Distribution of rodents in northern Michigan documented by Dr. Phil Myers, et al.
We use museum and other collection records to document large and extraordinarily rapid changes in the ranges and relative abundance of 9 species of mammals in the northern Great Lakes region (white-footed mice, woodland deer mice, southern red-backed voles, woodland jumping mice, eastern chipmunks, least chipmunks, southern flying squirrels, northern flying squirrels, common opossums). These species reach either the southern or the northern limit of their distributions in this region. Changes consistently reflect increases in species of primarily southern distribution (white-footed mice, eastern chipmunks, southern flying squirrels, common opossums) and declines by northern species (woodland deer mice, southern red-backed voles, woodland jumping mice, least chipmunks, northern flying squirrels). White-footed mice and southern flying squirrels have extended their ranges over 225 km since 1980, and at particularly well-studied sites in Michigan’s Upper Peninsula, small mammal assemblages have shifted from numerical domination by northern species to domination by southern species. Repeated re-sampling at some sites suggests that southern species are replacing northern ones rather than simply being added to the fauna. Observed changes are consistent with predictions from climatic warming but not with predictions based on recovery from logging or changes in human populations. Because of the abundance of these focal species (the 8 rodent species make up 96.5% of capture records of all forest-dwelling rodents in the region and 70% of capture records of all forest-dwelling small mammals) and the dominating ecological roles they play, these changes substantially affect the composition and structure of forest communities. They also provide an unusually clear example of change that is likely to be the result of climatic warming in communities that are experienced by large numbers of people.
We chose this assemblage of 8 species of small forest rodents for 4 reasons. First, each species reaches a distributional limit within or close to the northern Great Lakes region. Second, each is commonly captured by the techniques most widely used by collectors. Records of other species are available but were acquired through the use of trapping or hunting techniques that have not been employed consistently across the 150 years of collecting in this region (e.g., firearms and large traps are seldom used in recent collections, and mist nets for the capture of bats did not become available until the last half of the 20th century). Third, we focused on woodland species because trapping since 1980 has concentrated heavily on forest habitats, and consequently their record is stronger than that of mammal assemblages in other habitats. Fourth, these species are relatively common and frequently captured, often in the same trap-lines. We did not consider a few species that are extremely rare in the region (e.g., woodland voles, Microtus pinetorum) or that seldom enter woodlands (southern bog lemmings, Synaptomys cooperi; meadow voles, Microtus pennsylvanicus; grassland jumping mice, Zapus hudsonius).
Additionally, we report widespread changes in the distribution of common opossums. Opossums are a southern species whose range has extended gradually northwards since the early 20th century (Gardner & Sundquist, 2003).
Records from 1978-2008 came primarily from extensive live-trap sampling by field crews from the University of Michigan, Michigan State University, and Miami University. The purpose of these surveys was to document the current distribution and relative abundance of species of small mammals, and all captures were recorded. In almost all cases localities are believed to be accurate to within less than 500 m (Appendix). Questionable species identifications were confirmed using molecular techniques (Appendix). When identifications could not be confirmed, animals not readily identified using field characters were eliminated from the analysis (64 out of 10,273 Peromyscus and 11 out of 293 Glaucomys were deleted).
Recent opossum records were based on field observations and especially, records of road-killed animals made from 2006-present. Coordinates of road-killed animals were recorded using a GPS unit.
Most records prior to 1978 came from the specimens and field notes housed in the University of Michigan Museum of Zoology and the Michigan State University Museum. Additional specimen records were obtained from the MaNIS network http://www.manisnet.org (Appendix). Error in estimating locality coordinates varied widely (Appendix). We examined the estimated error associated with the coordinates of each specimen with the intent of eliminating records whose error overlapped either previously reported range limits or boundaries of the geographic regions on which comparisons of community composition are based (Appendix). A few records were not mapped because their estimated errors were extremely large, but in every case specimens were unambiguously assignable to one of the geographic regions of the study. For some critical records with uncertain localities, we were able to reduce estimated error considerably by referring to field notes and/or published descriptions of collecting expeditions.
We examined and verified the identifications of all museum specimens that suggested significant changes in distribution.
A few records were also provided by individual collectors or taken from published papers. In most cases they involve unexpected findings, usually occurrences outside of the normal range of a species (e.g., Ozoga & Verme, 1966; Haveman, 1976; Stormer & Sloane, 1976; Wells-Gosling, 1982). These records provide documentation of range expansion and are included below in maps and calculation of range change, but as no information was usually provided on what other species were trapped, these records were excluded from analyses of faunal composition.
