Thomas H. Kunz, Ph.D.
Center for Ecology and Conservation Biology
Department of Biology
Boston University
Boston, MA 02215
E-mail: kunz@bu.edu
Phone: 617-353-2474
Craig L. Frank, Ph.D.
Department of Biological Sciences
Fordham University
441 East Fordham Road
Bronx, NY 10458
E-mail: frank@fordham.edu
Phone: 914-273-2167
Eric P. Widmaier, Ph.D.
Department of Biology
Boston University
Boston, MA 02215
E-mail: widmaier@bu.edu
Phone: 617-353-5563
Jonathan D. Reichard, Ph.D. Candidate
Department of Biology
Boston University
Boston, MA 02215
E-mail: reichard@bu.edu
Phone: 617-529-9846
PROPOSAL SUMMARY
White-Nose Syndrome (WNS) has been identified as the cause of unprecedented morbidity and mortality in six of the nine species of bats in the northeastern United States. First observed in six hibernacula in New York State in the winter of 2006-2007, reports in the winter of 2007-2008 from at least 28 caves and mines in four states (New York, Vermont, Massachusetts, and Connecticut) indicated mortality as high as 95% at some sites. This proposal addresses one of the primary goals proposed at a recent conference on WNS that was convened in Albany, New York (June 9-11, 2008), and attended by over 100 research scientists and natural resource managers from most of the eastern US, representing several state and federal management agencies, federal and state laboratories, and academic institutions. Several hypotheses were proposed and discussed by the body of participating scientists, including those advanced in this proposal. The consensus among those in attendance is that the hypotheses proposed herein are among the highest priorities needed to address why hibernating bats are dying in such large numbers in the northeastern US.
We postulate that a reduction in the quantity and quality of insects during the pre-hibernation period in autumn may limit the deposition of adequate stores of white adipose tissue (WAT) and thus compromises successful hibernation, and ultimately reproductive success. WAT is the primary source of energy that sustains bats (and other hibernators) throughout the winter when they have no access to food. Over-winter survival and subsequent reproductive success requires a sufficient quantity and quality of WAT deposited during the pre-hibernation period, and sufficient fat reserves to sustain deep torpor and periodic arousals throughout the winter, and a final arousal in spring. Because insectivorous bats cannot synthesize polyunsaturated fatty acids (PUFAs), deficiencies in dietary PUFAs during the pre-hibernation period in autumn may reduce the duration and depth of torpor during. Frequent arousals during hibernation may result in premature depletion of WAT before the end of the hibernation period. Depleted WAT at this time may contribute to a decrease in leptin production (necessary for ovulation and successful reproduction by females), or, in the worst cases, the inability to arouse from torpor or inability to mount an immune response to possible pathogens.
Analyses of body composition and dietary composition (including PUFAs) of bats and the biomass and quality (i.e., PUFA contents) of insects available to little brown myotis (Myotis lucifugus) during the pre-hibernation period will be conducted at sites affected by and unaffected by WNS to test five hypotheses that may help reveal or rule out causes of premature deaths or compromised reproductive success in these hibernating bats. Destructive body composition analysis provides the most accurate and reliable estimates of total body water, WAT, and lean dry mass, and analyses of PUFAs in WAT collected from bats, stomach contents, and insects during the pre-hibernation fattening period. These data promise to provide valuable insight for testing proposed hypotheses to help explain why hibernating bats are dying prematurely at hibernacula in the northeastern US, and in turn suggest directions for future study to better understand WNS.
SCOPE OF WORK
Introduction
One of the most devastating conditions ever reported for bats, known as “White-Nose Syndrome” or WNS, has contributed to an unprecedented number of fatalities among five of the nine species of bats in the northeastern United States. First observed in six hibernacula in New York in the winter of 2007, WNS was observed in at least 26 caves and mines in four states (New York, Vermont, Massachusetts, and Connecticut), during the winter of 2008, with morbidity and mortality reported as high as 95% at some sites (A. Hicks, New York State Department of Environmental Conservation, pers. comm.). Tens of thousands of bats have died in caves and mines within the past year. To date, researchers from at least 12 different laboratories in the United States (US) are rallying to identify possible causes of this condition and to help identify ways to mitigate this unprecedented level of mortality. Bat populations cannot sustain such high mortality rates because females normally produce only one offspring per year, and thus it may take generations to replace what is being lost at current mortality rates. WNS is so called because of fungal growth on the faces and other body parts of affected bats (see supplemental document). The white-nose condition has been attributed to several species of non-pathogenic fungi, and may only be secondary infection rather than the underlying cause of WNS.
With depleted fat reserves, many hibernating bats during the winter of 2007-2008 were unable to arouse from the low body temperatures typical of hibernating mammals. Among the bats that were able to arouse, many were observed scattered across the landscape near caves in severely dehydrated conditions, with depleted fat reserves, and many with necrotic wing membranes. To date, mycologists and pathologists have identified over 46 species of fungi, but none appear to be pathogenic (B. Buckles, College of Veterinary Medicine, Cornell University), although one species (Geomyces spp.) appears to superficially invade sebaceous glands on the face. Current research is underway in several laboratories to explore the possible role of this cold-adapted fungus as a cause of WNS (D. Blehert, USGS, pers. comm.). No specific contaminants have been identified in bats at concentrations that might have caused winter mortality, but no data are available to rule out sub-lethal affects from certain contaminants (B. Rattner, USGS, pers. comm.).
Several other questions and hypotheses also may be at the root of the observed fatalities. Do bats with normal amounts of white adipose tissue (WAT) survive the winter? Are bats with insufficient quantities of WAT in autumn able to enter deep torpor and sustain this for periods to minimize mobilization of fat reserves? Are bats with inappropriate quantities of polyunsaturated fatty acids (PUFAs) in their fall diet able to survive hibernation? Are bats with low WAT reserves able to engage in non-shivering thermogenesis—the first stage of a successful arousal? Are bats with low WAT reserves able to mount appropriate immune responses? Do bats with WNS have plasma leptin levels upon arousal in spring that are at sufficient levels to initiate the cascade of hormones that lead to ovulation and successful reproduction? Do bats that show external symptoms of WNS and survive to emerge from hibernation survive and produce successful young at maternity roosts? Many of the bats that are now being found at maternity roosts have severely scarred and necrotic wing membranes (J. Reichard, pers. comm.), suggesting that these conditions may compromise the ability of bats to forage successfully, reproduce, and deposit sufficient quantities of fat during the following pre-migratory and pre-hibernating period in autumn. We cannot address all of these and other questions in this proposal, but we are planning to collaborate with other researchers who will simultaneously be addressing many complementary hypotheses.
