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Evaluating the Predicted Local Extinction of a Once‐Common Mouse
Abstract
In an earlier paper (Pergams & Nyberg 2001) we found that the proportion of the prairie deer mouse (Peromyscus maniculatus bairdii), among all local Peromyscus museum specimens collected in the Chicago region, had significantly declined over time. This proportion changed from about 50% before 1900 to <10% in the last 25 years. Based on this proportion a regression model predicted the local extinction of the prairie deer mouse in 2009. To evaluate that prediction, we estimated current deer mouse abundance by live trapping small mammals at 15 preserves in Cook and Lake counties, Illinois (USA) at which prairie deer mice had previously been caught or that still contained their preferred open habitat. In 1900 trap nights, 477 mammals were caught, including 251 white-footed mice (P. leucopus), but only one prairie deer mouse. The observed proportion of Peromyscus that were prairie deer mice, 0.4%, was even lower than the 4.5% predicted for 2000. Here we also introduce a simple, new community proportions model, which for any given geographic region compares the proportions of species recently caught with the proportions of species in museums. We compared proportions of seven species collected in Cook and Lake counties and examined by Hoffmeister (1989) with proportions of these species that we caught. Ten percent of the museum community was prairie deer mice, but only 0.2% of our catch was. The current local scarcity of the prairie deer mouse is consistent with the regression-based prediction of its eminent local extinction. More conservation attention should be paid to changes in relative abundance of once-common species.
... Indeed, a great many species once held to be extremely abundant may increasingly no longer be so. Here we highlight evidence of declines for species in three selected higher taxa (for other examples, see Carrier and Beebee, 2003; Poole and Downing, 2004; Pergams and Nyberg, 2005; Lehtinen and Skinner, 2006 ...
Introduction extract: Species-level conservation activities tend to be focused on those species that are highly threatened with global or regional extinction in the near future. This is broadly logical, if one of the principal goals is to retain as great a proportion of the composition of original species assemblages as possible, within the severe constraints of available conservation resources. In the main, those species which have a high likelihood of rapidly becoming regionally or globally extinct also have small total population sizes and/or restricted geographic ranges within the appropriate region or worldwide (Gaston, 1994; 2003). That is, the importance of each individual organism to the persistence of the species is on average high, and/or there is limited spatial spreading of risk, increasing the vulnerability of the species to quite localized threats.
INTRODUCTION Museum collections represent a valuable tool to understand the response of biotic communities to environmental modifications of human origin (e.g. Pergmans & Nyberg, 2001). Furthermore, natural history collections play an important role in systematic studies, public health and safety, providing a valuable service to the society (Suarez & Tsutsui, 2004). It is therefore essential that collecting efforts continue on a regular basis to monitor environmental changes inside and around the metropolitan areas and that such collections are stored in public museums for future studies. When Rome became the Capital City of Italy in 1870, it covered an area of about 20 km 2 and had a population of about 200,000. Fifty years later Rome had 700,000 inhabitants. A massive expansion of the population and of the urbanised landscape occurred after the Second World War. Actually the study area (around 300 km 2 ; see below) has almost 2,900,000 inhabitants. For a detailed discussion of environmental changes in the Rome area in the last 150 years see Zapparoli (1997). Carlo Luciano Bonaparte was the first who studied mammals in the Roman area. In his 'Iconografia della Fauna Italica' (Bonaparte, 1832-1841) several data are found concerning the presence of some species in the Roman area. However, the first attempt to document the Roman fauna began in 1883, when Antonio Carruccio was designated as director of the Institute of Zoology of the Rome University. He devoted great care in establishing and enriching the collections of local fauna, including mammals, at the relevant Museum of Zoology. After Carruccio's retirement in 1914, most of the collections were loaned to the Rome Municipality to create in 1932 the 'Museo Civico di Zoologia' inside the 'Giardino Zoologico' of Rome, where they are still preserved (Svampa & Gippoliti, 2003). Recent data on the mammals of Rome are provided by Cignini & Zapparoli (1995), Amori et al. (1997) and Zapparoli et al. (2005). For the first time, pre-1945 available museum and literature records are summarised and compared with modern data. Some considerations