Connecting higher‐order interactions with ecological stability in experimental aquatic food webs

Community ecology is built on theories that represent the strength of interactions between species as pairwise links. Higher‐order interactions (HOIs) occur when a species changes the pairwise interaction between a focal pair. Recent theoretical work has highlighted the stabilizing role of HOIs for large, simulated communities, yet it remains unclear how important higher‐order effects are in real communities. Here, we used experimental communities of aquatic protists to examine the relationship between HOIs and stability (as measured by the persistence of a species in a community). We cultured a focal pair of consumers in the presence of additional competitors and a predator and collected time series data of their abundances. We then fitted competition models with and without HOIs to measure interaction strength between the focal pair across different community compositions. We used survival analysis to measure the persistence of individual species. We found evidence that additional species positively affected persistence of the focal species and that HOIs were present in most of our communities. However, persistence was only linked to HOIs for one of the focal species. Our results vindicate community ecology theory positing that species interactions may deviate from assumptions of pairwise interactions, opening avenues to consider possible consequences for coexistence and stability

SEED: A framework for integrating ecological stoichiometry and eco‐evolutionary dynamics

Characterising the extent and sources of intraspecific variation and their ecological consequences is a central challenge in the study of eco‐evolutionary dynamics. Ecological stoichiometry, which uses elemental variation of organisms and their environment to understand ecosystem patterns and processes, can be a powerful framework for characterising eco‐evolutionary dynamics. However, the current emphasis on the relative content of elements in the body (i.e. organismal stoichiometry) has constrained its application. Intraspecific variation in the rates at which elements are acquired, assimilated, allocated or lost is often greater than the variation in organismal stoichiometry. There is much to gain from studying these traits together as components of an ‘elemental phenotype’. Furthermore, each of these traits can have distinct ecological effects that are underappreciated in the current literature. We propose a conceptual framework that explores how microevolutionary change in the elemental phenotype occurs, how its components interact with each other and with other traits, and how its changes can affect a wide range of ecological processes. We demonstrate how the framework can be used to generate novel hypotheses and outline pathways for future research that enhance our ability to explain, analyse and predict eco‐evolutionary dynamics

An experimental test of the growth rate hypothesis as a predictive framework for microevolutionary adaptation

The growth rate hypothesis (GRH) posits that the relative body phosphorus content of an organism is positively related to somatic growth rate, as protein synthesis, which is necessary for growth, requires P-rich rRNA. This hypothesis has strong support at the interspecific level. Here, we explore the use of the GRH to predict microevolutionary responses in consumer body stoichiometry. For this, we subjected populations of the rotifer Brachionus calyciflorus to selection for fast population growth rate (PGR) in P-rich (HPF) and P-poor (LPF) food environments. With common garden transplant experiments, we demonstrate that in HP populations evolution toward increased PGR was concomitant with an increase in relative phosphorus content. In contrast, LP populations evolved higher PGR without an increase in relative phosphorus content. We conclude that the GRH has the potential to predict microevolutionary change, but that its application is contingent on the environmental context. Our results highlight the potential of cryptic evolution in determining the performance response of populations to elemental limitation of their food resources

Functional diversity can facilitate the collapse of an undesirable ecosystem state

Biodiversity may increase ecosystem resilience. However, we have limited understanding if this holds true for ecosystems that respond to gradual environmental change with abrupt shifts to an alternative state. We used a mathematical model of anoxic-oxic regime shifts and explored how trait diversity in three groups of bacteria influences resilience. We found that trait diversity did not always increase resilience: greater diversity in two of the groups increased but in one group decreased resilience of their preferred ecosystem state. We also found that simultaneous trait diversity in multiple groups often led to reduced or erased diversity effects. Overall, our results suggest that higher diversity can increase resilience but can also promote collapse when diversity occurs in a functional group that negatively influences the state it occurs in. We propose this mechanism as a potential management approach to facilitate the recovery of a desired ecosystem state

Patterns of differentiation in the life history and demography of four recently described species of the Brachionus calyciflorus cryptic species complex

