Floral free fall in the Swiss lowlands: environmental determinants of local plant extinction in a peri‐urban landscape

Biodiversity is severely threatened by habitat destruction. As a consequence of habitat destruction, the remaining habitat becomes more fragmented. This results in time-lagged population extirpations in remaining fragments when these are too small to support populations in the long term. If these time-lagged effects are ignored, the long-term impacts of habitat loss and fragmentation will be underestimated. We quantified the magnitude of time-lagged effects of habitat fragmentation for 157 nonvolant terrestrial mammal species in Madagascar, one of the biodiversity hotspots with the highest rates of habitat loss and fragmentation. We refined species' geographic ranges based on habitat preferences and elevation limits and then estimated which habitat fragments were too small to support a population for at least 100 years given stochastic population fluctuations. We also evaluated whether time-lagged effects would change the threat status of species according to the International Union for the Conservation of Nature (IUCN) Red List assessment framework. We used allometric relationships to obtain the population parameters required to simulate the population dynamics of each species, and we quantified the consequences of uncertainty in these parameter estimates by repeating the analyses with a range of plausible parameter values. Based on the median outcomes, we found that for 34 species (22% of the 157 species) at least 10% of their current habitat contained unviable populations. Eight species (5%) had a higher threat status when accounting for time-lagged effects. Based on 0.95-quantile values, following a precautionary principle, for 108 species (69%) at least 10% of their habitat contained unviable populations, and 51 species (32%) had a higher threat status. Our results highlight the need to preserve continuous habitat and improve connectivity between habitat fragments. Moreover, our findings may help to identify species for which time-lagged effects are most severe and which may thus benefit the most from conservation actions.

Summary1. A critical need in conservation biology is to determine which species are most vulnerable to extinction. Freshwater mussels (Bivalvia: Unionacea) are one of the most imperilled faunal groups globally. Freshwater mussel larvae are ectoparasites on fish and depend on the movement of their hosts to maintain connectivity among local populations in a metapopulation.2. I calculated local colonisation and extinction rates for 16 mussel species from 14 local populations in the Red River drainage of Oklahoma and Texas, U.S. I used general linear models and AIC comparisons to determine which mussel life history traits best predicted local colonisation and extinction rates.3. Traits related to larval dispersal ability (host infection mode, whether a mussel species was a host generalist or specialist) were the best predictors of local colonisation.4. Traits related to local population size (regional abundance, time spent brooding) were the best predictors of local extinction. The group of fish species used as hosts by mussels also predicted local extinction and was probably related to habitat fragmentation and host dispersal abilities.5. Overall, local extinction rates exceeded local colonisation rates, indicating that local populations are becoming increasingly isolated and suffering an ‘extinction debt’. This study demonstrates that analysis of species traits can be used to predict local colonisation and extinction patterns and provide insight into the long‐term persistence of populations.

This paper investigates how different prioritizations of species for conservation can affect both the number of breeding individuals that receive protection and the distribution of conservation attention among different types of habitat. I use as a study example three red lists of the avifauna of Kanton Zurich in northern Switzerland. Species are weighted based on their placement in different red list categories to represent differences in species' relative conservation value. I examine how these weightings affect the number of breeding pairs benefiting from increasing conservation effort. Conservation effort is defined as the number of ranked land parcels that receive conservation attention, be it through habitat enhancement, protection, or other measures. I rank parcels' conservation value based on the number of weighted breeding pairs estimated for each parcel. Not surprisingly, the number of category-1, -2 and -3 breeding pairs that receive benefits varies greatly when different red lists are used. Changes in the relative conservation value of species in different categories influences both the number of breeding pairs and the number of parcels to receive conservation attention. The effect of increasing conservation effort on the number of breeding pairs and the proportion of each landscape type receiving attention also vary when different red lists and relative conservation values are used to determine conservation priorities. Use of the ‘official’ red list published by a governmental body (Bundesamt fur Umwelt, Wald und Landschaft, Bern, Switzerland) results in more emphasis on conservation in agricultural landscape than did use of either of the other two lists. The process of prioritization of sites for conservation should evaluate the effects of variation in both the relative conservation value of species and species categorization that may arise due to incomplete data and variation in opinion.

