Wasp-waist interactions in the North Sea ecosystem

Background

In a “wasp-waist” ecosystem, an intermediate trophic level is expected to control the abundance of predators through a bottom-up interaction and the abundance of prey through a top-down interaction. Previous studies suggest that the North Sea is mainly governed by bottom-up interactions driven by climate perturbations. However, few studies have investigated the importance of the intermediate trophic level occupied by small pelagic fishes.

Methodology/Principal Findings

We investigated the numeric interactions among 10 species of seabirds, two species of pelagic fish and four groups of zooplankton in the North Sea using decadal-scale databases. Linear models were used to relate the time series of zooplankton and seabirds to the time series of pelagic fish. Seabirds were positively related to herring (Clupea harengus), suggesting a bottom-up interaction. Two groups of zooplankton; Calanus helgolandicus and krill were negatively related to sprat (Sprattus sprattus) and herring respectively, suggesting top-down interactions. In addition, we found positive relationships among the zooplankton groups. Para/pseudocalanus was positively related to C. helgolandicus and C. finmarchicus was positively related to krill.

Conclusion/Significance

Our results indicate that herring was important in regulating the abundance of seabirds through a bottom-up interaction and that herring and sprat were important in regulating zooplankton through top-down interactions. We suggest that the positive relationships among zooplankton groups were due to selective foraging and switching in the two clupeid fishes. Our results suggest that “wasp-waist” interactions might be more important in the North Sea than previously anticipated. Fluctuations in the populations of pelagic fish due to harvesting and depletion of their predators might accordingly have profound consequences for ecosystem dynamics through trophic cascades.     

Egg production and hatching success in the calanoid copepods Calanus helgolandicus and Calanus finmarchicus in the North Sea from March to September 2001

Spatial and seasonal egg production rates (E_r) and egg hatchingsuccess in the copepods Calanus finmarchicus and Calanus helgolandicuswere measured in the North Sea from March to September. Foodavailability was monitored by chlorophyll and protist concentrationsand three size fractions of seston fatty acids. Seasonal andspatial distribution and production differed between the species.Calanus finmarchicus was found only offshore of the 50-m isobath,with decreasing E_r (37–28 eggs female^–1 day^–1)from March to July. Calanus helgolandicus had two abundancepeaks, in spring and autumn, with a low in May during whichtime the highest E_r were observed (38 eggs female^–1 day^–1).At other times, E_r in C. helgolandicus remained lower than inC. finmarchicus (     

Climate,copepods and seabirds in the boreal Northeast Atlantic – current state and future outlook

The boreal Northeast Atlantic is strongly affected by current climate change, and large shifts in abundance and distribution of many organisms have been observed, including the dominant copepod Calanus finmarchicus, which supports the grazing food web and thus many fish populations. At the same time, large‐scale declines have been observed in many piscivorous seabirds, which depend on abundant small pelagic fish. Here, we combine predictions from a niche model of C. finmarchicus with long‐term data on seabird breeding success to link trophic levels. The niche model shows that environmental suitability for C. finmarchicus has declined in southern areas with large breeding seabird populations (e.g. the North Sea), and predicts that this decline is likely to spread northwards during the 21st century to affect populations in Iceland and the Faroes. In a North Sea colony, breeding success of three common piscivorous seabird species [black‐legged kittiwake (Rissa tridactyla), common guillemot (Uria aalge) and Atlantic puffin (Fratercula arctica)] was strongly positively correlated with local environmental suitability for C. finmarchicus, whereas this was not the case at a more northerly colony in west Norway. Large seabird populations seem only to occur where C. finmarchicus is abundant, and northward distributional shifts of common boreal seabirds are therefore expected over the coming decades. Whether or not population size can be maintained depends on the dispersal ability and inclination of these colonial breeders, and on the carrying capacity of more northerly areas in a warmer climate.     

