Luca Santini

A mid-term analysis of progress toward international biodiversity targets

In 2010, the international community, under the auspices of the Convention on Biological Diversity, agreed on 20 biodiversity-related “Aichi Targets” to be achieved within a decade. We provide a comprehensive mid-term assessment of progress toward these global targets using 55 indicator data sets. We projected indicator trends to 2020 using an adaptive statistical framework that incorporated the specific properties of individual time series. On current trajectories, results suggest that despite accelerating policy and management responses to the biodiversity crisis, the impacts of these efforts are unlikely to be reflected in improved trends in the state of biodiversity by 2020. We highlight areas of societal endeavor requiring additional efforts to achieve the Aichi Targets, and provide a baseline against which to assess future progress. Although conservation efforts are accelerating, their impact is unlikely to improve the global state of biodiversity by 2020. Indicators of progress and decline The targets set by the Convention on Biological Diversity in 2010 focused international efforts to alleviate global biodiversity decline. However, many of the consequences of these efforts will not be evident by the 2020 deadline agreed to by governments of 150 countries. Tittensor et al. analyzed data on 55 different biodiversity indicators to predict progress toward the 2020 targets—indicators such as protected area coverage, land-use trends, and endangered species status. The analysis pinpoints the problems and areas that will need the most attention in the next few years. Science, this issue p. 241

Human pressures predict species' geographic range size better than biological traits.

Geographic range size is the manifestation of complex interactions between intrinsic species traits and extrinsic environmental conditions. It is also a fundamental ecological attribute of species and a key extinction risk correlate. Past research has primarily focused on the role of biological and environmental predictors of range size, but macroecological patterns can also be distorted by human activities. Here, we analyse the role of extrinsic (biogeography, habitat state, climate, human pressure) and intrinsic (biology) variables in predicting range size of the worlds terrestrial mammals. In particular, our aim is to compare the predictive ability of human pressure vs. species biology. We evaluated the ability of 19 intrinsic and extrinsic variables in predicting range size for 4867 terrestrial mammals. We repeated the analyses after excluding restricted-range species and performed separate analyses for species in different biogeographic realms and taxonomic groups. Our model had high predictive ability and showed that climatic variables and human pressures are the most influential predictors of range size. Interestingly, human pressures predict current geographic range size better than biological traits. These findings were confirmed when repeating the analyses on large-ranged species, individual biogeographic regions and individual taxonomic groups. Climatic and human impacts have determined the extinction of mammal species in the past and are the main factors shaping the present distribution of mammals. These factors also affect other vertebrate groups globally, and their influence on range size may be similar as well. Measuring climatic and human variables can allow to obtain approximate range size estimations for data-deficient and newly discovered species (e.g. hundreds of mammal species worldwide). Our results support the need for a more careful consideration of the role of climate change and human impact - as opposed to species biological characteristics - in shaping species distribution ranges.

On how much biodiversity is covered in Europe by national protected areas and by the Natura 2000 network: insights from terrestrial vertebrates

The European Union has made extensive biodiversity conservation efforts with the Habitats and Birds Directives and with the establishment of the Natura 2000 network of protected areas, one of the largest networks of conservation areas worldwide. We performed a gap analysis of the entire Natura 2000 system plus national protected areas and all terrestrial vertebrates (freshwater fish excluded). We also evaluated the level of connectivity of both systems, providing therefore a first estimate of the functionality of the Natura 2000 system as an effective network of protected areas. Together national protected areas and the Natura 2000 network covered more than one-third of the European Union. National protected areas did not offer protection to 13 total gap species (i.e., species not covered by any protected area) or to almost 300 partial gap species (i.e., species whose representation target is not met). Together the Natura 2000 network and national protected areas left 1 total gap species and 121 partial gap species unprotected. The terrestrial vertebrates listed in the Habitats and Birds Directives were relatively well covered (especially birds), and overall connectivity was improved considerably by Natura 2000 sites that act as stepping stones between national protected areas. Overall, we found that the Natura 2000 network represents at continental level an important network of protected areas that acts as a good complement to existing national protected areas. However, a number of problems remain that are mainly linked to the criteria used to list the species in the Habitats and Birds Directives. The European Commission initiated in 2014 a process aimed at assessing the importance of the Birds and Habitats Directives for biodiversity conservation. Our results contribute to this assessment and suggest the system is largely effective for terrestrial vertebrates but would benefit from further updating of the species lists and field management.

