Food webs in the era of molecular revolution – Like resolving the Gordian knot with a tricorder

Living nature consists of countless organisms, which are classified into millions of species. These species interact in many ways; for example predators when foraging on their prey, insect larvae consuming plants, and pathogenic bacteria drifting into humans. In addition, abiotic nature has a great initiative impact on life through many factors (including sunlight, ambient temperature, and water. In my thesis, I have studied interactions among different life forms in multifaceted ways. The webs of these interactions are commonly referred to as food webs, describing feeding relationships between species or energy transfer from one trophic level to another. These ecological interactions – whether they occur between species, between individuals, or between microorganisms within an individual – are among the greatest forces affecting natural communities. Relationships are tightly related to biological diversity, that is, species richness and abundances. A species is called a node in food web vocabulary, and its interactions to other species are called links. Generally, Artic food webs are considered to be loosely linked, simple structures. This conception roots into early modern food webs, where insects and other arthropods, for example, were clumped under one node. However, it has been shown that arthropods form the greatest part of diversity and biomass both in the tropics and in Arctic areas. Earlier challenges of revealing the role of insects and microorganisms in interactions webs have become possible with the help of recent advances in molecular techniques. In the first chapter, I studied the prey diversity of a common bat, Myotis daubentonii, in southwestern Finland. My results proved M. daubentonii being a versatile predator whose diet mainly consists of aquatic insects, such as chironomid midges. In the second chapter, I expanded the view to changes in seasonal and individual-based variation in the diet of M. daubentonii including the relationship between available and observed prey. I found out that chironomids remain the major prey group even though their abundance decreases in proportion to other insect groups. Diet varied a lot between individuals, although the differences were not statistically significant. The third chapter took the study to a large network in Greenland. I showed that Artic food webs are very complex when arthropods are taken into account. In the fourth chapter, I examined the bacterial flora of M. daubentonii and surveyed the zoonotic potential of these bacteria. I found Bartonella bacteria, of which one was described as a new species named after the locality of discovery. I have shown in my thesis that Myotis daubentonii as a predator links many insect species as well as terrestrial and aquatic environments. Moreover, I have exposed that Arctic food webs are complex structures comprising of many densely linked species. Finally, I demonstrated that the bacterial flora of bats includes several previously unknown species, some of which could possibly turn in to zoonosis. To summarize, molecular methods have untied several knots in biological research. I hope that this kind of increasing knowledge of the surrounding nature makes us further value all the life forms on earth.

Dynamic ecosystems under anthropogenic stress : how does macrotidal sandy fauna respond to green tides?

Highly dynamic systems, often considered as resilient systems, are characterised by abiotic and biotic processes under continuous and strong changes in space and time. Because of this variability, the detection of overlapping anthropogenic stress is challenging. Coastal areas harbour dynamic ecosystems in the form of open sandy beaches, which cover the vast majority of the world’s ice-free coastline. These ecosystems are currently threatened by increasing human-induced pressure, among which mass-development of opportunistic macroalgae (mainly composed of Chlorophyta, so called green tides), resulting from the eutrophication of coastal waters. The ecological impact of opportunistic macroalgal blooms (green tides, and blooms formed by other opportunistic taxa), has long been evaluated within sheltered and non-tidal ecosystems. Little is known, however, on how more dynamic ecosystems, such as open macrotidal sandy beaches, respond to such stress. This thesis assesses the effects of anthropogenic stress on the structure and the functioning of highly dynamic ecosystems using sandy beaches impacted by green tides as a study case. The thesis is based on four field studies, which analyse natural sandy sediment benthic community dynamics over several temporal (from month to multi-year) and spatial (from local to regional) scales. In this thesis, I report long-lasting responses of sandy beach benthic invertebrate communities to green tides, across thousands of kilometres and over seven years; and highlight more pronounced responses of zoobenthos living in exposed sandy beaches compared to semi-exposed sands. Within exposed sandy sediments, and across a vertical scale (from inshore to nearshore sandy habitats), I also demonstrate that the effects of the presence of algal mats on intertidal benthic invertebrate communities is more pronounced than that on subtidal benthic invertebrate assemblages, but also than on flatfish communities. Focussing on small-scale variations in the most affected faunal group (i.e. benthic invertebrates living at low shore), this thesis reveals a decrease in overall beta-diversity along a eutrophication-gradient manifested in the form of green tides, as well as the increasing importance of biological variables in explaining ecological variability of sandy beach macrobenthic assemblages along the same gradient. To illustrate the processes associated with the structural shifts observed where green tides occurred, I investigated the effects of high biomasses of opportunistic macroalgae (Ulva spp.) on the trophic structure and functioning of sandy beaches. This work reveals a progressive simplification of sandy beach food web structure and a modification of energy pathways over time, through direct and indirect effects of Ulva mats on several trophic levels. Through this thesis I demonstrate that highly dynamic systems respond differently (e.g. shift in δ13C, not in δ15N) and more subtly (e.g. no mass-mortality in benthos was found) to anthropogenic stress compared to what has been previously shown within more sheltered and non-tidal systems. Obtaining these results would not have been possible without the approach used through this work; I thus present a framework coupling field investigations with analytical approaches to describe shifts in highly variable ecosystems under human-induced stress.

