Habitat complexity dampens selection on prey activity level

Conspecific prey individuals often exhibit persistent differences in behavior (i.e., animal personality) and consequently vary in their susceptibility to predation. How this form of selection varies across environmental contexts is essential to predicting ecological and evolutionary dynamics, yet remains currently unresolved. Here, we use three separate predator–prey systems (sea star–snail, wolf spider–cricket, and jumping spider–cricket) to independently examine how habitat structural complexity influences the selection that predators impose on prey behavioral types. Prior to conducting staged predator–prey interaction encounters, we ran prey individuals through multiple behavioral assays to determine their average activity level. We then allowed individual predators to interact with groups of prey in either open or structurally complex habitats and recorded the number and individual identity of prey that were eaten. Habitat complexity had no effect on overall predation rates in any of the three predator–prey systems. Despite this, we detected a pervasive interaction between habitat structure and individual prey activity level in determining individual prey survival. In open habitats, all predators imposed strong selection on prey behavioral types: sea stars preferentially consumed sedentary snails, while spiders preferentially consumed active crickets. Habitat complexity dampened selection within all three systems, equalizing the predation risk that active and sedentary prey faced. These findings suggest a general effect of habitat complexity that reduces the importance of prey activity level in determining individual predation risk. We reason this occurs because activity level (i.e., movement) is paramount in determining risk within open environments, whereas in complex habitats, other behavioral traits (e.g., escape ability to a refuge) may take precedence.     

Silica particles with encapsulated DNA as trophic tracers

Ecological networks such as food webs are extremely complex and can provide important information about the robustness and productivity of an ecosystem. In most cases, it is not feasible to observe trophic interactions between predators and prey directly and with the available methods, it is difficult to quantify the connections between them. Here, we show that submicron‐sized silica particles (100–150 nm) with encapsulated DNA (SPED) enable accurate food and organism labelling and quantification of specific animal‐to‐animal transfer over more than one trophic level. We found that SPED were readily transferable and quantifiable from the bottom to the top of a two‐level food chain of arthropods. SPED were taken up in the gut system and remained persistent in an animal over several days. When uniquely labelled SPED were applied at predefined ratios, we found that information about their relative abundance was reliably conserved after trophic level transfer and over time. SPED were also applied to investigate the flower preference of fly pollinators and proved to be a fast and accurate analysis method. SPED combine attributes of DNA barcoding and stable isotope analysis such as unique labelling, quantification via real‐time PCR and exact backtracking to the tracer source. This improves and simplifies the analysis and monitoring of ecological networks.     

Predator personality structures prey communities and trophic cascades

Intraspecific variation is central to our understanding of evolution and population ecology, yet its consequences for community ecology are poorly understood. Animal personality – consistent individual differences in suites of behaviours – may be particularly important for trophic dynamics, where predator personality can determine activity rates and patterns of attack. We used mesocosms with aquatic food webs in which the top predator (dragonfly nymphs) varied in activity and subsequent attack rates on zooplankton, and tested the effects of predator personality. We found support for four hypotheses: (1) active predators disproportionately reduce the abundance of prey, (2) active predators select for predator‐resistant prey species, (3) active predators strengthen trophic cascades (increase phytoplankton abundance) and (4) active predators are more likely to cannibalise one another, weakening all other trends when at high densities. These results suggest that intraspecific variation in predator personality is an important determinant of prey abundance, community composition and trophic cascades.     

Caught in the web: Spider web architecture affects prey specialization and spider–prey stoichiometric relationships

