What can ecosystems learn? Expanding evolutionary ecology with learning theory.

BACKGROUND: The structure and organisation of ecological interactions within an ecosystem is modified by the evolution and coevolution of the individual species it contains. Understanding how historical conditions have shaped this architecture is vital for understanding system responses to change at scales from the microbial upwards. However, in the absence of a group selection process, the collective behaviours and ecosystem functions exhibited by the whole community cannot be organised or adapted in a Darwinian sense. A long-standing open question thus persists: Are there alternative organising principles that enable us to understand and predict how the coevolution of the component species creates and maintains complex collective behaviours exhibited by the ecosystem as a whole? RESULTS: Here we answer this question by incorporating principles from connectionist learning, a previously unrelated discipline already using well-developed theories on how emergent behaviours arise in simple networks. Specifically, we show conditions where natural selection on ecological interactions is functionally equivalent to a simple type of connectionist learning, 'unsupervised learning', well-known in neural-network models of cognitive systems to produce many non-trivial collective behaviours. Accordingly, we find that a community can self-organise in a well-defined and non-trivial sense without selection at the community level; its organisation can be conditioned by past experience in the same sense as connectionist learning models habituate to stimuli. This conditioning drives the community to form a distributed ecological memory of multiple past states, causing the community to: a) converge to these states from any random initial composition; b) accurately restore historical compositions from small fragments; c) recover a state composition following disturbance; and d) to correctly classify ambiguous initial compositions according to their similarity to learned compositions. We examine how the formation of alternative stable states alters the community's response to changing environmental forcing, and we identify conditions under which the ecosystem exhibits hysteresis with potential for catastrophic regime shifts. CONCLUSIONS: This work highlights the potential of connectionist theory to expand our understanding of evo-eco dynamics and collective ecological behaviours. Within this framework we find that, despite not being a Darwinian unit, ecological communities can behave like connectionist learning systems, creating internal conditions that habituate to past environmental conditions and actively recalling those conditions. REVIEWERS: This article was reviewed by Prof. Ricard V Solé, Universitat Pompeu Fabra, Barcelona and Prof. Rob Knight, University of Colorado, Boulder.

A novel approach to analysing the regimes of temporary streams in relation to their controls on the composition and structure of aquatic biota

Temporary streams are those water courses that undergo the recurrent cessation of flow or the complete drying of their channel. The structure and composition of biological communities in temporary stream reaches are strongly dependent on the temporal changes of the aquatic habitats determined by the hydrological conditions. Therefore, the structural and functional characteristics of aquatic fauna to assess the ecological quality of a temporary stream reach cannot be used without taking into account the controls imposed by the hydrological regime. This paper develops methods for analysing temporary streams' aquatic regimes, based on the definition of six aquatic states that summarize the transient sets of mesohabitats occurring on a given reach at a particular moment, depending on the hydrological conditions: Hyperrheic, Eurheic, Oligorheic, Arheic, Hyporheic and Edaphic. When the hydrological conditions lead to a change in the aquatic state, the structure and composition of the aquatic community changes according to the new set of available habitats. We used the water discharge records from gauging stations or simulations with rainfall-runoff models to infer the temporal patterns of occurrence of these states in the Aquatic States Frequency Graph we developed. The visual analysis of this graph is complemented by the development of two metrics which describe the permanence of flow and the seasonal predictability of zero flow periods. Finally, a classification of temporary streams in four aquatic regimes in terms of their influence over the development of aquatic life is updated from the existing classifications, with stream aquatic regimes defined as Permanent, Temporary-pools, Temporary-dry and Episodic. While aquatic regimes describe the long-term overall variability of the hydrological conditions of the river section and have been used for many years by hydrologists and ecologists, aquatic states describe the availability of mesohabitats in given periods that determine the presence of different biotic assemblages. This novel concept links hydrological and ecological conditions in a unique way. All these methods were implemented with data from eight temporary streams around the Mediterranean within the MIRAGE project. Their application was a precondition to assessing the ecological quality of these streams.