Importance of Proposed Research
WNS has been identified as the cause of unprecedented mortality and morbidity among six of the nine species of bats in the northeastern US, first observed in 6 hibernacula in New York State in the winter of 2006-2007. In the winter of 2007-2008, WNS was reported from at least 28 caves and mines in four states (New York, Vermont, Massachusetts, and Connecticut), with mortality reported as high as 95% at some sites. A recent conference on WNS was convened in Albany, NY (June 9-11, 2008), and attended by over 100 research scientists and natural resource managers from most of the eastern US, representing state and federal management agencies, federal and state laboratories, and academic institutions. Several hypotheses were proposed and discussed by the body of participating scientists, including the hypotheses in this proposal. The consensus among those in attendance concluded that the hypotheses proposed herein are among the highest priorities needed to address why hibernating bats are dying in such large numbers in the northeastern US. Our research promises to contribute to a better understanding of the mechanisms that influence winter survival and reproductive success following hibernation.
Why Are Bats Dying?
The hypothesis that depot WAT is depleted in mid-winter followed by high mortality could be explained if bats are unable to gain a sufficient quantity of WAT during the pre-hibernation period. The underlying cause of insufficient deposition of WAT in autumn may reflect low insect biomass at sites where bats typically forage in the vicinity of swarming sites, accumulate depot fat, and engage in courtship and mating activities before the onset of hibernation. Alternatively, bats may deposit sufficient quantities of WAT, but the autumn diet is in sufficient nutritional quality to sustain deep, prolonged torpor that minimizes energy expenditure during hibernation.
Low insect densities have been reported at some regions in northeastern North America during autumn (T. McCabe, New York State Entomologist, pers. comm.), and some insect populations may be below a certain threshold level that will prevent bats from obtaining sufficient fat reserves to sustain successful hibernation. Reductions in the population sizes of some insectivorous birds species, notably swifts and swallows, in North America have been attributed to reduced numbers of flying insects (41). Thus, it follows that the low insect numbers also may be an important factor that contributes to low or inappropriate fat reserves deposited by bats that hibernate in the northeastern United States. It has been postulated that increased use of some pesticides to control insect pest species has directly killed insects upon which insectivorous bats depend for food (T. McCabe, New York State Entomologist). Such contaminants that enter aquatic ecosystems or are deposited on plants upon which many insects feed may contribute to declines in insect populations and the cascade effect that these losses have directly and indirectly on aerial feeding birds and bats. Alternatively, the bats may be indirectly affected by eating insects that have bioacumulated contaminants.
Typically, little brown myotis deposit WAT over a period of four weeks during the pre-hibernation period, beginning in early September (in New England). Three decades before WNS was discovered in 2006, Kunz et al. (37) conducted a study that quantified the amount of total body fat deposited by young and adult little brown myotis of both sexes during the pre-hibernation period. Adult males and females gained 2.3 and 2.1 g, respectively, during this period, accounting for 32.9 and 29.6% of the pre-hibernation body mass. By contrast, young-of- the-year of both sexes weighed about 1 to 2 g less than adults as they entered hibernation in mid-October. The fat indices (fat mass/lean body mass) of both sexes and ages were not significantly different at this time. The absolute amount of WAT deposited by young-of-the-year was significantly less than adults. The similarity in fat indices among the sexes and the two age cohorts reflects the fact that lean body mass of young-of-the-year was significantly less than adults. Thus, young males and females enter hibernation in their first winter at lower lean mass and with less WAT than adults. All other factors being equal (similar hibernation conditions), this would suggest that young-of-the-year might be at greater risk of starvation from WNS than adults.
In addition to the quantity of WAT, the concentrations of different PUFAs in diets of hibernators during the autumn fattening period are an important ecological constraint influencing successful hibernation (21). PUFAs have more than one carbon-carbon double bond per molecule, as opposed to either saturated fatty acids containing no carbon-carbon double bonds, or monounsaturated fatty acids containing only one such bond per molecule. Bats, like many mammals can synthesize saturated and monounsaturated fatty acids, but they are not capable of producing PUFAs. Most plant species, however, produce two PUFAs: linoleic acid (18 carbon atoms, 2 double bonds; C18:2) and a-linolenic acid (18 carbon atoms, 3 double bonds C18:3). When mammals consume PUFAs they are incorporated into cell and organelle membranes and storage lipids (29). Laboratory experiments with several species of rodents and marsupials have revealed that the level of linoleic acid in the diet during pre-hibernation fattening influences their ability to hibernate (10, 19, 22, 24, 25, 37, 50). Thus, it appears that dietary PUFA content influences patterns of torpor in some mammals; this is unknown for hibernating bats?
Laboratory studies on golden-mantled grounds squirrels (Spermophilus lateralis) have shown that the ability to hibernate is greatest when the linoleic acid (C18:2) content of the diet is at least 33 mg/g, but less than 74 mg/g. Ground squirrels fed a 33-74 mg linoleic acid/g diet: 1) were more likely to hibernate, 2) spent less time fasting prior to the onset of torpor, 3) had lower metabolic rates during torpor, and 4) had longer torpor bouts than those maintained on diets containing either less or more linoleic acid (14, 16, 17, 18, 19). It also has been demonstrated that the amount of a-linolenic acid (C18:3) in the diet influences the torpor patterns of S. lateralis in a manner identical to that for linoleic acid (20).
Another consequence of low fat reserves in hibernating females may result in lower reproductive success in the following spring, assuming that WAT is the primary source of circulating leptin (37, 38). Temperate hibernating bats are unique among mammals in that they mate in the autumn before entering hibernation (32, 48). Females store sperm in their uteri and normally ovulate upon the final arousal from hibernation in spring. In other mammals that have been studied, including humans, WAT is the primary source of leptin that stimulates the cascade of hormones, starting with gonadotropin releasing-hormone (GnRH) from the hypothalamus, follicle stimulating hormone (FSH) and luteinizing hormone (LH) from the anterior pituitary gland, and ultimately to the ovaries that leads to follicle development and ovulation (2). Thus, WAT in hibernating bats provides the essential fuel needed for periodic arousals, and a certain minimal (but unknown) quantity of fat reserves are required in spring to secrete sufficient quantities of leptin for ovulation and subsequent gestation (46, 47, 52, 53). If bats with WNS deplete their WAT reserves before the end of hibernation, one can expect to find reduced fecundity among those females that survive the winter. In the northernmost geographic range of little brown myotis in North America, fewer than 50% of females produce young each year compared to over 90% of females at lower latitudes (37), adding support for the hypothesis that WAT and leptin are essential for successful reproduction.