Quantitative approaches to predator–prey interactions are central to understanding the structure of food webs and their dynamics. Different predatory strategies may influence the occurrence and strength of trophic interactions likely affecting the rates and magnitudes of energy and nutrient transfer between trophic levels and stoichiometry of predator–prey interactions. Here, we used spider–prey interactions as a model system to investigate whether different spider web architectures—orb, tangle, and sheet‐tangle—affect the composition and diet breadth of spiders and whether these, in turn, influence stoichiometric relationships between spiders and their prey. Our results showed that web architecture partially affects the richness and composition of the prey captured by spiders. Tangle‐web spiders were specialists, capturing a restricted subset of the prey community (primarily Diptera), whereas orb and sheet‐tangle web spiders were generalists, capturing a broader range of prey types. We also observed elemental imbalances between spiders and their prey. In general, spiders had higher requirements for both nitrogen (N) and phosphorus (P) than those provided by their prey even after accounting for prey biomass. Larger P imbalances for tangle‐web spiders than for orb and sheet‐tangle web spiders suggest that trophic specialization may impose strong elemental constraints for these predators unless they display behavioral or physiological mechanisms to cope with nutrient limitation. Our findings suggest that integrating quantitative analysis of species interactions with elemental stoichiometry can help to better understand the occurrence of stoichiometric imbalances in predator–prey interactions.     

Rethinking trophic niches: Speed and body mass colimit prey space of mammalian predators

1. Realized trophic niches of predators are often characterized along a one‐dimensional range in predator–prey body mass ratios. This prey range is constrained by an “energy limit” and a “subdue limit” toward small and large prey, respectively. Besides these body mass ratios, maximum speed is an additional key component in most predator–prey interactions.
2. Here, we extend the concept of a one‐dimensional prey range to a two‐dimensional prey space by incorporating a hump‐shaped speed‐body mass relation. This new “speed limit” additionally constrains trophic niches of predators toward fast prey.
3. To test this concept of two‐dimensional prey spaces for different hunting strategies (pursuit, group, and ambush predation), we synthesized data on 63 terrestrial mammalian predator–prey interactions, their body masses, and maximum speeds.
4. We found that pursuit predators hunt smaller and slower prey, whereas group hunters focus on larger but mostly slower prey and ambushers are more flexible. Group hunters and ambushers have evolved different strategies to occupy a similar trophic niche that avoids competition with pursuit predators. Moreover, our concept suggests energetic optima of these hunting strategies along a body mass axis and thereby provides mechanistic explanations for why there are no small group hunters (referred to as “micro‐lions”) or mega‐carnivores (referred to as “mega‐cheetahs”).
5. Our results demonstrate that advancing the concept of prey ranges to prey spaces by adding the new dimension of speed will foster a new and mechanistic understanding of predator trophic niches and improve our predictions of predator–prey interactions, food web structure, and ecosystem functions.

     

Temperature and prey density jointly influence trophic and non‐trophic interactions in multiple predator communities

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Understanding patterns and processes in models of trophic cascades

Climate fluctuations and human exploitation are causing global changes in nutrient enrichment of terrestrial and aquatic ecosystems and declining abundances of apex predators. The resulting trophic cascades have had profound effects on food webs, leading to significant economic and societal consequences. However, the strength of cascades–that is the extent to which a disturbance is diminished as it propagates through a food web–varies widely between ecosystems, and there is no formal theory as to why this should be so. Some food chain models reproduce cascade effects seen in nature, but to what extent is this dependent on their formulation? We show that inclusion of processes represented mathematically as density‐dependent regulation of either consumer uptake or mortality rates is necessary for the generation of realistic ‘top‐down’ cascades in simple food chain models. Realistically modelled ‘bottom‐up’ cascades, caused by changing nutrient input, are also dependent on the inclusion of density dependence, but especially on mortality regulation as a caricature of, e.g. disease and parasite dynamics or intraguild predation. We show that our conclusions, based on simple food chains, transfer to a more complex marine food web model in which cascades are induced by varying river nutrient inputs or fish harvesting rates.     

