Seedling survival patterns in Macaronesian laurel forest: a long-termstudy in Tenerife (Canary Islands)

S. Fernandez-Lugo1*, L. de Nascimento1, J. Mendez1, G. Gonzalez-Delgado1, E. P. C. Gomes2, R. Otto1, J. R. Arevalo1

and J. M. Fernandez-Palacios1

1Island Ecology and Biogeography Group, Instituto Universitario de Enfermedades Tropicales y Salud Publica de Canarias (IUETSPC),Universidad de La Laguna (ULL), Avda. Astrofısico Francisco Sanchez s/n, 38206 La Laguna, Tenerife, Spain

2Instituto de Botanica, Governo do Estado de Sao Paulo, Av. Miguel Stefano, 3687, Agua Funda, 04301-902 Sao Paulo/SP, Brazil

*Corresponding author. Tel: +34 649359796; E-mail: sfdezlu@ull.es

Received 2 June 2014

Seedling dynamics of the Macaronesian laurel forest have been monitored for the first time in a long-term study todetermine whether the survival of the seedling community is affected by slope aspect and forest structure. Morethan 4000 seedlings were monitored monthly from 2000 to 2003 in well-preserved laurel forest stands on Tenerife,Canary Islands. Trees and seedling bank species composition differed between windward and leeward slopes. Onboth slopes, differences in species composition between the canopy and the seedling bank suggest future shifts incanopy species composition towards a more advanced successional stage. Surprisingly, seedling survival washigher on the drier leeward than on the wetter windward slope. This seems to be related to environmental andstructural differences of the forest stand between slope aspects (e.g. larger trees, higher canopy cover and treedensity and lower light penetration in windward plots). Analysed species have long-lived seedling banks with sur-vival rates of 12 per cent and 5 per cent in the long term (12 years) for leeward and windward slopes, respectively,with significant differences among species. This result reflects the high regeneration potential of the forest in well-preserved stands, indicating that no management interventions are required to ensure the regeneration of thisendemic forest.

Introduction

The evergreen laurel forests of the Macaronesian Region are of ex-ceptional conservation importance due to their high species diver-sity and endemism. This vegetal formation is considered to be arelict of the subtropical North Tethyan forest, which was the dom-inant forest type in Central and Southern Europe, as well as inNorthern Africa, during the Tertiary, lasting until the final deterior-ation in the climate that reached its zenith at the onset of thePleistocene Glaciations (Mai, 1991; Postigo Mijarra et al., 2009;Fernandez-Palacios et al., 2011). The cooling trend that started inthe upper Tertiary made this ecosystem shift to the west where itfound refuge in the Atlantic islands (Azores, Canary Islands andMadeira) thanks to their stable and moderate oceanic climate.After the subsequent appearance of the drier Mediterraneanclimate, some 3 million years ago, the laurel forest was able towithstand the summer drought of this climate type due to the pres-ence of the trade winds that generate orographic cloud layers onMacaronesian islands. This forest grows on windward slopes indeep soils at altitudes of between 500 and 1500 m a.s.l. (Guimar-aes and Olmeda, 2008).

The floristic composition of the forest is dominated by perennialbroadleaf lauriphyllous trees, among which stand ancient endemicspecies (palaeoendemic species), such as trees of the genus

Persea, Ocotea and Picconia, which have barely evolved sincetheir arrival on the islands (Humphries, 1979; Guimaraes andOlmeda, 2008). The most representative family is the Lauraceae,with four genera and five species (Apollonias barbujana (Cav.)Bornm., Laurus novocanariensis Rivas-Mart., Lousa, Fern. Prieto,E. Dıas, J.C. Costa & C. Aguiar, L. azorica (Seub.) Franco, Ocoteafoetens (Aiton) Baill. and Persea indica C. K. Spreng.), although it isa plurispecific formation where other trees from several familiesare also present (e.g. Aquifoliaceae, Caprifoliaceae, Ericaceae,Myricaceae, Myrsinaceae, Oleaceae, Rhamnaceae, Rosaceae,Theaceae) (for more detailed information see del Arco et al.,2010). However, different species may be dominant dependingon site conditions, e.g. Erica platycodon (Webb & Berthel.) Rivas-Mart. & al. dominates on forest ridges, L. novocanariensis inmesic zones and Erica arborea L. in more disturbed areas.