All bats in temperate regions are insectivorous, and the summer diets of hibernating Myotis spp. in the northeastern US consists almost entirely of insects found in the Orders Coleoptera, Diptera, Hymenoptera, Lepidoptera, Neuroptera and Trichoptera(3, 6, 31, 40). The relative proportions of these insect groups in the diet, however, vary with location. Moreover, insect species vary in their ability to synthesize PUFAs, with plant-eating insects typically containing more PUFAs than those which feed on detritus, and insects in the orders Diptera and Lepidoptera cannot synthesize either linoleic or a-linolenic acids. Thus, the PUFA levels in some insects depend entirely upon their diets. In contrast, insects of the orders Neuroptera, Orthoptera, Homoptera, and Hymenoptera, are able to synthesize linoleic acid. The PUFA content of insects therefore varies with both species and with their diets (7, 51). It is quite likely that the inability of bats with WNS to remain torpid during hibernation reflects the consumption of insects in autumn with a PUFA content that is not conducive to torpor. The autumn diets of bats in areas where WNS has been reported may have PUFA contents that are substantially different from those in areas unaffected by WNS, in large part due to differences in insect species composition and/or PUFA contents of the same insect taxa found at both sites. Alternatively, differences in PUFA composition of insects at sites affected and unaffected sites may reflect differential mortality of certain insects due to pesticide-related effects.
Research Goals
Hypotheses and Predictions
Aerial insects will be sampled using Malaise traps and Hook rotator traps to assess the insects available to bats (35). These traps will be deployed at sites judged to be potential foraging habitats used by M. lucifugus. Malaise traps are designed to capture random samples of flying insects. Hook rotator UV light traps are designed to capture insects (mostly lepidopterans) at hourly intervals throughout the night. Total nightly biomass (dry mass) will be determined gravimetrically. Sub-samples of these insects will be sorted by family, weighed, and frozen for analysis of total fat content and PUFAs.
Bats will be captured bi-monthly, during nightly emergence and again upon return from nightly feeding from mid-August through mid-November at affected and unaffected swarming sites and hibernacula using harp traps (34, 38). Each bat will be sexed, aged (adult and young-of year), assessed for prior (females) and current (males) reproductive status, and weighed to the nearest 0.1 g. All captured bats will be marked with 2.9 mm lipped bands and released at the site of capture. Additionally, samples of 20 bats from each cohort will be collected from 2 affected and 2 unaffected sites in mid-February and again in mid-April to compare body composition and dietary PUFA.
A sub-sample of 20 bats of each sex and age cohort collected upon return from feeding will be euthanized for the purposes of assessing body composition (37, 43, 44), for collecting stomach contents, and for collecting biopsies for PUFA analysis (see below). To assess body composition, both whole carcasses and separate body components (heart, liver, lungs, spleen, brown fat, stomach, intestines) will be dissected, minced, dried to constant mass, and assessed for water content, lean dry mass, and total body fat. Total body fat will be extracted using Soxhlet distillation flasks. Water content, lean dry mass, and total body fat will be determined by difference (44). Hypothesis 1 will be supported if autumn body mass and WAT is significantly lower in bats collected at affected than at unaffected sites. Hypothesis 2 will be supported if body mass and WAT of bats at affected sites are significantly lower in mid-winter and late winter samples from unaffected sites.
The average fatty acid compositions of M. lucifugus diets during the fall fattening period will be determined by collecting biopsies of WAT from 20 bats captured at each study site (cave) and measuring their fatty acid compositions. The concentration of PUFAs found in the WAT of mammals depends on the amount of these fatty acids present in the diet during pre-hibernation fattening (Gunstone 1996). To provide a relative index of dietary PUFA content, WAT samples collected from each bat will be analyzed for fatty acid content using gas chromatography, as summarized by Frank (2002), which permits the isolation and identification of all fatty acid types with 12 to 22 carbon atoms in length. Hypothesis 3 will be supported if the mean total PUFA content (C18:2 + C18:3) in WAT from bats collected at WNS sites is significantly lower than WAT collected from bats at unaffected sites.
The insect species composition of the late summer and autumn diets of M. lucifugus collected atall study sites will be determined by analyzing the fecal contents (31, 36). Hypothesis 4 will be supported if the relative proportions of various insect species (orders) in the diets of bats collected from WNS sites are significantly different from those found at sites unaffected by WNS. The mean total (C18:2 + C18:3) PUFA content of each insect order available at each study site will be determined by first collecting samples of all flying insects present during the fall (September 2008) at each study site by deploying light traps at night. The insects collected will then be separated into orders, and each order will be analyzed for PUFAs using the techniques described above. Hypothesis 5 will be supported if the same insect taxa collected at the affected sites have mean total PUFA contents that are significantly lower than the mean total PUFA contents of the same insect orders collected at unaffected sites.
Impact of WNS on Bat Populations
Insectivorous bat species consume enormous quantities of insects nightly (3, 33, 37), and at times (especially during peak lactation) females may consume quantities of insects equal to their body mass in a single night (39). Many of the insect species upon which bats feed include pests that damage local gardens and agricultural crops (1, 49). Given that insectivorous bats in the US provide important ecosystem services by suppressing insect populations that otherwise would feed on agricultural crops, ornamental plants, and garden crops (8), loss of a major portion of bat populations could seriously alter ecosystem functions.
Broader Impacts
The PI and co-PIs each have excellent track records of including such students in their research. Environmental factors that contribute to the success of insectivorous bats that hibernate for several months of the year can provide new insight into the mechanisms that influence winter survival and reproductive success. Our research on bats with WNS, in particular, provides an opportunity to: 1) highlight the ecological and economic value of these fascinating mammals, 2) emphasize the fragile and complex nature of factors that contribute to mortality, 3) and to draw attention to conservation issues through traditional print, radio, and TV media, and web-based Internet sources. Within the past three months, the PI’s preliminary research and perspectives on WNS have been featured on NPR’s “Science Friday,” the Boston Globe, “What are these bats telling us about the environment that we live in?,” and Plenty Magazine “Experts still looking for cause of mysterious bat die-offs.” Recently, the PI was engaged by a Boston-area TV station (Channel 5), interviewed by anchor David Brown to discuss WNS, and aired on Monday and Tuesday, June 30 and July 1, 2008. Another TV interview is scheduled with.news reporter Ken Tucci (Channel 4-TV) for mid-July. The PI (Kunz) also presented a seminar on WNS on July 2 to the Boston Grotto, a caving organization in the northeastern US interested in working closely with scientists to help solve questions related to WNS.
