RESEARCH ARTICLE

Comparing the Performance of Tree Stakes and Seedlings to Restore Abandoned Tropical Pastures
Rakan A. Zahawi1,2 and Karen D. Holl3
Abstract Tree seedlings are commonly planted to restore abandoned agricultural lands, whereas vegetative plantings have received little study. We evaluated the ability of 10 tree species to establish and survive over 3 years by planting 2-m-tall vegetative stakes at three sites in southern Costa Rica. We quantied above- and belowground stake and seedling biomass for two species (Erythrina poeppigiana and Gliricidia sepium) after 1 year and canopy cover and height of E. poeppigiana stakes and saplings at 3 years. We also compared economic, logistical, and ecological advantages of each methodology. Erythrina poeppigiana and E. berteroana had the highest number of live stakes by the studys conclusion (>90%) and were among species with largest canopies. Most others ranged between 40 and 70% with highly site-specic survival and growth rates, whereas three species did poorly. Four species
developed fruit by year 3, including Ficus pertusa and Acnistus arborescens, that are consumed by frugivores. Above- and belowground biomass was 750 times greater in stakes (65125 g) than seedlings (215 g). Stake roots were considerably more extensive and reached lengths more than 6 m. Erythrina poeppigiana stakes had higher canopy cover than saplings after 3 years but not height. Seedlings are 210 times more expensive to establish, although transporting stakes is more cumbersome and the suite of species that establish vegetatively is limited. This underused technique should be included in the growing repertoire of tropical forest restoration tools. Given tradeoffs in propagation methods, a combination is likely to be most efcient and successful.
Key words: biomass production, live fences, tree stakes, tropical pasture restoration.

Introduction Tropical deforestation has been an issue of global concern for well over 30 years. Rates of forest loss in Central America have uctuated over the decades and current rates vary widely depending on the country (FAO 2005). Although considerable forest was cleared in Costa Rica during the 1970s and 1980s (OED 2000), deforestation rates have reduced dramatically in the past decade, and the area of forested land is slowly increasing in some regions due to changes in agricultural market forces and nchez-Azofeifa an increase in conservation initiatives (Sa et al. 2003; Arroyo-Mora et al. 2005). Current estimates put forest cover at 38% of the overall land area with approximately 46% under pasture cultivation (FAO 2004, 2005). Thus, when addressing restoration in Costa Rica, and even Central America, it is logical to focus on pastures as they are the dominant agricultural land use type. Many studies have explored the use of planting seedlings to facilitate forest recovery in tropical pastures. Most studies have been highly successful (e.g., Buttereld 1995;
1 Organization for Tropical Studies, Apdo 73-8257, San Vito de Coto Brus, Costa Rica 2 Address correspondence to R. A. Zahawi, email zahawi@ots.ac.cr 3 Environmental Studies Department, University of California, Santa Cruz, CA 95064, U.S.A.

2008 Society for Ecological Restoration International doi: 10.1111/j.1526-100X.2008.00423.x

Nichols et al. 2001; Carpenter et al. 2004), with seedling survival rates more than 80% and substantial forest regeneration beneath certain species (e.g., Guariguata et al. 1995; Haggar et al. 1997; Lamb 1998). Seedlings of the more successful hardwood species can increase in height at rates of up to 12 m/yr (Buttereld 1995; Carpenter et al. 2004). When planted in combination with fastgrowing species, such as Inga edulis, plantations can develop full canopy closure in as little as 2 years (Nichols et al. 2001). A number of factors, however, can limit this restoration strategy and are not always considered. First, although a substantial number of tree species have been successfully established in seedling eld trials, other trials have failed or resulted in poor survival (e.g., Kolb 1993; Ferguson 1995; Carpenter et al. 2004). Second, the economic cost of establishing a nursery or of purchasing seedlings can be substantial in larger restoration projects. Furthermore, the cost of maintaining seedlings in the eld until they reach a height tall enough to compete with grasses can be high as grass is often cleared or herbicided four to eight times annually the rst few years after planting to reduce grass competition with seedlings (Zahawi & Holl 2006, unpublished data; Buttereld 1995; Erskine et al. 2006). Last, mortality in the eld due to abiotic factors such as drought (Nepstad et al. 1996; Zahawi 2003) and biotic factors such as herbivory (Holl & Quiros Nietzen 1999; Zahawi 2003) can make a project cost prohibitive or even result in failure.
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An alternative method for establishing trees to facilitate pasture recovery is planting vegetative stakes (approximately 2 m tall) of species commonly used as live fencerows in the tropics. Live fences are ubiquitous throughout the tropics, and their ecological role has been widely documented (e.g., Estrada et al. 1997; Harvey et al. 2005). Individuals are typically planted vegetatively by harvesting stakes from nearby fencerows. Aside from their widespread use in agricultural practice, however, the methodology has been applied much less frequently in restoration (but see, e.g., Perino 1979; Hunter 1987; Nichols et al. 2001; Zahawi 2005), and little is known about their establishment requirements or their growth and development outside of an agricultural context. Only one study has examined belowground development of stakes (Messenger et al. 1997) and they did not quantify total biomass production. The technique may also be more advantageous than planting seedlings under certain circumstances although no studies have directly compared planting methods. The objectives of our study were to: (1) evaluate the ability of 10 tree species to establish from stakes and compare their growth and development, (2) compare aboveand belowground biomass of two species planted as stakes and as seedlings, and (3) compare the economic, logistical, and ecological costs and advantages of both planting methods. We conducted our study at three sites to make results more generalizable and better evaluate which species are most suitable for restoration.

