Soil seed bank assembly following secondary succession on abandoned agricultural fields in Nicaragua

The composition and density of seeds in soils of secondary forests derived on abandoned fields after 4, 9 and 14 years of aban- donment were quantified to examine whether the soil seed bank assembles during secondary succession as the plant communities assemble. A total of 18, 37 and 48 soil samples from 4-, 9- and 14-year old sites, respectively were collected in 15 cm × 15 cm plots up to 9 cm depth. A total of 3, 5 and 9 species were found on sites abandoned 4, 9 and 14 years ago, respectively, Among different life forms, trees were highly represented in the soil seed bank of 9-year （60%） and 14-year （33%） old sites compared to 4-year old site entirely dominated by non- woody flora. The total number of seeds ranged from 327 in the 4-year old site to 146 in the 14-year old site, and the corresponding density of viable seeds ranged from 141 seeds m^-2 in the 4- year old site to 26 seeds m^-2 in the 14-year old site with a consistent decreasing pattern in the chronosequence. The similarity between the soil seed flora and the standing woody vegetation was low for both 9- and 14-year old sites while complete dissimilarity was found for 4-year old site. We concluded that the species composition of soil seed banks assemble gradually during secondary succession, but the overall seed density is still low for natural regeneration of trees to rely on. To expedite the recovery of secondary forests on such abandoned fields, the seed bank needs to be supplemented by direct seeding, enrichment planting of desired species and installing artificial perches for facilitating seed dispersal.

NITROGEN NUTRIENT MECHANISM IN SECONDARY SUCCESSION PROCESS OF THE MIXED BROAD-LEAVED/ KOREAN PINE (PINUS KORAIENSIS) FOREST

Chemical and biochemical analysis methods were used to monitor the vedations of nitrogen nutrient among the dominance trees species in secondary succession process of the mixed broad - leaved/Korean pine forest on Changbai Mountains, Northeast China. Amounts of total nitrogen, anunonium and NRA in soils of virgin broad-leaved/Korean pine forest which is in climax were higher than those of secondary birch forests those are in succession Stage. The amount of nitrate was in the other hand. In climax, dominance trees species are tolerant mesophytic trees such as Pinus Koraiensis, Tilia amurensis, Acer mono and also Fraxinus mandshurica, they are all ammonium + nitrate adapted species, but they show a preference for the anunonium rather than those of the pioneer trees species in secondary birch forest, such as Populus davidiava and Betula platyphylla. Because they have more ammonium in their leaves and roots, especially Pinus koraiensis. Populus davidvana and Betula plaaphlla are intolerant trees, amounts of nitrate and total nitrogen is higher in their leaves and roots and also NRA in their leaves, so they preference for the nitrate rather than the others.In secondary birch forest, the regeneration trees species adapt their nitroggn nutrient to the variation of nitrogen nutrient situation in soil, finally they could survival well and the secondary birch forest would succession to climax. In climax, dominance trees species adapt their Nitrogen nutrient to the situation in soil and there are not strong competition in nitrogen nutrient among them, so they can coexist well and keep the climax as stable vegetation.

Soil microbes-mediated enzymes promoted the secondary succession in post-mining plantations on the Loess Plateau,China

The diversity of vegetation configuration is the key to ecological restoration in open-pit coal mine dump.However,the recovery outcomes of different areas with the same vegetation assemblage pattern are completely different after long-term evolution.Therefore,understanding the causes of differential vegetation recovery and the mechanism of plant succession is of great significance to the ecological restoration of mines.Three Pinus tabulaeformis plantations with similar initial site conditions and restoration measures but with different secondary succession processes were selected from the open-pit coal mine dump that has been restored for 30 years.Soil physicochemical properties,enzyme activities,vegetation and microbial features were investigated,while the structural equation models were established to explore the interactions between plants,soil and microbes.The results showed that original vegetation configuration and soil nutrient conditions were altered due to secondary succession.With the advancement of the secondary succession process,the coverage of plants increased from 34.8%to 95.5%(P<0.05),soil organic matter increased from 9.30 g kg^(-1)to 21.13 g kg^(-1)(P<0.05),and total nitrogen increased from 0.38 g kg^(-1)to 1.01 g kg^(-1)(P<0.05).The activities of soil urease and p-glucosidase were increased by 1.7-fold and 53.26%,respectively.Besides,the secondary succession also changed the soil microbial community structure and function.The relative abundance of Nitrospira genus which dominates the nitrification increased 5.2-fold.The results showed that urease andβ-glucosidase promoted the increase of vegetation diversity and biomass by promoting the accumulation of soil organic matter and nitrate nitrogen,which promoted the ecological restoration of mine dumps.

