A meta‐analysis of the effects of detritus on primary producers and consumers in marine,freshwater, and terrestrial ecosystems

Detritus is a central feature in marine, freshwater, and terrestrial ecosystems. Despite the ubiquity of detritus, ecologists have largely ignored its role in influencing food web structure. We used a meta‐analytic approach to ask three questions about how detritus affects food web structure in a wide variety of ecosystems. First, what is the effect strength of detritus on primary producers, detritivores, herbivores, and predators? Second, what functional role does detritus serve for consumers (energetic, habitat, or both)? Third, how does the effect of detritus on consumers vary between aquatic and terrestrial ecosystems? We found that detritus has strong positive effects on primary producers and consumers in a wide range of ecosystems types. Detritus has a positive direct effect on detritivores by providing both an energetic resource and habitat (refuge from predators). Detritus has equally strong positive effects on herbivores and predators, driven by a positive direct effect of habitat. Detritus has positive effects on consumers in both aquatic and terrestrial ecosystems with 1.7 times stronger effects in terrestrial ecosystems. These results suggest that detritus has strong effects on food‐web structure in a variety of ecosystem types. Even the portion of the food web that is linked most strongly to living plant tissue as its primary energy source is strongly positively affected.     

Terrestrial detritus supports the food webs in lowland intermittent streams of south‐eastern Australia: a stable isotope study

• 1 Large amounts of terrestrial detritus enter many low‐order forested streams, and this organic material is often the major basal resource in the metazoan food webs of such systems. However, despite their apparently low biomass, algae are the dominant food of organisms in a number of aquatic communities which conventionally would have been presumed to be dependent on allochthonous detritus, particularly those in the tropics and also in lowland intermittent streams in arid Australia.
• 2 The dual stable isotope signatures (δ¹³C and δ¹⁵N) of potential primary food sources were compared with the isotopic signatures of common aquatic animals in lowland intermittent streams in south‐eastern Australia, in both spring and summer, to determine whether allochthonous detritus was an important nutritional resource in these systems. The isotopic signatures of the major potential allochthonous plant food sources (Eucalyptus, Phalaris and Juncus) overlapped, but were distinct from algae and the dominant macrophytes growing in the study reaches. The isotopic signatures of biofilm were more spatially and temporally variable than those of the other basal resources.
• 3 Despite allochthonous detritus having relatively high C : N ratios compared to other potential basal resources, results from isosource mixing model calculations demonstrated that this detritus, and the associated biofilm, were the major energy sources assimilated by macroinvertebrate primary consumers in both spring and summer. The importance of these energy sources was also reflected in animals higher in the food web, including predatory macroinvertebrates and fish. These resources were supplemented by autochthonous sources of higher nutritional value (i.e. filamentous algae and macrophytes, which had relatively low C : N ratios) when they became more prolific as the streams dried to disconnected pools in summer.
• 4 The results highlight the importance of allochthonous detritus (particularly from Eucalyptus) as a dependable energy source for benthic macroinvertebrates and fish in lowland intermittent streams of south‐eastern Australia. This contrasts with previous stable isotope studies conducted in lowland intermittent streams in arid Australia, which have reported that the fauna are primarily dependent on autochthonous algae.

     

Food sources and foraging tactics in tropical rain pools

Pools on exposed rocks are common over much of Africa. Based on dimensions and position, those examined are of three types. Each type is inhabited by larvae of virtually a single dipteran species at high densities (over two million larvae m^-2).
Location of the pools suggests that food might be a limiting factor. However, events, including defecation in pools by civets and genets, fruit fall and wind-borne pollen, apparently ensure that this is not the case. In this environment of superabundance animals are presumably free to choose favoured items of food.
Each animal species does, indeed, take a characteristic assemblage of food items. However, each species is shown to eat whatever it can swallow, differences in gut contents being due to differences in the characteristic food items available in each type of pool. Most algae are excluded because they are too large or inaccessible, which means that the pool food chains are based largely on allochthonous detritus. There is no reason to believe that food type, perse , has any influence in determining which of the three dipteran species is present.     