1. Brachionus calyciflorus is arguably the most studied freshwater monogonont roti‐ fer. Although it has been recognised as a cryptic species complex for more than a decade, a formal (re‐)description of the four species known so far (B. calyciflorus, Brachionus dorcas, Brachionus elevatus, and Brachionus fernandoi) has only recently been made. Information on the ecology of these species is very scant and frag‐ mented. The aim of this study was to test for ecological divergence between these four species, specifically their life history strategy and population demography. 2. We conducted a life history experiment using 12–16 genotypes per species. For each species, genotypes were extracted from at least three different natural pop‐ ulations. In addition, we performed population‐level culture experiments with the aim to compare population growth rates and demographic structure of experi‐ mental populations among species. Finally, we searched the literature for life his‐ tory studies with molecular data allowing retrospective species identification. 3. We found pronounced differences in life history traits between B. fernandoi and the other three species. B. fernandoi had higher egg and juvenile development times and a lower egg production rate and mictic ratio. We detected no significant life history differences among B. calyciflorus, B. elevatus, and B. dorcas. 4. Population growth rates of B. fernandoi and B. calyciflorus were higher than those of B. elevatus and B. dorcas. Life history divergence resulted in marked differences in the demographic structure of populations. Populations of B. fernandoi con‐ tained larger fractions of pre‐reproductive females and lower fractions of adult females with sexual eggs than populations of B. calyciflorus, B. elevatus, and B. dor‐ cas. Mortality was found to be highest in B. elevatus and lowest in B. calyciflorus populations. 5. Our results show that a reverse taxonomy approach is powerful in revealing sources of variation in ecologically relevant traits of cryptic species, such as life history and demographic structure. Explicit consideration of this variation is cru‐ cial for future studies of their dynamics in natural communities. KEYWORDS ecological divergence, integrative taxonomy, monogonont rotifer, reverse taxonomy, sibling species</p

Functional diversity can facilitate the collapse of an undesirable ecosystem state

Biodiversity may increase ecosystem resilience. However, we have limited understanding if this holds true for ecosystems that respond to gradual environmental change with abrupt shifts to an alternative state. We used a mathematical model of anoxic–oxic regime shifts and explored how trait diversity in three groups of bacteria influences resilience. We found that trait diversity did not always increase resilience: greater diversity in two of the groups increased but in one group decreased resilience of their preferred ecosystem state. We also found that simultaneous trait diversity in multiple groups often led to reduced or erased diversity effects. Overall, our results suggest that higher diversity can increase resilience but can also promote collapse when diversity occurs in a functional group that negatively influences the state it occurs in. We propose this mechanism as a potential management approach to facilitate the recovery of a desired ecosystem state

Mitigating Elemental Imbalance : Heritable & non-heritable adaptive responses to phosphorus limitation in an aquatic consumer

Organisms must obtain elements (e.g. carbon, nitrogen, phosphorus) from the environment in specific ratios, yet elemental availability often do not match their requirements. These mismatches can make it difficult for organisms to survive, grow, and reproduce. However, organisms can adapt through genetic (i.e., evolutionary) and non-genetic mechanisms to lessen the negative effects of elemental limitation. The goal of this thesis was to investigate the capacity to respond to phosphorus limitation in herbivorous invertebrates (e.g. zooplankton). Intraspecific variation is generally considered essential for rapid microevolutionary change. To determine the extent of intraspecific variation of stoichiometric traits, and thus the potential for to rapid evolution, I first performed a meta-analysis of common garden studies (Chapter 2). We documented small to moderated levels of variation in elemental content. In contrast, there was substantial variation in the acquisition, assimilation, allocation, and excretion of elements, the magnitude of which was similar to life history traits measured in the same studies. These results suggests that there is potential for stoichiometric traits to rapidly evolve. I next investigated if the rapid evolution of stoichiometric traits could be predicted using the ecological stoichiometric framework. Specifically, I tested if the growth rate hypothesis, which posits that organismal P content is positively related to somatic growth rate, could predict the elemental composition of consumer populations (Chapter 3). The anticipated positive relationship between body P-content and growth rate was observed in populations provided high phosphorus resources during selection for fast growth rates, but not in populations provided low phosphorus resources. These results demonstrate that the success of the growth rate hypothesis as a predictive framework is dependent on the environmental context under which selection takes place. The production of de novo heritable variation has been proposed as an alternative pathway for rapid adaptation. Therefore, I wanted to explore whether heritable adaptation in consumer populations that initially lack genetic diversity could occur on in response to stoichiometric mismatch (Chapter 4). We observed heritable adaptation to nutrient limitation in the populations with a low phosphorus exposure history in one of the two clones tested. These results suggest that de novo sources of phenotypic variation may play an important role in facilitating adaptation in populations with low genetic diversity. As environments can change rapidly, plastic responses in addition to the previously documented heritable responses may play an important role in responding to stoichiometric mismatch. To investigate the effect of stoichiometric mismatch on a primary consumer’s functional response, I preformed a series of ingestion experiments with resources of varying elemental and biochemical content (Chapter 5). We demonstrated that at high but not low food densities, consumers with low phosphorus resources exhibit elevated ingestion rates compared to consumer with high phosphorus resources. This thesis demonstrates that primary consumers have the capacity to mitigate the negative effects of stoichiometric mismatches using both heritable and non-heritable mechanisms. By incorporating biological realism (e.g. intraspecific variation, alternative adaptive pathways) into the ecological stoichiometric framework, we can improve our capacity to predict organismal responses to changes in elemental availability

