Seedling bank demography over 11 years in an island laurel forest, Tenerife, Canary Islands

Forest Ecology and Management 462 (2020) 118001

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Seedling bank demography over 11 years in an island laurel forest, Tenerife, Canary Islands

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Eduardo Pereira Cabral Gomes (PhD)a, , Lea de Nascimento (PhD)b, Alistair Domínguez (Degree in Biological Sciences)b, Eduardo Balguerías (Degree in Biological Sciences)b, Javier Méndez (PhD)b, Silvia Fernández-Lugo (PhD)b, José Ramón Arévalo (PhD)b, José María Fernández-Palacios (PhD)b a b

Instituto de Botânica, São Paulo, Brazil Island Ecology and Biogeography Group, Departamento de Botánica, Ecología y Fisiología Vegetal, Universidad de La Laguna, Tenerife, Spain

A B S T R A C T

Confined to the humid cloud belt of the Macaronesian Islands the Laurel-forests are sensitive to climate changes. Intense natural disturbances are rare and regeneration includes asexual regeneration and dominance of shade intolerant species in the seedling bank. Long-term monitoring of the seedling bank showed that even under these relatively stable conditions high variations occurred. Studies point out to a downward shift of the trade winds cloud belt that confined laurel cloud forests. Only long-term studies can detect the effects of rare extreme events or the influence of slow processes on seedling dynamics. In nine 10 × 10 m plots (six in windward and three in leeward) we monitored the seedling bank monthly from 2000 to 2003 and recount it in 2005 and 2011. Our aim was to estimate seedling dynamics in a Laurel forest. We hypothesized that this forest seedling bank is relatively stable over time. Under present mild temperate climate, we hypothesized that this forest seedling bank is relatively stable over time; seedling recruitment will be positively related to rainfall; sprouting-species will be poorly represented in the seedling bank and growth rate will be higher than observed in other forests. Composition and abundance in seedling bank were stable across 2000–2003. The fluctuation in density, recruitment and mortality for Laurus novocanariensis was determinant for seedling community dynamic, and composition and abundance in seedling bank were stable across first three years and relative seeding growth rate is higher than observed in another subtropical wet montane forests. There was no significant relationship between mortality and recruitment and precipitation. However, in the 2011 count, an increase in density for all species. Except for a hot year in 2010 and a humid one in 2009 for the Canary Islands, there was no record of exceptional weather events or large-scale disturbance episodes in the previous eight years, and these are unlikely to explain the observed increase. Species with seedling banks were more abundant. Nonetheless, few seedlings survive more than two years. We emphasise the importance of long-term studies with fine-scale disturbance monitoring for understanding the dynamic processes of this unique forest.

1. Introduction Some ecological processes operate at different time and space scales from the events that produced them; thus, relatively brief or sudden events (floods, landslides, fires, etc.) can have significant long-term effects (Connell et al., 1997). Especially when rates of change are very slow, the detection of their effects requires long-term studies capable of separating trends from fluctuations (Connell and Green, 2000). The natural regeneration of forests ranges from the short cycle dynamics in days or weeks of ephemeral plant species to the long life span of the oldest trees. Knowledge of these natural regeneration processes is essential for the proper conservation and/or restoration of natural forests. The formation of seed banks, seedlings and/or regrowth is the means by which plant populations ensure their natural regeneration (Harper,

1977). These regeneration strategies imply demographic traits of plant populations in its initial life cycle, each strategy being more or less appropriated according to local conditions (Silvertown and Lovett, 2009). Seed bank regeneration is generally restricted to shade intolerant species that rely on large canopy gaps or large disturbances to germinate, while the contribution of the seedling bank increases over time and is the primary process in mature ecosystems (Bazzaz, 1996). Regeneration involving a “persistent seedling bank” that can hold for years is therefore the dominant regeneration medium in stable forests composed predominantly of shade tolerant trees when young (Grime, 1979) and is advantageous in regimes of low-severity disturbances associated with canopy gaps (DeRose and Long, 2010). However, in many forests it has been observed that understory seedling densities vary greatly over time, both at population and community levels (Connell

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Corresponding author at: Instituto de Botânica, NP Ecologia, Av. Miguel Estefno 3687, 04301-900, São Paulo, SP, Brazil. E-mail addresses: [email protected] (E.P.C. Gomes), [email protected] (L. de Nascimento), [email protected] (J. Ramón Arévalo), [email protected] (J.M. Fernández-Palacios). https://doi.org/10.1016/j.foreco.2020.118001 Received 27 October 2019; Received in revised form 13 February 2020; Accepted 14 February 2020 0378-1127/ © 2020 Published by Elsevier B.V.

