You are on page 1of 7

OPINION ARTICLE

Tertiary succession: a new concept to help


vegetation restoration
Gillian L. Rapson1,2

Restoration is the human activity of manipulating vegetation with the aim of accelerating attainment of stable vegetation. But
current procedures seem to arrest succession instead. A comparison of primary and secondary successions with restoration
activities suggests there is little overlap in these concepts. Thinking of the process of restoration as a tertiary succession helps
highlight managerial options which may improve success, especially by addressing environmental and biological legacies.
Key words: biological legacy, dispersal, disturbance, ecosystem property, function, traits

concept (Gleason 1927; Clements 1928), still debated today


Implications for Practice
(Walker et al. 2007; Pickett et al. 2009).
• Arrested successions, such as created by many restoration Primary succession is the natural process by which a climax
projects, need to be accelerated toward normal natural vegetation is ultimately emplaced on new or denuded land,
functioning. where no species were originally present (Clements 1916).
• Tertiary succession is a concept differentiating restoration Never precisely defined, it is typified by the sequence of
activities from natural processes. vegetation changes following glacial retreat at Glacier Bay,
• Tertiary succession should change manager’s expecta- Alaska, U.S.A., first reported by John Muir in 1879, and studied
tions of restorations’ progress. continuously since (e.g., Cooper 1923; Crocker & Major 1955;
• This concept should facilitating ongoing intervention to Buma et al. 2017). Secondary succession is the natural process
improve restorations’ prospects. on a site which has been partially, or even completely devege-
tated by a disturbance event. Though much of the above-ground
biomass is removed, some remnants may remain, along with
carbon and nutrients in coarse woody debris (Carmona
et al. 2002). The soil can be largely intact, with retention of
below-ground tissues, seeds, fungi, and microbes and even
Introduction invertebrates (Wardle & Peltzer 2007), all facilitating secondary
Vegetation restoration, particularly of wetlands and forests, is a succession. By contrast, in a primary succession physical space
crucial strategy in modern humans’ attempts to mitigate the and light are the only resources certain to be available to incom-
impacts of anthropic activities and anthropogenic climate ing plant species. Despite the logic of the terminology, second-
change. Most restoration activities take place on degraded land, ary succession is not a later stage of primary succession, and it
damaged by logging, mining, fire, floods, landslides, or aban- is possible to have multiple secondary successions commencing
doned after agricultural conversion (Prach & Walker 2020). on the same site, though only after an initial primary succession
Worldwide, 0.9 billion hectares are currently available for resto- and equally multiple disturbances.
ration plantings, which could store 205 gigatonnes of carbon
(Bastin et al. 2019). But what successional logic drives vegeta-
The Links Between Vegetation Succession and
tion restoration?
Restoration
Hobbs et al. (2007) say: “Succession has been, and still mostly
Vegetation Succession remains, a conceptual construct that aids in the understanding
The concept of succession was originated by Eugenius
Warming (1895), the Danish founder of ecology, his publication Author contributions: GLP conceived and wrote the paper.
translated into English as “Oecology of Plants – an introduction 1
Ecology, School of Natural Sciences, Massey University, Palmerston North,
to the study of plant-communities” (Warming & Vahl 1909). New Zealand
2
Succession is the gradual and putatively orderly sequence of Address correspondence to G. L. Rapson, email g.rapson@massey.ac.nz
vegetation change through natural processes to reach a stable
or climax vegetation (Clements 1916). Americans Frederic © 2022 Society for Ecological Restoration.
Clements and Henry Gleason subsequently developed the doi: 10.1111/rec.13683

