In situ warming strengthens trophic cascades in a coastal food web

Global warming may affect most organisms and their interactions. Theory and simple mesocosm experiments suggest that consumer top–down control over primary producer biomass should strengthen with warming, since consumer respiration increases faster with warming than plant photosynthesis. However, these predictions have so far not been tested on natural communities that have experienced warming over many generations. Natural systems display a higher diversity, heterogeneity and complexity than mesocosms, which could alter predicted effects of warming. Here we used an artificially heated part of the northern Baltic Sea (the Forsmark Biotest basin) to test how warming influences trophic interactions in a shallow coastal food web with four trophic levels: omnivorous fish, invertivorous fish, herbivorous invertebrates, and filamentous macroalgae. Monitoring of fish assemblages over six years showed that small invertivorous fish (gobiids, sticklebacks and minnows) were much less abundant in the heated basin than in unheated references areas. Stomach content analyses of the dominating omnivorous fish – Eurasian perch Perca fluviatilis – revealed a strikingly different diet within and outside the Biotest basin; gammarid crustaceans were the dominating prey at heated sites, whereas invertivorous fish (e.g. gobiids) dominated at unheated sites. A 45‐day cage experiment showed that fish exclusion did not affect the biomass of algal herbivores (gastropods and gammarids), but reduced algal biomass in heated sites (but not unheated). This suggests that warming induced a trophic cascade from fish to algae, and that this effect was mediated by predator‐induced changes in herbivore behavior, rather than number. Overall, our study suggests that warming has effectively compressed the food chain from four to three trophic levels (algae, gammarids and perch), which have benefitted the primary producers by reducing grazing pressure. Consequently, warming appears to have restructured this coastal food web through a combination of direct (physiological) and indirect (species interactions) effects.     

Predator diversity strengthens trophic cascades in kelp forests by modifying herbivore behaviour

Although human-mediated extinctions disproportionately affect higher trophic levels, the ecosystem consequences of declining diversity are best known for plants and herbivores. We combined field surveys and experimental manipulations to examine the consequences of changing predator diversity for trophic cascades in kelp forests. In field surveys we found that predator diversity was negatively correlated with herbivore abundance and positively correlated with kelp abundance. To assess whether this relationship was causal, we manipulated predator richness in kelp mesocosms, and found that decreasing predator richness increased herbivore grazing, leading to a decrease in the biomass of the giant kelp Macrocystis. The presence of different predators caused different herbivores to alter their behaviour by reducing grazing, such that total grazing was lowest at highest predator diversity. Our results suggest that declining predator diversity can have cascading effects on community structure by reducing the abundance of key habitat-providing species.     

Interspecific differences in milkweeds alter predator density and the strength of trophic cascades

Trophic cascades occur when predators benefit plants by consuming herbivores, but the overall strength of a trophic cascade depends upon the way species interactions propagate through a system. For example, plant resistance to, or tolerance of, herbivores reduces the potential magnitude of a trophic cascade. At the same time, plants can also affect predator foraging or consumption in ways that either increase or decrease the strength of trophic cascades. In this study, we investigated the effects of plant variation on cascade strength by manipulating predator access to aphid populations on two species of milkweed: the slower-growing, putatively more-defended Asclepias syriaca and the faster-growing, putatively less-defended Asclepias incarnata. Predatory insects increased plant growth and survival for both species, but the strength of these trophic cascades was greater on A. incarnata, which supported more aphid growth early in the season than did A. syriaca. More predators were observed per aphid on A. incarnata, and cage treatments generated significant patterns consistent with predator aggregation on A. incarnata, but not A. syriaca. Although predators strongly affected aphids, this effect did not differ consistently between milkweed species. Plant tolerance to herbivory may therefore be the primary driver of the difference in trophic cascade strength observed. Importantly, we observed that the timing of predator exclusion affected plant growth and survival differently, indicating that measures of “cascade strength” may change with phenology and plant physiological responses. Together, our results suggest a mechanism by which differences in resource allocation patterns could explain differences in growth, phenology, and cascade strength between species.     