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tolerant species such as Laurus novocanariensis Rivas Mart, Lousã, Fern.Prieto, E.Días, J.C.Costa & C.Aguiar, Persea indica (L.) Spreng, Picconia excelsa DC. and Viburnum rigidum Vent (Arévalo et al., 1999; Fernández-Lugo et al., 2015). On the other side, sprouts are very abundant in the forest gaps, edges of gaps and under the canopy, showing the importance of asexual reproduction in several tree species (Arévalo and Fernandez-Palacios, 1998). Even shade intolerant species like Morella faya, a long-lived pioneer, combine seed bank regeneration with the ability to persist under canopy thanks to their ability to regrow. Despite many studies on regeneration and natural disturbances in laurel forests (Arévalo and Fernández-Palacios, 1998, 2003; Arévalo et al., 2012; Fernández-Lugo et al., 2015; Arévalo et al., 2018; Ganivet et al., 2019) the role of the seedling bank is still poorly understood and there is a lack of information on how on-going climatic changes (Sperling et al., 2004; Martín et al., 2012; Cropper and Hanna, 2014; Expósito et al., 2015) may alter the dynamics, composition and diversity of these forests. For instance, in a 30-years study a significant increase in the relative humidity below the trade wind inversions was detected, pointing out to a future downward shift of the trade wind cloud belt (Sperling et al., 2004). In this study the dynamic of the laurel forest seedling bank was investigated over eleven years with a sample of ca. 15,000 individuals. Our purpose was to analyse how stable the structure and composition of the seedling bank in a forest characterized by a lack of frequent and/or severe disturbance episodes could be. With that aim, we compared patterns of recruitment and mortality among species along all seasons during three years, with additional data on seedling density five and eleven years after the first census. Specifically, we addressed the following questions: (i) How stable is the local seedling bank in terms of density and species composition over time? (ii) How do seedling bank characteristics differ among species? (iii) Are tree species depending on asexual reproduction poorly represented in the seedling bank? (iv) How long can seedlings be nourished from their seeds reserves? Under a climate of low seasonality with high and constant relative humidity throughout the year and absence of frequent intense disturbances we expected that: (i) the seedling bank will be relatively stable over time; (ii) seedling recruitment will be positively related to rainfall (especially those species that are relatively more abundant on the more humid slope); (iii) the species that present abundant sprouting would be poorly represented in the seedling bank and, (iv) growth rate will be higher than observed in other forests.

and Green, 2000; Norden et al., 2007; Metz et al., 2008). The seedling stage is an important bottleneck of the plant community dynamics and how seedlings establish, grow and survive has been widely studied (Dupuy and Chazdon, 2008, Yavitt and Wright, 2008, Comita et al., 2010, Parada and Lusk, 2011,Pérez-Ramos and Marañón, 2012). The role of vegetative regeneration however, until recently had attracted little attention (Klimesova and Klime, 2007). It has been noted that “sprouters generally produce fewer seeds, smaller seed banks, have slower growth and maturation rates (from the seeds), and almost always have fewer seedlings and a lower survival of the seedlings than non-sprouters” (Bond and Midgley, 2001). After the death of the main trunk, the shoots have a competitive advantage over the seedlings because they already have an established root system that allows for immediate development and does not have retarded growth beneath parent trees due to shading or intraspecific competition like seedlings (Klimesova and Klime, 2007). However, the predominance of sprouting in a given species does not always automatically characterise it into a given strategy (Closset-Kopp et al., 2007, Żywiec and Holeksa, 2012). Mixed strategies in which asexual regeneration plays a major role can be found both in long-lived pioneers who also maintain a seed bank or in shade-tolerant species that combine both a seedling bank and regrowth (Ganivet et al., 2019). The Macaronesian laurel-forest is an ecosystem of exceptional conservation value due to its high species endemicity and restricted distribution (Fernández-Palacios et al., 2017). It is a forest relic of the Tertiary that was once widespread in the Mediterranean Basin (Bramwell, 1976; Höllermann, 1981; Santos, 1990; Fernández-Palacios, 2009), surviving only nowadays in the Canary Islands, Madeira and Azores. Some tropical-like characteristics of the Macaronesian laurel forest include: (i) the participation of several families with tropical affinities (Clethraceae, Lauraceae, Myrsinaceae, Pittosporaceae, Sapotaceae or Theaceae) in their canopy; (ii) an important endemic tree species richness (ca. 30) especially for their latitude and such a small territory; (iii) a high biomass (up to 300 t ha−1) and basal area (up to 60 m2 ha−1); (iv) the dominance of evergreen species; (v) the presence of an important fraction of real (Juniperus, Laurus, Morella, Ilex) or functional (Ocotea, Persea, Picconia) dioecious species; (vi) the presence of cauliflory (Heberdenia, Pleiomeris, Sideroxylon); (vii) generalized entomophily and ornithochory traits; (viii) a quasi-permanent fructification across the year, without seasonality; (ix) the prevalence of recalcitrant seeds in seed banks and; (x) the importance of vegetative reproduction (Fernández-Palacios et al., 2017). These forests are nowadays confined to the humid cloud belt existing between 600 and 1200 m, on the north and northeast windward slopes of the Canary islands with a humid, mild temperate climate (Kämmer, 1974). Under present climatic conditions, intense natural disturbances such as landslides and hurricanes, leading to formation of large open areas, are rare (Fernández-Palacios and Arévalo, 1998). Nevertheless, due to the human impact, today there is less than 12% of the original Canarian laurel forest cover left (del Arco et al., 2010). This restricted distribution makes them especially sensitive to the on-going climate change (Sperling et al., 2004; Martín et al., 2012; Cropper and Hanna, 2014; Expósito et al., 2015). Some characteristics of the laurel forest regeneration include a high rate of asexual regeneration, primarily by suckers (Arévalo and Fernández-Palacios, 1998; Fernández-Palacios and Arévalo, 1998); low influence of canopy gaps in tree dynamics (Arévalo and FernándezPalacios, 1998, 2007) and dominance of shade intolerant species in the seed bank (Arévalo and Fernández-Palacios, 2000). Projection models that predict long-term compositional trends showed different output if asexual reproduction was included or not (Arévalo et al., 1999). However, when reproduction by suckers was considered the composition change is minor and the persistence of some species appears to be highly dependent of asexual reproduction (Arévalo et al., 1999). The Canarian laurel forest seedling bank is dominated by shade