Time Line
July 2008
Assemble and purchase needed equipment supplies. Identify field sites that represent localities affected and unaffected by WNS. Coordinate our research efforts with those being conducted in other laboratories (e.g. Cornell, USGS, New York State Department of Environmental Conservation).
August-November 2008
Pre-hibernating bats will be captured and processed (sexed, aged, measured, weighed, and banded) at bi-monthly intervals from mid-August through mid-November as they emerge nightly from and return to selected pre-hibernation swarming sites at caves and mines where WNS has been identified and where it has not (controls). Samples of bats will be euthanized and frozen in the field for subsequent laboratory analysis. Complete body composition analysis will be conducted using destructive sampling in the PI’s laboratory. Stomach contents and samples of subcutaneous WAT deposits of bats will be collected for analysis of PUFAs in Frank’s laboratory. Insects captured in Malaise and Hook rotator traps will be identified to Order and frozen for laboratory analysis of PUFAs.
December 2008-May 2009
Hibernating bats will be collected from selected mines and caves in December and in April and processed as described above. In addition, before bats are euthanized, 50 µL of blood will be collected from each bat for analysis of plasma leptin concentration (analyzed in Widmaier’s laboratory), and immune responses during hibernation, in collaboration with DeeAnn Reeder (Bucknell University), Beth Buckles (Cornell University), and Marianne Moore (Boston University). Biopsies of WAT will be collected from hibernating bats for analysis of PUFAs in Frank’s laboratory. Body composition analysis of bats collected during the pre-hibernation and hibernation periods will be conducted in Kunz’s laboratory. Statistical analyses and manuscript preparation will be conducted during this period both in the PI’s and Co-PI’s laboratories.
As part of our collaborative efforts, we will be coordinating our sample collections with investigators from other laboratories who will be assessing frequency and duration of torpor bouts using temperature-sensitive radiotransmitters. The latter data will be compared with our results from our analyses of WAT and PUFA at affected and unaffected sites. We will also coordinate our research with studies investigating the role of brown adipose tissue on arousal rates and immune functions.
Description |
Quantity |
Amount |
Amount Requested |
In-Kind |
Graduate Student Stipend |
12 months |
$32,170 |
|
$32,170 |
Field Assistant |
5 months |
$15,000 |
$15,000 |
|
Travel Expenses (gasoline, per diem) |
5 months |
$10,000 |
$10,000 |
$10,000 |
Supplies (glassware, petroleum ether, sample vials, batteries, insect traps, Tyvek suits) |
|
$5,000 |
$5,000 |
$6,000 |
Publication Cost (page charges) |
40 pages |
$100/page |
$4,000 |
|
Total Direct Cost |
|
|
$34,000 |
|
Indirect Cost (20% of Direct Cost) |
|
|
$6,800 |
|
TOTAL COST |
$40,800 |
$48,170 |
LITERATURE CITED
(1) Acosta, S.J., and D. Morton. 2003. Diet of the big brown bat, Eptesicus fuscus, from Pennsylvania and Western Maryland. Northeastern Naturalist, 10: 89-104.
(2) Anthony, E.L.P. 2000. Endocrinology of reproduction in bats: central control. Pp. 1-26, In: Reproductive Biology of Bats (E.G. Crichton and P.H. Krutzsch, eds.). Academic Press, San Diego.
(3) Anthony, E.L.P., and T.H. Kunz. 1977. Feeding strategies of the little brown bat, Myotis
lucifugus, in southern New Hampshire. Ecology, 58: 775-786.
(4) Anthony, E.L.P., M.H. Stack, and T.H. Kunz. 1981. Night roosting and the nocturnal time budgets of the little brown bat, Myotis lucifugus: effects of reproductive status, prey density, and environmental conditions. Oecologia, 51: 151-156.
(5) Barnes, B.M. 1989. Freeze avoidance in a mammal: body temperatures below 0°C in an Arctic hibernator. Science, 244: 1593-5.
(6) Brack, V., and R. K. LaVal. 1985. Food habits of the Indiana bat in Missouri. Journal of Mammalogy, 66: 308-315.
(7) Buckner, J.S. 1993. Cuticular polar lipids of insects. Pages 227-270, In: Insect Lipids: Chemistry, Biochemistry, and Biology (D. W. Stanley-Samuelson and D.R. Nelson, eds.). University of Nebraska Press, Lincoln.
(8) Cleveland, C.J., J.D. Frank, P. Federico, I. Gomez, T.G. Hallam, J. Horn, J. Lopez, G.F. McCracken, R.A. Medellin, A. Moreno-V, C. Sansone, J.K. Westbrook, and T.H. Kunz. 2006. Economic value of the pest control service provided by Brazilian free-tailed bat in south-central Texas. Frontiers of Ecology and the Environment, 4: 238-243.
(9) Feldhamer, G.A., L.C. Drickhamer, S.H. Vessey, and J.F. Merritt. 1999. Mammalogy: Adaptation, Diversity, and Ecology. WCB McGraw-Hill, New York.
(10) Florant, G.L., H.S. Ameednuddin, and D.A. Rintoul. 1993. The effect of a low essential fatty acid diet on hibernation in marmots. American Journal of Physiology, 264: R747-753.
(11) Florant, G.L. 1998. The importance of essential fatty acids. American Zoologist, 38: 331-340.
(12) Folch, J., M. Lees, and G. Stanley. 1957. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226: 497-507.
(13) Frank, C.L. 1991. Adaptations for hibernation in the depot fats of a ground squirrel (Spermophilus beldingi). Canadian Journal of Zoology, 69: 2707-2711.
(14) Frank, C.L. 1992. The influence of dietary fatty acids on hibernation by golden-mantled ground squirrels (Spermophilus lateralis). Physiological Zoology, 65: 906-920.
(15) Frank, C.L. 1994. Polyunsaturate content and diet selection by ground squirrels (Spermophilus lateralis). Ecology, 75: 458-463.