Development of empirical feeding models for a benthic predator

Feeding on Chironomus riparius, Glyptotendipes paripes (Chironomidae). and Daphnia magna by the predatory freshwater leech, Nephelopsis obscura , was investigated in the laboratory and predictive models developed to estimate prey capture rate in the field. Experimental arena (container) size significantly affected predation rates when arena diameter was less than twice the total body length of the predator. Both chironomid and Daphnia magna capture rates were influenced by predator size, temperature and prey density.     

Strong seasonality may attenuate trophic cascades: vertebrate predator exclusion in boreal grassland

We studied the indirect effects of vertebrate predator exclusion on plant communities in boreal grassland in western Finland to find out whether the removal of the top trophic level would result in a trophic cascade. Predators were excluded from 1996 to 2000 by eight predator-proof fences (each 0.5 ha) constructed on old fields. Despite a major increase in vole densities, the expected trophic cascade attenuated rapidly so that the indirect effects of predator exclusion were restricted to a few plant species. The cause for the rapid attenuation of the trophic cascade appeared to be strong seasonality, as peak densities of voles were attained at the end of the growing season of vegetation, and vole populations declined before the next growing season so that the herbivory pressure during the growing season remained low or moderate. Accordingly, most plants escaped the heaviest grazing pressure either in time (plants completed their reproduction and withered before winter) or in space (living parts hidden under frozen ground and ice). However, heavy winter herbivory reduced the biomass of available vegetation and killed woody species (willows) at vole peaks, which implies that predator exclusion may have a strong effect on secondary succession. During summer, voles reduced the coverage of only a few preferred food plants ( Elymus repens , Phleum pratense , Vicia cracca ). Voles also maintained annual and biennial species in the community by creating gaps in the closed vegetation. We conclude that abiotic factors (harsh winter conditions) limited peak numbers of herbivores below a threshold density where herbivores could have caused a community-level decline in the biomass of herbaceous plants during summer.     

Diel variation in use of cover and feeding activity of a benthic freshwater fish in response to olfactory cues of a diurnal predator

Some fish recognize the threat of predatory fish through chemical cues, which may result in variation in diel activity. However, there is little experimental evidence of diel shifts in activity of prey fish in response to the diel activity of a predator. We compared the total prey consumed and the use of cover by common bullies (Gobiomorphus cotidianus), a native benthic feeding eleotrid, when exposed to the odour of an exotic predator, European perch (Perca fluviatilis), over a 12-h period. Our results showed no significant effect of perch odour on feeding activity, but a significant increase in the use of cover at night and a decrease in the use of cover by day. While common bullies may recognize the presence of a predator through chemical cues, dark conditions may inhibit this and other sensory mechanisms, affecting their ability to recognize the proximity of a predator. For example, during the daytime they may rely on visual cues to initiate cover-seeking behavior, but in the dark, vision is impaired giving them less warning of predators, thus potentially making them more vulnerable.     

Interpopulation trophic niches and ontogenetic shifts of a mangrove fish predator

Fish trophic niches reflect important ecological interactions and provide insight into the structure of mangrove food webs. Few studies have been conducted in mangrove fish predators to investigate interpopulation trophic niches and ontogenetic shifts. Using stable isotope analysis and two complementary approaches, the authors investigated trophic niche patterns within and between two ontogenetic groups (juveniles and sub-adults) of a generalist predator (Acentrogobius viridipunctatus) in four mangroves with heterogeneous environmental conditions (e.g., tidal regimes, salinity fluctuations and mangrove tree community). The authors hypothesized that the trophic niche between populations would vary regionally and trophic position would increase consistently from juvenile to sub-adult stages. The results revealed that both δ¹³C and δ¹⁵N values varied greatly across populations and between ontogenetic groups, and complex spatio-ontogenetic variations were expressed by Layman's metrics. They also found some niche separation in space, which is most likely related to resource availability in spatially diverse ecosystems. In addition, trophic niche position increased consistently from juveniles to sub-adults, indicating ontogenetic feeding shifts. The isotopic plasticity index and Fulton's condition index also showed significant spatial-ontogenetic variation, which is consistent with optimal foraging theory. The findings highlight that trophic plasticity has a high adaptive value for mangrove fish predators in dynamic ecosystems.     