on local extinctions and conservation of mammal biodiversity are also put forward in the light of the recent European Union commitment to halt biodiversity loss by 2010. MATERIALS AND METHODS In this paper the following main literature record sources were utilised: (i) an unpublished catalogue of the Rome province mammals realised by Giulio Alessandrini (1895), an assistant of Carruccio, which is stored in the 'Museo Civico di Zoologia' of Rome, (ii) the catalogue by Miller (1912), who summarised the data available in the most important foreign and Italian museums. In addition, the mammal collection housed in the 'Museo Civico di Zoologia' of Rome as well as other sparse specimens (private collections) or written reports provided further historical data. It should be noticed that owing to taxonomic problems concerning some closely related species, a number of doubtful records was not considered. Finally, a comparison with the current mammal fauna living in Rome (Amori et al., 1997; Zapparoli et al., 2005) is presented. The study area entirely covers the city of Rome, i.e. an area of about 300 km 2 inside the ring currently corresponding with a circular motorway, the 'Grande Raccordo Anulare' (GRA). The climate of the study area is considered as Mesomediterranean with mild winters and severe summer droughts; a short description of the remaining natural vegetation is found in Ricotta et al. (2001). We assume that historical records simply reporting 'Rome' or 'near Rome' effectively originated from the 300 km 2 within the GRA ring.
The identification and inventory of remnant-dependent or conservative species is an essential prerequisite to sound reserve selection and management in severely fragmented regions. We expanded an ongoing study of insect conservatism to include approximately 1200 additional species on 50 prairie and savanna remnants in the Chicago Wilderness Region (CW). Approximately 700 surveys were conducted from 1995 to 2006, with special emphasis placed on 15 high quality reserves. Our objectives were to: (1) gauge the prevalence of conservatism among remnant-inhabiting insects; (2) determine the status of each conservative species; and (3) gauge the extent that small, isolated sites contribute to the preservation of biodiversity in this landscape. Seventeen percent of 2424 species considered were determined to be narrowly associated with remnant habitats, suggesting that the overall prevalence of conservatism among CW insects is low. One hundred and seventy nine (44%) of these species were rarely or never encountered and are considered to be of conservation concern. Species richness for 15 high quality sites of 2 to 600 ha in area ranged from 39 to 167 species, demonstrating that small, isolated sites contribute appreciably to the preservation of biodiversity in this fragmented landscape. A comparison of vulnerable insect, plant, and vertebrate species richness suggests that conservative insect species far outnumber conservative plant and special-concern vertebrate species, and given their apparent rarity, should play a pivotal role in the establishment of conservation priorities within the CW and probably throughout much of the midcontinental United States.
We report rapid change of morphology and mitochondrial genes in white-footed mice (Peromyscus leucopus) in the Chicago (Illinois, USA) region. We sequenced mitochondrial DNA COX2 from 55 museum skins of white-footed mice caught in the Chicago area since 1855 and from 44 mice recently trapped in the same locations. We found consistent directional genotype replacement at five separate collection locations. We later focused on a single one of these locations (Volo Bog State Natural Area) and sequenced mitochondrial D-loop control region from 58 museum skins of mice collected in 1903-1976 and 32 mice recently trapped there. We found complete and more recent replacement of D-loop haplotypes, apparently occurring between 1976 and 2001. We tested whether these genetic changes were mirrored by changes in morphology by comparing 15 external and cranial traits. We found no significant morphological differences between mice collected in 1903-1976; however, mice collected in 2001-2003 showed 9 of 15 measurements to be significantly changed relative to the earlier samples. Recent mice were longer in total length, with broader, longer noses, and longer but shallower skulls(1). Discriminant function analysis allowed for 100% correct classification using these traits. Principal components analysis shows variance over time is well distributed across both external and cranial measures. The sequential replacements of haplotypes and the rapid change of morphology can best be explained by replacement of the regional population with immigrants from genetically distinct neighbouring populations, likely facilitated by the large environmental changes occurring over the time period. Replacement with genotypes from external populations may be a common mechanism of evolution of newly adaptive local forms in an increasingly human-impacted world.