(16) Frank, C.L., and K.B. Storey. 1995. The optimal depot fat composition for hibernation by golden-mantled ground squirrels (Spermophilus lateralis). Journal of Comparative Physiology, B, 164: 536-542.
(17) Frank, C.L., and K.B. Storey. 1996. The effect of total unsaturated fat content on hibernation. Pp. 211-216, In:Adaptations to the Cold. (F. Geiser, A.J. Hulbert, and S.J. Nicol, eds.). University of New England Press.
(18) Frank, C.L., E.S. Dierenfeld, and K.B. Storey. 1998. The relationship between lipid peroxidation, hibernation, and food selection in mammals. Integrative and Comparative Biology, 38: 341-349.
(19) Frank, C.L. 2002. The effects of short-term variations in diet fatty acid composition on mammalian torpor. Journal of Mammalogy, 83: 1031-1019.
(20) Frank, C.L., W.R. Hood, and M.C. Donnelly. 2004. The role of a-Linolenic acid (18:3) in mammalian torpor. Pp. 71-80, In: Life in the Cold: Evolution, Mechanisms, Adaptation and Application(B.M. Barnes and H.V. Carey, eds.). Twelfth International Hibernation Symposium. Biological Papers of the University of Alaska. No. 27. Institute of Arctic Biology, University of Alaska, Fairbanks, Alaska.
(21) Frank, C. L., S. Karpovich, and B. M. Barnes. 2008. The relationship between natural variations in dietary fatty acid composition and the torpor patterns of a free-ranging arctic hibernator. Physiological and Biochemical Zoology, 81: 486-495
(22) Geiser, F., and G.J. Kenagy. 1987. Polyunsaturated lipid diet lengthens torpor and reduces body temperature in a hibernator. American Journal of Physiology, 252: R897-R901.
(23) Geiser, F., and G.J. Kenagy. 1993. Dietary fats and torpor patterns in hibernating ground squirrels. Canadian Journal of Zoology, 74: 1182-1186.
(24) Geiser, F., Stahl, B., and R.P. Learmonth. 1992. The effect of dietary fatty acids on the pattern of torpor in a marsupial. Physiological Zoology, 65: 1236-1245.
(25) Geiser, F. 1991. The effect of unsaturated and saturated dietary lipids on the patterns of daily torpor and the fatty acid composition of tissues and membranes of the deer mouse Peromyscus maniculatus. Journal of Comparative Physiology B, 161: 590-597.
(26) Geiser, F. 1994. Hibernation and daily torpor in marsupials: a review. Australian Journal of Zoology, 42: 1-16.
(27) Geiser, F., B.M. McAllen, and G.J. Kenagy. 1994. The degree of dietary fatty acid unsaturation affects torpor patterns and lipid composition of a hibernator. Journal of Comparative Physiology B, 164: 299-305.
(28) Geiser, F. 2004. Metabolic rate and body temperature. Annual Review of Physiology, 66: 239-274.
(29) Gunstone, F.D. 1996. Fatty Acid and Lipid Chemistry. Blackie Academic and Professional, Glasglow, Scotland.
(30) Kayser, C. 1965. Hibernation. Pp. 180-296, In: Physiological Mammalogy, Volume II. (W. Mayer and R. Van Gelder, eds.). Academic Press, New York.
(31) Kellner, A. M. E., and A. S. Harestad. 2005. Diets of bats in coastal rainforests on Vancouver Island, British Columbia. Northwestern Naturalist, 86: 45-48.
(32) Kronfeld-Schor, N., C. Richardson, B.A. Silvia, T.H. Kunz, and E.P. Widmaier. 2000. Dissociation of leptin secretion and adiposity during prehibernatory fattening in little brown bats. American Journal of Physiology, 279: R1277-R1281.
(33) Kunz, T.H. 1974. Feeding ecology of a temperate insectivorous bat (Myotis velifer). Ecology, 55:693-711.
(34) Kunz, T.H. (ed.). 1988a. Ecological and Behavioral Methods for the Study of Bats. Smithsonian Institution Press, Washington, D.C.
(35) Kunz, T.H. 1988b. Methods of assessing the availability of prey to insectivorous bats. Pp. 191-210, In: Ecological and Behavioral Methods for the Study of Bats (T.H. Kunz, ed.). Smithsonian Institution Press, Washington, D.C.
(36) Kunz, T.H., and J.O. Whitaker, Jr. 1983. An evaluation of fecal analysis for determining food habits of insectivorous bats. Canadian Journal of Zoology, 61: 1317-1321.
(37) Kunz, T.H., J.A. Wrazen, and C.D. Burnett. 1998. Changes in body mass and body composition in pre-hibernating little brown bats (Myotis lucifugus). Ecoscience, 5: 8-17.
(38) Kunz, T.H., E. Bicer, W.H. Hood, M. Axtell, W. Harrington, B. Silvia, and E.P. Widmaier. 1999. Plasma leptin decreases during lactation in female bats. Journal of Comparative Physiology B, 169: 61-66.
(39) Kurta, A., G.P. Bell, K.A. Nagy, and T.H. Kunz. 1989. Energetics of pregnancy and lactation in free-ranging little brown bats (Myotis lucifugus). Physiological Zoololgy, 62:804-818.
(40) Kurta, A. and J. O. Whittaker, Jr. 1998. Diet of the endangered Indiana bat (Myotis sodalis) in the northern edge of it’s range. American Midland Naturalist, 140: 280-286.
(41) McCracken, J. 2008. Common insect-eating birds suffer dramatic declines. http://www.birdlife.org/news/news/2008/03/Canada_insectivore_decline.html.
(42) Mead, J., Alfin-Slater, D., Howton, D., and G. Popjak. 1986. Lipids: Chemistry, Biochemistry, and Nutrition. Plenum Press, New York.
(43) Reynolds, R.S. and T.H. Kunz. 2000. Changes in body composition during reproduction and postnatal growth in the little brown bat, Myotis lucifugus (Chiroptera: Vespertilionidae). Ecoscience, 7: 10-17.
(44) Reynolds, D.S., and T.H. Kunz. 2001. Destructive body composition analysis: a practical guide, 39-55, In: Body Composition Analysis (J.R. Speakman, ed.). Oxford University Press, London.
