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Institut
Organism growth can be limited either by a single resource or by multiple resources simultaneously (co-limitation). Efforts to characterise co-limitation have generated two influential approaches. One approach uses limitation scenarios of factorial growth assays to distinguish specific types of co-limitation; the other uses growth responses spanned over a continuous, multi-dimensional resource space to characterise different types of response surfaces. Both approaches have been useful in investigating particular aspects of co-limitation, but a synthesis is needed to stimulate development of this recent research area. We address this gap by integrating the two approaches, thereby presenting a more general framework of co-limitation. We found that various factorial (co-)limitation scenarios can emerge in different response surface types based on continuous availabilities of essential or substitutable resources. We tested our conceptual co-limitation framework on data sets of published and unpublished studies examining the limitation of two herbivorous consumers in a two-dimensional resource space. The experimental data corroborate the predictions, suggesting a general applicability of our co-limitation framework to generalist consumers and potentially also to other organisms. The presented framework might give insight into mechanisms that underlie co-limitation responses and thus can be a seminal starting point for evaluating co-limitation patterns in experiments and nature.
Empirical data providing evidence for a colimitation of an herbivore by two or more essential nutrients are scarce, particularly in regard to biochemical resources. Here, a graphical model is presented, which describes the growth of an herbivore in a system with two potentially limiting resources. To verify this model, life-history experiments were conducted with the herbivore Daphnia magna feeding on the picocyanobacterium Synechococcus elongatus, which was supplemented with increasing amounts of cholesterol either in the presence or the absence of saturating amounts of eicosapentaenoic acid (EPA). For comparison, D. magna was raised on diets containing different proportions of S. elongatus and the cholesterol- and EPA-rich eukaryotic alga Nannochloropsis limnetica. Somatic and population growth of D. magna on a sterol- and EPA-deficient diet was initially constrained by the absence of sterols. With increased sterol availability, a colimitation by EPA became apparent and when the sterol requirements were met, the growth- limiting factor was shifted from a limitation by sterols to a limitation by EPA. These data imply that herbivores are frequently limited by two or more essential nutrients simultaneously. Hence, the concept of colimitation has to be incorporated into models assessing nutrient-limited growth kinetics of herbivores to accurately predict demographic changes and population dynamics.
Enhanced water temperatures promote the occurrence of cyanobacterial blooms, which may be detrimental to aquatic herbivores. Especially, the often-dominant crustaceans could be negatively affected because cyanobacteria are deficient in phytosterols, which are required by the crustaceans to form the membrane component cholesterol, which in turn plays a role in thermal adaptation. Here, we determined the influence of temperature on growth, reproduction and the allocation of dietary sterol into somatic tissues and eggs of the keystone species Daphnia magna raised along a dietary cholesterol gradient. Mass-specific growth rates of D. magna increased with the increasing availability of dietary cholesterol up to an incipient limiting level, which increased with increasing temperature. This indicates a higher demand for cholesterol for growth at higher temperatures and may explain the consistently smaller clutch sizes of reproducing females at the highest temperature. The cholesterol content of the individuals increased with increasing dietary cholesterol; this increase was enhanced at higher temperatures, indicating a higher demand for cholesterol for tissues and probably specifically for membranes. Surprisingly, the daphnids showed different allocation strategies with regard to temperature and dietary sterol availability. The cholesterol content of eggs was enhanced at higher temperature, which suggested that females allocate more cholesterol to their offspring, presumably to ensure sufficient egg development. When dietary cholesterol was limiting, however, females did not allocate more cholesterol to their eggs. Our data suggest that during cyanobacterial blooms, a potential dietary sterol limitation of Daphnia can be intensified at higher water temperatures, which can occur with global warming.
Ecosystems with highly pulsed water supply must be better understood as climate change may increase frequency and severity of intense storms, droughts and floods. Here we collected data over 3 years (2016-2018) in the episodic wetland outflow channel (Aluize), Banhine National Park, in which the system state changed from dry to wet to dry. Field sampling included vegetation records, small-scale vegetation zoning, the seed bank and water and soil quality. The same main plant species were found in both dry and wet conditions across the riverbed of the outflow channel. We found only very few diaspores of plants in the soil after prolonged drought. In the subsequent flooded state, we examined very dense vegetation on the water surface, which was dominated by the gramineous species Paspalidium obtusifolium. This species formed a compact floating mat that was rooted to the riverbed. The Cyperaceae Bolboschoenus glaucus showed high clonal growth in the form of root tubers, which likely serve as important food reservoir during drought. Soil and water analyses do not indicate a limitation by nutrients. We outline how resident people may change the plant community structure with an increasing practice of setting fire to the meadows in the dried-up riverbed to facilitate plant regrowth as food for their livestock.