Tres) were recently abandoned pastures dominated (>90%) by the exotic forage species Urochloa brizantha (Hochst. Ex. A. Rich.) R. D. Webster, whereas Santo Domingo was predominantly an abandoned coffee farm and was largely dominated by Pteridium arachnoideum (Kaulf.) Maxon, along with a mixture of forage and nonforage grasses. San Gabriel was originally a coffee plantation and had been under pasture agriculture less than 5 years before abandonment, whereas Campo Tres was under pasture use for more than 30 years. Composite surface (010 cm) soil samples collected within 25 m of the stake trial plots as part of a related restoration study suggest that at all sites are acidic (pH 4.75.1) and low in available P (range 4.48.6 mg/L). All sites were cleared of aboveground woody vegetation with machetes prior to planting.
Stake Field Trials

Methods The study was carried out from July 2004 to July 2007, approximately 7 km south of the Las Cruces Biological Station (lat 8479060 N, long 82579350 W; elevation 1,200 m) in Agua Buena de Coto Brus, southern Costa Rica. The forest is classied as a Tropical Premontane Rainforest by Holdridge et al. (1971), and mean annual rainfall for Las Cruces is approximately 4,000 mm, with a distinct dry season from December to March. Mean annual temperature is approximately 21C. Coto Brus County is a highly fragmented landscape made up of a mosaic of mixed-use agricultural elds and forest patches. Daily et al. (2001) estimated that approximately 27% of forest cover remains within a 15-km radius surrounding the Las Cruces station, and this gure is likely higher than in most other parts of the county. Originally a principal coffee-growing region, much of the agricultural land has since been converted to pasture in the past decade due to the global drop in coffee prices (Rickert 2005).

Study Sites

In June 2004, three sites were chosen within a 3-km radius of Agua Buena: Santo Domingo, San Gabriel, and Campo Tres (approximately 1,300, 1,100, and 100 m above sea level, respectively). Two sites (San Gabriel and Campo

In June 2004, 10 species were chosen for the study (Table 1). With the exception of Terminalia, all species were selected based on their regional ability to establish vegetatively under the harsh climatic conditions found in pastures (Sauer 1979; Budowski & Russo 1993; R. A. Zahawi 2004, personal communication from farmers) and their local use as live fencerows. All stakes (excepting Terminalia) were harvested from existing live fencerows within 3 km of study sites and were randomly assigned a site and transported there by truck. Stakes were chosen based on initial diameter, selecting for a range typically used by farmers (Table 1), and any lateral branches were removed. An average of three to four 2-mtall stakes were harvested from each parent tree, which will not die but resprout and produce new (harvestable) branches within 23 years. Terminalia was harvested from a nearby plantation that happened to be cleared at the time this study was started and the species was evaluated as it commonly used in regional reforestation efforts (e.g., Nichols et al. 2001). Stakes were cut a few days before planting to allow the base of each stake to heal over, which is considered a good planting strategy by farmers (R. A. Zahawi, personal communication from farmers). At each site, one stake from each of the 10 species was planted randomly in each row 1.5 m apart creating a 15 3 30m grid (n 20 species per site). Stakes were planted to a depth of 1520 cm by opening a small hole with a stick, and soil was compacted lightly around each stake after planting. All sites were planted between 6 and 21 July 2004. Vegetation was cleared around stakes and seedlings (see below) three to four times per year during the study. Diameter at breast height (dbh) of all stakes was measured at the onset of the study (Table 1); there was no signicant difference in initial dbh among sites overall, nor within a given species among sites (p > 0.05). We recorded whether stakes were dead or alive and calculated canopy area as for a circle (the radius was estimated by measuring the canopy diameter of two perpendicular

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Table 1. Mean initial dbh and range of stakes used in the eld trial (cm) and regional use and natural history traits of the species selected. Mean Initial dbh (Range)

Species

Regional Use

Natural History

Acnistus arborescens (L.) Schltdl. [Solanaceae]

3.75 (6.32.1)

Locally used as a live fencerow and as a substrate for orchids (corky bark)

Bursera simaruba (L.) Sarg. [Burseraceae]

4.48 (9.42.2)

Locally used as a live fencerow

Diphysa americana (Mill.) M. Sousa [Fabaceae] Erythrina berteroana (Urb.) [Fabaceae]

3.13 (5.21.8)

Locally used as a live fencerow Locally used as a live fencerow; used as a shade tree in coffee plantations Dominant live fencerow in area; extensive use as a shade tree in coffee plantations Locally used as a live fencerow Locally used as a live fencerow; used as a shade tree in coffee plantations

3.81 (6.22.4)

E. poeppigiana (Walp.) O. F. Cook [Fabaceae]

5.09 (7.72.9)

Ficus pertusa L. f. [Moraceae]

3.58 (5.92.2)

Gliricidia sepium (Jacq.) Kunth ex Walp. [Fabaceae]

3.65 (6.92.0)

Spathodea campanulata P. Beauv. [Bignoniaceae]

4.65 (72.7)

Locally used as a live fencerow, mostly at higher elevations (1,3001,500 m)

Spondias purpurea L. [Anacardiaceae]

3.57 (5.42.4)

Locally used as a live fencerow

Terminalia amazonia (J. F. Gmel.) Exell [Combretaceae]

a c

3.74 (5.62.3)

Widely planted as seedlings in reforestation projects, not used as a live fencerow

