Miguel N. Bugalho

Mediterranean cork oak savannas require human use to sustain biodiversity and ecosystem services

Mediterranean cork oak savannas, which are found only in southwestern Europe and northwestern Africa, are ecosystems of high socioeconomic and conservation value. Characterized by sparse tree cover and a diversity of understory vegetation – ranging from shrub formations to grasslands – that support high levels of biodiversity, these ecosystems require active management and use by humans to ensure their continued existence. The most important product of these savannas is cork, a non-timber forest product that is periodically harvested without requiring tree felling. Market devaluation of, and lower demand for, cork are causing a decline in management, or even abandonment, of southwestern Europes cork oak savannas. Subsequent shrub encroachment into the savannas grassland components reduces biodiversity and degrades the services provided by these ecosystems. In contrast, poverty-driven overuse is degrading cork oak savannas in northwestern Africa. “Payment for ecosystem services” schemes, such as Forest S...

Plant wax alkanes and alcohols as herbivore diet composition markers

Abstract The n-alkanes in plant cuticular wax have been used as markers for estimating the species composition of herbivore diets, but the long-chain fatty alcohols (LCOH) of plant wax may also be useful. The objective of this research was to assess if LCOH contributed extra information to differentiate plant species, compared with n-alkanes only. We used 3 data sets consisting of n-alkane and LCOH concentrations of plant species occurring in pastures of New South Wales, Australia. We used Principal Component Analysis (PCA) to summarise the data for n-alkane and LCOH concentrations obtained for the species in these data sets. The first 3 principal components explained 86 to 93% and 75 to 99% of the variance in n-alkane and LCOH concentrations, respectively. Orthogonal Procrustes Rotation (OPR) was then used to compare the results of PCA conducted with n-alkane and LCOH data, with a view to establishing whether LCOH provided discriminatory information in addition to that provided by the n-alkanes. Results of OPR indicated that this was so for all 3 data sets, and suggested that the LCOH would be useful additional markers for discriminating between plant species. We tested this by using Discriminant Analysis and cross-validation procedures in 2 data sets to distinguish between defined species groups of C3 grasses, C4 grasses, clovers and Lotus spp. The discrimination between these categories and the proportion of plant species correctly classified into the defined categories was better when using n-alkanes and LCOH together, compared with alkanes alone. Our results indicate that LCOH provided additional information that could be used for distinguishing plant species as part of estimating the species composition of herbivore diets.

Cuticular wax alkanes and alcohols used as markers to estimate diet composition of sheep (Ovis aries)

Abstract The chemical components in plant cuticular wax can be used as markers to estimate the species composition of the diet of grazing animals. In this experiment, sheep ( Ovis aries ) grazed swards consisting of two sown species of Lotus ( L. corniculatus and L. pedunculatus ), two sown grasses ( Phalaris aquatica and Austrodanthonia richardsonii ) and volunteer annual grasses and legumes (dominated by Vulpia myuros and Trifolium spp.). The botanical composition of the sward was estimated before and after grazing over three days by four sheep. During the grazing period, samples of whole plants of the species present, plus rectal faecal samples from the sheep, were collected, freeze-dried and ground prior to the extraction of cuticular wax n-alkanes and long-chain alcohols. Purified alkanes and alcohols in samples of faeces and plants were quantified by gas chromotography. The species composition of the sheep diets was estimated by relating faecal alkane and alcohol contents to those of the plant species on offer, using the ‘EatWhat’ software package. Principal Components Analysis explained 75% of the variance in the pattern of alkane concentrations between the species on the first two axes. PCA using alcohols accounted for 68% of the variance on the first two axes and separated the Lotus species from the grasses and clovers. Comparison of the two PCA, using Orthogonal Procrustes Rotation, indicated that the long-chain alcohols contributed extra information over and above that provided by the alkanes. Discriminant analysis of alkane and alcohol concentrations enabled a clear separation of Lotus , clover and grass species groups. Using alkanes as markers, the diet consumed by sheep contained 18±1.1% Lotus , whilst using both alkanes and alcohols, the estimated Lotus content of the diet (26±1.2%) was closer to the Lotus content of the sward (31%). Diet composition estimates indicated that the Lotus component consisted mostly (>90%) of L. corniculatus . This apparent selection against L. pedunculatus may relate to the much higher condensed tannin content in that species.

