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Home , Ecological succession, Primary succession, Regeneration (ecology), Ruderal species

Applied Science 12: 55–67, & 2008 International Association of Vegetation Science 55

Lessons from for restoration of severely damaged

Walker, Lawrence R.1Ã & del Moral, Roger2,3

1School of Life Sciences, University of Nevada Las Vegas, Las Vegas, NV 89154-4004, USA; 2E-mail [email protected]; 3Biology Department, University of Washington, Seattle, WA 98195-1800, USA; ÃCorresponding author; Fax111 702 895 3956; E-mail [email protected]

Abstract land managers need immediate guidance, risky be- cause focusing any scientific pursuit strictly on Questions: How can studies of primary succession applicability of results can impede serendipitous increase the effectiveness of restoration activities? Can discovery. One beneficial application of successional restoration methods be improved to contribute to our lessons is to guide ecological restoration (sensu lato, understanding of succession? Aronson et al. 1993), which is essentially the purpo- seful manipulation of succession (Bradshaw & Results: Successional studies benefit restoration in six areas: site amelioration, development of struc- Chadwick 1980; Walker et al. 2007a). Restoration ture, nutrient dynamics, life history traits, species practices benefit from successional discoveries in at interactions, and modeling of transitions and trajectories. least six areas: site amelioration, development of Primary succession provides valuable lessons for under- community structure, nutrient dynamics, species life standing temporal dynamics through direct, long-term history traits, species interactions, and modeling the observations on severely disturbed habitats. These lessons transitions between successional stages and how assist restoration efforts on infertile or even toxic sub- those stages fit together into trajectories. Scientific strates. Restoration that uses scientific protocols (e.g., approaches to restoration also can clarify succes- control treatments and peer-reviewed publications) can offer insights into successional processes. sional processes and improve the predictability of succession, thus leading to reciprocal benefits be- Conclusions: A century of studying successional dy- tween the two fields. namics has provided modern restoration activities with Primary succession is species change on sub- many useful lessons that are not being fully utilized. strates where the has left a scant biological legacy (Clements 1916). Many classic Keywords: Disturbance; Life history; Models; Nutrients; studies of plant succession have been conducted on Retrogressive succession; Species interactions; Trajectory. primary seres (successional sequences). These in- clude in (Warming 1895), Michigan, USA (Cowles 1901), and Australia (Coaldrake 1962); volcanoes in Indonesia (Ernst Introduction 1908), Alaska, USA (Griggs 1933), and Hawaii, USA (Eggler 1971); and glacial moraines in Alaska, Succession, the study of species change over USA (Cooper 1923) and New Zealand (Stevens & time, is a fundamental concept of (McIntosh Walker 1970). Primary succession is integral to any 1999). It addresses dynamics both during thorough examination of temporal dynamics for and beyond the life span of . Formal several reasons. First, valuable long-term studies studies of plant succession have been conducted have been conducted at some of the study sites listed since 1895 (Warming 1895) and much has been above and on many other primary seres (Walker & learned about how respond to a dynamic del Moral 2003). Direct observation over time is al- physical environment (Pickett & White 1985), how ways preferred over single measurements along the species colonize and interact (Glenn-Lewin et al. landscape (chronosequence) where assumptions of 1992), and how communities assemble and change similar development among differently-aged plots (Temperton et al. 2004). Applying these lessons to are problematic (Fastie 1995). Second, primary seres practical needs is urgent and risky – urgent because provide a contrast to studies of secondary succes- 56 WALKER,L.R.