MexicoSouth America; 600 1,500 m; small tree to 10 m, fruit yelloworange berries approximately 1 cm, dispersed by more than 40 species of frugivoresa MexicoColombia, Florida, and Caribbean; 01,100 m; deciduous tree to 25 m, fruit capsule, with a single approximately 1 cm eshy seed; frugivore dispersed (>20 species of birds)a,b,c MexicoPanama; 01,200 m; deciduous tree to 15 m, fruit a legume, indehiscent, wind disperseda,c,d MexicoSouth America; 900 1,300 m; small tree to 8 m, fruit long legume dehiscing red seeds approximately 1 cm, nitrogen xationd,e,f PanamaBolivia (naturalized in Costa Rica); 01,300 m; deciduous tree to 30 m, fruit a legume, seeds brown, nitrogen xationa,d,g MexicoParaguay; 02,000 m; tree to 25 m, fruit a g 12 cm, frugivore dispersedc,e MexicoColumbia; 01,500 m; deciduous small tree to 10 m; fruit a legume, seeds brown approximately 1 cm, dispersal explosive, nitrogen xationa,d Native to tropical West Africa, cultivated throughout neotropics; 1001,500 m; tree to 20 m; fruit a capsule with many wind-dispersed seedsa,c,d,h MexicoSouth America; 01,200 m; tree to 15 m; fruit a eshy drupe approximately 5 cm, animal disperseda,d MexicoSouth America; 501,200 m; tree to 50 m; fruit wind-dispersed samarasi,j

Zuchowski (2005). Trainer and Will (1984). Croat (1978). d Holdridge et al. (1997). e Haber et al. (2000). f Russo (2002). g Garibaldi (2002). h Connor and Francis (2002). i Zamora et al. (2004). j Flores (2002).
b

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axes) and measured dbh annually for 3 years. We measured maximum canopy height at the end of the study. In this article, we refer to stake establishment as those that sprouted in the rst year and survival as established stakes that survived through the remainder of the study. We focus our statistical analyses on the number of live stakes at the end of the study (2007), as this is most relevant for restoration. With the exception of the analysis of number of live stakes, Terminalia (n 1) and Diphysa (n 5) were excluded from all remaining analyses due to high mortality. Standard error values for continuous variables are reported throughout. All analyses were done using JMP 5.1.2 with the exception of log-linear models, which were analyzed using SAS 9.1. Data were log 1 1 normalized when necessary to meet assumptions of normality and homogeneity of variances. We tested the dependence of number of live stakes on site, species, and the site 3 species interaction term using a log-linear model and testing the maximum likelihood ratio. We used a two-way analysis of variance (ANOVA) to test whether initial dbh at the time of planting differed between stakes of species that did/did not survive through the end of the study. Both Erythrina species were also excluded from this analysis due to a lack of mortality (n 6 species evaluated). A number of individuals sprouted basally in the study. Accordingly, a log-linear analysis was used to determine whether basal/apical sprouting (yes/no) varied with respect to site or species; an interaction term was not included due to highly unbalanced data reecting differential species survival. We used two-way ANOVA to determine if site, species, and their interaction affected nal canopy area and height. Relative growth rate (rgr) of dbh was determined (3 years average) based on the formula: rgr [(ln (nal dbh) 2 ln (initial dbh))/(time nal 2 time initial)]. Given that many individuals sprouted basally and the original stake died, only individuals that retained the original stake through the end of the study (apical sprouters) were included in rgr analyses; because of the unbalanced dataset, we did not include an interaction term. For all other analyses, both apical and basal sprouters were included. Last, we calculated correlation coefcients between initial dbh and canopy area of surviving individuals as well as between nal canopy area, nal height, and rgr of dbh.
Seedling/Sapling Versus Stake Comparisons

taken in July 2007. We used two-way ANOVA with interaction terms to determine whether height and canopy area differed by site and planting form (n 57 stakes and 108 saplings).
Seedlings Versus Stakes. In June 2005, we initiated a separate seedling/stake above- and belowground comparative study. Two species, Gliricidia sepium and E. poeppigiana, were chosen based on their establishment success in the eld trial and on seed availability. Seeds for Erythrina were harvested locally, whereas seeds for Gliricidia were obtained from Centro Agronomico Tropical de Investiga n y Ensen anza in Turrialba. Fifteen seedlings and cio 15 stakes (approximately 2 m tall) of each species were planted alternately approximately 1.5 m apart at each of the three eld sites. Due to poor seed germination, Gliricidia seedlings (and accordingly stakes) were planted at two sites only (Santo Domingo and San Gabriel). Stakes were planted directly on site between 9 and 15 June, whereas seeds were planted in small nursery bags in June and then transplanted into the eld on 13 and 14 September 2005 when they measured approximately 30 cm height. Above- and belowground biomass production were harvested between 30 June and 5 July 2006, after 1 year of growth. Due to the labor-intensive nature of harvesting belowground biomass, a random subsample of surviving individuals was chosen (Gliricidia: n 8 seedlings and 10 stakes, Erythrina: n 18 seedlings and 17 stakes). Aboveground biomass was harvested with clippers. For stakes, only growth since planting was collected; for seedlings, the entire stem and all branches were included because the only initial biomass was that of the seed. Belowground biomass was harvested manually with a variety of handheld kitchen and garden implements. Roots for seedlings were entirely harvested; however, it was impossible to extract all stake roots due to the extensive radial network produced. Stake roots were followed laterally until their diameter was less than 2 mm and to approximately 1.5 m depth beyond which all roots were less than 2 mm diameter. Seedling roots did not pass 1 m in depth. All samples were dried at 65C for 2472 hours. Once dry (brittle), excess soil from roots was removed manually before weighing. We used two-way ANOVA to test whether above- and belowground biomass production for each species were affected by site, planting form, and their interaction.

We compared 3-year height and canopy area of surviving individuals of one stake species, Erythrina poeppigiana, with data from saplings of the same species planted as part of another restoration study that was initiated at the same time (June/July 2004) and at the same three sites. No other species were planted in both studies. Erythrina poeppigiana saplings were approximately 20 cm tall at the time of outplanting, and height and canopy measurements of surviving individuals were
Saplings Versus Stakes.