Responses to experimental fish manipulations in a shallow,hypereutrophic lake: the relative importance of benthic nutrient recycling and trophic cascade

The genetic polymorphism of twelve enzyme systems in two parthenogenetic tetraploidArtemia populations from N. Greece has been studied, using starch gel electrophoresis. The genetic distance within and among the two Greek populations was calculated. The high degree of genetic identity between the populations indicates that they belong to the same species. Each is composed of electrophoretically identifiable clones; the fitness of these clones under different environmental conditions is discussed.     

Effects of experimental duration and density of Japanese dace <Emphasis Type="Italic">Tribolodon hakonensis</Emphasis> on the strength of trophic cascades on benthic algae

To analyze density-mediated indirect effects through trophic cascades caused by Japanese dace Tribolodon hakonensis on the algal biomass and growth of ayu Plecoglossus altivelis altivelis, (freshwater fish belonging to Salmoniformes), I introduced zero, five, ten, and 20 dace with and without ayu into experimental pools. Ayu fed predominantly on benthic algae, whereas dace fed on both invertebrates and algae. The percentage of algae in the food content of dace was correlated with the number of dace in a pool. In the experiment lasting 8 days, trophic cascades on algae were not clear. In contrast, when the experimental duration was extended to 20 days, the number of gastropods and ephemeropteran nymphs was negatively correlated with the number of dace, consequently increasing the algal biomass and ayu growth through trophic cascades. Compared with pools with five dace, the presence of ten and 20 dace had similar gross effects on the number of algivorous invertebrates and algal biomass and greater gross effects on the ayu growth. The significant increase in ayu growth in pools with ten and 20 dace strongly suggests that small positive effects on algal growth by dace accumulated and extended to ayu during a 20-day experimental period. These results indicate the importance of analyzing interactions between the density and behavior of the top predator and the experimental duration on the intensity of trophic cascades.     

Effects of predator density and duration of predator occupancy on crustacean abundance and diversity in experimental pools

Keystone predators, by reducing the abundance of competitively superior prey, may have indirect positive effects on weak competitors, possibly increasing their abundance or preventing local competitive exclusion. By analogy to the Intermediate Disturbance Hypothesis, we would expect species diversity to peak at intermediate predator densities. In a replicated artificial pool experiment, we examined the relationships between density of the backswimmer Notonecta maculata (0, 1, 2, and 4 per 30 l pool) and invertebrate taxon diversity over an 11-week period of predator occupancy. Diversity reached high levels at high predator density sooner than at intermediate density. At the end of the experiment, taxon diversity was greatest at densities of 2 and 4 Notonecta per pool. While the overall predator density–diversity curve was in line with the intermediate disturbance hypothesis, the reduction in diversity from intermediate to high predator density was not statistically significant. Density of the preferred prey Daphnia magna decreased with Notonecta density, while densities of the smaller cladocerans Moina brachiata and Ceriodaphnia spp. increased. Suppression of Daphnia at high Notonecta densities may partially explain the increase in Moina and Ceriodaphnia densities. However, most of the relationship between Notonecta and the smaller cladocerans appears to be independent of Daphnia, suggesting complex interactions within the community. Our results suggest that keystone predation plays a strong role in structuring this community. Although diversity did not decrease significantly at the highest predator density as predicted, such a decrease may be more likely for pools with longer durations of predator occupancy or with higher predator densities.     

