Trophic cascades and trophic trickles in pelagic food webs

Prey-dependent models, with the predation rate (per predator) a function of prey numbers alone, predict the existence of a trophic cascade. In a trophic cascade, the addition of a top predator to a two-level food chain to make a three-level food chain will lead to increases in the population size of the primary producers, and the addition of nutrients to three-level chains will lead to increases in the population numbers at only the first and third trophic levels. In contrast, ratio-dependent models, with the predation rate (per predator) dependent on the ratio of predator numbers to prey, predict that additions of top predators will not increase the population sizes of the primary producers, and that the addition of nutrients to a three-level food chain will lead to increases in population numbers at all trophic levels. Surprisingly, recent meta-analyses show that freshwater pelagic food web patterns match neither prey-dependent models (in pelagic webs, ''prey'' are phytoplankton, and ''predators'' are zooplankton), nor ratio-dependent models. In this paper we use a modification of the prey-dependent model, incorporating strong interference within the zooplankton trophic level, that does yield patterns matching those found in nature. This zooplankton interference model corresponds to a more reticulate food web than in the linear, prey-dependent model, which lacks zooplankton interference. We thus reconcile data with a new model, and make the testable prediction that the strength of trophic cascades will depend on the degree of heterogeneity in the zooplankton level of the food chain.     

Influence of consumer mutual interference on the stabilization of a three-level trophic system

In this paper, we present a three-level (food–prey–predator) trophic food chain which includes consumer mutual interference (MIF). In contrast with other analyses, we consider the effect of both prey and predator MIF on the dynamics of a three-level trophic system. MIF is generally considered to exert a stabilizing effect on population dynamics based on the predator–prey model. However, results from analytical and numerical simulations utilizing a simple three-species food chain model suggest that while the addition of prey MIF to the model provides a stabilizing influence, as the chaotic dynamics collapse to a stable steady state, adding only predator MIF to the model can only stabilize the system at intermediate MIF values. The three-species trophic food chain is also stabilized when combination of both prey and predator MIF is added to the model. Our work serves to provide insight into the effects of MIF in the real world.     

The otic region of Doleserpeton (Temnospondyli) and its implications for the evolutionary origin of frogs

There is increasing evidence that the Palaeozoic temnospondyl amphibians had a frog‐like tympanic hearing system. For this reason, the otic region of Doleserpeton is described and compared with modern anurans. The otic capsules are expanded laterally and ventrally relative to other temnospondyls. The opisthotic has a bulbous ventral region resembling the ventrolateral ledge in modern frogs. Two lateral processes are located on the paroccipital process. Comparison with the condition in modern anurans with a tympanic hearing system shows that this may have been the attachment site for the tympanic annulus. Parts of the osseous labyrinth are also described. The inner ear shows numerous features resembling the condition found in frogs. These include strong evidence for the presence of a lissamphibian‐type perilymphatic duct most closely resembling that of anurans. This is the first time such a perilymphatic system has been described in any Palaezoic form. The posterior part of the braincase shows a jugular foramen closely associated with the perilymphatic foramen, as in anurans. Although the distribution of these traits among other temnospondyl groups remains little known, the sum of the evidence points to affinities between anurans and temnospondyls, and adds to the evidence for a close relationship between anurans and the Permian amphibamid Doleserpeton. © 2008 The Linnean Society of London, Zoological Journal of the Linnean Society, 2008, 154 , 738–751.     

Evolution of the amphibian tympanic ear and the origin of frogs

Recent anurans plus all but the most primitive temnospondyl labyrinthodont amphibians are proposed as a monophyletic taxon, based on shared stapedial characters which are derived with respect to all other tetrapods. Within temnospondyls, the mostly Lower Permian dissorophoids are proposed as most closely related to Recent anurans, based on interpretation of the dissorophoid dorsal quadrate process and the anuran tympanic annulus as sequential steps in a character transformation series. The otic features described here reinforce the concept of the amphibian tympanic ear as a prior "invention" with no genealogical relationship to amniote tympanic ears.     

