Ecology

For millions of years the Southern Ocean has been one of the most thermally constant of Earth’s environments, but is now undergoing multiple, complex, interacting physical changes1. This region includes a major centre of considerable, recent warming in the shallows, and this is forecast to be sustained1. It will likely drive varied and considerable biological change, which remains little investigated in situ. Most existing knowledge is for responses of individual species, in isolation2, but cumulative responses at assemblage and community levels, though poorly studied, will likely have greater consequences3. There is now a wide literature on indirect impacts of warming on biota (e.g., snow and ice retreat, freshening, and sedimentation from glaciers, among others4,5,6,7) but few field studies on specifically direct thermal effects. To date, warming impacts have been predicted to change species success4,8 and the first polar assemblage level data demonstrated increased growth9. However, this only occurred in a few species at moderately increased temperature. If sessile animals become larger (owing to increased growth) this is more likely to make space a limiting resource and increase the incidence, and importance, of spatial competition.
In the current study, we investigated how in situ warming impacts physical ‘fighting’ for space (so called contest competitive interactions), between species in assemblages. This is where the boundaries of colonies/individuals meet others, which leads to either a cessation and redirection of growth by both competitors (a tie or draw) or overgrowth of one (a loser) by the other (winner). To our knowledge, the impact of climate-forcing on spatial competition has not been considered in polar seas. Yet, for species unchanging in growth performance (and even some of those which do increase growth) competitive encounter frequency might be easier to detect and therefore be an earlier measure of response to environmental change. This is because snapshots of the extent of spatial competition can be obtained using still photographs either by SCUBA or Remotely Operated Vehicles. In comparison, growth has to be monitored over long periods of time and compared within species across years. Bryozoans and other encrusting cryptofauna have proved strong model taxa for investigating spatial competition and artificial substrata, in the form of settlement panels, are good experimental surfaces to investigate such encounter dynamics7,9,10,11,12,13. To investigate responses to global physical change, the next step is to be able to manipulate one aspect of artificial substrata in situ whilst not altering any others.
Heat controllable settlement panels9 allow exploration of predicted mid or end-century shallow sea temperature levels in situ, which is enhanced by including several warming regimes (year-round and summer only) and levels (0, +1, and +2 °C). Different levels of warming treatments aid prediction of future responses, but are also useful because warming is geographically highly variable, even around the West Antarctic Peninsula (WAP). Using this apparatus, Ashton et al.9 found that growth (and per cent cover change) responses varied considerably between warming levels in the six most common recruit species9. In particular, a 1 °C temperature rise led to one bryozoan species, Fenestrulina rugula, monopolising most space (~60%), despite being a weak spatial competitor (it is out competed and overgrown in physical encounters with most other species it meets)7. What does this mean for assemblage dynamics and intra- and interspecific competition for space? Other factors being equal, more-occupied space should increase the incidence and importance of spatial competition. Thus Ashton et al.’s9 findings led us to hypothesise that (1) competitive encounters per unit area, and the probability of a given individual, or colony, being involved in spatial competition would increase with moderate (1 °C) warming, but less so, if at all, with 2 °C warming. The reasoning behind increased competition with 1 °C but not 2 °C warming was that Ashton et al.9 found increased growth with 1 °C but not 2 °C warming—making it more likely that the boundaries of species should come into contact. Our hypothesis (2) was that the spatial dominance of F. rugula would lead to more competition involving this species and fewer interactions involving other species (less complexity). Typically, investigation of the impacts of treatments such as warming, compares changes in species composition across treatments14. We, however, compared competitive pairings between species (across treatments). We predicted that the similarity of competitor pairings would provide a stronger response signal to warming than mere species composition, as the number of potential competitive interactions between species is the factorial of presence/absence.