Persistence despite omnivory: benthic communities and the discrepancy between theory and observation

Omnivory is omnipresent in natural communities. However, most theoretical models predict that omnivory should be rare, especially at high basal productivity. To address this incongruity, we consider as an example benthic food webs with omnivory. We present a mathematical analysis of simple benthic food webs in which a number of mechanisms promote persistence of omnivory. As a model system, we focus on the interaction between detritus, bacteria and deposit feeders that feed on both bacteria and detritus. Biomass patterns change with increasing basal productivity, triggering mechanisms that weaken the interactions between components of omnivorous interactions. Consequently, these mechanisms extend the range of organic input rates at which omnivorous interactions persist, and prevent exclusion, promoting omnivorous interactions in productive environments. These mechanisms give potential explanations for the high incidence of omnivory in benthic communities and shed insight on the persistence of omnivory in other communities.     

Effects of transgenic American chestnut leaf litter on growth and survival of wood frog larvae

Biotechnology offers a new approach for the restoration of tree species affected by exotic pathogens; however, nontarget impacts of this novel strategy on other organisms have not been comprehensively assessed. We evaluated the effect of transgenic American chestnut (Castanea dentata) leaf litter on the growth and survival of larval wood frogs (Lithobates sylvaticus), a forest‐dwelling amphibian species widely sympatric with American chestnut, that forage almost entirely on periphyton and litter detritus that accumulate in temporary vernal pools in forests. We reared wood frog larvae on Castanea leaf litter (American chestnut genetically engineered for blight tolerance, nontransgenic American chestnut, Chinese chestnut [Castanea mollissima], and an American–Chinese chestnut hybrid) and litter from two non‐Castanea, nontransgenic “control” tree species, coupled with two levels of supplementary food. We observed no differences in growth or survival of wood frog larvae reared on transgenic versus nontransgenic American chestnut leaves. Without supplementary food, wood frog larvae provided leaves from American chestnut (both types) developed faster and grew larger than those exposed to other leaf litter treatments. Results of this study provide preliminary evidence that (1) American chestnut may have formerly been an important source of food for forest‐dwelling amphibians and (2) transgenic American chestnut litter generated as part of chestnut restoration efforts is unlikely to present direct novel risks to developing amphibian larvae in the forest environment.     

Food habits of the farmer damselfish <Emphasis Type="Italic">Stegastes nigricans</Emphasis> inferred by stomach content,stable isotope,and fatty acid composition analyses

The territorial damselfish, Stegastes nigricans, maintains algal farms by excluding invading herbivores and weeding unpalatable algae from its territories. In Okinawa, Japan, S. nigricans farms are exclusively dominated by Polysiphonia sp., a highly digestible filamentous rhodophyte. This study was aimed at determining the diet of S. nigricans in Okinawa and its dependency on these almost-monoculture algal farms based on stomach content and chemical analyses. Stomach content analyses revealed that all available food items in the algal farms (i.e., algae, benthic animal inhabitants, trapped detritus) were contained in fish stomachs, but amorphous organic matter accounted for 68% of the contents. Therefore, carbon and nitrogen stable isotope ratios and fatty acid (FA) compositions were analyzed to trace items actually assimilated in their bodies. Stable isotope analyses showed that benthic animals were an important food source even for this farmer fish. Two essential fatty acids (EFAs), 20:4n6 and 20:5n3, which are produced only by rhodophytes among available food items, were rich in the muscle tissue of S. nigricans as well as in algal mats and detritus, suggesting that algal mats contribute EFAs to S. nigricans directly and indirectly through the food web. In conclusion, S. nigricans ingested algal mats, detritus, and benthic animals maintained within its farm. Algae and detritus were original sources of EFAs, and benthic animals, which were much more abundant in the farms than in outside territories, provided a nitrogen-rich dietary source for the fish.     

