Species-specific behavioral patterns correlate with differences in synaptic connections between homologous mechanosensory neurons

We characterized the behavioral responses of two leech species, Hirudo verbana and Erpobdella obscura, to mechanical skin stimulation and examined the interactions between the pressure mechanosensory neurons (P cells) that innervate the skin. To quantify behavioral responses, we stimulated both intact leeches and isolated body wall preparations from the two species. In response to mechanical stimulation, Hirudo showed local bending behavior, in which the body wall shortened only on the side of the stimulation. Erpobdella, in contrast, contracted both sides of the body in response to touch. To investigate the neuronal basis for this behavioral difference, we studied the interactions between P cells. Each midbody ganglion has four P cells; each cell innervates a different quadrant of the body wall. Consistent with local bending, activating any one P cell in Hirudo elicited polysynaptic inhibitory potentials in the other P cells. In contrast, the P cells in Erpobdella had excitatory polysynaptic connections, consistent with the segment-wide contraction observed in this species. In addition, activating individual P cells caused asymmetrical body wall contractions in Hirudo and symmetrical body wall contractions in Erpobdella. These results suggest that the different behavioral responses in Erpobdella and Hirudo are partly mediated by interactions among mechanosensory cells

Neural circuits controlling behavior and autonomic functions in medicinal leeches

In the study of the neural circuits underlying behavior and autonomic functions, the stereotyped and accessible nervous system of medicinal leeches, Hirudo sp., has been particularly informative. These leeches express well-defined behaviors and autonomic movements which are amenable to investigation at the circuit and neuronal levels. In this review, we discuss some of the best understood of these movements and the circuits which underlie them, focusing on swimming, crawling and heartbeat. We also discuss the rudiments of decision-making: the selection between generally mutually exclusive behaviors at the neuronal level

Distributed network organization underlying feeding behavior in the mollusk Lymnaea

The aim of the work reviewed here is to relate the properties of individual neurons to network organization and behavior using the feeding system of the gastropod mollusk, Lymnaea. Food ingestion in this animal involves sequences of rhythmic biting movements that are initiated by the application of a chemical food stimulus to the lips and esophagus. We investigated how individual neurons contribute to various network functions that are required for the generation of feeding behavior such as rhythm generation, initiation ('decision making'), modulation and hunger and satiety. The data support the view that feeding behavior is generated by a distributed type of network organization with individual neurons often contributing to more than one network function, sharing roles with other neurons. Multitasking in a distributed type of network would be 'economically' sensible in the Lymnaea feeding system where only about 100 neurons are available to carry out a variety of complex tasks performed by millions of neurons in the vertebrate nervous system. Having complementary and potentially alternative mechanisms for network functions would also add robustness to what is a 'noisy' network where variable firing rates and synaptic strengths are commonly encountered in electrophysiological recording experiments

An Emerging Infectious Disease Triggering Large-Scale Hyperpredation

Hyperpredation refers to an enhanced predation pressure on a secondary prey due to either an increase in the abundance of a predator population or a sudden drop in the abundance of the main prey. This scarcely documented mechanism has been previously studied in scenarios in which the introduction of a feral prey caused overexploitation of native prey. Here we provide evidence of a previously unreported link between Emergent Infectious Diseases (EIDs) and hyperpredation on a predator-prey community. We show how a viral outbreak caused the population collapse of a host prey at a large spatial scale, which subsequently promoted higher-than-normal predation intensity on a second prey from shared predators. Thus, the disease left a population dynamic fingerprint both in the primary host prey, through direct mortality from the disease, and indirectly in the secondary prey, through hyperpredation. This resulted in synchronized prey population dynamics at a large spatio-temporal scale. We therefore provide evidence for a novel mechanism by which EIDs can disrupt a predator-prey interaction from the individual behavior to the population dynamics. This mechanism can pose a further threat to biodiversity through the human-aided disruption of ecological interactions at large spatial and temporal scales.MM and JASZ were partially supported by a project of the Spanish Ministerio de Educación y Ciencia (reference CGL-2006-10689/BOS)

A two-neuron system for adaptive goal-directed decision-making in Lymnaea

During goal-directed decision-making, animals must integrate information from the external environment and their internal state to maximize resource localization while minimizing energy expenditure. How this complex problem is solved by the nervous system remains poorly understood. Here, using a combined behavioural and neurophysiological approach, we demonstrate that the mollusc Lymnaea performs a sophisticated form of decision-making during food-searching behaviour, using a core system consisting of just two neuron types. The first reports the presence of food and the second encodes motivational state acting as a gain controller for adaptive behaviour in the absence of food. Using an in vitro analogue of the decision-making process, we show that the system employs an energy management strategy, switching between a low- and high-use mode depending on the outcome of the decision. Our study reveals a parsimonious mechanism that drives a complex decision-making process via regulation of levels of tonic inhibition and phasic excitation

On the Dynamics of the Spontaneous Activity in Neuronal Networks

Most neuronal networks, even in the absence of external stimuli, produce spontaneous bursts of spikes separated by periods of reduced activity. The origin and functional role of these neuronal events are still unclear. The present work shows that the spontaneous activity of two very different networks, intact leech ganglia and dissociated cultures of rat hippocampal neurons, share several features. Indeed, in both networks: i) the inter-spike intervals distribution of the spontaneous firing of single neurons is either regular or periodic or bursting, with the fraction of bursting neurons depending on the network activity; ii) bursts of spontaneous spikes have the same broad distributions of size and duration; iii) the degree of correlated activity increases with the bin width, and the power spectrum of the network firing rate has a 1/f behavior at low frequencies, indicating the existence of long-range temporal correlations; iv) the activity of excitatory synaptic pathways mediated by NMDA receptors is necessary for the onset of the long-range correlations and for the presence of large bursts; v) blockage of inhibitory synaptic pathways mediated by GABA(A) receptors causes instead an increase in the correlation among neurons and leads to a burst distribution composed only of very small and very large bursts. These results suggest that the spontaneous electrical activity in neuronal networks with different architectures and functions can have very similar properties and common dynamics