Experiments were conducted to compare the efficiency of drift-fence pitfalls with three types of snap traps for sampling small mammals and to determine the usefulness of pitfalls for sampling herpetofauna. During winter 1984, small mammal capture rates were lower in pitfalls and Victor rat traps than in Victor mouse traps (P<0.01). During summer and autumn 1984, capture rates in pitfalls were greater than in Victor mouse traps (P<0.01). During winter and summer 1985, capture rates of pitfalls and Museum Specials were similar. Pitfalls with drift fences also captured 220 individual reptiles and amphibians.
The prairie deer mouse (Peromyscus maniculatus bairdii ) was more common than the white-footed mouse (P. leucopus) in museum collections from the 6 Illinois counties of the Chicago region before 1920 but constitutes only 5% of specimens deposited since 1970. Because white-footed mouse prefers woody vegetation and because prairie deer mouse is limited to prairie or large open habitats, the change in proportion is likely driven by a disproportionate loss of prairie among remaining natural habitat and increases in woody vegetation within grasslands. The decline of the prairie vole ( Microtus ochrogaster) relative to the meadow vole (M. pennsylvanicus) and the lack of recent specimens of Franklin's ground squirrel (Spermophilus franklinii) corroborate the hypothesis that prairie habitats have declined much more so than wooded habitats in the Chicago region. Based on ex- tinction models using museum records, it is probable that S. franklinii is already locally extirpated. Regression analysis suggests the white-footed mouse will be the only local Peromyscus in 0-140 years.
Wild mice around Chicago may have switched genotype to keep pace with modern living.
At some time in any study of small mammal populations the investigator is faced with the problem of whether the particular kind of trap used will adequately sample the population. It is common knowledge that exclusive use of one type of trap will tend to bias the estimate of population density due to varying amounts of selectivity in obtaining a population sample, since different types of traps vary in efficiency with respect to numbers, genera and species caught. Trap size and the correlated mechanical sensitivity of the trap also are obviously selective with respect to the size of specimen taken. An apparent avoidance of certain kinds of traps by some genera and species may involve odor, the appearance of the trap to the animal, or trap placement. However, certain anthropocentric concepts are involved here which are difficult to evaluate. Painting traps or camouflaging them in various ways have been used by some to overcome any real or assumed behavior of this sort without giving much quantitative evidence of success. Successful fur-trappers apparently employ these methods with considerable success to overcome reaction of the animal to the trap. There may also be individual variation in response to traps, as suggested by Young et al. (1952), Tanaka (1952, 1956) and Geis (1955), which would, if present, introduce a bias with respect to numbers of particular species trapped. The behavior of individuals and species is thus an important factor to consider in sampling any small mammal population. Although bait preferences (Fitch, 1954) may play an important part in seasonal trap response, they are probably of little importance in determining success of different trap types and use of the same bait in all traps compared at the same season would tend to nullify this factor.
Cockrum (1947) found that live-trapping provided …
Small mammals were collected on six study areas, three of which had been burned (two, four, and 11 times) during the past 15 years and three of which had not been burned for 35 years. Each area was equally productive but the species composition varied, indicating a specific preference for either the brush prairie savanna (created and maintained by burning) or the oak forest (resulting from lack of fire). Peromyscus leucopus noveboracensis and Clethrionomys gapperi gapperi were common in the unburned forest, and Peromyscus maniculatus bairdii and Spermophilus tridecemlineatus tridecemlineatus responded to the prairie created by burning. Burning of the forest did not significantly reduce the numbers of rodents present.