&DEL MORAL,R. sion that occur on more fertile and stable substrates Table 1. Examples of restoration tactics to address (e.g., old field succession; Cramer & Hobbs 2007). problems at crucial stages of the restoration process. Third, in many severely disrupted ecosystems, par- Restoration Goal Tactics ticularly those dominated by long-lived organisms topic such as trees, shifts in vegetative composition are Establishment Ameliorate Create safe sites to enhance survival slow (hundreds to thousands of years). Primary stress Install fences to trap seeds succession is an important approach to these long- Install perches to enhance dispersal term processes and helps to link successional pro- Appropriate fertilization Dense stocking rates to create ‘nurse cesses with even longer processes such as soil plant effect’ by mutual protection formation and development (Wardle et al. 2004). Carbon Accelerate Surface preparations (e.g., mulch, safe Finally, primary succession provides the most ap- accumulation development sites) Direct planting of mature individuals propriate tools for restoring heavily damaged Stabilize erosion (short-lived cover systems of both natural and anthropogenic origin ) Limit grazing (e.g., fencing, thorny (del Moral et al. 2007). Ecosystems highly disrupted shrubs) by human activities can be unstable, infertile, or Nutrient Increase Adjust fertility by: use of N-fixing even toxic. Lessons from primary succession, in- dynamics availability species; adding carbon (e.g., sawdust) to immobilize excessive nutrients; add itially developed on naturally disturbed surfaces phosphorus and organic matter in with spontaneous recovery, are often relevant for later stages to provide nutrient restoration (directed recovery) of such anthro- retention Life history Enhance Consider local species pools (i.e., pogenic disturbances. diversity donors) and any seed bank In this paper, we highlight six ways that succes- Modify site for mix of growth forms planned sional studies in severely disturbed habitats have Select species based on its weakest contributed to the development of ecological prin- link (e.g., seedling survival or ciples and help to clarify the goals of ecological competitive ability, not its adult characteristics) restoration. The coverage of such a broad range of Species Self- Limit from nutrient- topics cannot be comprehensive, but we illustrate interactions sustaining responsive species through planned each topic with a few examples. We also briefly ex- species disturbances Include shade-tolerant species and N- amine how restoration can help advance the fixers understanding of succession. Our aim is to illustrate the usefulness of recognizing the tight, mutually beneficial links between succession and restoration. Biologists have long incorporated the impact of natural disturbances on populations of all organ- Site Amelioration isms, including humans. Now humans utilize at least 30% of all global net primary (Vitou- Studies of primary succession describe and at- sek et al. 1986), with that value reaching 100% in tempt to explain how plant, animal, and soil some regions (Foley et al. 2007). Because we have communities respond in the aftermath of severe dis- profoundly affected all of Earth’s ecosystems turbances (Walker 1999a). Inevitably, this involves (Steffen et al. 2007), humans now trigger, enhance, evaluating the attributes of the original disturbance or are otherwise involved in disturbances in a positive (magnitude, severity) and of any subsequent occur- feedback loop that not only increases disturbances rences (frequency) and explaining the amelioration but also increases human risk (Fig. 1; Keys 2000; of the initial physical conditions by both abiotic and Diamond 2005; del Moral & Walker 2007). One way biotic processes (Walker 1999b). Restoration can to break this cycle is through changes in human be- use this information to accelerate the amelioration haviors that contribute to disturbance, for without of harsh conditions (Table 1). However, restoration such changes, restoration of severely damaged habi- must be placed in a human context. Prediction, as- tats may be only temporary. For example, sessment, and mitigation of natural disasters have stabilization of triggered by road cutting been increasingly emphasized as human populations ultimately means that road construction should not expand and more human lives are at risk. Histori- continue unabated. However, lessons of natural re- cally, humans relied more on avoidance (Oliver- covery gleaned from successional studies can increase Smith & Hoffman 1999) but now disasters are the effectiveness of restoration of severely damaged analyzed by geologists, engineers, and sociologists habitats (Reice 2001; del Moral & Walker 2007), and, for their actual or potential impact on humans. at best, also inform policy and land management -RESTORATION OF SEVERELY DAMAGED HABITATS -57