In the Canary Islands, the laurel forest has been extensivelyexploited since the arrival of the early Castilian settlers in the fif-teenth century (Parsons, 1981), and nowadays, only 11.8 percent (10 181 ha) of the laurel forest remains (del Arco et al.,2010), of which 85 per cent is included in the Canarian Networkof Protected Areas and up to 92 per cent within the Natura 2000European Union Network (Guimaraes and Olmeda, 2008).The rele-vance of this ecosystem and the concern about its conservationstatus has led to an extensive bibliography on its ecology, with

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particular emphasis on natural forest regeneration (e.g. Arevaloand Fernandez-Palacios, 1998, 2000, 2003, 2007; Fernandez-Palacios and Arevalo, 1998; Arevalo et al., 1999, 2007, 2008,2011, 2012; Fernandez-Palacios et al., 2004). These studies haverevealed well-defined ecological groups. There are pioneerspecies, which are shade intolerant species that rely on an abun-dant seed bank (E. arborea and E. platyocodon), with Morella faya(Aiton) Wilbur being able to persist under a closed canopy due toits ability to produce suckers (persistent-pioneer species). Matureshade tolerant species are also present, which can be itinerant(Heberdenia excelsa (Aiton) Banks ex DC., Picconia excelsa (Aiton)DC., Rhamnus glandulosa Aiton and Viburnum rigidum Vent.),relying entirely on the seedling bank, persistent species (Ilex canar-iensis Poir., Ilex perado Aiton and Prunus lusitanica L.), relyingmainly on asexual reproduction, and facultative ones (Lauraceae),relying on both seedlings and suckers (Fernandez-Palacios andArevalo, 1998;Fernandez-Palacios et al., 2004;Fernandez-Palacios,2009).

Additionally, there are some studies that stress the importanceof the invertebrate herbivore community in this humid ecosystem(Ribeiro et al., 2005; Rodrıguez-Rodrıguez and Valido, 2011), point-ing to the possible negative effects of the endemic slug, Plutonialamarkii (A. Ferussac, 1821) on seedling survival (Runnquist,2005). However, the group that might affect plant regenerationof the laurel forest most could be mammals that were introducedinto the islands. These have been shown to negatively affect otherCanarian ecosystems (Irl et al., 2012). In the laurel forest, twospecies of introduced mammals can be found: rabbits and rats.The former are less abundant and almost absent in the best pre-served areas of this ecosystem (Fernandez, 2003), while thelatter are very common and eat plant matter as an importantpart of their omnivorous diet. It has been proven that rats cancause intense defoliation, debark certain species and predate ona high diversity of fruits and seeds in the laurel forest (see Travesetet al., 2009 and references therein). A decrease in tree recruitmenttrough seedling predation cannot be ruled out, as this occurs inother ecosystems (Campbell and Atkinson, 2002).

The structure and species composition of the forest dependconsiderably on the reproductive abilities of the tree species thatmake up its canopy. Seed dispersal and seedling establishmentare important constraints in plant population dynamics (Rey andAlcantara, 2000; Garcıa, 2001), thus processes occurring at theseedling level, the most vulnerable stage in the life of a plantspecies, have a major impact on natural regeneration of theforest (Peterken, 1996; Kitajima, 2007). However, although seed-lings play a key role in the canopy replacement process (Woods,1984; Silvertown and Lovett Doust, 1993), our knowledge of thefactors that influence the survival of the seedling community isstill very limited.

This paper represents the first long-term (12 years) monitoringof the laurel forest seedling bank in the Canary Islands, and in thewhole Macaronesian Region. Our aim is to offer some insights intothis topic, which is crucial for the sustainable management andpersistence of this unique forest. We not only examine the seedlingbank, but also the structure and composition of the canopy layer intwo laurel forest stands (windward and leeward). We hypothesizethat slope aspect is a decisive factor in determining the survival ofthe seedling community, since it can affect the structure anddynamic of the forest stands (Arevalo and Fernandez-Palacios,2000; Arevalo et al., 2007, 2012), specifically it was tested

whether windward slopes, directly exposed to trade winds actionand thus more humid, would show better seedling survival com-pared with drier leeward slopes. We also hypothesize that the re-cruitment of the species will be mainly determined by theirreproductive strategies, with those species relying more on asexualreproduction (e.g. Lauraceae, Ilex spp., P. lusitanica; Fernandez-Palacios and Arevalo, 1998) showing the lowest survival rates.

