Evolutionary and ecological response of pocket gophers (Thomomys talpoides) to late-Holocene climatic change

Biological Journal of the Linnean Society (1997), 60: 277–296. With 11 figures

Evolutionary and ecological response of pocket gophers (Thomomys talpoides) to late-Holocene climatic change ELIZABETH A. HADLY1 Museum of Vertebrate Zoology and Department of Integrative Biology, Berkeley, CA 94720, U.S.A.

Received 6 October 1995, accepted for publication 20 May 1996

Late-Holocene evolutionary and ecological response of pocket gophers (Thomomys talpoides) and other species to climatic change is documented by mammalian fossils from Lamar Cave, a palaeontological site in northern Yellowstone National Park. Pocket gophers illustrate ecological sensitivity to a series of mesic to xeric climatic excursions in the sagebrush-grassland ecotone during the last 3200 years, increasing in abundance during mesic intervals, and declining in abundance during xeric intervals. Four other small mammal taxa (Microtus sp., Peromyscus maniculatus, Neotoma cinerea and Spermophilus armatus) also show response to climatic change, increasing or decreasing in abundance in accordance with their preferred habitat requirements. To determine evolutionary response to climate, two craniodental characters for the northern pocket gopher (Thomomys talpoides) are investigated in modern representatives within a 400 km radius of Lamar Cave and then tracked through the time spanned by the fossils. One morphologic character shows that variation in body size, primarily a plastic response to the environment, demonstrates few taxonomically consistent patterns of geographic variation across 39 modern localities. In contrast, the other character indicates genetic relatedness within subspecies. Stasis in the genetically controlled character indicates that the same subspecies of pocket gopher (T. talpoides tenellus) has occupied northern Yellowstone for at least 3200 years. However, T. t. tenellus does show plastic response to climatic change because pocket gophers during the Medieval Warm Period were smaller than at any other time spanned by the deposit. ©1997 The Linnean Society of London

ADDITIONAL KEY WORDS: — evolution – plasticity – morphology – body size – population.

CONTENTS Introduction . . . . . Study area and methods . Temporal samples . Taphonomy . . . Geographic samples . Dating and stratigraphy Identification . . . Morphology . . .

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Present address: Department of Biology, Montana State University, Bozeman, MT 59717, U.S.A.

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E. A. HADLY Results . . . . . Climatic variation Faunal response Morphology . Discussion . . . . Conclusions . . . Acknowledgements . References . . . .

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INTRODUCTION

Pocket gophers (Thomomys spp.) are the most genetically and morphologically variable mammal known (Hall, 1981; Patton & Smith, 1994). Geographically, morphologic variation within this genus is both genetically based and ecophenotypically plastic (Smith & Patton, 1988). One morphologic character, body size, is affected by environmental characters such as nutritional quality, soil depth and friability, and altitude. Of these, only nutritional quality has been demonstrated experimentally to produce plastic body-size variation, but nutritional quality is likely to be influenced by the other environmental factors (Patton & Brylski, 1987; Smith & Patton, 1980). Although pocket gopher body size shows some plastic response to environmental variation over a short time scale ( ≤ 101 years), mammalian body size is a feature that influences such life history phenomena as home range size, female fecundity, and population density, all of which potentially feed into the evolutionary dynamics of populations expressed over longer time scales (Clutton-Brock & Harvey, 1983; Daly & Patton, 1986; Hansen, 1962; Miller, 1946, 1952). In this study I investigate the effects of environmental variation caused by climatic change on the northern pocket gopher (Thomomys talpoides) over a long time scale (102 to 103 years) in order to investigate the questions: Does pocket gopher population density remain constant through time at a given locality? Is morphological change coincident with a palaeoecological record of climatic change? If pocket gophers exhibit a morphological response through time, is it likely to involve heritable traits or be phenotypically plastic? And finally, and perhaps most interestingly, how does the magnitude of any change through time compare with the magnitude of geographically distributed variation observable today? Temporally distributed data for this study come from Lamar Cave, a late Holocene palaeontological site located in Yellowstone National Park, Wyoming (Hadly, 1995). According to palaeoclimatic evidence of the past 3000 years, several mesic to xeric excursions took place both locally and globally. The most prevalent and extensive of these were the warm, dry Medieval Warm Period circa 650 to 1000 yr BP (Hughes & Diaz, 1994; Lamb, 1977), and the cool, wet Little Ice Age from 100 to 700 yr BP, within which a warmer, drier interval occurred about 350 to 500 yr BP (Jones & Bradley, 1992; Porter, 1986). Other local climatic transitions are documented by proxy data such as neoglacial activity, alluvial history, and pollen records, all of which show a relatively mesic time before the Medieval Warm Period from 1300 to 1950 yr BP, a relatively xeric time from 1950 to 2700 yr BP, and a wetter period 2700 to 3450 yr BP (Baker, 1984; Gennett, 1977; Meyer, 1993; Meyer et al., 1992; Richmond, 1986; Whitlock, 1993).