The importance of understanding species extinctions and its consequences for ecosystems and human life has been getting increasing public attention. Nonetheless, regardless of how pressing the current biodiversity loss is, with rare exceptions, extinctions are actually not immediate. Rather, they happen many generations after the disturbance that caused them. This means that, at any point in time after a given disturbance, there is a number of extinctions that are expected to happen. This number is the extinction debt. As long as all the extinctions triggered by the disturbance have not happened, there is a debt to be paid. This delay in extinctions can be interpreted as a window of opportunity, when conservation measures can be implemented. In this thesis, I investigated the relative importance of ecological and evolutionary processes unfolding after different disturbances scenarios, to understand how this knowledge can be used to improve conservation practices aiming at controlling extinctions. In the Introduction (chapter 1), I present the concept of extinction debts and the complicating factors behind its understanding. Namely, I start by presenting i) the theoretical basis behind the definition of extinction debts, and how each theory informed different methodologies of study, ii) the complexity of understanding and predicting eco-evolutionary dynamics, and iii) the challenges to studying extinctions under a regime of widespread and varied disturbance of natural habitats. I start the main body of the thesis (chapter 2) by summarizing the current state of empirical, theoretical, and methodological research on extinction debts. In the last 10 years, extinction debts were detected all over the globe, for a variety of ecosystems and taxonomic groups. When estimated - a rare occurrence, since quantifying debts requires often unavailable data - the sizes of these debts range from 9 to 90\% of current species richness and they have been sustained for periods ranging from 5 to 570 yr. I identified two processes whose contributions to extinction debts have been studied more often, namely 1) life-history traits that prolong individual survival, and 2) population and metapopulation dynamics that maintain populations under deteriorated conditions. Less studied are the microevolutionary dynamics happening during the payment of a debt, the delayed conjoint extinctions of interaction partners, and the extinction dynamics under different regimes of disturbances (e.g. habitat loss vs. climate change). Based on these observations, I proposed a roadmap for future research to focus on these less studies aspects. In chapters 3 and 4, I started to follow this roadmap. In chapter 3, I used a genomically-explicit, individual-based model of a plant community to study the microevolutionary processes happening after habitat loss and climate change, and potentially contributing to the settlement of a debt. I showed that population demographic recovery through trait adaptation, i.e. evolutionary rescue, is possible. In these cases, rather than directional selection, trait change involved increase in trait variation, which I interpreted as a sign of disruptive selection. Moreover, I disentangled evolutionary rescue from demographic rescue and show that the two types of rescue were equally important for community resistance, indicating that community re-assembly plays an important role in maintaining diversity following disturbance. The results demonstrated the importance of accounting for eco-evolutionary processes at the community level to understand and predict biodiversity change. Furthermore, they indicate that evolutionary rescue has a limited potential to avoid extinctions under scenarios of habitat loss and climate change. In chapter 4, I analysed the effects of habitat loss and disruption of pollination function on the extinction dynamics of plant communities. To do it, I used an individual, trait-based eco-evolutionary model (Extinction Dynamics Model, EDM) parameterized according to real-world species of calcareous grasslands. Specifically, I compared the effects of these disturbances on the magnitude of extinction debts and species extinction times, as well as how species functional traits affect species survival. I showed that the loss of habitat area generates higher number of immediate extinctions, but the loss of pollination generates higher extinction debt, as species take longer to go extinct. Moreover, reproductive traits (clonal ability, absence of selfing and insect pollination) were the traits that most influenced the occurrence of species extinction as payment of the debt. Thus, the disruption of pollination functions arose as a major factor in the creation of extinction debts. Thus, restoration policies should aim at monitoring the status of this and other ecological processes and functions in undisturbed systems, to inform its re-establishment in disturbed areas. Finally, I discuss the implications of these findings to i) the theoretical understanding of extinction debts, notably via the niche, coexistence, and metabolic theories, ii) the planning conservation measures, including communicating the very notion of extinction debts to improve understanding of the dimension of the current biodiversity crisis, and iii) future research, which must improve the understanding of the interplay between extinction cascades and extinction debts.

Intensification or abandonment of agricultural land use has led to a severe decline of semi-natural habitats across Europe. This can cause immediate loss of species but also time-delayed extinctions, known as the extinction debt. In a pan-European study of 147 fragmented grassland remnants, we found differences in the extinction debt of species from different trophic levels. Present-day species richness of long-lived vascular plant specialists was better explained by past than current landscape patterns, indicating an extinction debt. In contrast, short-lived butterfly specialists showed no evidence for an extinction debt at a time scale of c. 40 years. Our results indicate that management strategies maintaining the status quo of fragmented habitats are insufficient, as time- delayed extinctions and associated co-extinctions will lead to further biodiversity loss in the future.