January 2023 Restoration Ecology Vol. 31, No. 1, e13683 1 of 7


1526100x, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/rec.13683 by Luiz Moraes - CAPES , Wiley Online Library on [04/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Tertiary succession in restoration

of how systems change over time. Restoration is primarily a (Phillips 1934), “stuck” (Hobbs et al. 2007), or “stalled”
practical activity that seeks to achieve outcomes in the most (Walker & del Moral 2008).
effective and efficient way possible” (Fig. 1). Thirty-five years There are many causes for this, such as presence, perhaps
ago, Bradshaw (1987) declared restoration an acid test for our overwhelmingly, of competitive aliens (Holl 2020; Lami
understanding of succession. And attempts to link the two have et al. 2021). Prach and Walker (2020) estimated aliens influence
been many (Clements 1949; Luken 1990; Walker et al. 2007; about a quarter of primary successions, though these are less
Pickett et al. 2009), though not necessarily successful susceptible to aliens than secondary successions, because less
(Luken 1990; Holl 2020; Rapson 2021). exposed to anthropic disturbance. The presence of herbivores
Mostly restorationists do not specify how they intend to inter- can hinder succession (Suzuki et al. 2021), especially if non-
act with natural successional processes. If they thought about it, native (Burns et al. 2012). Further, widespread agriculturaliza-
they might claim to be implementing a secondary succession, tion causes a paucity of naturally dispersing seeds to furnish
preferably an “accelerated” one. The term “accelerated succes- later successional stages (McAlpine et al. 2016), perhaps in par-
sion” was first published by Robinson (1942), though its con- allel with a paucity of dispersers (Kelly et al. 2010).
temporaneous frequency of use suggests it was already widely
established in practice. But what is the logic behind accelerating
a natural succession? Comparison Between Successions and Restoration
Generally restoration projects involve planting seedlings to Failure to accelerate succession suggests our thinking is arrested
accelerate establishment over the dispersal barrier and past the by the belief that restoration actually triggers such a secondary
very competitive phases of germination and recruitment, where succession in the first place. A tabulation of the characteristics
mortality can be very high (Fig. 2). Once canopy closure is in primary and secondary successions with vegetation restora-
achieved, the restoration is declared a success (Lockwood & tion suggests there is very little support for such thinking
Pimm 1999; Hobbs et al. 2007), and natural processes are left (Table 1).
to (hopefully) continue the sere. But timely success is not always Only one similarity in Ecological Situation (Table 1) exists
achieved, with restorations instead becoming “arrested” between secondary succession and vegetation restoration. (The

Figure 1. Volunteers plant native trees into a sward of exotic grasses and shrub weeds, created by felling a pine plantation for construction of a cycleway viaduct;
Keeble’s Farm, Massey University, Manawat u, New Zealand.

2 of 7 Restoration Ecology January 2023


1526100x, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/rec.13683 by Luiz Moraes - CAPES , Wiley Online Library on [04/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Tertiary succession in restoration

Figure 2. Conical juvenile Dacrycarpus dacrydioides (Podocarpaceae) to 15 m on the toe of a scarp above the Mungatungaroa stream. This successful
restoration planting was initiated by Michael Greenwood in 1985; Keeble’s Farm.

