Seasonal microbial processes in a high-latitude fjord (Kongsfjorden, Svalbard): I. Heterotrophic bacteria, picoplankton and nanoflagellates

Temporal dynamics of the microbial food web in the Barents Sea and adjacent water masses in the European Arctic are to a large extent unknown. Seasonal variation in stocks and production rates of heterotrophic bacteria and phototrophic and heterotrophic picoplankton and nanoflagellates was investigated in the upper 50 m of the high-latitude Kongsfjorden, Svalbard, during six field campaigns between March and December 2006. Heterotrophic bacteria, picoplankton and nanoflagellates contributed to ecosystem structure and function in all seasons. Activity within the microbial food web peaked during spring bloom in April, parallel to low abundances of mesozooplankton. In the nutrient-limited post-bloom scenario, an efficient microbial loop, fuelled by dissolved organic carbon from abundant mesozooplankton feeding on phytoplankton and protozooplankton, facilitated maximum integrated primary production rates. A tight microbial food web consisting of heterotrophic bacteria and phototrophic and heterotrophic picoplankton and nanoflagellates was found in the stratified water masses encountered in July and September. Microbial stocks and rates were low but persistent under winter conditions. Seasonal comparisons of microbial biomass and production revealed that structure and function of the microbial food web were fundamentally different during the spring bloom when compared with other seasons. While the microbial food web was in a regenerative mode most of the time, during the spring bloom, a microbial transfer mode represented a trophic link for organic carbon in time and space. The microbial food web’s ability to fill different functional roles in periods dominated by new and regenerated production may enhance the ecological flexibility of pelagic ecosystems in the present era of climate change.     

Intertidal meiofauna of a high-latitude glacial Arctic fjord (Kongsfjorden, Svalbard) with emphasis on the structure of free-living nematode communities

Meiofauna communities of four intertidal sites, two sheltered and two more exposed, in Kongsfjorden (Svalbard) were investigated in summer 2001 at two different tidal levels (i.e. the low-water line and close below the driftline, referred to as mid-water (MW) level). A total of seven meiofaunal higher taxa were recorded with nematodes, oligochaetes and turbellarians being numerically dominant. Mean total meiofaunal densities ranged between 50 ind. 10 cm⁻² and 903 ind. 10 cm⁻². Our data showed a clear decrease in total meiofaunal densities with increasing coarseness of the sediment. Total meiofaunal biomass varied from 0.2 g dwt m⁻² to 2 g dwt m⁻² and, in general, was high even at low meiofaunal densities, i.e. larger interstitial spaces in coarser sediments supported larger meiofauna, especially turbellarians. The results on the vertical distribution of meiofauna contrasted sharply with typical meiobenthic depth profiles on other beaches, probably in response to ice-scouring and concomitant salinity fluctuations. Oligochaetes were the most abundant taxon, with a peak density of 641 ind. 10 cm⁻² at Breoyane Island. They were mainly comprised of juvenile Enchytraeidae, which prohibited identification to species/genus level. Nematode densities ranged between 4 ind. 10 cm⁻² and 327 ind. 10 cm⁻². Nematodes were identified up to genus level and assigned to trophic guilds. In total, 28 nematode genera were identified. Oncholaimus and Theristus were the most abundant genera. The composition of the nematode community and a dominance of predators and deposit feeders were in agreement with results from other arctic and temperate beaches. Nematode genus diversity was higher at the more sheltered beaches than at the more exposed ones. Low-water level stations also tended to harbour a more diverse nematode communities than stations at the MW level. Differences in nematode community structure between low- and MW stations of single beaches were more pronounced than community differences between different beaches and were mainly related to resources quality and availability.     