2. Material and methods 2.1. Study site The study was carried out at the Anaga Rural Park (NE Tenerife) home of the best preserved laurel forest remnants in the island, comprising around 12% of its original cover (del Arco et al., 2010). The Park embraces a 7–8 million year old basaltic massif (Ancochea et al., 1990), covering ca. 130 km2. The Anaga laurel forest climate is characterized as subtropical montane, with a mean annual temperature close to 15 °C, with scarce annual or daily fluctuations. The long-term average annual rainfall is approximately 900 mm, but frog drip makes a significant contribution to this total (Kämmer, 1974; Marzol et al., 2010). The substrate consists mainly of volcanic bedrock where soils classified as order Entisol, suborder Orthens (Fernández-Caldas et al., 1985), containing high amounts of organic material and being weakly acid, have developed (Fernández-Palacios and Arévalo, 1998). Canopy height varies from 10 to 20 (25) m in relation to the slope and soil depth, with maximal heights being found at the ravine bed’s floor, decreasing progressively towards the ravine bed’s borders and crests (Arévalo and Fernández-Palacios, 2003, 2007). The forest in Anaga contains ca. 20 tree species, the big majority of them palaeoendemics shared with other Canary Islands (Gran Canaria, La Gomera, La Palma and El Hierro) and Madeira, such as L. novocanariensis 2

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–the dominant species in the forest–, Apollonias barbujana (Cav. Bornm), Erica arborea L, E. platycodon Webb & Berthel, Ilex canariensis Poir, I. perado Aiton, Morella faya Ait, Ocotea foetens (Aiton) Benth. & Hook. f, P. indica, P. excelsa, Prunus lusitanica L, Rhamnus glandulosa Aiton and Visnea mocanera L.f. The understory is sparse and dominated by tree seedlings and saplings, by the tall shrub V. rigidum, some vines (Smilax canariensis Willd, Semele androgyna Kunth) and in humid stands by ferns, such as Asplenium onopteris L, Culcita macrocarpa C. Presl, Diplazium caudatum (Cav.) Jermy, Dryopteris guanchica (Jermy 1980), D. oligodonta (Desv.) Pic.Serm, Polystichum setiferum (Forsk.) Woynar, and Woodwardia radicans (L.) Sm (Fernández-Palacios et al., 2017).

damaged; 4 = moribund; 5 = dead] were determined. We recorded all seedlings still keeping their seeds (or seed rests) and follow them monthly. This provided an estimate of the time that seedlings remain with seeds and not an average of seedlings number with seeds since we avoided disturbing individuals by actively digging. For genera with frequent resprouting (such as Ilex or Prunus) we carefully examined seedling avoiding resprout counting (Marais et al., 2014). Total monthly rainfall data were obtained from meteorological stations close to the study sites. Data for September 2001, May 2002 (windward station – C447F) and December 2003 (leeward stationC447O) were estimated by interpolation of precipitation data from neighbouring meteorological stations in Anaga (supplemental material). All meteorological stations data were significantly correlated (p < 0.001, r2 = 0.93).

2.2. Sampling design and fieldwork For analysing the seedling bank composition and dynamics we randomly established three 10 × 10 m permanent plots at each site in homogeneous forest stands of approximately 2–3 ha. The plots were laid out in three sites that represented some of the best laurel forest remnants within the Anaga massif: La Estercolada (810–820 m a.s.l.) and El Moquinal (685–790 m a.s.l.) sites at the windward slope, where the laurel forest is much wider distributed, and Monte de Aguirre (630–900 m a.s.l.) site at the leeward slope of the massif, where the laurel forest is more scarce (Table 1). These plots were distributed in the core area of the laurel forest, in homogeneous forest stands of approximately 2–3 ha, avoiding the lower boundary with Morella fayaErica arborea secondary woody trees and the upper boundary with Erica platycodon forests. At each site we randomly established three 10x10 m permanent plots. Previous investigations in this area indicated that this plot size is adequate for seedling community sampling since the more frequent gap canopy are 20–30 m2 large and gaps > 100 m2 are very rare (Arévalo and Fernández-Palacios, 1998, 2007). The designation of study sites, plot size and plot number were based on previous studies conducted in the area. In each plot the following biotic and abiotic parameters were recorded: location (UTM coordinates), elevation (m), basal area (m2 ha−1) of trees with diameter at breast height (DBH) > 20 cm, tree/ sapling (height > 2 m) density (ind. ha−1), canopy height (m) and canopy closure (%) using a spherical densitometer. A point quantum sensor was used to quantify the light penetration (%) taking a measure each 5 m (nine measures per plot). A survey of seedlings (height < 1.3 m) was carried out from November 2000 to November 2003 for La Estercolada; from December 2000 to October 2003 for El Moquinal (windward plots) and from March 2001 to December 2003 for Aguirre (leeward plots). Additional censuses were taken in October–November 2005 and October 2011–April 2012. Seedling survivorship and spatial analysis have been reported elsewhere (Fernández-Lugo et al., 2015). Each plot was visited every three weeks (average interval 20.9 days). At each visit, the status (dead or alive) of previously tagged seedlings, the height of surviving seedlings to the nearest 0.5 cm, the number of leaves and vitality index [1 = no damage; 2 < half of leaves damaged; 3 > half of leaves