Limb‐bone histology of temnospondyls: implications for understanding the diversification of palaeoecologies and patterns of locomotion of Permo‐Triassic tetrapods

The locomotion of early tetrapods has long been a subject of great interest in the evolutionary history of vertebrates. However, we still do not have a precise understanding of the evolutionary radiation of their locomotory strategies. We present here the first palaeohistological study based on theoretical biomechanical considerations among a highly diversified group of early tetrapods, the temnospondyls. Based on the quantification of microanatomical and histological parameters in the humerus and femur of nine genera, this multivariate analysis provides new insights concerning the adaptations of temnospondyls to their palaeoenvironments during the Early Permian, and clearly after the Permo‐Triassic crisis. This study therefore presents a methodology that, if based on a bigger sample, could contribute towards a characterization of the behaviour of species during great evolutionary events.     

Complex dynamics in a three-level trophic system with intraspecies interaction

In this paper, we present a three-level trophic food chain, including intraspecies interaction. In contrast with other analyses, we consider the effect on the third trophic level by the first-level parameters. The model shows complex, as well as, chaotic oscillations. Bifurcation diagrams show period doubling route to chaos and crises. Also from the forward and backwards sections of the bifurcation diagrams, we find hysteresis. This result implies the coexistence of attractors for the same parameter values. In particular, we consider the coexistence of a chaotic and a P1 attractors. Our results show that the regulation in the food chain is not exclusive to either a food-prey or prey-predator interaction, but to a more subtle food-prey-predator interaction, where, for some parameter values, a food-prey or a prey-predator regulation may dominate the system's dynamics. Finally, we consider the impact of the intraspecies interaction in the overall dynamics of the food chain.     

How body size and development biased the direction of evolution in early amphibians

Evolutionary change does not proceed in every direction with equal probability. Evolutionary biases or constraints are limitations on the mode, direction and tempo of evolution. Early tetrapods provide interesting examples, especially Paleozoic and Mesozoic amphibians. (1) Body size had a strong impact on morphology and development in early amphibians, resulting in manifold convergences imposed by design limitations. Miniaturisation had similar effects in a wide range of Paleozoic tetrapods, which are consistent with observations on extant salamanders. Gigantism was a common feature of Triassic temnospondyls, correlating with slow developmental rates similar to those of gigantic salamanders and the convergent evolution of bone density. (2) Ontogeny imposes constraints on evolution by canalised (buffered) developmental sequences. In Paleozoic temnospondyls, ontogenetic trajectories evolved by several different modes (truncation of the trajectory, shifting of events or condensation of events). Metamorphosis is an extreme example of a condensed developmental sequence, which first evolved in Paleozoic temnospondyls, increased in salamanders and culminated in anurans. It imposes strong biases that may be broken by three conceivable modes: (1) loss of the adult period (neoteny), (2) loss of the larval period (direct development) and (3) ‘unpacking’ of metamorphosis by re-evolving the plesiomorphic trajectory.     

A supertree of temnospondyli: cladogenetic patterns in the most species-rich group of early tetrapods

As the most diverse group of early tetrapods, temnospondyls provide a unique opportunity to investigate cladogenetic patterns among basal limbed vertebrates. We present five species-level supertrees for temnospondyls, built using a variety of methods. The standard MRP majority rule consensus including minority components shows slightly greater resolution than other supertrees, and its shape matches well several currently accepted hypotheses of higher-level phylogeny for temnospondyls as a whole. Also, its node support is higher than those of other supertrees (except the combined standard plus Purvis MRP supertree). We explore the distribution of significant as well as informative changes (shifts) in branch splitting employing the standard MRP supertree as a reference, and discuss the temporal distribution of changes in time-sliced, pruned trees derived from this supertree. Also, we analyse those shifts that are most relevant to the end-Permian mass extinction. For the Palaeozoic, shifts occur almost invariably along branches that connect major Palaeozoic groups. By contrast, shifts in the Mesozoic occur predominantly within major groups. Numerous shifts bracket narrowly the end-Permian extinction, indicating not only rapid recovery and extensive diversification of temnospondyls over a short time period after the extinction event (possibly less than half a million years), but also the role of intense cladogenesis in the late part of the Permian (although this was counteracted by numerous 'background' extinctions).     

