Influence of habitat quality, population size, patch size, and connectivity on patch-occupancy dynamics of the middle spotted woodpecker

Despite extensive research on the effects of habitat fragmentation, the ecological mechanisms underlying colonization and extinction processes are poorly known, but knowledge of these mechanisms is essential to understanding the distribution and persistence of populations in fragmented habitats. We examined these mechanisms through multiseason occupancy models that elucidated patch-occupancy dynamics of Middle Spotted Woodpeckers (Dendrocopos medius) in northwestern Spain. The number of occupied patches was relatively stable from 2000 to 2010 (15-24% of 101 patches occupied every year) because extinction was balanced by recolonization. Larger and higher quality patches (i.e., higher density of oaks >37 cm dbh [diameter at breast height]) were more likely to be occupied. Habitat quality (i.e., density of large oaks) explained more variation in patch colonization and extinction than did patch size and connectivity, which were both weakly associated with probabilities of turnover. Patches of higher quality were more likely to be colonized than patches of lower quality. Populations in high-quality patches were less likely to become extinct. In addition, extinction in a patch was strongly associated with local population size but not with patch size, which means the latter may not be a good surrogate of population size in assessments of extinction probability. Our results suggest that habitat quality may be a primary driver of patch-occupancy dynamics and may increase the accuracy of models of population survival. We encourage comparisons of competing models that assess occupancy, colonization, and extinction probabilities in a single analytical framework (e.g., dynamic occupancy models) so as to shed light on the association of habitat quality and patch geometry with colonization and extinction processes in different settings and species.     

Habitat-quality effects on metapopulation dynamics in greater white-toothed shrews, Crocidura russula

The effects of patch size and isolation on metapopulation dynamics have received wide empirical support and theoretical formalization. By contrast, the effects of patch quality seem largely underinvestigated, partly due to technical difficulties in properly assessing quality. Here we combine habitat-quality modeling with four years of demographic monitoring in a metapopulation of greater white-toothed shrews (Crocidura russula) to investigate the role of patch quality on metapopulation processes. Together, local patch quality and connectivity significantly enhanced local population sizes and occupancy rates (R2 = 14% and 19%, respectively). Accounting for the quality of patches connected to the focal one and acting as potential sources improved slightly the model explanatory power for local population sizes, pointing to significant source-sink dynamics. Local habitat quality, in interaction with connectivity, also increased colonization rate (R2 = 28%), suggesting the ability of immigrants to target high-quality patches. Overall, patterns were best explained when assuming a mean dispersal distance of 800 m, a realistic value for the species under study. Our results thus provide evidence that patch quality, in interaction with connectivity, may affect major demographic processes.     

A robust-design formulation of the incidence function model of metapopulation dynamics applied to two species of rails

The incidence function model (IFM) uses area and connectivity to predict metapopulation dynamics. However, false absences and missing data can lead to underestimates of the number of sites contributing to connectivity, resulting in overestimates of dispersal ability and turnovers (extinctions plus colonizations). We extend estimation methods for the IFM by using a hierarchical Bayesian model to account both for false absences due to imperfect detection and for missing data due to sites not surveyed in some years. We compare parameter estimates, measures of metapopulation dynamics, and forecasts using stochastic patch occupancy models (SPOMs) among three IFM models: (1) a Bayesian formulation assuming no false absences and omitting site-year combinations with missing data; (2) a hierarchical Bayesian formulation assuming no false absences but incorporating missing data; and (3) a hierarchical Bayesian formulation allowing for imperfect detection and incorporating missing data. We fit the models to multiyear data sets of occupancy for two bird species that differ in body size and presumed dispersal ability but inhabit the same network of sites: the small Black Rail (Laterallus jamaicensis) and the medium-sized Virginia Rail (Rallus limicola). Incorporating missing data affected colonization parameters and led to lower estimates of dispersal ability for the Black Rail. Detection rates were high for the Black Rail in most years but moderate for the Virginia Rail. Incorporating imperfect detection resulted in higher occupancy and lower turnover rates for both species, with largest effects for the Virginia Rail. Forecasts using SPOMs were sensitive to both missing data and false absences; persistence in models assuming no false absences was more optimistic than from robust models. Our results suggest that incorporating false absences and missing data into the IFM can improve (1) estimates of dispersal ability and the effect of connectivity on colonization, (2) the scaling of extinction risk with patch area, and (3) forecasts of occupancy and turnover rates.     