previous presence of a primary succession is axiomatic, and so is may also contain contaminants (Cavani et al. 2016), amelio-
unscored). Young only for primary successions, landscape age ration of which has no corollary with natural successional
does present a match between secondary succession and restora- processes, even if an important part of reclamation activities.
tion. Historical anthropic disturbances are generally triggers for In a process driven by plants, biological legacies are very
restoration projects (Holl & Aide 2011), even though “[r]estora- important, but again secondary succession shows few matches
tion is a unique form of disturbance” itself (del Moral with restoration (Table 1). The vegetation being replaced may
et al. 2007). Prior to restoration actions, exogenous disturbances be dominated by aliens, particularly if on abandoned farmland,
often occur with high frequency, perhaps annually in the case of cropland or old-fields (Tognetti et al. 2010). Natural biomass
agriculture, a frequency greater than in most disturbed natural is initially low in both restoration and secondary succession,
systems, except perhaps sand-dunes (Villacís Lozada & Rap- the latter being initiated by disturbance events, which, defini-
son 2021). Time scale to recovery is slower in secondary succes- tionally, remove biomass (Grime 1979). Plant species’ diversity
sion (Prach et al. 2016), but hopefully accelerated for is also low initially, with aliens dominating in both richness and
restoration, though this is debatable (see above). A primary suc- cover (Boscutti et al. 2017; Lami et al. 2021). In restorations,
cession probably has one or more trajectories converging on the native species are routinely added, though often not in suffi-
site’s climax vegetation (Clements 1916; Phillips 1934), while ciently great diversity to mimic natural systems (Hughes
secondary succession seems more variable and trajectories et al. 2018). Restoration deliberately reduces dispersal con-
may even be divergent (del Moral et al. 2007). The sere in resto- straints (Nolan et al. 2021), while K-selected species (with poor
ration plantings is pre-determined, at least in theory (Holl 2020), dispersal due to a tradeoff to a seed size favoring establishment
though the outcome may be unpredictable and equally divergent in competitive conditions) normally dominate in secondary suc-
(Tognetti et al. 2010), perhaps a partial match with secondary cession (Opler et al. 1980). A large seedbank is similarly present
succession. in secondary succession and restoration, though in restorations,
In terms of environmental legacies of the site, there are it is probably comprised of alien or inappropriate species
probably no aspects of secondary succession which overlap (Bekker et al. 1997), severely limiting succession. Litter depths
with restoration, though evidence for this is generally lack- are especially low in restoration situations, often a consequence
ing. However, Walker and del Moral (2003) and Wardle of years of biomass removal through harvesting (Novara
and Peltzer (2007) suggest that restoration will have soils et al. 2015), comparable with neither succession. The rich,
low in nutrients and organics, high in phosphorus, and com- fungal-dominated community of a secondary succession is
pacted by vehicle passages. Anthropically modified soils probably depauperate in restorations, or skewed toward bacteria

January 2023 Restoration Ecology 3 of 7


1526100x, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/rec.13683 by Luiz Moraes - CAPES , Wiley Online Library on [04/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Tertiary succession in restoration

Table 1. Comparison of initial stages of secondary with tertiary succession, with alternative terms. For the latter pair, pink indicates a conflict and green a match,
with lighter shades for possible comparisons; “Successional driver” is not assessed. Primary succession is included for reference.

Types

4 of 7 Restoration Ecology January 2023


1526100x, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/rec.13683 by Luiz Moraes - CAPES , Wiley Online Library on [04/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Tertiary succession in restoration

