Mechanisms of species persistence in fragmented landscapes: A demographic field study on four rodent species

Habitat loss and fragmentation are key drivers of global species loss. In fragmented landscapes species must persist in small, isolated and often degraded habitat patches where they can be subject to high risk of extinction due to deterministic and stochastic forces. Species respond to habitat fragmentation according to species-specific life-history traits, with habitat generalist, edge or mobile species being less impacted compared to specialists and less mobile species. The impact of habitat fragmentation on species and their consequent probability of persistence depends on a series of key, concatenated events occurring at different biological and spatial scales. The response of single individuals to landscape change can translate into effects at the level of populations; coexisting species can reciprocally influence their responses through the alteration of interspecific relationships; inter-population dynamics can also occur, involving the movement of individuals between populations in different habitat fragments and affecting the persistence of entire systems of populations. Given the complexity of factors involved, including direct and interacting responses, it is extremely difficult to understand the actual effects triggered by habitat fragmentation without a thorough knowledge of the underlying ecological mechanisms. The aim of this PhD project was to contribute to understanding the mechanisms underlying the response of species to habitat fragmentation. By following a holistic approach, I used a set of mechanistic field studies on four rodent species specifically designed to investigate the series of key events involved in the persistence of species in fragmented landscapes: 1) Population and individual scale responses of small mammals to patch size, isolation and quality. The aim of this section was to determine the relative effects of landscape structure (habitat amount and configuration) and patch quality (here measured as abundance of shrub resources) on individuals (survival and litter size) and populations (density and colonization/extinction dynamics). A large-scale demographic field study was conducted, encompassing 30 woodland sites nested within three landscapes and surveyed monthly for three years by means of a capture-mark-recapture protocol. Model species was an arboreal rodent, the hazel dormouse (Muscardinus avellanarius), known to be sensitive to habitat loss and fragmentation. Habitat quality influenced populations at different biological scales by concatenated effects: it enhanced individual survival, increased the chances of colonizing vacant patches and sustained higher population densities. It was therefore related to the performance of single populations and systems of populations through re-colonization dynamics. Habitat quality, however, did not influence local extinction probability, which was ultimately related to the extent of available habitat, likely due to the absolute size of populations: a high absolute number of individuals reduces the chances of population extinction. 2) The role of interspecific interactions in shaping small mammal communities in fragmented landscapes. The aim of this section was to evaluate the strength of interspecific interactions as a shaping force of animal communities in fragmented landscapes. A large-scale demographic field study was conducted to measure the degree of competitive interference between species. Model system was constituted by the community of forest-dwelling ground rodents of central Italy, including the species Apodemus sylvaticus, Apodemus flavicollis and Myodes glareolus. Populations, inhabiting 29 wood patches in a fragmented landscape, were surveyed for two years by means of a capture-mark-recapture protocol. I modeled species' distribution as a function of landscape (habitat cover and connectivity provided by hedgerows) and habitat variables (vegetation structure and food resources) to look for evidences of competitive spatial segregation. Then I tested for each species the effect of competitors on several biological parameters: survival, recruitment, reproduction, body mass, population density. Even though populations' relative distribution was consistent with a mechanism of competitive spatial segregation, with habitat specialists being favored by high-quality, well-connected fragments and generalists exploiting more isolated and degraded patches, results on demographic parameters did not fully confirm this result. The strongest competitive effects were exerted by A. sylvaticus on A. flavicollis, whereas a little degree of interference was found between Apodemus spp. and M. glareolus. Nevertheless, competitive effects were weak, acting on a few biological parameters and not translating into strong effects at the level of populations (density of individuals). These results suggest that populations were mainly distributed according to their ecological requirements; competitive exclusion of specialists from isolated and degraded fragments was actually acting but was likely to play a minor role in determining the observed pattern of distribution. 3) Perceptual range and movement ability of small mammals in fragmented landscapes. The aim of this section was to broaden our understanding of animal orientation and movements in the agricultural matrix, with a special attention on the use of plantation rows as navigation cues. Experiments consisted in releasing individuals of forest-dwelling small mammals (species A. flavicollis, A. sylvaticus, M. glareolus) in fields characterized by different types of matrices: a bare field, a grass field with random pattern of vegetation, and a wheat field at three different stages of growth. Animals (N=119) were marked with fluorescent powder and released at progressive distances from target wood fragments; in this type of experiments individuals are assumed to go directly toward the wood as soon as they perceive it. Animal tracks were then analyzed to determine perceptual ranges and movement abilities. Perceptual ranges were species-specific, with habitat specialists perceiving woods at smaller distances compared to generalists. The presence of vegetation in the fields (either grass or wheat) strongly reduced perceptual ranges of all species by obstructing individuals' view. Furthermore, wheat plantation rows drastically influenced animal movements, possibly facilitating or hampering the reaching of a wood. Individuals of all species, in fact, followed the direction of wheat rows at any stage of growth, even if they were not directed toward the target wood. This study is one of the few examples investigating in detail the demographic mechanisms of response of species to habitat fragmentation. The holistic approach allowed me to provide an overview on the process by which factors such as landscape features, habitat characteristics, and co-occurring species affect the performance of populations in fragmented landscapes. Interspecific interactions play a minor role in shaping the community of small mammals in the studied system. A major role, instead, is played by landscape characteristics (such as habitat cover, connectivity, matrix properties) and local features (such as food resources and habitat structure), in both cases depending on species-specific life-history traits. Increased individual performance (e.g. due to habitat quality) can help to increase the viability of systems of populations; at the same time animals are constrained by the physical structure of the landscape where they live, and individual-scale effects are not necessarily transferred to the level of population. Results suggest that in order to increase the viability of animal systems in fragmented landscapes there is the need to manage the quality of habitat, which proves to be a major determinant of animal populations' performance. Nevertheless, findings also strongly suggest not to ignore the overall landscape context where populations are embedded. In landscapes that have been extensively cleared, restoration aimed to increase the amount of habitat and management of outside-patch landscape elements (hedgerows, agricultural fields) might also be a critical step to ensure the persistence of animal communities