Materials and methods

Study site

The study was undertaken in the Anaga Rural Park, which is located in thenorth-eastern corner of the island of Tenerife, Canary Islands (28819′N,16834′W) (Figure 1). The park encompasses a 728 million-year-old basalticmassif (Ancochea et al., 1990) that covers a total of 14 224 ha, spans analtitudinal range from sea level to 1024 m a.s.l. (Cruz de Taborno) and repre-sents 7 per cent of Tenerife’s total surface area. The park is characterized bya complex topography dominated by ravines, valleys and cliffs and a centralridge running northeast to southwest, which results in well-defined nor-thern and southern slopes (Morales and Perez, 2000). The soils have beenclassified in the order Entisol, suborder Orthens (Fernandez-Caldas et al.,1982). The climate is influenced by the trade winds, which produce a ‘seaof clouds’ on the windward slopes and wetter conditions on the northernthan on the southern slopes (del Arco et al., 2010). The annual precipitationof the park reaches 900 mm but can be twice this amount if fog drip isincluded (Kammer, 1974). The mean annual temperature is close to 158Cwith minimal annual and daily fluctuations and no frost events.

The Park encompasses the best preserved laurel forest remnants andthe most biodiverse area of the island. In the laurel forest of Anaga, thereare a total of 19 tree species (Santos, 1990), with L. novocanariensis,E. platycodon, E. arborea, I. canariensis, P. lusitanica, M. faya and V. rigidumbeingthedominantspecies.Theforestunderstorey iscomposedofseedlings,saplings and suckers of tree species, and ferns (Woodwardia sp., Dryopterisspp., Diplazium sp.), with endemic shrubs and forbs (Canarina sp., Sideritisspp., Pericallis spp., Geranium sp., Isoplexis sp.) being only present in themost open areas (Fernandez-Palacios, 2009). Although the forest hasonly been officially protected since 1988, aerial photographs show thatthe extent, structure and canopy cover of the forest has not experienceddrastic changes since 1952 (Arevalo and Fernandez-Palacios, 2000), infact abandonment of agricultural land, environmental protection and res-toration programs are helping its restoration and expansion. Nowadays, thelaurel forest experiences almost no direct human disturbance (e.g. grazing,agriculture, logging), although it might experience some indirect effectssuch as those of introduced species and global warming (Sperling et al.,2004), with wildfires being exceptional due to the wet and cloudy natureof this forest (Hollermann, 2000). On the other hand, natural disturbancessuch as heavy winds can occur from specific events, such as the tropicalstorm that affected the islands in 2005 (Gonzalez et al., 2006).

Sampling designIn the year 2000, we selected three study sites, representing well-preservedlaurel forest stands, ‘El Moquinal’ and ‘Barranco de los Nunez’ on the wind-ward slopes (6852820 m a.s.l.) and ‘Monte de Aguirre’ on the leewardslopes (6302920 m a.s.l.) (Figure 1). Study sites consisted of homogeneousforest stands of �2–3 ha, where three randomly located permanent10×10 m plots were established. Study stations, number and size of theplots, were based on previous studies carried out in the area (e.g. Arevaloand Fernandez-Palacios, 2000, 2003; Arevalo et al., 2007, 2012). Eachplot was marked with iron bars at the corners and these points weregeo-referenced with fixed UTM coordinates to record data with a highdegree of precision and minimal amount of sampling error. In total, therewere three leeward plots and six windward plots.

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Starting in winter 2000, within each plot, emerging seedlings were per-manently tagged by tying a plastic label to the stem and mapped using aCartesian coordinate system. Each seedling received an X and a Y value de-pending on its distance to a reference point (the north corner of the plot).

The seedling bank was monitored every month and seedling establish-ment and death date were recorded. Seedling height, number of leavesand vitality index (five-point scale: 1¼ death, 2¼ greater than 75 percent, 3¼ 50–75 per cent; 4¼ 25–50 per cent; and 5¼ less than 25 percent of the leaves damaged) were also assessed monthly for each seedling.At the plot level, we also recorded the following abiotic and biotic para-meters: altitude (m a.s.l.), slope (degrees), diameter at breast height (DBHin cm for each individual tree, i.e. individuals taller than 1.30 m with aDBH of at least 1 cm), total basal area (m2 ha21), basal area of trees witha DBH . 20 cm (m2 ha21), which are the ones contributing most to thecanopy, tree density (individuals m22), seedling density (seedling m22),canopy height (m; using a clinometer and measuring the closest trees toeach plot corner and the plot centre, i.e. five measures per plot) andcanopy cover (per cent using a spherical densitometer and measuring ineach plot corner and in the plot centre, i.e. five measurements per plot).Additionally, we measured the percentage of light above the vegetationthat reached the ground surface. Percentage of light penetration was mea-sured using a point quantum sensor, at 1.30 m height in each corner,halfway along each side, and in the plot centre (i.e. nine measures perplot) to cope with spatial variation in light and obtain a value of theamount of light reaching the understorey. Additionally, two measures

were taken outside the canopy at 1.30 m height on the roads or pathsnearest to each plot to evaluate the amount of light that might reach theunderstorey in the absence of canopy cover. Sampling was carried outmonthly from 2000 to 2003, and the last assessment of seedling bank sur-vivorship was in November 2011 for the windward plots and April 2013 forthe leeward plots.