CO2 utilization in the perspective of industrial ecology, an overview

Carbon dioxide emissions from anthropic activities have accumulated in the atmosphere in excess of 800 Gigatons since preindustrial times, and are continuously increasing. Among other strategies, CO2 capture and storage is one option to mitigate the emissions from large point sources. In addition, carbon dioxide extraction from ambient air is assessed to reduce the atmospheric concentration of CO2. Both direct and indirect (through photosynthesis) pathways are possible. Geological sequestration has significant disadvantages (high cost, low public acceptance, long term uncertainty) whereas carbon dioxide recycling (or utilization) is more consistent with the basic principle of industrial ecology, almost closing material cycles. In this article, a series of technologies for CO2 capture and valorization is described as integrated and optimized pathways. This integration increases the environmental and economic benefits of each technology. Depending on the source of carbon dioxide, appropriate capture and valorization processes are evaluated based on material and energy constraints.

Importance of amoebae as a tool to isolate amoeba-resisting microorganisms and for their ecology and evolution: the Chlamydia paradigm.

Free-living amoebae are distributed worldwide and are frequently in contact with humans and animals. As cysts, they can survive in very harsh conditions and resist biocides and most disinfection procedures. Several microorganisms, called amoeba-resisting microorganisms (ARMs), have evolved to survive and multiply within these protozoa. Among them are many important pathogens, such as Legionella and Mycobacteria, and also several newly discovered Chlamydia-related bacteria, such as Parachlamydia acanthamoebae, Estrella lausannensis, Simkania negevensis or Waddlia chondrophila whose pathogenic role towards human or animal is strongly suspected. Amoebae represent an evolutionary crib for their resistant microorganisms since they can exchange genetic material with other ARMs and develop virulence traits that will be further used to infect other professional phagocytes. Moreover, amoebae constitute an ideal tool to isolate strict intracellular microorganisms from complex microbiota, since they will feed on other fast-growing bacteria, such as coliforms potentially present in the investigated samples. The paradigm that ARMs are likely resistant to macrophages, another phagocytic cell, and that they are likely virulent towards humans and animals is only partially true. Indeed, we provide examples of the Chlamydiales order that challenge this assumption and suggest that the ability to multiply in protozoa does not strictly correlate with pathogenicity and that we should rather use the ability to replicate in multiple and diverse eukaryotic cells as an indirect marker of virulence towards mammals. Thus, cell-culture-based microbial culturomics should be used in the future to try to discover new pathogenic bacterial species.

Feeding ecology and movements of the Barolo shearwater Puffinus baroli baroli in the Azores, NE Atlantic

Trophic ecology and movements are critical issues for understanding the role of marine predators in food webs and for facing the challenges of their conservation. Seabird foraging ecology has been increasingly studied, but small elusive species, such as those forming the"little shearwater" complex, remain poorly known. We present the first study on the movements and feeding ecology of the Barolo shearwater Puffinus baroli baroli in a colony from the Azores archipelago (NE Atlantic), combining global location-sensing units, stable isotope analyses of feathers (δ13C and δ15N), stomach flushings and data from maximum depth gauges. During the chick-rearing period, parents visited their nests most nights, foraged mainly south of the colony and fed at lower trophic levels than during the non-breeding period. Squid was the most diverse prey (6 families and at least 10 different taxa), but species composition varied considerably between years. Two squid families, Onychoteuthidae and Argonautidae, and the fish family Phycidae accounted for 82.3% of ingested prey by number. On average, maximum dive depths per foraging trip reached 14.8 m (range: 7.9 to 23.1 m). After the breeding period, birds dispersed offshore in all directions and up to 2500 km from the breeding colony, and fed at higher trophic levels. Overall, our results indicate that the Barolo shearwater is a non-migratory shearwater feeding at the lowest trophic level among Macaronesian seabirds, showing both diurnal and nocturnal activity and feeding deeper in the water column, principally on small schooling squid and fish. These traits contrast with those of 3 other Azorean Procellariiformes (Cory"s shearwater Calonectris diomedea, the Madeiran storm-petrel Oceanodroma castro and Monteiro"s storm-petrel O. monteiroi), indicating ecological segregation within the Azorean seabird community.