Photoacclimation in Antarctic bottom ice algae: an experimental approach

The aim of the study was to investigate the capacity of microalgae from the extremely low light habitat of bottom ice to acclimate to different light conditions. During austral spring 1997 the bottom layer of land-fast ice in Terra Nova Bay displayed high values of microalgal biomass up to 2,400 μg Chla L⁻¹ concentrated in a few centimetres ice layer. The algal assemblage was dominated by benthic pennate diatoms. Photoacclimation of the microalgae was addressed in terms of pigment spectra and photosynthetic parameters. Immediate and long term (minutes to days) changes in the photoprotective pigments (DD-cycle) were analysed. Severe photodamage occurred in microalgal assemblages exposed to high light. However, part of the bottom ice algal community showed a notable ability to acclimate to high irradiance levels. Changes in photosynthetic parameters preceded the sudden abrupt changes in pigment synthesis and the rapid increase in biomass and growth rates. This article belongs to a special topic: Five articles on Sea-ice communities in Terra Nova Bay (Ross Sea), coordinated by L. Guglielmo and V. Saggiomo, appear in this issue of Polar Biology. The studies were conducted in the frame of the National Program of Research in Antarctica (PNRA) of Italy.     

Effects of bottom trawling on fish foraging and feeding

The effects of bottom trawling on benthic invertebrates include reductions of biomass, diversity and body size. These changes may negatively affect prey availability for demersal fishes, potentially leading to reduced food intake, body condition and yield of fishes in chronically trawled areas. Here, the effect of trawling on the prey availability and diet of two commercially important flatfish species, plaice (Pleuronectes platessa) and dab (Limanda limanda), was investigated over a trawling intensity gradient in the Irish Sea. Previous work in this area has shown that trawling negatively affects the condition of plaice but not of dab. This study showed that reductions in local prey availability did not result in reduced feeding of fish. As trawling frequency increased, both fish and prey biomass declined, such that the ratio of fish to prey remained unchanged. Consequently, even at frequently trawled sites with low prey biomass, both plaice and dab maintained constant levels of stomach fullness and gut energy contents. However, dietary shifts in plaice towards energy-poor prey items were evident when prey species were analysed individually. This, together with a potential decrease in foraging efficiency due to low prey densities, was seen as the most plausible cause for the reduced body condition observed. Understanding the relationship between trawling, benthic impacts, fish foraging and resultant body condition is an important step in designing successful mitigation measures for future management strategies in bottom trawl fisheries.     

Cascading predator control interacts with productivity to determine the trophic level of biomass accumulation in a benthic food web

Large-scale exploitation of higher trophic levels by humans, together with global-scale nutrient enrichment, highlights the need to explore interactions between predator loss and resource availability. The hypothesis of exploitation ecosystems suggests that top–down and bottom–up control alternate between trophic levels, resulting in a positive relationship between primary production and the abundance of every second trophic level. Specifically, in food webs with three effective trophic levels, primary producers and predators should increase with primary production, while in food webs with two trophic levels, only herbivores should increase. We provided short-term experimental support for these model predictions in a natural benthic community with three effective trophic levels, where the number of algal recruits, but not the biomass of gastropod grazers, increased with algal production. In contrast, when the food web was reduced to two trophic levels by removing larger predators, the number of algal recruits was unchanged while gastropod grazer biomass increased with algal production. Predator removal only affected the consumer-controlled early life-stages of algae, indicating that both the number of trophic levels and the life-stage development of the producer trophic level determine the propagation of trophic cascades in benthic systems. Our results support the hypothesis that predators interact with resource availability to determine food-web structure.     

Structures associated with feeding in three broad-mouthed, benthic fish groups

Synopsis The flatheads, toadfishes, and goosefishes discussed here hold certain features in common. All are bottom-living forms with depressed head areas and broad gapes, and all eat large food items: fishes and/or crabs. All have developed structural specializations in association with this diet. The three groups are at most distantly related, and their feeding specializations are different and have evolved from different bases. In flatheads the combination of large food items and depressed head regions seems to have led to the separation of the two halves of the pelvic girdle, a feature in which they differ from their scorpaenoid relatives. Toadfish peculiarities associated with feeding are various but most notable in those that pass crabs they eat through the gape and into the mouth. Goosefish feeding is centered around the use of a lure to attract prey to within striking distance. The three fish groups are discussed separately, but their feeding structures are compared to one another in the final section of the paper.     