Statistical analyses

To ensure that selected study stations, both leeward and windward, werecomparable in terms of tree species composition, we used themultiple-response permutation procedure (MRPP) in PC-Ord statisticalpackage (version 6; MjM Software, Gleneden Beach, Oregon). RelativeSørensen (Bray–Curtis) was used as a distance measure because it takesinto account both composition (presence–absence of species) and abun-dance (basal area values). P-values (P , 0.05) were obtained with 999permutations.

Differences in structure of the study stations (altitude, slope, total basalarea, basal area (DBH . 20 cm), tree density, number of tree species, seed-ling density, sapling density, seedling height, annual height increment,numberof seedling species, canopy height and light penetration) were ana-lyzed using a one-way distance-based permutational analysis of variance(ANOVA) (Anderson et al., 2008). The analyses were based on similarity ma-trices computed using Euclidean distances on untransformed data. Statis-tical significance was assessed using 999 permutations and corrected with

Figure 1 Maps of (a) the Canary Islands, (b) Tenerife Island and Anaga Rural Park, showing the study area and (c) aerial photo with the location of thedifferent study stations (GRAFCAN, 2013).

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Monte Carlo correction where necessary (i.e. when the number ofpermutations was lower than 50). Primer 6 and Permanova+ (PRIMER-ELtd, Plymouth, UK) were used to perform all PERMANOVA statisticalprocedures.

Survival curves of seedlings were estimated using Kaplan–Meier’smethod (Kaplan and Meier, 1958). Survival time was calculated as thenumber of months between the first census record for a seedling and thedate when it was recorded as dead. Seedlings still alive at the final censuswere coded as right-censored. Independent analyses were run for: (1) thewhole-seedling bank, using slope aspect (windward vs leeward) as afactor; (2) each species seedling bank, using slope aspect as a factor; and(3) the whole-seedling bank grouped by aspect, using species as a factor.Species with ,20 recorded seedlings in any aspect were excluded fromthe analyses, thus five seedling species were included and six excluded(Table 1). Differences in the shapes of curves among aspect and specieswere tested by the log-rank test (Pyke and Thompson, 1986). Survivalcurves were built for the period 200022003, since a monitoring gapexists from 2003 to 201122013. Thus, the percentage of seedling surviv-ing up to 201122013 was compared using a one-way distance-basedpermutational ANOVA. To identify which biotic factors were most in-fluential on seedling survival, the Cox’s proportional hazard regressionnon-parametric test (Cox, 1972) was carried out with stepwise selectionof variables. Seven variables were used in the model: initial numberof leaves, height and vitality index, as well as growth rate (averagemonthly height increment) as time-independent covariates, final numberof leaves, height and vitality index (previous values to the month inwhich at least one seedling was recorded as dead) as time-dependentcovariates. Analyses were carried out using SPSS statistical package(version 12.0; SPSS Inc., Chicago, IL). Survival graphs were performedusing MedCalc for Windows (version 14.8.1, MedCalc Software, Ostend,Belgium).

ResultsWe monitored a total of 4427 seedlings during the study period,2951 seedlings in the windward plots and 1474 in the leewardplots. Dominant seedling species were L. novocanariensis (1633),P. indica (775) and P. excelsa (466) on the windward, and A. barbu-jana (663), L. novocanariensis (421) and V. rigidum (155) on theleeward slopes (Table 1). The main canopy species contributingto the basal area of the stands were E. arborea (10.82 m2 ha21),L. novocanariensis (8.78 m2 ha21) and I. perado (6.51 m2 ha21) inthe windward, and L. novocanariensis (13.32 m2 ha21), I. canariensis(8.04 m2 ha21) and M. faya (6.00 m2 ha21) in the leeward plots(Table 1).