Hyloidichnus bifurcatus Gilmore, 1927 and Limnopus heterodactylus (King, 1845) from the Early Permian of Southern Alps (N Italy): A New Equilibrium in the Ichnofauna

Studies on Early Permian tetrapod ichnofauna emphasized the scarcity of forms from Italian sites. A revision work on the entire collections revealed the presence of Hyloidichnus bifurcatus Gilmore, 1927 and Limnopus heterodactylus (King, 1845). The ichnoassociation now lists seven ichnogenera: Amphisauropus, Batrachichnus, Dromopus, Erpetopus, Hyloidichnus, Limnopus, Varanopus. These new data enlarge the ichnoceonosis, adding tracks of medium-size captorhinomorphs (Hyloidichnus) and temnospondyls (Limnopus) to the Italian ichnofauna, previously characterized by scarcity of predators and amphibians. Radiometric ages give a strong age constraint to the ichnoassociation (Early Kungurian), allowing useful correlations to contemporary successions all over the world. The main difference is the absence of Ichniotherium and Dimetropus, and this could have a stratigraphic or paleoenvironmental significance. The fauna is similar in two main basins, Collio and Orobic. It differs solely in the proportions between ichnotaxa, with a predominance of areoscelid traces (Dromopus) in the Collio Basin and of captorhinomorph traces (Erpetopus, Varanopus, Hyloidichnus) in the Orobic Basin. This datum could reflect slightly different environments, seasonal in the Collio Basin (alluvial plain) and more arid in the Orobic Basin (playa-like). The lack of some forms in smaller basins of the Athesian Volcanic Complex is probably due to a bias.     

Life cycles,plasticity and palaeoecology in temnospondyl amphibians

In the largest early tetrapod clade, the temnospondyls, ontogenies were diverse and quite distinct from the life cycles of extant amphibians. Three well‐studied clades exemplify the diversity of these long‐extinct ontogenies, here analysed with respect to their bearing on developmental plasticity, reaction norms and evolution. Sclerocephalus readily adjusted by means of developmental evolution to different lake environments. In addition, plasticity (reaction norm) played a significant role, apparent both morphologically and by altered developmental traits. Size increase and extension of the ontogenetic trajectory gave larger predators, a phenomenon also found in the dissorophoid Micromelerpeton. Whereas Sclerocephalus was throughout preying on the same fishes, Micromelerpeton was able to fit into different trophic levels. In the branchiosaurid Apateon, a biphasic life cycle was established, with metamorphosis producing a terrestrial morph in some species; truncation of the ontogenetic trajectory gave a sexually mature larva as an alternative morph (neoteny). Plasticity was high in the larval morphs, permitting neotenes to live as filter feeders or small carnivores. Fine‐tuning of development permitted Apateon populations to adjust to specific lake properties and readily change from a filter‐feeding to carnivorous mode of life. In the nonmetamorphosing Triassic Gerrothorax, morphology was extremely conserved, but histology reveals much plasticity at the microscopical level, correlating with fluctuating salinity and water energy. In responding to environmental fluctuations by enhanced plasticity, the studied temnospondyls managed to populate lakes inhabitable to other tetrapods and fishes.     

Trophic exploitation in grassland food chains: simple models and a field experiment

This study provides insight into the importance of top carnivores (top-down control) and nutrient inputs (bottom-up control) in structuring food chains in a terrestrial grassland system. Qualitative predictions about food chain structure are generated using 4 simple models, each differing in assumptions about some key component in the population dynamics of the herbivore trophic level. The four model systems can be classified broadly into two groups (1) those that assume plant resource intake by herbivores is limited by search rate and handling time as described by classic Lotka-Volterra models; and (2) those that assume plant resource intake by herbivores is limited externally by the supply rate of resources as described by alternatives to Lotka-Volterra formulations. The first class of models tends to ascribe greater importance to top-down control of food chain structure whereas the second class places greater weight on bottom-up control. I evaluated the model predictions using experimentally assembled grassland food chains in which I manipulated nutrient inputs and carnivore (wolf spider) abundance to determine the degree of top-down and bottom-up control of grassland plants and herbivores (grasshoppers). The experimental results were most consistent with predictions of the second class of models implying a predominance of bottom-up control of food chain structure.     

Fish predation regimes modify benthic diatom community structures: Experimental evidence from an in situ mesocosm study

Diatoms are important primary producers in shallow water environments. Few studies have assessed the importance of biological interactions in structuring these communities. In the present study, benthic diatom community structure in relation to manipulated food webs was assessed using in situ mesocosms, whereby predator‐free environments and environments comprising two different fish species were assessed. Zooplankton abundance, settled algal biomass and the diatom community were monitored over a 12‐day period across each of the three trophic scenarios. Differences among treatments over time were observed in zooplankton abundances, particularly copepods. Similarly, the benthic diatom community structure changed significantly over time across the three trophic treatments. However, no differences in total algal biomass were found among treatments. This was likely the result of non‐diatom phytoplankton contributions. We propose that the benthic diatom community structure within the mesocosms was influenced by trophic cascades and potentially through direct consumption by the fish. The study highlights that not only are organisms at the base of the food web affected by predators at the top of the food web, but that predator identity is potentially an important consideration for predator–prey interaction outcomes with consequences for multiple trophic levels.     

