Ivy (Hedera helix L.) dynamics in riverine forests ...

Forest Ecology and Management 236 (2006) 12–17 www.elsevier.com/locate/foreco

Ivy (Hedera helix L.) dynamics in riverine forests: Effects of river regulation and forest disturbance Annik Schnitzler *, Patricia Heuze´ Universite´ Paul Verlaine, Laboratoire Biodiversite´ et Fonctionnement des Ecosyste`mes (LBFE) Campus Bridoux, Avenue du Ge´ne´ral Delestraint, 57070 Metz Cedex, France Received 13 December 2005; received in revised form 16 May 2006; accepted 23 May 2006

Abstract Ivy (Hedera helix L.) favours moist nutrient-rich substrates of the floodplains of Western Europe. In this study we investigated ivy dynamics in two forest reserves of the upper Rhine. The aim was to determine the influence of flooding on ivy development following the cessation of cuttings at two forest sites of contrasting flooding regimes: the Rhinau Reserve is currently flooded while the Erstein site has not been flooded for 30 years. We also examined the impacts of severe storms in 1993 and 1999 and a long-lasting flood that occurred in 1999. Our results show that the population of Rhinau was smaller and younger because ivy is severely limited by long periods of anoxia, even though it is favoured by regular short-period floods. Indeed, juvenile growth was more rapid at Rhinau where nutrient and moist conditions are more favourable than in Erstein, but mortality was higher because of the long-lasting flood of 1999. At Erstein, the ivy showed a tendency to clump around several big trees, especially oaks and ashes, which may make the host tree vulnerable to windfall. Uprooted or broken ivies were found to survive better than the fallen host tree but could not climb to another trunk highlighting a strong dependence of ivy on its hosting tree. # 2006 Elsevier B.V. All rights reserved. Keywords: Hedera helix; Population dynamics; Floodplain

1. Introduction Knowledge of the taxonomy, ecology, physiology, genetics, and past glacial history of English ivy (Hedera helix L.) and subspecies has improved during recent decades (Hoflacher and Bauer, 1982; Clergeau, 1992; Nola, 1997; Grivet and Petit, 2002; Sack and Grubb, 2002; Metcalfe, 2005). The Hedera genera (split into many subspecies) is widely distributed throughout Europe and adjacent regions (e.g. Russia, North Africa, Macaronesian Islands). It favours moist nutrient-rich substrates, warm summers and mild winters, and is part of many forest and shrub communities thanks to ready capacity to polyploidy (Ackerfield and Wen, 2003; Vargas et al., 1999). In the floodplains of Europe, the presence and even abundance of ivy at all strata makes them a focus of interest to biologists, because the ivy can reach impressive sizes and develops as a single tree, which is rare for the species (Carbiener, 1970; Walter, 1979; Beekman, 1984; Tre´molie`res et al., 1998; Badre et al.,

* Corresponding author. Tel.: +33 3 87 37 84 27; fax: +33 3 87 37 84 25. E-mail address: [email protected] (A. Schnitzler). 0378-1127/$ – see front matter # 2006 Elsevier B.V. All rights reserved. doi:10.1016/j.foreco.2006.05.060

1998; Deiller et al., 2001; Heuze´ et al., 2005). The abundance of giant woody vines in riverine forests has been interpreted as a sign of globally exceptional conditions for the coexistence of woody elements. Favourable conditions include regular disturbances, water and nutrient resources, and buffered temperatures associated with high moisture content in the understorey (Carbiener, 1970). Riverine forests are disturbed ecosystems, and the lianas are part of this unstable forested landscape at all steps of forest succession and dynamic phases (Walter, 1979; Gentry, 1991; Schnitzler, 1995; Allen et al., 2005). In addition, Tre´molie`res et al. (1988) consider that ivy has a positive impact at the ecosystem level, particularly for the host tree, which enjoys complementary nutrient inputs during spring with the foliage fall and experiences no significant reduction in growth. Ivy distribution in the upper Rhine forest is mostly described in the context of intensive management, where canopy lianas (Clematis vitalba, H. helix) are regularly cut down by foresters. However, since 1989, 50–180 ha blocks of forests in the upper Rhine have been strictly protected, including both flooded and unflooded sites, and this provides opportunities for describing ivy dynamics without any direct human interference. Ivy shows local invasions in places and a marked decrease in others; these

