Matthijs Vos

Empirical and theoretical challenges in aboveground–belowground ecology

A growing body of evidence shows that aboveground and belowground communities and processes are intrinsically linked, and that feedbacks between these subsystems have important implications for community structure and ecosystem functioning. Almost all studies on this topic have been carried out from an empirical perspective and in specific ecological settings or contexts. Belowground interactions operate at different spatial and temporal scales. Due to the relatively low mobility and high survival of organisms in the soil, plants have longer lasting legacy effects belowground than aboveground. Our current challenge is to understand how aboveground–belowground biotic interactions operate across spatial and temporal scales, and how they depend on, as well as influence, the abiotic environment. Because empirical capacities are too limited to explore all possible combinations of interactions and environmental settings, we explore where and how they can be supported by theoretical approaches to develop testable predictions and to generalise empirical results. We review four key areas where a combined aboveground–belowground approach offers perspectives for enhancing ecological understanding, namely succession, agro-ecosystems, biological invasions and global change impacts on ecosystems. In plant succession, differences in scales between aboveground and belowground biota, as well as between species interactions and ecosystem processes, have important implications for the rate and direction of community change. Aboveground as well as belowground interactions either enhance or reduce rates of plant species replacement. Moreover, the outcomes of the interactions depend on abiotic conditions and plant life history characteristics, which may vary with successional position. We exemplify where translation of the current conceptual succession models into more predictive models can help targeting empirical studies and generalising their results. Then, we discuss how understanding succession may help to enhance managing arable crops, grasslands and invasive plants, as well as provide insights into the effects of global change on community re-organisation and ecosystem processes.

Induced defences in marine and freshwater phytoplankton: a review.

Many organisms have developed defences to avoid predation by species at higher trophic levels. The capability of primary producers to defend themselves against herbivores affects their own survival, can modulate the strength of trophic cascades and changes rates of competitive exclusion in aquatic communities. Algal species are highly flexible in their morphology, growth form, biochemical composition and production of toxic and deterrent compounds. Several of these variable traits in phytoplankton have been interpreted as defence mechanisms against grazing. Zooplankton feed with differing success on various phytoplankton species, depending primarily on size, shape, cell wall structure and the production of toxins and deterrents. Chemical cues associated with (i) mechanical damage, (ii) herbivore presence and (iii) grazing are the main factors triggering induced defences in both marine and freshwater phytoplankton, but most studies have failed to disentangle the exact mechanism(s) governing defence induction in any particular species. Induced defences in phytoplankton include changes in morphology (e.g. the formation of spines, colonies and thicker cell walls), biochemistry (such as production of toxins, repellents) and in life history characteristics (formation of cysts, reduced recruitment rate). Our categorization of inducible defences in terms of the responsible induction mechanism provides guidance for future work, as hardly any of the available studies on marine or freshwater plankton have performed all the treatments that are required to pinpoint the actual cue(s) for induction. We discuss the ecology of inducible defences in marine and freshwater phytoplankton with a special focus on the mechanisms of induction, the types of defences, their costs and benefits, and their consequences at the community level.

INDUCIBLE DEFENSES AND TROPHIC STRUCTURE

Resource edibility is a crucial factor in ecological theory on the relative importance of bottom-up and top-down control. Current theory explains trophic structure in terms of the relative abundance and succession of edible and inedible species across gradients of primary productivity. We argue that this explanation is incomplete owing to its focus on inedibility and the assumption that plants and herbivores have fixed defense levels. Consumer-induced defenses are an important source of variation in the vulnerability of prey and are prevalent in natural communities. Such induced defenses decrease per capita consumption rates of consumers but hardly ever result in complete inedibility. When defenses are inducible a prey population may consist of both undefended and defended individuals. Here we use food chain models with realistic parameter values to show that variation in consumption rates on different prey types causes a gradual instead of stepwise increase in the biomass of all trophic levels in response to enrichment. Such all-level responses have been observed in both aquatic and terrestrial ecosystems and in microbial food chains in the laboratory. We stress that, in addition to the known food web effects of interspecific variation in edibility, intraspecific variation in edibility is another form of within-trophic-level heterogeneity that also has such effects. We conclude that inducible defenses increase the relative importance of bottom-up control.