New data on synecology of Vyazniki terrestrial community (Terminal Permian,Central Russia)

New materials from terminal Permian localities of the Vyazniki Faunal Assemblage from the eastern Vladimir Region, including a tooth of the proterosuchid Archosaurus rossicus Tatarinov, 1960, which is recorded for the first time in a coprolite, are described. New data on tetrapod coprolites allow a more reliable reconstruction of trophic relationships and reorganization of the trophic structure of this terrestrial community. Interactions of the higher-rank consumers therocephals and early proterosuchid archosaurs were not restricted to competition for food resources, but also included preying of adult representatives of one taxon on juveniles of the other.     

Return time and vulnerability for a food chain model

Simulation studies have shown that the time it takes for a system of interacting species in a food chain to return to equilibrium after a disturbance increases as the number of trophic levels increase. It has been argued that this effect is important in limiting the length of food chains subject to perturbations of the real world. We show that for an asymptotically stable system a lower bound on the return time is directly proportional to the number of trophic levels in agreement with simulation studies. In addition, the lower bound on the return time is shown to be inversely proportional to the sum of products of the intraspecific competition coefficient and equilibrium population of the species. A new method for directly computing the vulnerability of a system to external perturbations is presented. Using this method we demonstrate that for a food chain where the number of species is equal to the number of trophic levels, the return time alone is not a proper measure of system vulnerability. Indeed, adding an additional trophic level may make the system less vulnerable to disturbances. Interspecific coupling between the trophic levels is shown to be an important factor in determining system vulnerability.     

Effects of Multi-chain Omnivory on the Strength of Trophic Control in Lakes

Omnivory has been implicated in both diffusing and intensifying the effects of consumer control in food chains. Some have postulated that the strong, community level, top-down control apparent in lakes is not expressed in terrestrial systems because terrestrial food webs are reticulate, with high degrees of omnivory and diverse plant communities. In contrast, lake food webs are depicted as simple linear chains based on phytoplankton-derived energy. Here, we explore the dynamic implications of recent evidence showing that attached algal (periphyton) carbon contributes substantially to lake primary and secondary productivity, including fish production. Periphyton production represents a cryptic energy source in oligotrophic and mesotrophic lakes that is overlooked by previous theoretical treatment of trophic control in lakes. Literature data demonstrate that many fish are multi-chain omnivores, exploiting food chains based on both littoral and pelagic primary producers. Using consumer-resource models, we examine how multiple food chains affect fourth-level trophic control across nutrient gradients in lakes. The models predict that the stabilizing effects of linked food chains are strongest in lakes where both phytoplankton and periphyton contribute substantially to production of higher trophic levels. This stabilization enables a strong and persistent top down control on the pelagic food chain in mesotrophic lakes. The extension of classical trophic cascade theory to incorporate more complex food web structures driven by multi-chain predators provides a conceptual framework for analysis of reticulate food webs in ecosystems.     

The responses of unstable food chains to enrichment

Summary This article investigates the mean abundances of trophic levels in simple models of two- and three-level food chains as a function of the rate of input of nutrients. The analysis concentrates on cases in which the equilibrium point with all species present is unstable. In most of the models, the instability arises because the consumer species become satiated when food density is high. In unstable two-level systems, bottom level abundance generally increases with increased nutrient input. The abundance of the second level may decrease with increased input. Changes in the intrinsic rate of increase and carrying capacity of the bottom level can have qualitatively opposite effects on trophic level abundances. Refuges for or immigration of the bottom level usually cause both levels to increase in mean abundance with an increased carrying capacity. A variety of different predator—prey models are discussed briefly and the results suggest that increased nutrient input will often increase the abundance of both levels; however, several circumstances can cause the top level to decrease. In three-level systems, an increased carrying capacity can cause extinction of the top level. Extinction may or may not be conditional on the initial densities of the three levels. These results may help explain the observed lack of correlation between productivity and the number of trophic levels in natural food webs, as well as the lack of very long food chains. The results suggest that patterns of abundances across productivity gradients cannot be used to assess the importance of top-down vs bottom-up effects.     