Published range maps of species of mammals in Michigan suggest a transition between a fauna associated with the oak hickory woodlands and savannahs typical of the southern part of the state, and a northern fauna associated with northern hardwood and coniferous forests (Hall, 1981; Baker, 1983). At the time these maps were compiled, northern and southern faunas met in the middle of the Lower Peninsula, in a region (“tension zone”) that is characterized by differences in soils and a transition from a more southern to a more boreal flora (Fig. 1; Medley & Harman, 1987). Our focus is on changes concentrated to the north of this zone, and consequently we restricted our attention to records north of 44oN latitude (Fig. 1).
A number of islands are found in Lakes Michigan, Superior, and Huron. Many are inhabited by small mammals, and extensive collection records are available for some. These islands have little or no opportunity to receive immigrants from the mainland, and the composition of their fauna likely reflects the species present when the islands were isolated by rising water as the lakes first formed, nearly 10,000 years ago. Records from islands separated from the mainland by at least 10 km (Beaver, High, Hog, Timm’s, Squaw, Whiskey, Trout, Gull, Garden, N and S Manitou, N and S Fox, Bois Blanc, Isle Royale) were not considered in this analysis. Further, we eliminated 4 sites in the northern Lower Peninsula, because since 1978 they were visited repeatedly, often several times a year, to obtain specimens or to follow the populations of particular species. Including them would have strongly biased the analyses in the direction of conditions at those sites, and for inferences concerning regional community composition, would represent a form of pseudoreplication (Hurlbert, 1984). These sites (and the area each encompasses) are as follows (Fig. 1):
1) 45.168 – 45.1775oN, 84.375 - 84.401oW (2.1 km2)
2) 45.088 – 45.1147 oN, 84.402 – 84.425 oW (5.34 km2)
3) 45.271 – 45.296 oN, 84.416 - 84.443 oW (5.88 km2)
4) 3 line transects, 300-500 m in length, at the University of Michigan Biological Station: 45.546°N, 84.667°W; 45.5567°N, 84.7015°W’; 45.4894°N, 84.6849°W.
Repeated collections made at a few sites in the Huron Mountains are especially informative. The Huron Mountains are a series of low granitic hills (maximum elevation 600 m) near the Lake Superior shoreline in the central Upper Peninsula of Michigan (Fig. 1). Approximately 7,300 ha are owned by a private association, the Huron Mountain Club, whose members support research on their property through the Huron Mountain Wildlife Foundation. This area includes a 2600 ha Nature Research Area of primary (never logged) forest. The Huron Mountain Wildlife Foundation has funded 3 surveys of the mammals of the region. The first, a comprehensive survey of vertebrates by Richard Manville, was carried out from autumn 1939 through summer 1942 (Manville, 1947, 1949). To sample small mammal populations, Manville set up 8 quadrats chosen to represent the habitats of the region. Each quadrat comprised an 11 x 11 trapping grid (30 ft between traps). Manville used live traps and trapped for 5 consecutive days 4 times over the course of the study. He deposited extensive series of voucher specimens in the collections of the University of Michigan Museum of Zoology, and we have confirmed his identifications of Peromyscus. In 1972-1973, John Laundre also conducted small mammal censuses in the Huron Mountains, trapping at or near the same locations as Manville and using similar techniques (Laundre, 1975). Unfortunately, his report does not list numbers of individuals of most species captured, and we are therefore unable to include his records in the analyses of relative abundance reported here. Nor have we been able to locate voucher specimens. His account, however, is useful in documenting the presence/absence of species in 1972-3 compared to other time periods. In 2004-2005, the survey was repeated by Allison Poor (Poor, 2005). Poor used live-trapping techniques similar to those of Manville and Laundre and located most of her quadrats at or very close to the same sites. Poor, however, trapped for 3 days/sampling period, taking 2 samples in 2004 and 1 in 2005. Like Manville, she recorded all captures, and she deposited vouchers (mainly tissue samples) in the University of Michigan Museum of Zoology.
Preliminary examination of maps and capture records suggested that for small mammals, change in distributional patterns accelerated during the late 20th century. While these preliminary results also suggested some differences among species in the timing of change, to simplify comparisons of SFR assemblages we arbitrarily chose to compare collections made from 1883 (when the first records were obtained) through 1980 with those made from 1981 to the present.
A total of 14,076 records of the 8 focal species of SFRs from north of 44oN latitude were used in the analyses reported below. Of these, 4,808 came from museum catalogues and records taken from the literature, and 9,268 from our sampling. These records include 4,099 captures from 564 localities recorded during the period 1883-1980, and 9,977 captures from 591 localities from 1981-2007. The focal small forest rodents make up 96.5% of all captures of forest-dwelling rodents (including tree squirrels and rare species) and 70% of all captures of forest-dwelling small mammals (including the above species plus shrews and moles). For opossums, we included 94 capture records from MaNIS, 163 records from a survey of road-killed animals carried out in 1968 (Brocke, 1970), and 281 records from a similar survey done in 2006-8.