Minimum viable metapopulation size, extinction debt, and the conservation of a declining species.

A key question facing conservation biologists is whether declines in species' distributions are keeping pace with landscape change, or whether current distributions overestimate probabilities of future persistence. We use metapopulations of the marsh fritillary butterfly Euphydryas aurinia in the United Kingdom as a model system to test for extinction debt in a declining species. We derive parameters for a metapopulation model (incidence function model, IFM) using information from a 625-km2 landscape where habitat patch occupancy, colonization, and extinction rates for E. aurinia depend on patch connectivity, area, and quality. We then show that habitat networks in six extant metapopulations in 16-km2 squares were larger, had longer modeled persistence times (using IFM), and higher metapopulation capacity (lambdaM) than six extinct metapopulations. However, there was a > 99% chance that one or more of the six extant metapopulations would go extinct in 100 years in the absence of further habitat loss. For 11 out of 12 networks, minimum areas of habitat needed for 95% persistence of metapopulation simulations after 100 years ranged from 80 to 142 ha (approximately 5-9% of land area), depending on the spatial location of habitat. The area of habitat exceeded the estimated minimum viable metapopulation size (MVM) in only two of the six extant metapopulations, and even then by only 20%. The remaining four extant networks were expected to suffer extinction in 15-126 years. MVM was consistently estimated as approximately 5% of land area based on a sensitivity analysis of IFM parameters and was reduced only marginally (to approximately 4%) by modeling the potential impact of long-distance colonization over wider landscapes. The results suggest a widespread extinction debt among extant metapopulations of a declining species, necessitating conservation management or reserve designation even in apparent strongholds. For threatened species, metapopulation modeling is a potential means to identify landscapes near to extinction thresholds, to which conservation measures can be targeted for the best chance of success.     

Leaf traits are good predictors of plant performance across 53 rain forest species

We compared the leaf traits and plant performance of 53 co-occurring tree species in a semi-evergreen tropical moist forest community. The species differed in all leaf traits analyzed: leaf life span varied 11-fold among species, specific leaf area 5-fold, mass-based nitrogen 3-fold, mass-based assimilation rate 13-fold, mass-based respiration rate 15-fold, stomatal conductance 8-fold, and photosynthetic water use efficiency 4-fold. Photosynthetic traits were strongly coordinated, and specific leaf area predicted mass-based rates of assimilation and respiration; leaf life span predicted many other leaf characteristics. Leaf traits were closely associated with growth, survival, and light requirement of the species. Leaf investment strategies varied on a continuum trading off short-term carbon gain against long-term leaf persistence that, in turn, is linked to variation in whole-plant growth and survival. Leaf traits were good predictors of plant performance, both in gaps and in the forest understory. High growth in gaps is promoted by cheap, short-lived, and physiologically active leaves. High survival in the forest understory is enhanced by the formation of long-lived well protected leaves that reduce biomass loss by herbivory, mechanical disturbance, or leaf turnover. Leaf traits underlay this growth-survival trade-off; species with short-lived, physiologically active leaves have high growth but low survival. This continuum in leaf traits, through its effect on plant performance, in turn gives rise to a continuum in species' light requirements.     

Populations in small, ephemeral habitat patches may drive dynamics in a Daphnia magna metapopulation

Migration is the key process to understand the dynamics and persistence of a metapopulation. Many metapopulation models assume a positive correlation between habitat patch size or stability and the number of emigrants. However, few empirical data exist, and habitat patch size and habitat stability may affect dispersal differently than they affect local persistence. Here, we studied the production of the migration stage (i.e., resting eggs called ephippia) of the cladoceran Daphnia magna in a metapopulation consisting of 530 rock pool habitat patches over 25 years. Earlier, the functioning of this metapopulation was explained with a Levins-type metapopulation model or with a mainland-island metapopulation model, based on local extinction and colonization data or time series data, respectively. We used pool volume, hydroperiod length, and number of desiccation events to calculate per-pool production of ephippia (i.e., migration stages). We estimated that populations in small and ephemeral habitat patches produced more than half of the 250 000 to 1 million ephippia that were produced in the metapopulation as a whole per year between 1982 and 2006. Furthermore, these small populations contributed approximately 90% of the ephippia exposed during desiccation events, while the contribution of the long-lived populations in large pools was minimal. We term this an "inverse mainland-island" type metapopulation and propose that populations in small, ephemeral habitat patches may also be the driving force for metapopulation dynamics in other systems.     