(45) Reynolds, R.S., J.C. Sullivan, and T.H. Kunz. 2008. Evaluation of total body electrical conductivity (TOBEC) to estimate the body composition of a small mammal, Myotis lucifugus (Chiroptera: Vespertilionidae). Journal of Wildlife Management (in press).
(46) Schulz, L.C, K.T. Townsend, T.H. Kunz, and E.P. Widmaier. 2006. Leptin and placental development in the little brown bat (Myotis lucifugus). Journal of Experimental Zoology. A, 305: 174-183.
(47) Schulz, L.C., K.T. Townsend, T.H. Kunz, and E.P. Widmaier. 2007. Inhibition of trophoblast invasiveness in vitro by immunoneutralization of leptin in the bat, Myotis lucifugus (Chiroptera). General and Comparative Endocrinology, 150: 59-65.
(48) Townsend, K.L, T.H. Kunz, and E.P. Widmaier. 2008. Changes in body mass, plasma leptin, and mRNA levels of leptin receptor isoforms during the premigration/prehibernation period in Myotis lucifugus. Journal of Comparative EndocrinologyB, 178: 217-223.
(49) Whitaker, J.O., Jr. 1995. Food of the big brown bat Eptesicus fuscus from maternity colonies in Indiana and Illinois. American Midland Naturalist, 134: 346-360.
(50) Withers, K., J. Billingsley, D. Hirning, A. Young, P. McConnell, and S. Carlin. 1996. Torpor in Smithopsis macroura: effects of dietary fatty acids. Pp. 217-22, In: Adaptations to the Cold (F. Geiser, A.J. Hulbert, and S.J. Nicol, eds.). University of New England Press.
(51) Urich, K. 1990. Comparative Animal Biochemistry. Springer-Verlag, New York.
(52) Zhao, J., T.H. Kunz, N. Tumba, L.C. Schulz, C. Li, M. Reeves, and E.P. Widmaier. 2003. Comparative analysis of expression and secretion of placental leptin in mammals. American Journal of Physiology (Integrative and Comparative Physiology), 285: R438-446.
(53) Zhao, J., K.L. Townsend, L.C. Schulz, T.H. Kunz, C. Li, and E.P. Widmaier. 2004. Leptin receptor expression increases in placenta, but not hypothalamus, during gestation in Mus musculus and Myotis lucifugus. Placenta, 25: 712-722.
INVESTIGATOR QUALIFICATIONS
Thomas H. Kunz, PI
a. Professional Preparation
University of Central Missouri, B.S. Biology, 1961
University of Central Missouri, M.S. Education, 1962
Drake University, M.S. Biology. 1968
University of Kansas, Ph.D. Systematics and Ecology, 1971
b. Appointments
Director, Center for Ecology and Conservation Biology, 1996-present
Professor, Department of Biology, Boston University, 1984-present
Chairman, Department of Biology, Boston University, 1985-1990
Associate Professor (with tenure), Department of Biology, Boston University, 1977-1984
Assistant Professor, Department of Biology, Boston University, 1971-1977
c. Publications
Five publications most closely related to proposed research
Anthony, E.L.P., and T.H. Kunz. 1977. Feeding strategies of the little brown bat, Myotis lucifugus, in southern New Hampshire. Ecology, 58: 775-786.
Anthony, E.L.P., M.H. Stack, and T.H. Kunz. 1981. Night roosting and the nocturnal time budgets of the little brown bat, Myotis lucifugus: effects of reproductive status, prey density, and environmental conditions. Oecologia, 51: 151-156.
Kronfeld-Schor, N., C. Richardson, B.A. Silvia, T.H. Kunz, and E.P. Widmaier. 2000. Dissociation of leptin secretion and adiposity during prehibernatory fattening in little brown bats. American Journal of Physiology, 279: R1277-R1281.
Reynolds, R.S. and T.H. Kunz. 2000. Changes in body composition during reproduction and postnatal growth in the little brown bat, Myotis lucifugus (Chiroptera: Vespertilionidae). Ecoscience, 7: 10-17.
Reynolds, D.S., and T.H. Kunz. 2001. Destructive body composition analysis: a practical guide, 39-55, In: Body Composition Analysis (J.R. Speakman, ed.). Oxford University Press, London.
d. Synergistic Activities
(i) Undergraduate Student Research Mentor: For the past 37 years, Kunz has advised and supervised research projects of over 60 undergraduate students, 25 of which have led to publications in peer-reviewed journals. During this period, he has been the PI on several NSF-funded undergraduate research programs (URP 10 years and REU 12 years).
(ii) Tropical Ecology Program in Ecuador: Kunz was instrumental in developing a semester-long tropical ecology program in Ecuador designed for undergraduate students. This program provides unique educational and research opportunities for qualified undergraduate students from Boston University and students who attend other colleges and universities (www.bu.edu/cecb).
(iii) Public and Professional Lectures: Kunz is regularly invited to give public lectures to local school groups (K-12), conservation organizations, and museums about his research on bats. He also is regularly invited to give lectures at colleges and universities and at national and international meetings on topics related to his research.
(iv) Professional Societies: Kunz is an active member of several professional societies and is the recent past president of the American Society of Mammalogists (2000-2002). Kunz also serves on the scientific advisory boards of several non-government organizations, including the Lubee Bat Conservancy (USA), Bat Conservation International (USA), and IUCN—World Conservation Union (Gland, Switzerland).
e. Collaborators and Other Affiliations
(i) Collaborators: Manfred Ayasse (University of Ulm, Germany); Margrit Betke (Boston University), Hari Bhat (Institute of Virology, India); Cutler Cleveland (Boston University); Brock Fenton (University of Western Ontario, Canada); Craig Frank (Fordham University); Gareth Jones (University of Bristol, UK); Sid Gauthreaux (Clemson University); Thomas Hallam (University of Tennessee); Elisabeth Kalko (University of Ulm, Germany); Jeffrey Kelly (University of Oklahoma); Ron Larkin (University of Illinois); Thomas Little, (Boston University), Gurpathy Marimuthu (Kamaraj Madurai University, India); Gary McCracken (University of Tennessee); Stuart Parsons (University of Aukland, New Zealand); John Westbrook (USDA); Eric Widmaier (Boston University); Akbar Zubaid (Universiti Kebangsaan Malaysia); Christian Voigt (Institute of Zoo and Wildlife Research, Germany).