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STUDY AREA AND METHODS

Temporal samples Lamar Cave is a palaeontological site located in northeastern Yellowstone National Park 4 km east of Tower Junction (UTM 555.3E 4974.0N). It is located on a south-facing cliff along the Lamar River at an elevation of 1835 m (6020 ft). The cliff is breached immediately to the west by a short, steep gully that funnels loosened material downslope into a small debris cone. Fine-grained gully material is occasionally carried along the edge of the debris cone by minor floods during heavy rainstorms and deposited into the cave forming alluvial layers. Organic material constitutes the bulk of the cave fill and alternates with the alluvial units. These stratigraphic layers form the basis for sorting specimens by their relative geologic age. The cave is relatively small (6.2 m deep) and before excavation was littered with organic detritus and roof fall. Lamar Cave was discovered in 1986 and excavated from 1987 through 1993. The cave was excavated in natural stratigraphic units as described by Hadly (1990, 1995). Unit numbers from 1 to 16 were assigned from top to bottom. Levels 2 and 4 were alluvial units almost devoid of bone and for all subsequent analyses, they are lumped with levels 3 and 5, respectively. Preservation at all levels generally was excellent, though bones were frequently broken and no skeletons were found in articulation. Specimens will be curated into the University of California’s Museum of Palaeontology at Berkeley (UCMP Loc.V96017) and with the National Park Service. A voucher collection will be maintained by the National Park Service Museum at Yellowstone National Park, Wyoming. Taphonomy Detailed investigations presented elsewhere (Hadly, 1995) document that the primary method of bone collection was by wood rats collecting carnivore scat, raptor pellets and pieces of dead animals within a 100 m radius of the cave entrance. A limited amount of material may also have been accumulated as a result of coyotes, wolves, mountain lions, bears, or badgers chewing their food in the cave. Taking into account all vectors of the taphonomic pathway, the maximum collection radius from the mouth of the cave was about 5 km. The available evidence suggests that whatever taphonomic bias has operated in the deposition of fossils in Lamar Cave, it was constant throughout the time spanned by the deposits (Barnosky, 1994); hence comparisons between levels and with modern samples collected from similar taphonomic vectors are likely to be valid. Geographic samples Geographically distributed samples of modern subspecies come from 39 sites throughout the northern Rocky Mountain region. Samples were chosen to reflect variation within and among subspecies of T. talpoides and closely related species currently living within a 400 km radius of Lamar Cave (Fig. 1). These include

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Figure 1. Geographic distribution of Thomomys talpoides in western North America. The distribution of 13 T. talpoides species-groups within a 400 km radius of Lamar Cave is shown. Dots indicate sampling localities. Lighter shading indicates subspecies of T. talpoides (1 - T. t. bridgerii, 2 - T. t. bullatus, 3 - T. t. fuscus, 4 - T. t. ocius, 5 - T. t. pryori, 6 - T. t. relicinus, 7 - T. t. saturatus, 8 - T. t. tenellus, 9 - T. t. wasatchensis). Darker shading indicates species other than Thomomys talpoides (10 - T. clusius clusius, 11 - T. idahoensis idahoensis, 12 - T. i. pygmaeus, 13 - T. i. confinus). Subspecies from the white areas within the 400 km radius were not examined for this study.

representatives of the following nine subspecies of the northern pocket gopher and two closely related species from the collection of the University of California Museum of Vertebrate Zoology: T. t. bridgeri (Bannock County, Idaho: 69 specimens; Sublette County, Wyoming: 2 specimens; Bear Lake County, Idaho: 44 specimens; Uinta County, Wyoming: 42 specimens), T. t. bullatus (Powder River County, Montana: 26 specimens; Rosebud County, Montana: 26 specimens), T. t. fuscus (Blaine County, Idaho: 10 specimens; Custer County, Idaho: 32 specimens; Fremont County, Idaho: 18 specimens; Idaho County, Idaho: 2 specimens; Teton County, Idaho: 20 specimens; Beaverhead County, Idaho: 2 specimens; Ravalli County, Montana: 4 specimens), T. t. ocius (Sweetwater County, Wyoming: 14 specimens), T. t. pryori (Carbon County, Montana: 24 specimens), T. t. relicinus (Gooding County, Idaho: 8 specimens; Lincoln County, Idaho: 6 specimens; Minidoka County, Idaho: 10 specimens), T. t. saturatus (Mineral County, Montana: 8 specimens; Missoula County, Montana: 20 specimens), T. t. tenellus (Park County, Wyoming: 40 specimens; Teton County, Wyoming: 2 specimens), T. t. wasatchensis (Weber County, Utah: 8 specimens), T. clusius (Natrona County, Wyoming: 4 specimens), T. idahoensis idahoensis (Clark County, Idaho: 14 specimens; Jefferson County, Idaho: 28 specimens). T. i. pygmaeus (Uinta County, Wyoming: 12 specimens), and T. i. confinus (Ravalli County, Montana: 16 specimens; Missoula County, Montana: 10 specimens). Five sparsely distributed subspecies within this radius were not available for study, but their exclusion is not thought to affect the results presented herein: T. t. attentuatus, T. t. caryi, T. t. kelloggi, T. t. talpoides, and T. t. trivialis. Taxonomy of the T.