Human geographic expansion

Growth

Risk to human lives Human

Natural disturbances Anthropogenic disturbances

Fig. 1. Human population growth leads to geographic expansion and both of these changes increase anthropogenic dis- turbances (e.g., agriculture, , urbanization) that precipitate and intensify natural disturbances (e.g., expansion, floods, landslides). Human lives are then increasingly at risk from the direct effects of larger population size and geographic expansion and indirectly through increased disturbance (both anthropogenic and natural). Disturbances also kill people, but not enough to offset rapid population growth. Solid lines indicate a positive influence, dashed lines a negative influence. Modified from del Moral & Walker (2007). about the ecological consequences of some human ac- surface temperatures, reduced erosion, and in- tivities. For example, successful restoration of Puerto creased animal activity). Rican landslides involves a thorough grasp of plant life Carbon accumulation is not continuous even in histories and species interactions but also an under- successional systems that are left undisturbed. Fol- standing of how soil stability is best achieved (through lowing a progressive accumulation of carbon and either physical or biotic manipulation; Walker et al. nutrients, many primary seres undergo a retro- 1996; Shiels et al. 2008). Coupling ecological and en- gressive phase where carbon and often phosphorus gineering tools with appropriate land use will decline (Walker et al. 2001; Wardle et al. 2004). Re- maximize recovery from specific disturbances at both storation strategies will differ between these two local and landscape levels. phases, with recovery of likely to be much more difficult during retrogression than progression (Walker & Reddell 2007), especially when thresh- Accumulation of Carbon and Development of olds of deterioration (e.g., loss of carbon or Community Structure community structure) have been passed that require extra effort to reverse (Whisenant 1999; Hobbs & The sequential development of different plant Harris 2001). Although retrogression is commonly communities after severe disturbances remains an viewed as occurring only after many centuries of intriguing mystery, despite a century of examina- gradual accumulation of carbon and community tion. How communities assemble is so complex that structure, shorter-term losses also alter successional there is little agreement on even general patterns, dynamics and subsequent restoration efforts although carbon certainly accumulates and com- (Walker & del Moral 2008). These losses can argu- munity structure becomes more complex. Primary ably be considered retrogression (Fig. 2). For succession is often less predictable than secondary example, frost damage reduced by a succession (Turner et al. 1997; Fukami et al. 2005). shrub on a 100-year-old volcanic surface in New Early in primary succession, recurrent (but stochas- Zealand and thereby delayed succession (Walker tic) disturbances are likely, and safe sites that are et al. 2003). Ongoing disturbances such as fires and both fertile and stable enough for establishment are flooding (Reice 2001), landslides (Walker et al. rare (Walker et al. 2006). Nonetheless, any guide- 1996) and invasions (Vitousek et al. 1987), or novel lines from successional observations or experiments disturbances such as vehicle tracks (Bolling & can help achieve the usual restoration goals of in- Walker 2002) can reduce carbon accumulation and creased plant cover and and their cause retrogression, as long as they are not so severe corollaries (e.g., more shade, leaf litter, moderated as to reset the sere. Indeed, any disturbed landscape 58 WALKER,L.R.&DEL MORAL,R.