Detection of earthworm prey by Ruff Philomachus pugnax

Ruff Philomachus pugnax staging in the Netherlands forage in agricultural grasslands, where they mainly eat earthworms (Lumbricidae). Food intake and the surface availability of earthworms were studied in dairy farmland of southwest Friesland in March–April 2011. Daily changes in earthworm availability were quantified by counting visible earthworms. No earthworms were seen on the surface during daytime, but their numbers sharply increased after sunset and remained high during the night. Nevertheless, intake rates of individual Ruff in different grasslands measured during daytime showed the typical Holling type II functional response relationship with the surfacing earthworm densities measured at night. Radiotagging of Ruff in spring 2007 revealed that most, if not all, feeding occurs during the day, with the Ruff assembling at shoreline roosts at night. This raises the question of why Ruff do not feed at night, if prey can be caught more easily than during daytime. In March–May 2013 we experimentally examined the visual and auditory sensory modalities used by Ruff to find and capture earthworms. Five males were kept in an indoor aviary and we recorded them individually foraging on trays with 10 earthworms mixed with soil under various standardized light and white noise conditions. The number of earthworms discovered and eaten by Ruff increased with light level, but only when white noise was played, suggesting that although they can detect earthworms by sight, Ruff also use auditory cues. We suggest that although surfacing numbers of earthworms are highest during the night, diurnal intake rates are probably sufficient to avoid nocturnal foraging on a resource that is more available but perhaps less detectable at that time.     

Ten real‐time PCR assays for detection of fish predation at the community level in the San Francisco Estuary–Delta

The effect of predation on native fish by introduced species in the San Francisco Estuary–Delta (SFE) has not been thoroughly studied despite its potential to impact species abundances. Species‐specific quantitative PCR (qPCR) is an accurate method for identifying species from exogenous DNA samples. Quantitative PCR assays can be used for detecting prey in gut contents or faeces, discriminating between cryptic species, or detecting rare aquatic species. We designed ten TaqMan qPCR assays for fish species from the SFE watershed most likely to be affected by non‐native piscivores. The assays designed are highly specific, producing no signal from co‐occurring or related species, and sensitive, with a limit of detection between 3.2 and 0.013 pg/μL of target DNA. These assays will be used in conjunction with a high‐throughput qPCR platform to compare predation rates between native and non‐native piscivores and assess the impacts of predation in the system.     

Effects of prey abundance,distribution, visual contrast and morphology on selection by a pelagic piscivore

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Systematic deviations from linear size spectra of lake fish communities are correlated with predator–prey interactions and lake‐use intensity

Size structure of organisms at logarithmic scale (i.e. size spectrum) can often be described by a linear function with a negative slope; however, substantial deviations from linearity have often been found in natural systems. Theoretical studies suggest that greater nonlinearity in community size spectrum is associated with high predator–prey size ratios but low predator–prey abundance ratios; however, empirical evaluation of the effects of predator–prey interactions on nonlinear structures remains scarce. Here, we aim to empirically explore the pattern of the size‐specific residuals (i.e. deviations from the linear regression between the logarithmic fish abundance and the logarithmic mean fish size) by using size spectra of fish communities in 74 German lakes. We found that nonlinearity was strong in lakes with high predator–prey abundance ratios but at low predator–prey size ratios. More specifically, our results suggest that only large predators, even if occurring in low abundances, can control the density of prey fishes in a broad range of size classes in a community and thus promote linearity in the size spectrum. In turn, the lack of large predator fishes may cause high abundances of fish in intermediate size classes, resulting in nonlinear size spectra in these lakes. Moreover, these lakes were characterized by a more intense human use including high fishing pressure and high total phosphorus concentrations, which have negative impacts on the abundance of large, predatory fish. Our findings indicate that nonlinear size spectra may reflect dynamical processes potentially caused by predator–prey interactions. This opens a new perspective in the research on size spectrum, and can be relevant to further quantify the efficiency of energy transfer in aquatic food webs.     