The species chromatogram,a new graphical method to represent,characterize, and compare the ecological niches of different species

The ecological niche sensu Hutchinson is defined as the set of environmental conditions allowing a species to grow, maintain, and reproduce. This conception of the niche, which is assimilated to a p‐dimensional hypervolume, with p representing all environmental variables, has been widely applied in ecology. However, displaying the niche hypervolume has proved challenging when more than three environmental dimensions are considered simultaneously. We propose a simple method (implemented in the specieschrom R package) that displays the full multidimensionality of the ecological niche of a species into a two‐dimensional space by means of a graphic we call species chromatogram. This method gives a graphical summary of the niche by representing together abundance gradients with respect to all environmental variables. A chromatogram enables niche optimums and breaths to be rapidly quantified, and when several chromatograms are examined (one per species), rapid comparisons can be made. From our chromatograms, we proposed a procedure that quantifies niche optimum and breadth as well as niche overlapping (index D) and the identification of the most discriminant combination of environmental variables. We apply these analyses on eight planktonic species collected by the Continuous Plankton Recorder (CPR) survey in the North Atlantic Ocean using 10 environmental variables. We display their full multidimensional niches and quantify their niche optimums and breadths along each dimension. We also compare our index D with other indices by means of hypervolume and dynRB R packages. By catching the full complexity of the niche, species chromatograms allow many different niche properties to be rapidly assessed and compared among species from niche optimums and breadths to the identification of the most relevant environmental parameters and the degree of niche overlapping among species. Species chromatograms may be seen as species’ fingerprint and may also allow a better identification of the mechanisms involved in species assembly.     

The occurrence of Calanus finmarchicus (Gunnerus) and Calanus helgolandicus (Claus) in the western Irish Sea

The seasonal abundance of Calanus finmarchicus and Calanus helgolandicusin the North Channel and stratified region of the western IrishSea is reviewed using data collected between 1992 and 1996.Both species occur in the western Irish Sea, but were more abundantin the stratified region during spring. Increased abundanceduring May/June was attributed to an increase in copepoditestages. Calanus helgolandicus dominated in both regions, exhibitingspring and autumn peaks in abundance in the stratified region.It is argued that the presence of ripe females and naupliarstages in the stratified region is evidence of an in situ breedingpopulation, rather than advection of individuals from populationcentres outside the Irish Sea. The lack of geographical separationof the two species in the western Irish sea, and reports thatboth species occur in the Celtic Sea and Malin Shelf, limitthe use of either species as indicators of exchange processesbetween the Irish Sea and neighbouring waters.     

Ecological Niche Transferability Using Invasive Species as a Case Study

Species distribution modeling is widely applied to predict invasive species distributions and species range shifts under climate change. Accurate predictions depend upon meeting the assumption that ecological niches are conserved, i.e., spatially or temporally transferable. Here we present a multi-taxon comparative analysis of niche conservatism using biological invasion events well documented in natural history museum collections. Our goal is to assess spatial transferability of the climatic niche of a range of noxious terrestrial invasive species using two complementary approaches. First we compare species’ native versus invasive ranges in environmental space using two distinct methods, Principal Components Analysis and Mahalanobis distance. Second we compare species’ native versus invaded ranges in geographic space as estimated using the species distribution modeling technique Maxent and the comparative index Hellinger’s I. We find that species exhibit a range of responses, from almost complete transferability, in which the invaded niches completely overlap with the native niches, to a complete dissociation between native and invaded ranges. Intermediate responses included expansion of dimension attributable to either temperature or precipitation derived variables, as well as niche expansion in multiple dimensions. We conclude that the ecological niche in the native range is generally a poor predictor of invaded range and, by analogy, the ecological niche may be a poor predictor of range shifts under climate change. We suggest that assessing dimensions of niche transferability prior to standard species distribution modeling may improve the understanding of species’ dynamics in the invaded range.     

Using Species Distribution Models to Predict Potential Landscape Restoration Effects on Puma Conservation

A mosaic of intact native and human-modified vegetation use can provide important habitat for top predators such as the puma (Puma concolor), avoiding negative effects on other species and ecological processes due to cascade trophic interactions. This study investigates the effects of restoration scenarios on the puma’s habitat suitability in the most developed Brazilian region (São Paulo State). Species Distribution Models incorporating restoration scenarios were developed using the species’ occurrence information to (1) map habitat suitability of pumas in São Paulo State, Southeast, Brazil; (2) test the relative contribution of environmental variables ecologically relevant to the species habitat suitability and (3) project the predicted habitat suitability to future native vegetation restoration scenarios. The Maximum Entropy algorithm was used (Test AUC of 0.84 ± 0.0228) based on seven environmental non-correlated variables and non-autocorrelated presence-only records (n = 342). The percentage of native vegetation (positive influence), elevation (positive influence) and density of roads (negative influence) were considered the most important environmental variables to the model. Model projections to restoration scenarios reflected the high positive relationship between pumas and native vegetation. These projections identified new high suitability areas for pumas (probability of presence >0.5) in highly deforested regions. High suitability areas were increased from 5.3% to 8.5% of the total State extension when the landscapes were restored for ≥ the minimum native vegetation cover rule (20%) established by the Brazilian Forest Code in private lands. This study highlights the importance of a landscape planning approach to improve the conservation outlook for pumas and other species, including not only the establishment and management of protected areas, but also the habitat restoration on private lands. Importantly, the results may inform environmental policies and land use planning in São Paulo State, Brazil.     