We found that panels that were warmed to 1 °C above ambient (either throughout the year or just summer only) increased the probability of spatial competition among encrusting nearshore Antarctic fauna. This level of warming also increased the density and complexity of spatial competitive interactions. In contrast, warming to 2 °C above ambient increased variance (rather than mean) in the probability and density of competition, but competition did not significantly differ from ambient (control) levels. Thus biological responses, in terms of spatial competition, to warming change alter with both level and (seasonal) timing of warming. We found evidence that changes in competitive structure may be detected before changes in species composition, thus panels may be a powerful tool for monitoring early community responses to stressors such as climate change. More

Soil freeze–thaw characteristics in different landscapes
In this study, the FT characteristics exhibited certain differences among the three landscapes. AS land had the largest frost depth and the longest freeze duration, followed by LT grassland, and then farmland (Fig. 3). These differences may be attributed to the differences in dependent soil physical properties, soil surface covers and initial soil water contents of the landscape17,18. The denser soil structure of the AS land quickened the more spread of the cold from the upper soils to the lower soils than LT land and farmland during freezing. Furthermore, AS land had the lowest snow cover and no residue, which promotes heat transport at the soil–atmosphere interface19. Therefore, the soil temperature decreased rapidly with the air temperature, resulting in a significant increase in the frost depth and freezing rate of AS land. These was in accordance with the conclusions of Iwata et al. (2010)20, who clearly demonstrated that the reduction in a snow cover deposition could cause a dramatic increase in the frost depth, as well as those of Fu et al. (2018)2 who reported that the decrease in snow cover strengthened the actions of soil temperature on freezing front. In addition, the higher SWC in the LT grassland (0.21 cm3/cm3) and AS land (0.32 cm3/cm3) would slow down soil temperature changes21, because more heat release from the soil when soil freezes, or more heat is needed when soil thaws. Consequently, the wetter conditions in the LT grassland and AS land would postpone the freeze–thaw processes, as indicated by other researches17. Similar results were obtained in the study of Yi et al. (2014) on soil freeze–thaw characteristics of different landscapes in the Heihe River Basin, Gansu, China22.
Influence of freeze–thaw process on the soil water content (SWC)
In this study, the freezing process led to an upward enrichment in soil water within different landscapes in the study area (Fig. 5). One possible reason for this phenomenon was that the soil temperature gradient drove the upward flux of water towards the frozen layers, and water finally accumulated in the frozen layers23,24. However, during the spring thawing, soil water in the upper soil layer and the deeper soil layers decreased and increased, respectively (Table 2). This was because soils thawed bi–directionally, the water above the frozen layer moved upwards and ultimately intensively evaporated away, whereas the water below the frozen infiltrated into the deeper layers. These results agreed with the findings of Zhang and Wang (2001)12, Wang et al. (2009)14 and Bing et al. (2015)4. Furthermore, this freeze-induced soil water enrichment in the frozen zone can facilitate to soil water conservation by reducing evaporation and seepage, thus maintaining a high water content1,3,22, which can be helpful to farming and plant germination in the following spring. However, in this study there were obvious differences in profiled water redistributions upon freezing in different landscapes. The SWC in the AS land at a depth of 0–5 cm decreased during freezing and increased during thawing. This may be attributed to fierce regional winds, no plant residue on the surface, lack of snow cover and frequent heat exchanges between the surface soil and air during winter in the study area. Furthermore, because of the higher initial moisture content, the greater frost depth and intensity in the AS land, the water in the frozen layer continuously replenished the surface soil, and even produced internal runoff during spring thawing, despite an intensification of evaporation. This occurrence thereby increased the surface SWC, which proved the conclusions of Iwata et al. (2010)20, Nagare et al. (2012)25 and Wu et al. (2019)21. In addition, the profiled soil water migration rates in the farmland, LT grassland and AS land were substantially different during the FT processes. It was the highest in the LT grassland, whereas the lowest in the farmland. This is because the LT grassland was less salinised than the AS land and surface soil of the former had the highest organic matter content (0–25 cm, 2.50%) (Table 1), which resulted in a good soil structure that facilitated a better movement of soil water compared to the AS land. Therefore, more water migrated in the LT grassland than that in AS land during the FT processes. However, for the farmland, the lower initial moisture content (0.11 cm3/cm3) and soil compaction caused by farming activity over many years inhibited soil water migration. Furthermore, the FT affect soil physical properties, such as soil structure, soil cracking, soil thermal properties and heat flux, which were also an important reason explaining the difference of water migration in soil profiles of different landscapes. For example, frozen soils are divided into layered and reticulate structures by ice, resulting in a higher soil water permeability coefficient; thus, water can be quickly discharged from cracking during soil thawing23,24,26. Additionally, the groundwater table declined during freezing and rose during thawing, thus suggesting that a mutual transport occurred between the soil water and groundwater in deeper soil.