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talpoides species-group and respective geographic ranges are based on Hall (1981), Thaeler (1972, 1977, 1985) and Thaeler & Hinesley (1979). Dating and stratigraphy To determine the time spanned by the Lamar Cave deposit, 18 organic samples were submitted for radiocarbon analysis. The sampling procedure was intended to uncover the within-level and between-level variation for the depth of the deposit. Samples were submitted for Level 3 (3 samples), Level 5 (1 sample), Level 6 (2 samples), Level 9 (4 samples), Level 12 (3 samples), Level 13 (2 samples), and Level 16 (3 samples). Though the results of these analyses suggest some vertical mixing of fossils, the radiocarbon dates generally increase in age with depth (Hadly, 1995). The youngest dates are modern and are from Level 3 (CAMS-20348; CAMS-20349). The oldest sample dated as 2777 to 3222 cal yr BP (CAMS-20356) is from Level 16, which rests on bedrock at 272 cm below datum. For the purposes of determining the age of each level, each radiocarbon-dated item was assessed for material type as some material has a longer environmental residence time, and therefore is more likely to be contaminated. All but three radiocarbon dates were used to develop the chronology presented herein. Interpretations of the radiocarbon dates and a complete discussion of the stratigraphy are found in Hadly (1995) and Hadly (in press). Dating of the Lamar Cave deposits reveals that within a given stratigraphic level a range of time is represented (i.e. evidence of time-averaging) and that the levels are to some extent overlapping, though the levels generally increase in age with depth. This makes level-by-level comparisons potentially inappropriate, since timeaveraging could obliterate the faunal signal across levels. Therefore, in addition to level-by-level analysis, a conservative method was employed to uncover the effects of climatic change through time: the individual stratigraphic levels were appropriately lumped into Time Intervals A through E. These intervals are based on the time curve produced by an exponential regression of the radiocarbon dates with depth, with boundaries chosen at points that yield the largest number of intervals with the least probability of mixing across the intervals. The interval boundary between A and B was between levels 3 and 4; the boundary between B and C was between levels 6 and 7; and the boundary between C and D was between levels 12 and 13. Dates for intervals D and E did not overlap and interval boundaries were chosen so that both intervals included two levels. Independently-calibrated climatic periods are plotted (Fig. 2) in order to reveal the climatic regime of a given interval. Faunal analyses utilize both the time intervals and individual stratigraphic levels. Identification Fossil mammals were identified to species when possible using comparative material from the University of California Museum of Vertebrate Zoology, University of California Museum of Palaeontology, Museum of Northern Arizona, and The Carnegie Museum of Natural History. Only cranial material was used to identify animals smaller than a lagomorph; all other mammals were identified using whatever skeletal material was present. Approximately 10000 mammalian specimens

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Figure 2. Late-Holocene climatic interpretation based on probability of fire-related debris-flow activity and alluvial events (y axis) from northern Yellowstone National Park (Meyer, 1993). The temporal range of the Lamar Cave Time Intervals is shown along the x axis.

were identified. Minimum numbers of individuals (MNI) and number of identified specimens (NISP) (Grayson, 1973, 1978) were calculated for each stratigraphic level, then stratigraphic counts were lumped within each time interval in order to assess the relative abundance observed through the late-Holocene sequence at Lamar Cave. Relative abundances were calculated for the five most common taxa by time interval to standardize for different numbers of specimens per interval. Abundances are based on 8589 total number of identified specimens (TNISP). The 95% confidence intervals for the five common taxa per interval are shown where SEˆpt =

p) ( √ pˆ (1-ˆ ) × 100 N t

t

when pˆ t =

Xt Nt

;

with Xt = NISP of taxon at interval t and Nt = TNISP at interval t. Morphology Only the lower jaws of pocket gophers were measured for this study because they were better preserved and more numerous than uppers (n = 231 and n = 108, respectively). Only specimens with completely erupted cheek teeth were examined and no other age control was performed. Both females and males are probably included in the fossil sample because the taphonomy of the deposit suggests that the Lamar Cave samples are random collections of the pocket gopher population near the cave. Thus both females and males were measured in the modern samples as well. In order to determine morphologic response to climatic change in pocket gophers, the investigation focused on two variables that have been examined in modern

