 2008, Menz et al. 2011).
their traits for specific edaphic/climatic condi- Many ecosystem services rely on interactions
tions, response traits are also affected by biotic between plants and other trophic levels (e.g.,
processes. Funk et al. (2008) suggested that Kremen et al. 2007), but few studies have
strategically increasing the abundance of native examined functional trait links between these
plant species with functional traits similar to non- components of biodiversity. Recently, Lavorel et
native plant species can increase biotic resistance al. (2013) developed a conceptual framework for

v www.esajournals.org 10 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

linking plant functional diversity with other possible that accepted restoration goals and
trophic levels for the quantification of ecosystem practices for rivers may need to be reassessed
services. In an application of this framework, because they are based on a reference situation
Moretti et al. (2013) demonstrated that, under that lacks the influence of beavers (Burchsted et
land management change, a plant trait (leaf dry al. 2010). Restoration may aim to reintroduce
matter content) related to the grasshopper trait of such engineers; indeed beavers have a long
dry body mass which then acted as an effect trait history of translocation accompanied by interest-
on primary production via a negative link to ing methodologies including via parachute (He-
plant biomass. Thus, the functional goal of ter 1950).
restoring ecosystem services likely needs to Recent debates discuss the extent to which
consider trophic levels other than plants. This species might be substitutable, and hence func-
consideration extends to vertebrates, but we are tions performed by recently extinct species could
not aware of research that has specifically be reinstated by the translocations of closely
utilized the response-effect framework to include related extant species (e.g., Griffiths et al. 2013,
these organisms. Hunter et al. 2013). An extreme form of this
Fauna affect the flow of energy through approach is what has been dubbed ‘‘rewilding’’
ecosystems via trophic cascades and networks (e.g., Donlan et al. 2005), in which functional
(Terborgh and Estes 2010, Sandom et al. 2013b, equivalents of long-extinct but presumably key-
Fleming et al. 2014). In addition to the impor- stone species are introduced to ecosystems.
tance of trophic cascades in determining ecosys- Debate over this approach has mirrored larger
tem composition (see previous section), trophic discussions in restoration about the appropriate-
network theory highlights the importance of key ness of different reference systems on which to
species in ensuring a functioning ecosystem. model restored ecosystems, and, if past ecosys-
Conceptual developments include acknowledg- tems are to be used as a template, how far into
ing that trophic networks contain strong and the past is it appropriate to consider? It is likely
weak links and trophic modules (Kondoh 2008). that some time spans are too large a gap to
Varying link strengths likely determine the extent restore across, because in the intervening time
to which loss or addition of a particular species ecosystems have almost certainly developed into
affects the success of restoration efforts. In a new condition. This time gap likely varies
addition, many recent studies have highlighted widely between ecosystems and continents and
how a changing environment (warming in whether restoration goals are compositional or
particular) has created a ‘trophic mismatch’ functional.
between the emergence of prey species and the The restoration of function may also rely on
breeding of their predators, typically leading to interactions among plants and soil, for example
reduced breeding success in the predators (Both nutrient cycling involves complex interactions
et al. 2009, Donnelly et al. 2011). While this between plants, soil biota and their associated
phenomenon, to the best of our knowledge, has traits (Kardol et al. 2015). Simulation modeling
not been studied in restored areas, it highlights using trait frameworks provides a means to
that the complexity of trophic networks provide advance fundamental understanding in this area,
many challenges to increasing the success of and may have application to ecological restora-
restoration efforts. tion (Ke et al. 2015). Additionally, recent techno-
Fauna can also be important ecosystem engi- logical advances in high throughput DNA
neers in many ecosystems (e.g., Sandom et al. sequencing and functional gene analysis may
2013a) and, by definition, their presence will allow rapid assessment of what functional genes
fundamentally influence the type of restored are present in systems and how they relate to soil
community that develops. Beavers provide a microbial composition and ecosystem function
classic example of an ecosystem engineer that act (Zimmerman et al. 2014). The functional (and
as potential restoration agents through slowing compositional) gap between reference and re-
water flows and altering stream morphology stored ecosystems (Rey-Benayas et al. 2009,
with subsequent cascading impacts (Albert and Banning et al. 2011) may likely be due to the
Trimble 2000, Pollock et al. 2014). Indeed, it is decoupling of above- and belowground linkages

v www.esajournals.org 11 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

that occurs following land clearance and the time There is ongoing effort to find cost-effective,
taken for ecosystems to approach the chosen practical and successful methods for achieving
reference. This idea remains an untested hypoth- broad-scale restoration (Jonson 2010, St Jack et al.
esis but the decreasing cost of these genetic 2013). Technological improvements can be com-
technologies should allow its investigation, in- plemented with the use of simulation models to
cluding testing the reintroduction of specific identify restoration priorities based on habitat
functional genes and phylogenetic diversity to characteristics and land-parcel prices (e.g., Tor-
improve restoration outcomes. rubia et al. 2014). However, upscaling may not
always be straightforward, with the adopted
MAGNITUDE OF ENVIRONMENTAL CHANGES management approach depending on the type of
REQUIRES RESTORATION AT SCALE landscape under consideration. Where individu-
al management units are significantly smaller
Restoration science and practice has tradition- than the landscape in which they sit (for instance,
ally considered mainly the restoration of partic- in agricultural landscapes with fragmented na-
ular ecosystems or patches in particular places. tive ecosystems or urban and peri-urban areas)
However, the scale of environmental changes effective landscape management requires co-
requires the adoption of a landscape perspective ordination of, and co-operation among, multiple
in restoration, for instance where there has been landholders and managers, each with potentially
regional hydrological change or large scale conflicting goals and approaches (Gobster 2001).
deforestation or tree mortality (Allen et al. This is presumably less of an issue in larger
2015). In this section we explore the ecological management units such as large pastoral prop-
concepts underpinning restoration at scale draw- erties or national parks.
ing on the field of landscape ecology in partic- Landscapes are likely to comprise an array of
ular. Further, we explore the challenges and patch or ecosystem types in different conditions,
opportunities that a multi-functional landscape each providing an array of benefits or dis-
perspective provides for ecological restoration in benefits, and each likely to require differing
a changing environment. management approaches, both individually and
The need to scale-up restoration activities as part of a broader landscape or regional
demands that the patch-based approach consider strategy (Zedler et al. 2012, Hobbs et al. 2014).
processes at the broader landscape- and regional- This patchwork provides an opportunity for
scales, for example movement of water or restoration: an overall goal of landscape multi-
dispersal of biota (Menz et al. 2013). This need functionality may allow the provision of multiple
has perhaps been most evident in efforts to ecosystem services that would not be possible by
restore aquatic ecosystems with consideration of considering the individual patch scale alone
processes from the scale of individual river (Jarchow and Liebman 2011, Potschin and
reaches through to entire regional river or Haines-Young 2011, Schindler et al. 2014). Recent
wetland systems (e.g., Culotta 1995, Gunderson initiatives point to effective ways to map and
et al. 1995). Advances in the application of assess ecosystem services at landscape scales
Geographic Information Systems (GIS) technolo- (Nelson et al. 2009, Kareiva et al. 2011) while
gy have brought new understanding to questions policy instruments such as payments for ecosys-
around aquatic dispersal. For instance, in the tem services provide mechanisms for achieving
Great Lakes Basin, common assumptions about multifunctionality through funding restoration
restoring connectivity for fish populations (van Noordwijk et al. 2012).
through tackling problems with dams misses Conceptually, discussion of landscape restora-
opportunities to aid dispersal by addressing tion has progressed from ideas about habitat size
barriers created by the far more numerous road and number (e.g., several small reserves versus
crossings; opportunities that were only made one large reserve) to habitat corridors and then to
apparent through GIS analysis (Januchowski- assessing the role of the whole landscape matrix
Hartley et al. 2013). Ecological restoration is in promoting or inhibiting biotic movement
harnessing the power of such technologies for (Lindenmayer et al. 2008). The management of
more effective landscape-scale restoration. the matrix could determine restoration outcomes