Distribution of Calanus species in Kongsfjorden, a glacial fjord in Svalbard

The distribution of Calanus species was investigated in Kongsfjordenin summer of 1996 and 1997. In both years Calanus finmarchicusand Calanus glacialis dominated, although the boreal C. finmarchicuswas more abundant than the Arctic C. glacialis in 1997. Thiscoincided with a 2°C higher water temperature at 50 m in1997, indicating stronger influence of Atlantic origin waterthat year. Advected Calanus finmarchicus occurred in deep andsubsurface layers of the outer fjord in 1996 (200 ind. m^-3,mainly CIII). A less abundant local population aggregated insurface layers of the inner fjord (100 ind. m^-3). Similarly,advected C. finmarchicus occurred in subsurface layers in 1997(446 ind. m^-3, mainly CIII and CIV) and a local population insurface layers (183 ind. m^-3, mainly CI). Calanus glacialisin 1996 aggregated as CII and CIII in the deep layers of theouter fjord (272 ind. m^-3), whereas CIII–CV were abundant(216 ind. m^-3) in cold surface waters of the inner fjord. In1997 C. glacialis (mostly CIII–CV) was more abundant inthe outer than in the inner part of the fjord (40 and 192 ind.m^-3, respectively). Within Kongsfjorden, Calanus finmarchicusneeds one year to complete its life cycle, whereas Calanus glacialisneeds two. Calanus hyperboreus seems to be an expatriate inthe fjord system.     

Decadal change in macrobenthic soft-bottom community structure in a high Arctic fjord (Kongsfjorden, Svalbard)

Marine benthic macrofauna communities are considered a good indicator of subtle environmental long-term changes in an ecosystem. In 1997/1998 and 2006, soft-bottom fauna of an Arctic glacial fjord Kongsfjorden was extensively sampled and major communities were identified along the fjord axis, which were related to the diminishing influence of glacial activity. Spatial patterns in community structure and species diversity were significantly different in the central basin of Kongsfjorden between periods while there was no change in the inner part of the fjord. In 1997/98, three faunal associations were distinguished with significant differences in species richness and diversity (H′) while in 2006 only two faunal associations were identified and there were no differences any more between the two formerly distinct associations in the central fjord. The increased input of Atlantic water due to a stronger West Spitsbergen Current may be the reason for unification of previous clear faunal division. The faunal association in the inner, well separated glacial part of the fjord, characterized by strong glacier influence, was protected from Atlantic water inflow and, hence, the macrobenthic fauna essentially remained unaffected. Reduced abundance of species typical for glacial bays in the central part of the fjord in 2006 may result from the decreasing effect of Blomstrandbreen glacier, strong increase of input of Atlantic water into the fjord and increased temperature of West Spitsbergen Current. Higher values of POC in 2006 than in 1998 are likely the effect of increased primary production resulting from warmer water temperatures.     

Temporal patterns of benthic community development in an Arctic fjord (Kongsfjorden, Svalbard): results of a 24-year manipulation study

We investigated temporal patterns of recolonisation and disturbance in a benthic hard bottom community in high-arctic Kongsfjorden from 1980 to 2003 through annual photographic surveys. A manipulative sampling design was applied, where half of the study area (treatment areas) was cleared at the beginning of the study. Twenty-three different taxa and groups of benthic epifauna were found in the photographs. The benthic community structures of treatments and controls converged within the first decade, but significant differences prevailed until ≤13 years after the start of the study. We could distinguish between three different time intervals with increased inter-annual changes. While the observed differences during the first two intervals could be attributed to recolonisation and succession, the changes in interval 3 were mostly due to increased external forcing and characterised by low inter-group and high inter-annual differences. During this interval, brown algae (mainly Desmarestia) and the sea urchin Strongylocentrotus droebachiensis emerged in high densities, while sea anemone populations declined. Different recolonisation patterns for individual species were related to life span, rate of maturity, predators and larval settlement. We could not find a climax stage in the succession for the benthic community at Kvadehuken, presumably due to the constant level of disturbances at the site.     

Free-living nematodes and macrobenthos in a high-latitude glacial fjord

Kongsfjord is an open glacial fjord on the west coast of Svalbard, where the influence of the West Spitzbergen current ameliorates the effects of high latitude (79°N). The fjord is heavily influenced by glacial discharges of meltwater, ice and till, and related environmental gradients in sediments from the glaciers to the open sea include sediment deposition, organic content and disturbance. Other factors, such as the formation and break up of sea ice, also affect benthic communities. In this study spatial patterns in nematode and macrofaunal communities, in samples collected using box-corers and van Veen grabs during a cruise in September 1997, are described, compared and contrasted. Non-parametric multivariate analyses demonstrate that there were clear differences in community structure between stations in both macrofaunal and nematode assemblages. At stations where macrofauna were sampled using both box-cores and grabs there were also significant differences between samples collected by different methods, although there is evidence that these were influenced in part by slight differences in sampling location. Some evidence of disturbance to macrofaunal assemblages in the centre of the fjord is apparent. Macrofaunal community composition varied most closely with a combination of depth and sediment C : N ratio, whereas that of nematodes varied most closely with C : N alone. Proportions of feeding groups of nematodes showed little variation along the fjord. There is no evidence of a specialised nematode assemblage inhabiting the part of the fjord subject to the heaviest deposition of sediment. The taxonomic distinctness of nematodes decreased with increasing distance from the source of disturbance. This is in contrast to studies showing that the taxonomic distinctness of nematodes tends to decrease with increasing anthropogenic stress.     