Additional sources specimen records:
Crider JE (1979) A Wildlife Inventory of the Sturgeon River Wilderness Study Area. M.S. thesis, Michigan Technological University, Houghton MI.
Teresa Friedrich -- UMMZ field notes
Allen Kurta -- personal communication to pm
Sean Maher-- UMMZ field notes
Manville RH (1947) The vertebrate fauna of the Huron Mountains, Marquette County, Michigan. Ph.D. thesis, University of Michigan, Ann Arbor, Michigan, 263 pp.
Rosa Moscarella -- personal communication to pm
pmrecords -- UMMZ field notes
Allison Poor -- UMMZ field notes; Poor AP (2005) Changes in the Small Mammal Fauna of the Huron Mountain Club, Marquette County, Michigan: an Effect of Global Warming? MS thesis, University of Michigan, Ann Arbor, Michigan, 62 pp.
Skillen R (2005) Changes in the Distribution of Michigan’s Flying Squirrels. MS thesis, Michigan State University, 105 pp.
Data sources for museum records—Specimen information was obtained through the MaNIS network (http://www.manisnet.org) from the following museums: California Academy of Sciences; Cornell University (CU); Field Museum of Natural History (FMNH); Florida Museum of Natural History (FLMNH); Harvard University Museum of Comparative Zoology (MCZ); Los Angeles County Museum of Natural Science (LACM); Louisiana State University (LSUMZ); Michigan State University Museum (MSU); Museum of Natural Science, Royal Ontario Museum (ROM); San Diego Natural History Museum (SDNHM); Santa Barbara Museum of Natural History; Texas A&M University, Texas Cooperative Wildlife Collection (TCWC); Texas Tech University Museum (TTU); United States National Museum of Natural History (USNM); Universidad Nacional Autonoma de Mexico, Instituto de Biologia (IBUNAM); University of Alaska Museum (UAM); Museum of Vertebrate Zoology, University of California (MVZ); Museum of Natural History, University of Kansas (KU); University of Michigan Museum of Zoology (UMMZ); University of Minnesota Bell Museum of Natural History (MMNH); University of Puget Sound Slater Museum of Natural History; University of Utah Museum of Natural History; Burke Museum, University of Washington (UWBM); Museum of Southwestern Biology, University of New Mexico (MSB).
Error—Records compiled from Museums and our sampling programs are subject to multiple sources of error. Assessing and correcting error, insofar as possible, is a difficult and time-consuming process, but it is essential; records such as these cannot simply be downloaded and incorporated into research (Williams et al., 2002; Chapman, 2005a). Further, when error is suspected but cannot be checked, it is important to consider what effect it might have on an analysis. Error that is unbiased with respect to the questions being considered is less of a problem than error that systematically skews an analysis one way or another. Unbiased error may make patterns harder to detect or obscure them entirely, but it is unlikely to create patterns where none exist.
Our goals in this paper are to identify distributional shifts and changes in local assemblages of small mammals and to discuss possible causes of change. With respect to those goals and the particular collections on which we relied, we addressed the following areas of uncertainty with regard to each record:
1. problems with species identifications
2. problems associated with the precision of location
3. collector bias– why properly identified and georeferenced collections might still provide a misleading picture of community composition.
1. Problems with species identifications
Most small mammal species in the northern Great Lakes region are fairly easy to identify in the field or as museum specimens, but among the forest rodents on which we focus, field identification of 2 pairs (Peromyscus, woodland deer mice and white-footed mice; Glaucomys, southern flying squirrels and northern flying squirrels) is sometimes difficult. For museum records, we examined and verified the identifications of all specimens that suggested significant changes in distribution. For field records, since 1980 almost all field identifications were made by the authors or by assistants trained by us. Identifications of most questionable Peromyscus were confirmed by electrophoretic examination of salivary amylase alleles (Aquadro & Patton, 1980) or restriction fragment length polymorphism (Poor, 2005).
2. Problems associated with the precision of location
Coordinates for localities associated with our field work (post 1980 records) were either georeferenced directly using GPS units, or located on maps (usually to quarter-quarter section) and later georeferenced using Topozone (http://www.topozone.com) and/or Google Earth (http://earth.google.com).