Economic Comparisons

To estimate seedling cost, we used the average purchase price of local nurseries and added the cost of planting, fertilizing, and postplanting maintenance of seedlings over a 2-year period, a typical time period needed for seedlings to overtop grasses. For stakes, we calculated labor hours for harvesting and planting. We also included postplanting eld maintenance, which would be less frequent or not necessary as stakes are unlikely to be shaded by grasses

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due to their initial height advantage. Field estimates were based on labor hours needed to plant the three stake trials (n 200 stakes per site), whereas the seedling cost estimate was determined from a larger restoration study associated with this project (n 400 seedlings per site). We calculated the cost of fuel for transporting stakes or seedlings. Based on our experience, we estimated that a typical pickup truck can carry 1012 times the number of seedlings (300400) as stakes (2030), as the latter must be placed horizontally and cannot be stacked without causing damage to the cortical tissue along the stem. Last, we used a salary of $1 per hour to calculate labor expenses, which is average pay for manual labor in our study area.

Results
Stake Field Trials

Most individuals that established within the rst year survived through the end of the study, with the exception of a few species, notably Gliricidia, Bursera, and Spondias, that suffered ongoing mortality (Fig. 1). The number of live stakes at the end of the study varied signicantly by species, site, and their interaction (Fig. 2; see legend for statistical tests). For both Erythrina species, more than 85% of stakes established and survived after 3 years at all sites, whereas establishment was poor (<30%) at all sites for Acnistus, Diphysa, and Terminalia. Several other species, including Gliricidia, Ficus, Bursera, Spondias, and Spathodea had intermediate survival values that were highly site specic. For example, Gliricidia and Ficus had dramatically more live stakes at Santo Domingo compared to the other sites; Spathodea and Bursera had more

Figure 2. Number of live stakes at year 3 presented as a percentage of the total originally planted and grouped by species and site. All species were planted in July 2004 (n 60 stakes per species). The number of live stakes varied signicantly by species: v2 129.7, df 9, p < 0.0001; site: v2 7.3, df 2, p 0.0265; and species 3 site: v2 56.5, df 18, p < 0.0001.

Figure 1. Number of live stakes at 1, 2, and 3 years presented as a percentage of the total originally planted and grouped by species. All species were planted in July 2004 (n 60 stakes per species).

live stakes at San Gabriel; and Spondias had the largest number of live stakes at Campo Tres. Overall, the number of live stakes was higher at Santo Domingo (55%) than San Gabriel (39%) and Campo Tres (42%), but this effect was swamped by species-specic trends. Stakes of species that established and survived through the end of the study had greater dbh at the time of planting (4.15 0.09 cm) than those that died (3.80 0.07 cm; F 7.5, df 1, p 0.0065); however, a species 3 survival interaction was also found (F 2.3, df 5, p 0.0431) and Acnistus showed the opposite trend. Three species developed fruit by the second year, including Erythrina berteroana (n 5), Ficus (n 2), and Acnistus (n 5). By the third year, the number increased to four species and 46 individuals, including E. berteroana (n 20), Ficus (n 17), Acnistus (n 7), and Gliricidia (n 2). Fruiting occurred predominantly at San Gabriel and Santo Domingo with only two fruiting individuals at Campo Tres. Stake sprouting location varied by species (v2 18.6, df 7, p 0.0097) and by site (v2 9.7, df 2, p 0.0078). Most species sprouted predominantly at the apex (range 6580%), whereas Acnistus was intermediate (50%) and E. berteroana tended to sprout more at the base (42% apex sprouting). Campo Tres had the lowest proportion of apical sprouts (51%), whereas apical sprouting at Santo Domingo (66%) and San Gabriel (73%) was higher. Canopy area, height, and rgr of dbh were all strongly correlated (canopy and height: r 0.79, df 266, p < 0.0001; canopy and rgr: r 0.68, df 166, p < 0.0001; and height and rgr: r 0.75, df 166, p < 0.0001) and,

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therefore, showed similar trends with strong species, site, and species 3 site interactions (Fig. 3; see legend for statistical analyses; only canopy area and height data are shown). Initial stake dbh and nal canopy area were weakly correlated (r 0.13, df 266, p 0.0326). Species can be loosely grouped into those that produced extensive canopies (Erythrina spp. and Spathodea), intermediate canopies (Gliricidia, Ficus, and Acnistus), or small canopies (Spondias and Bursera). Species groupings by height were similar, except that the range of values among species was lower and Acnistus fell into the tallest group. Two of the species with extensive canopy and height development (Erythrina spp.) also had the highest establishment values (Fig. 1) and one (Spathodea) had intermediate establishment. Although only ve individuals of Diphysa

survived (all at Santo Domingo), those that did were very tall (6.15 0.16 m). Overall canopy area, height, and rgr were all lowest at Campo Tres compared to the other sites (canopySanto Domingo: 7.00 0.48, San Gabriel: 6.81 0.63, and Campo Tres: 1.68 0.71 m2; heightSanto Domingo: 4.25 0.12, San Gabriel: 4.43 0.16, and Campo Tres: 2.03 0.19 m), but certain species showed different trends. For example, Spathodea had greater canopy development at San Gabriel, whereas other species (Gliricidia and Ficus) had greater growth at Santo Domingo (Fig. 3a).
Seedling/Sapling Versus Stake Comparisons

Saplings Versus Stakes. In comparing canopy cover of E. poeppigiana stakes and saplings at 3 years, there were strong site and planting form effects (site: F 46.7, df 2, p < 0.0001; planting form: F 9.9, df 1, p 0.002) but no signicant interaction (F < 1, df 2, p > 0.5). Stakes had signicantly greater canopy area (7.80 0.95 m2) than saplings (5.18 0.54 m2). Similarly, there was a strong site effect on height (F 82.6, df 2, p < 0.0001), but there was no planting form effect (F < 1, df 1, p > 0.5) and a weak interaction effect (F 3.26, df 2, p 0.0407); stakes were slightly taller than saplings at San Gabriel, whereas they were statistically equivalent at Campo Tres and Santo Domingo (least squared means [LSmeans] contrasts: p < 0.05). As with the stake eld trials, mean canopy area and height of both saplings and stakes were substantially lower at Campo Tres than the other two sites.