v www.esajournals.org 12 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

for biodiversity, with three core matrix effects restoration goals (Gold et al. 2006, Egan et al.
(movement and dispersal, resource availability 2011, Naiman 2013, Shackelford et al. 2013).
and abiotic environment) being modified by five There is growing emphasis on the requirement to
dimensions: spatial and temporal variation in consider ecological, socio-economic and gover-
matrix quality, its spatial scale, the longevity and nance aspects of ecosystem management (Car-
demographic rates of species relative to the penter et al. 2009, Hobbs et al. 2011). This idea is
temporal scale of matrix variation, and adapta- not new: As the Ecological Society of America
tion (Driscoll et al. 2013). Landscape connectivity was just emerging from its teenage years in 1935,
is increasingly seen as a key conservation and Aldo Leopold noted that: ‘‘One of the anomalies of
restoration goal, particularly as a strategy to modern ecology is the creation of two groups, each of
allow biotic movement in response to changing which seems barely aware of the existence of the other.
environments (Roever et al. 2013, Tambosi et al. The one studies the human community, almost as if it
2014, Okin et al. 2015). Deciding what and where were a separate entity, and calls its findings sociology,
to restore is a key challenge for future landscape- economics and history. The other studies the plant and
scale restoration efforts (McRae et al. 2012, animal community and comfortably relegates the
Torrubia et al. 2014). Decisions may be aided hodge-podge of politics to the liberal arts. The
by technological advances around, for instance, inevitable fusion of these two lines of thought will,
the application of climate velocity models in perhaps, constitute the outstanding advance of this
conjunction with more traditional ecological [20th] century’’ (quoted in Knight and Riedel
models to ascertain areas of potential future 2002).
habitat suitability as targets for restoration efforts Although restoration may focus on ecosystems
(Hamann et al. 2015). and non-human species, it is primarily a human
Landscape and regional approaches require endeavor, with a range of motivations and goals.
effective ways of directing and prioritizing Some types of restoration will be driven mostly
restoration efforts. Numerous decision support by economic considerations, while others will be
approaches to this problem are evolving (e.g., more focused on participatory or eco-cultural
Thomson et al. 2009, Wilson et al. 2011, Egoh et perspectives. Whichever perspective predomi-
al. 2014), although deciding what characteristics nates in any given situation, there is increasing
should be included in the prioritization process is recognition that cost-effectiveness is an essential
not a straightforward process (Knight et al. 2011, ingredient for good design of restoration projects
Tambosi et al. 2014). Decisions will in any case (McConnachie et al. 2012). Cost effectiveness will
continue to include both local and landscape be enhanced by solution scanning (Sutherland et
dimensions—for instance, priorities for restora- al. 2014) and is a pre-requisite for broad scale
tion involving weed management will depend on restoration. Additionally, restoration of ecosys-
the likelihood of weeds spreading from one patch tems and their services can be seen as having
to another (e.g., Trueman et al. 2014). important socio-economic benefits (e.g., job
creation, farm income) that have only recently
RESTORATION IN COMPLEX, SOCIO- begun to be factored into assessments of resto-
ECOLOGICAL SYSTEMS ration success (Aronson et al. 2010, Nielsen-
Pincus and Moseley 2013, Wortley et al. 2013)
The importance of the human dimension in and thus cost effectiveness. Ecological restoration
ecological restoration was recognized early (e.g., is now a big business, with many non-govern-
see remarks in Bradshaw 1983, Geist and mental organizations and government agencies
Galatowitsch 1999), and restoration is widely investing large amounts of money in the enter-
acknowledged to be value laden, context driven, prise and many businesses making money from
prone to disagreement and compromise, and undertaking restoration at all scales. Cunning-
experiential (Egan et al. 2011). There is increasing ham (2002) has suggested that we are entering
recognition of the importance of social and the era of the ‘‘restoration economy’’ where more
economic factors in determining restoration and more economic activity is derived from
success (e.g., Jacobs et al. 2013) and the need to restoring existing infrastructure and repairing
understand the human dimension in meeting ecosystems rather than investing in new infra-

v www.esajournals.org 13 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

structure. in, and overlap among, the social, technological

Egan et al. (2011) identified three themes and ecological spheres is enhanced (Jacobs et al.
characterizing human involvement in restora- 2013). Using American chestnut (Castanea denta-
tion: participation (e.g., volunteering; collabora- ta) as an example, Jacobs et al. (2013) demon-
tion); power (e.g., restoration economics; politics, strated how technological advances in blight
planning and governance); and, perspective (eco- resistance potentially allow C. dentata’s successful
cultural restoration; restoration-based educa- reintroduction. However, this would only be
tion). They suggest that to improve restoration possible with an adequate understanding of the
success, participation has to be embraced as an contemporary ecology of eastern North Ameri-
integral part of the process. There are two main can forests which are substantially changed from
arguments for embracing participation: on the when the chestnut was extirpated (McEwan et al.
one hand democratic rights and public skepti- 2011). Jacobs et al. (2013) note the critical need for
cism about science, and on the other involvement a deeper understanding of societal influences
of stakeholders leading to greater quality, dura- (including governmental policy and regulation,
bility and ownership of decisions (Reed 2008). collaborative networks and cultural or economic
There is surprisingly little empirical research to valuation) when setting and achieving realistic
test these arguments (e.g., van Marwijk et al. restoration goals, particularly around genetic
2012, Petursdottir et al. 2013), but decision modification. In their qualitative analysis, resto-
making quality appears to be strongly dependent ration of American chestnut to eastern North
on the processes involved, especially highly American forests will only be successful (i.e., C.
skilled facilitation (Reed 2008). Community dentata will once again be present) if social as
restoration/conservation projects that perceive well as technological and ecological aspects are
local people as the solution to habitat degrada- taken into account (Jacobs et al. 2013).
tion, and involve them at all stages of project Quantitative evaluations of coupled SES, espe-
development, appear to perform better than large cially in a restoration context, are even rarer (e.g.,
scale ‘integrated conservation and development Jellinek et al. 2014). However, the ability to
projects’ (Horwich and Lyon 2007). For instance, quantitatively describe these systems will likely
Reyes (2011) argued that a controlling and lead to better evaluation of broader policy
hierarchical approach to restoration led to a poor options and potential leverage points to improve
restoration outcome following a chemical spill in restoration outcomes, especially as situations
Spain, while an inclusive and heterarchical begin to lie outside the range of previous
approach led to successful restoration in Costa experience (Cooke et al. 2009, Hobbs et al. 2011,
Rica. Restoration outcomes will likely be im- Rounsevell et al. 2012). For instance, Watkinson
proved when power relations are overtly recog- et al. (2000) showed that an interaction between
nized and discussed and multiple perspectives of an ecological variable (field weed population)
restoration, nature and people’s role in both are and social variable (attitude to GM crops) was
dealt with respectfully (Egan et al. 2011). crucial to the ecological outcome (bird popula-
Effectively combining ecological and social tion dynamics) in agricultural landscapes. Simu-
considerations likely requires a coupled socio- lation models and game theory (Buckley and
ecological systems (SES) framework approach, Holl 2011) may be useful tools to understand
which recognizes complex interactions between complex SES and the effects of management
people and ecological entities and processes interventions. Agent based modeling offers an
(Peralta et al. 2014). Socio-ecological systems especially useful way forward as it has the
are the epitome of complex adaptive systems capacity to represent people, their behavior, and
(sensu Levin 1998) and generally consist of a decision making processes in coupled models.
resource system, resource units, users and Moreover, it is appealing for validation purposes
governance systems (Ostrom 2009). Qualitative due to a one-to-one mapping between virtual
investigations of SES have been conducted (e.g., and real-world entities as opposed to the
case studies in Turner II et al. 2003) though less ‘average’ characterization of people in top-down
commonly in a restoration context. Restoration is equation based models (Rounsevell et al. 2012). It
arguably more likely to be successful if capacity may be possible to use a trait-based approach to

v www.esajournals.org 14 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

support the expansion of such models beyond issues will likely require inclusive and participa-
case studies, while there is also a need to tory approaches, and the involvement of philos-
represent institutional agents in SES models. A ophers, economists, social scientists, landscape
key challenge in this approach is the identifica- planners and the broader community. Frame-
tion of actors who drive SES changes in the real works such as anthromes may provide a means
world and the mapping of such actors onto to aid decision making and prioritization at the
agents in the models (Rounsevell et al. 2012). global scale (Martin et al. 2014). Opportunities
Restoration is an inherently human enterprise, also exist for using simulation models to analyze
and as its scale of application broadens, more cost-effective prioritization of restoration at the
and more stakeholders will need to be included landscape scale (e.g., Torrubia et al. 2014).
in planning and implementation. With increased
participation, comes the challenge of reaching Addressing context dependency
consensus over goals and prioritization of effort. Understanding context dependency will
Coupled socio-ecological systems analysis, both strengthen the science of ecology (Belovsky et
qualitative and quantitative, will likely aid in al. 2004) but it remains, according to some, the
achieving restoration outcomes that are signifi- biggest challenge facing ecologists (Tylianakis et
cant and meaningful for nature and for people, al. 2008). Developing a global evidence base to
but it is not without its challenges, both understand when different interventions work
technological and conceptual. where, and why, would be a useful future avenue
to pursue (Sutherland et al. 2004, Pullin and
CHALLENGES AND OPPORTUNITIES FOR Knight 2009). Furthermore, it would be useful to
RESTORATION ECOLOGY consider how restoration ecologists can be
involved in the design and implementation of
Clearly, there is a solid conceptual foundation large restoration projects, while at the same time
from which restoration ecology can continue to encouraging more practitioners to explore the
build. Conceptual development, technological adoption of experimental approaches when
advances, and insights from other disciplines conducting practical restoration activities. While
appear to be better equipping ecological restora- this is largely classical adaptive management,
tion to tackle simultaneous environmental chang- there remain few examples of where this has
es. However, a number of intersecting challenges been effectively implemented. Context depen-
and opportunities remain for the coming de- dency may even determine when the scientific
cades. method can directly aid ecological restoration, or
when beneficial effects appear indirectly
Goals, priorities and human involvement through, for example, increased prestige and
for restoration visibility of projects (Cabin 2007).
An ongoing debate surrounds realistic and A complementary area of research is to
socially acceptable goals for restoration across understand which ecological concepts are most
scales and in a rapidly changing environment useful to achieving restoration goals in different
(Woodworth 2013, Hobbs et al. 2014, Murcia et environmental and socio-economic contexts. Ca-
al. 2014). Understanding people’s perceptions of pability now exists for carrying out synthetic
nature and how they value it, both historical and analyses of context dependencies in restoration
modern versions, will help to inform this debate outcomes using open access data and techniques
(Clayton and Myers 2009). The involvement of such as meta-analysis. However, interchange of
people provides a challenge of its own: how does information between restoration practitioners
one engage a globally ‘urban’ population which and the academic field of restoration ecology, as
has become more decoupled from nature to well as comparability of measures of restoration
become involved to do this? Allied questions outcomes, remains an important challenge
focus on how to prioritize restoration activities, (Young et al. 2005). Advances in digital technol-
and determining what interventions should be ogy, including speed and capacity of databases,
carried out where in multifunctional landscapes allows for the sharing and analysis of informa-
(Hobbs et al. 2011). Successful resolution of these tion in ways not previously encountered, while

