Species Diversity and Habitat Fragmentation Per Se: The Influence of Local Extinctions and Species Clustering.

AbstractAnthropogenic fragmentation of habitat is considered to be a critical factor contributing to the decline of species. However, a general consensus on the degree to which habitat loss and what has been called "habitat fragmentation per se" contribute to the loss of species diversity has not yet emerged. For empirical and theoretical reasons the topic has recently attracted renewed attention, thus reviving the "single large or several small" (SLOSS) debate. To study the effect of fragmentation per se, we use a spatially explicit and continuous, competitively neutral simulation model with immigration from a regional pool. The model accounts for the influence of ecological drift and intrafragment species clustering (due to limited dispersal) on local (plot) and global (landscape) diversity. We find that fragmentation increases global diversity but decreases local diversity, prominently so if fragments become more isolated. Cluster formation is a key mechanism reducing local diversity. By adding external disturbance events that lead to the occasional extinction of entire communities in habitat fragments, we show that the combined effect of such extinctions and cluster formation can create nonlinear interactive effects of fragmentation and fragment isolation on diversity patterns. We conclude that while in most cases fragmentation will decrease local and increase landscape diversity, universal predictions concerning the SLOSS debate should be taken with care.

Hill-Chao numbers allow decomposing gamma multifunctionality into alpha and beta components.

Biodiversity-ecosystem functioning (BEF) research has provided strong evidence and mechanistic underpinnings to support positive effects of biodiversity on ecosystem functioning, from single to multiple functions. This research has provided knowledge gained mainly at the local alpha scale (i.e. within ecosystems), but the increasing homogenization of landscapes in the Anthropocene has raised the potential that declining biodiversity at the beta (across ecosystems) and gamma scales is likely to also impact ecosystem functioning. Drawing on biodiversity theory, we propose a new statistical framework based on Hill-Chao numbers. The framework allows decomposition of multifunctionality at gamma scales into alpha and beta components, a critical but hitherto missing tool in BEF research; it also allows weighting of individual ecosystem functions. Through the proposed decomposition, new BEF results for beta and gamma scales are discovered. Our novel approach is applicable across ecosystems and connects local- and landscape-scale BEF assessments from experiments to natural settings.

Weather explains the decline and rise of insect biomass over 34 years.

Insects have a pivotal role in ecosystem function, thus the decline of more than 75% in insect biomass in protected areas over recent decades in Central Europe1 and elsewhere2,3 has alarmed the public, pushed decision-makers4 and stimulated research on insect population trends. However, the drivers of this decline are still not well understood. Here, we reanalysed 27 years of insect biomass data from Hallmann et al.1, using sample-specific information on weather conditions during sampling and weather anomalies during the insect life cycle. This model explained variation in temporal decline in insect biomass, including an observed increase in biomass in recent years, solely on the basis of these weather variables. Our finding that terrestrial insect biomass is largely driven by complex weather conditions challenges previous assumptions that climate change is more critical in the tropics5,6 or that negative consequences in the temperate zone might only occur in the future7. Despite the recent observed increase in biomass, new combinations of unfavourable multi-annual weather conditions might be expected to further threaten insect populations under continuing climate change. Our findings also highlight the need for more climate change research on physiological mechanisms affected by annual weather conditions and anomalies.

Soundscapes and deep learning enable tracking biodiversity recovery in tropical forests.

Tropical forest recovery is fundamental to addressing the intertwined climate and biodiversity loss crises. While regenerating trees sequester carbon relatively quickly, the pace of biodiversity recovery remains contentious. Here, we use bioacoustics and metabarcoding to measure forest recovery post-agriculture in a global biodiversity hotspot in Ecuador. We show that the community composition, and not species richness, of vocalizing vertebrates identified by experts reflects the restoration gradient. Two automated measures - an acoustic index model and a bird community composition derived from an independently developed Convolutional Neural Network - correlated well with restoration (adj-R² = 0.62 and 0.69, respectively). Importantly, both measures reflected composition of non-vocalizing nocturnal insects identified via metabarcoding. We show that such automated monitoring tools, based on new technologies, can effectively monitor the success of forest recovery, using robust and reproducible data.