Comparison of productivity and phytoplankton in a warm (Kongsfjorden) and a cold (Hornsund) Spitsbergen fjord in mid-summer 2002

Kongsfjorden and Hornsund are two glacial fjords without sills on the West Spitsbergen coast. Both sites are under the influence of relatively warm Atlantic-derived water, although Hornsund is more influenced by cold water from the Barents Sea. In this study, we compared the impacts of cold Arctic and warmer Atlantic waters on the pelagic ecosystems of Kongsfjorden and Hornsund. Both fjords were strongly influenced by Atlantic-derived waters during summer (2002). Diatoms were the most substantial contributors to phytoplankton biomass, especially in outer basins of both fjords, whereas the second most important contributors were autotrophic dinoflagellates in Kongsfjorden and nanoflagellates in Hornsund. Total phytoplankton biomass was highest in Hornsund. Primary production rates were an order of magnitude lower in Kongsfjorden than in Hornsund, and increased from inner to outer fjord (from 2.47 to 4.48 mg C m⁻² h⁻¹ in Kongsfjorden and from 14.00 to 86.65 mg C m⁻² h⁻¹ in Hornsund). Chlorophyll-a concentration was also substantially lower in Kongsfjorden. Zooplankton was dominated by omnivorous species in Kongsfjorden and herbivorous in Hornsund. Observed differences between the fjords may originate from (1) advection of different waters into the fjords; (2) differences in freshwater runoff and turbidity, and (3) timing of the phytoplankton bloom. Climate warming will likely increase the Atlantic water influence, and result in reduced production of diatoms and increase in flagellates.     

Microphytobenthos of Arctic Kongsfjorden (Svalbard, Norway): biomass and potential primary production along the shore line

During summer 2007, Arctic microphytobenthic potential primary production was measured at several stations around the coastline of Kongsfjorden (Svalbard, Norway) at ≤5 m water depth and at two stations at five different water depths (5, 10, 15, 20, 30 m). Oxygen planar optode sensor spots were used ex situ to determine oxygen exchange in the overlying water of intact sediment cores under controlled light (ca. 100 μmol photons m⁻² s⁻¹) and temperature (2–4°C) conditions. Patches of microalgae (mainly diatoms) covering sandy sediments at water depths down to 30 m showed high biomass of up to 317 mg chl a m⁻². In spite of increasing water depth, no significant trend in “photoautotrophic active biomass” (chl a, ratio living/dead cells, cell sizes) and, thus, in primary production was measured at both stations. All sites from ≤5 to 30 m water depth exhibited variable rates of net production from −19 to +40 mg O₂ m⁻² h⁻¹ (−168 to +360 mg C m⁻² day⁻¹) and gross production of about 2–62 mg O₂ m⁻² h⁻¹ (17–554 mg C m⁻² day⁻¹), which is comparable to other polar as well as temperate regions. No relation between photoautotrophic biomass and gross/net production values was found. Microphytobenthos demonstrated significant rates of primary production that is comparable to pelagic production of Kongsfjorden and, hence, emphasised the importance as C source for the zoobenthos.     