Impact of an introduced Crustacean on the trophic webs of Mediterranean wetlands

Based on a review and our own data, we present an overview of the ecological impacts on the trophic web of Mediterranean wetlands by an introduced Decapod Crustacean, the red swamp crayfish (Procambarus clarkii). P. clarkii lacks efficient dispersal mechanisms but is very well adapted to the ecological conditions of Mediterranean wetlands (fluctuating hydroperiods with regular intervals of drought). As an opportunistic, omnivorous species, which adapts its ecology and life history characteristics, such as timing and size at reproduction to changing environmental conditions, it became readily established in most of the Mediterranean wetland environments. High reproductive output, short development time and a flexible feeding strategy are responsible for its success as an invader. Like most crayfish, it occupies a keystone position in the trophic web of the invaded system and interacts strongly with various trophic levels. It efficiently grazes on macrophytes and is one of the main factors, besides the impact of flamingos, cattle and introduced fish, of the change of many water bodies from a macrophyte dominated, clear water equilibrium to a phytoplankton driven turbid water balance. Juveniles feed on protein rich animal food with the corresponding impact on the macroinvertebrate community in competition with other crayfish or fish species. At the same time, it serves as a prey for mammals, birds and fish. Due to its predatory and grazing activity, it efficiently canalises energy pathways reducing food web complexity and structure. Feeding also on detritus it opens, especially in marshlands, the detritic food chain to higher trophic levels which results in an increase of crayfish predators. As a vector of diseases, it has a severe impact on the preservation and reintroduction of native crayfish. P. clarkii accumulates heavy metals and other pollutants in its organs and body tissues and transmits them to higher trophic levels. Due to the long history of its presence, the complex interactions it established within the invaded ecosystems and the socio-economic benefits it provides to humans, prevention and control seem the most promising management measures to reduce the negative impact of this crayfish species. This revised version was published online in July 2006 with corrections to the Cover Date.     

Model of a coral reef ecosystem

The results of modelling of a coral reef ecosystem at French Frigate Shoals and independent field measures of benthic primary productivity indicate relatively good agreement between food required by consumer trophic levels and organic carbon produced by primary producers. Based upon the high internal predation necessary for the model to match primary production estimates, we reason that the ecosystem is primarily regulated from the top down by forces of predation and that primary production appears to be controlled by nutrients, rate limits, and the distribution of space and habitat. In spite of relatively high primary productivity, potential yield at the top of the food chain is low because of high internal predation and high trophic complexity (6 trophic levels). Fishery yield might be maximized by harvesting low on the food chain particularly if top carnivores can be cropped to release predator pressure on selected prey. Agreement between field measures of metabolism and model (ECOPATH) results provides reasonable confidence that the model can be used as one tool for resource management.     

The impact of thermal seasonality on terrestrial endotherm food web dynamics: a revision of the Exploitation Ecosystem Hypothesis

Many terrestrial endotherm food webs constitute three trophic level cascades. Others have two trophic level dynamics (food limited herbivores; plants adapted to tackle intense herbivory) or one trophic level dynamic (herbivorous endotherms absent, thus plants compete for the few places where they can survive and grow). According to the Exploitation Ecosystems Hypothesis (EEH), these contrasting dynamics are consequences of differences in primary productivity. The productivity thresholds for changing food web dynamics were assumed to be global constants. We challenged this assumption and found that several model parameters are sensitive to the contrast between persistently warm and seasonally cold climates. In persistently warm environments, three trophic level dynamics can be expected to prevail almost everywhere, save the most extreme deserts. We revised EEH accordingly and tested it by compiling direct evidence of three and two trophic level dynamics and by studying the global distribution of felids. In seasonally cold environments, we found evidence for three trophic level dynamics only in productive ecosystems, while evidence for two trophic level dynamics appeared in ecosystems with low primary productivity. In persistently warm environments, we found evidence for three trophic level dynamics in all types of ecosystems. The distribution of felids corroborated these results. The empirical evidence thus indicates that two trophic level dynamics, as defined by EEH, are restricted to seasonally cold biomes with low primary productivity, such as the artic–alpine tundra and the temperate steppe.