Context Extinction debt, the time-delayed species loss response to fragmentation associated with habitat clearance, is a conservation concern for management of biological diversity globally. Extinction debt is well defined but difficult to measure owing to the long-term data needed to measure species loss, particularly for communities of long-lived species. Aims We aimed to estimate extinction debt for two adjacent threatened communities with contrasting soil fertility in south-western Australia: banksia and tuart woodlands. Further, we assessed what species functional traits are associated with extinction risk. Methods Using contemporary (2016) and historical (1992) data on vegetation richness, and patch characteristics dating back to the time of European colonisation (1829), we examined 60 woodland patches using three methods to detect and quantify extinction debt. Key results We found evidence of extinction debt in banksia woodland, but not in tuart woodland. We estimated the extinction debt for banksia woodlands as a future average loss of 28% or ~13 species per patch. Conclusions Our study demonstrated a delay of species loss consistent with extinction debt in one of two vegetation communities. Despite sharing species and traits, these vegetation communities have responded differently to landscape change over the same timescale and within the same landscape. Implications Understanding how vegetation communities, and functional trait types, respond to time-delayed impacts helps land managers to prioritise intervention efforts to pre-empt species decline and extinction through species conservation, and ecological restoration of remnant vegetation patches.

Effects of extractive disturbance on bird assemblages, vegetation structure and floristics in tropical scrub forest, Sariska Tiger Reserve, India

Extinction from habitat loss is the signature conservation problem of the twenty-first century. Despite its importance, estimating extinction rates is still highly uncertain because no proven direct methods or reliable data exist for verifying extinctions. The most widely used indirect method is to estimate extinction rates by reversing the species-area accumulation curve, extrapolating backwards to smaller areas to calculate expected species loss. Estimates of extinction rates based on this method are almost always much higher than those actually observed. This discrepancy gave rise to the concept of an 'extinction debt', referring to species 'committed to extinction' owing to habitat loss and reduced population size but not yet extinct during a non-equilibrium period. Here we show that the extinction debt as currently defined is largely a sampling artefact due to an unrecognized difference between the underlying sampling problems when constructing a species-area relationship (SAR) and when extrapolating species extinction from habitat loss. The key mathematical result is that the area required to remove the last individual of a species (extinction) is larger, almost always much larger, than the sample area needed to encounter the first individual of a species, irrespective of species distribution and spatial scale. We illustrate these results with data from a global network of large, mapped forest plots and ranges of passerine bird species in the continental USA; and we show that overestimation can be greater than 160%. Although we conclude that extinctions caused by habitat loss require greater loss of habitat than previously thought, our results must not lead to complacency about extinction due to habitat loss, which is a real and growing threat.

Agricultural production strategies: world experience

The extinction debt, delayed species extinctions following landscape degradation, is a widely discussed concept. But a consensus about the prevalence of extinctions debts is hindered by a multiplicity of methods and a lack of comparisons among habitats. We applied three contrasting species–area relationship methods to test for plant community extinction debts in three habitats which had different degradation histories over the last century: calcareous grassland, heathland and woodland. These methods differ in their data requirements, with the first two using information on past and current habitat area alongside current species richness, whilst the last method also requires data on past species richness. The most data‐intensive, and hence arguably most reliable method, identified extinction debts across all habitats for specialist species, whilst the other methods did not. All methods detected an extinction debt in calcareous grassland, which had undergone the most severe degradation. We conclude that some methods failed to detect an extinction debt, particularly in habitats that have undergone moderate degradation. Data on past species numbers are required for the most reliable method; as such data are rare, extinction debts may be under‐reported.

Temporal patterns of origination and extinction are essential components of many paleontological studies, but it has been difficult to obtain accurate rate estimates because the observed record of first and last appearances is distorted by the incompleteness of the fossil record. Here I analyze observed first and last appearances of marine animal and microfossil genera in a way that explicitly takes incompleteness and its variation into consideration. This approach allows estimates of true rates of origination and extinction throughout the Phanerozoic. Substantial support is provided for the proposition that most rate peaks in the raw data are real in the sense that they do not arise as a consequence of temporal variability in the overall quality of the fossil record. Even though the existence of rate anomalies is supported, their timing is nevertheless open to question in many cases. If one assumes that rates of origination and extinction are constant through a given stratigraphic interval, then peaks in revised origination rates tend to be displaced backward and extinction peaks forward relative to the peaks in the raw data. If, however, one assumes a model of pulsed turnover, with true originations concentrated at lower interval boundaries and true extinctions concentrated at upper interval boundaries, the apparent timing of extinction peaks is largely reliable at face value. Thus, whereas rate anomalies may well be real, precisely when they occurred is a question that cannot be answered definitively without independent support for a model of smooth versus pulsed rate variation. The pattern of extinction, particularly the major events, is more faithfully represented in the fossil record than that of origination. There is a tendency for the major extinction events to occur during stages in which the quality of the record is relatively high and for recoveries from extinctions to occur when the record is less complete. These results imply that interpretations of origination and extinction history that depend only on the existence of rate anomalies are fairly robust, whereas interpretations of the timing of events and the temporal covariation between origination and extinction may require substantial revision.