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populations of another species of pocket gopher, T. bottae. The two mensural characters, diastemal length (DL) and toothrow length (TRL), were used because they are the best indicators of body size (non-shape) and size-independent (shaperelated) variables, respectively (Smith & Patton, 1988). Toothrow length is highly constant among individuals within a population, but variable between geographically separate populations. Although it is correlated to some extent with body size, toothrow length was determined to be the best overall shape predictor in a principal components analysis of 13 cranial characters (r = 0.59 for females, r = 0.53 for males) (Smith & Patton, 1988). Because toothrow length is not phenotypically plastic (Smith & Patton, 1988), it is useful in taxonomic discrimination of differentiated genetic groups. In contrast, the diastema of T. bottae is not a good predictor of the genetic relatedness of populations (r = –0.4 for females, r = –0.16 for males) and instead is highly correlated with body size, which is a highly plastic trait (r = 0.85 for females, r = 0.93 for males) (Smith & Patton, 1988). Two morphologic characters from 339 fossils from Lamar Cave and 555 modern specimens from 39 localities were digitized and measured through the use of MORPHOSYS (Meacham & Duncan, 1990), a computer imaging program and stereomicroscope combination accurate to ± 0.01 mm. Lack of reliable landmarks posterior to the third molar (M3) due to its inclined position and the fragility of the bone alveolus of M3 introduced uncertainty into measuring the entire tooth row (P4–M3). Therefore, toothrow length was taken between P4 and M2 (Fig. 3) instead of between P4 and M3 (Smith & Patton, 1988). Exclusion of the M3 is not likely to have altered results herein. Standard statistical comparisons among and within spatial samples and temporal samples were accomplished via analysis of variance with StatView (AbacusConcepts, 1992) and SuperAnova (AbacusConcepts, 1989). After determination of a significant F-ratio, post-hoc comparisons were performed in order to uncover spatial and temporal patterns of similarity. The Games-Howell test (Games & Howell, 1976) was used to compare fossil levels, time intervals, and modern localities of the local

Figure 3. Generalized Thomomys talpoides left dentary in mesial view with toothrow length (TRL) and diastemal length (DL) shown.

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subspecies (T. talpoides tennellus). For the rest of the species-group, the Games-Howell test was performed after lumping all localities by subspecies because of the large number of modern localities. Statistical significance was set at the P < 0.05 level.

RESULTS

Climatic variation The faunal data are compared to independent prehistoric climatic data. Variation in local climate is largely inferred from an alluvial and fire-related debris flow chronology produced by Meyer (1993) and Meyer et al. (1992) (Fig. 2). Generally, periods of high fire-related debris flow activity result from increased fire activity caused by lower effective moisture, which is controlled by both temperature and precipitation. Periods of low fire-related debris flow activity suggest an overall increase in effective moisture. Climatic interpretations and the time intervals plotted on Figure 2 show that the earliest portion of Time Interval E spans a period of low to moderate fire frequency (2350 to 3200 yr BP), while the latter part of this interval is characterized by increasing alluviation and high fire activity from 1950 to 2350 yr BP and decreasing fire-related activity from 1800 to 1950 yr BP. Time Interval D spans a period of reduced fire frequency, but uncharacteristically increased alluviation from 1100 to 1800 yr BP. Time Interval C, from 500 to 1200 yr BP, spans most of the Medieval Warm Period, which is a time of extreme fire-related debris flow activity and probable drought in Yellowstone and elsewhere in the western U.S. (Stine, 1994). Time Interval B, from 300 to 700 yr BP, straddles the early part of the Little Ice Age, a period of low fire frequency, as well as the period from 350 to 500 yr BP, a warm period of reduced glacial activity in the northern hemisphere within the classically defined Little Ice Age of 100 to 700 yr BP (Porter, 1986). Time Interval A, from 0 to 300 yr BP, spans the main, or latter part of the Little Ice Age to the present, which is a period in the Yellowstone region of decreased fire activity but increased climatic variability (Meyer, 1993). Faunal response Mammalian faunal remains recovered from Lamar Cave span approximately 3200 years and represent 6 orders, 16 families, 31 genera, and 40 species. Of the hundreds of thousands of mammalian bones and teeth, 10597 were identifiable at least to generic level. Rodents are the most abundant mammalian order represented in the fauna. Species that dominate the faunal assemblage over the entire 3200 years are also those most abundant in the current local fauna as demonstrated by trapping data (Hadly, 1995). The five most common mammals throughout the deposit are the montane vole (Microtus cf. M. montanus) with an average relative abundance of 33%, the Uinta ground squirrel (Spermophilus armatus, x¯ = 23%), the pocket gopher (Thomomys talpoides, x¯ = 20%), the bushy-tailed wood rat (Neotoma cinerea, x¯ = 13%) and the deer mouse (Peromyscus maniculatus, x¯ = 12%). Shrews, lagomorphs and bats are present throughout the cave deposits in relatively low frequency. Large mammals, such as ungulates and carnivores, are diverse but present in low frequency

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much as they are in the present mammalian community. Detailed discussions of the Lamar Cave mammalian fauna are found in Hadly (1995, in press). Relative abundances of the five most common mammalian taxa are presented in Figure 4. Indices of difference (ID) are shown for a taxon through time, where IDa = maximum