Nutritional and feeding ecology in the Cory"s shearwater (Calonectris diomedea).

In birds, parents adjust their feeding behaviour according to breeding duties, which ultimately may lead to seasonal adjustments in nutritional physiology and hematology over the breeding season. Although avian physiology has been widely investigated in captivity, few studies have integrated individual changes in feeding and physiological ecology throughout the breeding season in wild birds. To study relationships between feeding ecology and nutritional ecophysiology in Cory"s shearwater Calonectris diomedea, we weighed and took blood samples from 28 males and 19 females during the pre-laying, egg-laying, incubation, hatching and chick-rearing periods of the breeding season. In addition, we fitted 6 birds with geolocators to track their foraging movements throughout the reproductive period. Thus, we examined individual changes in (1) nutritional condition (biochemistry metabolites); (2) oxygen carrying capacity (hematology); and (3) feeding areas and foraging effort (stable isotopes and foraging movements). Geolocators revealed a latitudinal shift in main feeding areas towards more southern and more neritic waters throughout the breeding season, which is consistent with the steady increase in δ13C signatures in the blood. Geolocators also showed a decrease in foraging effort from egg-laying to hatching, reflecting the activity decrease associated with incubation duties. Plasma metabolites, body mass and oxygen carrying capacity were associated with temporal changes in nutritional state and foraging effort in relation to recovery after migration, egg formation, fasting shifts during incubation and chick provisioning. This study shows that combining physiological and ecological approaches can help us understand the influence of breeding duties on feeding ecology and nutritional physiology in wild birds.

Evolutionary Ecology of Mountain Birch in Subarctic Stress Gradients: Interplay of Biotic and Abiotic Factors in Plant-Plant Interactions and Evolutionary Processes

In nature, variation for example in herbivory, wind exposure, moisture and pollution impact often creates variation in physiological stress and plant productivity. This variation is seldom clear-cut, but rather results in clines of decreasing growth and productivity towards the high-stress end. These clines of unidirectionally changing stress are generally known as ‘stress gradients’. Through its effect on plant performance, stress has the capacity to fundamentally alter the ecological relationships between individuals, and through variation in survival and reproduction it also causes evolutionary change, i.e. local adaptations to stress and eventually speciation. In certain conditions local adaptations to environmental stress have been documented in a matter of just a few generations. In plant-plant interactions, intensities of both negative interactions (competition) and positive ones (facilitation) are expected to vary along stress gradients. The stress-gradient hypothesis (SGH) suggests that net facilitation will be strongest in conditions of high biotic and abiotic stress, while a more recent ‘humpback’ model predicts strongest net facilitation at intermediate levels of stress. Plant interactions on stress gradients, however, are affected by a multitude of confounding factors, making studies of facilitation-related theories challenging. Among these factors are plant ontogeny, spatial scale, and local adaptation to stress. The last of these has very rarely been included in facilitation studies, despite the potential co-occurrence of local adaptations and changes in net facilitation in stress gradients. Current theory would predict both competitive effects and facilitative responses to be weakest in populations locally adapted to withstand high abiotic stress. This thesis is based on six experiments, conducted both in greenhouses and in the field in Russia, Norway and Finland, with mountain birch (Betula pubescens subsp. czerepanovii) as the model species. The aims were to study potential local adaptations in multiple stress gradients (both natural and anthropogenic), changes in plant-plant interactions under conditions of varying stress (as predicted by SGH), potential mechanisms behind intraspecific facilitation, and factors confounding plant-plant facilitation, such as spatiotemporal, ontogenetic, and genetic differences. I found rapid evolutionary adaptations (occurring within a time-span of 60 to 70 years) towards heavy-metal resistance around two copper-nickel smelters, a phenomenon that has resulted in a trade-off of decreased performance in pristine conditions. Heavy-metal-adapted individuals had lowered nickel uptake, indicating a possible mechanism behind the detected resistance. Seedlings adapted to heavy-metal toxicity were not co-resistant to others forms of abiotic stress, but showed co-resistance to biotic stress by being consumed to a lesser extent by insect herbivores. Conversely, populations from conditions of high natural stress (wind, drought etc.) showed no local adaptations, despite much longer evolutionary time scales. Due to decreasing emissions, I was unable to test SGH in the pollution gradients. In natural stress gradients, however, plant performance was in accordance with SGH, with the strongest host-seedling facilitation found at the high-stress sites in two different stress gradients. Factors confounding this pattern included (1) plant size / ontogenetic status, with seedling-seedling interactions being competition dominated and host-seedling interactions potentially switching towards competition with seedling growth, and (2) spatial distance, with competition dominating at very short planting distances, and facilitation being strongest at a distance of circa ¼ benefactor height. I found no evidence for changes in facilitation with respect to the evolutionary histories of plant populations. Despite the support for SGH, it may be that the ‘humpback’ model is more relevant when the main stressor is resource-related, while what I studied were the effects of ‘non-resource’ stressors (i.e. heavy-metal pollution and wind). The results have potential practical applications: the utilisation of locally adapted seedlings and plant facilitation may increase the success of future restoration efforts in industrial barrens as well as in other wind-exposed sites. The findings also have implications with regard to the effects of global change in subarctic environments: the documented potential by mountain birch for rapid evolutionary change, together with the general lack of evolutionary ‘dead ends’, due to not (over)specialising to current natural conditions, increase the chances of this crucial forest-forming tree persisting even under the anticipated climate change.