Studies on food and feeding of marine demersal finfishes with special reference to trophic interactions

Food and feeding habits of fourteen demersal finfishes exploited off the Karnataka coast were studied to investigate trophic interactions within the marine food web. Index of Relative Importance (lRI),Ontogenetic, seasonal (pre-monsoon, monsoon and post-monsoon) variation in feeding and prey-predator relationship studies were conducted.The results of prey-predator trophic interaction studies identified four major trophic guilds based on the predators feeding similarity.Trophic guild I is 'copepod and detritus fceders'with an average group similarity of 61.4%. The second trophic guild, 'prawn and crab feeders'with an average similarity of 52.7%. 'Acetes feeders', the largest trophic guild with an average group similarity of 62.5%, composed of six demersal finfish species.The guild 'piscivores' is constituted by C. limba/us and P. arsius with an average similarity of 45%.For each predator, ontogenetic diet shift is common and is characterized by prey of low to high trophic level.Strong selection of certain prey types was observed in some predators while most of them avoided abundant prey.In addition to Acetes spp, strong predation impact was observed for penaeid prawns, epibenthic crabs and detritus.This information on trophic guilds and prey-predator interactions can be used to construct trophic model on the benthic ecosystem off Karnataka and to investigate fishery induced changes as well as predation impact of different animals on commercially important demersals

Food webs of Mediterranean coastal wetlands

En aquesta tesi doctoral s'han estudiat els efectes directes i indirectes de dos tipus d'espècies claus de la comunitat aquàtica dels aiguamolls de l'Empordà (aiguamolls costaners mediterranis amb una xarxa tròfica senzilla). S'han realitzat experiments al camp utilitzant microcosmos i mesocosmos i els resultats han estat analitzats mitjançant tres aproximacions: la taxonòmica, la funcional i la de mides. S'ha comprovat que en situacions amb absència de predadors i dominància d'una única espècie en el zooplàncton (en aquest cas Calanipeda aquaedulcis i Daphnia magna), la segregació del recurs entre els diferents estadis de desenvolupament de la mateixa espècie zooplanctònica és una estratègia per evitar la competència intraespecífica en condicions de limitació de recurs. Per altra banda, la presència de diferents top-predators a la comunitat aquàtica (en aquest cas la medusa Odessia maeotica i el peix Aphanius iberus) desencadena una cascada tròfica en el plàncton però amb efectes top-down diferents segons el top-predator.