(ii) Graduate and Postdoctoral Advisors
Rodney A. Rogers, Emeritus (M.A.), Drake University
J. Knox Jones, Jr.--deceased (Ph.D.), University of Kansas
(iii) Graduate Students and Post-doctoral Scholars Sponsored (past 5 years)
Graduate Students (40 total): Polly Campbell, University of New Mexico (2000-2005); Chris Richardson, University of Wisconsin (1998-2006); Lizabeth Southworth, Saginaw Valley State University (1996-2004); Gloriana Chaverri, Universidad Nacional, Costa Rica (2001-2006); Benjamin Rinehart, University of Colorado (1997-2007); Jason Horn, Cornell (2000-2007); Mariana Munoz-Romo, Universidad Simon Bolivar (2004-2008), Susan Murray, University of Massachusetts (1999-present); Pablo Jarrin, Pontificia Universidad Catolica del Ecuador (2001-present), Jonathan Reichard, Cornell University (2003-present); Louise Allen, Michigan State University (2003-present); Marianne Moore, Evergreen College (2005-present).
Post-doctoral Scholars (15 total): DeeAnn Reeder, University of California, Davis (2001-2004); Tigga Kingston, Boston University (2001-2005); Nickoloy Hristov, Wake Forest University (2004-2007); Robert Hodgkison, University of Aberdeen (2004-present), Christopher Richardson, Boston University (2006-present).
Craig L. Frank, Co-PI
a. Professional Preparation
Herkimer County Community College, A.S. Biology, 1981
State University of New York at Albany, B.S. Biology, 1984
Kansas State University, M.S. Biology, 1987
University of California, Irvine, Ph.D. Biology. 1992
NATO Postdoctoral Fellow, Carleton University, Canada, 1992-1994
NSERC Postdoctoral Fellow, Carleton University, Canada, 1994
b. Appointments
Associate Professor,Dept. of Biol. Sciences, Fordham University, 2001-present
Assistant Professor, Dept. of Biol. Sciences, Fordham University. 1994-2001
c. Publications
Five publications most closely related to proposed research
Carey, H.V., C.L. Frank, and, J. Seifert (2000). Hibernation induces oxidative stress and
activation of NFkB in ground squirrel intestine. Journal of Comparative Physiology B., 170: 551-559.
Harlow, H.J., and C.L. Frank (2001). The role of dietary fatty acids in the evolution of
spontaneous and facultative hibernation patterns in prairie dogs. Journal of Comparative Physiology B., 171:77-84.
Frank, C.L. (2002). The effects of short-term variations in diet fatty acid composition on
mammalian torpor. Journal of Mammalogy, 83: 1031-1019.
Frank, C.L., W.R. Hood, and M.C. Donnelly (2004). The role of a-Linolenic acid (18:3) in mammalian torpor. Pages 71-80 In: Life in the Cold: Evolution, Mechanisms, Adaptation and Application. Edited by B. M. Barnes and H.V. Carey. Institute of Arctic Biology Press.
Frank, C. L., S. Karpovich, and B. M. Barnes (2008). The relationship between natural
variations in dietary fatty acid composition and the torpor patterns of a free-ranging arctic hibernator. Physiological and Biochemical Zoology, 81(4):486-495.
d. Synergistic Activities
(i) Chair of the Electronic Communications Committee. Soc. of Integrative & Comp. Biol.
(ii) Associate Editor, Journal of Mammalogy
(iii) Chapter Secretary, Sigma Xi (Fordham University Chapter)
(iv) Editorial Board Member, Physiological and Biochemical Zoology
e. Collaborators and Other Affiliations
(i) Collaborators: Dr. Brian M. Barnes (Institute of Arctic Biology, University of Alaska), Dr. Hannah V. Carey (School of Veterinary Medicine, University of Wisconsin), Dr. Thomas H. Kunz (Department Biology, Boston University).
(ii) Graduate/Postdoctoral Advisors:
Dr. Christopher C. Smith, Division of Biology, Kansas State Univ. (M.S.)
Dr. O. J. Reichman, University of California at Santa Barbara (M.S.)
Dr. Albert F. Bennett, University of California at Irvine (Ph.D.)
Dr. Kenneth B. Storey, Carleton University, Ottawa (postdoctoral)
(iii) Thesis Advisor and Postgraduate-Scholar Sponsor:
Mcdonough, Anne A. (2009). The role of linoleic acid in the torpor patterns of free-ranging eastern chipmunks (Tamias striatus). (M.S.).
Serra, Theresa (2006). The torpor patterns and super-cooling of free-ranging Spermophilus lateralis. (B.S.)
Ardito, Christine (2006). The effects of diet a-tocopherol isomer levels on the rate of lipid peroxidation in Tamias striatus. (B.S.)
McCool, John (2000). Diet selection by the eastern chipmunk in relation to hibernation. (M.S.)
Hood, Wendy (2000–2002). Postdoctoral Research Associate, Fordham University.
Eric P. Widmaier, Co-PI
a. Professional Preparation
Northwestern University, BA/MA Biological Sciences, 1979
University of California, San Francisco, Ph.D. Endocrinology, 1984
Worcester Foundation for Experimental Biology, Post-doc 1984-1986
The Salk Institute, Post-doc 1986-1988
b. Appointments
Professor, Department of Biology, Boston University (1999-present)
Associate Professor (with tenure), Department of Biology, Boston University (1994-1999)
Assistant Professor, Department of Biology, Boston University (1988-1994)
c. Publications
Five publications most closely related to proposed research
Townsend KL, Lorenzi ML, Widmaier EP. 2008. High-fat diet-induced changes in body mass and hypothalamic gene expression in wild-type and leptin-deficient mice. Endocrine (in press).
Townsend KL, Kunz TH and Widmaier EP. 2008. Changes in body mass, plasma leptin, and mRNA levels of leptin receptor isoforms during the premigration/prehibernation period in Myotis lucifugus. J Comp Physiol B, 178:217-23.
Schulz LC, Townsend K, Kunz TH and Widmaier EP. 2007. Inhibition of trophoblast invasiveness in vitro by immunoneutralization of leptin in the bat, Myotis lucifugus (Chiroptera). Gen Comp Endo 150:59-65.
Reeder DM, Raff H, Kunz TH, and Widmaier EP. 2006. Characterization of pituitary-adrenocortical activity in the Malayan flying fox (Pteropus vampyrus). J Comp Physiol B, 176:512-519.