Tree species composition differed significantly between thestudy stations located on the windward (‘El Moquinal’ and‘Barranco de los Nunez’) and on the leeward slopes (‘Monte deAguirre’) (MRPP, P , 0.05). Consequently, survival analyses wererun separately for both aspects. The PERMANOVA procedure alsorevealed some structural differences between windward andleeward plots, with leeward plots having higher slope and higherlight penetration, and windward ones having higher basal area(DBH . 20 cm), higher tree density, and higher canopy cover(Table 2). Although not significant, a tendency for taller trees onwindward slopes was also detected.

Table 1 Mean basal area (m2 ha21) and total number of seedlings perspecies found in the leeward (three 100 m2 plots) and windward (six100 m2 plots) study stations

Species Windward Leeward

Basal area(m2 ha21)

Seedlingnumber

Basal area(m2 ha21)

Seedlingnumber

Apolloniasbarbujana

0.08 24 3.95 663

Erica arborea 10.82 0 1.58 0Erica platycodon – 0 4.32 0Heberdenia

excelsa0.01 0 – 58

Ilex canariensis 3.43 0 8.04 0Ilex perado 6.51 4 – 0Laurus

novocanariensis8.78 1633 13.32 421

Morella faya 4.84 0 6.00 0Ocotea foetens – 0 – 1Persea indica 4.75 775 0.27 49Picconia excelsa 1.37 466 – 95Prunus lusitanica 5.77 0 – 16Rhamnus

glandulosa,0.01 22 – 11

Visnea mocanera – 0 – 7Viburnum rigidum 0.15 27 0.30 155

Table 2 Mean values, standard error (in parentheses) and results ofpermutational ANOVA for the abiotic and biotic parameters recorded inthe leeward and windward study stations

Windward Leeward P (perm)

Altitude (m) 783.33 (20.64) 783.33 (80.07) 0.99Slope (degrees) 20.00 (2.21) 33.33 (6.01) 0.04*Total basal area (m2 ha21) 46.50 (4.17) 37.77 (5.28) 0.23Basal area DBH . 20 cm

(m2 ha21)26.91 (4.02) 7.83 (6.32) 0.04*

Density of trees(no. ind. m22)

0.88 (0.08) 0.38 (0.12) 0.01*

Richness of trees(no. of species)

6.83 (0.79) 4.33 (0.88) 0.08

Density of seedlings(no. of seedlings ha21)a

12 300 (2700) 16 400 (10 300) 0.62

Richness of seedlings(no. of species)

5.00 (0.52) 7.33 (1.76) 0.11

Canopy height (m) 14.54 (1.15) 10.71 (1.43) 0.08Canopy cover (%) 98.06 (0.42) 96.26 (0.12) 0.02*Light penetration (%) 2.37 (0.37) 6.81 (2.61) 0.04*Survival rate (2011–2013)

(%)5.68 (1.83) 12.28 (1.06) 0.04*

Survival seedling height(cm)b

53.53(10.03) 51.21(9.17) 0.43

Growth rate (cm year21)c 2.43 (0.21) 2.71 (0.22) 0.42Density of saplings

(no. of sapings ha21)d267 (207) 366 (202) 0.61

aMean number of seedling recorded by year and by m2.bSeedlings older than 8 years which were alive at last census.cHeight increment per year.dSeedlings that reached the sapling stage (height . 1 m).*Significant differences.

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Average seedling life for the period 200022003 was 20.1months on the leeward and 17.5 months on the windwardslopes. The shape of the survival curve differed by aspects(log-rank test, P , 0.05). Kaplan–Meier’s survival curves indicatedthat the proportion of individuals surviving continuously decreasesduring the first 3 years of life. On leeward slopes nearly 55 per centof seedlings reached the third yearof life; while on windward slopesonly �20 per cent of the seedlings did so (Figure 2a). The per-centage of seedlings surviving until the last monitoring date

(201122013) was significantly greater on the leeward (12.3 percent) than on the windward slopes (5.7 per cent) (Table 2).

In the following survival analysis, the seedlings were grouped byspecies. Survival was significantly higher in the leeward plots forA. barbujana, L. novocanariensis and P. excelsa (log-rank test,P , 0.05), while no differences were found for P. indica andV. rigidum (Figure 2b–f). However, at the end of the survival curveof these two species, there was a higher survival rate on leewardslopes. Additionally, for all the analyzed species slightly higher

Figure 2 Survival curves of seedlings estimated using Kaplan–Meier’s method: (a) total seedling bank; (b) Apollonias barbujana seedling bank; (c) Laurusnovocanariensis seedling bank; (d) Persea indica seedling bank; (e) Picconia excelsa seedling bank; (f) Viburnum rigidum seedling bank. Confidence intervalsat 95% (thin lines) are shown. Shape of the survival curve differed between aspects in the cases of the whole-seedling bank community, A. barbujana,L. novocanariensis and P. excelsa (log-rank test P , 0.05).