Consequences of warming and resource quality on the stoichiometry and nutrient cycling of a stream shredder

As a result of climate change, streams are warming and their runoff has been decreasing in most temperate areas. These changes can affect consumers directly by increasing their metabolic rates and modifying their physiology and indirectly by changing the quality of the resources on which organisms depend. In this study, a common stream detritivore (Echinogammarus berilloni Catta) was reared at two temperatures (15 and 20°C) and fed Populus nigra L. leaves that had been conditioned either in an intermittent or permanent reach to evaluate the effects of resource quality and increased temperatures on detritivore performance, stoichiometry and nutrient cycling. The lower quality (i.e., lower protein, soluble carbohydrates and higher C:P and N:P ratios) of leaves conditioned in pools resulted in compensatory feeding and lower nutrient retention capacity by E. berilloni. This effect was especially marked for phosphorus, which was unexpected based on predictions of ecological stoichiometry. When individuals were fed pool-conditioned leaves at warmer temperatures, their growth rates were higher, but consumers exhibited less efficient assimilation and higher mortality. Furthermore, the shifts to lower C:P ratios and higher lipid concentrations in shredder body tissues suggest that structural molecules such as phospholipids are preserved over other energetic C-rich macromolecules such as carbohydrates. These effects on consumer physiology and metabolism were further translated into feces and excreta nutrient ratios. Overall, our results show that the effects of reduced leaf quality on detritivore nutrient retention were more severe at higher temperatures because the shredders were not able to offset their increased metabolism with increased consumption or more efficient digestion when fed pool-conditioned leaves. Consequently, the synergistic effects of impaired food quality and increased temperatures might not only affect the physiology and survival of detritivores but also extend to other trophic compartments through detritivore-mediated nutrient cycling.

Feeding ecology and trophic position of three sympatric demersal chondrichthyans in the Northwestern Mediterranean.

