Estimation of species shifts
Out of the 252 species with an occurrence above 50 at each inventory and with good identification reliability, 251 displayed a significant global model of distribution (P < 0.001). Among these, 175 had both a unimodal (bell-shaped) response curve along the altitudinal gradient (a different from 0 at the P < 0.05 level and a negative) and a calculated optimum, Optelev, between 0 and 2200 m a.s.l. Seventy-four out of these 175 species showed a significant shift of the optimum elevation (Table 1, and see Appendix S2). For illustration, two examples of observed and modelled data are presented in Fig. 5, one of an ascending species and the other of a descending species.
Figure 5. Observed frequency distribution (dotted line) and modelled probability of presence (full line) at each inventory (1985 in grey and 1999 in black) along the elevation gradient for two selected species: one shifting downward (Quercus petraea, left) and one shifting upward (Teucrium chamaedrys, right). The modelled probability of presence was calculated using the observed average value of exposure for each species at each inventory.
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Table 1. Number of species responding to elevation in a quadratic logistic model and displaying an altitudinal shift between the last two national forest inventories (1985–1999) in all forest types and in closed forests alone
| ||Number of species displaying a global significant response||No response to elevation or optimum outside the sampled range||Unimodal response curve to elevation and optimum within the sampled range|
|Descending species all species (sign. shift)||Ascending species all species (sign. shift)|
|All forests||251||76||62 (18)||113 (56)|
|Closed forests only||231||67||63 (23)||101 (39)|
The total number of ascending species was 1.8 times higher than that of descending species (113 and 62 species, respectively) and this difference was significant (Fisher's exact test, P < 0.001). When considering significant shifts only, three times more species displayed an upward shift than a downward shift and this difference was also significant (56 and 18 species, respectively, Fisher's exact test, P < 0.001; Table 1, Appendix S3).
Over the 175 species responding to elevation in a unimodal way, the mean altitudinal shift was positive and significantly different from zero (+17.9 m, P < 0.05). Interestingly, species with an optimum below 1300 m a.s.l. displayed, on average, a much larger shift (+35.4 m, n = 113 species, P < 0.001; Appendix S3) than those having their optimum above 1300 m a.s.l. (n = 62, mean shift not significant). The shift even tended to reverse for the few species having an optimum elevation above 1800 m a.s.l. When only considering the 74 species shifting significantly, the mean shift was +47.3 m (significantly different from zero, P < 0.05)
Along the exposure gradient, only 45 species displayed both a bell-shaped distribution (d different from 0 at the P < 0.05 level and d negative) and a calculated optimum, Optexpo, between −1 and 1, of which 21 shifted northward and 24 southward. Among these, only nine showed a significant shift of their exposure optimum, with three species shifting significantly northward and six southward. The mean exposure shift was not significantly different from zero. The analysis will not be developed further on exposure shift since the response appears negligible.
Species shifts and plant species traits
We analysed differences in species traits according to their shift in elevation. Odds ratio and mean elevation shifts for categorical traits are listed by trait category in Table 2. Mean values of quantitative traits for descending and ascending species are presented in Table 3. Values of the main traits are given in Appendix S2 for species displaying both a unimodal response curve to elevation and an optimum within the sampled range. Species optimum elevation in 1999 as a function of the optimum elevation in 1985 are presented for different traits categories in Appendix S3.