2.3. Data analysis Seedling density, recruitment, mortality and growth rate between seasons across the whole period were compared using ANOVA for repeated measures. Data normality was tested with Kolmogorov-Smirnov goodness of fit test. If standard statistical assumptions were not met, data were square-root transformed (Zar, 1996). In the absence of a widely accepted definition of stability, we assumed that the absence of significant statistical differences in density over time was sufficient to define the seedling bank as stable (Vanhellemont et al., 2009). For correlation between relative growth rate and number of dead and germinated individuals data were transformed dividing each value by the largest observed value in the plot (Legendre and Legendre, 1998). Because differences in data gathering, only seasons with data for all nine plots, from spring 2001 to summer 2003, were considered in the statistical analysis. A post-hoc Tukey-Kramer test was performed. Statistical analyses were carried out in software Past version 3.15 (Hammer et al., 2001). 2.4. Seedling height growth We analysed the relative growth rate (RGR) of seedling height for each species at the end of the seasons. RGR for surviving seedlings was calculated as (Hoffmann and Poorter, 2002):

RGR = log(Hs/H0)T−1 where Hs is the height of the seedling in the last season, H0 the initial height of the seedling and T the elapsed time (months). Furthermore, a correlation analysis between numbers of surviving months and seedling height (or leaves number) in the first month of life was done. 3. Results We recorded 4427 seedlings belonging to 13 different tree species from November 2000 to March 2004. In the windward plots 96 new seedlings were recorded in November 2005 whereas in 2011–12 we

Table 1 General characteristics of the plots sampled. Plots 1 to 3 (La Estercolada), 4–6 (El Moquinal) and 7–9 (Aguirre). Slope: w - windward; l - leeward. No.

Altitude (m)

Slope (°)

Exposition (°)

Tree density (ind. > 2 m ha−1)

Basal area (m2 ha−1)

Cover (%)

Light penetration (%)

1 2 3 4 5 6 7 8 9

815 820 810 685 790 780 630 900 820

27 25 18 18 12 20 25 45 30

350 (w) 220 (w) 240 (w) 310 (w) 260 (w) 45 (w) 190 (l) 180 (l) 180 (l)