Figure 3. (a) Tree canopy area and (b) height of stakes at year 3 grouped by species and site (mean 1 1 SE). Canopy areaspecies: F 15.8, df 7, p < 0.0001; site: F 34.0, df 2, p < 0.0001; and species 3 site: F 3.3, df 14, p < 0.0001. Heightspecies: F 14.1, df 7, p < 0.0001; site: F 41.2, df 2, p < 0.0001; and species 3 site: F 6.9, df 14, p < 0.0001. For rgr based on dbh (data not shown) species: F 13.0, df 7, p < 0.0001 and site: F 13.1, df 2, p < 0.0001.

Above- and belowground biomass of Gliricidia stakes were more than 50 and 10 times higher, respectively, than for seedlings (F 106.2, df 1, p < 0.0001; F 27.0, df 1, p 0.0001; Fig. 4a). There were no site or site 3 planting form interaction effects on either above- or belowground biomass for Gliricidia (F < 1, df 1, p > 0.3 in all cases). Above- and belowground biomass of E. poeppigiana stakes were 8 and 7 times greater, respectively, than for seedlings (F 31.4, df 2, p < 0.0001; F 39.3, df 2, p 0.0001; Fig. 4b). Aboveground biomass production in E. poeppigiana was signicantly lower at Campo Tres as compared to the other two sites (Santo Domingo: 90.15 37.95, San Gabriel: 116.03 58.60, Campo Tres: 22.99 12.70 g; F 5.4, df 2, p 0.0105), but there was no signicant site effect on belowground biomass (Santo Domingo: 49.87 20.63, San Gabriel: 54.71 18.16, Campo Tres: 25.12 9.51 g; F 1.1, df 2, p 0.3615), although a similar pattern was present. There were no interactions between site and planting form for above- or belowground biomass (F < 1, df 2, p > 0.5 in both cases). Belowground growth form of E. poeppigiana and Gliricidia seedlings and stakes was also dramatically different. Whereas seedlings tended to develop a strong tap root with considerably smaller lateral roots and roots hairs, stakes developed numerous smaller sized roots that would
Seedlings Versus Stakes.

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Figure 4. Above- and belowground biomass production (mean 1 1 SE) for (a) Gliricidia and (b) Erythrina poeppigiana stakes and seedlings at 1 year (Gliricidia: n 8 seedlings and 10 stakes planted at two sites; Erythrina: n 18 seedlings and 17 stakes planted at three sites; ***p  0.0001).

radiate outward in all directions in an adventitious-like growth form (Fig. 5a & 5b). In some cases, stake roots reached more than 6 m in length.
Economic, Logistic, and Ecological Comparisons

Based on our calculations, the use of seedlings costs approximately 210 times more than planting stakes, depending on whether stakes are maintained (Table 2). Harvesting and transporting stakes are more time-consuming than for seedlings, as are transport expenses, if the appropriate species cannot be located nearby. Seedlings, however, are costly to grow or purchase and require more labor during planting and postplanting maintenance. The varied advantages of each planting method are summarized in Table 3.

Figure 5. (a) Above- and belowground biomass of an Erythrina poeppigiana stake (left) and seedling (right) harvested at 1 year. The base of the stake was not included in the belowground biomass estimate. A machete and pocketknife are shown for scale and (b) excavation of an E. poeppigiana at 1 year, necessitating root excavation in all directions.

Discussion
Stake Establishment and Growth

Our results strongly conrm an extensive body of agricultural literature (e.g., Sauer 1979; Budowski 1987;

Budowski & Russo 1993; Messenger et al. 1997), and a few previous restoration studies (Perino 1979; Hunter 1987; Zahawi 2005), indicating that a number of tree species can be successfully established as large (approximately 2 m tall) stakes in the tropics making tree stakes a promising restoration tool. Clearly, a range of factors needs to be considered in selecting appropriate species for

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Table 2. Cost estimate (U.S. $) to establish seedlings and stakes per 100 individuals. Task Stakes Seedlings

Harvesting and/or transfer to worksite Nursery cost Transport expense (fuel 010 km) Planting Fertilizer/insecticide application Postplanting eld maintenance Total estimate

$1216 * $03 $67.50 $040 $1866.50

$1.502 $1525 $0.25 $2025 $010 $80120 $116.75182.25

* Of the 10 species used in this study, only 1 was purchased as it was difcult to nd in large numbers (Diphysa). Purchase price was equivalent to seedlings (Budowski 1987). In most cases, farmers use what is plentiful (e.g., Erythrina) and is hence free of charge.

restoration including establishment and survival, growth variables, as well as a given species habitat value and effect on long-term successional processes (Harvey et al. 2005; Zahawi & Augspurger 2006). Whereas a number of species established well in this study, several grew slowly (e.g., Bursera). Others showed a dramatic increase in growth and canopy development by the second and third year, which will likely attract frugivores more rapidly than slower growing species by simply creating more vegetation structure or habitat and thereby increasing visitation (Harvey et al. 2005; Zahawi & Augspurger 2006). Greater canopy area also facilitates the establishment of seedlings directly by ameliorating microclimatic extremes and by