Ambient and substrate energy influence decomposer diversity differentially across trophic levels.

The species-energy hypothesis predicts increasing biodiversity with increasing energy in ecosystems. Proxies for energy availability are often grouped into ambient energy (i.e., solar radiation) and substrate energy (i.e., non-structural carbohydrates or nutritional content). The relative importance of substrate energy is thought to decrease with increasing trophic level from primary consumers to predators, with reciprocal effects of ambient energy. Yet, empirical tests are lacking. We compiled data on 332,557 deadwood-inhabiting beetles of 901 species reared from wood of 49 tree species across Europe. Using host-phylogeny-controlled models, we show that the relative importance of substrate energy versus ambient energy decreases with increasing trophic levels: the diversity of zoophagous and mycetophagous beetles was determined by ambient energy, while non-structural carbohydrate content in woody tissues determined that of xylophagous beetles. Our study thus overall supports the species-energy hypothesis and specifies that the relative importance of ambient temperature increases with increasing trophic level with opposite effects for substrate energy.

Enhancing the structural diversity between forest patches-A concept and real-world experiment to study biodiversity, multifunctionality and forest resilience across spatial scales.

Intensification of land use by humans has led to a homogenization of landscapes and decreasing resilience of ecosystems globally due to a loss of biodiversity, including the majority of forests. Biodiversity-ecosystem functioning (BEF) research has provided compelling evidence for a positive effect of biodiversity on ecosystem functions and services at the local (α-diversity) scale, but we largely lack empirical evidence on how the loss of between-patch ß-diversity affects biodiversity and multifunctionality at the landscape scale (γ-diversity). Here, we present a novel concept and experimental framework for elucidating BEF patterns at α-, ß-, and γ-scales in real landscapes at a forest management-relevant scale. We examine this framework using 22 temperate broadleaf production forests, dominated by Fagus sylvatica. In 11 of these forests, we manipulated the structure between forest patches by increasing variation in canopy cover and deadwood. We hypothesized that an increase in landscape heterogeneity would enhance the ß-diversity of different trophic levels, as well as the ß-functionality of various ecosystem functions. We will develop a new statistical framework for BEF studies extending across scales and incorporating biodiversity measures from taxonomic to functional to phylogenetic diversity using Hill numbers. We will further expand the Hill number concept to multifunctionality allowing the decomposition of γ-multifunctionality into α- and ß-components. Combining this analytic framework with our experimental data will allow us to test how an increase in between patch heterogeneity affects biodiversity and multifunctionality across spatial scales and trophic levels to help inform and improve forest resilience under climate change. Such an integrative concept for biodiversity and functionality, including spatial scales and multiple aspects of diversity and multifunctionality as well as physical and environmental structure in forests, will go far beyond the current widely applied approach in forestry to increase resilience of future forests through the manipulation of tree species composition.

Dung-visiting beetle diversity is mainly affected by land use, while community specialization is driven by climate.

Dung beetles are important actors in the self-regulation of ecosystems by driving nutrient cycling, bioturbation, and pest suppression. Urbanization and the sprawl of agricultural areas, however, destroy natural habitats and may threaten dung beetle diversity. In addition, climate change may cause shifts in geographical distribution and community composition. We used a space-for-time approach to test the effects of land use and climate on α-diversity, local community specialization (H 2') on dung resources, and γ-diversity of dung-visiting beetles. For this, we used pitfall traps baited with four different dung types at 115 study sites, distributed over a spatial extent of 300 km × 300 km and 1000 m in elevation. Study sites were established in four local land-use types: forests, grasslands, arable sites, and settlements, embedded in near-natural, agricultural, or urban landscapes. Our results show that abundance and species density of dung-visiting beetles were negatively affected by agricultural land use at both spatial scales, whereas γ-diversity at the local scale was negatively affected by settlements and on a landscape scale equally by agricultural and urban land use. Increasing precipitation diminished dung-visiting beetle abundance, and higher temperatures reduced community specialization on dung types and γ-diversity. These results indicate that intensive land use and high temperatures may cause a loss in dung-visiting beetle diversity and alter community networks. A decrease in dung-visiting beetle diversity may disturb decomposition processes at both local and landscape scales and alter ecosystem functioning, which may lead to drastic ecological and economic damage.