Role of African protected areas in maintaining connectivity for large mammals

The African protected area (PA) network has the potential to act as a set of functionally interconnected patches that conserve meta-populations of mammal species, but individual PAs are vulnerable to habitat change which may disrupt connectivity and increase extinction risk. Individual PAs have different roles in maintaining connectivity, depending on their size and location. We measured their contribution to network connectivity (irreplaceability) for carnivores and ungulates and combined it with a measure of vulnerability based on a 30-year trend in remotely sensed vegetation cover (Normalized Difference Vegetation Index). Highly irreplaceable PAs occurred mainly in southern and eastern Africa. Vegetation cover change was generally faster outside than inside PAs and particularly so in southern Africa. The extent of change increased with the distance from PAs. About 5% of highly irreplaceable PAs experienced a faster vegetation cover loss than their surroundings, thus requiring particular conservation attention. Our analysis identified PAs at risk whose isolation would disrupt the connectivity of the PA network for large mammals. This is an example of how ecological spatial modelling can be combined with large-scale remote sensing data to investigate how land cover change may affect ecological processes and species conservation.

(Un-)expected nocturnal activity in "diurnal" Lemur catta supports cathemerality as one of the key adaptations of the lemurid radiation

The ability to operate during the day and at night (i.e., cathemerality) is common among mammals but has rarely been identified in primates. Adaptive hypotheses assume that cathemerality represents a stable adaptation in primates, while nonadaptive hypotheses propose that it is the result of an evolutionary disequilibrium arising from human impacts on natural habitats. Madagascar offers a unique opportunity to study the evolution of activity patterns as there we find a monophyletic primate radiation that shows nocturnal, diurnal, and cathemeral patterns. However, when and why cathemeral activity evolved in lemurs is the subject of intense debate. Thus far, this activity pattern has been regularly observed in only three lemurid genera but the actual number of lemur species exhibiting this activity is as yet unknown. Here we show that the ring-tailed lemur, Lemur catta, a species previously considered to be diurnal, can in fact be cathemeral in the wild. In neighboring but distinct forest areas these lemurs exhibited either mainly diurnal or cathemeral activity. We found that, as in other cathemeral lemurs, activity was entrained by photoperiod and masked by nocturnal luminosity. Our results confirm the relationship between transitional eye anatomy and physiology and 24-h activity, thus supporting the adaptive scenario. Also, on the basis of the most recent strepsirrhine phylogenetic reconstruction, using parsimony criterion, our findings suggest pushing back the emergence of cathemerality to stem lemurids. Flexible activity over 24-h could thus have been one of the key adaptations of the early lemurid radiation possibly driven by Madagascars island ecology.

Contrasting changes in the abundance and diversity of North American bird assemblages from 1971 to 2010

Although it is generally recognized that global biodiversity is declining, few studies have examined long-term changes in multiple biodiversity dimensions simultaneously. In this study, we quantified and compared temporal changes in the abundance, taxonomic diversity, functional diversity, and phylogenetic diversity of bird assemblages, using roadside monitoring data of the North American Breeding Bird Survey from 1971 to 2010. We calculated 12 abundance and diversity metrics based on 5-year average abundances of 519 species for each of 768 monitoring routes. We did this for all bird species together as well as for four subgroups based on breeding habitat affinity (grassland, woodland, wetland, and shrubland breeders). The majority of the biodiversity metrics increased or remained constant over the study period, whereas the overall abundance of birds showed a pronounced decrease, primarily driven by declines of the most abundant species. These results highlight how stable or even increasing metrics of taxonomic, functional, or phylogenetic diversity may occur in parallel with substantial losses of individuals. We further found that patterns of change differed among the species subgroups, with both abundance and diversity increasing for woodland birds and decreasing for grassland breeders. The contrasting changes between abundance and diversity and among the breeding habitat groups underscore the relevance of a multifaceted approach to measuring biodiversity change. Our findings further stress the importance of monitoring the overall abundance of individuals in addition to metrics of taxonomic, functional, or phylogenetic diversity, thus confirming the importance of population abundance as an essential biodiversity variable.

Ecological and Anthropogenic Correlates of Activity Patterns in Eulemur

The ultimate determinants of cathemerality, i.e., activity spread over the 24-h cycle, in primates have been linked to various ecological factors. Owing to the fast rate of habitat modification, it is imperative to know whether and how this behavioral flexibility responds to anthropogenic disturbance. The true lemurs (Eulemur clade) constitute a valuable case to study these potential effects, as all species studied so far exhibit cathemerality. Here we explored the effects of anthropogenic disturbance on activity patterns of Eulemur while controlling for ecological factors proposed as determinants of activity shifts. We first performed a meta-analysis using 13 long-term studies conducted over the last three decades on various populations of Eulemur. We fitted a beta regression using the proportion of diurnality (the activity taking place between sunrise and sunset) as the response variable and seven climatic, ecological, and anthropogenic disturbance variables at each site as predictors. We also present a validation with original data using year-round, 24-h activity of collared brown lemurs (Eulemur collaris) in forest fragments with different levels of disturbance in southeastern Madagascar. Diurnality was prevalent at most sites. Seasonality, proportions of leaves in the diet, and group size were all found to be significant predictors of the proportion of diurnal activity. After controlling for socioecological factors in the model, overall anthropogenic disturbance emerged as a negative predictor of diurnality. Our validation suggests that the lemurs in the more disturbed area exhibited more nocturnal activity than those in the less disturbed area. It is unclear whether the plasticity observed might allow populations of Eulemur to persist in disturbed areas longer than lemurs with less flexible activity patterns.