v www.esajournals.org 15 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

novel analytical methods to transfer results to recent study used scenarios to understand the
data-poor systems are being developed (e.g., role of governance in achieving large-scale
Lester et al. 2014). These endeavors may be restoration in the agricultural landscape of the
further aided by developing globally distributed Tasmanian Midlands of Australia. The study
experiments (Borer et al. 2014), along gradients helped to clarify the roles and responsibilities of
of management action and environmental fac- landowners, government and other stakeholders,
tors, and through support of developing cyber- and to identify the types of restoration initiatives
infrastructure (Michener et al. 2012). Ultimately, and political support likely to result in successful
embracing complexity and context dependency outcomes for biodiversity conservation (Mitchell
in restoration activities may lead to more et al. 2014).
successful restoration as ecological principles Restoration ecologists also have the opportu-
are adopted, tested and adapted (Eviner and nity to become more involved in policy debates
Hawkes 2008). and development (Jorgensen et al. 2014). It is
argued that integrating their research with policy,
Maintaining evolutionary potential as well as tackling the challenges and opportu-
Maintaining evolutionary potential in frag- nities of public outreach at the interface of
mented landscapes is a common ultimate goal ecology and society (Groffman et al. 2010), will
of restoration (Mijangos et al. 2015) and this may improve restoration outcomes. For instance,
be aided by offsite preservation of seeds in vaults Jorgensen et al. (2014) showed only three out of
(Holsinger 1995), and the application of contro- 58 articles in restoration-related journals that
versial new techniques such as de-extinction referred to climate change or global warming in
(Sherkow and Greely 2013). However, the use the abstract identified specific policies relevant to
of seed vaults, while maintaining the legacy of their research results. In two of the three cases,
biodiversity, should not de-emphasize the im- the lead author was not a restoration ecologist.
portance of in situ adaptation that can occur in a They argue that more explicit reference to
changing environment (Schoen and Brown 2001, policies and terminology recognizable to policy
Leger 2008). The technique of de-extinction, and makers might enhance impact of restoration
allied ideas around genetic modification, trans- ecology on decision making processes (Jorgensen
location and taxon substitution, raise serious et al. 2014).
ethical concerns (Minteer 2014) that will likely
only be addressed through public debate. CONCLUDING REMARKS: MEETING THE
ENVIRONMENTAL CHALLENGES OF THE
Inter-disciplinary socio-ecological research COMING DECADES
with improved links to policy
It is increasingly important for restoration In the 100 years since the founding of the
ecologists to become more aware of, and adept Ecological Society of America (ESA), ecological
in applying, social science methods and concep- concepts have been developed, refined, recycled
tual frameworks; in essence, both ecologists and and sometimes discarded. Restoration ecology,
social scientists need to understand each other and its practice ecological restoration, provides
better (Cooke et al. 2009, St John et al. 2014, an arena to further test established and emerging
Buizer et al. 2015). This understanding may be ecological theories. We reviewed how composi-
best achieved through training young researchers tional and functional restoration goals, across
in both social and ecological approaches rather scales, may be reached through the application of
than bringing teams of disciplinary focused ecological understanding. An understanding of
researchers together that often speak very differ- which concepts are most usefully applied where,
ent languages (St John et al. 2014). It will also and when, is a critical research priority. Impor-
likely require a greater variety of techniques than tantly, we showed how the restoration enterprise
are currently utilized to quantify human values will be unlikely to succeed without considering
and cultural ecosystem services, and greater the human dimension. The need for interdisci-
emphasis on assessing the credibility of integrat- plinary approaches and the integration of the
ed models (Cooke et al. 2009). For example, a social sphere and values-based perspectives with

v www.esajournals.org 16 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

‘objective’ science remains a challenge for meet- Murphy. 2011. Soil microbial community succes-
ing restoration targets. Now, as the ESA looks to sional patterns during forest ecosystem restoration.
its next century, this integration is of paramount Applied and Environmental Microbiology
importance, as the scale of the environmental 77:6158–6164.
Bardgett, R. D., and W. H. van der Putten. 2014.
challenges facing humanity becomes ever more
Belowground biodiversity and ecosystem function-
apparent. ing. Nature 515:505–511.
Barnosky, A. D., et al. 2012. Approaching a state shift
ACKNOWLEDGMENTS in Earth’s biosphere. Nature 486:52–58.
Bastyan, G. R., and M. L. Cambridge. 2008. Transplan-
All authors contributed to discussions and wrote tation as a method for restoring the seagrass
sections of the paper. We acknowledge support from Posidonia australis. Estuarine, Coastal and Shelf
an Australian Research Council (ARC) Laureate Science 79:289–299.
Fellowship (R. J. Hobbs), the ARC Centre of Excellence Belnap, J., J. A. Ludwig, B. P. Wilcox, J. L. Betancourt,
for Environmental Decisions, the Natural Environ- W. R. J. Dean, B. D. Hoffman, and S. J. Milton. 2012.
mental Research Program Environmental Decisions Introduced and invasive species in novel rangeland
Hub, the Western Australia Fellowship Programme (A. ecosystems: friends or foes? Rangeland Ecology
S. Whiteley) and support MPP received from the and Management 65:569–578.
National Socio-Environmental Synthesis Center (SE- Belovsky, G. E., D. B. Botkin, T. A. Crowl, K. W.
SYNC), NSF Award DBI-1052875. Thanks to two Cummins, J. F. Franklin, M. L. Hunter, Jr., A. Joern,
anonymous reviewers, Erle Ellis, Stephen Murphy, D. B. Lindenmayer, J. A. MacMahon, C. R. Mar-
Lyn Perring, Tim Seastedt, Kris Verheyen and Natasha gules, and J. M. Scott. 2004. Ten suggestions to
Wiggins for valuable comments on earlier drafts of this strengthen the science of ecology. BioScience
article. Funding bodies had no bearing on the contents 54:345–351.
of the manuscript, nor the decision to submit. Booth, M. G., and J. D. Hoeksema. 2010. Mycorrhizal
networks counteract competitive effects of canopy
LITERATURE CITED trees on seedling survival. Ecology 91 2294 - 2302.
Borer, E. T., W. S. Harpole, P. B. Adler, E. M. Lind, J. L.
Albert, S., and T. Trimble. 2000. Beavers are partners in Orrock, E. W. Seabloom, and M. D. Smith. 2014.
riparian restoration on the Zuni Indian Reserva- Finding generality in ecology: a model for globally
tion. Ecological Restoration 18:87–92. distributed experiments. Methods in Ecology and
Allen, C. D., D. D. Breshears, and N. G. McDowell. Evolution 5:65–73.
2015. On underestimation of global vulnerability to Both, C., M. Van Asch, R. G. Bijlsma, A. B. Van Den
tree mortality and forest die-off from hotter Burg, and M. E. Visser. 2009. Climate change and
drought in the Anthropocene. Ecosphere 6(8):129. unequal phenological changes across four trophic
Anacker, B. L., J. N. Klironomos, H. Maherali, K. O. levels: Constraints or adaptations? Journal of
Reinhart, and S. Y. Strauss. 2014. Phylogenetic Animal Ecology 78:73–83.
conservatism in plant-soil feedback and its impli- Bradshaw, A. D. 1983. The reconstruction of ecosys-
cations for plant abundance. Ecology Letters tems: Presidential address to the British Ecological
17:1613–1621. Society, December 1982. Journal of Applied Ecolo-
Aronson, J., et al. 2010. Are socioeconomic benefits of gy 20:1–17.
restoration adequately quantified? A meta-analysis Brand, F. S., and K. Jax. 2007. Focusing meaning(s) of
of recent papers (2000–2008) in Restoration Ecology resilience: resilience as a descriptive concept and a
and 12 other scientific journals. Restoration Ecolo- boundary object. Ecology and Society 12:23.
gy 18:143–154. Brooker, R. W., et al. 2008. Facilitation in plant
Baeten, L., H. Jacquemyn, H. Van Calster, E. Van Beek, communities: the past, the present, and the future.
R. Devlaeminck, K. Verheyen, and M. Hermy. 2009. Journal of Ecology 96:18–34.
Low recruitment across life stages partly accounts Brudvig, L. A. 2011. The restoration of biodiversity:
for the slow colonization of forest herbs. Journal of Where has research been and where does it need to
Ecology 97:109–117. go? American Journal of Botany 98:549–558.
Balvanera, P., I. Siddique, L. Dee, A. Paquette, F. Isbell, Buckley, M., and K. Holl. 2011. Game theory tools for
A. Gonzalez, J. Byrnes, M. I. O’Connor, B. A. improving ecological restoration outcomes. Pages
Hungate, and J. N. Griffin. 2014. Linking biodiver- 239–253 in D. Egan, E. E. Hjerpe, and J. Abrams,
sity and ecosystem services: Current uncertainties editors. Human dimensions of ecological restora-
and the necessary next steps. BioScience 64:49–57. tion. Integrating science, nature and culture. Island
Banning, N. C., D. B. Gleeson, A. H. Grigg, C. D. Press, Washington, D.C., USA.
Grant, G. L. Andersen, E. L. Brodie, and D. V. Buizer, M., K. X. Ruthrof, S. A. Moore, E. J. Veneklaas,