and other microbes (Wardle & Peltzer 2007; Cavani et al. 2016). all groupings, but since the “Ecological situation” cannot logi-
Soil floras in restorations may be inappropriate for the inplanted cally be changed, the priority requirements clearly are under
species, lacking essential mycorrhizae or other symbionts “Environmental legacies,” since these relate to the past manage-
(Koziol & Bever 2017). Similarly resident and transient fauna ment of the site, and “Biological legacies,” since these represent
are likely inappropriate for the vegetation being restored, and the restoration actions plannable or being undertaken. “Ecosys-
perhaps aggressively herbivorous without providing seed dis- tem properties” are sensibly reserved for measures of success
persal services (Parker et al. 2006). (Ruiz-Jaen & Aide 2005). The common needs highlighted are
Considering ecosystem properties operating in the initial that soil condition be considered, more native biodiversity
stages of restorations and secondary successions (Table 1), included, use of duff (containing litter, seed, nutrients, microbes,
the biota is the dominant filter for both (Török et al. 2020). fungi, invertebrates, etc.) incorporated, functional groups
The filtration spectrum changes from facilitation to competition balanced, and herbivory, especially of aliens, managed.
in both situations. Hard to evaluate, competition is probably Experts have long been aware of these needs. For example,
more important in restoration plantings (Backhaus et al. 2021), del Moral et al. (2007) conclude that “restoration tactics should
due to resistance by residents, often alien (del Moral focus on site amelioration, improving establishment success,
et al. 2007), creating ecosystems impenetrable to natives. How- and protecting desirable species from herbivory and competition
ever the use of nurse species, even if alien, is actually facilitative during their development,” while Halassy et al. (2019), promot-
(Gomez-Aparicio et al. 2004). Functional traits are those ing more interactive interventions, say “targeting the dispersal
characteristics which affect the adaptability of species and environmental filters in parallel would improve restoration
(Bruelheide et al. 2018), general trends of which allow multiple outcomes.” But too often mangers trust to the “magic” of a
species to be assigned to guilds with similar operational strate- quick, natural fix, free and effort-less, once restoration has been
gies (Adams 1985). Differences in traits and even guilds initiated, not appreciating the need for what SER (2004) referred
between native and alien species can alter a community’s inva- to as “more post-installation aftercare.”
sibility (Mahaney et al. 2015; Abella & Chiquoine 2019), but “Tertiary succession” should be a helpful concept here in
are seldom intentionally manipulated under restoration (Ruiz- communications between managers, restorationists, and ecolo-
Jaen & Aide 2005). gists studying vegetation succession, highlighting the unique,
Of the 32 comparisons made in Table 1, only 7 (22%) show a anthropogenic problems a restoration project faces in becoming
close or weak match between secondary succession and restora- a self-propelling successional system, and directing research
tion. And the match with primary succession is even poorer needed to promote this.
(18%) with more decided mis-matches, though perhaps the seres
of novel ecosystems (Cole 2019) are closer to primary succes-
sion. Convincingly, restoration, even if successful, cannot be Acknowledgments
regarded as engaging a secondary succession. The same conclu- The author thanks Lars and Libby Walker for sharing amazing
sion applies to those activities related to restoration, such as mental and physical landscapes, and to Bastow Wilson for clar-
rehabilitation, where successful re-establishment of ecological ifying the Clements/Gleason debate. Referees generously gave
processes is valued over historical biotic integrity (SER 2004); useful feedback.
there only Ecosystem Properties (as per Table 1) matter. For rec-
lamation, which has the goal of being useful to humans, the
associated revegetation may entail few of the species historically
LITERATURE CITED
present and addition of above-ground biomass is the only crite-
Abella SR, Chiquoine LP (2019) The good with the bad: when ecological resto-
rion valued within Biological Legacies, while ecological engi-
ration facilitates native and non-native species. Restoration Ecology 27:
neering lacks even the successional goal of the addition of 343–351. https://doi.org/10.1111/rec.12874
biomass. Ecosystem creation engages with Environmental Leg- Adams J (1985) The definition and interpretation of guild structure in ecological
acies but may result in novel ecosystems with an unknown tra- communities. Journal of Animal Ecology 54:43–59. https://doi.org/10.
jectory rather than promoting a natural succession. 2307/4619
Backhaus L, Albert G, Cuchietti A, Jaimes Nino LM, Fahs N, Lisner A, et al.
(2021) Shift from trait convergence to divergence along old-field succes-
Conclusion sion. Journal of Vegetation Science 32:e12986. https://doi.org/10.1111/
jvs.12986
In common use by the 1900s (Shantz 1906), it is not clear why Bastin JF, Finegold Y, Garcia C, Mollicone D, Rezende M, Routh D, Zohner CM,
the original terminological choice was of “primary” and “sec- Crowther TW (2019) The global tree restoration potential. Science 365:
ondary” succession, when “initialising succession” and “regen- 76–79. https://doi.org/10.1126/science.aax0848
eration succession” would be more intuitive. But since we Bekker RM, Verweij GL, Smith RE, Reine R, Bakker JP, Schneider S (1997) Soil
humans entrench our ideas (Pickett et al. 2009; Rapson 2018), seed banks in European grasslands: does land use affect regeneration per-
spectives? Journal of Applied Ecology 34:1293–1310. https://doi.org/10.
we should stick to the same nomenclatural theory, and add “ter-
2307/2405239
tiary (3 ) succession” (meaning “restoration succession”) to our Boscutti F, Vianello A, Bozzato F, Casolo V (2017) Vegetation structure, species
vocabulary, specifically to help our restoration activities. This life span, and exotic status elucidate plant succession in a limestone quarry
terminology should focus managers on factors which can reclamation. Restoration Ecology 25:595–604. https://doi.org/10.1111/rec.
improve a project’s success. In Table 1, disparities occur under 12476

January 2023 Restoration Ecology 5 of 7


1526100x, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/rec.13683 by Luiz Moraes - CAPES , Wiley Online Library on [04/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Tertiary succession in restoration