Vertical distribution of benthic community responses to fish predators, and effects on algae and suspended material

The vertical positioning of benthic invertebrates should be a trade-off between the risky, but productive, sediment surface and the safer, but physiologically harsher, conditions deeper down in the sediment. This is because the foraging efficiency of benthic fish decreases with sediment depth, whereas the sediment surface is generally better oxygenated and has a higher resource quality than lower layers. We studied how two benthic fish predators, bream (Abramis brama) and ruffe (Gymnocephalus cernuus), affected the community composition and vertical distribution of benthos, and their indirect effects on algae and suspended material, in field enclosures. Whereas bream had significant effects on the density, composition and distribution of the benthos, ruffe had no such effects. The total benthos biomass in bream treatments was an-order of magnitude lower in the upper sediment layer (0–1 cm) and three times lower in the middle layer (1–3 cm) than in the controls, whereas there were no significant effects in the deepest layer (3–10 cm). Bivalves persisted in the deepest layer although their density was reduced in shallow sediment, whereas gastropods faced the risk of local extinction in the presence of bream. As indirect effects, small-bodied cladocerans, phytoplankton, periphyton and both organic and inorganic suspended material were higher in the bream treatments. We␣conclude that the impact of bream diminished substantially with increasing sediment depth, enabling invertebrates to survive in the sediment and to persist in the presence of bream. However, there were␣no␣indications of any group adjusting their vertical position behaviourally as a response to predation threat.     

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.     

High assemblage persistence in heterogeneous habitats: an experimental test with stream benthic algae

1. The persistence of biological assemblages is positively affected by spatial heterogeneity. This influence may be indirect, through increased species richness. Another possibility is the increased availability of refuges from disturbances, which would prevent local loss. 2. We conducted a field experiment to test the hypothesis that greater roughness (a form of spatial heterogeneity) on the surface of substrata allows higher persistence of assemblages of stream benthic algae and that this relationship does not depend on species richness. Samples were taken on six occasions from smooth and rough artificial substrata used for algal colonisation. We calculated the persistence of assemblages using two analytical approaches: the mean distance to group centroid and the sum of the Euclidean distances between consecutive sampling occasions, both in a multivariate space. We also subsampled the data to take into account differences in species richness between treatments and thus to evaluate the effect of species richness on persistence. 3. Assemblages on rough substrata were more persistent than assemblages on smooth substrata. The effects detected were not due to the greater species richness on rough substrata, since a higher persistence of the assemblages on rough substrata remained after the subsampling procedures. 4. Our results indicate a strong positive relationship between substratum roughness and the persistence of stream benthic algal assemblages. We suggest that this is due to the presence of physical refuges in heterogeneous habitats.     

Cascading effects of predatory fish on the composition of benthic algae in high‐altitude streams

Cascading effects of predators can affect ecosystem properties by changing plant biomass, distribution and assemblage composition. Using data from field surveys and whole‐stream experiments we tested the hypothesis that predatory trout change assemblage composition of benthic algae in high‐elevation streams mediated by grazer behavior. Field surveys revealed that the taxonomic composition of algal assemblages differed significantly between streams that contained trout and those that were fishless; but comparisons of palatable versus unpalatable algal taxa between fish and fishless streams were equivocal because of high natural variability. Therefore, we tested for a behavioral (non‐consumptive) trophic cascade experimentally by adding brook trout chemical cues to six naturally fishless streams for 25 days and compared responses of grazers and algae to six reference streams without fish cues added. Algal response variables included rates of change in the abundance of three physiognomic categories, from most palatable (attached erect and prostrate diatoms) to least palatable (non‐diatoms), as determined from food selectivity analyses of the most common grazers (mayflies and caddisflies). Fish cues did not affect the mean densities or changes in densities of total grazers or any individual grazer species. However, in streams where fish cues were added, rates of accrual of attached erect diatoms, which was the preferred algal type for the grazer most vulnerable to trout predation (Baetis), were higher and their densities increased significantly faster with increasing densities of this grazer species than in reference streams. Results of his experiment support the hypothesis that predator induced suppression of grazer foraging behavior, rather than cascading effects of top predators on grazer density, may contribute to variation in the composition of algal assemblages among streams by allowing proliferation of most palatable algal species.