Influence of freeze-thaw process on the soil salinity and alkalinity
According to the data obtained from this study, the profiled soil salinity distributions were characterised by an accumulation of soil salt towards the frozen layer with soil water during the freezing. Consequently, the salt content obviously increased throughout the entire frozen layer, which experimentally verified the findings of Stahli and Stadler (1997)27 and Wang et al. (2009)14. A possible explanation for these results was that the soil salt along with water in the deeper unfrozen layer and groundwater both moved upward towards the frozen layer because of temperature gradient between the frozen and unfrozen layer. In fact, the freeze-induced soil salt migration was exceedingly complex and could not be solely attributed to the temperature gradient. Instead, this dynamic represented the integrated result of many factors, such as land use, initial soil water, soil salinisation, soil temperature, groundwater level. Furthermore, our results also showed that the salinised ratio in the upper soil profile was substantially higher than that in the deeper soil profile during freezing. This behavior may be attributed to the liquid water occurring in the frost layer and temperature gradient forcing the liquid water to carry the salt upwards. Some researchers have observed that it is possible for liquid water to exist as membrane water, wherein its thickness gradually becomes thinner from the deep soil to the upper soil, thereby causing salt to move upwards along with water28.
Furthermore, our study showed that the salification layer moved upwards and expanded, and the surface soil exhibited the significant salt accumulations in the LT grassland and AS land during spring thawing. This appears to experimentally explain the phenomenon of topsoil salt explosive increases that resemble an ‘eruption’ during spring thawing12,14. The results were in accordance with Han et al. (2010)29, who pointed out that the surface soil salinity increased rapidly in spring because of strong evaporation, more FT cycles and longer freezing durations. This is because the quantity of evaporation is five times higher than the amount of rainfall in the western Songnen Plain; thus, this intense soil evaporation induces a redistribution of the accumulated salt in the frozen layer, and transports a large quantity of salt upwards to the surface. More importantly, these findings revealed that FT processes were mainly responsible for the obvious soil salinisation in our study, which aligns with the analysis of Bing et al. (2015)4, who determined that FT processes are the main driving force of soil water and salt movement and are responsible for soil salinisation during the spring in cold and arid regions. However, these results slightly contradicted the findings of Wang. (1993)8, who noted that the surface soil salt ‘eruption’ in spring was controlled by ‘the critical depth of ground water’ rather than FT actions, yet which contradicted the local practical condition of using phreatic water as the only water source influencing the soil salinisation in this study area. The water exchanges were blocked by the frozen layers between the soil surface and underground water; therefore, soil salinisation during the spring was not related to groundwater5,12. However, their findings slightly contradicted with the results observed in our study that suggested that bi-directional thawing also possibly caused the salt under the freezing layer to accumulate in the middle soil profile. This was because the thawed water carrying salt infiltrated towards the deeper soil into the groundwater, which implied that the profiled salt distributions had a relationship with the groundwater. Moreover, the results from our study also revealed that landscapes affected the salification of the soil surface and the desalinisation of the subsurface soil, with the trend being AS land  > LT grassland  > farmland. This discrepancy may be interpreted by four aspects. Firstly, the initial soil salt content of AS land was 19.3 times higher than that of the LT grassland, consequently causing a higher accumulation ratio of soil salt, as indicated by Wan et al. (2019)6, who observed that the salt crystallisation increased the salt migration during the freezing process, and that salt migration was positively correlated with the salt content. Secondly, LT grassland had a larger coverage area and a higher litter amount reduced the quantity of ground evaporation and avoided surface salt accumulation. Thirdly, the improved soil structure of the LT grassland, with its larger root system and higher organic content was beneficial to increase infiltration and promote the downward movement of salt from the upper soil layers30. Finally, the soil of AS land started to thaw earliest because of its lowest freezing point resulted from its highest salt content at corresponding depths, which accelerated the consumption of soil water by evaporation. Additionally, the salinised ratio of the farmland was weaker than that of AS land and LT grassland, which was attributed to its lower initial salt content (64.73 mg/kg), initial water content (0.11 cm3/cm3), lower frost depth and intensity in farmland21,25.