v www.esajournals.org 17 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

G. Hardy, and C. Baudains. 2015. A critical natural grasslands. Journal of Vegetation Science
evaluation of interventions to progress transdisci- 26:409–420.
plinary research. Society and Natural Resources Dirzo, R., H. S. Young, M. Galetti, G. Ceballos, N. J. B.
28:670–681. Isaac, and B. Collen. 2014. Defaunation in the
Burchsted, D., M. Daniels, R. Thorson, and J. Vokoun. Anthropocene. Science 345:401–406.
2010. The river discontinuum: applying beaver Dixson, D. L., D. Abrego, and M. E. Hay. 2014.
modifications to baseline conditions for restoration Chemically mediated behavior of recruiting corals
of forested headwaters. BioScience 60:908–922. and fishes: A tipping point that may limit reef
Cabin, R. J. 2007. Science-driven restoration: A square recovery. Science 345:892–897.
grid on a round earth? Restoration Ecology 15:1–7. Dobson, A. P., A. D. Bradshaw, and A. J. M. Baker.
Campbell, A. H., E. M. Marzinelli, A. Verges, M. A. 1997. Hopes for the future: restoration ecology and
Coleman, and P. D. Steinberg. 2014. Towards conservation biology. Science 277:515–522.
restoration of missing underwater forests. PLoS Doherty, J. M., J. C. Callaway, and J. B. Zedler. 2011.
ONE 9:e84106. Diversity-function relationships changed in a long-
Cardinale, B. J., et al. 2012. Biodiversity loss and its term restoration experiment. Ecological Applica-
impact on humanity. Nature 486:59–67. tions 21:2143–2155.
Carpenter, S. R., et al. 2009. Science for managing Doley, D., and P. Audet. 2013. Adopting novel
ecosystem services: Beyond the Millennium Eco- ecosystems as suitable rehabilitation alternatives
system Assessment. Proceedings of the National for former mine sites. Ecological Processes 2:22.
Academy of Sciences USA 106:1305–1312. Donlan, J., et al. 2005. Re-wilding North America.
Carrick, P. J., T. E. Erickson, C. H. Becker, C. E. Nature 436:913–914.
Mayence, and A. R. Bourne. 2015. Comparing Donnelly, A., A. Caffarra, and B. F. O’Neill. 2011. A
ecological restoration in South Africa and Western review of climate-driven mismatches between
Australia: the benefits of a ‘travelling workshop.’ interdependent phenophases in terrestrial and
Ecological Management and Restoration 16:86–94. aquatic ecosystems. International Journal of Bio-
Clayton, S., and G. Myers. 2009. Conservation psy- meteorology 55:805–817.
chology: understanding and promoting human Driscoll, D. A., S. C. Banks, P. S. Barton, D. B.
care for nature. Wiley-Blackwell, Chichester, UK. Lindenmayer, and A. L. Smith. 2013. Conceptual
Cooke, I. R., et al. 2009. Integrating socio-economics domain of the matrix in fragmented landscapes.
and ecology: a taxonomy of quantitative methods Trends in Ecology & Evolution 28:605–613.
and a review of their use in agro-ecology. Journal of Egan, D., E. E. Hjerpe, and J. Abrams, editors. 2011.
Applied Ecology 46:269–277. Human dimensions of ecological restoration: inte-
Côté, S. D., T. P. Rooney, J.-P. Tremblay, C. Dussault, grating science, nature and culture. Island Press,
and D. M. Waller. 2004. Ecological impacts of deer Washington, D.C., USA.
overabundance. Annual Review of Ecology and Egoh, B. N., M. L. Paracchini, G. Zulian, J. P. Schägner,
Systematics 35:113–147. and G. Bidoglio. 2014. Exploring restoration op-
Crawford, A. D., K. J. Steadman, J. A. Plummer, A. tions for habitats, species and ecosystem services in
Cochrane, and R. J. Probert. 2007. Analysis of seed- the European Union. Journal of Applied Ecology
bank data confirms suitability of international 51:899–908.
seed-storage standards for the Australian flora. Elliott, M., D. Burdon, K. L. Hemingway, and S. E.
Australian Journal of Botany 55:18–29. Apitz. 2007. Estuarine, coastal and marine ecosys-
Culotta, E. 1995. Bringing back the Everglades. Science tem restoration: confusing management and sci-
268:1688–1690. ence—a revision of concepts. Estuarine, Coastal
Cunningham, S. 2002. The restoration economy. and Shelf Science 74:349–366.
Berrett-Koehler, San Francisco, California, USA. Ellis, E. C. 2015. Ecology in an anthropogenic
De Deyn, G. B., C. E. Raaijmakers, H. R. Zoomer, M. P. biosphere. Ecological Monographs. doi: 10.1890/
Berg, P. C. de Ruiter, H. A. Verhoef, T. M. Bezemer, 14-2274.1
and W. H. van der Putten. 2003. Soil invertebrate Eviner, V. T., and C. V. Hawkes. 2008. Embracing
fauna enhances grassland succession and diversity. variability in the application of plant-soil interac-
Nature 422:711–713. tions to the restoration of communities and
DeFries, R. S., et al. 2012. Planetary opportunities: a ecosystems. Restoration Ecology 16:713–729.
social contract for global change science to contrib- Fleming, P. A., H. Anderson, A. S. Prendergast, M. R.
ute to a sustainable future. BioScience 62:603–606. Bretz, L. E. Valentine, and G. E. S. Hardy. 2014. Is
Demey, A., P. De Frenne, L. Baeten, G. Verstraeten, M. the loss of Australian digging mammals contribut-
Hermy, P. Boeckx, and K. Verheyen. 2015. The ing to a deterioration in ecosystem function?
effects of hemiparasitic plant removal on commu- Mammal Review 44:94–108.
nity structure and seedling establishment in semi- Forup, M. L., K. S. E. Henson, P. G. Craze, and J.