NISPa

– minimum

NISPa

TNISPt TNISPi when NISPa is the number of identified specimens for taxon a, and TNISP is the total NISP inclusive of the five small mammals for given time intervals t and i. Two species, P. maniculatus and N. cinerea, show relatively constant abundances throughout the time spanned by the Lamar Cave deposit, which is concordant with their habitat requirements. Peromyscus maniculatus reaches a minor high at Interval C, though the fluctuations of this taxon do not equal the relative abundance changes of Microtus, Thomomys or Spermophilus. Variation in relative abundance is greatest in Spermophilus,

Figure 4. Relative abundance (in percent) of the five most common small mammals in the Lamar Cave fauna by Time Interval with 95% confidence limits indicated. Abundances are based on a total number of identified specimens of 8589 for these five taxa for the entire deposit. Schematic climate for Time Intervals is shown at bottom of diagram. The Index of Difference is a numerical expression of the spread between the lowest and highest relative abundances as reflected by the horizontal dotted lines.

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(ID = 31), while Microtus (ID = 15) and Thomomys (ID = 13) show somewhat less relative abundance variation. These contrast with IDs of 11 and 4 in Peromyscus and Neotoma, respectively. Spermophilus relative abundances counter those of Microtus and Thomomys throughout the deposit. Percentages of Spermophilus reach a high at Time Interval B and lows are found at intervals D and E, while Microtus and Thomomys peak at intervals D and E with a low for both taxa found at Interval B. While both Spermophilus and Microtus are found in the sagebrush grassland outside Lamar Cave, they tend to prefer different microhabitats. Ground squirrels are found in less dense, relatively xeric portions of the grassland, and voles are found in mesic areas that promote denser vegetative cover (Hadly, 1995). Morphology To determine if a given range of toothrow lengths indicates genetic relatedness in modern T. talpoides as it does in T. bottae, data were analysed from 555 specimens of the T. talpoides species-group from 39 localities within a 400 km radius of Lamar Cave. Variance between localities within a subspecies was much less than variance between subspecies; no significant differences in TRL were found within subspecies. Of the 13 subspecies of T. talpoides and closely related species investigated, 4 could not be statistically distinguished from T. t. tenellus based on toothrow length: T. idahoensis confinus, T. clusius, T. t. fuscus, and T. t. relicinus (Fig. 5). Of these, only T. t. fuscus has a geographic distribution that abuts that of T. t. tenellus. In either a time interval analysis or a level-by-level analysis, none of the fossil specimens were significantly different in toothrow length from modern T. t. tenellus (Fig. 6). There also were no significant differences between the Lamar Cave levels or intervals for toothrow length. Contrary to the pattern shown by toothrow length, diastemal data from 553 specimens of the T. talpoides species-group from the 39 localities show few consistent taxonomic patterns of variation across geography or among subspecies (Fig. 7). Additionally, diastemal length consistently shows greater variance within subspecies than does toothrow length (Fig. 8). Not only is there broad overlap among subspecies of T. talpoides, there are significant differences among localities within subspecies, as exhibited by T. t. tenellus (Fig. 9a). This pattern is consistent with the conclusion of Smith & Patton (1988) for T. bottae that diastemal length is not a good predictor of genetic relatedness of populations but rather is highly correlated with environmentally plastic responses in body size variation. Diastemal lengths within modern T. t. tenellus from four localities showed significant differences, with a significant positive relationship with elevation (P < 0.001) (Fig. 9b). The modern specimens of T. t. tenellus from the Lamar Cave area (1835 m) are most similar to those from Jackson Hole (1980 m), which is across the continental divide and approximately 140 km south of the cave (Fig. 9a). Pocket gophers of this subspecies from two other localities, Canyon (2560 m) and near Cooke City, Montana (2590 m), show significantly larger diastemal lengths than the modern specimens near Lamar Cave, though they are only 20 and 60 km away, respectively. In contrast to the results of toothrow lengths, diastemal length does vary across the time represented by the deposits of Lamar Cave. Pairwise comparisons of time intervals show no significant differences in diastemal length from the modern pocket

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gophers immediately outside the cave (Fig. 10). However, significant differences between the modern T. t. tenellus specimens from near Canyon and the fossils from the cave were found for all time intervals except Interval A (Fig. 9). Diastemal lengths from every time interval of Lamar Cave are significantly smaller than those near Cooke City, Montana. Although there were no significant differences between the pocket gophers outside Lamar Cave and pocket gophers from the Lamar Cave time intervals, pairwise comparison shows that among the time intervals, diastemal lengths from time intervals C and D are significantly smaller than those from Interval A. Closer scrutiny within the time intervals with a level-by-level analysis indicates that diastemal length of pocket gophers from Level 7 is indeed significantly smaller than those of the present population outside the cave (Fig. 11).

DISCUSSION

Pocket gophers in the Yellowstone region exhibit changes in morphology and relative abundance that coincide with climatic change during the late Holocene. Changes in relative abundance are assumed to grossly equate to population-size

Figure 5. Plot of toothrow length of the 13 modern subspecies of the T. talpoides species-group within the 400 km radius of Lamar Cave. Bars around data points indicate 95% confidence limits. Horizontal nested bars indicate the minimum non-significant subsets at the 95% confidence interval. Note the large number of subsets and low degree of overlap across subspecies.

