Nurse plants,tree saplings and grazing pressure: changes in facilitation along a biotic environmental gradient

Current conceptual models predict that an increase in stress shifts interactions between plants from competitive to facilitative; hence, facilitation is expected to gain in ecological importance with increasing stress. Little is known about how facilitative interactions between plants change with increasing biotic stress, such as that incurred by consumer pressure or herbivory (i.e. disturbance sensu Grime). In grazed ecosystems, the presence of unpalatable plants is reported to protect tree saplings against cattle grazing and enhance tree establishment. In accordance with current conceptual facilitation-stress models, we hypothesised a positive relationship between facilitation and grazing pressure. We tested this hypothesis in a field experiment in which tree saplings of four different species (deciduous Fagus sylvatica, Acer pseudoplatanus and coniferous Abies alba, Picea abies) were planted either inside or outside of the canopy of the spiny nurse shrub Rosa rubiginosa in enclosures differing in grazing pressure (low and high) and in exclosures. During one grazing season we followed the survival of the different tree saplings and the level of browsing on these; we also estimated browsing damage to the nurse shrubs. Shrub damage was highest at the higher grazing pressure. Correspondingly, browsing increased and survival decreased in saplings located inside the canopy of the shrubs at the high grazing pressure compared to the low grazing pressure. Saplings of both deciduous species showed a higher survival than the evergreens, while sapling browsing did not differ between species. The relative facilitation of sapling browsing and sapling survival – i.e. the difference between saplings inside and outside the shrub canopy – decreased at high grazing pressure as the facilitative species became less protective. Interestingly, these findings do not agree with current conceptual facilitation-stress models predicting increasing facilitation with abiotic stress. We used our results to design a conceptual model of facilitation along a biotic environmental gradient. Empirical studies are needed to test the applicability of this model. In conclusion, we suggest that current conceptual facilitation models should at least consider the possibility of decreasing facilitation at high levels of stress.     

Conditional outcomes in plant–herbivore interactions: neighbours matter

Spatial distribution of palatable and unpalatable plants can influence the foraging behaviour of herbivores, thereby changing plant‐damage probabilities. Moreover, the immediate proximity to certain plants can benefit other plants that grow below them, where toxicity or spines act as a physical barrier or concealment against herbivores. This paper presents the results of a multi‐scale experiment performed to test the effect of shrubs as protectors of tree saplings against herbivores and the mechanism involved in Mediterranean ecosystems. We performed a factorial design in two mountain ranges, similar in physiognomy and vegetation, planting saplings of a palatable tree, the maple (Acer opalus subsp. granatense), and an unpalatable tree, the black pine (Pinus nigra), under three different types of shrubs. We considered four experimental microhabitats: highly palatable shrub (Amelanchier ovalis), palatable but spiny shrub (Crataegus monogyna or Prunus ramburii), unpalatable spiny shrub (Berberis vulgaris subsp. australis) and control (gaps of bare soil without shrubs). Three main factors were found to determine the probability of sapling attack: sapling palatability, experimental microhabitat and plot. Palatable saplings (maples) were browsed much more than unpalatable ones (pines). The degree of protection provided by the shrub proved greater as its palatability decreased with respect to sapling palatability, the unpalatable spiny shrub being the safest microhabitat for palatable saplings and bare soil for unpalatable ones. The differences found in number of attacked saplings between plots may be attributable to differences in herbivore pressure. The community context in which interaction takes place, namely the characteristics of the neighbours and the intensity of herbivore pressure, are determining factors for understanding and predicting the damage undergone by a target plant species. The mechanism that best explains these results is associational avoidance of saplings that grow near to unpalatable shrubs. It is necessary to introduce this neighbour effect in theoretical models and food‐web approaches that analyse the plant–herbivore relationships, since it can strongly determine not only the intensity of the interaction, but also the spatial distribution and diversity of the plant community.     

Does the strength of facilitation by nurse shrubs depend on grazing resistance of tree saplings?