CLASSIC CONTINUOUS

FUNCTION

CYCLIC IRREGULAR

STALLED RETROGRESSION STALLED PROGRESSION

TIME Fig. 2. Possible patterns for retrogressive change during succession based on a single ecosystem function (e.g., biomass, nutrient pool). The classic pattern involves a long build-up phase (longer in primary than secondary succession) followed by a long decline. Other possible patterns include continuous decline, regular or irregular alternating periods of progressive and retrogressive change, or even a stalled retrogression (analogous to arrested or stalled progression). The time scales may differ among the patterns (e.g., the classic pattern may involve centuries, the cyclic pattern only decades). may have patches of both progressive and retro- Nutrient Dynamics gressive change. Restoration efforts to accelerate the accumula- The accumulation of nutrients in primary seres tion of carbon and structure can involve direct that are initially very infertile is a critical determi- carbon inputs through mulching or transplanting nant of successional pathways and an issue with (Table 1). Such efforts, especially the use of fast- implications for restoration. In many infertile seres, growing ground cover, might help stabilize the sur- the almost universal increase in nitrogen is largely face but the introduction of species that produce due to microbial nitrogen fixation, particularly dense swards or thickets often can make establish- when fixation occurs symbiotically with vascular ment of natives and development of subsequent plants (Van Cleve et al. 1971; Walker 1993). Com- stages difficult (see ‘Species interactions’). Re- mon limits to nitrogen fixation include available vegetation with grass species on construction sites in phosphorus and moisture (Sprent 1987). Therefore, the Alaskan tundra, for example, delayed establish- vascular plants with nitrogen fixing symbionts ment by native plants (Densmore 1992). Other (hereafter called ‘nitrogen-fixers’) are more success- restoration efforts attempt to skip successional ful invaders of habitats with some initial soil stages and introduce large, late-successional vegeta- development than of recently exposed, highly in- tion directly. This is most effective in stable and fertile sites (Uliassi & Ruess 2002). Subsequent fertile habitats where the transplants are initially successional dynamics (exactly which plant species protected from competition (Whisenant 2005). follow the nitrogen-fixers) depend on the density, Planting young shrubs or trees can act as mutual life form, and longevity of the nitrogen-fixer, its im- protection from physical stress, eliminate competi- pact on and microclimate, and its tion from other species, and limit grazing effects historical role in the community (Vitousek et al. (Bradshaw & Chadwick 1980). 1987; Walker & del Moral 2003). Unlike nitrogen, -RESTORATION OF SEVERELY DAMAGED HABITATS -59 phosphorus levels typically decline through primary Species Life Histories succession as labile forms are leached or im- mobilized (Walker & Syers 1976; Vitousek & One important lesson from successional studies Farrington 1997); the balance between nitrogen and is that each species has a range of responses to the phosphorus levels in both soils and plants affects environment, depending on its life history stage and is impacted by successional processes (Sterner & (seed, seedling, juvenile, and reproductive adult) and Elser 2002). whether the plant is colonizing, establishing, grow- There are several implications of nutrient dy- ing, or senescent (Grubb 1977). How species namics for restoration. First, primary seres occur respond differentially to disturbances is particularly under initially infertile conditions, so fertilization accentuated in the inhospitable environments of may impede rather than aid restoration (del Moral early primary succession (Bruno 2000; Levine 2000; et al. 2007). This can happen when too much fertili- see ‘Site amelioration’). Species interactions such as zer favors fast-growing weeds over slow-growing facilitation and competition within a successional natives, when nutrient ratios become altered, or community also vary by life history stage. For ex- when either of these effects leads to different suc- ample, nitrogen-fixing shrubs on a volcano in New cessional trajectories. The utilization of nitrogen- Zealand (Walker et al. 2003) and a glacial moraine fixers may provide an optimum nutrient balance, in Alaska (Chapin et al. 1994) both inhibited and but there can be unintended consequences such as facilitated subsequent species and these effects var- the inhibition of succession. For example, the her- ied by life-history stage and successional stage. In baceous nitrogen-fixer Lupinus nootkatensis was both cases, the shrubs inhibited germination and widely planted in Iceland to restore in areas establishment but had a net positive effect because of severe soil erosion but had negative impacts on of the large increase in organic matter and the facil- native legumes and small shrubs where it formed itation of growth of the later successional species. thick mats (Aradottir 2004). A common method for A thorough knowledge of the life-history stages restoring favorably low nutrient levels is the addi- of the plants used in any restoration effort is clearly tion of a carbon source such as sawdust or mulch in helpful. Huberty et al. (1998) found that nitrogen order to immobilize available nutrients in soil additions improved overall growth, but did not microbes (Blumenthal et al. 2003). Such addi- cause displacement of one growth form by another tions frequently counteract as well even though individual species were affected differ- (Alpert & Maron 2000). Second, highly variable ently. Details at the species level concerning traits spatial patterns in soil nutrients are common so re- such as dispersal ability, germination requirements, storation efforts must account for them (Walker & growth rates, life spans, and functional types can del Moral 2003). Steep nutrient gradients, often at help plan the best approach (Table 1). When these very small scales as found around desert shrubs details are unknown, one must rely on known life (Bolling & Walker 2002) or in sand dunes (Groot- histories of closely related species, but often with jans et al. 1998), suggest that careful soil analyses unfortunate results (Simmons et al. 2007). When re- would help most restoration efforts. Finally, when covery is allowed to proceed spontaneously, the retrogressive conditions exist due, for example, to results are unpredictable and they are satisfactory long-term salt accumulation or nutrient leaching, only under special conditions (Prach & Pysˇek 2001). these conditions must be ameliorated before pro- Dispersal and physical stresses limit establish- gressive succession can be established. Vegetation ment and growth of plants in early primary can be used to improve freshwater retention and or- succession. Overcoming these obstacles is central to ganic matter accumulation (Walker & Reddell any acceleration (restoration) of recovery processes. 