For most other specimens, localities, including (when available) latitude, longitude, and estimated coordinate error, were downloaded from http://www.manisnet.org/. For localities that were missing coordinates and/or estimates of coordinate uncertainty, we used Topozone, Google Earth, and an assortment of local maps to supply coordinates. Missing coordinate uncertainties were calculated using the MaNIS Georeferencing calculator (http://www.manisnet.org/gci2.html; see also Chapman & Wieczorek, 2006). In some instances, we were able to refine coordinates and/or reduce uncertainty significantly by using field notes, papers published by collectors, and in the case of recent collections, first-hand knowledge of the sites where collections were made.
For SFR species, collection records are available from 977 identifiable localities in Michigan north of 44oN latitude (records whose coordinate uncertainty overlapped the 44th parallel were eliminated). Of these, 936 (95.8%) had uncertainties < 20 km. The maximum uncertainty for any locality was for 2 records that could be restricted only to the Upper Peninsula. Because analyses of community composition involved combining records of specimens captured over large geographic areas (Lower Peninsula, Upper Peninsula, Huron Mountains), placement of any locality at any point within even the largest area of uncertainty did not change its geographic area. Thus, we were able to include specimens from all 977 localities.
For documentation of range change, we examined all localities with estimated uncertainty > 20km to determine if the area of uncertainty overlapped the edge of the known distribution when the collection was made. This was never the case; most records suggesting range extensions were from our own (post 1980) surveys, and the estimated errors associated with their localities are small.
3. Collector bias–properly identified and georeferenced collections might still provide a misleading picture of community composition
Collecting is usually done for a particular purpose. Collectors sometimes have the goal of determining species composition and abundance in a community, and they record everything they capture. Collectors are often, however, looking for particular species or sampling particular habitats. They may or may not take exemplars of other species or record them in their notes. If specimens are taken, their numbers are likely to be biased in favor of the species under study. Collectors are also likely to keep or report specimens that surprise them because they represent rare or unexpected finds, while perhaps under-representing or ignoring common species. They sometimes take only “vouchers,” specimens placed in collections to document the presence and identification of a particular species at a locality. Collection of vouchers is seldom done in the context of community composition. Further, collections may be biased geographically. Areas that are easily accessible or particularly attractive may be over-represented, while remote or, at the opposite extreme, heavily urban areas are often less frequently collected.
It is possible to address some or all of these problems, but the methods and effectiveness of doing so depend on the sources of data and the goals of a study. Here, we are fortunate in several respects. Almost all collections after 1980 were made by us or by our students, and they include a full list of animals captured. Further, the majority of earlier records were accumulated from the first half of the 20th century, when the goal of many collectors was explicitly to document the total fauna of the areas collected (e.g., Wenzel, 1911; Dice & Sherman, 1922; Hatt, 1923; Dice, 1925; Green, 1925; Blair, 1941; Appendix Fig. 1).
By restricting our study to a subset of species (small forest rodents, SFRs) that are often found together and are likely to be captured using trapping methods widely employed by collectors, we minimize both the tendency of collectors to favor certain habitats and biases introduced by evolving collection methods.
Because collecting effort is seldom documented for early collections, differences among collections might simply represent the intensity of the collecting effort. We therefore compared SFR assemblages in 2 ways. First, we examined the abundance of each species relative to other SFR species in the collection. Relative abundance analyses, however, rely on collectors reporting all individuals of each species. This assumption is met by post-1980 collections but perhaps not by some earlier ones, Consequently, we further compared the results of relative abundance analyses to “occurrence analyses” that require only that collectors report the presence of each species captured (see Methods and Discussion, above). The general agreement between relative abundance and occurrence analyses suggests that their collections give us a reasonable and consistent picture of SFR assemblages at the time the collections were made.
Bias might also result from changes in the geographic pattern of collecting. If early collecting had concentrated in one area and late collecting in another, differences in the SFR assemblages found would not be surprising. Both the Upper and Lower Peninsulas, however, were widely collected during both time periods (Appendix Fig. 2) and consequently, geographic bias favoring one region or another is unlikely to be significant. Further, over 230 collectors contributed to the records comprising our database. The bias of an individual collector for a particular place or species is unlikely to have a large effect.
Finally, for mammals, the susceptibility to capture varies widely among species. Estimates of the relative abundance of a species obtained from trapping records may be strongly affected by its propensity to enter traps as well as by its actual representation in the community. Here, however, we focus on change over time. We cannot be certain that, for example, the abundance of white-footed mice in collections (38% of the SFRs captured prior to 1980) means that they made up precisely 38% of the actual SFR community. The fact, however, that after 1981 their relative abundance increased to 78% demonstrates that their representation in the SFR community has increased dramatically (Table 1).