11. Biodiversity and Ecosystem Functioning: The Role of Trophic Interactions and the Importance of System Openness

The relationship between biodiversity and ecosystem functions (BEFs) has attracted great interest. Studies on BEF have so far focused on the average trend of ecosystem function as species diversity increases. A tantalizing but rarely addressed question is why large variations in ecosystem functions are often observed across systems with similar species diversity, likely obscuring observed BEFs. Here we use a multi-trophic food web model in combination with empirical data to examine the relationships between species richness and the variation in ecosystem functions (VEFs) including biomass, metabolism, decomposition, and primary and secondary production. We then probe the mechanisms underlying these relationships, focusing on the role of trophic interactions. While our results reinforce the previously documented positive BEF relationships, we found that ecosystem functions exhibit significant variation within each level of species richness and the magnitude of this variation displays a hump-shaped relationship with species richness. Our analyses demonstrate that VEFs is reduced when consumer diversity increases through elevated nonlinearity in trophic interactions, and/or when the diversity of basal species such as producers and decomposers decreases. This explanation is supported by a 34-year empirical food web time series from the Gulf of Riga ecosystem. Our work suggests that biodiversity loss may not only result in ecosystem function decline, but also reduce the predictability of functions by generating greater function variability among ecosystems. It thus helps to reconcile the debate on the generality of positive BEF relationships and to disentangle the drivers of ecosystem stability. The role of trophic interactions and the variation in their strengths mediated by functional responses in shaping ecosystem function variation warrants further investigations and better incorporation into biodiversity-ecosystem functioning research.

Plant protection products (PPPs) have historically been one of the classes of chemical compounds at the frontline of raising scientific and public awareness of the global nature of environmental pollution and the role of trophic interactions in shaping the impacts of chemicals on ecosystems. Despite increasingly strong regulatory measures since the 1970s designed to avoid unintentional effects of PPPs, their use is now recognised as a driver of biodiversity erosion. The French Ministries for the Environment, Agriculture and Research commissioned a collective scientific assessment to synthesise the current science and knowledge on the impacts of PPPs on biodiversity and ecosystem services. Here we report a literature review of the state of knowledge on the propagation of PPP residues and the effects of PPPs in food webs, including biopesticides, with a focus on current-use PPPs. Currently used PPPs may be stronger drivers of the current biodiversity loss than the banned compounds no longer in use, and there have been far fewer reviews on current-use PPPs than legacy PPPs. We first provide a detailed overview of the transfer and propagation of effects of PPPs through trophic interactions in both terrestrial and aquatic ecosystems. We then review cross-ecosystem trophic paths of PPP propagation, and provide insight on the role of trophic interactions in the impacts of PPPs on ecological functions. We conclude with a summary of the available knowledge and the perspectives for tackling the main gaps, and address areas that warrant further research and pathways to advancing environmental risk assessment.

Virulence and biodegradation potential of dynamic microbial communities associated with decaying Cladophora in Great Lakes

Increased global temperatures caused by climate change are causing species to shift their ranges and colonize new sites, creating novel assemblages that have historically not interacted. Species interactions play a central role in the response of ecosystems to climate change, but the role of trophic interactions in facilitating or preventing range expansions is largely unknown. The goal of our study was to understand how predators influence the ability of range-shifting prey to successfully establish in newly available habitat following climate warming. We hypothesized that fish predation facilitates the establishment of colonizing zooplankton populations, because fish preferentially consume larger species that would otherwise competitively exclude smaller-bodied colonists. We conducted a mesocosm experiment with zooplankton communities and their fish predators from lakes of the Sierra Nevada Mountains in California, USA. We tested the effect of fish predation on the establishment and persistence of a zooplankton community when introduced in the presence of higher- and lower-elevation communities at two experimental temperatures in field mesocosms. We found that predators reduce the abundance of larger-bodied residents from the alpine and facilitate the establishment of new lower-elevation species. In addition, fish predation and warming independently reduced the average body size of zooplankton by up to 30%. This reduction in body size offset the direct effect of warming-induced increases in population growth rates, leading to no net change in zooplankton biomass or trophic cascade strength. We found support for a shift to smaller species with climate change through two mechanisms: (a) the direct effects of warming on developmental rates and (b) size-selective predation that altered the identity of species' that could colonize new higher elevation habitat. Our results suggest that predators can amplify the rate of range shifts by consuming larger-bodied residents and facilitating the establishment of new species. However, the effects of climate warming were dampened by reducing the average body size of community members, leading to no net change in ecosystem function, despite higher growth rates. This work suggests that trophic interactions play a role in the reorganization of regional communities under climate warming.