Lactation patterns of pinnipeds are not explained by optimization of maternal energy delivery rates

Within pinnipeds, phocids and otariids show differing maternal care strategies. Phocids rear young out of body stores in a yearly cycle with a single stay ashore when the mother fasts while lactating, whereas otariids provision their young by repeated foraging trips to sea alternating with brief stays ashore where they suckle their young. In a previous optimality model, these differences have been interpreted as adaptations based on differing energy requirements of large (phocid) and smaller (otariid) species, and the time budget of the large elephant and the much smaller Antarctic fur seal were correctly predicted. Our refined model—extended to pinniped species of all sizes—predicts lactation strategies to shift from attendance cycles to 1-year cycles with increasing body mass and provides an explanation for the finding that phocid pups are weaned at lower relative mass than otariid pups. However, other predictions do not correspond to empirical findings. In particular, the model does not explain the behavior of large otariids and small phocids. Thus, maternal metabolic requirements alone appear insufficient to explain observed lactation patterns. In the light of our results, we discuss more generally the scope and limitations of optimality models when applied in a comparative framework to a group of related species.     

Architecture of 54 moist-forest tree species: traits, trade-offs, and functional groups

Tree architecture is an important determinant of the height extension, light capture, and mechanical stability of trees, and it allows species to exploit the vertical height gradient in the forest canopy and horizontal light gradients at the forest floor. Tropical tree species partition these gradients through variation in adult stature (Hmax) and light demand. In this study we compare 22 architectural traits for 54 Bolivian moist-forest tree species. We evaluate how architectural traits related to Hmax vary with tree size, and we present a conceptual scheme in which we combine the two axes into four different functional groups. Interspecific correlations between architecture and Hmax varied strongly from negative to positive, depending on the reference sizes used. Stem height was positively related to Hmax at larger reference diameters (14-80 cm). Species height vs. diameter curves often flattened toward their upper ends in association with reproductive maturity for species of all sizes. Thus, adult understory trees were typically shorter than similar-diameter juveniles of larger species. Crown area was negatively correlated with Hmax at small reference heights and positively correlated at larger reference heights (15-34 m). Wide crowns allow the small understory species to intercept light over a large area at the expense of a reduced height growth. Crown length was negatively correlated with Hmax at intermediate reference heights (4-14 m). A long crown enables small understory species to maximize light interception in a light-limited environment. Light-demanding species were characterized by orthotropic stems and branches, large leaves, and a monolayer leaf arrangement. They realized an efficient height growth through the formation of narrow and shallow crowns. Light demand turned out to be a much stronger predictor of tree architecture than Hmax, probably because of the relatively low, open, and semi-evergreen canopy at the research site. The existence of four functional groups (shade-tolerant, partial-shade-tolerant, and long- and short-lived pioneer) was confirmed by the principal component and discriminant analysis. Both light demand and Hmax capture the major variation in functional traits found among tropical rain forest tree species, and the two-way classification scheme provides a straightforward model to understand niche differentiation in tropical forests.     

Ranking individual habitat patches as connectivity providers: Integrating network analysis and patch removal experiments

Here we propose an integrated framework for modeling connectivity that can help ecologists, conservation planners and managers to identify patches that, more than others, contribute to uphold species dispersal and other ecological flows in a landscape context. We elaborate, extend and partly integrate recent network-based approaches for modeling and supporting the management of fragmented landscapes. In doing so, experimental patch removal techniques and network analytical approaches are merged into one integrated modeling framework for assessing the role of individual patches as connectivity providers. In particular, we focus the analyses on the habitat availability metrics PC and IIC and on the network metric Betweenness Centrality. The combination and extension of these metrics jointly assess both the immediate connectivity impacts of the loss of a particular patch and the resulting increased vulnerability of the network to subsequent disruptions. In using the framework to analyze the connectivity of two real landscapes in Madagascar and Catalonia (NE Spain), we suggest a procedure that can be used to rank individual habitat patches and show that the combined metrics reveal relevant and non-redundant information valuable to assert and quantify distinctive connectivity aspects of any given patch in the landscape. Hence, we argue that the proposed framework could facilitate more ecologically informed decision-making in managing fragmented landscapes. Finally, we discuss and highlight some of the advantages, limitations and key differences between the considered metrics.     