Facilitation of tree regeneration by nurse shrubs that offer protection against large herbivores is an important driver of wood-pasture dynamics. Here we asked whether the response to facilitation by nurse shrubs depends on the grazing resistance of the protégé saplings. We experimentally tested the protective effects of the thorny Rosa rubiginosa on browsing frequency, survival, and biomass change of saplings of two species-groups, presumably differing in grazing resistance: the coniferous Abies alba and Picea abies and the deciduous Acer pseudoplatanus and Fagus sylvatica saplings. The saplings were planted under and outside (1.5 m) planted nurse shrubs, under zero, low and high grazing intensity. In total, 1920 young saplings were transplanted to 60 blocks and followed for 1 year.Although the number of saplings browsed did not differ between species-groups, the coniferous saplings showed lower resistance to cattle browsing (i.e. lower survival and growth rates) than the deciduous saplings. The less resistant coniferous saplings benefited significantly more from nurse shrubs than the more resistant deciduous species in terms of growth of the surviving saplings, but not in terms of overall survival. This was likely due to herbivory on the nurse shrubs causing incidental browsing on protégé saplings and differences in biomass off-take. At high grazing intensity facilitative effects of the nurse shrubs decreased, especially for the coniferous species.These results have important management implications for the endangered wood-pastures in Western Europe. For a sustainable management and conservation that allows tree recruitment, grazing intensity should remain low to best promote facilitation processes for all tree species, but in particular for the less resistant conifer saplings.     

From protégé to nurse plant: establishment of thorny shrubs in grazed temperate woodlands

Question: Thorny shrubs play keystone roles in grazed ecosystems by defending non‐protected plants against herbivores, but their establishment in grazed ecosystems is poorly understood. Which factors control establishment of recruits of thorny nurse shrubs in grazed temperate woodlands? Location: Ancient grazed temperate woodlands (52°32′N, 6°36′E), The Netherlands. Methods: We surveyed biotic and abiotic factors for saplings of thorny nurse shrubs in plots with and without saplings. To disentangle these factors, we performed a transplantation experiment over two growing seasons with nurse shrub saplings (Prunus spinosa and Crataegus monogyna) planted in two dominant vegetation types – tall unpalatable swards and short grazed lawns – half of them protected from herbivory via exclosures. Results: Plots with shrub saplings had taller surrounding vegetation, higher soil pH and higher soil moisture than plots without saplings. These plots predominantly contained unpalatable sward species, while plots without saplings mainly contained palatable lawn species. After transplantation, sapling survival was higher in exclosures than in the open, and higher in sward exclosures than in lawn exclosures. Sapling growth was higher in swards than in lawns, higher inside than outside exclosures, and higher for Prunus than Crataegus, while browsing on saplings was higher in lawns. Conclusion: Unpalatable swards form essential establishment niches for thorny shrubs in grazed temperate woodlands: they protect against herbivores before thorns fully develop in saplings, and sapling growth is better due to improved micro‐environmental conditions. Once established and thorny, shrub saplings grow out of the protective range of the swards and in turn facilitate tree seedlings, which are essential for long‐term persistence of grazed temperate woodlands. This study shows that nurse plants may start as protégés before becoming facilitators for other plants in a later life stage. This may be common for nurse plants in various ecosystems. We argue that improved understanding of establishment of nurse plants and their constraining factors is crucial for effective conservation and restoration in various ecosystems.     

Limits of pine forest distribution at the treeline: herbivory matters

Herbivores can affect future forest composition by feeding selectivity. At temperature-sensitive treelines, herbivory can exacerbate or constrain climate-driven distributional shifts in tree species. This study analyses the impact of herbivory in a Mediterranean treeline of widespread Pinus sylvestris and P. nigra pinewoods, testing whether herbivory damage reinforces or inhibits the climatic responses of these trees. We used naturally occurring sapling pairs of similar size and age of both species, thereby isolating plant characteristics from environmental effects in herbivore behaviour. Herbivory damage by ungulates proved higher than that caused by insects in saplings of both species. Low plant density and extreme abiotic conditions at the treeline could in part be responsible for the observed low incidence of insect herbivory. Ungulates preferred P. sylvestris over P. nigra, implying heavier browsing damage for a large number of P. sylvestris saplings, suffering reduced internode growth as a consequence. In addition, P. sylvestris could not compensate height-growth reductions due to browsing with higher growth rate than P. nigra. In fact, P. sylvestris showed similar or lower relative height growth with respect to P. nigra. Under a scenario of increasing aridity and maintenance of ungulate populations, the upward migration of P. sylvestris in its southern range could be restricted by higher drought vulnerability than P. nigra, a situation exacerbated by ungulate herbivory. Our results indicate that ungulate herbivory reinforces climatic response of coexisting P. sylvestris and P. nigra at treeline, favouring a potential change in community dominance towards Mediterranean P. nigra.     