Eco-evolutionary Dynamics of Individual-Based Food Webs

The past decade has seen the rise of high resolution datasets. One of the main surprises of analysing such data has been the discovery of a large genetic, phenotypic and behavioural variation and heterogeneous metabolic rates among individuals within natural populations. A parallel discovery from theory and experiments has shown a strong temporal convergence between evolutionary and ecological dynamics, but a general framework to analyse from individual-level processes the convergence between ecological and evolutionary dynamics and its implications for patterns of biodiversity in food webs has been particularly lacking. Here, as a first approximation to take into account intraspecific variability and the convergence between the ecological and evolutionary dynamics in large food webs, we develop a model from population genomics and microevolutionary processes that uses sexual reproduction, genetic-distance-based speciation and trophic interactions. We confront the model with the prey consumption per individual predator, species-level connectance and prey–predator diversity in several environmental situations using a large food web with approximately 25,000 sampled prey and predator individuals. We show higher than expected diversity of abundant species in heterogeneous environmental conditions and strong deviations from the observed distribution of individual prey consumption (i.e. individual connectivity per predator) in all the environmental conditions. The observed large variance in individual prey consumption regardless of the environmental variability collapsed species-level connectance after small increases in sampling effort. These results suggest (1) intraspecific variance in prey–predator interactions has a strong effect on the macroscopic properties of food webs and (2) intraspecific variance is a potential driver regulating the speed of the convergence between ecological and evolutionary dynamics in species-rich food webs. These results also suggest that genetic–ecological drift driven by sexual reproduction, equal feeding rate among predator individuals, mutations and genetic-distance-based speciation can be used as a neutral food web dynamics test to detect the ecological and microevolutionary processes underlying the observed patterns of individual and species-based food webs at local and macroecological scales.

Chapter Six – Individual Trait Variation and Diversity in Food Webs

In recent years, there has been a renewed interest in the ecological consequences of individual trait variation within populations. Given that individual variability arises from evolutionary dynamics, to fully understand eco-evolutionary feedback loops, we need to pay special attention to how standing trait variability affects ecological dynamics. There is mounting empirical evidence that intra-specific phenotypic variation can exceed species-level means, but theoretical models of multi-trophic species coexistence typically neglect individual-level trait variability. What is needed are multispecies datasets that are resolved at the individual level that can be used to discriminate among alternative models of resource selection and species coexistence in food webs. Here, using one the largest individual-based datasets of a food web compiled to date, along with an individual trait-based stochastic model that incorporates Approximate Bayesian computation methods, we document intra-population variation in the strength of prey selection by different classes or predator phenotypes which could potentially alter the diversity and coexistence patterns of food webs. In particular, we found that strongly connected individual predators preferentially consumed common prey, whereas weakly connected predators preferentially selected rare prey. Such patterns suggest that food web diversity may be governed by the distribution of predator connectivity and individual trait variation in prey selection. We discuss the consequences of intra-specific variation in prey selection to assess fitness differences among predator classes (or phenotypes) and track longer term food web patterns of coexistence accounting for several phenotypes within each prey and predator species.

Dispersal dynamics in food webs

Studies of food webs suggest that limited nonrandom dispersal can play an important role in structuring food webs. It is not clear, however, whether density-dependent dispersal fits empirical patterns of food webs better than density-independent dispersal. Here, we study a spatially distributed food web, using a series of population-dispersal models that contrast density-independent and density-dependent dispersal in landscapes where sampled sites are either homogeneously or heterogeneously distributed. These models are fitted to empirical data, allowing us to infer mechanisms that are consistent with the data. Our results show that models with density-dependent dispersal fit the α, β, and γ tritrophic richness observed in empirical data best. Our results also show that density-dependent dispersal leads to a critical distance threshold beyond which site similarity (i.e., β tritrophic richness) starts to decrease much faster. Such a threshold can also be detected in the empirical data. In contrast, models with density-independent dispersal do not predict such a threshold. Moreover, preferential dispersal from more centrally located sites to peripheral sites does not provide a better fit to empirical data when compared with symmetric dispersal between sites. Our results suggest that nonrandom dispersal in heterogeneous landscapes is an important driver that shapes local and regional richness (i.e., α and γ tritrophic richness, respectively) as well as the distance-decay relationship (i.e., β tritrophic richness) in food webs.