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Figure 6. Toothrow lengths of T. talpoides tenellus for four modern populations (n = 42) and 16 levels from Lamar Cave (n = 172) with 95% confidence limits. Time Intervals also are shown. Mean at Level 6 is based on n = 2.

fluctuations, which represent a community-level response that may or may not be linked to morphologic response. Deciphering the nature of temporal morphologic response to climatic change requires an uncoupling of the variation that is attributable to genetic change and variation that is a plastic response to environmental change (Straney & Patton, 1980). The degree of concordance between population density, phenotypic plasticity, genetic change, and climatic variation provides a measure of the effects of climate on pocket gophers in this ecosystem, which has important consequences for understanding organismal evolution and community dynamics through both space and time. In pocket gophers, toothrow length reflects the genetic relatedness of individuals. In the T. talpoides group within 400 km of Lamar Cave, toothrow length is a reasonable predictor of geographically separated populations (i.e. subspecies). On the other hand, diastemal length is a relatively plastic character that reflects body size and indirectly habitat (i.e. nutritional) quality (Smith & Patton, 1988). The distinction between these two morphologic characters means that in this study it is possible to determine whether the morphologic response of pocket gophers to climatic change is a result of genetic change or plasticity. If climatic change has contributed to large distributional range-shifts of subspecies or in situ genetic change of the pocket gophers near Lamar Cave during the past 3200 years, a shift in toothrow length would be expected. Local populations of pocket gophers are known to experience high extinction rates, and in fact, this is thought to contribute to the high degree of genetic and morphologic variation in the genus (Dalquest & Scheffer, 1944; Patton & Smith, 1994). Despite the significant amount of spatial variation in toothrow length exhibited among the T. talpoides group, no significant temporal differences were found in the Lamar Cave deposit. Therefore it is inferred that there has been no genetic change in this trait throughout the past

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Figure 7. Plot of diastemal length of the 13 modern subspecies of the T. talpoides species-group within the 400 km radius of Lamar Cave. Bars around data points indicate 95% confidence limits. Horizontal nested bars indicate the minimum non-significant subsets at the 95% confidence interval. Note the low number of subsets and high degree of overlap across subspecies, especially for mid-sized pocket gophers. Significant extremes include the smallest (T. i. idahoensis, T. i. pygmaeus) and largest pocket gophers (T. t. bridgerii, T. t. pryori) in the area.

Figure 8. Plot of variance of toothrow length and diastemal length for the 13 modern subspecies of the T. talpoides species-group within the 400 km radius of Lamar Cave. Note that variance for diastemal length generally is higher than toothrow length.

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3200 years. These data suggest that the same subspecies of pocket gopher, T. t. tenellus, has occupied the area around Lamar Cave for at least 3200 years. To hypothesize that the other subspecies with similarly-sized toothrows are represented would require convoluted scenarios of dispersal and retraction, because only one, T. t. fuscus, has a geographic range that is parapatric to T. t. tenellus. Whatever the community-level and morphological effects of climatic change on pocket gophers in the Yellowstone region, it is unlikely that the effects are due to the incursion of a different subspecies of the northern pocket gopher into the area near Lamar Cave. Contrary to the pattern shown by toothrow length, pocket gopher diastemal length exhibits significant spatio-temporal variation. The spatial pattern of diastemal length (i.e. body size) is seemingly random with little concordance to subspecies designation. In other pocket gophers, body size scales positively with nutritive quality (Miller, 1952; Patton & Brylski, 1987; Smith & Patton, 1980), soil thickness and friability (Davis, 1938; Patton & Brylski, 1987), and has been shown to have in some cases a positive and in some cases a negative correlation with increasing elevation

Figure 9. (a) Diastemal lengths in four modern populations of T. talpoides tenellus as a function of distance from Lamar Cave. (b) Plot of diastemal lengths of individuals from the same four modern populations by elevation.

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Figure 10. Summary of late-Holocene responses of T. talpoides tenellus to climatic change in Yellowstone National Park. Figure at the left is summary of relative abundance changes in pocket gophers through time at Lamar Cave (see Fig. 6). Center diagram is diastemal length (i.e. body size) change in this species through time, with 95% confidence limits shown. Shaded bar indicates diastemal length of modern pocket gophers in the vicinity of Lamar Cave at the 95% confidence level. Note differences between Interval A and Intervals C and D. Diagram on the right is toothrow length through time indicating no significant difference through this time. Shaded bar shows modern population in vicinity of Lamar Cave.

Figure 11. Diastemal lengths of T. talpoides tenellus for 4 modern populations (n = 42) and 16 levels from Lamar Cave (n = 207) with 95% confidence limits. Time Intervals also are shown. Mean at Level 6 is based on n = 2. Note significant differences across space and time for this character, notably between all modern localities and Level 7 and between Level 7 and fossil levels 3, 12, and 15.