Stoichiometry and food-chain dynamics

Traditional models of chemostat systems looking at interactions between predator, prey and nutrients have used only a single currency, such as energy or nitrogen. In reality, growth of autotrophs and heterotrophs may be limited by various elements, e.g. carbon, nitrogen, phosphorous or iron. In this study we develop a dynamic energy budget model chemostat which has both carbon and nitrogen as currencies, and examine how the dual availability of these elements affects the growth of phytoplankton, trophic transfer to zooplankton, and the resulting stability of the chemostat ecosystem. Both species have two reserve pools to obtain a larger metabolic flexibility with respect to changing external environments. Mineral nitrogen and carbon form the base of the food chain, and they are supplied at a constant rate. In addition, the biota in the chemostat recycle nutrients by means of respiration and excretion, and organic detritus is recycled at a fixed rate. We use numerical bifurcation analysis to assess the model's dynamic behavior. In the model, phytoplankton is nitrogen limited, and nitrogen enrichment can lead to oscillations and multiple stable states. Moreover, we found that recycling has a destabilizing effect on the food chain due to the increased repletion of mineral nutrients. We found that both carbon and nitrogen enrichment stimulate zooplankton growth. Therefore, we conclude that the concept of single-element limitation may not be applicable in an ecosystem context.     

HSS revisited: multi‐channel processes mediate trophic control across a productivity gradient

Classical food web theory holds that energy channels are regulated by top‐down control with increasing productivity, arising from within‐channel processes. However, these hypotheses do not consider the existence of parallel energy channels linked by shared resource pools and which can fuel generalist predators, imposing trophic control arising from multi‐channel processes. Using 23 large marine food webs, we show that food web responses to increasing productivity are consistent with the apparent trophic cascade hypothesis (ATCH) – with rising productivity predators derive an increasing fraction of their diet from increasingly productive bottom‐up controlled detritus channels, thereby subsidising predator biomass, and in turn strengthening top‐down control in parallel grazing channels. These results testify to a fundamental role of detritus channels specifically and multi‐channel processes in general in mediating food web response to productivity and demonstrate that the ATCH provides an alternative explanation for classical predictions of top‐down control.     

Food web structure in Mediterranean streams: exploring stabilizing forces in these ecosystems

We constructed the food webs of six Mediterranean streams in order to determine ecological generalities derived from analysis of their structure and to explore stabilizing forces within these ecosystems. Fish, macroinvertebrates, primary producers and detritus are the components of the studied food webs. Analysis focused on a suite of food web properties that describe species’ trophic habits, linkage complexity and food chains. A great structural similarity was found in analyzed food webs; we therefore suggest average values for the structural properties of Mediterranean stream food webs. Percentage of omnivorous species was positively correlated with connectance, and there was a predominance of intermediate trophic level species that had established simple links with detritus. In short, our results suggest that omnivory and the weak interactions of detritivores have a stabilizing role in these food webs.     

Detritus, trophic dynamics and biodiversity

Traditional approaches to the study of food webs emphasize the transfer of local primary productivity in the form of living plant organic matter across trophic levels. However, dead organic matter, or detritus, a common feature of most ecosystems plays a frequently overlooked role as a dynamic heterogeneous resource and habitat for many species. We develop an integrative framework for understanding the impact of detritus that emphasizes the ontogeny and heterogeneity of detritus and the various ways that explicit inclusion of detrital dynamics alters generalizations about the structure and functioning of food webs. Through its influences on food web composition and dynamics, detritus often increases system stability and persistence, having substantial effects on trophic structure and biodiversity. Inclusion of detrital heterogeneity in models of food web dynamics is an essential new direction for ecological research.     

The fate of cyanobacterial detritus in the food web of Lake Taihu: a mesocosm study using 13C and 15N labeling

The ecosystem of the highly eutrophic Lake Taihu (China) is seriously affected by recurrent cyanobacterial blooms, but little is known about the contribution made by cyanobacteria to the food web. In this study, we investigated the fate of detritus of the cyanobacterium Microcystis in the food web of Lake Taihu through a 19-day mesocosm experiment using stable-isotopic tracers of carbon (¹³C) and nitrogen (¹⁵N). ¹³C- and ¹⁵N-labeled Microcystis detritus was added to the mesocosm tanks and tracked through different elements of the food web. We found clear enrichment with both ¹³C and ¹⁵N in some zooplankton species, including Daphnia, Diaphanosoma, and Sinocalanus, which suggests that these zooplankters can utilize cyanobacterial detritus as a food source. Benthic animals, chironomid larvae and Limnodrilus, also showed pronounced increases in ¹³C and ¹⁵N, but the isotope increase was relatively smaller in the gastropods, Radix sp. and Bellamya sp., implying that they either exploited this food source differently or responded slower than the zooplankton, which apparently grew faster than the snails. Our study suggests that cyanobacterial detritus, originating almost wholly from the bloom-forming Microcystis, is an important food source for both planktonic and benthic food webs in eutrophic lakes such as Lake Taihu.     