Freshwater mesocosm experiment 2012 in Vancouver, Canada on effects of increased temperature and food chain length on oxygen fluxes and plankton community structure

Over broad thermal gradients, the effect of temperature on aerobic respiration and photosynthesis rates explains variation in community structure and function. Yet for local communities, temperature dependent trophic interactions may dominate effects of warming. We tested the hypothesis that food chain length modifies the temperature-dependence of ecosystem fluxes and community structure. In a multi-generation aquatic food web experiment, increasing temperature strengthened a trophic cascade, altering the effect of temperature on estimated mass-corrected ecosystem fluxes. Compared to consumer-free and 3-level food chains, grazer-algae (2-level) food chains responded most strongly to the temperature gradient. Temperature altered community structure, shifting species composition and reducing zooplankton density and body size. Still, food chain length did not alter the temperature dependence of net ecosystem fluxes. We conclude that locally, food chain length interacts with temperature to modify community structure, but only temperature, not food chain length influenced net ecosystem fluxes.

Fluctuating silicate:nitrate ratios and coastal plankton food webs

Marine diatoms require dissolved silicate to form an external shell, and their growth becomes Si-limited when the atomic ratio of silicate to dissolved inorganic nitrogen (Si:DIN) approaches 1:1, also known as the “Redfield ratio.” Fundamental changes in the diatom-to-zooplankton-to-higher trophic level food web should occur when this ratio falls below 1:1 and the proportion of diatoms in the phytoplankton community is reduced. We quantitatively substantiate these predictions by using a variety of data from the Mississippi River continental shelf, a system in which the Si:DIN loading ratio has declined from around 3:1 to 1:1 during this century because of land-use practices in the watershed. We suggest that, on this shelf, when the Si:DIN ratio in the river decreases to less than 1:1, then (i) copepod abundance changes from >75% to <30% of the total mesozooplankton, (ii) zooplankton fecal pellets become a minor component of the in situ primary production consumed, and (iii) bottom-water oxygen consumption rates become less dependent on relatively fast-sinking (diatom-rich) organic matter packaged mostly as zooplankton fecal pellets. This coastal ecosystem appears to be a pelagic food web dynamically poised to be either a food web composed of diatoms and copepods or one with potentially disruptive harmful algal blooms. The system is directed between these two ecosystem states by Mississippi River water quality, which is determined by land-use practices far inland.

Comparison of aquatic food chains using nitrogen isotopes.

Recent studies have shown the utility of delta(15)N to model trophic structure and contaminant bioaccumulation in aquatic food webs. However, cross-system comparisons in delta(15)N can be complicated by differences in delta(15)N at the base of the food chain. Such baseline variation in delta(15)N is difficult to resolve using plankton because of the large temporal variability in the delta(15)N of small organisms that have fast nitrogen turnover. Comparisons using large primary consumers, which have stable tissue isotopic signatures because of their slower nitrogen turnover, show that delta(15)N increases markedly with the human population density in the lake watershed. This shift in delta(15)N likely reflects the high delta(15)N of human sewage. Correcting for this baseline variation in delta(15)N, we report that, contrary to expectations based on previous food-web analysis, the food chains leading up to fish varied by about only one trophic level among the 40 lakes studied. Our results also suggest that the delta(15)N signatures of nitrogen at the base of the food chain will provide a useful tool in the assessment of anthropogenic nutrient inputs.