Temperature,predator–prey interaction strength and population stability

Warming could strongly stabilize or destabilize populations and food webs by changing the interaction strengths between predators and their prey. Predicting the consequences of warming requires understanding how temperature affects ingestion (energy gain) and metabolism (energy loss). Here, we studied the temperature dependence of metabolism and ingestion in laboratory experiments with terrestrial arthropods (beetles and spiders). From this data, we calculated ingestion efficiencies (ingestion/metabolism) and per capita interaction strengths in the short and long term. Additionally, we investigated if and how body mass changes these temperature dependencies. For both predator groups, warming increased metabolic rates substantially, whereas temperature effects on ingestion rates were weak. Accordingly, the ingestion efficiency (the ratio of ingestion to metabolism) decreased in all treatments. This result has two possible consequences: on the one hand, it suggests that warming of natural ecosystems could increase intrinsic population stability, meaning less fluctuations in population density; on the other hand, decreasing ingestion efficiencies may also lead to higher extinction risks because of starvation. Additionally, predicted long‐term per capita interaction strengths decreased with warming, which suggests an increase in perturbation stability of populations, i.e., a higher probability of returning to the same equilibrium density after a small perturbation. Together, these results suggest that warming has complex and potentially profound effects on predator–prey interactions and food‐web stability.     

Size‐based interactions across trophic levels in food webs of shallow Mediterranean lakes

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Molecular detection of invertebrate prey in vertebrate diets: trophic ecology of Caribbean island lizards

Understanding community assembly and population dynamics frequently requires detailed knowledge of food web structure. For many consumers, obtaining precise information about diet composition has traditionally required sacrificing animals or other highly invasive procedures, generating tension between maintaining intact study populations and knowing what they eat. We developed 16S mitochondrial DNA sequencing methods to identify arthropods in the diets of generalist vertebrate predators without requiring a blocking primer. We demonstrate the utility of these methods for a common Caribbean lizard that has been intensively studied in the context of small island food webs: Anolis sagrei (a semi‐arboreal ‘trunk‐ground’ anole ecomorph). Novel PCR primers were identified in silico and tested in vitro. Illumina sequencing successfully characterized the arthropod component of 168 faecal DNA samples collected during three field trips spanning 12 months, revealing 217 molecular operational taxonomic units (mOTUs) from at least nine arthropod orders (including Araneae, Blattodea, Coleoptera, Hemiptera, Hymenoptera, Isoptera, Lepidoptera and Orthoptera). Three mOTUs (one beetle, one cockroach and one ant) were particularly frequent, occurring in ≥50% of samples, but the majority of mOTUs were infrequent (180, or 83%, occurred in ≤5% of samples). Species accumulation curves showed that dietary richness and composition were similar between size‐dimorphic sexes; however, female lizards had greater per‐sample dietary richness than males. Overall diet composition (but not richness) was significantly different across seasons, and we found more pronounced interindividual variation in December than in May. These methods will be generally useful in characterizing the diets of diverse insectivorous vertebrates.     

Changes in trophic level of Squatina guggenheim with increasing body length: relationships with type, size and trophic level of its prey

The occurrence of changes in the trophic level (TL) of sharks with growth has not been quantified until now. Here length-related changes on Squatina guggenheim Marini trophic level were determined, and shifts in type, size and trophic level of its prey were analysed. Sampling took place during five bottom trawl surveys conducted in the Argentine–Uruguayan Common Fishing Zone during spring (December/1995, October/1997) and fall (March/1997, March–April/1998, May–June/1998), using an Engel bottom-trawl net to capture the sharks. Three length groups were defined based on diet composition and using a cluster analysis (group I, 23–60 cm; group II, 61–80 cm; group III, 81–91 cm L _T). An ANOSIM procedure detected significant differences (P < 0.05) in the diet spectrum between the three length groups. The smallest sharks (group I) ingested fish prey ranging from 5 to 21 cm L _T, medium sharks (group II) fed on fish prey between 11 and 35 cm L _T, and largest sharks (group III) preyed on fish between 13 and 40 cm L _T. Diet structure of length groups were discriminated by almost the same prey taxa that characterized them. The increase of S. guggenheim body length promoted a decrease in the relative importance of small pelagic fishes. Contrarily, prey as medium benthopelagic fishes, medium pelagic squid and medium benthopelagic fishes showed an inverse tendency, indicating a broad diet spectrum of adults. Predator-length and prey-length relationship indicated a trend where 44.8% of S. guggenheim diet was integrated by prey <20% of their own body length and 32.8% of their diet was composed by prey >30% of their own length. The increase of mean prey weight was associated with the increase of predator weight and length. Smallest sharks (group I) were identified as secondary consumers (TL < 4) whereas medium sharks (group II) and largest sharks (group III) were placed as tertiary consumers (TL > 4). The study revealed an increase in S. guggenheim TL with shark growth as a consequence of changes on type, size and TL of prey ingested.     