The Millennial model: in search of measurable pools and transformations for modeling soil carbon in the new century

Soil organic carbon (SOC) can be defined by measurable chemical and physical pools, such as mineral-associated carbon, carbon physically entrapped in aggregates, dissolved carbon, and fragments of plant detritus. Yet, most soil models use conceptual rather than measurable SOC pools. What would the traditional pool-based soil model look like if it were built today, reflecting the latest understanding of biological, chemical, and physical transformations in soils? We propose a conceptual model—the Millennial model—that defines pools as measurable entities. First, we discuss relevant pool definitions conceptually and in terms of the measurements that can be used to quantify pool size, formation, and destabilization. Then, we develop a numerical model following the Millennial model conceptual framework to evaluate against the Century model, a widely-used standard for estimating SOC stocks across space and through time. The Millennial model predicts qualitatively similar changes in total SOC in response to single factor perturbations when compared to Century, but different responses to multiple factor perturbations. We review important conceptual and behavioral differences between the Millennial and Century modeling approaches, and the field and lab measurements needed to constrain parameter values. We propose the Millennial model as a simple but comprehensive framework to model SOC pools and guide measurements for further model development.     

Relationship between digestive enzymes and food habit of Lutzomyia longipalpis (Diptera: Psychodidae) larvae: Characterization of carbohydrases and digestion of microorganisms

The sandfly Lutzomyia longipalpis (Lutz and Neiva, 1912) is the main vector of American Visceral Leishmaniasis. In spite of its medical importance and several studies concerning adult digestive physiology, biochemistry and molecular biology, very few studies have been carried out to elucidate the digestion in sandfly larvae. Even the breeding sites and food sources of these animals in the field are largely uncharacterized. In this paper, we describe and characterize several carbohydrases from the gut of L. longipalpis larvae, and show that they are probably not acquired from food. The enzyme profile of this insect is consistent with the digestion of fungal and bacterial cells, which were proved to be ingested by larvae under laboratory conditions. In this respect, sandfly larvae might have a detritivore habit in nature, being able to exploit microorganisms usually encountered in the detritus as a food source.     

A computational proposal for designing structured RNA pools for in vitro selection of RNAs

Although in vitro selection technology is a versatile experimental tool for discovering novel synthetic RNA molecules, finding complex RNA molecules is difficult because most RNAs identified from random sequence pools are simple motifs, consistent with recent computational analysis of such sequence pools. Thus, enriching in vitro selection pools with complex structures could increase the probability of discovering novel RNAs. Here we develop an approach for engineering sequence pools that links RNA sequence space regions with corresponding structural distributions via a "mixing matrix" approach combined with a graph theory analysis. We define five classes of mixing matrices motivated by covariance mutations in RNA; these constructs define nucleotide transition rates and are applied to chosen starting sequences to yield specific nonrandom pools. We examine the coverage of sequence space as a function of the mixing matrix and starting sequence via clustering analysis. We show that, in contrast to random sequences, which are associated only with a local region of sequence space, our designed pools, including a structured pool for GTP aptamers, can target specific motifs. It follows that experimental synthesis of designed pools can benefit from using optimized starting sequences, mixing matrices, and pool fractions associated with each of our constructed pools as a guide. Automation of our approach could provide practical tools for pool design applications for in vitro selection of RNAs and related problems.     

The Theory and Applications of Measuring Broad-Range and Chromosome-Wide Recombination Rate from Allele Frequency Decay around a Selected Locus