3600 2900 1300 1500 2900 2600 3000 4900 1500

67.0 31.5 76.8 32.1 53.2 42.2 31.6 42.5 29.6

98 98 98 96 99 98 96 96 96

3.0 2.8 3.5 1.5 1.2 2.3 4.5 12.0 3.8

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species, there were no significant differences in seedling density between seasons (F = 1.08, df = 9, p = 0.39). For this species there were significant differences along the seasons with a maximum population density in autumn 2002 (ca. 1.4 seedlings m−2; F = 5.62, df = 9, p < 0.001), germination in summer 2002 (ca. 0.6 seedlings m−2; F = 6.06, df = 9, p < 0.001) and mortality in winter 2003 (ca. 0.3 seedlings m−2; F = 3.07, df = 9, p < 0.01). As was to be expected due to the prevalence of L. novocanariensis in the seedling community (Fig. 2), the increased recruitment of this species and the resulting increase in mortality rates affected the general pattern observed. For the other species analysed (Fig. 2), there was a significant mortality increase for P. excelsa in autumn 2002 (F = 2.96, df = 9, p < 0.01) and there was a significant recruitment increase for V. rigidum in summer 2003 (F = 2.67, df = 9, p < 0.5). There was also a peak, in recruitment, although non-significant, for P. excelsa in summer 2001 (F = 3.33, df = 9, p < 0.5). Persea indica only presented a slight increase in the overall density in summer and autumn 2002, but this was not significant (p = 0.14). The general pattern observed is essentially the one occurring in the windward quadrats, where the relative abundance of L. novocanariensis approaches 55.0% (for only 28.5% in leeward plots). In the leeward quadrats the average density was kept around 3.5 seedlings m−2, although the spatial variability was higher, with plot 7 embracing ca. 42% of the total individuals counted (appendix 1 in supplemental material). Although the dominant canopy species (L. novocanariensis) is also the most abundant seedling, there is a negative (Spearman’s D, p = 0.66), albeit non-significant, correlation between adults and seedlings abundance (Fig. 3). Species showing a regeneration pattern characterized by asexual regeneration as more frequent strategy, such as Prunus lusitanica L. and Ilex spp. (Fernández-Palacios et al., 2004) were poorly (< 1%) represented in the seedling bank, whereas seedlings of pioneer species such as Erica arborea, E. platycodon and Morella faya (Fernández-Palacios et al., 2004) were simply absent. We found no statistically significant correlations between new, dead and total number of seedlings and either annual or seasonal rainfall. The correlations with the previous season's rainfall were also not significant. Furthermore, there was a moderate, but non-significant correlation, between seasonal precipitation and recruitment for P. indica (p = 0.19) and P. excelsa (p = 0.14). In the windward plots the density in November 2005 was not different from the 2001–2003 period, but in 2011–12 there were around four times more seedlings (Fig. 4). As the period of re-census lasted longer than two months in 2011 (plots 5 and 6) due to the high number of seedlings found that year, we performed a statistical analysis for plots 1 to 4 data. The seedling density in the last census (2011) was significantly higher than in the first three years (F = 4.7, df = 7, p = 0.003). If in 2001–2003 period there was a greater variability in density between plots (Coefficient of Variation (CV) from 78 to 134%) than between seasons (5–59%), the additional density data showed another pattern (Fig. 4). The temporal variability over 11 years was from 86 to 173% CV and 31–59% between plots. In the 2011–2012 census the density was greater for all species (Fig. 5) and it was possible to identify up to 76 individuals tagged in the first census. There is a trend to increase dying probability within one month with higher vitality index, although the values were similar for the first three classes (Table 2). Higher and more leaf-bearing seedlings of L. novocanariensis survived longer (Table 2). However, Persea indica seedlings had a negative significant correlation between initial height and lifespan (Table 2). The seed reserve lasts two months on average and for 90% of seedlings recorded their seed lasts attached to the seedling no longer than four months (Fig. 6) (see Table 3). Relative growth rate (RGR) is low for most seedlings (Fig. 7) and the average growth rate is 28 mm year−1 (median: 17 mm year−1). RGR were greater in summer 2002, autumn 2002 and spring 2003 (nonparametric Kruskal-Wallis analysis of variance, p < 0.001) than in

Fig. 1. Seedling density (A), recruitment (B) and mortality (C) by season (winter (w), spring (sp), summer (su) and autumn (au) from 2001 to 2003. Mean (bar) ± Standard Error (segments) values are given for each season. Different letters o letter combinations indicate significant differences among seasons along years.

counted 11438 individuals. Five species (L. novocanariensis, P. indica, P. excelsa, A. barbujana and V. rigidum) out of the 13 recorded contributed with 97.3% of the total seedling number. The overall density was ca. 2 seedlings m−2 (Fig. 1). Density was significantly higher in summer and autumn 2002 (Fig. 1a, ANOVA, F = 6.72, df = 9, p < 0.001). There was an increase in seedling numbers for five months, from July to November 2002. This surge in density was due to the increase in seedling recruitment from summer throughout autumn 2002 (F = 5.68, df = 9, p < 0.001) (Fig. 1b). The mortality was higher in the second month following the highest recruitment. The highest mortality occurred in February 2003 and the number of dead seedlings was significant higher in winter 2003 (F = 3.26, df = 9, p < 0.01) (Fig. 1c). In the spring 2003, the average density (Fig. 1a) has stabilized at a slightly higher level (ca. 2.4 seedlings m−2) than that recorded in the first three monitoring semesters (ca. 2.0 seedlings m−2). The overall density variation was basically due to changes in L. novocanariensis seedlings population ((Fig. 2) and apart from this 4

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Fig. 2. Seedling density (A), germination (B) and mortality (C) of the more frequent species (L. novocanariensis, A. barbujana, P. indica, P. excelsa and V. rigidum). Mean ± SE values are given. Different letters indicate significant differences among seasons.

climate, with less intense seasonality and with high relative humidity and reduced diurnal and annual temperature ranges (Marzol et al., 2010). Large-scale natural disturbances such as landslides and hurricanes are rare and outbreaks of pests or diseases have been unnoticed for this forest. Its dynamics are characterized by small-scale disturbance where large gaps (> 100 m2) are uncommon and have a weak negative effect on the germination and growth of shade-tolerant species (Arévalo and Fernández-Palacios, 2007). Under such conditions we expected low variability in density and a relatively stable seedling bank. The first three years of the seedling bank monitoring pointed to a relative stability in seedling abundance, germination and mortality. The overall density variation was basically due to changes in L. novocanariensis seedlings population. Recruitment peaks had little relationship with fruiting peaks, which were evaluated in a previous study in six of the nine plots (Arévalo et al., 2007). Thus, the fruit peaks of L. novocanariensis (November 2001), P. indica (September 2001 in El Moquinal) and V. rigidum (March 2001) did not lead to an increase in recruitment. Only the higher fruit production of A. barbujana in February

winter 2002. Among species the distribution of growth classes differed. P. indica had the highest percentage of seedlings above median yearly increment (Fig. 7b) whereas L. novocanariensis had it under median yearly increment (χ2 = 66.57, df = 24, p < 0.001). The maximum relative growth rate was observed in the first year for all species. After eleven years the maximum increment among the 76 remnant seedlings identified was of V. rigidum with 160 mm year−1. Only six individuals showed an increment > 50 mm year−1, from which five belong to V. rigidum and one to L. novocanariensis. Both species showed positive survivorship in function of initial height and average yearly increment for these remnant seedlings was 23 mm year−1 (median 18 mm year−1), very close to values observed during the monitoring. 4. Discussion Data of the seedling bank development over 11 years highlighted the regeneration dynamics on the long-term. The laurel forest grows under the influence of the sea of clouds in an attenuated Mediterranean 5