Dietary Flexibility and Feeding Strategies of Eulemur: A Comparison with Propithecus

Despite the great variety of habitats in Madagascar, Eulemur has successfully populated most forested habitats on the island. Although the high dietary flexibility of Eulemur is often credited as one of the drivers of its evolutionary success, other behavioral evidence suggests a limited capacity for dietary switching. To shed light on the feeding strategies of Eulemur, we compared the dietary flexibility between populations of this genus with that of another widespread lemur taxon, Propithecus. We hypothesized that Eulemur would show greater dietary flexibility than Propithecus, which has a digestive system specialized for folivory, and that Eulemur living in dry forests would switch its diet from fruit to other food seasonally. To examine these hypotheses, we performed a phylogenetic least-squares analysis on 10 populations of Eulemur and 7 of Propithecus to assess the contribution of environmental variables and body mass on their dietary flexibility while controlling for phylogenetic relatedness. Eulemur relied heavily on fruit and did not show large variations in primary food over the year. Propithecus consumed leaves and fruits equally and exhibited considerable flexibility across seasons. Therefore, in contrast to our predictions, the anatomical specialization for fiber digestion heightens dietary flexibility in Propithecus. At the intrageneric level, we found similar ecogeographic variation; populations of both genera with heavier body mass consumed more fruit. As we predicted, Eulemur in drier habitats switched the diet from fruit to alternative food more frequently. To compensate for low dietary flexibility, Eulemur mostly adopts a power-feeding strategy by which it increases energy expenditure to acquire patchily distributed fruit resources.

Performance tradeoffs in target‐group bias correction for species distribution models

Species distribution models (SDMs) are often calibrated using presence- only datasets plagued with environmental sampling bias, which leads to a decrease of model accuracy. In order to compensate for this bias, it has been suggested that background data (or pseudoabsences) should represent the area that has been sampled. However, spatially-explicit knowledge of sampling effort is rarely available. In multi-species studies, sampling effort has been inferred following the target-group (TG) approach, where aggregated occurrence of TG species informs the selection of background data. However, little is known about the species- specific response to this type of bias correction. The present study aims at evaluating the impacts of sampling bias and bias correction on SDM performance. To this end, we designed a realistic system of sampling bias and virtual species based on 92 terrestrial mammal species occurring in the Mediterranean basin. We manipulated presence and background data selection to calibrate four SDM types. Unbiased (unbiased presence data) and biased (biased presence data) SDMs were calibrated using randomly distributed background data. We used real and TG-estimated sampling efforts in background selection to correct for sampling bias in presence data. Overall, environmental sampling bias had a deleterious effect on SDM performance. In addition, bias correction improved model accuracy, and especially when based on spatially-explicit knowledge of sampling effort. However, our results highlight important species-specific variations in susceptibility to sampling bias, which were largely explained by range size: widely-distributed species were most vulnerable to sampling bias and bias correction was even detrimental for narrow-ranging species. Furthermore, spatial discrepancies in SDM predictions suggest that bias correction effectively replaces an underestimation bias with an overestimation bias, particularly in areas of low sampling intensity. Thus, our results call for a better estimation of sampling effort in multispecies system, and cautions the uninformed and automatic application of TG bias correction. This article is protected by copyright. All rights reserved.

A Composite Network Approach for Assessing Multi-Species Connectivity: An Application to Road Defragmentation Prioritisation

One of the biggest challenges in large-scale conservation is quantifying connectivity at broad geographic scales and for a large set of species. Because connectivity analyses can be computationally intensive, and the planning process quite complex when multiple taxa are involved, assessing connectivity at large spatial extents for many species turns to be often intractable. Such limitation results in that conducted assessments are often partial by focusing on a few key species only, or are generic by considering a range of dispersal distances and a fixed set of areas to connect that are not directly linked to the actual spatial distribution or mobility of particular species. By using a graph theory framework, here we propose an approach to reduce computational effort and effectively consider large assemblages of species in obtaining multi-species connectivity priorities. We demonstrate the potential of the approach by identifying defragmentation priorities in the Italian road network focusing on medium and large terrestrial mammals. We show that by combining probabilistic species graphs prior to conducting the network analysis (i) it is possible to analyse connectivity once for all species simultaneously, obtaining conservation or restoration priorities that apply for the entire species assemblage; and that (ii) those priorities are well aligned with the ones that would be obtained by aggregating the results of separate connectivity analysis for each of the individual species. This approach offers great opportunities to extend connectivity assessments to large assemblages of species and broad geographic scales.