Functional responses modified by predator density.

Realistic functional responses are required for accurate model predictions at the community level. However, controversy remains regarding which types of dependencies need to be included in functional response models. Several studies have shown an effect of very high predator densities on per capita predation rates, but it is unclear whether this predator dependence is also important at low predator densities. We fit integrated functional response models to predation data from 4-h experiments where we had varied both predator and prey densities. Using an information theoretic approach we show that the best-fit model includes moderate predator dependence, which was equally strong even at low predator densities. The best fits of Beddington–DeAngelis and Arditi–Akçakaya functional responses were closely followed by the fit of the Arditi–Ginzburg model. A Holling type III functional response did not describe the data well. In addition, independent behavioral observations revealed high encounter rates between predators. We quantified the number of encounters between predators and the time the focal predator spent interacting with other individuals per encounter. This time “wasted” on conspecifics reduced the total time available for foraging and may therefore account for lower predation rates at higher predator densities. Our findings imply that ecological theory needs to take realistic levels of predator dependence into account.

SPECIES DIVERSITY MODULATES PREDATION

Predation occurs in a context defined by both prey and non-prey species. At present it is largely unknown how species diversity in general, and species that are not included in a predators diet in particular, modify predator-prey interactions. Therefore we studied how both the density and diversity of non-prey species modified predation rates in experimental microcosms. We found that even a low density of a single nonprey species depressed the asymptote of a predators functional response. Increases in the density and diversity of non-prey species further reduced predation rates to very low levels. Controls showed that this diversity effect was not due to the identity of any of the non-prey species. Our results establish that both the density and diversity of species outside a predators diet can significantly weaken the strength of predator-prey interactions. These results have major implications for ecological theory on species interactions in simple vs. complex communities. We discuss our findings in terms of the relationship between diversity and stability.

INDUCED DEFENSES IN HERBIVORES AND PLANTS DIFFERENTIALLY MODULATE A TROPHIC CASCADE

Inducible defenses are dynamic traits that modulate the strength of both plant-herbivore and herbivore-carnivore interactions. Surprisingly few studies have considered the relative contributions of induced plant and herbivore defenses to the overall balance of bottom-up and top-down control. Here we compare trophic cascade strengths using replicated two-level and three-level plankton communities in which we systematically varied the presence or absence of induced defenses at the plant and/or herbivore levels. Our results show that a trophic cascade, i.e., significantly higher plant biomass in three-level than in two-level food chains, occurred whenever herbivores were undefended against carnivores. Trophic cascades did not occur when herbivores exhibited an induced defense. This pattern was obtained irrespective of the presence or absence of induced defenses at the plant level. We thus found that herbivore defenses, not plant defenses, had an overriding effect on cascade strength. We discuss these results in relation to variation in cascade strengths in natural communities.

Infochemicals structure marine, terrestrial and freshwater food webs: Implications for ecological informatics.

Here we consider how information transfer shapes interactions in aquatic and terrestrial food webs. All organisms, whether they are dead or alive, release certain chemicals into their environment. These can be used as infochemicals by any other individual in the food web that has the biological machinery to sense and process such information. Such machinery has evolved in bacteria, plants and animals and has thus become an inextricable part of the mechanisms that underlie feeding relations in food webs. Organisms live in environments suffused with infochemicals and this information network can be tapped into by both predators and their prey. However, it also opens doors to confusion in the face of a bewildering abundance and complexity of information. Infochemical mixing, masking, crypsis and mimicry could cause such confusion, especially in species-rich communities. We provide a point of entry into this field of enquiry by identifying seminal papers and major reviews and by discussing research lines that might enhance our mechanistic understanding of interactions in food webs. We highlight empirical work on the ways in which individuals use infochemicals and discuss model results on how this mediates patterns of population dynamics. We consider implications for ecosystem management and indicate how classical models and novel approaches from ecological informatics may contribute to linking the levels of individuals, populations and communities and their interactions with abiotic structuring forces in ecosystems.