Understanding how marine predators interact is a scientific challenge. In marine ecosystems, segregation in feeding habits has been largely described as a common mechanism to allow the coexistence of several competing marine predators. However, little is known about the feeding ecology of most species of chondrichthyans, which play a pivotal role in the structure of marine food webs worldwide. In this study, we examined the trophic ecology of 3 relatively abundant chondrichthyans coexisting in the Mediterranean Sea: the blackmouth catshark Galeus melastomus , the velvet belly lanternshark Etmopterus spinax and the rabbit fish Chimaera monstrosa. To examine their trophic ecology and interspecific differences in food habits, we combined the analysis of stomach content and stable isotopes. Our results highlighted a trophic segregation between C. monstrosa and the other 2 species. G. melastomus showed a diet composed mainly of cephalopods, while E. spinax preyed mainly on shrimps and C. monstrosa on crabs. Interspecific differences in the trophic niche were likely due to different feeding capabilities and body size. Each species showed different isotopic niche space and trophic level. Specifically, C. monstrosa showed a higher trophic level than E. spinax and G. melastomus. The high trophic levels of the 3 species highlighted their important role as predators in the marine food web. Our results illustrate the utility of using complementary approaches that provide information about the feeding behaviour at short (stomach content) and long-term scales (stable isotopes), which could allow more efficient monitoring of marine food-web changes in the study area.

The influence of substratum type and nutrient supply on biofilm organic matter utilization in streams

We investigated the effect of benthic substratum type (sand and rocks) and nutrient supply (N and P) on biofilm structure and heterotrophic metabolism in a field experiment in a forested Mediterranean stream (Fuirosos). Rock and sand colonization and biofilm formation was intensively studied for 44 d at two stream reaches: control and experimental (continuous addition of phosphate, ammonia, and nitrate). Structural (C, N, and polysaccharide content and bacterial and chlorophyll density) and metabolic biofilm parameters (b-glucosidase, peptidase, and phosphatase enzyme activities) were analyzed throughout the colonization process. The epilithic biofilm (grown on rocks) had a higher peptidase activity at the impacted reach, together with a higher algal and bacterial biomass. The positive relationship between the peptidase activity per cell and the N content of the epilithic biofilm suggested that heterotrophic utilization of proteinaceous compounds from within the biofilm was occurring. In contrast, nutrient addition caused the epipsammic biofilm (grown on sand) to exhibit lower b-glucosidase and phosphatase activities, without a significant increase in bacterial and algal biomass. The differential response to nutrient addition was related to different structural characteristics within each biofilm. The epipsammic biofilm had a constant and high C:N ratio (22.7) throughout the colonization. The epilithic biofilm had a higher C:N ratio at the beginning of the colonization (43.2) and evolved toward a more complex structure (high polysaccharide content and low C:N ratio) during later stages. The epipsammic biofilm was a site for the accumulation and degradation of organic matter: polysaccharides and organic phosphorus compounds had higher degradation activities

Brook Trout Removal as a Conservation Tool to Restore Eagle Lake Rainbow Trout

Nonnative brook trout Salvelinus fontinalis are abundant in Pine Creek and its main tributary, Bogard Spring Creek, California. These creeks historically provided the most spawning and rearing habitat for endemic Eagle Lake rainbow trout Oncorhynchus mykiss aquilarum. Three-pass electrofishing removal was conducted in 2007–2009 over the entire 2.8-km length of Bogard Spring Creek to determine whether brook trout removal was a feasible restoration tool and to document the life history characteristics of brook trout in a California meadow stream. After the first 2 years of removal, brook trout density and biomass were severely reduced from 15,803 to 1,192 fish/ha and from 277 to 31 kg/ha, respectively. Average removal efficiency was 92–97%, and most of the remaining fish were removed in the third year. The lack of a decrease in age-0 brook trout abundance between 2007 and 2008 after the removal of more than 4,000 adults in 2007 suggests compensatory reproduction of mature fish that survived and higher survival of age-0 fish. However, recruitment was greatly reduced after 2 years of removal and is likely to be even more depressed after the third year of removal assuming that immigration of fish from outside the creek continues to be minimal. Brook trout condition, growth, and fecundity indicated a stunted population at the start of the study, but all three features increased significantly every year, demonstrating compensatory effects. Although highly labor intensive, the use of electrofishing to eradicate brook trout may be feasible in Bogard Spring Creek and similar small streams if removal and monitoring are continued annually and if other control measures (e.g., construction of barriers) are implemented. Our evidence shows that if brook trout control measures continue and if only Eagle Lake rainbow trout are allowed access to the creek, then a self-sustaining population ofEagle Lake rainbow trout can become reestablished