Using Energetic Models to Investigate the Survival and Reproduction of Beaked Whales (family Ziphiidae)

Mass stranding of several species of beaked whales (family Ziphiidae) associated with exposure to anthropogenic sounds has raised concern for the conservation of these species. However, little is known about the species’ life histories, prey or habitat requirements. Without this knowledge, it becomes difficult to assess the effects of anthropogenic sound, since there is no way to determine whether the disturbance is impacting the species’ physical or environmental requirements. Here we take a bioenergetics approach to address this gap in our knowledge, as the elusive, deep-diving nature of beaked whales has made it hard to study these effects directly. We develop a model for Ziphiidae linking feeding energetics to the species’ requirements for survival and reproduction, since these life history traits would be the most likely to be impacted by non-lethal disturbances. Our models suggest that beaked whale reproduction requires energy dense prey, and that poor resource availability would lead to an extension of the inter-calving interval. Further, given current information, it seems that some beaked whale species require relatively high quality habitat in order to meet their requirements for survival and reproduction. As a result, even a small non-lethal disturbance that results in displacement of whales from preferred habitats could potentially impact a population if a significant proportion of that population was affected. We explored the impact of varying ecological parameters and model assumptions on survival and reproduction, and find that calf and fetus survival appear more readily affected than the survival of adult females.     

Future climate‐driven shifts in distribution of Calanus finmarchicus

Calanus finmarchicus is a key‐structural species of the North Atlantic polar biome. The species plays an important trophic role in subpolar and polar ecosystems as a grazer of phytoplankton and as a prey for higher trophic levels such as the larval stages of many fish species. Here, we used a recently developed ecological niche model to assess the ecological niche (sensu Hutchinson) of C. finmarchicus and characterize its spatial distribution. This model explained about 65% of the total variance of the observed spatial distribution inferred from an independent dataset (data of the continuous plankton recorder survey). Comparisons with other types of models (structured population and ecophysiological models) revealed a clear similarity between modeled spatial distributions at the scale of the North Atlantic. Contemporary models coupled with future projections indicated a progressive reduction of the spatial habitat of the species at the southern edge and a more pronounced one in the Georges Bank, the Scotian Shelf and the North Sea and a potential increase in abundance at the northern edge of its spatial distribution, especially in the Barents Sea. These major changes will probably lead to a major alteration of the trophodynamics of North Atlantic ecosystems affecting the trophodynamics and the biological carbon pump.     

Genome-wide genetic variation coupled with demographic and ecological niche modeling of the dusky-footed woodrat (Neotoma fuscipes) reveal patterns of deep divergence and widespread Holocene expansion across northern California

Understanding how species have responded to past climate change may help refine projections of how species and biotic communities will respond to future change. Here, we integrate estimates of genome-wide genetic variation with demographic and niche modeling to investigate the historical biogeography of an important ecological engineer: the dusky-footed woodrat, Neotoma fuscipes. We use RADseq to generate a genome-wide dataset for 71 individuals from across the geographic distribution of the species in California. We estimate population structure using several model-based methods and infer the demographic history of regional populations using a site frequency spectrum-based approach. Additionally, we use ecological niche modeling to infer current and past (Last Glacial Maximum) environmental suitability across the species’ distribution. Finally, we estimate the directionality and possible spatial origins of regional population expansions. Our analyses indicate this species is subdivided into three regionally distinct populations, with the deepest divergence occurring ~1.7 million years ago across the modern-day San Francisco-Bay Delta region; a common biogeographic barrier for the flora and fauna of California. Our models of environmental suitability through time coincide with our estimates of population expansion, with relative long-term stability in the southern portion of the range, and more recent expansion into the northern end of the range. Our study illustrates how the integration of genome-wide data with spatial and demographic modeling can reveal the timing and spatial extent of historic events that determine patterns of biotic diversity and may help predict biotic response to future change.Subject terms: Evolutionary genetics, Molecular evolution     

Spatial Transferability of Habitat Suitability Models of Nephrops norvegicus among Fished Areas in the Northeast Atlantic: Sufficiently Stable for Marine Resource Conservation?