A. Schnitzler, P. Heuze´ / Forest Ecology and Management 236 (2006) 12–17

patterns could be linked to the inundation regime or severe environmental impacts during the period 1993–1999, during which time there was a thousand-year flood (1999) and two large storms (1993 and 1999). The main objective of the present study is to examine ivy population dynamics in these two floodplain forests of contrasting flooding regimes. Specific questions that we address are: (1) How do floods influence ivy structure and density? and (2) What are the retroactive processes that occur between ivy and forest disturbance patterns? 2. Study site The study area (488260 N, 78430 E) is situated in the upper part of the Rhine floodplain, northeast France, at about 148 m above sea level. The climate of the upper Rhine rift valley is continental with an oceanic influence; the mean annual temperature is 10 8C and the annual rainfall ranges from 500 to 600 mm. During the 19th and 20th centuries, alluvial braids and anastomosing sections of the upper Rhine were successively regulated by diversions, dams, and canals (Dister, 1987). A few sectors remained flooded (artificial islands between the Rhine and the Grand Canal d’Alsace), and these provide baseline information for assessing the impact of river regulation on riparian forests. Areas studied in the current project consist of oak-elm forest (Querco-Ulmetum minoris according to phytosociological classification, Schnitzler, 1994). Many record individuals remain in the canopy (Quercus robus, Fraxinus excelsior, Populus alba) and the understorey (Coylus avellana, Crataegus monogyna, Prunus spinosa, Malus sylvestris: 18–20 m high). There are two main woody lianas in the canopy: H. helix and C. vitalba. Architecture is characterized by a multi-stored, dense vegetation between 8 and 15 m in height (Fig. 1), and high levels of mean total species richness (about 32 species) and mean woody species richness (about 15 species). We characterized patterns of ivy in two natural reserves called Rhinau (311 ha) and Erstein (180 ha). These areas have been free of logging since their creation at the end of the 1980s, and lianas were no longer destroyed by woodcutters. The two reserves presented contrasting flooding histories: the Rhinau

Fig. 1. Structure of the oak-helm forest in Erstein and Rhinau (from Schnitzler, 1994).

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Reserve (311 ha) which floods briefly every year when the Rhine discharge exceeds 2500 m3 s!1, and the Erstein Reserve (180 ha) in which flooding was interrupted at the end of the 1960s by the construction of a large canal. Since elimination of floods, the Erstein forest has developed differently from Rhinau, with a net tendency to loss hygrophilic elements. Primary productivity is also lower, which explains the lower basal area measured in 1 ha in Erstein (23.7 m2 ha!1) and in Rhinau (34.6 m2 ha!1). In both areas, 5.6% of the trees were dead. The oak-elm forest community occupies only a very small area in Rhinau (around 12 ha) at the difference of Erstein (nearly the totality of the reserve). 3. Methods Sampling was carried out during the winter and spring of 2004–2005. Concerning Erstein, the plots were chosen within the better-preserved parts of the reserve, where the forest was very similar to the present-day 12 ha oak-elm forest of Rhinau, regarding species richness, architecture and tree age (Carbiener, oral communication). Thus, one limit of the present study was the lack of replication, impossible because of the too small area of oak-elm forest in the flooded site of Rhinau. 3.1. Ivy density, mortality, and interaction with host trees We studied both the juvenile and adult life phases of the ivy. We emphasize that the terms ‘juvenile’ and ‘adult’ denote exclusively the life phases and not the chronological age of the individual (Hoflacher and Bauer, 1982), because juveniles may be older than adults if they did not yet find opportunities for climbing. Ivy was recorded in terms of two categories of climbing ivies: (i) juveniles that are palmately lobed with 3–5 triangular lobes. We recorded only those that reached at least halfway up the host trunk, which corresponds to half of the potential height for the ivy and (ii) adults characterized by oval, entire leaves. Adults recorded were arbitrarily limited to those with a stem diameter >2 cm at breast height. Our study was carried out at two spatial scales. First, to evaluate the proportion of invaded hosts, the contribution of ivy to total basal area, and the ability of ivy to select hosts, all woody stems of >2.5 cm diameter at breast height (dbh) were inventoried and dbh was measured in a 100 m " 100 m (1 ha) plot located in a well-preserved part of each of the two forests. We limited the sample area to a single hectare because of the time and cost involved in such an evaluation, given the high densities of woody stems in the Rhine forests. Second, to study ivy density per strata, its tendency to clump, and its ability to survive windthrow of the host, we tagged and measured the dbh of all ivies and host trees (dead and alive) over a 10 ha area in each forest divided into 100 m " 100 m plots. The number of surviving host trees and ivy following disturbances was recorded. Species were also noted. We also used a x2-test to evaluate the influence of ivy on canopy and subcanopy tree-fall in the Erstein forest, in which a storm caused the felled of many big trees. Data were sourced