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(Davis, 1938; Hoffmeister, 1956). In T. t. tenellus, the relationship between spatial variation of diastemal length and elevation is significant. Body size in this subspecies, as in T. bottae, thus is surmised to be an ecophenotypically plastic trait related to nutritional regime, which scales with elevation. Abiotic factors linked to elevation that are likely to influence habitat quality (e.g. primary productivity) include length of growing season, precipitation, and temperature (Martner, 1986). Abiotic factors conceivably also influence pocket gopher population size by controlling the availability of relatively mesic vegetation, primarily forbs (Bailey, 1915; Huntly & Reichman, 1994; Tryon, 1947). Although the relationship between population density and elevation requires further study for this genus as a whole, the link between diastemal size (i.e. body size) and population density to climate clearly is suggested by the elevational patterns observed for T. t. tenellus. Therefore when the environment is mesic, pocket gophers (at least in the subspecies T. t. tenellus) should be large and abundant; when the environment is xeric, pocket gophers should be small and less abundant. In general the data on diastemal length are concordant with climatic patterns inferred from fire-related debris flows: when pocket gophers are large, the climate is effectively cool and wet; when they are small, the climate is warm and dry (Fig. 11). During the Little Ice Age, from 150 to 450 yr BP, represented by Time Interval A, pocket gophers from Lamar Cave (1835 m) were larger than at any other time in the record, and are not significantly different from the size of modern pocket gophers near Canyon at 2560 m. During the Medieval Warm Period, represented by Intervals B and C, pocket gophers were small. In fact the smallest pocket gophers from any level throughout the late Holocene are from Level 7 which is within the time spanned by the Medieval Warm Period. These animals are significantly smaller than the modern specimens outside the cave today, and are smaller than any population of T. t. tenellus sampled for this study. The sole exception to the pattern of agreement between inferred climate based on the proxy climate data and pocket gopher body size is Time Interval D. Time Interval D spans a mesic period, suggesting that pocket gophers should have been large, yet the diastemal data shows that pocket gophers were small. If body size in pocket gophers suggests that the environment was effectively more xeric, yet decreased activity of fire-related debris flows suggest a relatively more mesic time, is there an explanation that can account for this apparent discrepancy? The relative abundance data of small mammals, which is an index of population density (Hadly, 1995), may provide pertinent information because the discrepancy could be accounted for if body size primarily was tracking temperature whereas population density was tracking precipitation. In general, when fire-related debris-flow activity is high (i.e. xeric climate), pocket gophers are relatively rare, and when it is low (i.e. mesic climate), pocket gophers are more abundant. Pocket gophers vary from 13% to 26% of the small mammal fauna. Minima for the late Holocene are reached during the Medieval Warm Period and the warmer, drier period within the Little Ice Age spanned by Intervals C and B, which is in agreement with both fire-related debris flow activity and diastemal-length estimates of pocket gopher body size. Thus, during the Medieval Warm Period pocket gophers were significantly less abundant than at any other time during the last 3200 years, and they were as small as or smaller than at any other time in the Lamar Cave record. High abundance of pocket gophers generally appears to track periods of low fire-

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related debris flow activity (Figs 2 and 10). Pocket gophers are relatively abundant during Interval A, which spans the Little Ice Age, and also is a time when pocket gopher body size was larger than at any other time during the last 3200 years (Fig. 11). The highest relative abundance of pocket gophers is during intervals D and E. Interval D is when fire-related debris flows are at a minimum (Fig. 2), which suggests that the climate was effectively moist. Relative abundances of Microtus also indicate more mesic conditions at Interval D, as Microtus prefers mesic, dense vegetation (Hadly, 1995). However, Interval D is where pocket gophers are as small as they were during the Medieval Warm Period (Fig. 11), suggesting that ‘effective elevation’, or some variable that scales with elevation, was low. The decoupling of evidence from pocket gopher relative abundance, body size, and fire frequency at Interval D is potentially informative about pocket gopher response to climatic change, which includes variation both in temperature and precipitation. The exact nature of the moisture and temperature gradients that govern body size and density of pocket gophers for the Yellowstone region is unknown, but data from other studies may be pertinent (Reichman, Whitham & Ruffner, 1982; Tryon, 1947). The link between moisture and body size in pocket gophers is most strongly evident in a study of T. bottae which shows both an increase in body size and increased population density in irrigated alfalfa fields, though increased nutritional intake due to a longer growing season and crop availability also may play a role (Patton & Brylski, 1987). In the Bridger Mountains of Montana, T. talpoides reaches a maximum population density at 2300 m (7500 ft), where effective moisture is high relative to the surrounding plains (Tryon, 1947). Moreover, temperature also may influence body size in pocket gophers, as it does in other small mammals. For example, in a morphometric study of 14 species of kangaroo rats (Dipodomys) where body size was related to several abiotic variables, including temperature, precipitation and actual evapotranspiration, annual temperature was found to be the best size predictor, although only in approximately 30% of the analyses (Baumgardner & Kennedy, 1993). The difficulty in extrapolating from this study and other studies is that it is unclear whether this response is due to plastic or genetic response. There is a general tendency for body size to increase with decreasing annual temperature in mammalian species (e.g. Lundelius et al., 1983; Mayr, 1956, 1965; Purdue, 1989), but other intercorrelated factors also play a role (McNab, 1971). Pocket gophers from intervals D and E are abundant but not as large as they are in Interval A, which may be in accord with a wet, warm climate during intervals D and E. Interval D spans a time of low fire frequency, though Interval E bridges a period that alternates between low to high fire frequency. Relative precipitation must have been high enough to support abundant mesic vegetation, which in turn supported large populations of gophers not significantly different in size than modern gophers through both intervals. Interval E is not significantly different from Interval D either for the relative abundance of small mammals or pocket gopher diastemal size. However, Interval E is the only interval where the relative abundances of small mammals do not completely agree with the climatic conditions manifested by the fire-related debris flow activity. The time spanned by Interval E includes periods of contrasting climate, with a period of low fire activity early in the interval from 2700 to 3200 yr BP, moderate activity from 2300 to 2700 yr BP, high fire frequency from 1950 to 2300 yr BP, and low fire frequency during the latter part of Interval E from 1800 to 1950 yr BP (Fig. 2). The small mammal patterns from intervals D and E indicate that these