Knowledge of the spatial distribution and habitat associations of species in relation to the environment is essential for their management and conservation. Habitat suitability models are useful in quantifying species-environment relationships and predicting species distribution patterns. Little is known, however, about the stability and performance of habitat suitability models when projected into new areas (spatial transferability) and how this can inform resource management. The aims of this study were to model habitat suitability of Norway lobster (Nephrops norvegicus) in five fished areas of the Northeast Atlantic (Aran ground, Irish Sea, Celtic Sea, Scotland Inshore and Fladen ground), and to test for spatial transferability of habitat models among multiple regions. Nephrops burrow density was modelled using generalised additive models (GAMs) with predictors selected from four environmental variables (depth, slope, sediment and rugosity). Models were evaluated and tested for spatial transferability among areas. The optimum models (lowest AICc) for different areas always included depth and sediment as predictors. Burrow densities were generally greater at depth and in finer sediments, but relationships for individual areas were sometimes more complex. Aside from an inclusion of depth and sediment, the optimum models differed between fished areas. When it came to tests of spatial transferability, however, most of the models were able to predict Nephrops density in other areas. Furthermore, transferability was not dependent on use of the optimum models since competing models were also able to achieve a similar level of transferability to new areas. A degree of decoupling between model ‘fitting’ performance and spatial transferability supports the use of simpler models when extrapolating habitat suitability maps to different areas. Differences in the form and performance of models from different areas may supply further information on the processes shaping species’ distributions. Spatial transferability of habitat models can be used to support fishery management when the information is scarce but caution needs to be applied when making inference and a multi-area transferability analysis is preferable to bilateral comparisons between areas.     

Multi-Axis Niche Examination of Ecological Specialization: Responses to Heat,Desiccation and Starvation Stress in Two Species of Pit-Building Antlions

Classical ecological studies discussing specialization usually focus on species’ performance along one niche axis. This approach may overlook niche differentiation evident in another dimension which could explain species co-occurrence. The present research exemplifies a comprehensive approach to examining local adaptation. Specifically, we examined multiple niche axes by subjecting a model organism to various experimental conditions to monitor responses to extreme stress associated with heat, desiccation and starvation. Our model system comprised two pit-building antlions: the habitat generalist Myrmeleon hyalinus and the habitat specialist Cueta lineosa. Previous research has shown that the foraging performance of the generalist is better than that of the specialist, even in the latter’s characteristic habitat. We illustrate that this apparent superiority of the habitat generalist does not manifest itself along other niche axes; rather, the habitat specialist holds a set of traits that provide an advantage under harsh environmental conditions. Specifically, C. lineosa has an advantage over M. hyalinus at high temperatures, exhibiting a higher survival rate and improved foraging success (i.e., high-temperature specialist). C. lineosa is also more efficient in its energy budget, losing less mass during starvation and gaining mass more efficiently during feeding. This superior efficiency is a result of physiological adaptations as well as behavioural responses to harsh conditions. In conclusion, our results imply that the habitat specialization of C. lineosa has not led it towards an evolutionary dead-end.     

Integrating conventional microscopy and molecular analysis to analyse the abundance and distribution of four Calanus congeners in the North Atlantic

Analysis of the demographic structure of Calanus species inthe North Atlantic presents particular difficulties due to theoverlapping spatial distributions of four main congeneric species(Calanus finmarchicus, Calanus helgolandicus, Calanus glacialisand Calanus hyperboreus). These species have similar morphologies,making microscopic discrimination only possible between someof the species at late copepodite or adult stages. However,molecular techniques now offer the possibility of screeningsignificant numbers of specimens and unambiguously identifyingthem to species, regardless of developmental stage. Unfortunately,the processing rate of specimens by molecular methods is stilltoo low to offer a realistic alternative to microscopy for analysisof samples from large field surveys. Here, we outline and testan approach involving the use of molecular methodology in conjunctionwith conventional microscopy to assess the species assignmentof developmental stage abundances of Calanus congeners. Ourstudy has highlighted many important methodological issues.First, it cannot be assumed that the species composition ishomogeneous across the development stages; applying proportionalspecies composition of adults to morphologically undistinguishableearlier development stages can result in error. The second importantconclusion is that prosome length may be a highly unreliablediscriminator of C. finmarchicus and C. glacialis.     