Direct and indirect effects of tree canopy facilitation in the recruitment of Mediterranean oaks

Summary 1. Tree recruitment in Mediterranean ecosystems is strongly limited at the seedling stage by drought. Increasing evidence shows the critical positive role of the canopy nurse effect on seedling survival which results from direct and indirect, positive and negative interactions between species. 2. Most studies, however, have only focused on the effects of tree canopy on water and light, ignoring other critical factors affecting seedling regeneration, such as canopy effects on high temperatures and the competing herb biomass. 3. Here, we evaluate how tree canopy cover and removal of herbs affect the survival and growth of seedlings of two dominant Mediterranean Quercus species during a 3-year study. We use an integrated model that combines several data sets to quantify and predict regeneration dynamics along environmental gradients of soil moisture, temperature and light. 4. Low soil moisture, increased soil temperature and herb biomass negatively affected seedling survival of both Quercus species. Seedling growth was positively associated with increasing soil moisture and light. 5. Although tree canopy cover directly facilitated seedling survival in both Quercus species, it also negatively affected herb biomass and thus indirectly facilitated the survival of Quercus suber, but not of Quercus ilex seedlings at low levels of soil moisture. 6. Overall, tree canopies increased seedling survival but not growth during the establishment phase, mainly by ameliorating the effects of low soil moisture and high temperatures. Tree canopy indirectly facilitated survival of Q. suber seedlings by negatively affecting the competing herb layer. 7. Synthesis and applications. To improve tree recruitment and conserve Mediterranean Quercus woodlands, the removal of herbs should be integrated into management plans for dry habitats. Interactions between abiotic and biotic factors may also effect the regeneration of these tree species. In particular, a healthy tree canopy will become important for providing conditions to facilitate seedling establishment if these habitats become drier and warmer, as predicted by some climate change scenarios.

Synergy of extreme drought and shrub invasion reduce ecosystem functioning and resilience in water-limited climates

Extreme drought events and plant invasions are major drivers of global change that can critically affect ecosystem functioning and alter ecosystem-atmosphere exchange. Invaders are expanding worldwide and extreme drought events are projected to increase in frequency and intensity. However, very little is known on how these drivers may interact to affect the functioning and resilience of ecosystems to extreme events. Using a manipulative shrub removal experiment and the co-occurrence of an extreme drought event (2011/2012) in a Mediterranean woodland, we show that native shrub invasion and extreme drought synergistically reduced ecosystem transpiration and the resilience of key-stone oak tree species. Ecosystem transpiration was dominated by the water use of the invasive shrub Cistus ladanifer, which further increased after the extreme drought event. Meanwhile, the transpiration of key-stone tree species decreased, indicating a competitive advantage in favour of the invader. Our results suggest that in Mediterranean-type climates the invasion of water spending species and projected recurrent extreme drought events may synergistically cause critical drought tolerance thresholds of key-stone tree species to be surpassed, corroborating observed higher tree mortality in the invaded ecosystems. Ultimately, this may shift seasonally water limited ecosystems into less desirable alternative states dominated by water spending invasive shrubs.

Assessing foraging strategies of herbivores in Mediterranean oak woodlands: a review of key issues and selected methodologies

Montados are agro-silvo-pastoral ecosystems, typical of the Southwest Iberian Peninsula, of high socio-economic and conservation importance, where grazing is a dominant activity. Montados are characterized by an open tree canopy of Quercus sp. and a diverse undercover of shrubs and grasslands that constitute the plant food resources for grazing animals. Plant food resources of Montados are highly variable, both spatially and seasonally, in quantity and quality. Reliable and easy to use methods to monitor grazing are necessary to allow proper understanding of foraging strategies of grazing animals and to set sustainable grazing management. We describe the main characteristics of the plant food resources available for grazing animals, striking its variability, and revise the potential of using N-alkanes and saliva proteome methods to assess foraging strategies in Montados. In a scenario of dynamic multiple choices, we discuss the use of n-alkane methodology for the simultaneous estimation of diet composition and voluntary intake and saliva proteome as a mean of increasing the knowledge on diet adjustments.

Using the high conservation value forest concept and Pareto optimization to identify areas maximizing biodiversity and ecosystem services in cork oak landscapes

Montados are silvo-pastoral systems, typical of the western Mediterranean Basin. When well managed, these ecosystems provide relevant ecosystem services and biodiversity conservation. In the northern part of the Mediterranean Basin, cork oak areas are mainly privately owned and a source of income to landowners, chiefly through cork and livestock production. Sustainable use is essential to maintain the ecological sustainability and socio-economic viability of these ecosystems. Biodiversity conservation and non-provisioning ecosystem services may generate additional incentives promoting sustainable use and conservation of montados, but require adequate mapping and identification. The high conservation value forest (HCVF) framework allows systematic inventory of biodiversity and non-provisioning ecosystem services and is widely applied in forest ecosystems. Here we exemplify the application of HCVF to the cork oak landscape of southern Portugal using a WebGIS tool that integrates the HCVF framework, in conjunction with Pareto optimization, to identify areas important for the conservation of biodiversity and ecosystem services. We present a case study using threatened bird and reptile species, as examples of biodiversity attributes, and carbon storage and water recharge rate of aquifers, as examples of ecosystem services attributes. We identify those areas in a cork oak landscape of southern Portugal where biodiversity and ecosystem services attributes are optimized. These areas can be prioritized for implementing conservation mechanisms, such as payment for ecosystem services, to promote sustainable forest management.