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Fig. 3. Relative seedling (grey) and tree (black) abundances (% of all individuals) at the beginning of the study (winter of 2001). Seedling abundance was log transformed. Table 2 Death probability (%) per month for various species and various classes of vitality index (1 = no damage; 2 < half of leaves damaged; 3 > half of leaves damaged; 4 = moribund). Vitality Index

Laurus novocanariensis

Apollonias barbujana

Persea indica

Picconia excelsa

Viburnum rigidum

1 2 3 4

0.86 0.60 1.08 33.83

1.73 0.16 3.74 41.51

1.66 0.32 0.39 19.34

1.68 1.10 2.43 40.89

0.01 0.01 0.01 0.02

2001 and, to a lesser extent, P. excelsa in July 2001 led to a higher recruitment trend in the following months. Low relationship between fruit production and seedling germination has also been found in other forests (e.g. beech forests in central Europe, Szwagrzyk et al., 2015). The relationship between seed and seedling establishment limitations depends on plant species life traits (Chen et al., 2013) and seed mass has shown to have a positive effect (higher survivorship) for tropical tree species (Muscarella et al., 2012). Laurus novocanariensis seed weight is the second heaviest of the community whereas V. rigidum seed is the lightest (Table 4, Arévalo et al., 2007). Causes of seedling limitation would probably be different for each species. The two months delay between recruitment and mortality peaks agrees with our estimation that the seed reserve lasts for two months on average, showing that after the end of seed reserve the seedling could either be: (i) established in an unsuitable microhabitat; (ii) experiencing a strong inter or intraspecific competition, (iii) depleted by herbivory or (iv) pathogens. In a long-term study (eight years) carried out in a Taiwanese subtropical rainforest mortality lags from three to six months after the recruitment peak (Chang-Yang et al., 2013). Our data from 2001 to 2003, and also from autumn 2005, showed a more stable seedling bank composition and density than in other studies, such as sites subject to large disturbances as flooding events (Streng et al., 1989), heavy storms (Comita et al., 2010; Chang-Yang et al., 2013), or small-scale light disturbances as in mature tropical (Connell and Green, 2000; Dezzeo et al., 2008) or temperate forests (Szwagrzyk et al., 2001), as expected. There was no statistical correlation with either monthly, seasonal or annual rainfall, and the only

−2

Fig. 4. Autumn density (seedlings m ) in windward (dark grey) and leeward (light grey) plots. Mean ± SE values are given. Different letters indicate significant differences among years (only for windward plots).

Fig. 5. Seedling log-transformed abundance (total number of seedlings) in windward plots in November 2001, 2002, 2003, 2005 and 2011.

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Fig. 6. Percentage of seedlings retaining seed after their germination.

census since the peak of mortality occurs a few months after recruitment (data from 2000 to 2003). Nevertheless, it is a hypothesis to be verified. A second possible cause could be a massive masting event, but it does not seem probable because density increased substantially for all species, although L. novocanariensis showed the greatest increase. Along the three monitoring years there was no formation of tree falling gaps either in the plots or in their vicinity that can explain such increase. This is indirectly confirmed by the absence of seedlings of light-demanding species such as Erica arborea, E. platycodon and Morella faya. However, there were trees of these species in the plots and a previous study (Arévalo and Fernández-Palacios, 2000) showed that they maintain a viable seed bank in the area. A possible explanation for the observed patterns is that other abiotic factors could be affecting seedling establishment and germination. In a mature tropical moist forest in Australia there was no correlation between seedling numbers of Chrysophyllum species and dry months per year, El Niño Southern Oscillation (ENSO) and either annual or seasonal rainfall, but there were significant correlations with mean seasonal air temperatures in the years preceding flowering, and masting seed production and seedling germination (Connell and Green, 2000). Although after 2000 we have no data available for canopy coverage and light penetration it is possible that small changes in light environment could have cause changes in the seedling bank. In a beech forest in Central Europe Szwagrzyk et al. (2001) found that small differences between 4% and 9% of full sunlight were sufficient for a transition from an unstable to a stable seedling bank. Probably, forest dynamics is being carried out by a mixture of strong deterministic and random processes of regeneration and not driven by completely predictable or unpredictable patterns (Harcombe et al., 2002). Both deterministic and stochastic processes could act on seedling dynamics. A low level of disturbance as the fall of branches with a consequent partial canopy opening, slightly rising the light reaching the forest floor, could cause an enhancement of germination ad recruitment. The interactions between low levels of light, moisture and biotic factors as herbivory or fungi pathogens is complex (Packer & Clay 2000; Szwagrzyk et al., 2015). For instance, with increasing soil moisture