The influence of competition from herbaceous vegetation and shade on simulated browsing tolerance of coniferous and deciduous saplings

The ability of saplings to tolerate browsing (i.e. the ability to persist with reduced biomass and to compensate for biomass loss) is influenced by the level of stress and their growth strategies. Ultimately, insight into species‐specific responses of saplings to browsing, shade and competition from neighbours will help explain diversity, structure and function of grazed ecosystems such as the endangered wood‐pasture systems. We measured the survival, whole‐sapling biomass and compensatory growth responses of two coniferous (Picea abies and Abies alba) and two deciduous (Acer pseudoplatanus and Fagus sylvatica) tree species to simulated summer browsing (one single clipping event), shade (installation of a shade cloth) and neighbour removal (mowing surrounding vegetation to ground level) treatments and the interactions between them after two‐growing seasons. For all species, there were interacting effects on growth of browsing and environmental condition (shade and neighbours). Simulated browsing resulted in relatively smaller growth losses when plants were growing slowly due to competitive conditions related to herbaceous neighbours. Although none of the clipped saplings could fully compensate for their biomass losses, the saplings were closer to compensation under high competitive conditions than under low competitive conditions. Survival of the clipped saplings remained relatively high and was only significantly reduced for Picea and Acer. Picea was least tolerant of competition and was the only species for which growth was not negatively affected by strong irradiance of a mountain pasture. Surprisingly, the tolerance of saplings to herbivory as browsing tolerance was enhanced under conditions that negatively affected sapling performance (i.e. survival and growth). Apparently, the relative impact of browsing at the early sapling stage is linked to tree life history characteristics such as competition and shade tolerance and will be lower in situations with intense competitive interactions and/or strong irradiance.     

Disentangling herbivore impacts on Populus tremuloides: a comparison of native ungulates and cattle in Canada’s Aspen Parkland

Ungulates impact woody species’ growth and abundance but little is understood about the comparative impacts of different ungulate species on forest expansion in savanna environments. Replacement of native herbivore guilds with livestock [i.e., beef cattle (Bos taurus)] has been hypothesized as a factor facilitating trembling aspen (Populus tremuloides Michx.) encroachment into grasslands of the Northern Great Plains. We used a controlled herbivory study in the Parklands of western Canada to compare the impact of native ungulates and cattle on aspen saplings. Native ungulate treatments included a mixed species guild and sequences of herbivory by different ungulates [bison (Bison bison subsp. bison), elk (Cervus elaphus) then deer (Odocoileus hemionus); or deer, elk, then bison]. Herbivory treatments were replicated in three pastures, within which sets of 40 marked aspen saplings (<1.8 m) were tracked along permanent transects at 2-week intervals, and compared to a non-grazed aspen stand. Stems were assessed for mortality and incremental damage (herbivory, leader breakage, stem abrasion and trampling). Final mortality was greater with exposure to any type of herbivore, but remained similar between ungulate treatments. However, among all treatments, the growth of aspen was highest with exposure only to cattle. Herbivory of aspen was attributed primarily to elk within the native ungulate treatments, with other forms of physical damage, and ultimately sapling mortality, associated with exposure to bison. Overall, these results indicate that native ungulates, specifically elk and bison, have more negative impacts on aspen saplings and provide evidence that native and domestic ungulates can have different functional effects on woody plant dynamics in savanna ecosystems.     