Quantifying wood decomposition by insects and fungi using computed tomography scanning and machine learning.

Wood decomposition is a central process contributing to global carbon and nutrient cycling. Quantifying the role of the major biotic agents of wood decomposition, i.e. insects and fungi, is thus important for a better understanding of this process. Methods to quantify wood decomposition, such as dry mass loss, suffer from several shortcomings, such as destructive sampling or subsampling. We developed and tested a new approach based on computed tomography (CT) scanning and semi-automatic image analysis of logs from a field experiment with manipulated beetle communities. We quantified the volume of beetle tunnels in wood and bark and the relative wood volume showing signs of fungal decay and compared both measures to classic approaches. The volume of beetle tunnels was correlated with dry mass loss and clearly reflected the differences between beetle functional groups. Fungal decay was identified with high accuracy and strongly correlated with ergosterol content. Our data show that this is a powerful approach to quantify wood decomposition by insects and fungi. In contrast to other methods, it is non-destructive, covers entire deadwood objects and provides spatially explicit information opening a wide range of research options. For the development of general models, we urge researchers to publish training data.

The rising moon promotes mate finding in moths.

To counteract insect decline, it is essential to understand the underlying causes, especially for key pollinators such as nocturnal moths whose ability to orientate can easily be influenced by ambient light conditions. These comprise natural light sources as well as artificial light, but their specific relevance for moth orientation is still unknown. We investigated the influence of moonlight on the reproductive behavior of privet hawkmoths (Sphinx ligustri) at a relatively dark site where the Milky Way was visible while the horizon was illuminated by distant light sources and skyglow. We show that male moths use the moon for orientation and reach females significantly faster with increasing moon elevation. Furthermore, the choice of flight direction depended on the cardinal position of the moon but not on the illumination of the horizon caused by artificial light, indicating that the moon plays a key role in the orientation of male moths.

Relationship of insect biomass and richness with land use along a climate gradient.

Recently reported insect declines have raised both political and social concern. Although the declines have been attributed to land use and climate change, supporting evidence suffers from low taxonomic resolution, short time series, a focus on local scales, and the collinearity of the identified drivers. In this study, we conducted a systematic assessment of insect populations in southern Germany, which showed that differences in insect biomass and richness are highly context dependent. We found the largest difference in biomass between semi-natural and urban environments (-42%), whereas differences in total richness (-29%) and the richness of threatened species (-56%) were largest from semi-natural to agricultural environments. These results point to urbanization and agriculture as major drivers of decline. We also found that richness and biomass increase monotonously with increasing temperature, independent of habitat. The contrasting patterns of insect biomass and richness question the use of these indicators as mutual surrogates. Our study provides support for the implementation of more comprehensive measures aimed at habitat restoration in order to halt insect declines.

Natural Zeitgebers Under Temperate Conditions Cannot Compensate for the Loss of a Functional Circadian Clock in Timing of a Vital Behavior in Drosophila.