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from our results for the 10 ha area and from a previous study in the same area (Internal report, ONF 1985).

Table 1 General characteristics of the two ivy populations (data from ten 100 m " 100 m plots) Erstein Rhinau Statistics

3.2. Ages of the largest ivies Two cores were taken from the 35 largest ivies found in each of the two 10 ha areas, using a Pressler bore; the ivies were sampled as close as possible to the ground to obtain the maximum number of annual rings. Cores were then mounted and polished and rings were measured and counted using a binocular microscope and a digitizing tablet coupled to a computer at the INRA, Nancy, France. 3.3. Germination, growth and mortality during youth We examined germination, growth, and mortality during youth using two different methods. Densities of seedlings (recently germinated and seedlings aged 1 year) were counted within 20 plots of 1 m2 area in each forest. These plots were selected under the largest canopy ivies, and counting was conducted from September to December. All cases where ivy had begun to expand laterally were rejected, to assure that we counted only the very first steps of life (less than 1 year and 1 year). The growth of young climbing juveniles was examined by measuring the annual ivy height increment within each of the two 10 ha areas. For this purpose, we labelled ivies less than 2 m in height within a circle of 20 m diameter located within the middle of each 1 ha plot; the ivies were labelled in winter 2004 and measured again in winter 2005, including mortality. The features of the bark of the host tree (soft or rough) were also recorded. 3.4. Statistical analysis Most results were examined using a t-test. As only 10 values (1 ha!1) were available to describe densities, the nonparametric Mann–Whitney U-test was used to compare data between the two forests. For other data (dbh, age, and growth rate), the Mann–Whitney U-test was used when the distribution was not Gaussian; otherwise the t-test was used. x2 analysis was used to test the distribution homogeneity of dead or dying individuals and juvenile ivies from the two forests. The relationship between quantitative dbh and age data was tested using Pearson’s R. 4. Results 4.1. Structure of the ivy populations 4.1.1. Densities The mean density of ivy per hectare was significantly higher in Erstein (61.9 versus 29.4 stems per ha), although a higher proportion of juveniles was recorded in Rhinau (42.8% versus 14.6%; Table 1). The peak density of ivy was found in the Erstein subcanopy, with 24.5 ivies per ha. This is in sharp contrast with the Rhinau subcanopy, which housed only 4.9 ivies per ha (Table 2). Ivies were also more numerous in the understorey at Erstein (22.7 ivies per ha) than at Rhinau (14.2 ivies per ha).