Soil legacy effects and plant-soil feedback contribution to secondary succession processes

Secondary succession is the process by which a community develops into a climax community over time.However,knowledge on the mechanisms,relating to soil legacy effects(soil chemistry and enzyme activity)and plant-soil feedback(PSF),driving community succession remains limited.In this work,we examined the PSF associated with three succession stage species through a 2-year greenhouse experiment.Setaria viridis,Stipa bungeana,and Bothriochloa ischemum were selected to represent dominant and representative early-,mid-,and late-successional stage species,respectively,of semiarid grasslands on the Loess Plateau.In response to the different soil origin,the shoot biomass of early-,mid-,and late-species were all higher when grown in their own soil than in other species’soils,which indicated that the PSF of three species were positive.Over two growth periods,the early-species experienced a negative PSF,but the mid-and late-species experienced negative,neutral and positive PSF in the soil of early-,mid-and late-species,respectively.Our study demonstrates that soil legacy effects and PSF have a significant impact on community succession processes.

Positive effects of tree species diversity on litterfall quantity and quality along a secondary successional chronosequence in a subtropical forest

Aims Litterfall,as an important link between aboveground and belowground processes,plays a key role in forest ecosystems.Here,we test for effects of tree species richness on litter production and litter quality in subtropical forest.The study further encompasses a factorial gradient of secondary succession that resulted from human exploitation.Given that a large percentage of subtropical forests are in secondary successional stages,understanding the role of biodiversity on forest re-growth after disturbance appears critical.Methods From January 2009 to December 2014,we monitored forest litterfall in 27 Comparative Study Plots that spanned a gradient of tree species richness(3-20 species)and secondary successional ages(~20 to 120 years)in Gutianshan Natural Nature Reserve,Zhejiang Province,China.The experiment is part of the biodiversity-ecosystem functioning research platform‘BEF-China’.Tree litterfall was collected in monthly intervals using litter traps.Samples were separated into leaf and non-leaf components.Leaf litter was further sorted into dominant and other species.Community level monthly leaf litter C and N contents were analysed through a full year.General linear mixed-effects models were applied to test for effects of tree species richness and successional age on litter quantity and leaf litter C/N.Important Findings Litterfall increased with species richness among and within successional age and this effect was consistent across years.Successionally older stands had higher litterfall and this effect was related to increased tree species richness.However,species richness did not change the intra-and inter-annual temporal stability of litterfall.Increasing tree species richness increased leaf litter quality(decreased C/N),while successional age had no effect.Our study indicates that more diverse forest stands produce more leaf litter and that this litter has higher N concentrations,which could promote forest growth through accelerated nutrient re-cycling.

Leguminosae plants play a key role in affecting soil physical-chemical and biological properties during grassland succession after farmland abandonment in the Loess Plateau,China

Leguminosae are an important part of terrestrial ecosystems and play a key role in promoting soil nutrient cycling and improving soil properties.However,plant composition and species diversity change rapidly during the process of succession,the effect of leguminosae on soil physical-chemical and biological properties is still unclear.This study investigated the changes in the composition of plant community,vegetation characteristics,soil physical-chemical properties,and soil biological properties on five former farmlands in China,which had been abandoned for 0,5,10,18,and 30 a.Results showed that,with successional time,plant community developed from annual plants to perennial plants,the importance of Leguminosae and Asteraceae significantly increased and decreased,respectively,and the importance of grass increased and then decreased,having a maximum value after 5 a of abandonment.Plant diversity indices increased with successional time,and vegetation coverage and above-and below-ground biomass increased significantly with successional time after 5 a of abandonment.Compared with farmland,30 a of abandonment significantly increased soil nutrient content,but total and available phosphorus decreased with successional time.Changes in plant community composition and vegetation characteristics not only change soil properties and improve soil physical-chemical properties,but also regulate soil biological activity,thus affecting soil nutrient cycling.Among these,Leguminosae have the greatest influence on soil properties,and their importance values and community composition are significantly correlated with soil properties.Therefore,this research provides more scientific guidance for selecting plant species to stabilize soil ecosystem of farmland to grassland in the Loess Plateau,China.