Recombination is the exchange of genetic material between homologous chromosomes via physical crossovers. High-throughput sequencing approaches detect crossovers genome wide to produce recombination rate maps but are difficult to scale as they require large numbers of recombinants individually sequenced. We present a simple and scalable pooled-sequencing approach to experimentally infer near chromosome-wide recombination rates by taking advantage of non-Mendelian allele frequency generated from a fitness differential at a locus under selection. As more crossovers decouple the selected locus from distal loci, the distorted allele frequency attenuates distally toward Mendelian and can be used to estimate the genetic distance. Here, we use marker selection to generate distorted allele frequency and theoretically derive the mathematical relationships between allele frequency attenuation, genetic distance, and recombination rate in marker-selected pools. We implemented nonlinear curve-fitting methods that robustly estimate the allele frequency decay from batch sequencing of pooled individuals and derive chromosome-wide genetic distance and recombination rates. Empirically, we show that marker-selected pools closely recapitulate genetic distances inferred from scoring recombinants. Using this method, we generated novel recombination rate maps of three wild-derived strains of Drosophila melanogaster, which strongly correlate with previous measurements. Moreover, we show that this approach can be extended to estimate chromosome-wide crossover interference with reciprocal marker selection and discuss how it can be applied in the absence of visible markers. Altogether, we find that our method is a simple and cost-effective approach to generate chromosome-wide recombination rate maps requiring only one or two libraries.     

Terrestrial food web of the Malpelo Fauna and Flora Sanctuary,Colombia: An analysis from a topological approach

Malpelo Island is the largest marine protected area (MPA) in the Colombian Pacific; however, the lack of information regarding its ecological dynamics suggests that management and conservation strategies are developed from an individual approach (species or groups of species) and not from an ecosystem one. This study analyzes the terrestrial food web of Malpelo Island, Colombia, based on topological analysis (e.g., centrality). The food web was constructed from 27 nodes representing the main trophogroups, which consist of species or functional groups. Malpelo Island had a food web of four steps with a maximum separation among all trophogroups and trophic pathways, with two steps in average length. Furthermore, the food web was divided into three food web compartments, with a recurrence of connectivity patterns dominated by apparent and exploitative competition, followed by tri-trophic chains and omnivory. Five key trophogroups control the energy flow throughout the food web (detritus, the land crab Johngarthia malpilensis, the lizard Anolis agassizi, the Malpelo dotted galliwasp Diploglossus millepunctatus, and the Nazca booby Sula granti). The high importance of detritus suggests that bottom-up processes act as a control and regulation mechanism of trophic flows. The low number of food web compartments and a high recurrence of specific connectivity patterns in the Malpelo Island terrestrial ecosystem evidence different ecological processes centered on five trophogroups, allowing stability against disturbances. In addition, the simulation of trophogroup removal (randomly or directed) suggests that food web can be vulnerable to structural alterations in their properties, which may have consequences on the resilience of this ecosystem. This study contributes to the knowledge of the trophic dynamics of Malpelo Island, providing a potential tool for management and conservation measures from an ecosystemic approach.     

Determining biological tissue turnover using stable isotopes: the reaction progress variable

The reaction progress variable is applied to stable isotope turnover of biological tissues. This approach has the advantage of readily determining whether more than one isotope turnover pool is present; in addition, the normalization process inherent to the model means that multiple experiments can be considered together although the initial and final isotope compositions are different. Consideration of multiple isotope turnover pools allows calculation of diet histories of animals using a time sequence of isotope measurements along with isotope turnover pools. The delayed release of blood cells from bone marrow during a diet turnover experiment can be quantified using this approach. Turnover pools can also be corrected for increasing mass during an experiment, such as when the animals are actively growing. Previous growth models have been for exponential growth; the approach here can be used for several different growth models. Electronic Supplementary Material The online version of this article () contains supplementary material, which is available to authorized users.     

Ketocarotenoid circulation,but not retinal carotenoid accumulation,is linked to eye disease status in a wild songbird