The adaptive significance of adjusting behavioral activities to the right time of the day seems obvious. Laboratory studies implicated an important role of circadian clocks in behavioral timing and rhythmicity. Yet, recent studies on clock-mutant animals questioned this importance under more naturalistic settings, as various clock mutants showed nearly normal diel activity rhythms under seminatural zeitgeber conditions. We here report evidence that proper timing of eclosion, a vital behavior of the fruit fly Drosophila melanogaster, requires a functional molecular clock under quasi-natural conditions. In contrast to wild-type flies, period01 mutants with a defective molecular clock showed impaired rhythmicity and gating in a temperate environment even in the presence of a full complement of abiotic zeitgebers. Although period01 mutants still eclosed during a certain time window during the day, this time window was much broader and loosely defined, and rhythmicity was lower or lost as classified by various statistical measures. Moreover, peak eclosion time became more susceptible to variable day-to-day changes of light. In contrast, flies with impaired peptidergic interclock signaling (Pdf01 and han5304 PDF receptor mutants) eclosed mostly rhythmically with normal gate sizes, similar to wild-type controls. Our results suggest that the presence of natural zeitgebers is not sufficient, and a functional molecular clock is required to induce stable temporal eclosion patterns in flies under temperate conditions with considerable day-to-day variation in light intensity and temperature. Temperate zeitgebers are, however, sufficient to functionally rescue a loss of PDF-mediated clock-internal and -output signaling.

A Novel Thermal-Visual Place Learning Paradigm for Honeybees (Apis mellifera).

Honeybees (Apis mellifera) have fascinating navigational skills and learning capabilities in the field. To decipher the mechanisms underlying place learning in honeybees, we need paradigms to study place learning of individual honeybees under controlled laboratory conditions. Here, we present a novel visual place learning arena for honeybees which relies on high temperatures as aversive stimuli. Honeybees learn to locate a safe spot in an unpleasantly warm arena, relying on a visual panorama. Bees can solve this task at a temperature of 46°C, while at temperatures above 48°C bees die quickly. This new paradigm, which is based on pioneering work on Drosophila, allows us now to investigate thermal-visual place learning of individual honeybees in the laboratory, for example after controlled genetic knockout or pharmacological intervention.

The Circadian Clock Improves Fitness in the Fruit Fly, Drosophila melanogaster.

It is assumed that a properly timed circadian clock enhances fitness, but only few studies have truly demonstrated this in animals. We raised each of the three classical Drosophila period mutants for >50 generations in the laboratory in competition with wildtype flies. The populations were either kept under a conventional 24-h day or under cycles that matched the mutant's natural cycle, i.e., a 19-h day in the case of per s mutants and a 29-h day for per l mutants. The arrhythmic per 0 mutants were grown together with wildtype flies under constant light that renders wildtype flies similar arrhythmic as the mutants. In addition, the mutants had to compete with wildtype flies for two summers in two consecutive years under outdoor conditions. We found that wildtype flies quickly outcompeted the mutant flies under the 24-h laboratory day and under outdoor conditions, but per l mutants persisted and even outnumbered the wildtype flies under the 29-h day in the laboratory. In contrast, per s and per 0 mutants did not win against wildtype flies under the 19-h day and constant light, respectively. Our results demonstrate that wildtype flies have a clear fitness advantage in terms of fertility and offspring survival over the period mutants and - as revealed for per l mutants - this advantage appears maximal when the endogenous period resonates with the period of the environment. However, the experiments indicate that per l and per s persist at low frequencies in the population even under the 24-h day. This may be a consequence of a certain mating preference of wildtype and heterozygous females for mutant males and time differences in activity patterns between wildtype and mutants.

Explaining the variability in the response of annual eusocial insects to mass-flowering events.

Empirical studies of annual eusocial insects in agricultural landscapes report contrasting findings with regard to colony responses to mass-flowering of crops such as oilseed rape. In particular, total sexual production is often unaffected by such events, whereas worker number responds with a prominent increase. To resolve these conflicting observations, we model-using an established approach-the expected change in worker and sexual numbers in response to an increased worker productivity induced by mass-flowering events at different times of the season. We find that the predicted response pattern is mainly shaped by the degree to which individual worker productivity is reduced by an increasing number of workers in the colony. Different environmental conditions and colony characteristics result in different levels of interference of workers, for example, during foraging or nest construction. Reduction in individual productivity is low, when worker interference is negligible ("weak limitation") and high when an increasing number of workers substantially decreases per-capita efficiency ("strong limitation"). For weak limitation, any mass-flowering event that ends before the production of sexuals starts has a strong multiplicative impact on both worker and sexual numbers. The magnitude of the effect is quite independent of the precise timing of such an event. After the onset of sexual production, mass-flowering has a weaker effect, as the added resource supply is only linearly transferred into production of additional sexuals. For colonies under strong limitation, the predicted impact of mass-flowering events is generally weaker, especially on the production of sexuals, and the timing of mass-flowering events becomes more influential: Production of sexuals profits more from late than from early mass-flowering events. Consequently, early mass-flowering events are predicted to have a prominent effect on worker numbers but a negligible one on the output of sexuals. The model presented provides a mechanistic explanation of why increased worker abundances do not necessarily translate into increased production of sexuals. The model is also applicable to other eusocial insects such as paper wasps whenever brief pulses of massive resource availability shortly elevate resource intake rates above the "normal" levels.