Economic land use, ecosystem services and microfounded species dynamics

In an integrated economy–ecosystem model humans choose their land use and leave the residual land as habitat for three species forming a food chain. The size of habitat determines the diversity and abundance of species. That biodiversity generates, in turn, a flow of ecosystem services with public-good characteristics for human consumption. The ecosystem submodel yields (rather than assumes!) population growth functions with each species’ growth depending on the size of habitat. First the relationship between habitat and species growth (sustenance, decline and extinction) is explored. The laissez-faire economy is shown to result in an underprovision of habitat making the case for land use restrictions for nature protection. The optimal land use policy is characterized with full regard of ecosystem dynamics. Finally, labor-augmenting technical change is introduced to generate ever increasing pressure towards further habitat reductions. In the laissez-faire economy the habitat is consequently squeezed to zero in the long-run so that all species are doomed. Social optimality demands, however, to refrain from using all land for economic purposes despite ever growing labor productivity.     

Interactions between environment, species traits, and human uses describe patterns of plant invasions

Although invasive alien species (IAS) are a major threat to biodiversity, human health, and economy, our understanding of the factors controlling their distribution and abundance is limited. Here, we determine how environmental factors, land use, life-history traits of the invaders, residence time, origin, and human usage interact to shape the spatial pattern of invasive alien plant species in South Africa. Relationships between the environmental factors and the extrinsic and intrinsic attributes of species were investigated using RLQ analysis, a multivariate method for relating a species-attribute table to an environmental table by way of a species presence/absence table. We then clustered species according to their position on the RLQ axes, and tested these groups for phylogenetic independence. The first three axes of the RLQ explained 99% of the variation and were strongly related to the species attributes. The clustering showed that, after accounting for environmental factors, the spatial pattern of IAS in South Africa was driven by human uses, life forms, and reproductive traits. The seven clusters of species strongly reflected geographical distribution, but also intrinsic species attributes and patterns of human use. Two of the clusters, centered on the genera Acacia and Opuntia, were phylogenetically non-independent. The remaining clusters comprised species of diverse taxonomic affinities, but sharing traits facilitating invasion in particular habitats. This information is useful for assessing the extent to which the potential spread of recent introductions can be predicted by considering the interaction of their biological attributes, region of origin, and human use.     

Running to stand still: temperature effects on species richness, species turnover, and functional community dynamics

The information on temperature-mediated changes in biodiversity in local assemblages is scarce and mainly addresses the change in species richness. However, warming may have more consistent effects on species turnover than on the number of species. Moreover, very few studies extended the analysis of changes in biodiversity and species composition to questions of associated ecosystem functions such as primary production. Here, we synthesize 4 case studies employing microalgal microcosms within the Aquashift priority program to ask (1) do warming-related shifts in species richness correspond to changes in the rate of biomass production, (2) do similar relationships prevail for evenness, and (3) do warming-related shifts in species turnover stabilize or destabilize biomass production? Two of the four cases are previously unpublished, and for a third case, the link between diversity and functional consequences of temperature was not analyzed before. We found accelerated loss of species with warming in all cases. Biomass production was lower with lower species richness in most cases but increased with lower evenness. Most importantly, the relation between functional and compositional stability was different between cases: More rapid extinction resulted in more variable biomass in 2 cases conducted with a limited species pool, indicating that compositional destabilization relates to functional variability. By contrast, the only experiment with a large species pool (30 species) allowed previously rare species to become dominant in the community and showed more stable biomass at high turnover, indicating that compensatory dynamics (turnover) can promote functional stability. These 4 independent experiments highlight the need to consider both compositional and functional consequences of altered temperature regimes.     