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survival can be observed on windward slopes during the firstmonths of life, although in general there is an overlap of confidenceintervals. The shape of the survival curves differed among speciesin both aspects (log-rank test, P , 0.05). In the leeward plots, thehighest survival rate was for P. excelsa, followed by A. barbujanaand V. rigidum, showing 3-year survival rates of .55 per cent,while L. novocanariensis showed a survival rate close to 35 percent and P. indica survival rate was �15 per cent (Figure 3a). Inthe windward plots, the highest survival rate was shown by P.excelsa and V. rigidum, both of them with a survival rate ofalmost 40 per cent in the third year of life, while the Lauraceaespecies had survival rates of nearly 25 per cent in the third year,with the exception of P. indica, where no seedlings survived toreach the third year of life (Figure 3b). However, when drawing

conclusions from Figure 3 we need to be cautious due to thewide confidence intervals for some species at the end of theperiod (see Figure 2b–f).

The Cox’s proportional hazard regression showed that shorterlifespans are expected for seedlings with low growth, low finalheight, low foliar development, and which have suffered predation,wilting or pathogen attacks (i.e. low vitality index). However, theinitial vitality index did not significantly affect survival probability,and initial height was not significant when included in the model(Table 3).

DiscussionComparison between the composition of the canopy and of theseedling bank showed an uneven distribution of species (Table 1).Certain species, such as E. arborea, E. platycodon and M. faya, didnot appear in the seedling bank, despite their frequencies asadults in the canopy. These species are characterized by having apioneer reproductive strategy (Whitmore, 1989), being very abun-dant in the seed bank but unable to germinate under the shadyconditions of a closed canopy (Arevalo and Fernandez-Palacios,2000; Fernandez-Palacios et al., 2004). The abundance of thesespecies as adult trees in the studied stands may indicate amid-late successional stage of the forest (Fernandez-Palaciosand Arevalo, 1998; Dias et al., 2004; Arevalo et al., 2012), sincetheir regeneration strategy is heavily dependent on disturbanceevents, such as gap formation (Elias and Dias, 2009). Otherspecies, such as I. canariensis, I. perado and P. lusitanica also oc-curred rarely as seedlings. However, several suckers of thesespecies were found in stands, since they have a persistent repro-ductive strategy, which is characterized by the dominance ofasexual reproduction (Eriksson, 1996; Fernandez-Palacios et al.,2004). On the other hand, species such as H. excelsa, P. excelsaand R. glandulosa, itinerant-mature species that rely mainly onsexual regeneration (Fernandez-Palacios et al., 2004) werepresent in the seedling bank, despite their low frequencies asadults in the canopy, which indicate the importance of frugivorousdispersal in the laurel forest (Valido and Delgado, 1996). Thedetected differences between the canopy and the seedling bankmay lead to future shifts in canopy species composition (Perez-

Figure 3 Survival curves of seedlings byspecies estimated using Kaplan–Meier’s method: (a) leeward seedling bank; (b) windward seedling bank. Shape ofthe survival curves differed among species in both aspects (log-rank test P , 0.05). Confidence intervals are not shown for clarity.

Table 3 Results of Cox’s proportional hazard regression based on 4427monitored seedlings

b SE Wald P-value

Variables included in the modelInitial number of leaves 20.10 0.01 55.13 0.00Growing ratea 20.35 0.03 108.27 0.00Final heightb 20.82 0.01 853.61 0.00Final vitality indexb 20.75 0.01 86.26 0.00Final number of leavesb 20.25 0.01 51.38 0.00

Variables not included in the modelInitial vitality index 0.70Initial height 0.00

For the variables included in the model, the following parameters are given:b regression coefficient (negative values mean that the variable reducesthehazard rate, increasing the above-ground persistence); standard error (SE),the Wald statistics, and the level of significance. For variables not included inthe model significance levels before being included in the model are given.aAverage height increment per month.bFinal values correspond with previous values to the month in which at leastone seedling was recorded as dead, and were included as time-dependentcovariates.

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Ramos and Maranon, 2012)towards a more advanced succession-al stage. This has been suggested previously for the forest butevidence was lacking until this study (Arevalo et al., 1999).