v www.esajournals.org 18 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

Memmott. 2008. The restoration of ecological Harris, J. 2009. Soil microbial communities and
interactions: plant-pollinator networks on ancient restoration ecology: Facilitators or followers? Sci-
and restored heathlands. Journal of Applied ence 325:573–574.
Ecology 45:742–752. Harris, J. A., R. J. Hobbs, E. Higgs, and J. Aronson.
Frick, K. M., A. L. Ritchie, and S. L. Krauss. 2014. Field 2006. Ecological restoration and global climate
of dreams: restitution of pollinator services in change. Restoration Ecology 14:170–176.
restored bird-pollinated plant populations. Resto- Heter, E. W. 1950. Transplanting beavers by airplane
ration Ecology 22:832–840. and parachute. Journal of Wildlife Management
Funk, J. L., E. E. Cleland, K. N. Suding, and E. S. 14:143–147.
Zavaleta. 2008. Restoration through reassembly: Hiers, J. K., R. J. Mitchell, A. Barnett, J. R. Walters, M.
plant traits and invasion resistance. Trends in Mack, B. Williams, and R. Sutter. 2012. The
Ecology & Evolution 23:695–703. dynamic reference concept: measuring restoration
Geist, C., and S. M. Galatowitsch. 1999. Reciprocal success in a rapidly changing no-analogue future.
model for meeting ecological and human needs in Ecological Restoration 30:27–36.
restoration projects. Conservation Biology 13:970– Higgs, E., D. A. Falk, A. Guerrini, M. Hall, J. Harris,
979. R. J. Hobbs, S. T. Jackson, J. M. Rhemtulla, and W.
Gobster, P. H. 2001. Visions of nature: conflict and Throop. 2014. The changing role of history in
compatability in urban park restoration. Landscape restoration ecology. Frontiers in Ecology and the
and Urban Planning 56:35–51. Environment 12:499–506.
Gold, W., K. Ewing, J. Banks, M. Groom, T. Hinckley, Hobbs, R. J. 2009. Woodland restoration in Scotland:
D. Secord, and D. Shebitz. 2006. Collaborative ecology, history, culture, economics, politics and
ecological restoration. Science 312:1880–1881. change. Journal of Environmental Management
Graham, N. A. J., J. E. Cinner, A. V. Norstrom, and M. 90:2857–2865.
Nystrom. 2014. Coral reefs as novel ecosystems: Hobbs, R. J., L. M. Hallett, P. R. Ehrlich, and H. A.
embracing new futures. Current Opinion in Envi- Mooney. 2011. Intervention ecology: applying
ronmental Sustainability 7:9–14. ecological science in the 21st Century. BioScience
Griffiths, C. J., N. Zuel, C. G. Jones, Z. Ahamud, and S. 61:442–450.
Harris. 2013. Assessing the potential to restore Hobbs, R. J., and J. A. Harris. 2001. Restoration
historic grazing ecosystems with tortoise ecological ecology: repairing the Earth’s ecosystems in the
replacements. Conservation Biology 27:690–700. new millennium. Restoration Ecology 9:239–246.
Grime, J. P. 1979. Plant strategies and vegetation Hobbs, R. J., E. S. Higgs, and C. M. Hall, editors. 2013.
processes. First edition. John Wiley and Sons, Novel ecosystems: intervening in the new ecolog-
Chichester, UK. ical world order. Wiley-Blackwell, Oxford, UK.
Grinath, J. B., B. D. Inouye, and N. Underwood. 2015. Hobbs, R. J., E. Higgs, and J. A. Harris. 2009. Novel
Bears benefit plants via a cascade with both ecosystems: implications for conservation and
antagonistic and mutualistic interactions. Ecology restoration. Trends in Ecology & Evolution
Letters 18:164–173. 24:599–605.
Groffman, P. M., C. Stylinski, M. C. Nisbet, C. M. Hobbs, R. J., and D. A. Norton. 1996. Towards a
Duarte, R. Jordan, A. Burgin, M. A. Previtali, and J. conceptual framework for restoration ecology.
Coloso. 2010. Restarting the conversation: chal- Restoration Ecology 4:93–110.
lenges at the interface between ecology and society. Hobbs, R. J., et al. 2006. Novel ecosystems: theoretical
Frontiers in Ecology and the Environment 8:284– and management aspects of the new ecological
291. world order. Global Ecology and Biogeography
Groffman, P. M., et al. 2006. Ecological thresholds: The 15:1–7.
key to successful environmental management or an Hobbs, R. J., et al. 2014. Managing the whole
important concept with no practical application? landscape: historical, hybrid and novel ecosystems.
Ecosystems 9:1–13. Frontiers in Ecology and the Environment 12:557–
Gunderson, L. H., S. S. Light, and C. S. Holling. 1995. 564.
Lessons from the Everglades. BioScience The Holling, C. S. 1973. Resilience and stability of
Science and Biodiversity Policy Supplement:S66– ecological systems. Annual Review of Ecology
S73. and Systematics 4:1–23.
Halpern, B. S., et al. 2008. A global map of human Holmgren, M., B. C. Lopez, J. R. Gutierrez, and F. A.
impact on marine ecosystems. Science 319:948–952. Squeo. 2006. Herbivory and plant growth rate
Hamann, A., D. R. Roberts, Q. E. Barber, C. Carroll, determine the success of El Nino Southern Oscil-
and S. E. Nielsen. 2015. Velocity of climate change lation-driven tree establishment in semiarid South
algorithms for guiding conservation and manage- America. Global Change Biology 12:2263–2271.
ment. Global Change Biology 21:997–1004. Holsinger, K. E. 1995. Conservation programs for

v www.esajournals.org 19 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

endangered plant species. Encyclopedia of Envi- approach to predicting plant-soil feedback. New
ronmental Biology 1:385–400. Phytologist 206:1–4.
Horwich, R. H., and J. Lyon. 2007. Community Kardol, P., and D. A. Wardle. 2010. How understand-
conservation: practitioners’ answer to critics. Oryx ing above-belowground linkages can assist resto-
41:376–385. ration ecology. Trends in Ecology & Evolution
Hughes, F. M. R., W. M. Adams, and P. A. Stroh. 2012. 25:670–679.
When is open-endedness desirable in restoration Kareiva, P., H. Tallis, T. H. Ricketts, G. C. Daily, and S.
projects? Restoration Ecology 20:291–295. Polasky, editors. 2011. Natural capital: theory and
Hunter, E. A., J. P. Gibbs, L. J. Cayot, and W. Tapia. practice of mapping ecosystem services. Oxford
2013. Equivalency of Galapagos giant tortoises University Press, Oxford, UK.
used as ecological replacement species to restore Ke, P.-J., T. Miki, and T.-S. Ding. 2015. The soil
ecosystem functions. Conservation Biology 27:701– microbial community predicts the importance of
709. plant traits in plant-soil feedback. New Phytologist
Jacobs, D. F., H. J. Dalgleish, and C. D. Nelson. 2013. A 206:329–341.
conceptual framework for restoration of threatened Knight, A. T., S. Sarkar, R. J. Smith, N. Strange, and
plants: the effective model of American chestnut K. A. Wilson. 2011. Engage the hodgepodge:
(Castanea dentata) reintroduction. New Phytologist management factors are essential when prioritizing
197:378–393. areas for restoration and conservation action.
James, J. J., R. L. Sheley, T. Erickson, K. S. Rollins, M. H. Diversity and Distributions 17:1234–1238.
Taylor, and K. W. Dixon. 2013. A systems approach Knight, R. L., and S. Riedel, editors. 2002. Aldo
to restoring degraded drylands. Journal of Applied Leopold and the ecological conscience. Oxford
Ecology 50:730–739. University Press, Oxford, UK.
James, J. J., T. J. Svejcar, and M. J. Rinella. 2011. Koch, J. M., J. Richardson, and B. B. Lamont. 2004.
Demographic processes limiting seedling recruit- Grazing by kangaroos limits the establishment of
ment in arid grassland restoration. Journal of the grass trees Xanthorrhoea gracilis and X. preissii in
Applied Ecology 48:961–969. restored bauxite mines in eucalypt forest of
Januchowski-Hartley, S. R., P. B. McIntyre, M. Diebel, southwestern Australia. Restoration Ecology
P. J. Doran, D. M. Infante, C. Joseph, and J. D. 12:297–305.
Allan. 2013. Restoring aquatic ecosystem connec- Kondoh, M. 2008. Building trophic modules into a
tivity requires expanding inventories of both dams persistent food web. Proceedings of the National
and road crossings. Frontiers in Ecology and the Academy of Sciences USA 105:16631–16635.
Environment 11:211–217. Kowarik, I. 2011. Novel urban ecosystems, biodiversi-
Jarchow, M., and M. Liebman. 2011. Maintaining ty, and conservation. Environmental Pollution
multifunctionality as landscapes provide ecosys- 159:1974–1983.
tem services. Frontiers in Ecology and the Envi- Kramer, U. 2010. Metal hyperaccumulation in plants.
ronment 9:262. Annual Review of Plant Biology 61:517–534.
Jellinek, S., L. Rumpff, D. A. Driscoll, K. M. Parris, and Kremen, C., et al. 2007. Pollination and other ecosys-
B. A. Wintle. 2014. Modelling the benefits of habitat tem services produced by mobile organisms: a
restoration in socio-ecological systems. Biological conceptual framework for the effects of land-use
Conservation 169:60–67. change. Ecology Letters 10:299–314.
Jonson, J. 2010. Ecological restoration of cleared Laliberté, E., et al. 2010. Land-use intensification
agricultural land in Gondwana Link: lifting the reduces functional redundancy and response di-
bar at ‘Peniup.’ Ecological Management and versity in plant communities. Ecology Letters
Restoration 11:16–26. 13:76–86.
Jorgensen, D., C. Nilsson, A. R. Hof, E. M. Hasselquist, Larson, B. M. H. In press. New wine and old
S. Baker, F. S. Chapin III, K. Eckerberg, J. Hjalten, L. wineskins? Novel ecosystems and conceptual
Polvi, and L. A. Meyerson. 2014. Policy language in change. Nature and Culture.
restoration ecology. Restoration Ecology 22:1–4. Larson, J. E., R. L. Sheley, S. P. Hardegree, P. S.
Kardol, P., T. M. Bezemer, and W. H. van der Putten. Doescher, and J. J. James. 2015. Seed and seedling
2006. Temporal variation in plant-soil feedback traits affecting critical life stage transitions and
controls succession. Ecology Letters 9:1080–1088. recruitment outcomes in dryland grasses. Journal
Kardol, P., T. M. Bezemer, and W. H. van der Putten. of Applied Ecology 52:199–209.
2009. Soil organism and plant introductions in Laughlin, D. C. 2014. Applying trait-based models to
restoration of species-rich grassland communities. achieve functional targets for theory-driven eco-
Restoration Ecology 17:258–269. logical restoration. Ecology Letters 17:771–784.
Kardol, P., G. F. Veen, F. P. Teste, and M. P. Perring. Lavorel, S., and K. Grigulis. 2012. How fundamental
2015. Peeking into the black box: a trait-based plant functional trait relationships scale-up to