Mitigating Elemental Imbalance : Heritable & non-heritable adaptive responses to phosphorus limitation in an aquatic consumer

Organisms must obtain elements (e.g. carbon, nitrogen, phosphorus) from the environment in specific ratios, yet elemental availability often do not match their requirements. These mismatches can make it difficult for organisms to survive, grow, and reproduce. However, organisms can adapt through genetic (i.e., evolutionary) and non-genetic mechanisms to lessen the negative effects of elemental limitation. The goal of this thesis was to investigate the capacity to respond to phosphorus limitation in herbivorous invertebrates (e.g. zooplankton). Intraspecific variation is generally considered essential for rapid microevolutionary change. To determine the extent of intraspecific variation of stoichiometric traits, and thus the potential for to rapid evolution, I first performed a meta-analysis of common garden studies (Chapter 2). We documented small to moderated levels of variation in elemental content. In contrast, there was substantial variation in the acquisition, assimilation, allocation, and excretion of elements, the magnitude of which was similar to life history traits measured in the same studies. These results suggests that there is potential for stoichiometric traits to rapidly evolve. I next investigated if the rapid evolution of stoichiometric traits could be predicted using the ecological stoichiometric framework. Specifically, I tested if the growth rate hypothesis, which posits that organismal P content is positively related to somatic growth rate, could predict the elemental composition of consumer populations (Chapter 3). The anticipated positive relationship between body P-content and growth rate was observed in populations provided high phosphorus resources during selection for fast growth rates, but not in populations provided low phosphorus resources. These results demonstrate that the success of the growth rate hypothesis as a predictive framework is dependent on the environmental context under which selection takes place. The production of de novo heritable variation has been proposed as an alternative pathway for rapid adaptation. Therefore, I wanted to explore whether heritable adaptation in consumer populations that initially lack genetic diversity could occur on in response to stoichiometric mismatch (Chapter 4). We observed heritable adaptation to nutrient limitation in the populations with a low phosphorus exposure history in one of the two clones tested. These results suggest that de novo sources of phenotypic variation may play an important role in facilitating adaptation in populations with low genetic diversity. As environments can change rapidly, plastic responses in addition to the previously documented heritable responses may play an important role in responding to stoichiometric mismatch. To investigate the effect of stoichiometric mismatch on a primary consumer’s functional response, I preformed a series of ingestion experiments with resources of varying elemental and biochemical content (Chapter 5). We demonstrated that at high but not low food densities, consumers with low phosphorus resources exhibit elevated ingestion rates compared to consumer with high phosphorus resources. This thesis demonstrates that primary consumers have the capacity to mitigate the negative effects of stoichiometric mismatches using both heritable and non-heritable mechanisms. By incorporating biological realism (e.g. intraspecific variation, alternative adaptive pathways) into the ecological stoichiometric framework, we can improve our capacity to predict organismal responses to changes in elemental availability

Experimental evidence of rapid heritable adaptation in the absence of initial standing genetic variation

The success of genetically depauperate populations in the face of environmental change is contrary to the expectation that high genetic diversity is required for rapid adaptation. Alternative pathways such as environmentally induced genetic modifications and non-genetic heritable phenotypes have been proposed mechanisms for heritable adaptation within an ecologically relevant time frame. However, experimental evidence is currently lacking to establish if, and to what extent, these sources of phenotypic variation can produce a response. To test if adaptation can rapidly occur in the absence of initial standing genetic variation and recombination in small populations, we (a) exposed replicate monoclonal populations of the microzooplankton Brachionus calyciflorus to a culturing regime that selected for phenotypic variants with elevated population growth with either high or low phosphorus food for a period of 55 days and (b) examined population level response in two fully factorial common garden experiments at day 15 and 35 of the exposure experiment. Within six generations, we observed heritable local adaptation to nutrient limitation. More specifically, populations with a history of exposure to low P food exhibited higher population growth rates under low P food conditions than populations with a high P exposure history. However, the capacity for such a response was found to vary among clones. Our study finds that although standing genetic variation is considered essential for rapid heritable adaptation, the rapid emergence of de novo genetic variation or alternative sources of phenotypic variation could aid in the establishment and persistence of low-diversity populations