Reeder DM, Kosteczko NS, Kunz TH and Widmaier EP. 2006. The hormonal and behavioral response to group formation, seasonal changes and restraint stress in the highly social Malayan flying fox (Pteropus vampyrus) and the less social little golden-mantled flying fox (P. pumilus) (Chiroptera: Pteropodidae). Horm Behav 49:484-500.
d. Synergistic Activities
(i) Undergraduate Student Research Mentor
Since 1988, I have mentored the research projects of 45 undergraduates (29 women/16 men; 7 underrepresented minorities), including many sponsored by NSF-REU. All of these students have since completed or enrolled in MD, PhD, or MD/PhD programs, Biology Teaching positions, biotechnology, or physician’s assistant programs. In addition, I teach Systems Physiology and Comparative Physiology to undergraduates and graduate students, and recently received the University’s highest award for Teaching Excellence.
(ii) Public Outreach and Educational Programs
K-12: Developer of educational Cable Television program (“Widmaier’s World of Animals”), 1995-1998, designed to increase science awareness in K-12 students in Massachusetts.
Biology Education for Teaching Professionals (Howard Hughes Undergraduate Progress in Biology) Frontiers of Biology (1993-98): This was a team-taught, televised educational program offered by Boston University for graduate credit, directed to secondary school science teachers in New England. The aim of this lecture series was to update science teachers on current topics in biology, to assist them in achieving their goal of educating young people in the state-of-the-art life sciences. I was co-creator of the series, one of the lecturers, and co-PI on the grant that funded the series.
Textbooks and Popularization of Science
I have authored two tradebooks on physiology targeted to the general public. The goal was to portray the process of doing science, and the relationship of current discoveries in physiology to our everyday lives. The first book, “Why Geese Don’t Get Obese (and we do): How Evolution’s Strategies for Survival Affect our Everyday Lives,” won the Choice Award from the American Libraries Association (Best Academic Book, 1998). “The Stuff of Life: Profiles of The Molecules That Make Us Tick,” was released September 2002. I have also published educational articles in lay journals and magazines on evolution, obesity, and stress, and been invited to appear on many radio and television programs to discuss science and research. I have also recently coauthored the 9th through 11th editions of the textbook Human Physiology: The Mechanisms of Body Function (McGraw-Hill), and the 1st edition of Biology, an introductory textbook (McGraw-Hill).
(iii) Recent Professional Service
Editorial Boards: Neuroendocrinology (1997-2001); Endocrinology (1992-2001); J Experimental Zoology (1998-present); Endocrine (1999-present); American Journal of Physiology (1992-1996); NIH Study Section (ICP) 2002, 2003; NSF IBN Review Panel (IAB) 2002; Ad-hoc reviewer for NSF and Veteran’s Administration; Member, Faculty of Biology 1000
e. Collaborators and Other Affiliations
(i) Collaborators last 48 months: H. Raff and E. Bruder, Med. Coll. WI
(ii)
Graduate and Postdoctoral Advisors: Mary F. Dallman (Ph.D.), University of California, San Francisco; Peter F. Hall (Post-doc), Worcester Foundation for Experimental Biology; Wylie Vale (Post-doc), The Salk Institute
(iii) Thesis Advisor (Ph.D. only) and Post-doctoral Sponsor
M. Lynes (2007-present); J. Hong (2000-05); K. Townsend (2003-08); J. Zhao (1998-03); J. Wang (1999-02); Kyeong-Hoon Jeong (1993-98); A. Zilz (1995-98); I. Sarel, (1990-95); M. Nagaya (1990-94); M. Arai, (1989-93); Dr. C. Richardson (postdoc 2007-present); Dr. D. Reeder (post-doc 2001-04); Dr. L. Schulz (post-doc 2002-05); Dr. N. Kronfeld-Schor (post-doc 1998-99); Dr. E. Pride (post-doc 2005-06)
(iv) Total number of graduate students advised: 10 (does not include MA students)
(v) Total number of postdoctoral scholars advised: 4
Jonathan D. Reichard, Ph.D. Candidate
a. Professional Preparation
Cornell University, B.S. Natural Resource Management. 1996
Boston University, Ph.D. Candidate, Biology
b. Appointments
Peace Corp Volunteer, Mali, West Africa, 1997-1999
Biology Teacher, Newman School, Boston, MA. 1999-2003
Research Assistant, Vermont Fish and Wildlife Service and University of Vermont, 2003
Graduate Teaching Fellow, Department of Biology, Boston University, 2003-2005
Research Assistant, Department of Biology, Boston University, 2005-present
c. Publications
Betke, M., D.E. Hirsh, N.C. Makris, G.F. McCracken, M. Procopio, N.I. Hristov, S. Teng, A. Bacchi, J.D. Reichard, J.W. Horn, S. Crampton, C.J. Cleveland, and T.H. Kunz. 2008. Thermal imaging reveals significantly smaller Brazilian free-tailed bat colonies than previously estimated. Journal of Mammalogy, 89:18-24.
Reichard, J.D., L. Gonzalez, C. Casey, and T.H. Kunz. (Submitted). Nightly emergence behavior of the Brazilian free-tailed bat, Tadarida brasiliensis: Influence of intrinsic and extrinsic factors. Journal of Mammalogy.
d. Honors and Awards
(i) Awards
Best Student Poster Award, North American Symposium on Bat Research, 2004
(ii) Honors
Honorable Mention, National Science Foundation Graduate Research Fellowship, 2005
(iii) Grants
American Society of Mammalogists Grant-in-Aid, 2006
e. Synergistic Activities
(i) Undergraduate Student Research Mentor
Since 2003, I have mentored five undergraduate biology majors on bat projects.
(ii) Public Outreach and Educational Programs
Since 2003, I have given four presentations on bat biology to elementary and high schools.
Since 2004, I have given several presentations on bat biology at local parks and nature reserves.
Since 2005, I have mentored four high school students on science fair projects.
(iii) Media Interactions
Since 2004, I have been featured in several newspaper articles (three in The Boston Globe) about bats and have been interviewed during production of several television and radio programs.
(iv) Professional Society
Since 2003, I have been a member of the American Society of Mammalogists
f. Collaborators and Other Affiliations
(i) Collaborators last 48 months: Margrit Betke, Jason W. Horn, Cutler J. Cleveland, Gary F. McCracken, Nickolay I. Hristov, Louise Allen, Marianne Moore, Alan Hicks (New York Department of Environmental Conservation), Charles Keller (Greehey Children’s Cancer Research Institute),
(ii) Graduate Advisor: Thomas H. Kunz