2007). However, inappropriate additions of vegeta- Direct introduction of propagules can offset dis- tion or fertilizers can trigger new shifts in persal limitations, especially when disturbed areas trajectories and changes in the balance between are large, or when propagules are limited in number progressive and retrogressive change (Fig. 2). Ulti- or when the species are poor dispersers. Successful mately, no restoration effort can ignore nutrient introductions depend on knowledge of the most dynamics. Indeed, a successful (self-maintaining) favorable microsite conditions for each species. restored ecosystem will have at least a semblance of Slight differences in topography or substrate can the original nutrient cycles. These cycles are best re- improve microclimates for germination and sur- established indirectly via restoration of plant and vival (del Moral & Deardorff 1976). For instance, soil fauna communities; fertilizers should be used gravel-covered microsites on Mauna Kea volcano only sparingly (Table 1). in Hawaii provided optimal conditions for seed 60 WALKER,L.R.&DEL MORAL,R. germination and transplanted seedling survival of Many seeds reach a site without germinating the rare silversword (Agyroxiphium sandwicense; (Wood & del Moral 1987), so understanding germi- Walker & Powell 1999a). However, the presence of nation requirements is crucial for successful woody vegetation favored seed germination but in- restoration. Seeds can persist in a seed bank, only to hibited seedling growth, so each restoration germinate years later, perhaps following a major approach had both advantages and disadvantages. disturbance such as fire (Willis & Read 2007). This Attempts at direct introductions often fail due to a hidden pool of colonists can adversely affect plan- lack of understanding of the tolerances of the target ned trajectories, so the seed bank should be species in each life stage. Indirect methods of in- considered carefully. Conditions for successful seed troductions can allow for the sorting of various germination include not just specific microsite natural processes. For example, artificial perches requirements (e.g., safe-sites; Jones & del Moral were successful in attracting birds and hence seeds of 2005), but also proper pre-germination con- many trees to Puerto Rican landslides (Shiels ditions (Satterthwaite 2007). Sowing seeds that & Walker 2003), but few seeds germinated, in part require stratification requires quite different because they were inhibited by dense vegetation timing from agricultural species that lack dormancy. dominated by wind-dispersed grasses. Further, in- Many species require scarification (Pugnaire et al. direct means can be spatially constrained, or can 2006) or heat treatments. These pre-conditions allow the introduction of undesirable species. Dis- are often difficult to apply, but stratification persal, germination, and early seedling survival are (cold, wet, dark conditions) or treatment with stages during which a particular species may have hormones (e.g., gibberellins) can be effective subtly different environmental optima (Brooker & substitutes. In contrast, unforeseen natural dis- Callaghan 1998; Levine 2000). turbances can alter succession. In Panama, fire Models of succession demonstrate that seed inhibited seed germination of many species, dispersal usually dictates trajectories in early suc- leading to competitive dominance by a few pioneer cession and can be more important than species (Hooper et al. 2004). Slow germinating availability (Martineau & Saugier 2007). Studies of species may be at a substantial disadvantage when spontaneous succession in the Czech Republic de- sown with rapidly emerging species, so phased monstrated that pioneer communities were highly planting or sowing may be required. Differential heterogeneous and determined by dispersal avail- longevity also affects trajectories (Connell & Slatyer ability, while, after several years, soil properties 1977) and determines competitive dominance in imposed a deterministic structure on the vegetation many types of vegetation (Schippers & Kroptt (Lepsˇet al. 2000). This study suggested that the 2001). course of restoration would be affected first by the The fate of viable and potent seeds is rarely appropriate selection of species and then by proper considered when succession is being investigated, yet preparation of the soil. Dispersal limitations seed can seriously alter or arrest succes- (Rehounkova & Prach 2006) can create unpredic- sion. When Barbera et al. (2006) explored reasons table trajectories, so planning for restoration starts for arrested succession in degraded Mediterranean with knowledge of the dispersal potential of the scrublands now dominated by perennial tussock surrounding vegetation. Sowing desirable species grasses, they found that the former dominant oak is nearly always required if any control of early species suffered very high predation rates. Arrested restoration is needed. Lepsˇet al. (2007), in a large- succession occurred even before potential domi- scale study in five European countries, demon- nants could establish. Alternatively, various forms strated that sowing different seed mixtures over of facilitation can promote successional transitions. existing vegetation markedly altered successional Trema micrantha, a pioneer of Brazilian rain forests, trajectories. Spontaneously