reducing competition with aggressive shade-intolerant grasses (reviewed in Holl 2002). Last, four species developed fruit by the end of the study including two (Acnistus and Ficus) that may attract a broad range of frugivores (e.g., Scott & Martin 1984; Guevara & Laborde 1993; lez et al. 2000; Luck & Daily 2003). This is Galindo-Gonza especially important to accelerating restoration as lack of zoochorous seed dispersal is often a key limiting factor a & Aide 2001). (e.g., Holl 1999; Cubin The given suite of species suitable for use at a particular location will vary over various spatial scales and eld trials to determine appropriate species should be considered prior to initiating large-scale restoration projects. For example, Zahawi (2005) found Gliricidia to be an excellent candidate in northern lowland Honduras; however, establishment and growth of Gliricidia were comparatively poor in the current study as well as in an earlier study in the area (Nichols et al. 2001). It appears that the viability of a given species in a region is largely dependent on climatic and geographic factors, such as the duration and severity of the dry season, site elevation, and soil characteristics such as drainage (Sauer 1979; Budowski & Russo 1993; Zahawi 2005). In this study, we found strong site-specic differences in growth and apical versus basal sprouting even on a small scale. The slower growth variables and higher basal sprouting recorded at Campo Tres may have been due to the extensive use of this site as a cattle pasture (>30 years), which has led to signicant soil erosion such as cattle ruts and loss of topsoil (R. A. Zahawi 2004, personal observation), and likely increased soil compaction which can impede root growth and drainage (e.g., Holl 1999; Zahawi & Augspurger 2006); similarly, saplings of all four

Table 3. Economic, logistical, and ecological advantages of planting species as seedlings or stakes in tropical forest restoration efforts. Seedlings Stakes

Economic Logistical Transportation of seeds and seedlings easier, unless stakes of desired species are located nearby Easier to transport to areas distant from roadways Generally easier to obtain large numbers but will vary depending on location and timing

Cost of planting and maintaining is lower; can be substantial for larger restoration projects No space and equipment needed for nursery setup Less advance preparation needed (can be acquired just before planting) Stakes of a few species almost always available; many tree species do not set seed annually and germination is highly variable More rapid planting in the eld May require less postplanting site maintenance Greater early above- and belowground growth, which likely results in higher seed rain and improved erosion control More rapid fruit production in some species

Ecological

Wider range of species can establish as seedlings and be used in restoration, including many valuable timber species Potentially higher genetic variability, depending on seed source

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species planted as part of our related restoration study have shown much lower growth rates at Campo Tres (Holl and Zahawi 2006, unpublished data). Differences in the number of live stakes at the three sites are more difcult to explain as they are largely species specic and highlight the need for eld trials at multiple sites. The initial dbh of stakes also affects their establishment and growth; with the apparent exception of Acnistus, larger diameter stakes had a greater probability of establishing, suggesting that stake diameter should be considered in restoration projects (Zahawi 2005; this study). There are, however, tradeoffs, as using larger diameter stakes increases transport costs, especially over large distances.
Comparison of Seedlings/Saplings and Stakes for Restoration

Both planting methods present distinct advantages, which should be carefully considered when selecting how to propagate a given species. Clearly, stakes grow much faster in the rst year, outpacing seedlings in above- and belowground biomass production by 750 times in the species studied. Stake versus seedling comparisons of other species and in other regions are needed to conrm whether this trend is consistent. Although this dramatic difference will likely change as seedlings develop and their growth rate increases, our results suggest that in the short term, stakes provide a more rapid way of developing vegetation structure in a degraded site and this appears to be the case for Erythrina poeppigiana even 3 years after planting. This rapid development, likely driven by the greater biomass reserve of stakes, should in turn accelerate the rate of forest recovery at a given site as compared to planting seedlings (e.g., greater seed rain). Moreover, the more extensive and adventitious-like growth form of stake roots suggest that they may provide rapid erosion control, particularly on steep, erosion-prone slopes (Nabhan & Sheridan 1977; Perino 1979). From an economic perspective, our calculations suggest that planting seedlings costs 210 times more than stakes and requires propagation facilities or a supplier for seedlings. Although maintenance was included in the stake cost estimate, it is not necessary in many cases, as the 2 m height advantage likely provides a sufcient competitive edge against shorter pasture grasses. Even if maintenance is retained in the estimate, the overall economic difference is still considerable, especially considering the large scale of tropical forest restoration projects that are currently being undertaken or proposed (Lamb et al. 2005). Although there are clear advantages to using stakes, harvesting and transporting stakes to a planting site is slow, and labor intensive when nearby sources are not available. Transport also needs to be done with great care as it is easy to damage the cortex of some species during transport (bruising along the length of the stake), which can affect sprouting and decrease the probability of establishment (R. A. Zahawi, personal observation). Moreover, a much wider range of species can be propagated as seed-

lings, although more species may establish vegetatively than are commonly used in agricultural practice (Sauer 1979; Budowski & Russo 1993), necessitating further eld trials of promising nonagricultural tree species. Last, extensive use of stakes may result in reduced genetic variability, although drawing plants from numerous sources is an important consideration regardless of propagation method. Logistical constraints, such as the availability of propagules, must also be considered regardless of propagation method. When seeds are available, they can be collected in large numbers and much more quickly than stakes. But, interannual variability in seed set is notoriously high in the tropics, which can delay restoration efforts especially in regions with strong seasonality. Seed viability is also an issue for many tropical species and can often be very low. In contrast, most areas in the tropics have at least two to three species widely planted as live fencerows, so that stakes are almost always available. A few studies have evaluated the use of smaller cuttings (1520 cm) as an alternative to seeding (e.g., Aide & Cavelier 1994; Ray & Brown 1995; Bonl-Sanders et al. 2007). Although the technique is important in the absence of seed availability, and it is easier to acquire large numbers of small cuttings, the ecological advantages of using larger vegetative stakes, such as greater initial biomass production and height, are lost. Given the numerous tradeoffs, using a combination of the two propagation methods is likely to yield the highest success in most cases (Nichols et al. 2001). Stakes may provide more rapid canopy development and erosion control, whereas planting a wider range of species will enhance biodiversity and ecosystem services (Lamb et al. 2005; Erskine et al. 2006). Regardless of the method used careful consideration should be given to the effect of the planted species on long-term vegetation dynamics because in the vast majority of tropical restoration efforts, a small subset of species are planted to overcome obstacles to forest recovery (e.g., lack of seed dispersal, competition with pasture grasses) and facilitate the establishment of a diverse tropical forest community (reviewed in Holl 2002).