Using n-alkanes to estimate diet composition of herbivores: a novel mathematical approach

N-alkanes are long-chain saturated hydrocarbons occurring in plant cuticles that can be used as chemical markers for estimating the diet composition of herbivores. An important constraint of using n-alkanes to estimate diet composition with currently employed mathematical procedures is that the number of markers must be equal or larger than the number of diet components. This is a considerable limitation when dealing with free-ranging herbivores feeding on complex plant communities. We present a novel approach for the estimation of diet composition using n-alkanes which applies equally to cases where the number of markers is lower, equal or greater than the number of plant species in the diet. The model uses linear programming to estimate the minimum and maximum proportions of each plant in the diet, and avoids the need for grouping species in order to reduce the number of estimated dietary components. We illustrate the model with two data sets of n-alkane content of plants and faeces obtained from a sheep grazing experiment conducted in Australia and a red deer study in Portugal. Our results are consistent with previous studies on those data sets and provide additional information on the proportions of individual species in the diet. Results show that sheep included in the diet high proportions of white clover (from 0.25 to 0.37), and relatively high proportions of grasses (e.g. brome from 0.14 to 0.26) but tended to avoid Lotus spp. (always less than 0.04 of the diet). For red deer we found high proportions of legumes (e.g. Trifolium angustifolium and Vicia sativa reaching maximum proportions of 0.42 and 0.30 of the diet, respectively) with grasses being less important and Cistus ladanifer, a browse, also having relevance (from 0.21 to 0.42 of the diet).

Habitat use at fine spatial scale: how does patch clustering criteria explain the use of meadows by red deer?

Large mammalian herbivores are keystone species in different ecosystems. To mediate the effects of large mammalian herbivores on ecosystems, it is crucial to understand their habitat selection pattern. At finer scales, herbivore patch selection depends strongly on plant community traits and therefore its understanding is constrained by patch definition criteria. Our aim was to assess which criteria for patch definition best explained use of meadows by wild, free-ranging, red deer (Cervus elaphus) in a study area in Northeast Portugal. We used two clustering criteria types based on floristic composition and gross forage classes, respectively. For the floristic criteria, phytosociological approach was used to classify plant communities, and its objectivity evaluated with a mathematical clustering of the floristic relevés. Cover of dominant plant species was tested as a proxy for the phytosociological method. For the gross forage classes, the graminoids/forbs ratio and the percentage cover of legumes were used. For assessing deer relative use of meadows we used faecal accumulation rates. Patches clustered according to floristic classification better explained selection of patches by deer. Plant community classifications based on phytosociology, or proxies of this, used for characterizing meadow patches resulted useful to understand herbivore selection pattern at fine scales and thus potentially suitable to assist wildlife management decisions.

Too Many Is Too Bad: Long-Term Net Negative Effects of High Density Ungulate Populations on a Dominant Mediterranean Shrub.

Plant–animal interactions imply costs and benefits with net balance depending on interacting species and ecological context. Ungulates, in particular, confer costs (e.g., plant leaf consumption, flower bud predation) and benefits (e.g., plant overcompensation, seed dispersal) to plants. Magnitude of costs and benefits may be altered by habitat management or ecological conditions favoring high density ungulate populations. Little is known however on whether plant costs or benefits predominate over the years, or the long-term outcomes of plant-animal interactions in habitat types sustaining high density ungulate populations. We investigated how high density ungulate populations alter plant costs and benefits by quantifying ungulate long-term effects on the shrub Cistus ladanifer (Cistaceae) individual size, seed weight and number, seed bank, and population density, through a 12-year ungulate exclusion experiment in a Mediterranean scrubland. We monitored plant size and flower buds in plants exposed or protected from ungulates and number of developed capsules and seeds consumed (potential seed dispersal) by ungulates during three reproductive seasons. We found that ungulates negatively affected shrub size and led to a dramatically decline of shrub reproductive structures and seed production, affecting the plant reproductive cycle. Number of buds was 27 times higher and number of developed seed 5 times higher in ungulate-excluded as compared to ungulate-exposed plots. After 9 years of ungulate exclusion, the C. ladanifer seed bank was 2.6 times higher in ungulate-excluded plots. The population density of C. ladanifer was 4 times higher in ungulate-excluded plots. Our long-term experiment showed that high density ungulate populations can alter plant-animal interactions by reducing plant benefits and increasing plant costs.