Bradshaw AD (1987) Restoration: an acid test for ecology. Pages 23–29. In: recovery. Conservation Letters 11:e12419. https://doi.org/10.1111/conl.
Jordan WR III, Gilpin M, Aber JD (eds) Restoration ecology. Cambridge 12419
University Press, Cambridge, UK Kelly D, Ladley JJ, Robertson AW, Anderson SH, Wotton DM, Wiser SK (2010)
Bruelheide H, Dengler J, Purschke O, Lenoir J, Jiménez-Alfaro B, Mutualisms with the wreckage of an avifauna: the status of bird pollination
Hennekens SM, et al. (2018) Global trait–environment relationships of and fruit-dispersal in New Zealand. New Zealand Journal of Ecology 34:
plant communities. Nature Ecology & Evolution 2:1906–1917. https:// 66–85
doi.org/10.1038/s41559-018-0699-8 Koziol L, Bever JD (2017) The missing link in grassland restoration: arbuscular
Buma B, Bisbing S, Krapek J, Wright G (2017) A foundation of ecology redis- mycorrhizal fungi inoculation increases plant diversity and accelerates suc-
covered: 100 years of succession on the William S. Cooper plots in Glacier cession. Journal of Applied Ecology 54:1301–1309. https://doi.org/10.
Bay, Alaska. Ecology 98:1513–1523. https://doi.org/10.1002/ecy.1848 1111/1365-2664.12843
Burns B, Innes J, Day T (2012) The use and potential of pest-proof fencing for Lami F, Vitti S, Marini L, Pellegrini E, Casolo V, Trotta G, Sigura M, Boscutti F
ecosystem restoration and fauna conservation in New Zealand. Pages (2021) Habitat type and community age as barriers to alien plant invasions
65–90. In: Somers MJ, Hayward MW (eds) Fencing for conservation: in coastal species-habitat networks. Ecological Indicators 133:108450.
65 restriction of evolutionary potential or a riposte to threatening pro- https://doi.org/10.1016/j.ecolind.2021.108450
cesses?. New York, NY: Springer Science+Business Media Lockwood JL, Pimm SL (1999) When does restoration succeed? Pages 363–392.
Carmona MR, Armesto JJ, Aravena JC, Pérez CA (2002) Coarse woody debris In: Weiher E, Keddy P (eds) Ecological assembly: advances, perspectives,
biomass in successional and primary temperate forests in Chiloé Island, retreats. Cambridge University Press, Cambridge, UK. https://doi.org/10.
Chile. Forest Ecology and Management 164:265–275. https://doi.org/10. 1017/CBO9780511542237.014
1016/S0378-1127(01)00602-8 Luken JO (1990) Directing ecological succession. Chapman and Hall,
Cavani L, Manici LM, Caputo F, Peruzzi E, Ciavatta C (2016) Ecological resto- London, UK
ration of a copper polluted vineyard: long-term impact of farmland aban- Mahaney WM, Gross KL, Blackwood CB, Smemo KA (2015) Impacts of prairie
donment on soil bio-chemical properties and microbial communities. grass species restoration on plant community invasibility and soil processes
Journal of Environmental Management 182:37–47. https://doi.org/10. in abandoned agricultural fields. Applied Vegetation Science 18:99–109.
1016/j.jenvman.2016.07.050 https://doi.org/10.1111/avsc.12128
Clements FE (1916) Plant succession: an analysis of the development of vegeta- McAlpine C, Catterall CP, Nally RM, Lindenmayer D, Reid JL, Holl KD, et al.
tion. Washington, DC: Carnegie Institution of Washington. https://doi.org/ (2016) Integrating plant- and animal-based perspectives for more effective
10.5962/bhl.title.56234 restoration of biodiversity. Frontiers in Ecology and the Environment 14:
Clements FE (1928) Plant succession and indicators. HW Wilson, New York 37–45. https://doi.org/10.1002/16-0108.1
Clements FE (1949) Plant succession and human problems. Pages 1–21. In: Nolan M, Dewees S, Ma Lucero S (2021) Identifying effective restoration
Allred BW, Clements ES (eds) Dynamics of vegetation. HW Wilson Com- approaches to maximize plant establishment in California grasslands
pany, New York through a meta-analysis. Restoration Ecology 29:e13370. https://doi.org/
Cole CA (2019) Created ecosystems and the concept of succession. Landscape 10.1111/rec.13370