v www.esajournals.org 20 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

trade-offs and synergies in ecosystem services. Martin, L. J., et al. 2014. Conservation opportunities
Journal of Ecology 100:128–140. across the world’s anthromes. Diversity and Dis-
Lavorel, S., J. Storkey, R. D. Bardgett, F. de Bello, M. P. tributions 20:745–755.
Berg, X. Le Roux, M. Moretti, C. Mulder, R. J. Martyn, A., D. Merritt, and S. Turner. 2009. Seed
Pakeman, S. Dı́az, and R. Harrington. 2013. A novel banking. Pages 63–86 in C. A. Offord and P. F.
framework for linking functional diversity of plants Meagher, editors. Plant germplasm conservation in
with other trophic levels for the quantification of Australia: strategies and guidelines for developing,
ecosystem services. Journal of Vegetation Science managing and utilising ex situ collections. Austra-
24:942–948. lian Network for Plant Conservation, Canberra,
Lawton, J. H. 1996. Corncrake pie and prediction in ACT, Australia.
ecology. Oikos 76:3–4. Matthews, A., et al. 2013. The success of GPS collar
Leger, E. A. 2008. The adaptive value of remnant deployments on mammals in Australia. Australian
native plants in invaded communities: an example Mammalogy 35:65–83.
from the Great Basin. Ecological Applications McCauley, D. J., M. L. Pinsky, S. R. Palumbi, J. A. Estes,
18:1226–1235. F. H. Joyce, and R. R. Warner. 2015. Marine
Leopold, A. 1949. A Sand County almanac: and defaunation: Animal loss in the global ocean.
sketches here and there. Oxford University Press, Science 347:1255641.
Oxford, UK. McConnachie, M. M., R. M. Cowling, B. W. van
Lester, R. E., P. G. Close, J. L. Barton, A. J. Pope, and Wilgen, and D. A. McConnachie. 2012. Evaluating
S. C. Brown. 2014. Predicting the likely response of the cost-effectiveness of invasive alien plant clear-
data-poor ecosystems to climate change using ing: a case study from South Africa. Biological
space-for-time substitution across domains. Global Conservation 155:128–135.
Change Biology 20:3471–3481. McEwan, R. W., J. M. Dyer, and N. Pederson. 2011.
Levin, S. A. 1998. Ecosystems and the biosphere as Multiple interacting ecosystem drivers: toward an
complex adaptive systems. Ecosystems 1:431–436. encompassing hypothesis of oak forest dynamics
Lindenmayer, D., et al. 2008. A checklist for ecological across eastern North America. Ecography 34:244–
management of landscapes for conservation. Ecol- 256.
ogy Letters 11:78–91. McRae, B. H., S. A. Hall, P. Beier, and D. M. Theobald.
Lomov, B., D. A. Keith, and D. F. Hochuli. 2010. 2012. Where to restore ecological connectivity?
Pollination and plant reproductive success in Detecting barriers and quantifying restoration
restored urban landscapes dominated by a perva- benefits. PLoS ONE 7:e52604.
sive exotic pollinator. Landscape and Urban Plan- Menz, M. H., K. W. Dixon, and R. J. Hobbs. 2013.
ning 96:232–239. Hurdles and opportunities for landscape-scale
Mace, G. M. 2014. Whose conservation? Science restoration. Science 339:526–527.
345:1558–1560. Menz, M. H., R. D. Phillips, R. Winfree, C. Kremen,
Mace, G. M., K. Norris, and A. H. Fitter. 2012. M. A. Aizen, S. D. Johnson, and K. W. Dixon. 2011.
Biodiversity and ecosystem services: a multilayered Reconnecting plants and pollinators: challenges in
relationship. Trends in Ecology & Evolution 27:19– the restoration of pollination mutualisms. Trends in
26. Plant Science 16:4–12.
Madsen, M. D., K. W. Davies, D. L. Mummey, and T. J. Merritt, D. J., and K. W. Dixon. 2011. Restoration
Svejcar. 2014. Improving restoration of exotic seedbanks—a matter of scale. Science 332:424–425.
annual grass-invaded rangelands through activat- Merritt, D. J., S. R. Turner, S. Clarke, and K. W. Dixon.
ed carbon seed enhancement technologies. Range- 2007. Seed dormancy and germination stimulation
land Ecology and Management 67:61–67. syndromes for Australian temperate species. Aus-
Madsen, M. D., K. W. Davies, C. J. Williams, and T. J. tralian Journal of Botany 55:336–344.
Svejcar. 2012. Agglomerating seeds to enhance Michener, W. K., S. Allard, A. Budden, R. B. Cook, K.
native seedling emergence and growth. Journal of Douglass, M. Frame, S. Kelling, R. Koskela, C.
Applied Ecology 49:431–438. Tenopir, and D. A. Vieglais. 2012. Participatory
Majer, J. D., K. E. C. Brennan, and M. L. Moir. 2007. design of DataONE—enabling cyberinfrastructure
Invertebrates and the restoration of a forest for the biological and environmental sciences
ecosystem: 30 years of research following bauxite Ecological Informatics 11:5–15.
mining in Western Australia. Restoration Ecology Middleton, E. L., and J. D. Bever. 2012. Inoculation
15:s104–s115. with a native soil community advances succession
Marrs, R. H. 1993. Soil fertility and nature conservation in a grassland restoration. Restoration Ecology
in Europe: theoretical considerations and practical 20:218–226.
management solutions. Advances in Ecological Mijangos, J. L., C. Pacioni, P. B. S. Spencer, and M. D.
Research 24:241–300. Craig. 2015. Contribution of genetics to ecological

v www.esajournals.org 21 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

restoration. Molecular Ecology 24:22–37. D. P. C. Peters. 2015. Connectivity in dryland