Arthropod assemblages are best predicted by plant species composition

Insects and spiders comprise more than two-thirds of the Earth's total species diversity. There is wide concern, however, that the global diversity of arthropods may be declining even more rapidly than the diversity of vertebrates and plants. For adequate conservation planning, ecologists need to understand the driving factors for arthropod communities and devise methods, that provide reliable predictions when resources do not permit exhaustive ground surveys. Which factor most successfully predicts arthropod community structure is still a matter of debate, however. The purpose of this study was to identify the factor best predicting arthropod assemblage composition. We investigated the species composition of seven functionally different arthropod groups (epigeic spiders, grasshoppers, ground beetles, weevils, hoppers, hoverflies, and bees) at 47 sites in The Netherlands comprising a range of seminatural grassland types and one heathland type. We then compared the actual arthropod composition with predictions based on plant species composition, vegetation structure, environmental data, flower richness, and landscape composition. For this we used the recently published method of predictive co-correspondence analysis, and a predictive variant of canonical correspondence analysis, depending on the type of predictor data. Our results demonstrate that local plant species composition is the most effective predictor of arthropod assemblage composition, for all investigated groups. In predicting arthropod assemblages, plant community composition consistently outperforms both vegetation structure and environmental conditions (even when the two are combined), and also performs better than the surrounding landscape. These results run against a common expectation of vegetation structure as the decisive factor. Such expectations, however, have always been biased by the fact that until recently no methods existed that could use an entire (plant) species composition in the explanatory role. Although more recent experimental diversity work has reawakened interest in the role of plant species, these studies still have not used (or have not been able to use) entire species compositions. They only consider diversity measures, both for plant and insect assemblages, which may obscure relationships. The present study demonstrates that the species compositions of insect and plant communities are clearly linked.     

Sequestration of dietary secondary metabolites by three species of sea hares: location,specificity and dynamics

We examined the location of squuestered secondary metabolites in three species of sea hares, Stylocheilus longicauda, Dolabella auricularia, and Aplysia californica (Opisthobranchia: Anaspidea). The sea hares ate a natural diet or were fed an artificial diet containing secondary metabolites in the laboratory. In all three species, sequestered secondary metabolites were located almost exclusively in the digestive gland, an internal organ, rather than in the exterior parts of the body, in eggs, or in ink (released when sea hares are disturbed). S. longicauda, a specialist sea hare, was able to sequester measur-able amounts of all six algal metabolites offered (caulerpenyne, halimedatetraacetate, pachydictyol A, malyingamides A and B, and ochtodene) and two (luffariellolide and Dysidea spp. brominated diphenyl ether) of three sponge metabolites offered (chondrillin was not sequestered). Malyngamides A and B, found in the host plant of S. longicauda, were sequestered at high, but not unique concentrations. D. auricularia, a generalist sea hare, was fed caulerpenyne, pachydictyol A and malyngamide B; patterns of sequestration of these three compounds did not differ markedly between S. longicauda and D. auricularia. S. longicauda did not lose measurable amounts of malyngamides after 18 d on a malyngamide-free diet. These results suggest that sea hares have generic mechanisms for sequestering algal metabolites rather than mechanisms that are tightly linked to particular compounds, that these mechanisms do not differ dramatically between species, and that sequestered secondary metabolites are not located optimally for defense.     

Sperm allocation in relation to male traits, female size, and copulation behaviour in freshwater crayfish species

Sperm competition is a well-recognised agent in the evolution of sperm and ejaculate structure, as well as variation in female quality. Models of the evolution of ejaculate expenditure predict that male body condition, female fecundity and the risk and intensity of sperm competition may be the ultimate factors shaping optimal ejaculate size. We investigated sperm allocation in Austropotamobius italicus, a freshwater crayfish exhibiting a coercive mating system and external fertilisation, in relation to male and female traits and copulation behaviour under laboratory conditions. We found that mating males were sensitive to female size and produced larger ejaculates when mating with larger females, which were more fecund in terms of number of eggs produced. We found no evidence for female egg production being sperm-limited, as the number of eggs was not dependent on male sperm expenditure. Copulation duration and number of ejaculations reliably predicted the amount of sperm transferred, and both these behavioural measures positively covaried with female body size. These results indicate that male freshwater crayfish can modulate their sperm expenditure in accordance with cues that indicate female fecundity. In addition, a novel finding that emerged from this study is the decrease in sperm expenditure with male body size, which may either suggest that large, old male crayfish are better able than small males to economise sperm at a given mating to perform multiple matings during a reproductive season, or that they experience senescence of their reproductive performance.     