Trajectories in nitrogen availability during forest secondary succession:illustrated by foliarδ^(15)N

Background:Forest succession is an important ecological process and has been studied for more than a century.However,changes in nitrogen(N)availability during succession remain unclear as they may lead to either N satura-tion or N limitation.Here,we propose a conceptual model to illustrate changes in N availability during four stages of secondary succession using the natural abundance of ^(15) N in plant leaves(foliarδ^(15)N).We predicted that N availability would decline in the early stages of succession and then increase in late stages,coinciding with the changes in foliarδ^(15)N,with the inflection point varying in different climate zones.Data on foliarδ^(15)N from 16 succession sequences were synthesized to explore changes in N availability during forest succession.Results:The compiled data were consistent with the proposed conceptual model.Foliarδ^(15)N in boreal and temperate forests decreased significantly in the first two stages of succession(estimated to last at least 66 years in temperate forests),at a rate of 0.18‰and 0.38‰per decade,respectively,and decreased slightly in tropical forests in the first 23 years.Foliarδ^(15)N is projected to increase in later stages in all forests,which is supported by observations in both temperate and tropical forests.The inflection points of N availability when N limitation peaked during succession were different in different climate zones,implying different ecosystem N turnovers.Conclusions:Our study reconciles the controversies regarding changes in N availability during forest secondary succession.Our findings are also useful for predicting the recovery of N and carbon accumulation during succession.Nonetheless,studies on forest secondary succession using foliarδ^(15)N have thus far been limited,and more research should be conducted to further verify the conceptual model proposed here.

Vegetation cover of the lahar valley on the Sarychev Peak volcano(Matua Isl.,Middle Kuril Islands) after the Eruption in 2009: current state and features of succession processes

The paper presents the study of the vegetation recovery after the descent of the lahar during the eruption of the Sarychev Peak volcano(Matua Isl.,Middle Kuriles) in 2009.The works were carried out in 2017.It was found that during the secondary succession,plant communities,typical of the altitudinal zonation of the volcanic structure vegetation,are formed on lahar sediments in the following manner: the upper sections of the slope are occupied by sparse meadow and shrub vegetation,the middle are presented by shrub belt with a developed canopy,and the lower are representative of shrub large-grass belt.At the same time,the ordination analysis of the vegetation cover of the lahar valley by the detrended correspondence analysis(DCA) revealed the dispersion of the counting areas along the altitudinal gradient.This is opposite to that characteristic for both,the background communities on the slopes of the studied volcanic structure,and for communities in dynamical equilibrium of a typical altitude profile.Besides,directly correlating indicators of α-diversity of communities indicate the presence of open young communities at the stage of a complex grouping.Since the species Duschekia fruticosa which is an identifier in buried sites,forms communities in a state of dynamic equilibrium,with individuals of 40–50 years old,and at the time of the work,formed a canopy with individuals of 7–8 years old,a complete recovery of the communities of the lahar valley is possible in no less than 40 years.The acquired data on the recovery of vegetation on lahar contribute to the study of succession processes in the sites located in the zone of active volcanism.In addition,in this work,for the first time,the rates of restoration of the vegetation cover following its destruction as a result of burial by lahar products,are estimated.The specific features of this process are also considered.Employing the broad range of mathematical methods for quantitative analysis of indicators of young communities inhabiting the substrate makes it possible to identify patterns of vegetation formed during succession processes.The specifics of this organization are taken into account in this analysis.

A chronosequence analysis of forest recovery on abandoned agricultural fields in Nicaragua