Overwintering temperature and body condition shift emergence dates of spring-emerging solitary bees.

Solitary bees in seasonal environments must align their life-cycles with favorable environmental conditions and resources; the timing of their emergence is highly fitness relevant. In several bee species, overwintering temperature influences both emergence date and body weight at emergence. High variability in emergence dates among specimens overwintering at the same temperatures suggests that the timing of emergence also depends on individual body conditions. However, possible causes for this variability, such as individual differences in body size or weight, have been rarely studied. In a climate chamber experiment using two spring-emerging mason bees (Osmia cornuta and O. bicornis), we investigated the relationship between temperature, emergence date, body weight, and body size, the last of which is not affected by overwintering temperature. Our study showed that body weight declined during hibernation more strongly in warm than in cold overwintering temperatures. Although bees emerged earlier in warm than in cold overwintering temperatures, at the time of emergence, bees in warm overwintering temperatures had lower body weights than bees in cold overwintering temperatures (exception of male O. cornuta). Among specimens that experienced the same overwintering temperatures, small and light bees emerged later than their larger and heavier conspecifics. Using a simple mechanistic model we demonstrated that spring-emerging solitary bees use a strategic approach and emerge at a date that is most promising for their individual fitness expectations. Our results suggest that warmer overwintering temperatures reduce bee fitness by causing a decrease in body weight at emergence. We showed furthermore that in order to adjust their emergence dates, bees use not only temperature but also their individual body condition as triggers. This may explain differing responses to climate warming within and among bee populations and may have consequences for bee-plant interactions as well as for the persistence of bee populations under climate change.

Eusociality outcompetes egalitarian and solitary strategies when resources are limited and reproduction is costly.

Explaining the evolution and maintenance of animal groups remains a challenge. Surprisingly, fundamental ecological factors, such as resource variance and competition for limited resources, tend to be ignored in models of cooperation. We use a mathematical model previously developed to quantify the influence of different group sizes on resource use efficiency in egalitarian groups and extend its scope to groups with severe reproductive skew (eusocial groups). Accounting for resource limitation, the model allows calculation of optimal group sizes (highest resource use efficiency) and equilibrium population sizes in egalitarian as well as eusocial groups for a broad spectrum of environmental conditions (variance of resource supply). We show that, in contrast to egalitarian groups, eusocial groups may not only reduce variance in resource supply for survival, thus reducing the risk of starvation, they may also increase variance in resource supply for reproduction. The latter effect allows reproduction even in situations when resources are scarce. These two facets of eusocial groups, resource sharing for survival and resource pooling for reproduction, constitute two beneficial mechanisms of group formation. In a majority of environmental situations, these two benefits of eusociality increase resource use efficiency and lead to supersaturation-a strong increase in carrying capacity. The increase in resource use efficiency provides indirect benefits to group members even for low intra-group relatedness and may represent one potential explanation for the evolution and especially the maintenance of eusociality and cooperative breeding.

Evolving mutation rate advances the invasion speed of a sexual species.