Implications for Practice d Our results suggest that stakes should be more widely used as a tool for tropical forest restoration as they: (1) more rapidly develop both above- and belowground biomass than seedlings, (2) do not require nursery facilities for propagation, and (3) are less costly to propagate, plant, and maintain than seedlings. d However, because only certain species can be propagated as stakes and they are more challenging to transport, a mix of both approaches is recommended to facilitate recovery of tropical forests in abandoned agricultural lands.

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Acknowledgments We would like to thank our onsite manager J. A. Rosales for assistance in the eld and for project oversight in our absence. Many thanks to our numerous eld assistants who helped on this project; they include local assistants, Earthwatch volunteers, and several undergraduate students. Special thanks to H. Cringan and R. Cole for excellent eld assistance and for motivating volunteers during root excavations. Support for this project was provided by grants from the National Science Foundation (DEB 0515577), Earthwatch Institute, and the Organization for Tropical Studies.

LITERATURE CITED
Aide, T. M., and J. Cavelier. 1994. Barriers to lowland tropical forest restoration in the Sierra Nevada de Santa Marta, Colombia. Restoration Ecology 2:219229. nchez-Azofeifa, B. Rivard, J. C. Calvo, and Arroyo-Mora, J. P., G. A. Sa D. H. Janzen. 2005. Dynamics in landscape structure and composition for the Chorotega region, Costa Rica from 1960 to 2000. Agriculture Ecosystems and Environment 106:2739. ndez, and J. A. Ulloa-Nieto. Bonl-Sanders, C., P. E. Mendoza-Herna n de callos en estacas de siete espe2007. Enraizamiento y formacio nero Bursera. Agrociencia 41:103109. cies del ge Budowski, G. 1987. Living fences in tropical America, a widespread agroforestry practice. Pages 169178 in H. L. Gholz, editor. Agroforestry: realities, possibilities, and potentials. Martinus Nijhoff, Dordrecht, The Netherlands. Budowski, G., and R. O. Russo. 1993. Live fence posts in Costa Rica: a compilation of the farmers beliefs and technologies. Journal of Sustainable Agriculture 3:6587. Buttereld, R. P. 1995. Promoting biodiversity: advances in evaluating native species for reforestation. Forest Ecology and Management 75:111121. Carpenter, F. L., J. D. Nichols, and E. Sandi. 2004. Early growth of native and exotic trees planted on degraded tropical pasture. Forest Ecology and Management 196:367378. Connor, K. F., and J. K. Francis. 2002. Spathodea campanulata P. Beauv. Pages 716718 in J. A. Vozzo, editor. Tropical tree seed manual. U.S. Department of Agriculture Forest Service, Washington, D.C. Croat, T. B. 1978. Flora of Barro Colorado Island. Stanford University Press, Stanford, California. a, A., and T. M. Aide. 2001. The effect of distance from forest edge Cubin on seed rain and soil seed bank in a tropical pasture. Biotropica 33: 260267. Daily, G. C., P. R. Ehrlich, and G. A. Sanchez-Azofeifa. 2001. Countryside biogeography: use of human-dominated habitats by the avifauna of southern Costa Rica. Ecological Applications 11:113. Erskine, P. D., D. Lamb, and M. Bristow. 2006. Tree species diversity and ecosystem function: can tropical multi-species plantations generate greater productivity? Forest Ecology and Management 233:205210. Estrada, A., R. Coates-Estrada, and D. Merritt Jr. 1997. Anthropogenic landscape changes and avian diversity at Los Tuxtlas, Mexico. Biodiversity and Conservation 6:1943. FAO (Food and Agriculture Organization). 2004. Food and Agriculture Organization of the United Nations. Statistical country prole Costa Rica. Rome, Italy. FAO (Food and Agriculture Organization). 2005. Food and Agriculture Organization of the United Nations. State of the worlds forests. 6th edition. Rome, Italy. Ferguson, B. G. 1995. Surmounting barriers to succession in a degraded tropical pasture. M.S. thesis. University of Michigan, Ann Arbor.