Table 3 Correlation between life span and initial height of seedling and life span vs. number of leaves for Laurus novocanariensis, Persea indica, Picconia excelsa, Apollonias barbujana and Viburnum rigidum. Spearman rank of correlation (rS) and probability of uncorrelated (p). Species

Laurus novocanariensis Persea indica Picconia excelsa Apollonias barbujana Viburnum rigidum **

Height (cm)

No. of leaves

rS

p

rS

p

0.078 * −0.101 * 0.028 −0.110 0.341 ***

0.011 0.020 0.181 0.424 < 0.001

0.120 *** 0.085 −0.082 0.120 0.13

< 0.001 0.515 0.323 0.380 0.130

p < 0.01. * p < 0.05. *** p < 0.001.

intense disturbance observed, the heavy storm in November 2001, had limited effects on the seedling community, both in space (plot 2) and time (< 3 months). This flooding episode could be responsible for the mortality increase of P. indica and P. excelsa in the following season, Perhaps by the mechanical action of rain itself or by the potentialization of attacks by fungi due to soil saturation by moisture (Packer and Clay, 2000; Hersh et al., 2012). The additional census in 2011–2012, however, showed a high increase in seedling densities. This change could have been related to climatic conditions, but in this year (2011) there was also a non-significant relationship with monthly or seasonal precipitation. The reports of the “Agencia Estatal de Meteorologia de España” inform that for the Canary Islands, between 2005 and 2011, the year 2009 was particularly wet, with a dry year (2008) and two hot years, 2008 and 2010, with a thermal anomaly higher than 1.5 °C for the latter. The others did not deviate from normality (temperature and precipitation), though incomplete, data from stations close to the study area (supplemental material 2) show the highest precipitation values in the year of 2009. We consider it unlikely that the wettest year of 2009 and the warmest year of 2010 are directly related to the recruitment of the last 7

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or depleted seedling bank to a recruitment of new individuals to older age classes. Growth rates are generally reported as very low for seedlings in various forest types ranging from < 2 mm year−1 for cold temperate (Antos et al., 2005) and Quercus (Alvarez-Aquino, 2004) forests, to 12.7 mm year−1 in undisturbed tropical forests (Dezzeo et al., 2008) and 15.5 mm year−1 in subtropical montane forests (Chang-Yang et al., 2013). For the average seedling height in our study (133 mm) published relative growth rates would be equivalent to an increment from near to zero (Baraloto and Goldberg 2004; Comita et al., 2010) to 11.7 mm year−1 in tropical forests (Baraloto and Goldberg, 2004), below of 28 mm year−1 in our study plots. In general, studies point to low seedling growth rates under undisturbed forest canopies until the appropriate conditions to grow appear (Martínez-Ramos and Soto-Castro, 1993). It should be also considered that growth rates distributions used to be biased due to the existence of few fast-growing individuals in gaps (Comita et al., 2007) or under patches of favourable light conditions (Walker et al., 2003), so that average values can be poor representative for the most. Our results showed that relative growth rates of seedlings in the laurel forest were relatively higher than in other forests. Maybe the mesic, mild climatic and microclimatic conditions favour the continuous growth of seedlings over all the seasons. This is important because the majority of the species with seedlings (including Lauraceae, but not Picconia and Viburnum, which seem able to keep growing under a closed canopy) will grow during the first year after the seed germination until depleting all the reserves existing in their attached seed, achieving a more or less fixed size (ca. 10–15 cm). They can keep this size for several years, unless the opening of the canopy, when they will continue growing, or their disappearance, either due to herbivore (mainly slugs) consumption, wilting or water crawl (Fernández-Lugo et al., 2015). The high growth rates of V. rigidum, five of the six largest increments in height, confirm the uniqueness of this species in which growth is exponential as in the pioneers but without their regenerative functional traits (Ganivet et al., 2019). Initially classified as a species of the “persistent” group and a tree, was recently described rather as a tall shrub able to grow to a small tree (Fernández-Palacios et al., 2017). The present results reinforce the proposal to classify it with its own regeneration strategy as ‘understory specieś (Ganivet et al., 2019). Among the more than 4000 seedlings recorded between 2000 and 2003 and over 11,000 in 2011, none belonged to species in the shortlived or long-lived pioneer group. With less than 0.22% of the forest canopy in the gap phase registered when the study plots were implemented (Arévalo and Fernández-Palacios, 1998) and already at that time no major disturbances such as landslides, insect outbreaks or hurricanes have been recorded over the last 100 years (Arévalo and Fernández-Palacios, 1998). The seedling bank is almost exclusively composed of shade-tolerant or understory species confirming that this forest is still maturing (Ganivet et al. 2019). Even with survival rates of 12% (leeward) and 5% (windward) over 12 years (Fernández-Lugo et al., 2015) recorded growth rates indicate that virtually no seedlings can reach the canopy before two or more decades. The results confirm previous projections that showed that in the absence of high intensity and/or frequent disturbances asexual reproduction is of relatively greater importance and decreases the magnitude of successional shifts (Arévalo et al. 1999). Studies with larger spatial extent and longer duration are invaluable for understanding plant population dynamics (Clark et al., 1999). Without the additional census (2011) our conclusions would be very limited. After 11 years only six individuals attained a stem > 1 m and there were great differences in density between censuses not explained by exceptional climatic events or episodic large-scale disturbance. Climatic data and models predicted a downward shift of the cloud belt (Sperling et al., 2004), an increase in average temperature (Martín et al., 2012) and a significant wind intensity increase (Cropper and Hanna, 2014) in the Canaries. Under these climatic changes species