Table 2. Number of descending and ascending species (desc./asc.) between 1985 and 1999, odds ratio (o.r.) and mean species shifts for different plant trait categories, in all forest types (left) and only in closed forests (right)
| ||Species shift in all forests||Species shift in closed forests only|
|Number of species (desc./asc.)||o.r.||Mean (m)||Number of species (desc./asc.)||o.r.||Mean (m)|
| Raunkiaer's life form |
| Phanerophytes||48 (14/34)||1.48||+44.5**||47 (18/29)||1.01||+1.2|
|Evergreen phanerophytes||18 (9/9)||0.51||+1.3||18 (12/6)||0.27**||−9.0|
|Deciduous phanerophytes||30 (5/25)||3.24*||+70.4**||29 (6/23)||2.80*||+7.6|
| Nanophanerophytes (incl. ev. and dec.)||42 (9/33)||2.43*||+25.9||38 (12/26)||1.47||+2.2|
| Chamaephytes||32 (13/19)||0.76||+40.0||30 (7/23)||2.36||+17.1|
|Woody chamaephytes||25 (9/16)||0.97||+50.1*||24 (3/21)||5.25**||+50.2**|
|Herbaceous chamaephytes||7 (4/3)||0.39||+1.8||6 (4/2)||0.30||−115.1|
| Hemicryptophytes||33 (15/18)||0.59||+7.0||31 (17/14)||0.43*||+3.5|
| Geophytes||19 (11/8)||0.35*||−88.0*||17 (9/8)||0.52||−85.1*|
| Therophytes||1 (0/1)||/||+65.7||1 (0/1)||/||+186.0|
| Woodiness |
| Herbaceous species||60 (30/30)||0.39**||−22.7||55 (30/25)||0.36**||−33.5|
| Woody species||115 (32/83)||2.59**||+39.0***||109 (33/76)||2.76**||+12.3|
|Tall trees||32 (10/22)||1.26||+54.2**||31 (12/19)||0.98||−9.0|
|Low trees and shrubs||83 (22/61)||2.13*||+33.2||78 (21/57)||2.59**||+20.8|
| Deciduousness |
| Evergreen||48 (19/29)||0.44*||+19.0||45 (19/26)||0.47||−1.1|
| Deciduous||71 (16/55)||2.25*||+49.3***||67 (17/50)||2.15||+8.4|
| Dynamic stages |
| Found in immature stages||128 (42/86)||1.52||+22.2*||119 (41/78)||1.82||+5.2|
| Not found in immature stages||47 (20/27)||0.66||+6.0||45 (22/23)||0.55||−24.9|
| Pioneer habit |
| Non-pioneer species||34 (11/23)||0.48||+38.3*||33 (11/22)||1.78||−1.7|
| Pioneer species||16 (3/13)||2.07||+49.4*||17 (8/9)||0.56||+2.7|
| Dispersal mode |
| Gravity/autodispersed||21 (6/15)||1.26||+21.9||20 (4/16)||2.56||+32.3|
|Gravity||18 (6/12)||0.98||+20.1||17 (2/15)||4.93*||+37.0*|
| Wind||42 (14/28)||0.97||+53.4**||37 (15/22)||0.78||+11.6|
| Ants||12 (6/6)||0.46||−25.4||9 (5/4)||0.43||−48.2|
| Birds||29 (8/21)||1.36||+30.4||26 (10/16)||0.89||+16.6|
| Other animals||45 (15/30)||0.97||+4.6||46 (16/30)||1.10||−25.3|
| Biogeography |
| Ubiquitous||142 (48/94)||1.44||+17.6||135 (50/85)||1.38||−5.6|
| Exclusively mountainous||33 (14/19)||0.69||+18.8||29 (13/16)||0.72||+9.0|
| All species ||175 (62/113)|| ||+17.9*||164 (63/101)|| ||−3.0|
Table 3. Mean value of quantitative traits for descending and ascending species, in all forests and only in closed forests
| ||Mean value of quantitative traits for descending/ascending species|
|In all forests||In closed forests only|
|Light (Landolt)||2.7/3.1* (n = 150)||2.7/3.1** (n = 141)|
|Temperature (Landolt)||3.4/3.9** (n = 150)||3.6/3.9 (n = 141)|
|Moisture (Landolt)||2.5/2.2 (n = 147)||2.5/2.2* (n = 138)|
|Seed Mass (mg, Leda)||179.8/187.5* (n = 107)||327.0/106.0 (n = 98)|
Landolt's indicator values were available for 150 species among the 175 studied (Table 3). Ascending species had a significantly (n = 150, P < 0.01 in a Student's t-test) higher mean Landolt's indicator value for temperature (T = 3.9) than descending species (T = 3.4), meaning that they were more thermophilous. The difference in Landolt's indicator values for light was also significant (n = 150, P < 0.05), with again a higher mean value for ascending species (L = 3.1) than for descending species (L = 2.7), meaning that ascending species were more light demanding. The two indicator values for temperature and light were significantly, but not highly, correlated among the set of studied species (Spearman rank correlation r = 0.33, n = 150, P < 0.001; see also Appendix S4). There were no other significant differences in Landolt's indicator values.
Raunkiaer's life forms were available for all the 175 studied species (see details in Table 2). They were significantly not randomly distributed between ascending and descending species (Fisher's exact test of association: P < 0.05). Relative to other categories, there were more ascending species belonging to deciduous phanerophytes (o.r. = 3.24), deciduous nanophanerophytes (o.r. = 2.35) and evergreen nanophanerophytes (o.r. = 1.98), whereas there were relatively more descending species among evergreen phanerophytes (o.r. = 0.51), herbaceous chamaephytes (o.r. = 0.39), hemicryptophytes (o.r. = 0.59) and geophytes (o.r. = 0.35). Woody chamaephytes did not display any departure from the general trend. In terms of average elevation shifts, only geophytes showed a significant downward shift (−88.0 m) whereas deciduous phanerophytes (+70.4 m) and woody chamaephytes (+50.1 m) showed a significant upward shift. The upward response of nanophanerophytes was large (mean shift = +25.9 m, o.r. = 2.43), mainly due to the shift of deciduous nanophanerophytes (+27.2 m).