Spatial and temporal distribution of tintinnid (Ciliophora: Tintinnida) communities in Kongsfjorden, Svalbard (Arctic), during summer

Information of tintinnid community, as an important component of plankton, was limited in Kongsfjorden, Svalbard (Arctic), which is an important Arctic monitoring site for global change. In this paper, we studied the species composition, spatial, and vertical distribution of tintinnids in Kongsfjorden in July 2012. Water samples for tintinnid study were taken in different depths at eight grid stations in the fjord and time series (5–23 July) at one station at the pier (St. C). Eight species (morphotypes) were found: Acanthostomella norvegica, Leprotintinnus pellucidus, Parafavella edentata, Parafavella gigantea, Ptychocylis obtusa, Stenosemella spp., Tintinnopsis parvula, and Tintinnopsis spp. Total tintinnid abundance and biomass ranged from undetectable (<1 ind L^?1) to 2,435 ind L^?1 and 0–6.33 μg C L^?1, respectively. Cluster analysis of the tintinnid community in the grid stations and St. C showed that tintinnid community was uniform throughout the fjord. Four species (morphotypes) showed distinct vertical distributions: T. parvula occurred throughout the water column but showed a peak at the surface; Tintinnopsis spp. occurred only in the upper 30 m; A. norvegica occurred in low abundance throughout the water column; and Stenosemella spp. was not detected in surface waters. There was variation in abundance of different species in St. C in the 18-day period. However, the tintinnid community did not change according to cluster analysis. These results are helpful in understanding the distribution of other plankton taxon and in long-term monitoring of the Kongsfjorden marine ecosystem.     

Feeding of <Emphasis Type="Italic">Themisto libellula</Emphasis> (Amphipoda Crustacea) on natural copepods assemblages in an Arctic fjord (Kongsfjorden,Svalbard)

Ingestion rates and selectivity of the Arctic pelagic amphipod Themisto libellula were studied experimentally in Kongsfjorden (Svalbard, 78°N) during the summer period. Feeding incubations were conducted on naturally occurring copepod communities at different concentrations ranging from 25 to 250 preys L⁻¹. The ingestion rates increased with food availability from 1.3 to 17.7 preys ind⁻¹ day⁻¹, which corresponded to 0.3–11% of body carbon day⁻¹. Despite the high prey concentration used in the experiments the satiation level was not reached. We suggested that T. libellula is able to take the maximum benefit from dense patches of preys, which represent a good adaptation to the high variability in food supply characteristic of polar environment. Copepodids stage III of Calanus spp. appeared to be the preferred preys of T. libellula. Smaller copepods such as Oithona similis and Pseudocalanus spp., were also selected but only when their relative abundance exceeded 25% of the total prey available. The potential predation impact of T. libellula is discussed in relation to the mesozooplankton small-scale patchiness and predator abundance.     

Spring bloom dynamics in Kongsfjorden,Svalbard: nutrients,phytoplankton, protozoans and primary production

The marine ecosystem in Kongsfjorden (79°N), a glacial fjord in Svalbard, is to a large extent well known with regard to hydrography, mesozooplankton and higher trophic levels. Research on primary production and lower trophic levels is still scare and especially investigations from winter and spring periods. The spring bloom dynamics in Kongsfjorden were investigated in 2002. The development in nutrient conditions, phytoplankton, protozoans and primary production were followed from 15 April until 22 May. The winter/spring in 2002 was categorized as a cold year with sea ice cover and water masses dominated by local winter-cooled water. The spring bloom started around 18 April and lasted until the middle of May. The bloom probably peaked in late April, but break-up of sea ice made it impossible to sample frequently in this period. Diatoms dominated the phytoplankton assemblage. We estimated the total primary production during the spring bloom in 2002 to range 27–35 g C m⁻². There was a mismatch situation between the mesozooplankton and the phytoplankton spring bloom in 2002.     

Life histories of the copepods Pseudocalanus minutus, P. acuspes (Calanoida) and Oithona similis (Cyclopoida) in the Arctic Kongsfjorden (Svalbard)

The year-round variation in abundance and stage-specific (vertical) distribution of Pseudocalanus minutus and Oithona similis was studied in the Arctic Kongsfjorden, Svalbard. Maxima of vertically integrated abundance were found in November with 111,297 ind m⁻² for P. minutus and 704,633 ind m⁻² for O. similis. Minimum abundances comprised 1,088 ind m⁻² and 4,483 ind m⁻² in June for P. minutus and O. similis, respectively. The congener P. acuspes only occurred in low numbers (15–213 ind m⁻²), and successful reproduction was debatable. Reproduction of P. minutus took place in May/June, and stage distribution revealed a 1-year life cycle with copepodids CIII, CIV, and CV as the overwintering stages. Oithona similis exhibited two main reproductive peaks in June and August/September, respectively. Moreover, it reproduced more or less continuously throughout the whole year with all stages occurring during the entire sampling period, suggesting two generations per year. Both species migrated towards greater depth in November, but O. similis preferred to stay longer in the upper 100 m as compared to Pseudocalanus. The reproduction of the two species in Kongsfjorden seemed to be linked to phytoplankton dynamics.     