Maladaptive Habitat Selection of a Migratory Passerine Bird in a Human-Modified Landscape

In human-altered environments, organisms may preferentially settle in poor-quality habitats where fitness returns are lower relative to available higher-quality habitats. Such ecological trapping is due to a mismatch between the cues used during habitat selection and the habitat quality. Maladaptive settlement decisions may occur when organisms are time-constrained and have to rapidly evaluate habitat quality based on incomplete knowledge of the resources and conditions that will be available later in the season. During a three-year study, we examined settlement decision-making in the long-distance migratory, open-habitat bird, the Red-backed shrike (Lanius collurio), as a response to recent land-use changes. In Northwest Europe, the shrikes typically breed in open areas under a management regime of extensive farming. In recent decades, Spruce forests have been increasingly managed with large-size cutblocks in even-aged plantations, thereby producing early-successional vegetation areas that are also colonised by the species. Farmland and open areas in forests create mosaics of two different types of habitats that are now occupied by the shrikes. We examined redundant measures of habitat preference (order of settlement after migration and distribution of dominant individuals) and several reproductive performance parameters in both habitat types to investigate whether habitat preference is in line with habitat quality. Territorial males exhibited a clear preference for the recently created open areas in forests with higher-quality males settling in this habitat type earlier. Reproductive performance was, however, higher in farmland, with higher nest success, offspring quantity, and quality compared to open areas in forests. The results showed strong among-year consistency and we can therefore exclude a transient situation. This study demonstrates a case of maladaptive habitat selection in a farmland bird expanding its breeding range to human-created open habitats in plantations. We discuss the reasons that could explain this decision-making and the possible consequences for the population dynamics and persistence

Habitat-Specific Population Growth of a Farmland Bird

BACKGROUND: To assess population persistence of species living in heterogeneous landscapes, the effects of habitat on reproduction and survival have to be investigated. METHODOLOGY/PRINCIPAL FINDINGS: We used a matrix population model to estimate habitat-specific population growth rates for a population of northern wheatears Oenanthe oenanthe breeding in farmland consisting of a mosaic of distinct habitat (land use) types. Based on extensive long-term data on reproduction and survival, habitats characterised by tall field layers (spring- and autumn-sown crop fields, ungrazed grasslands) displayed negative stochastic population growth rates (log lambda(s): -0.332, -0.429, -0.168, respectively), that were markedly lower than growth rates of habitats characterised by permanently short field layers (pastures grazed by cattle or horses, and farmyards, log lambda(s): -0.056, +0.081, -0.059). Although habitats differed with respect to reproductive performance, differences in habitat-specific population growth were largely due to differences in adult and first-year survival rates, as shown by a life table response experiment (LTRE). CONCLUSIONS/SIGNIFICANCE: Our results show that estimation of survival rates is important for realistic assessments of habitat quality. Results also indicate that grazed grasslands and farmyards may act as source habitats, whereas crop fields and ungrazed grasslands with tall field layers may act as sink habitats. We suggest that the strong decline of northern wheatears in Swedish farmland may be linked to the corresponding observed loss of high quality breeding habitat, i.e. grazed semi-natural grasslands

Identifying and Prioritizing Greater Sage-Grouse Nesting and Brood-Rearing Habitat for Conservation in Human-Modified Landscapes

BACKGROUND: Balancing animal conservation and human use of the landscape is an ongoing scientific and practical challenge throughout the world. We investigated reproductive success in female greater sage-grouse (Centrocercus urophasianus) relative to seasonal patterns of resource selection, with the larger goal of developing a spatially-explicit framework for managing human activity and sage-grouse conservation at the landscape level. METHODOLOGY/PRINCIPAL FINDINGS: We integrated field-observation, Global Positioning Systems telemetry, and statistical modeling to quantify the spatial pattern of occurrence and risk during nesting and brood-rearing. We linked occurrence and risk models to provide spatially-explicit indices of habitat-performance relationships. As part of the analysis, we offer novel biological information on resource selection during egg-laying, incubation, and night. The spatial pattern of occurrence during all reproductive phases was driven largely by selection or avoidance of terrain features and vegetation, with little variation explained by anthropogenic features. Specifically, sage-grouse consistently avoided rough terrain, selected for moderate shrub cover at the patch level (within 90 m(2)), and selected for mesic habitat in mid and late brood-rearing phases. In contrast, risk of nest and brood failure was structured by proximity to anthropogenic features including natural gas wells and human-created mesic areas, as well as vegetation features such as shrub cover. CONCLUSIONS/SIGNIFICANCE: Risk in this and perhaps other human-modified landscapes is a top-down (i.e., human-mediated) process that would most effectively be minimized by developing a better understanding of specific mechanisms (e.g., predator subsidization) driving observed patterns, and using habitat-performance indices such as those developed herein for spatially-explicit guidance of conservation intervention. Working under the hypothesis that industrial activity structures risk by enhancing predator abundance or effectiveness, we offer specific recommendations for maintaining high-performance habitat and reducing low-performance habitat, particularly relative to the nesting phase, by managing key high-risk anthropogenic features such as industrial infrastructure and water developments