Number of stem per hectare 61.9 Percentage of juveniles (1) 14.6 Percentage of dead or dying ivies 2.1 Mean age for 34 of the biggest ivies (2) 42.1 Mean dbh of adult ivies 5.7 Total number of host trees 48.5 Percentage of host trees with more than one ivy 26 Number of host trees with ivy and Clematis 14.5

29.4 42.8 4.3 26.7 5.1 35.5 0.2 0.4

b * a ** a * b ***

NS

b

b * a *** b ***

(1) More than half of the total height of the trunk, (2) time-lag for reaching the canopy excluded. Statistics: ax2-test, bMann–Whitney U-test. *P < 0.05; ** P < 0.01; ***P < 0.001; NS: non-significant.

4.1.2. Correlation between dbh host and dbh ivy Correlations between the dbh of host trees and of ivy indicate that small ivies are significantly more represented on of understorey hosts with small dbh values (Pearson’s R = 0.35, P < 0.001), but most of the ivies are adults and produce fruit. 4.1.3. Age The ivy population at Erstein is younger than that at Rhinau (42.1 years at Erstein; 26.7 years at Rhinau; Table 1). The oldest ivies at Erstein are at least 66 years old, while the oldest ivies at Rhinau are a maximum of 50 years old. The ages given in Table 1 are minimum values, as they rather reflect the time when the ivy took a climbing habit rather than its exact age. Indeed, in most cores, rings around the heart were not distinguishable, so the first ring measured with certainty did not correspond to the first year of growth (Heuze´ et al., 2005). The diameters of the largest adult ivies show a positive correlation with age (Pearson’s R = 0.71, P < 0.001). 4.1.4. Mortality pattern No senescent ivy was found in the area, even for the most aged individuals, suggesting that the population in 2005 is quite

Table 2 Distribution of ivy (juveniles and adults) and host tree per strata (data for ten 100 m " 100 m plots) Erstein

Rhinau

U-test

Canopy (1) Number of host trees per hectare Number of ivy per hectare Mean dbh of ivy (cm)

11 14.7 5.9

8.4 10.2 5.9

NS NS NS

Subcanopy (2) Number of host trees per hectare Number of ivy per hectare Mean dbh of ivy (cm)

16.9 24.5 6

4.9 4.9 6.9

***

Understorey (3) Number of host trees per hectare Number of ivy per hectare Mean dbh of ivy (cm)

19.5 22.7 4.2

13.8 14.2 3.3

***

NS NS NS **

(1) Height >25 m and dbh >60 cm, (2) height 15–25 m and dbh 40–59 cm, (3) height 7–14 m and dbh 10–39 cm. Mann–Whitney U-test. **P < 0.01; *** P < 0.001; NS: non-significant.


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young. Dead or dying ivies were, however, relatively abundant in relation to two main mortality episodes (Table 1): (i) prolonged floods in Rhinau (in this forest, the storms of 1993 and 1999 had little impact) and (ii) the impact of the two storms (1993 and 1999), which was very strong in Erstein. In this forest, 30 trees from the canopy and subcanopy suffered severe branch loss (3 stems per ha) or uprooting (5.5 stems per ha). Mortality of host was high: 73% after breakage and 78% after uprooting. Ivies survived better than hosts, with only 17% dying after breakage and 15% after uprooting. Survival after uprooting was problematic only if roots had been torn off during the fall, but even in this case ivy could survive thanks to the development of adventitious roots emerging from the trunk after the fall. When uprooted, ivies loose the foliage of the trunk in less than 3 years, keeping only the foliage of the crown.

Trees that hosted large ivies (a total of 191 trees, including 24 fallen trees) were more susceptible to fall than trees without ivies (1514 trees, including 41 fallen trunks; X2 = 79.4; d.f. = 1; P < 0.000). However, large, old trees are likely to have accumulated more ivy, and be more likely to fall down, than younger, small trees. We thus addressed the likelihood of collapse of ivy-covered versus ivy-free trees within hosting trees size classes. The sample size of canopy and subcanopy trees was reduced in such a way that the x2-test could not be run accurately (more than 20% of theoretical values