Species composition, diversity and population structure of woody species recovered on three abandoned agricultural fields after 4, 9 and 14 years were characterized. Seedlings, saplings/poles and mature trees were identified and counted in 70 plots of 100 m^2 in each abandoned site. A total of 13, 29 and 22 families represented by 17, 48 and 44 species were registered in 4-, 9- and 14-year-old stands, respectively. There was a shift in dominant species across successional stages. Lonchocarpus acuminatus had the highest importance value in the 4-year old stand, whereas, Myrospermun frutescens, Guazurna ulmifolia and Cordia alliodora had the highest importance value in the 9-year-old-stand and Caesaeria corymbosa, Muntingia calabura, Gliricidia sepium and Tabebuia rosea in the 14-year-old stand. The total stem density increased from 5011 to 9631 individuals per hectare as the age of abandonment increased from 4 to 14 years. The total basal area of individuals _〉 I cm d.b.h, also increased with the age of abandonment. Overall, small individuals （〈 10 cm dbh） contributed to more than half of the total basal area. Species diversity was the highest in the 9-year old stand followed by 14- and 4-year-old stands. We concluded that floristic composition of secondary forests recovers rapidly to the mature forest level compared to structural attributes, which is consistent with the general successional trajectories of tropical dry forest.

Decline of Traditional Landscape in a Protected Area of the Southwestern Alps:the Fate of Enclosed Pasture Patches in the Land Mosaic Shift

【Title】【Author】【Addresses】1Traditional landscape elements such as pasture patches enclosed in a forest matrix are progressively disappearing throughout the European Alps. We assessed the land mosaic shift of a protected area located in the western Italian Alps. In particular, the dynamics of pasture patches were studied at both landscape and stand level. Land-cover mapping through object-oriented analysis of historical aerial photographs was used to assess land-cover changes between 1954 and 2000. Spatial statistics were used to quantify landscape patterns, and field samplings within pasture patches were used to explore tree regeneration structure and composition. Our results showed a significant increase in the number of pasture patches caused by their fragmentation following forest expansion. The total surface area of pasture patches decreased by 43% and their core area decreased by 94%. The encroachment of trees on less accessible areas of the pasture patches caused a reduction of patch shape at landscape scale. The gap filling process started 40-50 years ago and began with an early invasion of light demanding species like sycamore maple （Acer pseudoplatanus L.） and common ash （Fraxinus excelsior L.）, followed by European beech （Fagus sylvatica L.） and secondarily silver fir （Abies alba Mill.）. Traditional land-use and population decline in the Pesio Valley led to a reduction in ecotone areas. A transition to a more homogeneous landscape is expected in the next decades. Given the cultural and productive nature of these mountain meadow-pasture communities, extensive livestock grazing systems could be used to manage their future conservation.

A chronosequence analysis of forest recovery on abandoned agricultural fields in Nicaragua

Species composition, diversity and population structure of woody species recovered on three abandoned agricultural fields after 4, 9 and 14 years were characterized. Seedlings, saplings/poles and mature trees were identified and counted in 70 plots of 100 m2 in each abandoned site. A total of 13, 29 and 22 families represented by 17, 48 and 44 species were registered in 4-, 9-and 14-year-old stands, respectively. There was a shift in dominant species across successional stages. Lonchocarpus acuminatus had the highest importance value in the 4-year old stand, whereas, Myrospermun frutescens, Guazuma ulmifolia and Cordia alliodora had the highest importance value in the 9-year-old-stand and Caesaeria corymbosa, Muntingia calabura, Gliricidia sepium and Tabebuia rosea in the 14-year-old stand. The total stem density increased from 5011 to 9631 individuals per hectare as the age of abandonment increased from 4 to 14 years. The total basal area of individuals ≥ 1cm d.b.h. also increased with the age of abandonment. Overall, small individuals (< 10 cm dbh) contributed to more than half of the total basal area. Species diversity was the highest in the 9-year old stand followed by 14-and 4-year-old stands. We concluded that floristic composition of secondary forests recovers rapidly to the mature forest level compared to structural attributes, which is consistent with the general successional trajectories of tropical dry forest.

Shifts in community leaf functional traits are related to litter decomposition along a secondary forest succession series in subtropical China