recovering control plots facilitated the invasion of other forest trees in a were more diverse, but the least productive. This highly fragmented system (Rodrigues et al. 2004). study demonstrated that proper sowing regimes re- This pattern is repeated in habitats as diverse as dry sult in highly productive communities within which European (Kunstler et al. 2007) and undesirable species (i.e., weeds) were suppressed. open North African savannas (Aerts et al. 2006). Experimental work in a successional context that Once plants are established, they still must face couples both scientific and restoration goals will be competitive threats from other species, so the com- most productive in discovering and ameliorating the petitive abilities of species must be considered. dispersal limitations for each life history stage of Often, functional types (sensu Grime 2001) can be each species of concern (Walker & del Moral 2003). used to assess longer-term competitive ability and -RESTORATION OF SEVERELY DAMAGED HABITATS -61 success. Caccianiga et al. (2006) demonstrated that Species Interactions functional types shifted during primary succession on an alpine glacier foreland, from ruderal to stress- As the physical stability and fertility of a pri- tolerant species. Erschbamer (2007) provided ex- mary sere increase, the impact of biotic interactions perimental confirmation for differential responses on succession increases. Although complex, these among species in a similar . Purely pioneer or interactions have been categorized into those that ruderal species, common to young glacier forelands, are facilitative, inhibitory or neutral (Connell & were less able to adapt to increasing temperatures Slatyer 1977), and they can impact all stages of suc- when compared to competitive, stress-tolerant spe- cession (Walker & Chapin 1987) and each life cies. Her results suggested that more plastic or history stage of the dominant species (Walker tolerant species should be preferred in restoration et al. 2003). The balance between facilitative and projects to ensure greater success under changing inhibitory interactions often varies along environ- conditions. mental gradients, and facilitation tends to increase Herbivory can have various impacts on vegeta- with environmental stress (Callaway & Walker tion dynamics (Horsley et al. 2003; Graaf et al. 2007) 1997; Brooker & Callaghan 1998). However, this and can arrest, retard or accelerate succession, de- generalization may not be universally applicable pending on circumstances (Walker & del Moral (Maestre et al. 2005). Any species interaction will be 2003). Invertebrate herbivory can impact succes- described differently, depending on the perspective sional trajectories by impeding or facilitating plant chosen. A positive outcome for one species can be establishment (Brown & Gange 1992; Bach 1994) negative for another. In a successional context, but is most likely to affect species change in later facilitative interactions tend to promote succession stages of succession (Walker & Chapin 1987). Peri- and the order of species replacement while inhibi- odic insect outbreaks, especially those that reduce tory interactions tend to arrest the rate of change the viability of one dominant species (Fagan et al. (McCook 1994; Walker et al. 2003). Successful re- 2005), are most likely to occur in favorable habitats storation clearly must addresses species interactions and represent the biggest influence of invertebrate that impact successional trajectories. herbivory on succession (Walker & del Moral 2003). Nitrogen-fixers (see ‘Nutrient dynamics’) have The influence of vertebrate herbivory, in contrast, the potential to facilitate primary succession by generally declines over successional time, as multi- adding nitrogen to developing soils (del Moral & ple, better-defended plant parts mature. Vertebrates Rozzell 2005). However, a comparison of five pri- are also more likely to impact species change in fa- mary seres where the impact of woody nitrogen- vorable than unfavorable habitats (Walker & del fixers has been examined showed little or no impact Moral 2003). Restoration activities must first evalu- on the arrival of subsequent species, mostly negative ate conditions for the particular case, then decide to effects on their germination, and a mixed impact on either factor in herbivory by establishing species that growth (Table 2). The net effect on growth (whether resist grazing (or mixing them with more vulnerable positive or negative) was not explained by the ones) or consider the exclusion of (del amount or increase in nitrogen (Table 2). The two Moral et al. 2007). Herbivory also impacts succes- seres where the nitrogen-fixer had a net negative sion indirectly through alterations of nutrient effect on the growth of subsequent species had dynamics (Wardle & Peltzer 2007). either the highest or lowest increase in nitrogen. Life-history characteristics of species planned Net negative effects were generally due to root for use in restoration programs are rarely considered competition, while soil nitrogen increases usually in detail, yet they are crucial. Many projects benefited growth of subsequent species in pot have failed due to inattention to such details. experiments. The net negative effect of the Hawaiian Failing detailed knowledge, functional group classi- nitrogen-fixer Myrica (an invasive species) on fications based on available information can be Metrosideros (the native) summarizes a complex useful to enhance the prospects for success. Atten- set of both positive and negative impacts of dif- tion must be paid to the likely pool of beneficial and ferent environmental effects of Myrica on various detrimental species, germination requirements (both life stages of Metrosideros (Table 3). The net physiological and physical), responsiveness to ferti- effect of a nitrogen-fixer is dependent on many lity levels, the ability to tolerate herbivory and variables, including its growth form, density, and disease, competitive abilities, and the ability of the impact on soil phosphorus or water (Walker & species to protect and facilitate other desirable Vitousek 1991; Walker & del Moral 2003; Aradottir species. 2004). 62 WALKER,L.R.&DEL MORAL,R.