The importance of marine subsidies for terrestrial consumers in coastal Peru

The Peruvian coast is one the best examples of cross-ecosystem food web exchanges, in which resources from one of the richest marine ecosystems subsidize consumers in one of the driest deserts on Earth. Marine subsidies are resources that originate in the marine ecosystem, and that contribute to increase the density of consumers in the recipient ecosystem. I examined the effects of marine subsidies on animal populations in the Peruvian coastal desert. ^ I combined several approaches to study the linkages between marine resources and terrestrial consumers, such as surveying the spatial distribution and estimating the relative abundance of terrestrial consumers, studying the diet of geckos and lizards through stomach content analyses, and examining the desert food web with carbon and nitrogen stable isotope analyses. ^ I found that the distribution and diet of desert consumers were tightly coupled to the availability of marine subsidies. I revealed linkages along two pathways of nutrient fluxes: tidal action that washes ashore macroalgae and cadavers of marine organisms, and animal transport in places where pinnipeds and seabirds congregate for reproduction. In the first pathway, intertidal algivivores made marine resources available to terrestrial consumers by moving between the intertidal and supratidal zone. The relative contribution of terrestrial and algal carbon sources varied among terrestrial consumers, because scorpions assimilated a lower proportion of energy from macroalgae than did geckos and solifuges. In the second pathway, I found that pinniped colonies influenced the diet of desert consumers, and contributed to support large populations of lizards and geckos. By combining field observations, and stomach and stable isotope analyses, I constructed a simplified food web for a large sea lion colony, showing the number of trophic levels that originate from pinniped-derived nutrients. ^ My study demonstrates the enormous importance of marine resources for the diet of desert consumers. The near absence of rainfall along the Peruvian coast promotes an extreme dependence of terrestrial consumers on marine resources, and causes permanent food web effects that are affected by temporal variability in marine productivity, rather then temporal patterns of desert plant growth. ^

Exploring the role of large predators in marsh food webs: evidence for a behaviorally-mediated trophic cascade

The influence of large predators on lower trophic levels in oligotrophic, structurally complex, and frequently disturbed aquatic environments is generally thought to be limited. We looked for effects of large predators in two semi-permanent, spikerush-dominated marshes by excluding large fish (>12 mm body depth) and similarly sized herpetofauna from 1 m2 cages (exclosures) for 2 weeks. The exclosures allowed for colonization by intermediate (in size and trophic position) consumers, such as small fish, shrimp, and crayfish. Exclosures were compared to control cages that allowed large fish to move freely in and out. At the end of the experiment, intermediate-consumer densities were higher in exclosures than in controls at both sites. Decapod crustaceans, especially the riverine grass shrimp (Palaemonetes paludosus), accounted for the majority of the response. Effects of large fish on shrimp were generally consistent across sites, but per capita effects were sensitive to estimates of predator density. Densities of intermediate consumers in our exclosures were similar to marsh densities, while the open controls had lower densities. This suggests that these animals avoided our experimental controls because they were risky relative to the surrounding environment, while the exclosures were neither avoided nor preferred. Although illuminating about the dynamics of open-cage experiments, this finding does not influence the main results of the study. Small primary consumers (mostly small snails, amphipods, and midges) living on floating periphyton mats and in flocculent detritus (“floc”) were less abundant in the exclosures, indicative of a trophic cascade. Periphyton mat characteristics (i.e., biomass, chlorophyll a, TP) were not clearly or consistently affected by the exclosure, but TP in the floc was lower in exclosures. The collective cascading effects of large predators were consistent at both sites despite differences in drought frequency, stem density, and productivity.