Ecosystems with highly pulsed water supply must be better understood as climate change may increase frequency and severity of intense storms, droughts and floods. Here we collected data over 3 years (2016-2018) in the episodic wetland outflow channel (Aluize), Banhine National Park, in which the system state changed from dry to wet to dry. Field sampling included vegetation records, small-scale vegetation zoning, the seed bank and water and soil quality. The same main plant species were found in both dry and wet conditions across the riverbed of the outflow channel. We found only very few diaspores of plants in the soil after prolonged drought. In the subsequent flooded state, we examined very dense vegetation on the water surface, which was dominated by the gramineous species Paspalidium obtusifolium. This species formed a compact floating mat that was rooted to the riverbed. The Cyperaceae Bolboschoenus glaucus showed high clonal growth in the form of root tubers, which likely serve as important food reservoir during drought. Soil and water analyses do not indicate a limitation by nutrients. We outline how resident people may change the plant community structure with an increasing practice of setting fire to the meadows in the dried-up riverbed to facilitate plant regrowth as food for their livestock.
1. Herbivores show stronger control of element homoeostasis than primary producers, which can lead to constraints in carbon and nutrient transfer efficiencies from plants to animals. Insufficient dietary phosphorus (P) availability can cause reduced body P contents along with lower growth rates of animals, leading to a positive relationship between growth and body P.
2. We examined how a second limiting food component in combination with dietary P limitation influences growth and P homoeostasis of a herbivore and how this colimitation influences the hypothesized positive correlation between body P content and growth rates. Therefore, we investigated the responses in somatic growth and P stoichiometry of Daphnia magna raised on a range of diets with different amounts of P and the sterol cholesterol.
3. Somatic growth rates of D. magna increased asymptotically with increasing P as well as with increasing cholesterol availability. The body P content increased with increasing dietary P and stabilized at high dietary P availability. The observed plasticity in D. magna's P stoichiometry became stronger with increasing cholesterol availability, i.e. with decreasing colimitation by cholesterol.
4. At P-limiting conditions, the positive correlation between body P content and growth rate, as predicted by the growth rate hypothesis (GRH) applied to the within-species level, declined with increasing cholesterol limitation and disappeared entirely when cholesterol was not supplied. Thus, even when Daphnia shows no growth response owing to strong limitation by the colimiting nutrient, the body P content may vary substantially, calling into question the unconditional use of herbivores' P content as predictor of a potential P limitation in nature.
5. The observed interaction between dietary P and cholesterol on Daphnia's growth and stoichiometry can be used as a conceptual framework of how colimiting essential nutrients affect herbivore homoeostasis, and provide further insights into the applicability of the GRH within a consumer species.
Previous studies examining the effects of food quality on zooplankton often controlled for maternal effects of resource provisioning using standardized maternal diets. However, varying nutritional history of mothers may change resource provisioning to their progeny, especially regarding polyunsaturated fatty acids (PUFAs), which may change the interpretation of previously observed fitness responses of offspring. To assess PUFA-mediated maternal provisioning effects on offspring, we raised females of the cladoceran Daphnia magna on diets differing considerably in PUFA composition and raised their offspring on a PUFA-lacking diet supplemented with the omega 3 PUFAs alpha-linolenic acid (ALA) and/or eicosapentaenoic acid (EPA). The mass-specific growth responses of offspring to their own diets were affected by the maternal diet regime, probably due to varying maternal PUFA provisioning. A low maternal provisioning of EPA or ALA was sufficient to prevent growth limitation of offspring by these PUFAs until reaching maturity. A comparison with results of published ALA and EPA supplementation experiments suggests that the previously observed limitation effects depended on the usage of a single algae genus as maternal diet. Therefore, we suggest that maternal diets should be deliberately varied in future studies assessing ecological relevant food quality effects on zooplankton, especially regarding PUFAs.
There is growing consensus that the growth of herbivorous consumers is frequently limited by more than one nutrient simultaneously. This understanding, however, is based primarily on theoretical considerations and the applicability of existing concepts of co-limitation has rarely been tested experimentally. Here, we assessed the suitability of two contrasting concepts of resource limitation, i.e. Liebigs minimum rule and the multiple limitation hypothesis, to describe nutrient-dependent growth responses of a freshwater herbivore (Daphnia magna) in a system with two potentially limiting nutrients (cholesterol and eicosapentaenoic acid). The results indicated that these essential nutrients interact, and do not strictly follow Liebigs minimum rule, which consistently overestimates growth at co-limiting conditions and thus is not applicable to describe multiple nutrient limitation of herbivorous consumers. We infer that the outcome of resource-based modelling approaches assessing herbivore population dynamics strongly depends on the applied concept of co-limitation.