Table 2. Effects of woody vascular plants with nitrogen-fixing symbionts (‘nitrogen-fixer’) on the arrival, germination, and growth of the subsequent woody species and on soil nitrogen in five different successional sequences.

Site Habitat Nitrogen-fixer Subsequent species Arrival Germination Growth N Before N During Increase

Hawaii Volcano Myrica Metrosideros Neutral Negative Negative 2 13 6.5 New Zealand Volcano Coriaria Griselinia Positive No data Positive 15 78 5.2 New Zealand Floodplain Carmichaelia Griselinia Neutral No data Positive 22 106 4.8 Alaska Floodplain Alnus Picea Neutral Negative Negative 40 110 2.7 Alaska Moraine Alnus Picea Neutral Negative Positive 4 22 5.5 References: Hawaii: Vitousek & Walker (1989), Walker & Vitousek (1991); New Zealand volcano: Walker et al. (2003); New Zealand floodplain: Bellingham et al. (2001); Alaska floodplain: Walker et al. (1986), Walker & Chapin (1986); Alaska moraine: Chapin et al. (1994). Soil nitrogen levels are shown for before the nitrogen-fixer was present (‘N Before’) and during its dominance at each site (‘N During’) (total nitrogen in g/m2 except for Hawaii: available nitrogen in mg/g). Increase in soil nitrogen was calculated as N During/N Before.