The soil SAR and ESP have been recommended the sensitive indicators of soil alkalisation for a soil alkalisation assessment in the Songnen grassland31. In this study, FT cycles induced the increases in the SAR and ESP in the upper soil layers for all three landscapes (Fig. 8 and Table 5), which implied that the FT processes not only contributed to soil salinisation but also to soil alkalisation. As indicated in Table 6, the soil salinisation within the frozen soil layer shows a significantly positive correlation with the soil alkalisation, which was similar to the findings observed by Yu et al. (2018)31. This occurrence may be mainly attributed to the fact that the salts migrating towards the frozen layer had a prevalence of NaHCO3 and Na2CO313. Wang et al. (2009)14 also reported that soil FT were one of the most important causes of soil salinisation and alkalisation in the western Songnen Plain and further proved that the influence of groundwater could not be ignored. Groundwater in the study area comprises a weak mineralised water of NaHCO3 type, where Na+, CO32− and HCO3−contents can be up to 853.55 mg/L, the salinity is as high as 1.21 g/L and the SAR can reach 88.65. Accordingly, groundwater migrating upwards due to soil freezing induced soil both salinisation and alkalisation, which accelerated soil degradation13. Conversely, some studies have reported that FT cycles had no significant effects on soil CEC or exchangeable Ca2+ and Mg2+ but significantly decreased the exchangeable K+32 that indicated that FT cycles can possibly reduce the soil alkalisation, which was different from our results. The cause of this difference is not clear that is the integrated result of various factors, such as soil types, vegetation types, microbial activity, ground level, and so on. The experimental conditions in this study were different from Hinman (1970)32 in which soils were fumigated and sterilize without groundwater exchange and vegetation. Furthermore, the influences of soil FT on soil alkalisation varied with soil types and soil depths. In this study, the FT-induced soil alkalisation in the AS land was more pronounced than that in the farmland and LT grassland (Table 4). This may be a comprehensive consequence of land use, groundwater levels, topography, soil-human activities, and so on.
Hypothetical mechanism of freeze–thaw influences on soil salinity and alkalinity
The FT process caused variations in profiled soil water and salt distributions12, yet the internal mechanism still stayed at an exploration stage. During freezing, the potential head gradients between the frozen and unfrozen zones created by the temperature gradient exerted a certain driving force behind an upward flux of water towards the upper zones3,25. Salt, using water as the carrier, also rose towards the upper layer and was finally enriched in the frozen layer, which thereby increased the salinity. The enriched salts in the frozen layer were driven by intense surface evaporation to move towards soil surface and then accumulated, which been characterized as ‘eruptions’ during the spring. Therefore, the intensity of freezing during the winter and the strength of surface evaporation during the spring determined the extent of surface soil salinity-alkalinity.
Moreover, there was sufficient evidence to prove that soil salt migration was related to land use and vegetation. Soil colloidal particles were dispersed most widely in the AS land because of the highest Na+ contents, and most dispersed fine clay particles moved downward through the subsoil to act as a dense water barrier. Additionally, the poor soil structure of the AS land directly slowed down the soil water and salt migration rate on the unfrozen layer and the upward migration of groundwater toward the frozen layer. The relatively superior soil structure in the LT grassland promoted soil water and salt removal. Furthermore, various types of vegetation have differentially improved the soil physical, chemical and biological properties31,33, and these differential reactions may contribute to the response to FT actions. The vegetation coverages and the sizes of their root networks influenced evapotranspiration and soil water percolation, which consequently further influenced the upward water and salt migrations during FT. Maize vegetation has been found to have a greater impact than grass vegetation on repairing saline-sodic soils in the study area, and were both found to have superior soil physical properties compared to non-vegetated AS land28. Therefore, the FT processes, as associated with different landscapes and vegetation coverage, controlled soil water and salt migration during the winter and spring, which were mainly responsible for the variations in the soil salinity and alkalinity in the study area. More

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Monocultures differ significantly in their ability to colonize the C. elegans intestine
To investigate community assembly in the gut of C. elegans, we fed germ-free synchronized adult worms with different bacterial species, in monoculture or in mixture, over 4 days in a well-mixed rich liquid medium (Methods, Fig. S1A). The majority of worms survived the 4-day period of feeding and colonization, after which we allowed live worms to feed briefly on heat-killed E. coli OP50 to remove transient colonizers [35, 45]. We then cleaned the surface of the worms with consecutive washes, and measured the intestinal bacterial densities by grinding batches of worms, plating, and counting colony forming units (CFU, Fig. S1B) with distinct morphologies [46]. The supernatant of each sample was plated to verify that CFU counts came from the worm digestions instead of the background media (Methods). This protocol allowed us to construct and quantify simple microbiotas in C. elegans.