Prediction of germination rates of weed species: Relationships between germination speed parameters and species traits

In fields, the timing of weed emergence flushes is mostly related to the timing and rate of seed germination, which depend on seed dormancy level, soil temperature and water potential conditions as well as soil tillage and crop sowing date. Seed germination parameters are essential in weed dynamics models to account for the effects of soil conditions on weed demography. Since these parameters are difficult to measure, our objective was to test the possibility of estimating them from easily accessible information. Seed germination parameters (germination lag-time, time to mid-germination and mid-germination rate) were measured or collected from the literature for 25 weed species with contrasted seed characteristics. Correlations were then searched for between these parameters and morphological, chemical and physiological seed traits as well as seed dormancy level. The dormancy level was positively correlated with speed of germination parameters. Earliness of germination was positively correlated with seed lipid content and the seed area to mass ratio. Germination was also earlier and faster in species with a high base temperature for germination. These relationships explained about half the observed variability in germination speed parameters but should be further tested before being used to predict the germination behaviour of weed species in the field in different seasons.     

Risk spreading, connectivity, and optimal reserve spacing

Two important processes determining the dynamics of spatially structured populations are dispersal and the spatial covariance of demographic fluctuations. Spatially explicit approaches to conservation, such as reserve networks, must consider the tension between these two processes and reach a balance between distances near enough to maintain connectivity, but far enough to benefit from risk spreading. Here, we model this trade-off. We show how two measures of metapopulation persistence depend on the shape of the dispersal kernel and the shape of the distance decay in demographic covariance, and we consider the implications of this trade-off for reserve spacing. The relative rates of distance decay in dispersal and demographic covariance determine whether the long-run metapopulation growth rate, and quasi-extinction risk, peak for adjacent patches or intermediately spaced patches; two local maxima in metapopulation persistence are also possible. When dispersal itself fluctuates over time, the trade-off changes. Temporal variation in mean distance that propagules are dispersed (i.e., propagule advection) decreases metapopulation persistence and decreases the likelihood that persistence will peak for adjacent patches. Conversely, variation in diffusion (the extent of random spread around mean dispersal) increases metapopulation persistence overall and causes it to peak at shorter inter-patch distances. Thus, failure to consider temporal variation in dispersal processes increases the risk that reserve spacings will fail to meet the objective of ensuring metapopulation persistence. This study identifies two phenomena that receive relatively little attention in empirical work on reserve spacing, but that can qualitatively change the effectiveness of reserve spacing strategies: (1) the functional form of the distance decay in covariance among patch-specific demographic rates and (2) temporal variation in the shape of the dispersal kernel. The sensitivity of metapopulation recovery and persistence to how covariance of vital rates decreases with distance suggests that estimating the shape of this function is likely to be as important for effective reserve design as estimating connectivity. Similarly, because temporal variation in dispersal dynamics influences the effect of reserve spacing, approaches to reserve design that ignore such variation, and rely instead on long-term average dispersal patterns, are likely to lead to lower metapopulation viability than is actually achievable.     

Parameterizing,evaluating and comparing metapopulation models with data from individual-based simulations

Due to the lack of sufficient data and appropriate ecological information parameterizing predictive population dynamical models usually is a difficult task. The approach proposed in this study is meant to overcome this problem by using detailed individual-based simulations to generate artificial data. With short-term data samples, the models to be investigated can be parameterized and their predictions be compared. The flexibility of individual-based simulations as experimental tools also facilitates the evaluation and comparison of different (aggregated) model types. The presented approach is a step towards unifying models of different complexity. As an example we applied it to two metapopulation models of insect species in a highly fragmented landscape: the well-known incidence function model with a patch-based representation of space and a grid-based analogue. The models are tested with respect to their data requirement and recommendations for a better data sampling are derived.