Pathogenic or parasitic infections pose numerous physiological challenges to organisms. Carotenoid pigments have often been used as biomarkers of disease state and impact because they integrate multiple aspects of an individual’s condition and nutritional and health state. Some diseases are known to influence carotenoid uptake from food (e.g. coccidiosis) and carotenoid use (e.g. as antioxidants/immunostimulants in the body, or for sexually attractive coloration), but there is relatively little information in animals about how different types of carotenoids from different tissue sources may be affected by disease. Here we tracked carotenoid accumulation in two body pools (retina and plasma) as a function of disease state in free-ranging house finches (Haemorhous mexicanus). House finches in eastern North America can contract mycoplasmal conjunctivitis (Mycoplasma gallisepticum, or MG), which can progress from eye swelling to eye closure and death. Previous work showed that systemic immune challenges in house finches lower carotenoid levels in retina, where they act as photoprotectors and visual filters. We assessed carotenoid levels during the molt period, a time of year when finches uniquely metabolize ketocarotenoids (e.g. 3-hydroxy-echinenone) for acquisition of sexually selected red plumage coloration, and found that males infected with MG circulated significantly lower levels of 3-hydroxy-echinenone, but no other plasma carotenoid types, than birds exhibiting no MG symptoms. This result uncovers a key biochemical mechanism for the documented detrimental effect of MG on plumage redness in H. mexicanus. In contrast, we failed to find a relationship between MG infection status and retinal carotenoid concentrations. Thus, we reveal differential effects of an infectious eye disease on carotenoid types and tissue pools in a wild songbird. At least compared to retinal sources (which appear somewhat more temporally stable than other body carotenoid pools, even to diseases of the eye evidently), our results point to either a high physiological cost of ketocarotenoid synthesis (as is argued in models of sexually selected carotenoid coloration) or high benefit of using this ketocarotenoid to combat infection.     

Examination of the role of detritus food quality,phytoplankton intracellular storage capacity,and zooplankton stoichiometry on planktonic dynamics

Nutrient stoichiometric ratios are primary driving factors of planktonic food web dynamics. Ecological stoichiometry theory postulates the elemental ratios of consumer species to be homeostatic, while primary-producer stoichiometry may vary with ambient nutrient availability. The notion of phytoplankton intracellular storage is far from novel, but remains largely unexplored in modeling studies of population dynamics. We constructed a seasonally-unforced, zero-dimensional, nutrient–phytoplankton–zooplankton–detritus (NPZD) model that considers dynamic phytoplankton phosphorus reserves and quasi-dynamic zooplankton stoichiometry. A generic food quality term is used to express seston biochemical composition, ingestibility, and digestibility. We examined the sensitivity of the planktonic food web patterns to light and nutrient availability, zooplankton mortality, and detritus food quality as well as to phytoplankton intracellular storage and zooplankton stoichiometry. Our results reinforce earlier findings that high quality seston exerts a stabilizing effect on food web dynamics. However, we also found that the combination of low algal and high detritus food quality with high zooplankton mortality yielded limit cycles and multiple steady states, suggesting that the heterogeneity characterizing seston nutritional quality may have more complicated ecological ramifications. Our numerical experiments identify resource competition strategies related to nutrient transport rates and internal nutrient quotas that may be beneficial for phytoplankton to persevere in resource-limiting habitats. We also highlight the importance of the interplay between optimal stoichiometry and the factors controlling homeostatic rigidity in zooplankton. In particular, our predictions show that the predominance of phosphorus-rich and tightly-homeostatic herbivores in nutrient-enriched environments with low seston food quality can potentially result in high phytoplankton abundance, high phytoplankton-to-zooplankton ratios, and acceleration of oscillatory dynamics. Generally, our modeling study emphasizes the impact of both intracellular/somatic storage and food quality on prey–predator interactions, pinpointing an important aspect of food web dynamics usually neglected by the contemporary modeling studies.     

Resource defense in a group-foraging context

When foraging in groups, animals frequently use either scrambleor contest tactics to obtain food at clumps found by others.The question of which competitive tactic should be used hasbeen addressed from two different perspectives: a simple optimalityapproach and a game theoretic approach. Surprisingly, both approachesmake strikingly different predictions about how per-capita frequencyof aggression within groups should change as a function of foodabundance and competitor density. Resource defense theory typicallypredicts dome-shaped relationships between the per-capita frequencyof aggression and both food abundance and competitor density,whereas game theoretic models predict an increase in aggressionwith competitor density and a decline in aggression with increasedfood abundance. We developed a game theoretic model to explorewhether the predictions of resource defense theory and the gametheoretic approach can be reconciled. Our model assumes thatplayers have different competitive abilities and can adopt rolesof either finder or joiner that affect the quantity of foodthat can be gained from a food clump. In accordance with earliergame theoretic models, we predict an increase in aggressionwith competitor density when animals compete by pair-wise contests.However, when food clumps can be challenged by more than onecompetitor, both the costs and benefits of defending increasewith competitor density, which results in a dome-shaped relationshipbetween the two variables. Our model predicts that aggressionshould always decrease as the density of food clumps increases.