Canopy composition and structure differed between windwardand leeward stations (Tables 1 and 2), as has been shown in previ-ous studies (Arevalo et al., 2007, 2012). In the laurel forest, differ-ences in aspect include wetter windward slopes, directly exposedto the orographic cloud layer, and drier leeward slopes, onlyaffected by the overflowing clouds. These contrasting environmen-tal conditions, related to topographical gradients, can alter bothspecies composition and structure of forests (Weaver, 1991; Clarkand Clark, 2000), making it possible to differentiate betweenhumid laurel forest, dominant in the north, and dry laurel forest,dominant in the south (del Arco et al., 2010). The results indicatethat larger trees occuron the windward slopes, which also have sig-nificantly highercanopy coverand densityof trees. This may be dueto higher wateravailability on these slopes, since these parameterscan decline with decreasing rainfall (Williams et al., 1996).Environ-mental differences also affect several aspects of the sexual regen-eration of the forest such as species composition (Rees, 1997;Arevalo et al., 2012), with the seedling bank being dominated byA. barbujana, one of the characteristic species of the dry laurelforest, on the leeward, and by L. novocanariensis, characteristicof the mesic laurel forest, on the windward slopes.

Survival of seedlings was relatively high when compared withother relict or subtropical forests (Augspurger, 1984; Hampe andArroyo, 2002), reaching almost 55 per cent and 20 per cent in thethird year of life for leeward and windward slopes, respectively(Figure 2a), and falling to 12 per cent and 5 per cent, respectively(Table 2), in the long term. Longer lifespans are expected for seed-lings with better fitness (leaf number, height, growth rate and vital-ity index; Table 3). In shady conditions, such as those of the laurelforest, faster growth and development of leaves can help seedlingsto exploit scarce light resources, increasing their long-term survivaland decreasing the duration of this vulnerable life stage (Kitajima,2007). On the other hand, the absence of an initial vitality indexeffect on survival could simply be the result of monthly monitoring,since at the first census, most seedlings had hardly experiencedany kind of disturbance such as desiccation, pathogen attack orherbivore predation.

Higher seedling survival was found on the leeward than on thewindward slopes, a pattern that prevailed in most of the analysedspecies (Figure 2a–f). However, during the first months of life, seed-lings of all the species seem to survive better on the windwardslopes. At this vulnerable stage of seedlings’ lives, the higherhumidity of the windward slopes may decrease the impact ofwater stress and thus the risk of seedling desiccation, a majorfactor in seedling mortality (Hampe and Arroyo, 2002; Engelbrechtet al., 2005). Nevertheless, the higher basal area and density oftrees found on the windward slopes results in seedlings with ahigher probability of being surrounded byadult trees. Neighbouringtrees can shade the seedlings and deplete the soil water and nutri-ents, and consequently windward seedlings are less likely tosurvive due to the competition for resources with established vege-tation (Clark and Clark, 1984; Begon et al., 2005). Additionally, ashorter distance between seedlings and trees also favours density-dependent predation and pathogen attack (Augspurger, 1983;Rodrıguez-Echeverria et al., 2007). In the laurel forest, the negativeeffect of the proximity to parent trees has been already demon-strated for species such as P. excelsa (Arteaga et al., 2006).

Moreover, light is a major limiting factor of seedling establishmentin forest (Medina, 2007).The leaf canopy reduction of light penetra-tion is more severe on windward than on leeward slopes; as a resultthe lower light availability at ground level on windward slopes candecrease the survival of the seedling bank (Perez-Ramos andMaranon, 2012). Detected differences in seedling survival mightalso be related to different foraging habits of predators such asrats across topographical locations (Delgado et al., 2001).