Flores, E. M. 2002. Terminalia amazonia (J.F. Gmel.) Exell. Pages 748751 in J. A. Vozzo, editor. Tropical tree seed manual. U.S. Department of Agriculture Forest Service, Washington, D.C. lez, J., S. Guevara, and V. J. Sosa. 2000. Bat- and bird-genGalindo-Gonza erated seed rains at isolated trees in pastures in a tropical rainforest. Conservation Biology 14:16931703. Garibaldi, C. 2002. Erythrina poeppigiana (Walp.) O.F. Cook. Pages 461463 in J. A. Vozzo, editor. Tropical tree seed manual. U.S. Department of Agriculture Forest Service, Washington, D.C. Guariguata, M. R., R. Rheingans, and F. Montagnini. 1995. Early woody invasion under tree plantations in Costa Ricaimplications for forest restoration. Restoration Ecology 3:252260. Guevara, S., and J. Laborde. 1993. Monitoring seed dispersal at isolated standing trees in tropical pastures: consequences for local species availability. Vegetatio 107/108:319338. Haber, W. B., W. Zuchowski, and E. Bello. 2000. An introduction to cloud forest trees: Monteverde, Costa Rica. 2nd edition. Mountain Gem Publications, Monteverde, Costa Rica. Haggar, J., K. Wightman, and R. Fisher. 1997. The potential to foster woody regeneration within a deforested landscape in lowland Costa Rica. Forest Ecology and Management 99:5564. s, M. Chaco n, D. Mun oz, M. Harvey, C. A., C. Villanueva, J. Villac pez, et al. 2005. Contribution of live fences to the ecological Lo integrity of agricultural landscapes. Agriculture, Ecosystems and Environment 111:200230. Holdridge, L. R., W. C. Grenke, W. H. Hatheway, T. Liany, and J. A. Tosi Jr. 1971. Forest environments in tropical life zones. Pergamon Press, New York. nez. 1997. Arboles de Costa Holdridge, L. R., L. J. Poveda, and Q. Jime co Tropical, San Jose , Costa Rica, vol. 1. 2nd edition. Centro Cient Rica. Holl, K. D. 1999. Factors limiting tropical rain forest regeneration in abandoned pasture: seed rain, seed germination, microclimate, and soil. Biotropica 31:229242. Holl, K. D. 2002. Tropical moist forest restoration. Pages 539558 in A. J. Davy and M. Perrow, editors. Handbook of ecological restoration. Vol. II. Cambridge University Press, Cambridge, United Kingdom. Holl, K. D., and E. Quiros Nietzen. 1999. The effect of rabbit herbivory on reforestation of an abandoned pasture in southern Costa Rica. Biological Conservation 87:391395. Hunter, R. J. 1987. Reforestation with Bombacopsis quinatum (Jacq.) Dugand (Bombaceae) in Costa Rica by means of vegetative reproa Tropical 35:195201. duction. Revista de Biolog Kolb, S. R. 1993. Islands of secondary vegetation in degraded pastures of Brazil: their role in reestablishing Atlantic coastal forest. Ph.D. dissertation. University of Georgia, Athens. Lamb, D. 1998. Large-scale restoration of degraded tropical forest lands: the potential role of timber plantations. Restoration Ecology 6: 271279. Lamb, D., P. D. Erskine, and J. A. Parrotta. 2005. Restoration of degraded tropical forest landscapes. Science 310:16281632. Luck, G. W., and G. C. Daily. 2003. Tropical countryside bird assemblages: richness, composition, and foraging differ by landscape context. Ecological Applications 13:235247. Messenger, A. S., J. F. Di Stefano, and L. A. Fournier. 1997. Rooting and growth of cuttings of Bursera simaruba, Gliricidia sepium, and Spondias purpurea in upland stony, upland non-stony and lowland nonstony soils in Ciudad Colon, Costa Rica. Journal of Sustainable Forestry 5:139151. Nabhan, G. P., and T. E. Sheridan. 1977. Living fencerows of the rio San Miguel. Sonora, Mexico: traditional technology for oodplain management. Human Ecology 5:97111. Nepstad, D. C., C. Uhl, C. A. Pereira, and J. M. C. Da Silva. 1996. A comparative study of tree establishment in abandoned pasture and mature forest of eastern Amazonia. Oikos 76:2539.

NOVEMBER 2009

Restoration Ecology

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Live Fences and Seedlings in Restoration

Nichols, J. D., M. E. Rosemeyer, F. L. Carpenter, and J. Kettler. 2001. Intercropping legume trees with native timber trees rapidly restores cover to eroded tropical pasture without fertilization. Forest Ecology and Management 152:195209. OED (Operations Evaluation Department). 2000. Costa Rica: forest strategy and the evolution of land use. The World Bank, Washington, D.C. Perino, J. M. 1979. Rehabilitation of a denuded watershed through the introduction of kakawate (Gliricidia sepium). Sylvatrop 4:4968. Ray, G. J., and B. J. Brown. 1995. Restoring Caribbean dry forests: evaluation of tree propagation techniques. Restoration Ecology 3:8694. Rickert, E. 2005. Environmental effects of the coffee crisis: a case study of land use and avian communities in Agua Buena, Costa Rica. M.S. thesis. Evergreen State College, Olympia, Washington, D.C. Russo, R. O. 2002. Erythrina berteroana (Urb.). Pages 452454 in J. A. Vozzo, editor. Tropical tree seed manual. U.S. Department of Agriculture Forest Service, Washington, D.C. nchez-Azofeifa, G. A., G. C. Daily, A. S. P. Pfaff, and C. Busch. 2003. Sa Integrity and isolation of Costa Ricas national parks and biological reserves: examining the dynamics of land-cover change. Biological Conservation 109:123135.

Sauer, J. D. 1979. Living fences in Costa Rican agriculture. Turrialba 29: 255261. Scott, P. E., and R. F. Martin. 1984. Avian consumers of Bursera, Ficus, n. Biotropica 16:319323. and Ehretia fruit in Yucata Trainer, J. M., and T. C. Will. 1984. Avian methods of feeding on Bursera simaruba (Burseraceae) fruits in Panama. Auk 101:193195. Zahawi, R. A. 2003. Island biogeography and restoration: the role of living fence islands as regeneration foci in the rehabilitation of degraded lands in Honduras. Ph.D. dissertation. University of Illinois, Urbana. Zahawi, R. A. 2005. Establishment and growth of living fence species: a overlooked tool for the restoration of degraded areas in the tropics. Restoration Ecology 13:92102. Zahawi, R. A., and C. K. Augspurger. 2006. Tropical forest restoration: tree islands as recruitment foci in degraded lands of Honduras. Ecological Applications 16:464478. rboles de Costa Rica, nez, and J. Poveda. 2004. A Zamora, N., Q. Jime co Tropical, San Jose , Costa Rica. vol. 3. Centro Cient Zuchowski, W. 2005. A guide to tropical plants of Costa Rica. Ditribuidores Zona Tropical, Miami, Florida.

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Restoration Ecology

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