Table 3. Effects of the invasive Myrica tree on the native Similarly, facilitating succession may not be the goal Metrosideros tree in Volcanoes National Park, Hawaii, where intermediate stages are themselves desirable. USA. Responses in parentheses are non-significant trends. They may be productive, support characteristic spe- Modified from Walker & del Moral (2003). cies, produce valuable commodities, or provide Metrosideros life Myrica Effect of Myrica on other services such as low maintenance power line Stage factor Metrosideros corridors (Niering et al. 1986; De Blois et al. 2004). Clarity about restoration goals is essential, whether Germination Litter Negative Shade Positive the goals are to decrease erosion, increase biodi- Leaf (Negative) versity, favor a specific successional pathway, or leachate Seedling growth Litter (Positive) promote flexibility in a community to respond to a Shade (Negative) variety of scenarios (Hobbs et al. 2007). Roots Negative Soils Positive Seedling Shade Positive survivorship Roots Negative Modeling of Transitions and Trajectories Soil Neutral Tree growth Neutral Models help to clarify the successional role of Data from Vitousek & Walker (1989) and Walker & Vitousek (1991). each of the above processes (response to dis- turbance, carbon accumulation, nutrient dynamics, Humans consider restoration successful when species life histories, species interactions). Each the newly established community has several native process is influential in how one community under- species that interact and where succession eventually goes the transition to a new community and how occurs with minimal additional input. Many re- these transitions combine to form complex trajec- storation efforts fail when a single species dominates tories. Most restoration activities focus on only one the resources and is long-lived or self-replacing. or two of these processes and rarely address their These arrested seres occur when the dominant spe- integration into longer-term trajectories, spatial cies forms a mat (e.g., bryophytes), sward (grasses), consequences at the landscape level (van Diggelen or thicket (shrubs) that impedes growth of other 2006), or whether those trajectories are in a pro- species through reduction of light or nutrients gressive or retrogressive phase (Fig. 2). (Walker & del Moral 2003). Sometimes arresting Ecological models have recently been in- succession is desirable in order to build up nutrients. corporated into the nascent development of For example, the climbing (Gleicheniaceae) restoration theory (Temperton et al. 2004; van that dominate disturbed areas such as burns, land- Andel & Aronson 2006; Walker et al. 2007b; Suding slides or road edges in the tropics delay forest & Hobbs 2008) and some of these models address succession by shading out forest trees (Walker 1994; succession. However, the lack of predictability Slocum et al. 2004) but also reduce soil erosion about the details of successional trajectories makes through extensive rhizomes and accumulate large predicting the consequences of a given set of re- amounts of organic matter (Russell et al. 1998). Re- storation actions difficult. Two paths hold promise, moval of mats does not necessarily result in however, in linking successional models to restora- rapid tree colonization because initially infertile or tion activities. These are the modeling of restoration unstable conditions may persist (Slocum et al. 2006). effects on immediate transition dynamics and the -RESTORATION OF SEVERELY DAMAGED HABITATS -63 modeling of broader landscape impacts. Good ex- examined how plants respond to disturbance, how amples of both approaches come from detailed plant communities grow by accumulating carbon research on progressive and retrogressive succession and developing spatial structure, how nutrients flow and restoration of fens in northwestern Europe between soils and plants, how species colonize, es- (Schrautzer et al. 2007) and of arid lands in Aus- tablish, grow and interact, and how all of these tralia (Walker & Reddell 2007). Other modeling interactions produce transitions between commu- approaches use simulations (Schippers & Kroptt nities and eventually create complex trajectories. 2001), functional type, or process-based approaches This basic understanding of vegetation change is a (Martineau & Saugier 2007). phenomenally rich source of ideas for planning re- storation programs. Unfortunately, it has not yet been adequately tapped by practitioners of restora- How Restoration Can Help Explain Succession tion (Walker et al. 2007a), despite the pioneering work of Bradshaw and colleagues (Bradshaw & Ecological restoration developed as a practical, Chadwick 1980; Bradshaw 1983, 1987, 1996). In goal-driven activity on lands disturbed by humans turn, restoration programs have a great potential to and has only recently started assembling a set of help elucidate successional principles. Facilitating fundamental principles. Succession has its founda- the mutual exchange of information will help both tions in observations about natural ecosystems and succession and restoration to reach their respective a well-developed body of theory. Yet, better linkage goals of understanding and manipulating vegetation between these disciplines is inevitable because re- change. storation is essentially managed succession. Restoration activities that follow scientific protocols such as hypothesis testing, un-manipulated controls, Acknowledgements. We thank Richard Hobbs and Joe and peer-reviewed publication of results can provide Walker for helpful conversations and Scott Meiners for practical tests of successional principles. For ex- the invitation to attend the symposium: ‘The success of ample, of a short mining road in succession: The development of a fundamental ecological southern Nevada involved ripping the entire road theory and its application to a changing world.’ Viki Cra- but sowing native seeds on only half of its length. mer, Kern Ewing and two anonymous reviewers provided This simple procedure allowed a comparison of helpful comments on the manuscript. This work was sup- ported by grant DEB-0620910 from the US National natural colonization vs. sowing on ripped surfaces Science Foundation as part of the LTER Program in (Walker & Powell 1999b). A more thorough in- Puerto Rico and by grant DEB-0541972 to Roger del vestigation could have involved a factorial design to Moral from the US National Science Foundation. evaluate the benefits of ripping or various watering, This paper is dedicated to the memory of Professor A.D. fertilizing or planting regimes. 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