森林光环境对4种乔木幼树光合和光谱反射特性的影响

在林窗、林缘、林下3种自然光环境下,对吉林蛟河阔叶红松林常见树种拧筋槭、白牛槭、色木槭和红松的光合和光谱特性进行对比研究,以期从生理生态角度探讨它们对自然光环境的适应能力和响应机制。结果表明：4种乔木幼树叶片的光饱和点（LSP）和光补偿点（LCP）随着生长环境光强的下降而减小,林下各树种幼树LSP和LCP显著低于林窗内幼树（P<0.05）;除白牛槭外林下其他树种最大净光合效率（P_nmax）均显著小于林窗内幼树（P<0.05）;不同树种幼树表观量子效率（AQY）和暗呼吸速率（R_d）随光环境的变化并没有出现明显的变化规律,各环境间差异较小。除白牛槭外,其他树种幼树叶绿素归一化指数（Chl NDI）随环境光强的减少而增大,林下树种的光化学反射指数（PRI）普遍高于光条件更好环境下树种,说明林下幼树叶片叶绿素含量和光合速率大于其他光环境;各树种植物叶片水分指数（WI）在不同光环境之间存在显著差异,环境光强越大植物叶片WI越小,植物叶片水分浓度越小。林缘下3种槭属幼树结构不敏感植被光谱指数（SIPI）显著小于其他光环境（P<0.05）,说明林缘下幼树受到相对较小的环境胁迫。林窗内,红松具有最高的LCP、LSP、P_nmax、R_d和PRI,说明红松具有较高的光合潜力,更加适应高光生长环境,3种槭属中,白牛槭拥有最高的Chl NDI和PRI值,表现出较好的适应性,说明红松和白牛槭能在林窗环境内较好更新并逐步占据林冠层。     

Shoot growth and tree architecture of saplings of the major canopy dominants in a warm-temperate rainforest

Sapling density, shoot growth, and sapling architecture were studied in five major canopy dominants both under closed canopy and gaps in a warm-temperate rainforest. The five species showed wide variations in distribution, shoot growth, and sapling architecture. Distylium racemosum and Quercus acuta had significantly higher sapling densities under closed canopy than in gaps. Castanopsis sieboldii and Machilus thunbergii had significantly higher sapling densities in gaps than under closed canopy. Quercus salicina showed no significant difference in sapling density between the two habitats. Under closed canopy, C. sieboldii and M. thunbergii had wider crowns than the other species. Distylium racemosum had the greatest number of terminal shoots among the species. Quercus acuta had a branchless small crown. Quercus salicina showed intermediate values in crown width, depth and the number of terminal shoots among the species. Distylium racemosum showed the greatest height-growth rate among the species under the closed canopy, but was the slowest in gaps. Castanopsis sieboldii and M. thunbergii showed the greatest height-growth rates among the species in gaps. Quercus salicina showed the slowest height-growth rates both under closed canopy and gaps. All of the five species showed low mortality under closed canopy. For the major canopy dominants: (i) sapling architecture may not be an important factor in determining mortality but it may be important for height-growth rate; and (ii) sprouting helps saplings to survive until gap formation and facilitates rapid growth in the gaps.     

Spatial patterns and associations in a Quercus‐Betula forest in northern China

Question: Are species‐specific regeneration strategies and competition the dominant processes facilitating species coexistence in a Quercus liaotungensis dominated temperate deciduous forest? Location: Dongling Mountains, North China, 1300 m a.s.l. Methods: Ripley's K‐function was used to characterize the spatial patterns and spatial associations of two dominant tree species, Quercus liaotungensis and Betula dahurica, and a common subcanopy species, Acer mono, at different growth stages (adult, sapling, seedling). Results: Seedlings, saplings and adults of all three species exhibited clumped distributions at most spatial scales. Quercus seedlings and saplings were positively associated with conspecific adult trees and spatially independent of dead trees suggesting that seed dispersal and vegetative regeneration influenced the spatial patterning of Quercus trees. Betula seedlings and saplings were positively associated with both live and dead trees of conspecific adults at small scales (<5 m) but negatively associated with live and dead trees of other species indicating sprouting as an important mechanism of reproduction. Saplings of Acer had a strong spatial dependence on the distribution of conspecific adult trees indicating its limited seed dispersal range. Negative associations between adult trees of Betula and Quercus demonstrated interspecific competition at local scales (<5 m). Conclusions: Different regeneration strategies among the three species play an important role in regulating their spatial distribution patterns, while competition between individuals of Betula and Quercus at the adult stage also contributes to spatial patterning of these communities. The recruitment limitations of Betula and Quercus may affect the persistence of these species and the long‐term dynamics of the forest.