We began by feeding C. elegans in monoculture to quantify the ability of a range of bacterial species to colonize and grow in the worm intestine. As a starting point, we first utilized an immunocompromised C. elegans mutant (AU37) and a set of eleven non-native bacterial species (Fig. 1B), representing the phyla Firmicutes (gram-positive) and Proteobacteria (gram-negative). We found that all bacterial species colonize (i.e., accumulate with or without active growth) the C. elegans intestine, with mean population sizes (Figs. 1C, S1C) ranging from 200 CFU per worm in the case of B. cereus, up to 20,000 CFU/worm in the case of S. marcescens. Our three Firmicutes reach low population sizes in the worm gut and low carrying capacities in the liquid media (Fig. S1E), but the carrying capacities in the liquid media do not explain the variation in monoculture colonization (Fig. S1F, G). These results indicate that different non-native bacterial species have a wide range of abilities to colonize the C. elegans intestine in monoculture.
Composition of two-species microbiotas are influenced by competitive and hierarchical bacterial interspecies interactions
To assess the compositional trends of the C. elegans microbiota, we constructed the simplest intestinal communities in this worm by feeding it with all possible two-species mixtures from the same eleven non-native bacteria as before (55 pairs, Figs. 2A, S2A). We fed worms with both bacteria present at similar concentrations (~107 CFU/mL, Methods) to normalize the rate of ingestion. We found that a majority (41 out of 55, ~75%) of pairs displayed coexistence, with both species present above the detection limit of 2%, whereas the remainder (14 out of 55, ~25%) led to competitive exclusion of a species (Figs. 2B, S2B). These results show that bacteria with no prior conditioning for the C. elegans gut commonly reach coexistence in two-species microbiotas.
Fig. 2: Monoculture colonization of the worm intestine often fails to predict composition of two-species microbiotas.

A LEFT panels: Fractional abundances of 55 co-culture experiments in C. elegans intestine (AU37); error bars are the s.e.m. of 2–8 biological replicates (Fig. S2). Bacterial species are ordered from left to right by their mean fraction across all co-cultures. RIGHT panels: Null expectation for the fractional abundances based on a noninteracting model where each bacterial species reaches its population size in monoculture; error bars are the s.e.m. from bootstrapping over the monoculture data. * and ** represent a statistically significant difference between the two panels at p values of 0.05 and 0.01, respectively (Welch’s T test). B Coexistence of two species is more common than competitive exclusion in the worm intestine. C Low yields in two species microbiotas—relative to monocultures—are indicative of competitive interactions (Fig. S2); error bars on X-axis are the s.e.m. and on Y-axis the s.e.m. from bootstrapping over monoculture and pairwise data simultaneously. D Competitive ability, defined as the mean fractional abundance in co-culture experiments, relates to monoculture population size, but there are significant deviations; error bars on Y-axis are the propagated error from the s.e.m. of the co-culture experiments.

Full size image

The interactions between bacterial species in a microbiota can be classified as positive, negative, or neutral based on the yields of the bacteria relative to their monoculture population sizes. To classify the interactions in our two-species microbiotas, we calculated the relative yield of species “i” with species “j”, RYi|j, as its population size in co-culture, Ni|j, divided by its population size in monoculture, Ni (RYi|j = Ni|j/Ni, see Methods for detailed implementation). We found that most species cannot reach their monoculture population size in co-culture experiments, RY  More

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