Journal 38:75–85. https://doi.org/10.3368/lj.38.1-2.75 Novara A, Rühl J, La Mantia T, Gristina L, La Bella S, Tuttolomondo T (2015)
Cooper WS (1923) The recent ecological history of Glacier Bay, Alaska. Ecology Litter contribution to soil organic carbon in the processes of agriculture
4:93–128. https://doi.org/10.2307/1929485 abandon. Solid Earth 6:425–432. https://doi.org/10.5194/se-6-425-2015
Crocker RL, Major J (1955) Soil development in relation to vegetation and sur- Opler PA, Baker HG, Frankie GW (1980) Plant reproductive characteristics dur-
face age at Glacier Bay, Alaska. Journal of Ecology 43:427–448. https:// ing secondary succession in neotropical lowland forest ecosystems. Biotro-
doi.org/10.2307/2257005 pica 12:40–46. https://doi.org/10.2307/2388155
del Moral R, Walker LR, Bakker JP (2007) Insights gained from succession for the Parker JD, Burkepile DE, Hay ME (2006) Opposing effects of native and exotic
restoration of landscape structure and function. Pages 19–44. In: Walker LR, herbivores on plant invasions. Science 311:1459–1461. https://doi.org/10.
Walker J, Hobbs RJ (eds) Linking restoration and ecological succession. 1126/science.1121407
Springer, New York, NY. https://doi.org/10.1007/978-0-387-35303-6_2 Phillips J (1934) Succession, development, the climax, and the complex organ-
Gleason HA (1927) Further views on the succession-concept. Ecology 8:299– ism: an analysis of concepts. Part I. Journal of Ecology 22:554–571.
326. https://doi.org/10.2307/1929332 https://doi.org/10.2307/2256189
Gomez-Aparicio L, Zamora R, G omez JM, H odar JA, Castro J, Baraza E (2004) Pickett S, Cadenasso ML, Meiners SJ (2009) Ever since Clements: from succes-
Applying plant facilitation to forest restoration: a meta-analysis of the use sion to vegetation dynamics and understanding to intervention. Applied
of shrubs as nurse plants. Ecological Applications 14:1128–1138. https:// Vegetation Science 12:9–21. https://doi.org/10.1111/j.1654-109X.2009.
doi.org/10.1890/03-5084 01019.x
Grime JP (1979) Plant strategies and vegetation processes. John Wiley & Sons, Prach K, Tichý L, Lencova K, Adamek M, Koutecký T, Sadlo J, et al. (2016)
London, UK Does succession run towards potential natural vegetation? An analysis
Halassy M, Botta-Dukat Z, Csecserits A, Szitar K, Török K (2019) Trait-based across seres. Journal of Vegetation Science 27:515–523. https://doi.org/
approach confirms the importance of propagule limitation and assembly 10.1111/jvs.12383
rules in old-field restoration. Restoration Ecology 27:840–849. https:// Prach K, Walker LR (2020) Comparative plant succession among terrestrial
doi.org/10.1111/rec.12929 biomes of the world. Cambridge University Press, Cambridge, UK.
Hobbs RJ, Walker LR, Walker J (2007) Integrating restoration and succession. https://doi.org/10.1017/9781108561167
Pages 168–179. In: Walker LR, Walker J, Hobbs RJ (eds) Linking restora- Rapson GL (2018) Changing methodology results in operational drift in the
tion and ecological succession. Springer, New York, NY. https://doi.org/ meaning of leaf area index, necessitating implementation of foliage layer
10.1007/978-0-387-35303-6_8 index. Ecology and Evolution 8:638–644. https://doi.org/10.1002/ece3.
Holl KD (2020) Primer of ecological restoration. Island Press, Washington D.C. 3662
Holl KD, Aide TM (2011) When and where to actively restore ecosystems? For- Rapson GL (2021) Testing the acid in plant succession. Conservation Biology 35:
est Ecology and Management 261:1558–1563. https://doi.org/10.1016/j. 1704–1705. https://doi.org/10.1111/cobi.13825
foreco.2010.07.004 Robinson R (1942) Some ecological aspects of afforestation and forestry in Great
Hughes AR, Grabowski JH, Leslie HM, Scyphers S, Williams SL (2018) Inclu- Britain. Forestry: An International Journal of Forest Research 16:1–12.
sion of biodiversity in habitat restoration policy to facilitate ecosystem https://doi.org/10.1093/forestry/16.1.1