Population and individual-scale responses to patch size, isolation and quality in the hazel dormouse

Patch size, isolation and quality are key factors influencing species persistence in fragmented landscapes. However, we still lack a detailed understanding of how these variables exert their effects on populations inhabiting fragmented landscapes. At which ecological scale do they have an effect (e.g., individuals versus populations) and, on which demographic parameters? Answering these questions will identify the mechanisms that underlie population turnover rather than solely predicting it based on proxies (e.g., presence/absence data). We report the results of a large-scale, three-year study focused on the relative effects of patch size, isolation and quality on individuals and populations of an arboreal rodent, the hazel dormouse (Muscardinus avellanarius). We examined 30 sites nested within three landscapes characterized by contrasting levels of habitat amount and habitat quality (food resources). We quantified the effects of patch size and quality on the response of individuals (survival and litter size) and populations (density and colonization/extinction dynamics). We identified demographic mechanisms which led to population turnover. Habitat quality positively affected survival (not litter size) and population density (measured through an index). We infer that the decline in survival due to patch quality reduced patch recolonization rather than increasing extinction, while extinction was mainly affected by patch size. Our findings suggest that the effect of patch quality on individual and population parameters was constrained by the physical structure of the surrounding landscapes. At the same time, our results highlight the importance of preserving habitat quality to help the persistence of entire systems of patches

Empirical evaluation of the strength of interspecific competition in shaping small mammal communities in fragmented landscapes

Context: Theory predicts that habitat loss and fragmentation may have drastic consequences on species’ interactions. To date, however, little empirical evidence exists on the strength of interspecific competition in shaping animal communities in fragmented landscapes. Objectives: Our aim was to measure the degree of ongoing competitive interference between species in fragmented landscapes. Our model system was the community of ground-dwelling rodents in deciduous woodlands in central Italy, composed of a habitat generalist species (Apodemus sylvaticus) and two forest specialists (Apodemus flavicollis and Myodes glareolus). Our objectives were to test whether species were segregated among forest patches and whether spatial segregation was determined by interspecific competition or habitat and resource availability. Methods: We surveyed the populations inhabiting 29 woodland patches in a highly fragmented landscape using a capture-mark-recapture protocol, capturing >4500 individuals. First we modelled species’ distribution as a function of habitat, resource availability and landscape variables. The second stage of our analyses involved measuring the response of vital rate parameters (body mass, reproduction, survival, recruitment, population density) to competitor density. Results: The relative distribution of species reflected a spatial segregation of habitat generalists and specialists according to habitat quality, cover and connectivity. Interspecific competition mainly affected individual level vital rates, whereas we found no substantial effects at the population level. Conclusions: Competitive exclusion of specialist species by generalist species was occurring. However, when compared to other factors such as habitat connectivity and resource availability, interspecific competition played a relatively minor role in shaping the studied community

