Copepod production : The interplay between abiotic environment, prey biochemical composition and consumers' requirements

Abstract

Ecosystems are complex adaptive systems because their living components are capable of adapting to environmental change, be it biotic or abiotic change. Organisms however can experience adverse consequences if environmental change exceeds levels they can tolerate by relying on their adaptive capabilities. Hence, our ability to understand, predict and mitigate the effects of ecological stressors, such as those associated with global climate change, pollution, and harvesting, depends largely on how we incorporate organismic adaptation into ecological investigations.

This is true for trophic ecology as for any other aspect of ecology, because animals demonstrate varying feeding regulation mechanisms in order to satisfy their demands for energy and chemical substances. Most can preferentially feed on prey organisms that promote fitness against disadvantageous ones, and those incapable of prey selection are endowed (by evolution) with physiological capabilities for dealing with disadvantageous food constituents. Hence, trophic adaptation among consumers does not only help define the structure of food webs and thus the complexity of ecological communities, it also determines the fate as well as the ecological transfer efficiency of biomass (and carbon). Adaptive trophic behaviour is however ignored or poorly represented in ecosystem models because a realistic framework, for effecting trophic behaviour, that incorporates relevant natural history details and is capable of providing mechanistic understanding of trophic processes is lacking.

Currently in aquatic ecology, trophic behaviour is assumed to be mainly dictated by food quality (Q), which is determined by employing food quality models (FQMs) that mimic consumers’ mechanism for anticipating the fitness consequences for feeding on specific prey items. Heuristically however, progress has been limited because previous FQMs are based on frameworks that a priori identify specific food components, usually nitrogen, phosphorus, and/or essential compounds, as pre-eminent or limiting. This suppresses trophic adaptability by negating the effect of habitat conditions (fluctuating temperature, etc), as well as that of consumers’ behaviour and physiology on food quality.

This thesis addresses the shortfalls in existing models by proposing a new FQM. The model determines food quality by considering (i) the biochemical characteristics of prey items, (ii) consumers’ demand for energy and structural constituents, and (iii) consumers’ capacity for food intake and metabolism based on physiological principles. It employs parameters that areadaptive to the relevant habitat conditions encountered by consumers. The model relies on the balance between the biochemical composition of prey items and consumer’s requirements to determine the potential fate and utilisation efficiencies of acquired chemical substances. The yardstick for food quality is the potential growth performance of consumers. The form of the model makes it applicable to all heterotrophs. Here, the focus is on copepod consumers because of the critical role they play in aquatic ecosystems. The model has been used to evaluate the growth performance of Acartia tonsa (Copepoda: Calanoida) over wide range of food conditions and the results are consistent with experimental observations. It predicts Acartia’s response to changes in prey biochemical composition to be unimodal, with growth being highest only when the biochemical composition of the prey imposes no constrain on egg production. This is consistent with experimental observations. Existing food quality models are incapable of this prediction. Hence, the FQM here is a better alternative, which, when employed could help in understanding substrate acquisition and utilisation for growth and reproduction by heterotrophs.

This was demonstrated by embedding the FQM here in a secondary production model for a consumer whose food intake and metabolic capabilities are bounded within a maximum threshold needed for growth and maintenance when food is “nutritionally good”, and a minimum threshold needed for only maintenance when food is “nutritionally poor”. The consumer relies on the food quality model to evaluate the growth limiting potentials of individual prey constituents. This information then dictates its regulatory response, in terms of feeding and metabolism, to the available prey. The demonstration was used to re-evaluate the hypothesis that carbon (C), relative to nitrogen (N), is a non-limiting resource for egg production by marine copepods. The results here challenge the hypothesis, and reveal potential causes for carbon limitation that previous models do not predict because they suffer from the above-stated shortfalls. Within the range of ecologically realistic algal C:N < 17, C-limitation was determined to be higher than that of N, due partly to the low metabolic availability of C associated with cellulose and structural carbohydrates. This result emphasizes the importance of biochemical substances in animal nutrition and production.

The dynamics of zooplankton production may be determined by the interaction between ambient temperature and prey biochemical composition. While this has been documented in experiments, previous zooplankton models contain no explicit description of it. Chapter 4 of this thesis shows how this could be done. It makes the new food quality model adaptive tochanges in ambient temperature by making animals’ demand for energy and structural constituents temperature dependent. This was then integrated into a model framework that allows consumers to regulate food ingestion, assimilation and metabolism based on their temperature-specific needs. Using this approach, growth rate, growth efficiency, as well as optimum temperatures for egg production by two copepod species with significantly different ranges of thermal tolerance were realistically simulated. Consistent with the results from other studies, the results here show that the growth response of copepods to changes in ambient temperature is driven mainly by temperature-induced changes in animals’ demand for maintenance. This observation emphasizes the cost of maintenance as a major constraint on zooplankton production.

Food quality models suffer from an important practical problem: it is difficult to define the biochemical traits of organisms and how those traits are dependent on the several relevant environmental conditions. To tackle this problem, published data on the proteins, carbohydrates, lipids, essential amino and fatty acids composition of microalgae (68 species belonging to 7 taxonomic classes species) and marine zooplankton (female: 42 species, eggs: 29 species) cultured under diverse conditions were reviewed. From the results, robust parameters, not restricted to specific species or habitat conditions, were determined. They have been employed for this study and could be used by others to characterize the biochemical composition of algae and zooplankton, independent of the environment. In addition, an experiment was conducted to investigate the impact of food availability on the reproductive strategy of copepods, in terms of females’ biochemical investment into eggsproduction. No food availability effect on the biochemical composition of females was observed. However, protein composition of eggs was higher in food-limited females. It has been argued that the production of protein-rich eggs by food-limited copepods is a reproductive strategy for ensuring the survival of offspring during poor feeding conditions.

In conclusion, this thesis provides realistic conceptual and mathematical frameworks for modelling trophic behaviour. It contributes to our understanding of trophic processes and their implications for nutrient cycling by grounding food quality on the behaviour, physiology, and habitat conditions of consumers. The model has been successfully integrated into an egg production model for copepods and implemented under variable temperature and food conditions.