Fig. 7. Distribution of growth rate (cm year−1) classes overall (A) and by species (B). Growth rates classes (g) are given in cm/year. Class 0 = 0 cm; class 1 = 0 < g ≤ 1; class 2 = 1 < g ≤ 2; class 3 = 2 < g ≤ 3; …… class 10 = 9 < g ≤ 10; class > 10 > 10 cm year−1. Symbols: Laurus novocanariensis (LANO), Persea indica (PEIN), Picconia excelsa (PIEX), Apollonias barbujana (APBA) and Viburnum rigidum (VITI).

probability of fungi incidence is greater but high soil moisture improves host survival (Hersh et al., 2012). For the Macaronesian archipelagos a significant increase in wind intensity has been noticed in the last decades (Cropper and Hanna, 2014), which can lead to more frequent damages in tree crown and to changes in the understorey light environment. Unfortunately, we do not have available data for wind patterns for the monitoring interval. Tree species regenerating by asexual reproduction were poorly represented and species with a viable seed bank strategy were absent among the ca. 15,000 seedlings tagged. Shade-tolerant species dominate the seedling bank, but there are some differences between them Szwagrzyk et al. (2015). The density increment of P. indica in the 2011–12 census was lower than for L. novocanariensis, but conversely the former displayed the highest relative growth rate, while V. rigidum and L. novocanariensis showing the lowest, suggesting a certain “regeneration niche differentiation” (sensu Grubb, 1977) between species of this group and a trade-off between growth and reproductive effort as widely reported (Hubbell and Foster, 1992). On the other hand, the increase of individual numbers of Ilex and Heberdenia in the last census could be correlated with a small-scale disturbance. Ilex species regenerate preferentially by vegetative resprout (Fernández-Palacios et al., 2017), whereas Heberdenia species is a relatively rare species that regenerate exclusively by advanced regeneration, i.e., by seedlings or saplings that are already present in the understory. Maybe for these species small scales episodic disturbances could be the key for a change from a prevalence of asexual reproduction 8

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redistribution does not always occur directly via a downward or upward altitudinal shift of the actual distribution (Moritz et al., 2008; Chen et al., 2009). These changes can lead to a laurel forest with a distinct relative species abundance and disturbance regime than nowadays. Long-term studies are critical to understand the forest dynamics and management decisions facing the conservation or restoration of this unique and vulnerable forest should be based on them.

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5. Conclusions To conclude, the apparent stability of the seedling bank observed in the first years was not confirmed in the following censuses, and there was a large increase in density in the last census with no significant relation with rainfall either annual or seasonal. As expected, species whose main regeneration strategy is asexual were poorly represented in the seedling bank while shade tolerant species were the most abundant. Growth rates were high for most species relative to other growth rates reported in the literature. Most individuals retain the seed for up to 2 months but for the three species of Lauraceae at least one seedling can retain the seed for more than 6 months. For the high seedling density recorded in the last census without a clear relationship to rare climatic events (< 5% frequency) such as drought, windstorms or high rainfall, we suggest that possibly small changes in one factor, probably illumination, present nonlinear responses in seedling recruitment. It was clear that if the study had been limited to the short-term census we would have changed part of our conclusions. Long-term demographic studies are indispensable for understanding the dynamics and natural regeneration of the forest. Author contribution Eduardo Pereira Cabral Gomes: Data curation, Methodology, Investigation, Formal analysis, Writing - original draft, Writing - review & editing. Lea de Nascimento: Data curation, Methodology, Investigation. Alistair Domínguez: Data curation, data organization. Eduardo Balguerías: Data curation, data organization. Javier Méndez: Methodology, Data curation, Investigation. Silvia FernándezLugo: Methodology, Data curation, Investigation. José Ramón Arévalo: Funding acquisition, Methodology, Investigation. José María Fernández-Palacios: Conceptualization, Funding acquisition, Project administration, Resources, Supervision, Writing - review & editing. Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper Acknowledgements We are grateful to Cristina Blandino, Gustavo Morales and Priscila Rodrıguez for assistance with fieldwork. Finally, we record our appreciation to anonymous reviewers for giving useful comments on an earlier version of this paper. Appendix A. Supplementary material Supplementary data to this article can be found online at https:// doi.org/10.1016/j.foreco.2020.118001. References Ancochea, E., Fúster, J.M., Ibarrola, E., Cendrero, A., Coello, J., Hernán, F., Cantagrel, J.M., Jamond, C., 1990. Volcanic evolution of the island of Tenerife (Canary Islands) in the light of new K-AR data. J. Volcan. Geotherm. Res. 44, 231–249. https://doi. org/10.1016/0377-0273(90)90019-C.

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