Soft bottom species richness and diversity as a function of depth and iceberg scour in Arctic glacial Kongsfjorden (Svalbard)

Macrozoobenthic soft-sediment communities of central Arctic Kongsfjorden inhabiting six depth zones between 5 and 30 m were sampled using SCUBA-diving during June–August 2003 and analysed comparatively. About 63 taxa were found, nine of which had not been reported for Kongsfjorden and four for Svalbard. Suspension feeding or surface and sub-surface detritivorous polychaetes and deposit-feeding amphipods were dominant. Only 11 of the 63 taxa (45 species and additional 18 families not further identified) inhabited the complete depth range. Biomass ranged from 3.5 to 25.0 g ash free dry mass m⁻² and mean Shannon diversity (Log e) was 2.06. Similarity clustering from abundance and biomass data showed a significant difference between the shallow station (5 m) and the rest. The latter formed two sub-groups (10–20 and 25–30 m). Depth is irrevocably correlated with ice-scouring. Thus the differences in diversity together with the predicted iceberg scour intensity support the ‘intermediate disturbance hypothesis’ indicating that habitats impacted by moderate iceberg scouring enable higher diversity. In contrast, biotopes frequently affected only host pioneer communities, while mature, less diverse assemblages dominate depths of low impact.     

Observations on diatoms inhabiting natural and artificial substrates in Kongsfjorden,Svalbard, the Arctic

Polar Biology - The most dramatic effects of global climate change are predicted for the Arctic, and there is a raising concern about the lack of baseline information on microalgal biodiversity....     

The distribution of picoplankton and nanoplankton in Kongsfjorden,Svalbard during late summer 2006

Abundance and biomass of pico- (<2 μm) and nanoplankton (2–20 μm) were investigated in relation to hydrography in Kongsfjorden, Svalbard (79°N, 12°E) during late summer 2006. Autotrophic and heterotrophic picoplankton abundance ranged from 0.1 × 10⁶ to 35.2 × 10⁶ cells L⁻¹ and from 0.4 × 10⁶ to 20.3 × 10⁶ cells L⁻¹, respectively. The highest number of bacteria in the entire water column was recorded at station 2 at 10 m (22.3 × 10⁸ cells L⁻¹); the lowest concentration was observed at station 1 (6.0 × 10⁸ cells L⁻¹). The abundance of autotrophic and heterotrophic nanoplankton varied from 0.4 × 10⁵ cells L⁻¹ to 46 × 10⁵ cells L⁻¹ and from 0.3 × 10⁶ to 9.1 × 10⁶ cells L⁻¹, respectively. Our results demonstrated that heterotrophic nanoflagellates and bacteria in Kongsfjorden microbial community were relatively important. The structure of plankton communities integrated with environmental variables could act as indicators of the variability of the inflow of Atlantic Water into Kongsfjorden.     

Microbial Assemblages in Soil Microbial Succession After Glacial Retreat in Svalbard (High Arctic)