Index trapping with small quadrats in southern Scandinavia, with either only snap or live traps, revealed significantly more trapped animals of Apodemus flavicollis (Melch.), Apodemus sylvaticus (L.) and Sorex araneus (L.) in live traps. The variation due to trap type was in the two latter species greater than variations from summer to autumn. In the voles Microtus agrestis (L.) and Clethrionomys glareolus (Schr.) there was no significant variation due to trap type.
Chaparral fire brings decided changes in the species composition and density of both plant and animal populations in the Sierra Nevada foothills. Some species decrease whereas others increase following a burn, but not species is totally eliminated, nor is there any apparent diminution of total life on a burn after plant growth resumes. These conclusions were reached in the course of a 4-year study of adjoining burnedand unburned areas near Glennville, Kern County, California. Field work began in 1953 at which time study plots were selected and plant and vertebrate population were censused. A year later part of the study area was burned, and ensuing investigation compared populations on the burned and check areas for a period of 3 years, terminating in 1957. At the time of the fire, temperatures were recorded in sites both above and below ground, and the actions of animals were observed. There was very little evidence of direct mortality among any of the vertebrates, most of them escaping the heat in one way or another. The woodrat was perhaps the most vulnerable species because of its dependence on houses made of dry twigs. However, in the bare ash after the fire many species were severely exposed to predation, and populations of the most small mammals and some brush-dwelling birds decreased rapidly. Predatory birds and mammals increased, as did some seed-eating birds that found good foraging on the exposed earth. When the rains stimulated new plant growth, a very different habitat developed in the area of burned chaparral. Most of the original trees sustained little damage, although the pitchy digger pines were largely eliminated. However, the extensive brush stands were reduced by almost 90%, and there was a corresponding increase in invading grasses and forbs. Birds and mammals that normally exhibit a strong preference for chaparral habitat were substantially reduced in numbers in the years following the burn. Conversely, some of the birds that normally prefer grassland or oak woodland increased in number. The fire resulted in an overall increase in densities of nesting birds. None of the small mammals increased in numbers but some of the larger predators, such as the coyote and badger, moved into the burn during the months following the fire.
Changes in populations of small mammals were investigated on four jack pine tracts in northeastern Minnesota. One tract was left uncut, one was cut with slash evenly distributed, and two were cut and subjected to controlled burning. North American census trapping methods were used in July and October for three consecutive years. Populations of deer mice (Peromyscus maniculatus) were significantly higher on burned tracts than on unburned tracts the first and third post-fire years. This increase was related to the supply of seed released by burned jack pine and also other seed exposed in the upper layers of soil, as well as to cover conditions. Since burning created habitat and food conditions favorable to the increase of seed eating mouse species they must be taken into consideration in post-fire reforestation.
Methods for statistical inference about extinction from a record of sightings are described. It is possible to infer a species' extinction from the time of the most recent sighting.