There is increasing evidence that rare species play an important role in trophic interactions, but the function of rare species with low biomass in these processes remains unclear. Phytoplankton is placed at the base of lentic and marine food webs and is characterised by a few dominant species and many rare species. While the dominant species contribute most to the primary production, they are often low‐quality food for primary consumers. The rare species may instead provide the essential biochemical nutrients for consumers, especially in eutrophic waters. We hypothesised that the biomass of rare eukaryotic phytoplankton species significantly determines the concentrations of sestonic long‐chain highly unsaturated fatty acids, directly linking them to the functioning of aquatic ecosystems. We applied redundancy analysis and Lasso regression models to identify the species whose population dynamics explain the variations of sestonic fatty acids concentrations in tropical reservoirs and lakes. The lasso models predicted that the dominant phytoplankton species determined the concentration of saturated sestonic fatty acids and that rare phytoplankton species were the main determinant for polyunsaturated fatty acids, which are critical for the food quality of consumers such as zooplankton and promote the energy transfer from primary producers to higher trophic levels in natural waters. In particular, the biomass of the rare species Scenedesmus obliquus was a key variable explaining the variations of α‐linolenic acid, α‐linoleic acid, γ‐linolenic acid, and eicosapentaenoic acid concentrations. We conclude that the population dynamics of rare phytoplankton species can define the food quality associated with eicosapentaenoic acid for consumers and thus play a critical role in the trophic transfer in the food webs of tropical waterbodies.

An evaluation of implementing long-term MSY in ecosystem-based fisheries management: Incorporating trophic interaction, bycatch and uncertainty

Planktonic herbivory has been studied from a variety of perspectives (e.g. LEHMAN & SANDGREN 1985, STERNER 1989, CARPENTER et al. 1991, 1998, STERNER & HESSEN 1994). It is a focal trophic interaction in biomanipulation and a key process for us to understand. However, despite its obvious role in trophic interactions and nutrient cycling, there is no clear way to predict the level of planktonic herbivory in lakes (e.g. CYR & PACE 1992, 1993, CYR 1998). This study had two objectives: to obtain a community-level estimate of grazing in a variety of lakes; and to relate estimates of grazing to various physical, chemical and biological characteristics of the lakes.

Parasites are essential components of ecosystems and can be instrumental in maintaining host diversity and populations; however, their role in trophic interactions has often been overlooked. Three apicomplexan parasite species of Sarcocystis (S. singaporensis, S. zamani, and S. villivillosi) use the reticulated python as their definitive hosts and several species within the Rattus genus as intermediate hosts, and they form a system useful for studying interactions between host–parasite and predator–prey relationships, as well as anthropogenic impacts on parasite transmission. Based on predictions from a 1998 survey, which detected an inverse relationship between urban development and Sarcocystis infection in Rattus, we tested the hypothesis that Sarcocystis transmission in Singapore will decrease over time due to anthropogenic activities. Despite a large proportion of the reticulated python diet consisting of Rattus species at all sizes of pythons, Sarcocystis infection rates decreased from 1998 to 2010. Pythons found in industrial areas had lower Sarcocystis infection rates, particularly in the western industrial area of Singapore Island. Average python size also decreased, with implications that we predict may disrupt host–parasite relationships. Anthropogenic activities such as habitat modification, fragmentation, and systematic removal and translocation of pythons have negative impacts on Sarcocystis transmission in Singapore, which in turn may augment pest rat populations. Trends observed may ultimately have negative impacts on human health and biodiversity in the region.

The Palaearctic predator Dicyphus errans (Hemiptera: Miridae) lives omnivorously on various host plants, preying on a wide range of small arthropods, including some new invasive alien species. These characteristics make it a promising biological control agent (BCA) in organic greenhouses. The capacity of a BCA to find, kill and consume prey plays a fundamental role in trophic interactions and population dynamics in a predator-prey system. The functional response of a predator, which describes how the individual rate of prey consumption changes in response to prey density, is a key component to assess its effectiveness in pest control and the stability of its own populations. Therefore, the functional response of D. errans on different prey was studied to improve our knowledge on the potential of this mirid, which is naturally widespread in European organic greenhouses. Laboratory experiments were carried out on three exotic pests: the poinsettia thrips Echinothrips americanus (Thysanoptera: Thripidae), the greenhouse whitefly Trialeurodes vaporariorum (Hemiptera: Aleyrodidae), and the tomato borer Tuta absoluta (Lepidoptera: Gelechiidae), to build functional response curves. Prey was offered at different densities to single females of D. errans for 24 h. The predation behaviour of D. errans on all the prey species was defined by Type II functional response curves. The female could daily prey about 62 adults of E. americanus, 114 pupae of T. vaporariorum, and 236 eggs of T. absoluta. The high voracity of this generalist predator on different prey confirmed its suitability as a BCA. For effective and stable pest control strategies, a prior to pest establishment of D. errans in organic greenhouses may prevent pest escaping in case of high infestation rates, even if the type II functional response reaches saturation at very high prey densities.