Despite different survival rates between windward and leewardslopes, no significant differences were found in the density of seed-lings that reached the sapling stage (height . 1 m) or in the growthrate (Table 2). In closed tropical forests, growth rates of seedlingsare typically low (Clark and Clark, 1992), with the presence of along-lived seedling bank being a characteristic feature of thestudied species (Fernandez-Palacios et al., 2004). Laurel forestseedlings are able to survive for years without promoting to thesapling stage, experiencing a fast growth only under favourableconditions such as gap openings (Arevalo and Fernandez-Palacios,2000). The height of those seedlings that were alive at the lastcensus (i.e. seedlings older than eight years) remained onaverage �50 cm, with ,1 per cent of the monitored seedlingsreaching the sapling stage and most of them belonging to thespecies P. excelsa, H. excelsa and A. barbujana. Although this per-centage might seem small, it represents a densityof .250 saplingsha21, and .10 000 seedlings ha21 year21. The high survival rates,the abundance of seedlings and their promotion to the saplingstage, combined with the major contribution of the asexual regen-eration (Arevalo and Fernandez-Palacios, 1998) ensure natural re-generation of the laurel forest, as evidenced by the considerablerestoration and expansion that this subtropical forest has experi-enced in the last decades (Wildpret and del Arco, 1999). Althoughthe historical regime of disturbance is similar in both forest stands,previous studies in nearby research sites have suggested that dif-ferences in environmental conditions have led leeward laurelforest to a less advanced successional stage (Arevalo andFernandez-Palacios, 2000).This is also suggested by its higher re-production success, since self-regulation in the late stages offorest succession results in scarce natural regeneration (Silvertownand Charlesworth, 2001).

Despite the fact that the analysed species share the commonfeature of maintaining seedling/sapling banks over long timeperiods, survival curves showed that they have different recruit-ment abilities (Perez-Ramos and Maranon, 2012). The lower sur-vival rates were those of the Lauraceae species (Figure 3), withthe exception of A. barbujana that showed one of the highest sur-vival rates on the leeward slopes, probably because this speciesfinds optimal environmental conditions in the dry laurel forest.Actually, in the nearby island of Madeira, where A. barbujanais also native, plant-ecologists differentiate an altitudinal lowerdry-thermic laurel forest dominated by Apollonias (laurissilva dobarbusano) from an altitudinal higher wet-mesic laurel forestdominated by O. foetens (laurissilva do til) (Sequeira et al., 2007).

Although, seed size has been found to be an important factorrelated to seedling survival in shaded conditions (Kitajima, 2007),this advantage is only temporary, since the species with largerseeds (Lauraceae; Arevalo et al., 2007) are not the ones with thehighest survival. The higher survival of P. excelsa and V. rigidumcanberelatedto its regenerationstrategy.Bothspeciesare itinerant-mature species, whose reproduction depends entirely on the seed-ling bank (Fernandez-Palacios et al., 2004; Fernandez-Palacios,

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2009). Consequently, to ensure recruitment, seedlings are able togrow under a closed canopy, which in the absence of disturbancesmight lead to higher survival rates. On the contrary, Lauraceaespecies also have asexual reproduction (producing both seedlingand suckers), and its seedlings depend on canopy openings togrow, having a greater risk of experiencing desiccation or predation(Fernandez-Palacios et al., 2004). Among Lauraceae, the lowestsurvival rate was for P. indica probably because this species to-gether with O. foetens, for which only one seedling was found, ismore demanding in terms of moisture than L. novocanariensisand A. barbujana (Santos, 1979).

Conclusions

This study has reported for the first time on the long-term (over 12years) seedling dynamics of Macaronesian Laurel forests, and hasenabled the detection of substantial differences in recruitmentbetween slope aspect and species that were previously unknown.Itinerant-mature species, despite not being dominant in the seed-ling bank, showed better recruitment abilities than dominant Laur-aceae species. Additionally, contrary to what was expected,seedling survival was higher on the drier leeward than on thewetter windward slope, which might be related to environmentaland structural differences of the forest stands of the differentslope aspects (e.g. basal area, density of trees, canopy cover andlight penetration). The results showed that over a 12-year period,survival rates of 12 and 5 per cent for leeward and windwardslopes, respectively, reflect the high regeneration potential of theforest in well-preserved stands, indicating that no managementinterventions are needed to ensure forest regeneration. Althoughthe laurel forest stands out for a high variability in compositionand structure, the results could be extrapolated to other cloudforest stands. Results from this study might be useful in plantationsand reforestation programs that are currently underway in areaswhere the laurel forest has been eliminated or is heavily disturbed,since it provides information on natural regeneration patterns.Future studies should attempt to identify the role of predators,such as rats and slugs, on laurel forest seedling survival.

NomenclatureFor nomenclature of wild species refer Canary Islands checklist(Acebes et al. 2010).

AcknowledgementsWe are grateful to all the field-work collaborators: Eduardo Balguerıas,Cristina Blandino, Alistair Domınguez, Gustavo Morales and PriscilaRodrıguez.

Conflict of interest statementNone declared.

FundingThis work has been partially funded by the Rolle Foundation and the Pro-grama de Apoyo a la Investigacion 2012 from the University of La Laguna.

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