A new approach to interspecific synchrony in population ecology using tail association

Standard methods for studying the association between two ecologically important variables provide only a small slice of the information content of the association, but statistical approaches are available that provide comprehensive information. In particular, available approaches can reveal tail associations, that is, accentuated or reduced associations between the more extreme values of variables. We here study the nature and causes of tail associations between phenological or population‐density variables of co‐located species, and their ecological importance. We employ a simple method of measuring tail associations which we call the partial Spearman correlation. Using multidecadal, multi‐species spatiotemporal datasets on aphid first flights and marine phytoplankton population densities, we assess the potential for tail association to illuminate two major topics of study in community ecology: the stability or instability of aggregate community measures such as total community biomass and its relationship with the synchronous or compensatory dynamics of the community''s constituent species; and the potential for fluctuations and trends in species phenology to result in trophic mismatches. We find that positively associated fluctuations in the population densities of co‐located species commonly show asymmetric tail associations; that is, it is common for two species’ densities to be more correlated when large than when small, or vice versa. Ordinary measures of association such as correlation do not take this asymmetry into account. Likewise, positively associated fluctuations in the phenology of co‐located species also commonly show asymmetric tail associations. We provide evidence that tail associations between two or more species’ population‐density or phenology time series can be inherited from mutual tail associations of these quantities with an environmental driver. We argue that our understanding of community dynamics and stability, and of phenologies of interacting species, can be meaningfully improved in future work by taking into account tail associations.     

Marine biological shifts and climate

Phenological, biogeographic and community shifts are among the reported responses of marine ecosystems and their species to climate change. However, despite both the profound consequences for ecosystem functioning and services, our understanding of the root causes underlying these biological changes remains rudimentary. Here, we show that a significant proportion of the responses of species and communities to climate change are deterministic at some emergent spatio-temporal scales, enabling testable predictions and more accurate projections of future changes. We propose a theory based on the concept of the ecological niche to connect phenological, biogeographic and long-term community shifts. The theory explains approximately 70% of the phenological and biogeographic shifts of a key zooplankton Calanus finmarchicus in the North Atlantic and approximately 56% of the long-term shifts in copepods observed in the North Sea during the period 1958–2009.     

In a comfort zone and beyond—Ecological plasticity of key marine mediators

Copepods of the genus Calanus are the key components of zooplankton. Understanding their response to a changing climate is crucial to predict the functioning of future warmer high‐latitude ecosystems. Although specific Calanus species are morphologically very similar, they have different life strategies and roles in ecosystems. In this study, C. finmarchicus and C. glacialis were thoroughly studied with regard to their plasticity in morphology and ecology both in their preferred original water mass (Atlantic vs. Arctic side of the Polar Front) and in suboptimal conditions (due to, e.g., temperature, turbidity, and competition in Hornsund fjord). Our observations show that “at the same place and time,” both species can reach different sizes, take on different pigmentation, be in different states of population development, utilize different reproductive versus lipid accumulation strategies, and thrive on different foods. Size was proven to be a very mutable morphological trait, especially with regard to reduced length of C. glacialis. Both species exhibited pronounced red pigmentation when inhabiting their preferred water mass. In other domains, C. finmarchicus individuals tended to be paler than C. glacialis individuals. Gonad maturation and population development indicated mixed reproductive strategies, although a surprisingly similar population age structure of the two co‐occurring species in the fjord was observed. Lipid accumulation was high and not species‐specific, and its variability was due to diet differences of the populations. According to the stable isotope composition, both species had a more herbivorous diatom‐based diet in their original water masses. While the diet of C. glacialis was rather consistent among the domains studied, C. finmarchicus exhibited much higher variability in its feeding history (based on lipid composition). Our results show that the plasticity of both Calanus species is indeed impressive and may be regulated differently, depending on whether they live in their “comfort zone” or beyond it.     