The control of spider mites in protected crops is often critical due to the development of mite resistance to acaricides. Studies of the side-effects of pesticides on beneficial mites are required in order to improve integrated spider mite management. Pesticide side-effects on predatory mites of the family Phytoseiidae can be studied at the field or laboratory level. In the field, phytoseiid abundance can be related to the presence of prey and/or alternative foods, which can affect the response of predatory mites to pesticides. We investigated whether pesticide side-effects on phytoseiids may be mediated by trophic interactions. In the laboratory we evaluated the effects of two insecticides (derived from pyrethrins and Beauveria bassiana) on the predatory mite Phytoseiulus persimilis by testing the same under various exposure conditions (leaf residues, treated prey, topical application). The effects of these insecticides on P. persimilis were higher when the predators were fed with treated prey. Furthermore, we investigated the effects of pyrethrins on the predatory mite Amblyseius andersoni on vines with low or high incidence of the plant pathogenic fungus Plasmopara viticola (grape downy mildew, GDM). GDM mediated interactions between pyrethrins and A. andersoni since it is alternative food for this predatory mite. The implications of these studies for the development of toxicological methods and integrated pest management are discussed.

Bacterial community play an essential role in regulating water quality and the global biogeochemical cycle in aquatic ecosystems. However, how trophic interactions (i.e., biotic factors) regulate the diversity and composition of bacterial community in lake ecosystems remains unknown. Here, we employed DNA meta-barcoding of water samples to explore the impact of bacterivorous protozoans on the bacterial community. The results showed significant seasonal variations in the diversity and composition of both bacterial and protist communities. The composition of bacterivorous protozoans was identified as the primary predictor for the bacterial community alpha diversity in spring and summer, and for beta diversity in spring and autumn, indicating that biotic interactions play a greater role in driving the diversity of bacterial community across different seasons. Biological factors were more important than environmental factors for explaining the variations in the relative abundance of several bacterial genera (i.e., Pseudoxanthomonas, hgcI_clade, and Pseudorhodobacter). Network analyses showed that bacterial networks differed among seasons, and the autumn network exhibited the highest stability. Our findings indicated that the bacterial community stability was significantly affected by environmental factors, specifically SO42–and PO43–, rather than bacterivorous protozoans. Overall, our findings provide new perspectives on the role of trophic interactions in maintaining the structure of bacterial community in different seasons, and enhance our understanding of the bacterial community assembly in lake ecosystems.

Coastal marsh habitats are impacted by many disturbances, including habitat destruction, pollution, and the introduction of invasive species. The common reed, Phragmites australis, has been particularly invasive in the mesohaline regions of the Chesapeake Bay, but few studies have investigated its role in trophic interactions with North American marsh consumers. The marsh periwinkle snail Littoraria irrorata is a common grazer in marshes and grazes on the native grass Spartina alterniflora. Whether this snail grazes on Phragmites has not been addressed. We found Spartina leaves to be tougher than those of Phragmites, but despite this, snails consumed significantly more Spartina than Phragmites. Subsequent experiments demonstrated that Phragmites is chemically deterrent to snails by an unknown, moderately polar, compound. Further studies are required to more fully understand the interactions between Phragmites, herbivores, and Spartina, and how they may impact marsh ecosystems.

Interactions between trophic levels in upwelling and non-upwelling regions during summer monsoon

Plant–herbivore interactions provide critical insights into the mechanisms that govern the spatiotemporal distributions of organisms. These interactions are crucial to understanding the impacts of climate change, which are likely to have an effect on the population dynamics of alpine herbivores. The Royle's pika (Ochotona roylei, hereafter pika) is a lagomorph found in the western Himalaya and is dependent on alpine plants that are at risk from climate change. As the main prey of many carnivores in the region, the pika plays a crucial role in trophic interactions. We examined topographical features, plant genera presence and seasonal dynamics as drivers of the plant richness in the pika's diet across an elevational gradient (2,600–4,450 m). We identified 79 plant genera in the faecal pellets of pikas, of which 89% were forbs, >60% were endemic to the Himalaya, and 97.5% of the diet plant genera identified followed the C3 photosynthetic pathway. We found that, during the premonsoon season, the number of genera in the pika's diet decreased with increasing elevation. We demonstrate that a large area of talus supports greater plant diversity and, not surprisingly, results in higher species richness in the pika's diet. However, in talus habitat with deep crevices, pikas consumed fewer plant genera suggesting they may be foraging suboptimally due to predation risk. The continued increase in global temperature is expected to have an effect on the distribution dynamics of C3 plants and consequently influence pika diet and distribution, resulting in a significant negative cascading effect on the Himalayan ecosystem.

Switching from simple to complex dynamics in a predator–prey–parasite model: An interplay between infection rate and incubation delay