BACKGROUND: Many species are shifting their ranges in response to global climate change. Range expansions are known to have profound effects on the genetic composition of populations. The evolution of dispersal during range expansion increases invasion speed, provided that a species can adapt sufficiently fast to novel local conditions. Genetic diversity at the expanding range border is however depleted due to iterated founder effects. The surprising ability of colonizing species to adapt to novel conditions while being subjected to genetic bottlenecks is termed 'the genetic paradox of invasive species'. Mutational processes have been argued to provide an explanation for this paradox. Mutation rates can evolve, under conditions that favor an increased rate of adaptation, by hitchhiking on beneficial mutations through induced linkage disequilibrium. Here we argue that spatial sorting, iterated founder events, and population structure benefit the build-up and maintenance of such linkage disequilibrium. We investigate if the evolution of mutation rates could play a role in explaining the 'genetic paradox of invasive species' for a sexually reproducing species colonizing a landscape of gradually changing conditions. RESULTS: We use an individual-based model to show the evolutionary increase of mutation rates in sexual populations during range expansion, in coevolution with the dispersal probability. The observed evolution of mutation rate is adaptive and clearly advances invasion speed both through its effect on the evolution of dispersal probability, and the evolution of local adaptation. This also occurs under a variable temperature gradient, and under the assumption of 90% lethal mutations. CONCLUSIONS: In this study we show novel consequences of the particular genetic properties of populations under spatial disequilibrium, i.e. the coevolution of dispersal probability and mutation rate, even in a sexual species and under realistic spatial gradients, resulting in faster invasions. The evolution of mutation rates can therefore be added to the list of possible explanations for the 'genetic paradox of invasive species'. We conclude that range expansions and the evolution of mutation rates are in a positive feedback loop, with possibly far-reaching ecological consequences concerning invasiveness and the adaptability of species to novel environmental conditions.

Saving the injured: Rescue behavior in the termite-hunting ant Megaponera analis.

Predators of highly defensive prey likely develop cost-reducing adaptations. The ant Megaponera analis is a specialized termite predator, solely raiding termites of the subfamily Macrotermitinae (in this study, mostly colonies of Pseudocanthotermes sp.) at their foraging sites. The evolutionary arms race between termites and ants led to various defensive mechanisms in termites (for example, a caste specialized in fighting predators). Because M. analis incurs high injury/mortality risks when preying on termites, some risk-mitigating adaptations seem likely to have evolved. We show that a unique rescue behavior in M. analis, consisting of injured nestmates being carried back to the nest, reduces combat mortality. After a fight, injured ants are carried back by their nestmates; these ants have usually lost an extremity or have termites clinging to them and are able to recover within the nest. Injured ants that are forced experimentally to return without help, die in 32% of the cases. Behavioral experiments show that two compounds, dimethyl disulfide and dimethyl trisulfide, present in the mandibular gland reservoirs, trigger the rescue behavior. A model accounting for this rescue behavior identifies the drivers favoring its evolution and estimates that rescuing enables maintenance of a 28.7% larger colony size. Our results are the first to explore experimentally the adaptive value of this form of rescue behavior focused on injured nestmates in social insects and help us to identify evolutionary drivers responsible for this type of behavior to evolve in animals.

The Adequate Use of Limited Information in Dispersal Decisions.

Several theoretical studies predict that informed (e.g., density-dependent) dispersal should generally result in lower emigration probabilities than uninformed (random) dispersal. In a 2012 publication, Bocedi et al. surprisingly come to the opposite conclusion. For most scenarios investigated, they found that noninformed and, particularly, less precisely informed dispersers evolve lower dispersal propensity than dispersers following "fully informed" strategies. Further, they observed that fully informed individuals evolved a steplike dispersal response-a response to local density that contradicts theoretical predictions for organisms with nonoverlapping generations. Replicating the individual-based simulations of Bocedi et al. we find that these conclusions are not justified and are based on a misinterpretation of simulation results: their controversial findings result from (i) a misleading use of the term "population density," (ii) a misconception concerning the true informative value of the different decision criteria they compared, and (iii) arbitrary constraints on the evolution of the dispersal response that prevented the evolution of strategies that allow for a fitness-enhancing utilization of available information.