Environmental gradients of selection for an alpine-obligate bird,the white-tailed ptarmigan (Lagopus leucura)

The warming climate will expose alpine species adapted to a highly seasonal, harsh environment to novel environmental conditions. A species can shift their distribution, acclimate, or adapt in response to a new climate. Alpine species have little suitable habitat to shift their distribution, and the limits of acclimation will likely be tested by climate change in the long-term. Adaptive genetic variation may provide the raw material for species to adapt to this changing environment. Here, we use a genomic approach to describe adaptive divergence in an alpine-obligate species, the white-tailed ptarmigan (Lagopus leucura), a species distributed from Alaska to New Mexico, across an environmentally variable geographic range. Previous work has identified genetic structure and morphological, behavioral, and physiological differences across the species’ range; however, those studies were unable to determine the degree to which adaptive divergence is correlated with local variation in environmental conditions. We used a genome-wide dataset generated from 95 white-tailed ptarmigan distributed throughout the species’ range and genotype–environment association analyses to identify the genetic signature and environmental drivers of local adaptation. We detected associations between multiple environmental gradients and candidate adaptive loci, suggesting ptarmigan populations may be locally adapted to the plant community composition, elevation, local climate, and to the seasonality of the environment. Overall, our results suggest there may be groups within the species’ range with genetic variation that could be essential for adapting to a changing climate and helpful in guiding conservation action.Subject terms: Ecological genetics, Evolutionary ecology     

Vertical distribution and seasonal numerical abundance of the Calanidae in oceanic waters to the south-west of the British Isles

The vertical distribution and seasonal abundance of the copepodite and adult stages of Calanus finmarchicus, C. helgolandicus, C. tenuicornis, Neocalanus gracilis, Nannocalanus minor and Calanoides carinatus from a series of Longhurst Hardy Plankton Recorder hauls taken in the oceanic waters, off the continental shelf, to the south-west of the British Isles are described. The sampling area was selected because the geographical distributions of the major Calanidae copepods of the north-east Atlantic Ocean are shown to overlap in this region. It marks the southern boundary of the distribution of C. finmarchicus, the central area of C. helgolandicus and the approximate northern limit of distribution of C. tenuicornis, N. gracilis, N. minor and C. carinatus. These four southern species occasionally penetrate further north (60° N) in the open ocean but do not breed at these northern latitudes. In autumn and winter, when C. finmarchicus and C. helgolandicus were overwintering below 400 m primarily as Stage V copepodites, N. gracilis occurred in the upper 200 m of the water column in a breeding condition; all copepodite stages were present. This copepod reproduced throughout the year in this regions while C. tenuicornis was observed to breed primarily in spring and summer. The geographical and vertical distributions of the Calanidae are related to the observed seasonal temperatures of the North Atlantic and the breeding strategies of species are compared.     

Global changes explain the long-term demographic trend of the Eurasian common lizard (Squamata: Lacertidae)

The demographic trend of a species depends on the dynamics of its local populations, which can be compromised by local or by global phenomena. However, the relevance of local and global phenomena has rarely been investigated simultaneously. Here, we tested whether local phenomena compromised a species’ demographic trend using the Eurasian common lizard Zootoca vivipara, the terrestrial reptile exhibiting the widest geographic distribution, as a model species. We analyzed the species’ ancient demographic trend using genetic data from its 6 allopatric genetic clades and tested whether its demographic trend mainly depended on single clades or on global phenomena. Zootoca vivipara’s effective population size increased since 2.3 million years ago and started to increase steeply and continuously from 0.531 million years ago. Population growth rate exhibited 2 maxima, both occurring during global climatic changes and important vegetation changes on the northern hemisphere. Effective population size and growth rate were negatively correlated with global surface temperatures, in line with global parameters driving long-term demographic trends. Zootoca vivipara’s ancient demography was neither driven by a single clade, nor by the 2 clades that colonized huge geographic areas after the last glaciation. The low importance of local phenomena, suggests that the experimentally demonstrated high sensitivity of this species to short-term ecological changes is a response in order to cope with short-term and local changes. This suggests that what affected its long-term demographic trend the most, were not these local changes/responses, but rather the important and prolonged global climatic changes and important vegetation changes on the northern hemisphere, including the opening up of the forest by humans.