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time periods encompassed the most mesic environmental conditions in the Lamar Cave record, including the Little Ice Age spanned by Interval A. However, this may not indicate that intervals D or E were colder or wetter than the Little Ice Age, just of longer duration as the extent of the Little Ice Age is shorter than the time spanned by Interval A, which suggests that time-averaging may explain the signal from Interval E. Even if the mammals from Interval E are in fact representative of the range of environmental conditions indicated by fire frequency data, it is possible to accept both data sets if the effects of temperature and moisture are decoupled. The postulated warm, wet climate for Interval E is consistent with high frequency of firerelated debris flows. Monsoonal climatic patterns that include high temperatures combined with increased summer precipitation, which leads to increased fuel load, correlate with catastrophic fire events in the Yellowstone region since 1890 (Balling, Meyer & Wells, 1992). If the fire-related debris flow activity for this period is correct, the alternative explanation to a warm, wet climate is that the climate during this time was variable and the diastemal size has captured one climatic regime while relative abundance has captured another. This explanation is less plausible because the specimens on which relative abundance was calculated are the same as those that provided the diastemal measurements, and the relative abundance data also are supported by other small mammals, namely Microtus.

CONCLUSIONS

Evidence from Lamar Cave demonstrates that the changing climate of the last 3200 years has elicited a variety of responses in pocket gophers. A geneticallyconstrained character, toothrow length, suggests that the same subspecies of pocket gopher, T. t. tenellus, has occupied the Yellowstone region throughout the late Holocene. In contrast, an ecophenotypically plastic trait, pocket gopher diastemal length, shows variability over 3200 years. The two morphologic traits and relative abundance in T. t. tenellus demonstrate population-level and community-level responses to climatic change during the late Holocene. Environmental conditions during this time were punctuated by a series of mesic to xeric climatic excursions. Mesic conditions prevailed from 2700 to 3200 yr BP, from 1350 to 1950 yr BP and during most of the Little Ice Age 100 to 700 yr BP. Xeric conditions persisted from 1950 to 2300 yr BP and from 450 to 1350 yr BP; the height of which is known as the Medieval Warm Period and the effectively warmer, drier period within the Little Ice Age. Generally, when the environment was wet, pocket gophers were abundant; when the environment was dry, pocket gophers were rare. During the Little Ice Age, pocket gophers had high population densities and were large in body size, which is not significantly different than pocket gophers from a higher elevation today. During the prolonged period of warm, dry climate of the Medieval Warm Period, pocket gophers were rare and significantly smaller. However, the apparent mesic Interval D from 1100 to 1800 yr BP, decouples this relationship. Pocket gophers were abundant, but no different in body size than pocket gophers during the Medieval Warm Period, or local pocket gophers today. Because temperatures had to have been warm enough to support an increased fire frequency during this time, the pocket gopher body-size data from Interval D may be a result of relatively high temperatures in a wet climatic regime.

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ACKNOWLEDGEMENTS

Financial support while I was a student at Berkeley was provided by the Museum of Vertebrate Zoology Annie Alexander Scholarship and Louise Kellogg Grants-inAid, University of California Regents Fellowship, and research grants from the National Park Service (CA1570-7-8002) and National Science Foundation EPSCoR Program ( EPS-9640667). I am grateful for the inspiration and invaluable guidance from J.L. Patton. This manuscript was greatly improved by reviews from G. Baumgardner, E. Lessa, J.L. Patton, M.F. Smith and one anonymous reviewer.

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