When comparing all woody species pooled together (phanerophytes, nanophanerophytes and woody chamaephytes) against all herbaceous species (herbaceous chamaephytes, hemicryptophytes and geophytes), the odds ratios were highly different from one (2.59 for woody species), indicating a strong tendency for woody species to shift upward and the reverse for herbaceous species (see Appendix S3). Woody species displayed an average altitudinal shift of +39.0 m, significantly different from zero.
Both low and tall woody species were significantly shifting upward. But only low trees had an odds ratio significantly different from one, i.e., a higher relative proportion of ascending species in comparison with all other herbaceous or tall tree species (Table 2).
The information about deciduousness was mostly available for woody species. Deciduous species were significantly more shifting upward (o.r. = 2.25) than evergreen species, with a mean shift of +49.3 m, significantly different from zero (n = 71). The difference became even more significant when considering phanerophytes only, with an odds ratio of 2.92 for deciduous species (51 ascending and 12 descending among deciduous vs 16 ascending and 11 descending among evergreens).
Seed masses were available in the Leda Traitbase for 107 out of the 175 studied species. Seed mass was significantly higher among ascending species (mean = 187.5 mg) than among those descending (mean = 179.8 mg) when considering all 107 species (t-test of difference in means of the logarithms, n = 107, P < 0.05). However, it must be pointed out that a significant positive relationship exists between seed mass and woodiness (n = 107, P < 0.001, r² = 0.15 in an analysis of variance of woodiness effect on seed mass logarithm; see also Appendix S4).
Considering the species according to their presence in stages of forest development, there were relatively more ascending species among species found in early stages (o.r. = 1.52) than among other species (o.r. = 0.66), and the former displayed a larger shift (mean = +22.2 m) than the latter (mean = +6.0 m). The same trend was observed for pioneer vs non-pioneer species. However, because this latter information was only available for woody species, both categories displayed a significant upward shift.
Species dispersed by ants were less ascending than those with other dispersal modes (o.r. = 0.46) and presented a negative average shift, although not significant. In contrast, species dispersed by birds were slightly more ascending than other species (o.r. = 1.36, not significant).
There were no marked differences between species restricted to mountain belts and ubiquitous species. However, there were less ascending species among exclusively mountain species (o.r. = 0.69) than among ubiquitous species (o.r. = 1.44).
Species shifts and successional dynamics
When considering closed forests only, the sampling area was restricted to 1 266 803 ha at the first inventory (11 745 plots) and 1 733 310 ha (12 623 plots) at the second one. Closed forests still showed a significant ageing trend at most of the lowest elevations classes (Fig. 4). This was also accompanied by a homogeneous increase of basal area throughout the elevation gradient (Fig. 4).
When fitting the logistic model to data from closed forests alone, 164 species (Table 1) showed a bell-shaped response to elevation (compared to 175 with all the data), among which 63 were descending and 101 ascending (ratio = 1.60, vs 1.82 in all forests). Although the number of species shifting upward was higher than that of descending species, the mean elevation shift was no longer significantly different from zero and even became negative (−3.0 m) (Table 2). Out of these 164 species, 62 species presented a shift statistically significantly different from zero, among which 23 were descending and 39 ascending (odds ratio of 1.70, mean of −8.4 m).
Ascending species still had a significantly higher mean Landolt's indicator value for light (mean L = 3.1) than descending species (mean L = 2.7, n = 141, P < 0.01). The difference was no longer significant for temperature (P = 0.09). A difference appeared for the moisture indicator value, with more hygrophilous species among descending species (mean indicator value for moisture F = 2.5) than ascending species (F = 2.2, n = 134, P < 0.05).
The most prominent difference from previous results was that average shifts were lower, more often negative and no longer significantly different from zero for most of the plant trait categories (light-demanding species, ubiquitous species, phanerophytes, woody species, tall and low trees, deciduous species, species found in immature stages of forest dynamics, pioneer and non-pioneer species, species dispersed by wind), although the relative number of species shifting upward (o.r.) was still significant for some of those categories (Table 2). Evergreen phanerophytes and hemicryptophytes displayed a significant odds ratio for ascending vs descending behaviour in closed forests, whereas it was not significant in the entire sample, although in the same direction (relatively more descending species). Woody chamaephytes comprised many more ascending species (o.r. = 5.25), whereas they did not show any pattern in the entire sample. For the pioneering habit, the pattern was reversed in closed forests in comparison to that in all forests: pioneer species comprised relatively less ascending species. Species dispersed by gravity, which displayed no trend in the entire sample, were now composed of more ascending than descending species (o.r. = 4.93), and their mean shift was significantly positive (+37.0 m).