The importance of marine subsidies for terrestrial consumers in coastal Peru

The Peruvian coast is one the best examples of cross-ecosystem food web exchanges, in which resources from one of the richest marine ecosystems subsidize consumers in one of the driest deserts on Earth. Marine subsidies are resources that originate in the marine ecosystem, and that contribute to increase the density of consumers in the recipient ecosystem. I examined the effects of marine subsidies on animal populations in the Peruvian coastal desert. I combined several approaches to study the linkages between marine resources and terrestrial consumers, such as surveying the spatial distribution and estimating the relative abundance of terrestrial consumers, studying the diet of geckos and lizards through stomach content analyses, and examining the desert food web with carbon and nitrogen stable isotope analyses. I found that the distribution and diet of desert consumers were tightly coupled to the availability of marine subsidies. I revealed linkages along two pathways of nutrient fluxes: tidal action that washes ashore macroalgae and cadavers of marine organisms, and animal transport in places where pinnipeds and seabirds congregate for reproduction. In the first pathway, intertidal algivivores made marine resources available to terrestrial consumers by moving between the intertidal and supratidal zone. The relative contribution of terrestrial and algal carbon sources varied among terrestrial consumers, because scorpions assimilated a lower proportion of energy from macroalgae than did geckos and solifuges. In the second pathway, I found that pinniped colonies influenced the diet of desert consumers, and contributed to support large populations of lizards and geckos. By combining field observations, and stomach and stable isotope analyses, I constructed a simplified food web for a large sea lion colony, showing the number of trophic levels that originate from pinniped-derived nutrients. My study demonstrates the enormous importance of marine resources for the diet of desert consumers. The near absence of rainfall along the Peruvian coast promotes an extreme dependence of terrestrial consumers on marine resources, and causes permanent food web effects that are affected by temporal variability in marine productivity, rather then temporal patterns of desert plant growth.

Diversity and Stability in Food Webs : Impacts of Non-Equilibrium Dynamics, Topology and Variation

With progressive climate change, the preservation of biodiversity is becoming increasingly important. Only if the gene pool is large enough and requirements of species are diverse, there will be species that can adapt to the changing circumstances. To maintain biodiversity, we must understand the consequences of the various strategies. Mathematical models of population dynamics could provide prognoses. However, a model that would reproduce and explain the mechanisms behind the diversity of species that we observe experimentally and in nature is still needed. A combination of theoretical models with detailed experiments is needed to test biological processes in models and compare predictions with outcomes in reality. In this thesis, several food webs are modeled and analyzed. Among others, models are formulated of laboratory experiments performed in the Zoological Institute of the University of Cologne. Numerical data of the simulations is in good agreement with the real experimental results. Via numerical simulations it can be demonstrated that few assumptions are necessary to reproduce in a model the sustained oscillations of the population size that experiments show. However, analysis indicates that species "thrown together by chance" are not very likely to survive together over long periods. Even larger food nets do not show significantly different outcomes and prove how extraordinary and complicated natural diversity is. In order to produce such a coexistence of randomly selected species—as the experiment does—models require additional information about biological processes or restrictions on the assumptions. Another explanation for the observed coexistence is a slow extinction that takes longer than the observation time. Simulated species survive a comparable period of time before they die out eventually. Interestingly, it can be stated that the same models allow the survival of several species in equilibrium and thus do not follow the so-called competitive exclusion principle. This state of equilibrium is more fragile, however, to changes in nutrient supply than the oscillating coexistence. Overall, the studies show, that having a diverse system means that population numbers are probably oscillating, and on the other hand oscillating population numbers stabilize a food web both against demographic noise as well as against changes of the habitat. Model predictions can certainly not be converted at their face value into policies for real ecosystems. But the stabilizing character of fluctuations should be considered in the regulations of animal populations.

Spatial variation in the strength of mutualism between a jumping spider and a terrestrial bromeliad: Evidence from the stable isotope N-15

Psecas chapoda, a neotropical jumping spider strictly associated with the terrestrial bromeliad Bromelia balansae in cerrados and semi-deciduous forests in South America, effectively contributes to plant nutrition and growth. In this study, our goal was to investigate if spider density caused spatial variations in the strength of this spider-plant mutualism. We found a positive significant relationship between spider density and delta N-15 values for bromeliad leaves in different forest fragments. Open grassland Bromeliads were associated with spiders and had higher delta N-15 values compared to forest bromeliads. Although forest bromeliads had no association with spiders their total N concentrations were higher. These results suggest that bromeliad nutrition is likely more litter-based in forests and more spider-based in open grasslands. This study is one of the few to show nutrient provisioning and conditionality in a spider-plant system. (c) 2008 Elsevier Masson SAS. All rights reserved.