Mice on the move: wheat rows as a means to increase permeability in agricultural landscapes

A crucial factor in determining the persistence of animal populations in fragmented landscapes is the individual’s ability to move through a hostile man-made environment (the agricultural matrix). Previous studies suggested appropriate orientation of manioc plantation rows as a possible means to facilitate animal movements and to increase landscape functional connectivity. The goal of our work was to broaden our understanding of plantation rows as a means to increase permeability in cereal-crop-dominated landscapes. In particular, we focused on (a) analyzing animals’ ability to localize and move towards habitat fragments in different matrix types (i.e. their perceptual ranges) and (b) testing whether the orientation of wheat rows acted as dispersal route during three stages of the wheat plant maturation. We carried out release experiments in an agricultural landscape of central Italy on three species of rodents: two forest specialists (Apodemus flavicollis and Myodes glareolus) and a habitat generalist (Apodemus sylvaticus). We released individuals in three matrix types (a bare field, a grass field and a wheat field at three maturation stages) and followed their movements. We found that (a) perceptual ranges were species- and matrix-specific, (b) individuals followed plantation rows when moving through the matrix at any stage of wheat growth, including recently planted wheat, (c) in the grass field individuals did not follow any preferential direction. These results provide strong empirical evidence that wheat plantation rows should be planted orientated between habitat patches and should be considered as a complementary conservation strategy to increase connectivity in agricultural landscapes

Mice on the move: Wheat rows as a means to increase permeability in agricultural landscapes

A crucial factor in determining the persistence of animal populations in fragmented landscapes is the individual's ability to move through a hostile man-made environment (the agricultural matrix). Previous studies suggested appropriate orientation of man

Ultrasonic communication in Gliridae (Rodentia): the hazel dormouse (Muscardinus avellanarius) as a case study

Ultrasonic vocalizations (USVs) have been detected in a range of small mammals, particularly rodents, and are associated not only with different social behaviours, e.g. sexual behaviour and aggression, but also with non-social behaviour in several species of mammals, including echolocation and as a by-product of respiration. Rodents in the Gliridae family are known to broadcast a variety of signals, but the behavioural relevance of the latter is poorly known. The aim of our study was to describe the vocal signals of Muscardinus avellanarius and to assess their function. By recording vocal and non-vocal behaviour of captive individuals in different social contexts, we demonstrate that M. avellanarius emits USVs and provide contextual evidence that such sounds are largely used for social communication. We identified six different vocalizations with an overall frequency range between 6.5 and 52.1 kHz, five out of six being ultrasonic (>18 kHz). The vocal repertoire in M. avellanarius was associated with social behaviours, e.g. mother-infant reunion, isolation and paired opposite-sex courtship, all activities involving individuals that are out of mutual visual contact. We therefore infer that this repertoire constitutes a medium-distance (in the range of a few metres) communication system. Further research testing different social contexts both in nature and in captivity is needed for a more complete assessment of the vocal repertoire of this species and its function

Long distance field crossings by hazel dormice (Muscardinus avellanarius) in fragmented landscapes

The hazel dormouse (Muscardinus avellanarius) is an arboreal species with suspected limited capabilities Of moving over open ground. To date, however, only one study has investigated gap crossing capabilities in an experimental manner. We here report the results of an empirical assessment of hazel dormice gap crossing capabilities by means of a translocation study. We translocated 12 dormice, 10 in completely isolated patches and 2 in a hedgerow. Our results show how, at least under conditions of an experimental homing, hazel dormice may abandon forest areas and cross open fields (with grass or mowed) travelling up to 106 m. In most cases the gap crossing was relatively quick (concluded within one night) but in one case it lasted several days. The results of our experiment suggest that a stepping stone approach to connectivity may be a possible management strategy where it is not possible to implement a continuous network of hedgerows. (C) 2012 Deutsche Gesellschaft fur Saugetierkunde. Published by Elsevier GmbH. All rights reserved

Conservation of species occupying ephemeral and patchy habitats in agricultural landscapes: The case of the Eurasian Reed Warbler

Habitat loss and fragmentation are amongst the main threats for animal populations. These two processes are mainly due to the conversion of natural habitats to agroecosystems and have effects at different spatial scales. The identification of their lands