Microbial community composition (cyanobacteria and eukaryotic microalgae abundance and diversity, bacterial abundance, and soil respiration) was studied in subglacial and periglacial habitats on five glaciers near Ny-Alesund, Svalbard (79 degrees N). Soil microbial communities from nonvegetated sites (subglacial, recently deglaciated, and cryoconite sediments) and sites with plant cover (deglaciated some hundreds of years ago) were analyzed. Physicochemical analyses (pH, texture, water content, organic matter, total C and N content) were also performed on the samples. In total, 57 taxa of 23 genera of cyanobacteriaand algae were identified. Algae from the class Chlorophyceae (25 species) and cyanobacteria (23 species) were richest in biodiversity. The numbers of identified species in single habitat types were 23 in subglacial, 39 inbarren, 22 in cryoconite, and 24 in vegetated soils. The highest cyanobacterial and algal biovolume and cell numbers, respectively, were present in cryoconite (13x10(4) microm3 mg-1 soil and 508 cells per mg of soil), followed by barren (5.7x10(4) and 188), vegetated (2.6x10(4) and 120), and subglacial (0.1x10(4) and 5) soils. Cyanobacteria prevailed in all soil samples. Algae (mainly green algae) were present only as accessory organisms. The density of bacteria showed a slightly different trend to that of the cyanobacterial and algal assemblages. The highest number of bacteria was present in vegetated (mean: 13,722x10(8) cells per mg of soil dry wt.), followed by cryoconite (3802x10(8)), barren (654x10(8)), and subglacial (78x10(8)) soils. Response of cyanobacteria and algae to physical parameters showed that soil texture and water content are important for biomass development. In addition, it is shown that nitrogen and water content are the main factors affecting bacterial abundance and overall soil respiration. Redundancy analysis (RDA) with forward selection was used to create a model explaining variability in cyanobacterial, algal, and bacterial abundance. Cryoconites accounted for most of the variation in cyanobacteria and algae biovolume, followed by barren soils. Oscillatoriales, desmids, and green coccoid algae preferred cryoconites, whereas Nostocales and Chroococcales occurred mostly in barren soils. From the data obtained, it is evident that of the studied habitats cryoconite sediments are the most suitable ones for the development of microbial assemblages. Although subglacial sediments do not provide as good conditions as cryoconites, they support the survival of microbial communities. Both mentioned habitats are potential sources for the microbial recolonization of freshly deglaciated soil after the glacier retreat.     

Microbial community dynamics in a seasonally anoxic fjord: Saanich Inlet, British Columbia

Dissolved oxygen concentration plays a major role in shaping biotic interactions and nutrient flows within marine ecosystems. Throughout the global ocean, regions of low dissolved oxygen concentration (hypoxia) are a common and expanding feature of the water column, with major feedback on productivity and greenhouse gas cycling. To better understand microbial diversity underlying biogeochemical transformations within oxygen-deficient oceanic waters, we monitored and quantified bacterial and archaeal community dynamics in relation to dissolved gases and nutrients during a seasonal stratification and deep water renewal cycle in Saanich Inlet, British Columbia, a seasonally anoxic fjord. A number of microbial groups partitioned within oxygen-deficient waters including Nitrospina and SAR324 affiliated with the δ- proteobacteria , SAR406 and γ- proteobacteria related to thiotrophic gill symbionts of deep-sea clams and mussels. Microbial diversity was highest within the hypoxic transition zone decreasing dramatically within anoxic basin waters and temporal patterns of niche partitioning were observed along defined gradients of oxygen and phosphate. These results provide a robust comparative phylogenetic framework for inferring systems metabolism of nitrogen, carbon and sulfur cycling within oxygen-deficient oceanic waters and establish Saanich Inlet as a tractable model for studying the response of microbial communities to changing levels of water column hypoxia.     

Late-Holocene succession of dinoflagellates in an Antarctic fjord using a multi-proxy approach: paleoenvironmental genomics, lipid biomarkers and palynomorphs

Recent work has shown that paleoenvironmental genomics, i.e. the application of genomic tools to analyze preserved DNA in sedimentary records, is a promising approach to reconstruct the diversity of past planktonic communities. This provides information about past ecological and environmental changes. A major advantage of this approach is that individual species, including those that did not leave other characteristic markers, can be identified. In this study, we determined which dinoflagellate marker (i.e. 18S rDNA, dinosterol or dinocysts) provided the most detailed information about the late-Holocene succession of dinoflagellates in an Antarctic Fjord (Ellis Fjord, Vestfold Hills). The preserved rDNA revealed two intervals in the 2750-year-old sediment record. The dinoflagellate diversity was the highest until ∼1850 cal yr bp and included phylotypes related to known dinosterol producers. A lower concentration of dinosterol in sediments <1850 cal yr bp coincided with a community shift towards a predominance of the autotrophic sea-ice dinoflagellate Polarella glacialis , which is not a source of dinosterol. Remarkably, cultures of P. glacialis are known to produce other diagnostic sterols, but these were not recovered here. In addition, conspicuous resting cysts of P. glacialis were not preserved in the analyzed sediments. Overall, dinocysts were rare and the paleoenvironmental genomics approach revealed the highest diversity of dinoflagellates in Ellis Fjord, and was the only approach that recorded a shift in dinoflagellate composition at ∼1850 cal yr bp indicative of a colder climate with more extensive ice cover – this timing coincides with a period of changing climate reported for this region.