Herb layer extinction debt in highly fragmented temperate forests – Completely paid after 160 years?

A significant challenge in both measuring and predicting species extinction rates at global and local scales is the possibility of extinction debt, time-delayed extinctions that occur gradually following an initial impact. Here we examine how relative abundance distributions and spatial aggregation combine to influence the likely magnitude of future extinction debt following habitat loss or climate-driven range contraction. Our analysis is based on several fundamental premises regarding abundance distributions, most importantly that species abundances immediately following habitat loss are a sample from an initial relative abundance distribution and that the long-term, steady-state form of the species abundance distribution is a property of the biology of a community and not of area. Under these two hypotheses, the results show that communities following canonical lognormal and broken-stick abundance distributions are prone to exhibit extinction debt, especially when species exhibit low spatial aggregation. Conversely, communities following a logseries distribution with a constant Fisher's α parameter never demonstrate extinction debt and often show an "immigration credit," in which species richness rises in the long term following an initial decrease. An illustration of these findings in 25 biodiversity hotspots suggests a negligible immediate extinction rate for bird communities and eventual extinction debts of 30-50% of initial species richness, whereas plant communities are predicted to immediately lose 5-15% of species without subsequent extinction debt. These results shed light on the basic determinants of extinction debt and provide initial indications of the magnitude of likely debts in landscapes where few empirical data are available.

AimMany species exhibit a time‐lag between habitat loss and its extinction, resulting in extinction debt. Although extinction debt is considered a widespread phenomenon, differences in methodological approaches can affect its detection. We aim to contribute to this methodological debate by exploring whether extinction debt is either a phenomenon common to all patches or idiosyncratic to the patch and landscape attributes of a given patch. We also aim to determine whether the scale dependency of species richness might help to explain extinction debt.LocationSouthern Catalonia (NE Iberian Peninsula).MethodsWe studied the effects of habitat loss on plant species richness (total, specialists and generalists) in stable (habitat loss < 40% since 1956) and regressive (habitat loss more than 40% since 1956) patches of Mediterranean grasslands at both quadrat and patch scales using general linear models.ResultsWe detected extinction debt at patch scale but only in regressive patches. The magnitude of extinction debt was not constant but was related to the percentage of patch area reduction. Contrastingly, regressive patches presented fewer species than stable patches at quadrat scale.Main conclusionQuadrat scale extinctions in regressive patches lead to rarefaction, but not immediate extinction, of some species at patch scale and created an extinction debt. Species loss at quadrat scale constitutes an early warning indicator of the effects of habitat loss on biodiversity, while delayed extinctions offer an opportunity for conservation initiatives.

There are two major processes of species disassembly after landscape changes: non-random loss of species resulting in nested assemblages and species replacement resulting in spatial species turnover. Although time-lagged responses of species to landscape change have been widely recognized, few studies have empirically evaluated which of these two processes is more closely related to extinction debt (i.e., postponed species extinction following habitat loss). This study aimed to understand the underlying processes of extinction debt by partitioning β-diversity into components of species nestedness and species turnover. We measured grassland species richness at three spatial extents in a highly fragmented semi-natural grassland landscape in Japan. Dissimilarity-based β-diversity was partitioned into two components (i.e., nestedness-resultant dissimilarity [βsne] and turnover-resultant dissimilarity [βsim]), which were further analyzed using principal coordinates analyses (PCoA). The relationships between the variability of PCoA axis 1 scores and the current and past habitat proportions were evaluated. A significant positive relationship between current grassland species richness and past (i.e., the 1910s) grassland proportion was found at the largest spatial extent. The first axis of PCoA based on βsne showed significant correlation with past habitat proportions, whereas the PCoA axis based on βsim showed no significant correlation with either the current or past habitat proportions. A non-random loss of grassland species represented by nestedness underlay the extinction debt found at the landscape level. There is a chance of predicting the loss of species from the nested ranks of species which likely reflects the gradient of species vulnerability to historical landscape changes.