Revolution in food web analysis and trophic ecology: diet analysis by DNA and stable isotope analysis

Characterization of energy flow in ecosystems is one of the primary goals of ecology, and the analysis of trophic interactions and food web dynamics is key to quantifying energy flow. Predator‐prey interactions define the majority of trophic interactions and food web dynamics, and visual analysis of stomach, gut or fecal content composition is the technique traditionally used to quantify predator‐prey interactions. Unfortunately such techniques may be biased and inaccurate due to variation in digestion rates ( Sheppard & Hardwood 2005 ); however, those limitations can be largely overcome with new technology. In the last 20 years, the use of molecular genetic techniques in ecology has exploded ( King et al. 2008 ). The growing availability of molecular genetic methods and data has fostered the use of PCR‐based techniques to accurately distinguish and identify prey items in stomach, gut and fecal samples. In this month’s issue of Molecular Ecology Resources, Corse et al. (2010) describe and apply a new approach to quantifying predator‐prey relationships using an ecosystem‐level genetic characterization of available and consumed prey in European freshwater habitats ( Fig. 1a ). In this issue of Molecular Ecology, Hardy et al. (2010) marry the molecular genetic analysis of prey with a stable isotope (SI) analysis of trophic interactions in an Australian reservoir community ( Fig. 1b ). Both papers demonstrate novel and innovative approaches to an old problem – how do we effectively explore food webs and energy movement in ecosystems?

Figure 1 Open in figure viewer PowerPoint The aquatic habitats used for two studies of diet and trophic interactions that employed molecular genetic and stable isotope analyses. Panel a: Example of Rhone basin habitat (France) where fish diet was determined using PCR to classify prey to a series of ecological clades (photo by Emmanuel Corse). Panel b: A weir pool on the lower Murray River (Australia) where food web and prey use was evaluated using a combination of advanced molecular genetic and stable isotope analyses (photo credit: CSIRO).     

Variable prey development time suppresses predator–prey cycles and enhances stability

Although theoretical models have demonstrated that predator–prey population dynamics can depend critically on age (stage) structure and the duration and variability in development times of different life stages, experimental support for this theory is non‐existent. We conducted an experiment with a host–parasitoid system to test the prediction that increased variability in the development time of the vulnerable host stage can promote interaction stability. Host–parasitoid microcosms were subjected to two treatments: Normal and High variance in the duration of the vulnerable host stage. In control and Normal‐variance microcosms, hosts and parasitoids exhibited distinct population cycles. In contrast, insect abundances were 18–24% less variable in High‐ than Normal‐variance microcosms. More significantly, periodicity in host–parasitoid population dynamics disappeared in the High‐variance microcosms. Simulation models confirmed that stability in High‐variance microcosms was sufficient to prevent extinction. We conclude that developmental variability is critical to predator–prey population dynamics and could be exploited in pest‐management programs.     

Predator diversity and the functioning of ecosystems: the role of intraguild predation in dampening trophic cascades

Single trophic‐level studies of the relationship between biodiversity and ecosystem functioning highlight the importance of mechanisms such as resource partitioning, facilitation, and sampling effect. In a multi‐trophic context, trophic interactions such as intraguild predation may also be an important mediator of this relationship. Using a salt‐marsh food web, we investigated the interactive effects of predator species richness (one to three species) and trophic composition (strict predators, intraguild predators, or a mixture of the two) on ecosystem functions such as prey suppression and primary production via trophic cascades. We found that the trophic composition of the predator assemblage determined the impact of increasing predator species richness on the occurrence of trophic cascades. In addition, increasing the proportion of intraguild predator species present diminished herbivore suppression and reduced primary productivity. Therefore, trophic composition of the predator assemblage can play an important role in determining the nature of the relationship between predator diversity and ecosystem function.