Inducible defenses, competition and shared predation in planktonic food chains

Ecologists have long debated the role of predation in mediating the coexistence of prey species. Theory has mainly taken a bitrophic perspective that excludes the effects of inducible defenses at different trophic levels. However, inducible defenses could either limit or enhance the effects of predation on coexistence, by means of effects on bottom-up control and population stability. Our aim was to investigate how inducible defenses at different trophic levels affect the possibilities for predator-mediated coexistence, as opposed to competitive exclusion, in replicated experimental plankton communities. In particular, we analyzed how the presence or absence of inducible defenses in algal basal prey affected the outcome of competition between an inducible defended and an undefended herbivore, in the presence or absence of a carnivore. We found the undefended herbivore to be a superior competitor in the absence of predation. This outcome was reversed in the presence of a shared carnivore: populations of the undefended herbivore then strongly declined. The extent of this population decline differed between food webs based on undefended as opposed to inducible defended algal prey. In the former the undefended herbivore became undetectable for most of the duration of the experiment. In the latter the undefended herbivore also crashed to low densities, but it could still be detected during most of the experiment. In food webs based on inducible defended algae, the carnivore failed to reach high densities and exerted weaker top–down control on the two competing herbivores. We conclude that the inducible defense in one of our two competing herbivores allowed the outcome of competition to be reversed when a shared carnivore was added. Inducible defenses in algae did not change this outcome, but they significantly delayed extinction of the undefended herbivore. Predation itself did not promote coexistence in these experimental plankton communities.

Inducible defenses and rotifer food chain dynamics

Theoretical studies have predicted that inducible defenses affect food chain dynamics and persistence. Here we review and evaluate laboratory experiments that tested hypotheses developed from these theoretical studies. This review specifically focuses on the effects of inducible defenses in phytoplankton-rotifer food chain dynamics. First, we describe the occurrence of colony formation within different strains of green algae (Scenedesmaceae) in response to infochemicals released during grazing by the herbivorous rotifer Brachionus calyciflorus. Then we examined the effects of inducible defenses on the population dynamics of this planktonic system in which algal strains that differed in their defense strategies were used. Simple food chains were composed of green algae (Scenedesmaceae), herbivorous rotifers (Brachionus calyciflorus) and carnivorous rotifers (Asplanchna brightwellii). In this system B. calyciflorus exhibits an inducible defense against predation by developing long postero-lateral spines. Experimental studies showed that inducible defenses, as opposed to their absence, could prevent high-amplitude population fluctuations. We discuss the dual effects of induced defenses on extinction probabilities and consider the fit of a theoretical model to experimental data to understand the mechanisms that underlie the observed dynamics.

The Good, the Bad and the Plenty: Interactive Effects of Food Quality and Quantity on the Growth of Different Daphnia Species

Effects of food quality and quantity on consumers are neither independent nor interchangeable. Although consumer growth and reproduction show strong variation in relation to both food quality and quantity, the effects of food quality or food quantity have usually been studied in isolation. In two experiments, we studied the growth and reproduction in three filter-feeding freshwater zooplankton species, i.e. Daphnia galeata x hyalina, D. pulicaria and D. magna, on their algal food (Scenedesmus obliquus), varying in carbon to phosphorus (C∶P) ratios and quantities (concentrations). In the first experiment, we found a strong positive effect of the phosphorus content of food on growth of Daphnia, both in their early and late juvenile development. Variation in the relationship between the P-content of animals and their growth rate reflected interspecific differences in nutrient requirements. Although growth rates typically decreased as development neared maturation, this did not affect these species-specific couplings between growth rate and Daphnia P-content. In the second experiment, we examined the effects of food quality on Daphnia growth at different levels of food quantity. With the same decrease in P-content of food, species with higher estimated P-content at zero growth showed a larger increase in threshold food concentrations (i.e. food concentration sufficient to meet metabolic requirements but not growth). These results suggest that physiological processes such as maintenance and growth may in combination explain effects of food quality and quantity on consumers. Our study shows that differences in response to variation in food quality and quantity exist between species. As a consequence, species-specific effects of food quality on consumer growth will also determine how species deal with varying food levels, which has implications for resource-consumer interactions.