Aims We investigated shifts in community-weighted mean traits(CWm)of 14 leaf functional traits along a secondary successional series in an evergreen broadleaf forest in subtropical southeast China.most of the investigated traits have been reported to affect litter decomposition in previous studies.We asked whether changes in CWms along secondary succession followed similar patterns for all investigated traits and whether the shifts in CWm indicated a change in resource use strategy along the successional gradient.using community decomposition rates(k-rates)estimated from annual lit-ter production and standing litter biomass,we asked whether the dynamics of litter decomposition were related to changes in leaf functional traits along the successional series.Methods twenty-seven plots were examined for shifts in leaf CWm traits as well as in k-rates along a series of secondary forest succession cov-ered in the framework of the bEF-China project.We investigated whether the changes in CWms followed similar patterns for all traits with ongoing succession.three alternative linear models were used to reveal the general patterns of shifts in CWm trait values.moreover,multiple regression analysis was applied to investigate whether there were causal relationships between the changes in leaf functional traits and the dynamics of litter decomposition along secondary succession.We furthermore assessed which traits had the highest impact on community litter decomposition.Important Findingsshifts in CWm values generally followed logarithmic patterns for all investigated traits,whereas community k-rates remained stable along the successional gradient.In summary,the shifts in CWm values indicate a change in community resource use strategy from high nutrient acquisition to nutrient retention with ongoing succession.stands with higher CWm values of traits related to nutrient acquisition had also higher CWm values of traits related to chemical resistance,whereas stands with higher CWm values of traits related to nutrient retention exhibited higher CWm values in leaf physical defense.moreover,high values in CWm values related to nutritional quality(such as high leaf phosphorus concentrations)were found to promote com-munity k-rates,whereas high values in physical or chemical defense traits(such as high contents in polyphenols or high leaf toughness)decreased litter decomposition rates.In consequence,litter decom-position,which was simultaneously affected by these characteristics,did not change significantly along succession.our findings show that leaf decomposition within the investigated communities is dependent on the interplay of several traits and is a result from interactions of traits that affect decomposition in opposing directions.

Successive formation of secondary pores via feldspar dissolution in deeply buried feldspar-rich clastic reservoirs in typical petroliferous basins and its petroleum geological significance

Clastic rock reservoirs in petroliferous basins are generally rich in feldspars. Feldspar dissolution has developed widely in clastic reservoirs, and the resulting secondary pores are crucial in deeply buried reservoirs. Based on a study of the diagenesis of clastic reservoirs in the Bohai Bay Basin, Tarim Basin, and Pearl River Mouth Basin and physical and numerical simulation experiments of fluid-rock interactions, this paper proposed a successive formation model of secondary pores via feldspar dissolution in deeply buried clastic reservoirs, considering the global research progresses in feldspar dissolution in clastic rocks. Feldspar dissolution can occur from shallow open systems to deep-ultra deep closed systems in petroliferous basins, resulting in the successive formation of secondary pores at different diagenetic stages. The successive mechanism includes three aspects. The first aspect is the succession of corrosive fluids that dissolve minerals. Meteoric freshwater dominates at the Earth’s surface and the early diagenetic A stage. Subsequently, organic acids and COformed via kerogen maturation dominate at the early diagenetic B stage to the middle diagenetic stage. COand organic acids formed via hydrocarbon oxidation in hydrocarbon reservoirs dominate at the middle diagenetic B stage to the late diagenetic stage. The second aspect is the successive formation processes of secondary pores via feldspar dissolution. Large-scale feldspar secondary pores identified in deep reservoirs include secondary pores formed at shallow-medium depths that are subsequently preserved into deep layers, as well as secondary pores formed at deep depths. Existing secondary pores in deeply buried reservoirs are the superposition of successively feldspar dissolution caused by different acids at different stages. The third aspect is a successive change in the feldspar alteration pathways and porosity enhancement/preservation effect. Open to semi-open diagenetic systems are developed from the Earth’s surface to the early diagenetic stage, and feldspar dissolution forms enhanced secondary pores. Nearly closed to closed diagenetic systems develop in the middle to late diagenetic stages, and feldspar dissolution forms redistributional secondary pores. The associated cementation causes compression resistance of the rock, which is favorable for the preservation of secondary pores in deep layers. These new insights extend the formation window of secondary pores in petroliferous basins from the traditional acid-oil generation window to a high-temperature gas generation window after hydrocarbon charging. The proposed model explains the genesis of deep-ultra deep high-quality reservoirs with low-permeability, medium-porosity and dominating feldspar secondary pores, which is significant for hydrocarbon exploration in deep to ultra-deep layers.