Miller, J. R., and R. J. Hobbs. 2007. Habitat restora- landscapes: shifting concepts of spatial interactions.
tion—Do we know what we’re doing? Restoration Frontiers in Ecology and the Environment 13:20–
Ecology 15:382–390. 27.
Minteer, B. 2014. Is it right to reverse extinction? Ostrom, E. 2009. A general framework for analyzing
Nature 509:261. sustainability of social-ecological systems. Science
Mitchell, M., M. Lockwood, S. A. Moore, and S. 325:419–422.
Clement. 2014. Incorporating governance influenc- Padilla, F. M., and F. I. Pugnaire. 2006. The role of
es into social-ecological system models: a case nurse plants in the restoration of degraded
study involving biodiversity conservation. Journal environments. Frontiers in Ecology and the Envi-
of Environmental Planning and Management. doi: ronment 4:196–202.
10.1080/09640568.2014.967387 Palmer, M. A., R. F. Ambrose, and N. L. Poff. 1997.
Montoya, D., L. Rogers, and J. Memmott. 2012. Ecological theory and community restoration ecol-
Emerging perspectives in the restoration of biodi- ogy. Restoration Ecology 5:291–300.
versity-based ecosystem services. Trends in Ecolo- Peralta, A. L., D. Stuart, A. D. Kent, and J. T. Lennon.
gy & Evolution 27:666–672. 2014. A social-ecological framework for ‘‘micro-
Moretti, M., F. de Bello, S. Ibanez, S. Fontana, G. B. managing’’ microbial services. Frontiers in Ecology
Pezzatti, F. Dziock, C. Rixen, and S. Lavorel. 2013. and the Environment 12:524–531.
Linking traits between plants and invertebrate Perring, M. P., G. Edwards, and C. de Mazancourt.
herbivores to track functional effects of land-use 2009. Removing phosphorus from ecosystems
changes. Journal of Vegetation Science 24:949–962. through nitrogen fertilization and cutting with
Morse, N. B., P. A. Pellissier, E. N. Cianciola, R. L. removal of biomass. Ecosystems 12:1130–1144.
Brereton, M. M. Sullivan, N. K. Shonka, T. B. Perring, M. P., R. J. Standish, and R. J. Hobbs. 2013.
Wheeler, and W. H. McDowell. 2014. Novel Incorporating novelty and novel ecosystems into
ecosystems in the Anthropocene: a revision of the restoration planning and practice in the 21st
novel ecosystem concept for pragmatic applica- century. Ecological Processes 2:18.
tions. Ecology and Society 19:12. Perring, M. P., R. J. Standish, K. B. Hulvey, L. Lach,
Murcia, C., J. Aronson, G. H. Kattan, D. Moreno- T. K. Morald, R. Parsons, R. K. Didham, and R. J.
Mateos, K. Dixon, and D. Simberloff. 2014. A Hobbs. 2012. The Ridgefield Multiple Ecosystem
critique of the ‘novel ecosystem’ concept. Trends in Services Experiment: Can restoration of former
Ecology & Evolution 29:548–553. agricultural land achieve multiple outcomes? Ag-
Naiman, R. J. 2013. Socio-ecological complexity and riculture, Ecosystems and Environment 163:14–27.
the restoration of river ecosystems. Inland Waters Petursdottir, T., A. L. Aradottir, and K. Benediktsson.
3:391–410. 2013. An evaluation of the short-term progress of
Nelleman, C., and E. Corcoran. 2010. Dead planet, restoration combining ecological assessment and
living planet—biodiversity and ecosystem restora- public perception. Restoration Ecology 21:75–85.
tion for sustainable development. A Rapid Re- Pineiro, J., F. T. Maestre, L. Bartoleme, and A.
sponse Assessment. United Nations Environment Valdecantos. 2013. Ecotechnology as a tool for
Program, GRID-Arendal, Norway. restoring degraded drylands: a meta-analysis of
Nelson, E., et al. 2009. Modeling multiple ecosystem field experiments. Ecological Engineering 61:133–
services, biodiversity conservation, commodity 144.
production, and tradeoffs at landscape scales. Poff, N. L. 2014. Rivers of the Anthropocene? Frontiers
Frontiers in Ecology and the Environment 7:4–11. in Ecology and the Environment 12:427.
Newsome, T. M., et al. 2015. Resolving the value of the Pollock, M. M., T. J. Beechie, J. M. Wheaton, C. E.
dingo in ecological restoration. Restoration Ecology Jordan, N. Bouwes, N. Weber, and C. Volk. 2014.
23:201–208. Using beaver dams to restore incised stream
Nielsen-Pincus, M., and C. Moseley. 2013. The eco- ecosystems. BioScience 64:279–290.
nomic and employment impacts of forest and Potschin, M. B., and R. H. Haines-Young. 2011.
watershed restoration. Restoration Ecology Ecosystem services: exploring a geographical per-
21:207–214. spective. Progress in Physical Geography 35:575–
Norgaard, R. B., G. Kallis, and M. Kiparsky. 2009. 594.
Collectively engaging complex socio-ecological Price, J. N., and M. Pärtel. 2013. Can limiting similarity
systems: re-envisioning science, governance, and increase invasion resistance? A meta-analysis of
the California Delta. Environmental Science and experimental studies. Oikos 122:649–656.
Policy 12:644–652. Prober, S. M., R. J. Standish, and G. Wiehl. 2011. After
Okin, G. S., M. M.-d. l. Heras, P. M. Saco, H. L. Throop, the fence: vegetation and topsoil condition in
E. R. Vivoni, A. J. Parsons, J. Wainwright, and grazed, fenced and benchmark eucalypt wood-

v www.esajournals.org 22 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

lands of fragmented agricultural landscapes. Aus- effective ecosystem engineers? Restoration Ecology
tralian Journal of Botany 59:369–381. 21:336–343.
Probert, R. J., J. Adams, J. Coneybeer, A. D. Crawford, Sandom, C. J., J. Hughes, and D. W. Macdonald. 2013b.
and F. Hay. 2007. Seed quality for conservation is Rooting for rewilding: quantifying wild boar’s Sus
critically affected by pre-storage factors. Australian scrofa rooting rate in the Scottish Highlands.
Journal of Botany 55:326–335. Restoration Ecology 21:329–335.
Pullin, A. S., and T. M. Knight. 2009. Doing more good Schindler, S., et al. 2014. Multifunctionality of flood-
than harm: building an evidence-base for conser- plain landscapes: relating management options to
vation and environmental management. Biological ecosystem services. Landscape Ecology 29:229–244.
Conservation 142:931–934. Schoen, D. J., and A. H. D. Brown. 2001. The
Pywell, R. F., J. M. Bullock, K. J. Walker, S. J. Coulson, conservation of wild plant species in seed banks.
S. J. Gregory, and M. J. Stevenson. 2004. Facilitating BioScience 51:960–966.
grassland diversification using the hemiparasitic Seddon, P. J., C. J. Griffiths, P. S. Soorae, and D. P.
plant Rhinanthus minor. Journal of Applied Ecology Armstrong. 2014. Reversing defaunation: restoring
41:880–887. species in a changing world. Science 345:406–412.
Reed, M. S. 2008. Stakeholder participation for SERI. 2004. The SER International primer on ecological
environmental management: a literature review. restoration. Society for Ecological Restoration
Biological Conservation 141:2417–2431. International, Tucson, Arizona, USA.
Requena, N., E. Perez-Solis, C. Azcon-Aguilar, P. Shackelford, N., R. J. Hobbs, J. M. Burgar, T. E.
Jeffries, and J.-M. Barea. 2001. Management of Erickson, J. B. Fontaine, E. Laliberté, C. E. Ramalho,
indigenous plant-microbe symbioses aids restora- M. P. Perring, and R. J. Standish. 2013. Primed for
tion of desertified ecosystems. Applied and Envi- change: developing ecological restoration for the
ronmental Microbiology 67:495–498. 21st Century. Restoration Ecology 21:297–304.
Rey-Benayas, J. M., A. C. Newton, A. Diaz, and J. M. Sherkow, J. S., and H. T. Greely. 2013. What if
Bullock. 2009. Enhancement of biodiversity and extinction is not forever? Science 340:32–33.
ecosystem services by ecological restoration: a Siles, G., P. J. Rey, J. M. Alcantara, and J. M. Ramirez.
meta-analysis. Science 325:1121–1124. 2008. Assessing the long-term contribution of nurse
Reyes, J. E. 2011. Public participation and socioeco- plants to restoration of Mediterranean forests
logical resilience. Pages 79–92 in D. Egan, E. E. through Markovian models. Journal of Applied
Hjerpe, and J. Abrams, editors. Human dimensions Ecology 45:1790–1798.
of ecological restoration: integrating science, nature Simard, S. W., and D. M. Durall. 2004. Mycorrhizal
and culture. Island Press, Washington, D.C., USA. networks: a review of their extent, function, and
Ripple, W. J., and R. L. Beschta. 2007. Restoring importance. Canadian Journal of Botany 82:1140–
Yellowstone’s aspen with wolves. Biological Con- 1165.
servation 138:514–519. Standish, R. J. et al. 2014. Resilience in ecology:
Ripple, W. J., et al. 2014. Status and ecological effects of Abstraction, distraction, or where the action is?
the world’s largest carnivores. Science 343:1241484. Biological Conservation 177:43–51.
Roever, C. L., R. J. van Aarde, and K. Leggett. 2013. Steffen, W., J. Grinevald, P. Crutzen, and J. McNeill.
Functional connectivity within conservation net- 2011. The Anthropocene: conceptual and historical
works: delineating corridors for African elephants. perspectives. Philosophical Transactions of the
Biological Conservation 157:128–135. Royal Society A 369:842–867.
Rogers, A., et al. 2015. Anticipative management for Steffen, W., R. A. Sanderson, P. D. Tyson, J. Jager, P. A.
coral reef ecosystem services in the 21st century. Matson, B. Moore III, F. Oldfield, K. Richardson,
Global Change Biology 21:504–514. H. J. Schellnhuber, B. L. Turner, and R. J. Wasson.
Rounsevell, M. D. A., D. T. Robinson, and D. Murray- 2005. Global change and the earth system: a planet
Rust. 2012. From actors to agents in socio-ecolog- under pressure. Springer-Verlag, Berlin, Germany.
ical systems models. Philosophical Transactions of Steffen, W., et al. 2015. Planetary boundaries: guiding
the Royal Society B 367:259–269. human development on a changing planet. Science
Ruiz-Jaen, M. C., and T. M. Aide. 2005. Restoration 347:1259855.
success: How is it being measured? Restoration St Jack, D., D. C. Hesterman, and A. L. Guzzomi. 2013.
Ecology 13:569–577. Precision metering of Santalum spicatum (Australian
Samhouri, J. F., P. S. Levin, and C. H. Ainsworth. 2010. sandalwood) seeds. Biosystems Engineering
Identifying thresholds for ecosystem-based man- 115:171–183.
agement. PLoS ONE 5:e8907. St John, F. A. V., A. M. Keane, J. P. G. Jones, and E. J.
Sandom, C. J., J. Hughes, and D. W. Macdonald. 2013a. Milner-Gulland. 2014. Robust study design is as
Rewilding the Scottish Highlands: Do wild boar, important on the social as it is on the ecological
Sus scrofa, use a suitable foraging strategy to be side of applied ecological research. Journal of

v www.esajournals.org 23 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

Applied Ecology 51:1479–1485. to revegetate: a quantitative method for scheduling