Population structure in a highly pelagic seabird, the Cory's shearwater (Calonectris diomedea): an examination of genetics, morphology and ecology

Increasing evidence suggests oceanic traits may play a key role in the genetic structuring of marine organisms. Whereas genetic breaks in the open ocean are well known in fishes and marine invertebrates, the importance of marine habitat characteristics in seabirds remains less certain. We investigated the role of oceanic transitions versus population genetic processes in driving population differentiation in a highly vagile seabird, the Cory"s shearwater, combining molecular, morphological and ecological data from 27 breeding colonies distributed across the Mediterranean (Calonectris diomedea diomedea) and the Atlantic (C. d. borealis). Genetic and biometric analyses showed a clear differentiation between Atlantic and Mediterranean Cory"s shearwaters. Ringing-recovery data indicated high site fidelity of the species, but we found some cases of dispersal among neighbouring breeding sites (<300 km) and a few long distance movements (>1000 km) within and between each basin. In agreement with this, comparison of phenotypic and genetic data revealed both current and historical dispersal events. Within each region, we did not detect any genetic substructure among archipelagos in the Atlantic, but we found a slight genetic differentiation between western and eastern breeding colonies in the Mediterranean. Accordingly, gene flow estimates suggested substantial dispersal among colonies within basins. Overall, genetic structure of the Cory"s shearwater matches main oceanographic breaks (Almería-Oran Oceanic Front and Siculo-Tunisian Strait), but spatial analyses suggest that patterns of genetic differentiation are better explained by geographic rather than oceanographic distances. In line with previous studies, genetic, phenotypic and ecological evidence supported the separation of Atlantic and Mediterranean forms, suggesting the 2 taxa should be regarded as different species.

Environmental factors, spatial variation, and specific requirements of Chironomidae in Mediterranean reference streams

Chironomidae spatial distribution was investigated at 63 near-pristine sites in 22 catchments of the Iberian Mediterranean coast. We used partial redundancy analysis to study Chironomidae community responses to a number of environmental factors acting at several spatial scales. The percentage of variation explained by local factors (23.3%) was higher than that explained by geographical (8.5%) or regional factors(8%). Catchment area, longitude, pH, % siliceous rocks in the catchment, and altitude were the best predictors of Chironomidae assemblages. We used a k-means cluster analysis to classified sites into 3 major groups based on Chironomidae assemblages. These groups were explained mainly by longitudinal zonation and geographical position, and were defined as 1) siliceous headwater streams, 2) mid-altitude streams with small catchment areas, and 3) medium-sized calcareous streams. Distinct species assemblages with associated indicator taxa were established for each stream category using IndVal analysis. Species responses to previously identified key environmental variables were determined, and optima and tolerances were established by weighted average regression. Distinct ecological requirements were observed among genera and among species of the same genus. Some genera were restricted to headwater systems (e.g., Diamesa), whereas others (e.g., Eukiefferiella) had wider ecological preferences but with distinct distributions among congenerics. In the present period of climate change, optima and tolerances of species might be a useful tool to predict responses of different species to changes in significant environmental variables, such as temperature and hydrology.

New strategies for treatment and reuse of spent sulfidic caustic stream from petroleum industry

This work examines traditional and new routes for removal of H2S and other sulfur compounds from spent sufidic caustic (SSC). SH- (hydrogenosulfide) and S2- (sulfide) ions were quantitatively oxidized at 25 ºC using H2O2, NaOCl or a spent sulfochromic mixture. SH-/S2- ions were also removed via reaction with freshly prepared iron or manganese hydroxides, or after passing the SSC through strong basic anion exchange resins (OH- form). The treated caustic solution, as well as iron/manganese hydroxides, removed H2S from diesel samples at 25 ºC. SSC treatment via strong basic anion-exchange resins produced the treated caustic solution with the highest free alkalinity.