Earthworms promote greater richness and abundance in the emergence of plant species across a grassland-forest ecotone

Aims Chalk grasslands are subject to vegetation dynamics that range from species-rich open grasslands to tall and encroached grasslands,and woods and forests.In grasslands,earthworms impact plant communities and ecosystem functioning through the modification of soil physical,chemical and microbiological properties,but also through their selective ingestion and vertical transportation of seeds from the soil seed bank.Laboratory experiments showed that seed-earthworm interactions are species specific,but little is known on the impact of seed-earthworm interactions in the field.The overall aim of this study was to better understand seed-earthworm interactions and their impact on the plant community.First we analyzed the composition of seedlings emerging from casts after earthworm ingestion.Then we compared seedling composition in casts to the plant composition of emerging seedlings from the soil and of the aboveground vegetation along four stages of the secondary succession of chalk grasslands.Methods Four stages of the secondary succession of a chalk grassland—from open sward to woods—were sampled in Upper Normandy,France,in February 2010.Within each successional stage(×3 replicates),we sampled the standing vegetation,soil seed bank at three soil depths(0-2,2-5 and 5-10 cm)and earthworm surface casts along transects.Soil and cast samples were water sieved before samples were spread onto trays and placed into a greenhouse.Emerging seedlings were counted and identified.Effect of successional stage and origin of samples on mean and variability of abundance and species richness of seedlings emerging from casts and soil seed banks were analyzed.Plant compositions were compared between all sample types.We used generalized mixed-effect models and a distance-based redundancy multivariate analysis.Important Findings Seedling abundance was always higher in earthworm casts than in the soil seed bank and increased up to 5-fold,4-fold and 3.5-fold,respectively,in the tall grassland,woods and encroached grassland compared to the soil surface layer.Species richness was also higher in earthworm casts than in the soil seed bank in all successional stages,with a 4-fold increase in the encroached grassland.The plant composition of the standing vegetation was more similar to that of seedlings from casts than to that of seedlings from the soil seed bank.Seedlings diversity emerging from casts in the tall and encroached grasslands tended toward the diversity found in woods.Our results indicate that earthworms may promote the emergence of seedlings.We also suggest that the loss of some plant species in the seed bank and the tall grass vegetation in intermediary successional stages modify the local conditions and prevent the further establishment of early-successional plant species.

Patterns of grassland invasions by trees: insights from demographic and genetic spatial analyses

Aims Woody invasions into grasslands have increased globally due to changing land use,climate and introduced woody species,but spatial processes generating and sustaining these invasions are not well understood.To gain insight into the patterns of spread of tree populations within grasslands,and to propose a full spatial analytical toolbox for studying native and non-native woody spe-cies spread when long-term data are not available,we tested if 50 years of grassland invasion in Western Carpathians by Norway spruce(Picea abies Karst.)proceeded by one of the two tradi-tionally competing hypotheses of species spread:(i)by frontier expansion,or(ii)by advanced groups established ahead of the population frontier.We also tested whether the pattern of invasion changed over time.Methods We analyzed the spatial demographic and genetic patterns of a Norway spruce population invading a Western Carpathian grass-land using ripley’s L(t)and genetic kinship coefficients(Fij).We mapped and genotyped spruce trees across the invasion front(from the invasion leading edge to fully colonized grassland near the source population)using three demographic classes(adults,juve-niles and seedlings)to approximate the temporal aspects of the invasion.We studied how the spatial patterns of invasion by indi-vidual demographic classes and their genetic kinship varied among adjacent plots established at different distances from the source population(ranging from 0 to 160 m,in 40-m distance increments).Important Findings Juveniles were positively genetically related to adults on fine scales(<4 m),suggesting that adults within the grassland acted as a seed source and accelerated early invasion.However,adults did not act as nucleation centers for the formation of advanced juvenile groups.Instead,geneti-cally unrelated juveniles formed groups independently of adults.These groups were small and separate at the leading edge but they increased in size and graded into a continuous zone near the source population.Thus,juvenile recruitment occurred as a frontier expansion near the source population and as advanced groups controlled by environmental variation at the leading edge.unlike juveniles,seedlings were clustered on all scales across the invasion front and formed groups around adult crowns at the invasion leading edge.The bulk of seedling establishment occurred at intermediate distances from the source population,indepen-dently from the adults,suggesting that the invasion front continued to expand as a frontier,gradually coalescing with the advanced groups at the leading edge.Thus,the grassland invasion was driven by a gradual frontier expansion of the original population during the first 50 years,with advanced groups enhancing but not driving the invasion process.Frontier expansion appeared more important as a mechanism of woody species spread early in the invasion process in this study,while advanced groups may play a larger role over longer temporal scales.