Sudduth, E. B., B. A. Hassett, P. Cada, and E. S. landscape reconstruction. Ecological Applications
Bernhardt. 2011. Testing the field of dreams 19:817–828.
hypothesis: functional responses to urbanization Tilman, D. 1982. Resource competition and community
and restoration in stream ecosystems. Ecological structure. First edition. Princeton University Press,
Applications 21:1972–1988. Princeton, New Jersey, USA.
Suding, K., et al. 2015. Committing to ecological Torrubia, S., B. H. McRae, J. J. Lawler, S. A. Hall, M.
restoration. Science 348:638–640. Halabisky, J. Langdon, and M. Case. 2014. Getting
Suding, K. N. 2011. Towards an era of restoration in the most connectivity per conservation dollar.
ecology: successes, failures, and opportunities Frontiers in Ecology and the Environment 12:491–
ahead. Annual Review of Ecology, Evolution and 497.
Systematics 42:465–487. Trueman, M., R. J. Standish, and R. J. Hobbs. 2014.
Suding, K. N., K. L. Gross, and G. R. Houseman. 2004. Identifying management options for modified
Alternative states and positive feedbacks in resto- vegetation: application of the novel ecosystems
ration ecology. Trends in Ecology & Evolution framework to a case study in the Galapagos
19:46–53. Islands. Biological Conservation 172:37–48.
Suding, K. N., and R. J. Hobbs. 2009. Threshold models Tucker, N. I. J., and T. M. Murphy. 1997. The effects of
in restoration and conservation: a developing ecological rehabilitation on vegetation recruitment:
framework. Trends in Ecology & Evolution some observations from the Wet Tropics of North
24:271–279. Queensland. Forest Ecology and Management
Suding, K. N., S. Lavorel, F. S. Chapin III, J. H. C. 99:133–152.
Cornelissen, S. Diaz, E. Garnier, D. Goldberg, D. U. Turner, II, B. L., et al. 2003. Illustrating the coupled
Hooper, S. T. Jackson, and M. L. Navass. 2008. human-environment system for vulnerability anal-
Scaling environmental change through the com- ysis: Three case studies. Proceedings of the
munity-level: a trait-based response-and-effect National Academy of Sciences USA 100:8080–8085.
framework for plants. Global Change Biology Turner, S. R., B. Pearce, D. P. Rokich, R. R. Dunn, D. J.
14:1125–1140. Merritt, J. D. Majer, and K. W. Dixon. 2006.
Sutherland, W. J., A. S. Pullin, P. M. Dolman, and T. M. Influence of polymer seed coatings, soil raking,
Knight. 2004. The need for evidence-based conser- and time of sowing on seedling performance in
vation. Trends in Ecology & Evolution 19:305–308. post-mining restoration. Restoration Ecology
Sutherland, W. J., et al. 2014. Solution scanning as a 14:267–277.
key policy tool: identifying management interven- Turner, S. R., K. J. Steadman, S. Vlahos, J. M. Koch, and
tions to help maintain and enhance regulating K. W. Dixon. 2013. Seed treatment optimizes
ecosystem services. Ecology and Society 19:3. benefits of seed bank storage for restoration-ready
Swetnam, T. W., C. D. Allen, and J. L. Betancourt. 1999. seeds: the feasibility of prestorage dormancy
Applied historical ecology: using the past to alleviation for mine-site revegetation. Restoration
manage for the future. Ecological Applications Ecology 21:186–192.
9:1189–1206. Tylianakis, J. M., R. K. Didham, J. Bascompte, and
Tambosi, L. R., A. C. Martensen, M. C. Ribeiro, and J. P. D. A. Wardle. 2008. Global change and species
Metzger. 2014. A framework to optimize biodiver- interactions in terrestrial ecosystems. Ecology
sity restoration efforts based on habitat amount Letters 11:1351–1363.
and landscape connectivity. Restoration Ecology van der Putten, W. H., et al. 2013. Plant–soil feedbacks:
22:169–177. the past, the present and future challenges. Journal
Terborgh, J., and J. A. Estes, editors. 2010. Trophic of Ecology 101:265–276.
cascades: predators, prey and the changing dy- van Marwijk, R. B. M., B. H. M. Elands, J. K. Kampen,
namics of nature. Island Press, Washington, D.C., S. Terlouw, D. G. Pitt, and P. Opdam. 2012. Public
USA. perceptions of the attractiveness of restored nature.
Teste, F. P., S. W. Simard, D. M. Durall, R. D. Guy, Restoration Ecology 20:773–780.
M. D. Jones, and A. L. Schoonmaker. 2009. Access van Noordwijk, M., B. Leimona, R. Jindal, G. B.
to mycorrhizal networks and roots of trees: Villamor, M. Vardhan, S. Namirembe, D. Catacu-
importance for seedling survival and resource tan, J. Kerr, P. A. Minang, and T. P. Tomich. 2012.
transfer. Ecology 90:2808–2822. Payments for environmental services: Evolution
Thomas, R. 2009. Regent honeyeater habitat restora- toward efficient and fair incentives for multifunc-
tion project Lurg Hills, Victoria. Ecological Man- tional landscapes. Annual Review of Environment
agement and Restoration 10:84–97. and Resources 37:389–420.
Thomson, J. R., A. J. Moilanen, P. A. Vesk, A. F. Verheyen, K., et al. In press. Contributions of a global
Bennett, and R. MacNally. 2009. Where and when network of tree diversity experiments to sustain-

v www.esajournals.org 24 August 2015 v Volume 6(8) v Article 131

ESA CENTENNIAL PAPER PERRING ET AL.

able forest plantations. AMBIO. nated soils. Chemosphere 50:775–780.

Vesk, P. A., R. Nolan, J. R. Thomson, J. W. Dorrough, Woodworth, P. 2013. Our once and future planet:
and R. MacNally. 2008. Time lags in provision of restoring the world in the climate change century.
habitat resources through revegetation. Biological University of Chicago Press, Chicago, Illinois, USA.
Conservation 141:174–186. Wortley, L., J.-M. Hero, and M. Howes. 2013. Evalu-
Vitousek, P. M., H. A. Mooney, J. Lubchenco, and J. M. ating ecological restoration success: a review of the
Melillo. 1997. Human domination of Earth’s eco- literature. Restoration Ecology 21:537–543.
systems. Science 277:494–499. Yin, R., and G. Yin. 2010. China’s primary programs of
Wardle, D. A., R. D. Bardgett, J. N. Klironomos, H. terrestrial ecosystem restoration: initiation, imple-
Setala, W. H. van der Putten, and D. H. Wall. 2004. mentation, and challenges. Environmental Man-
Ecological linkages between aboveground and agement 45:429–441.
belowground biota. Science 304:1629–1633. Young, T. P. 2000. Restoration ecology and conserva-
Watkinson, A. R., R. P. Freckleton, R. A. Robinson, and tion biology. Biological Conservation 92:73–83.
W. J. Sutherland. 2000. Predictions of biodiversity Young, T. P., D. A. Petersen, and J. J. Clary. 2005. The
response to genetically modified herbicide-tolerant ecology of restoration: historical links, emerging
crops. Science 289:1554–1557. issues and unexplored realms. Ecology Letters
Webb, C. T., J. A. Hoeting, G. M. Ames, M. I. Pyne, and 8:662–673.
N. L. Poff. 2010. A structured and dynamic Zahawi, R. A., K. D. Holl, R. J. Cole, and J. L. Reid.
framework to advance traits-based theory and 2013. Testing applied nucleation as a strategy to
prediction in ecology. Ecology Letters 13:267–283. facilitate tropical forest recovery. Journal of Ap-
Whisenant, S. G. 1999. Repairing damaged wildlands: plied Ecology 50:88–96.
a process-oriented, landscape-scale approach. Zedler, J. B. 2007. Success: An unclear, subjective
Cambridge University Press, Cambridge, UK. descriptor of restoration outcomes. Ecological
Wiens, J. A., and R. J. Hobbs. 2015. Integrating Restoration 25:162–168.
conservation and restoration in a changing world. Zedler, J. B., J. M. Doherty, and N. A. Miller. 2012.
BioScience 65:302–312. Shifting restoration policy to address landscape
Wilson, K. A., M. Lulow, J. Burger, Y.-C. Fang, C. change, novel ecosystems, and monitoring. Ecolo-
Andersen, D. Olson, M. O’Connell, and M. F. gy and Society 17:36.
McBride. 2011. Optimal restoration: accounting for Zimmerman, N. E., J. Izard, C. Klatt, J. Zhou, and E.
space, time and uncertainty. Journal of Applied Aronson. 2014. The unseen world: environmental
Ecology 48:715–725. microbial sequencing and identification methods
Wong, M. H. 2003. Ecological restoration of mine for ecologists. Frontiers in Ecology and the Envi-
degraded soils, with emphasis on metal contami- ronment 12:224–231.

v www.esajournals.org 25 August 2015 v Volume 6(8) v Article 131