6 of 7 Restoration Ecology January 2023


1526100x, 2023, 1, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/rec.13683 by Luiz Moraes - CAPES , Wiley Online Library on [04/01/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
Tertiary succession in restoration

Ruiz-Jaen MC, Aide TM (2005) Restoration success: how is it being measured? Villacís Lozada SP, Rapson GL (2021) Morphodynamics of short-lived
Restoration Ecology 13:569–577. https://doi.org/10.1111/j.1526-100X. wetlands of coastal dune slacks, Manawat u, New Zealand. Wetlands
2005.00072.x Ecology and Management 29:1–17. https://doi.org/10.1007/s11273-
SER (2004) Society for Ecological Restoration International Science & policy 020-09776-3
working group. In: The SER international primer on ecological restoration. Walker LR, del Moral R (2003) Primary succession and ecosystem rehabilitation.
Society for Ecological Restoration International, Tuscon. www.ser.org Cambridge University Press, Cambridge, UK. https://doi.org/10.1017/
Shantz HL (1906) A study of the vegetation of the Mesa region east of Pike’s CBO9780511615078
peak: the Bouteloua formation. II. Development of the formation. Botanical Walker LR, del Moral R (2008) Lessons from primary succession for restoration
Gazette 42:179–207. https://doi.org/10.1086/328960 of severely damaged habitats. Applied Vegetation Science 12:55–67.
Suzuki M, Karukome T, Fujihira K, Mitsugi M, Hisamoto, Y. (2021) Clear- https://doi.org/10.1111/j.1654-109X.2009.01002.x
cutting triggers regeneration of abandoned secondary forests but risks alter- Walker LR, Walker J, Hobbs RJ (2007) Linking restoration and ecological suc-
native successional trajectories with high deer density. Applied Vegetation cession. Springer, London. https://doi.org/10.1007/978-0-387-35303-6
Science, 24(3), e12596. https://doi.org/10.1111/avsc.12596 Wardle DA, Peltzer DA (2007) Aboveground-belowground linkages, ecosystem
Tognetti PM, Chaneton EJ, Omacini M, Trebino HJ, Le on RJ (2010) Exotic development, and ecosystem restoration. Pages 45–68. In: Walker LR,
vs. native plant dominance over 20 years of old-field succession on set- Walker J, Hobbs RJ (eds) Linking restoration and ecological succession.
aside farmland in Argentina. Biological Conservation 143:2494–2503. Springer, New York, NY. https://doi.org/10.1007/978-0-387-35303-6_3
https://doi.org/10.1016/j.biocon.2010.06.016 Warming E (1895) Pages 335. Plantesamfund – Grundtræk af den økologiske
Török P, Bullock James MJM, Jiménez-Alfaro B, Sonkoly J (2020) The impor- Plantegeografi. P.G. Philipsens Forlag, Copenhagen, Denmark
tance of dispersal and species establishment in vegetation dynamics and Warming E, Vahl M (1909) Pages 422. Oecology of plants – an introduction to
resilience. Journal of Vegetation Science 31:935–942. https://doi.org/10. the study of plant-communities. Clarendon Press, Oxford, UK. https://
1111/jvs.12958 doi.org/10.5962/bhl.title.160223

Coordinating Editor: Stephen Murphy Received: 17 November, 2021; First decision: 16 February, 2022; Revised: 22
February, 2022; Accepted: 16 March, 2022

January 2023 Restoration Ecology 7 of 7

You might also like