The results are described of comparisons between actual values for patch occupancy for two species of Australian small mammals (Bush Rat Rattus fuscipes and Agile Antechinus Antechinus agilis) determined from field sampling and predictions of patch occupancy made using VORTEX, a generic simulation model for Population Viability Analysis (PVA). The work focussed on a fragmented forest in south-eastern Australia comprised of a network of 39 patches of native eucalypt forest surrounded by extensive stands of exotic softwood Radiata Pine (Pinus radiata) plantation. A range of modelling scenarios were completed in which four broad factors were varied: (1) inter-patch variation in habitat quality; (2) the pattern of inter-patch dispersal; (3) the rate of inter-patch dispersal; and (4) the population sink effects of the Radiata Pine matrix that surrounded the eucalypt patches. Model predictions were made for the total number of animals, the distribution of animal density among patches, the total number of occupied patches, and the probability of patch occupancy. Predictions were then compared with observed values for these same measures based on extensive field surveys of small mammals in the patch system. For most models for the Bush Rat, the predicted relative density of animals per patch correlated well with the values estimated from field surveys. Predictions of patch occupancy were not significantly different from the actual value for the number of occupied patches in half the models tested. The better models explained 10–16% of the log-likelihood of the probability of patch occupancy. While some of the models gave reasonable forecasts of the number of occupied patches, even in these cases, they had only moderate ability to predict which patches were occupied. Field surveys revealed there was no relationship between patch area and population density for the Agile Antechinus—an outcome correctly predicted by only a few models. Five of the 18 scenarios completed for the Agile Antechinus gave predicted numbers of occupied patches not significantly different from the observed number. In each of these five cases, large standard deviations around the mean predicted value meant uncertainty generated by the simulation model limited the predictive power of the PVA. Some of the models gave reasonable predictions for the number of occupied patches, but those models were unable to predict which ones were actually occupied. The results of our study suggest that key processes influencing which specific patches would be occupied were not modelled appropriately. High levels of variability and fecundity drive the population dynamics of the Bush Rat and Agile Antechinus, making the patch system unpredictable and difficult to model accurately. Despite the fact that both the Bush Rat and the Agile Antechinus are two of the most studied mammals in Australia, there are attributes of their biology that are presently poorly understood (which were not included in the VORTEX model), but which could strongly influence patch occupancy. For example, local landscape features may be important determinants of inter-patch movement and habitat utilisation in the patch system. Further empirical studies are needed to explore this aspect of small mammal biology.
Methods for inferring threat from scientific collections were tested using museum records of marsupials and monotremes in south-west Western Australia. A modification of Solow's equation is presented that accounts for changes in collection effort. A runs test, sensitive to runs of zeroes anywhere in the collection record, was only marginally useful for identifying declining and threatened species. The two forms of Solow's equation, a trend analysis based on rank correlation, and a partial trend analysis to account for changes in collection effort, appeared the most promising of the methods tested. The results demonstrated that the use of these methods to infer threat may be useful when expert opinion is limited or not available. In conjunction with other relevant information, it appears that the methods can help to prioritise species on the basis of relative levels of threat.
We studied the use of agricultural landscapes in eastern Ontario, Canada, by white-footed mice Peromyscus leucopus. P. leucopus was common in all patch types except hay and pasture. Densities were similar in woods and in corn Zea mays (maize) fields. Temporal changes in numbers also were similar in crops and woods with low numbers in spring rising to a peak in early autumn. Some mice remained in ploughed corn fields all winter. Monthly turnover of individuals was 75% in areas up to 13·5 ha. Agricultural intensity had little effect on numbers of mice, but did influence the relative use of fencerows by P. leucopus. On low-intensity farms many more mice were captured in fencerows than in crop fields. P. leucopus has adapted to agricultural fields in the landscape mosaic of eastern Ontario.
There is a growing debate about the ability of Population Viability Analysis (PVA) to predict the risk of extinction. Previously, the debate has focused largely on models where spatial variation and species movement are ignored. We present a synthesis of the key results for an array of different species for which detailed tests of the accuracy of PVA models were completed. These models included spatial variation in habitat quality and the movement of individuals across a landscape. The models were good approximations for some species, but poor for others. Predictive ability was limited by complex processes typically overlooked in spatial population models, these being interactions between landscape structure and life history attributes. Accuracy of models could not be determined a priori, although model tests indicated how they might be improved. Importantly, model predictions were poor for some species that are among the best studied vertebrates in Australia. This indicated that although the availability of good life history data is a key part of PVA other factors also influence model accuracy. We were also able to draw broad conclusions about the sorts of populations and life history characteristics where model predictions are likely to be less accurate. Predictions of extinction risk are often essential for real-world population management. Therefore, we believe that although PVA has been shown to be less than perfect, it remains a useful tool particularly in the absence of alternative approaches. Hence, tests of PVA models should be motivated by the cycle of testing and improvement.
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