27 REPRODUCTIVE PARAMETERS OF MOOSE DURING POPULATION EXPANSION IN NORTH DAKOTA William F. Jensen 1, James J. Maskey, Jr.2, Jason R. Smith 3, and Eric S. Michel4 1Present address: North Dakota Game and Fish Department, 100 North Bismarck Expressway, Bismarck, North Dakota 58501 USA; 2University of Mary, 7500 University Drive, Bismarck, North Dakota 58504 USA; 3North Dakota Game and Fish Department, 3320 East Lakeside Road, Jamestown, North Dakota 58401 USA; 4Department of Natural Resource Management, South Dakota State University, South Dakota 57007 USA. ABSTRACT: Understanding reproductive parameters of a population is vital to management, especially during periods of population fluctuation. Therefore, our objective was to provide the first estimates of reproductive parameters such as pregnancy rates, litter size, fecundity rates, conception dates, and fetal sex ratios for a moose (Alces alces) population in North Dakota, USA. Between 1978 and 1986, the North Dakota Game and Fish Department necropsied 54 hunter-killed cow moose which were all harvested after the rut (10 November to 12 December). Pregnancy rates for calves (n = 7), yearlings (1.5 years, n = 6), and adults (≥ 2.5 years, n = 41) were 0%, 100% and 95%, respectively. Mean conception date was 2 October. Overall, mean litter size was 1.76 fetuses, twinning rate was 73.3%, and mean fecundity was 1.66 fetuses and 0.85 female fetuses/cow. Fetal sex ratio did not differ from the expected 50:50 ratio, but the odds of producing at least one male calf increased with dam age, but not dam weight or litter size. This population displayed reproductive parameters consistent with an irruptive and expanding moose population. ALCES VOL. 54: 27–36 (2018) Key words: Alces alces, reproduction, pregnancy, litter size, fetal growth rates, conception dates, fetal sex ratio, fecundity, North Dakota Several parameters influence population growth rates including offspring and adult survival rates (Coulson et al. 2001, Delgiudice et al. 2006), fecundity rates (Raithel et al. 2007, Chitwood et al. 2015), offspring sex ratio (Reuterwall 1981), and adult sex ratio (Olsson and van der Jeugd 2002). Although these parameters all affect population dynamics, their relative impor- tance varies among species and populations (Johnson et al. 2010). For moose (Alces alces), all have proved important when assessing population dynamics of certain populations. Although survival and reproductive parameters greatly influence population dynamics, biologists managing game species such as moose frequently make management decisions based upon incomplete data sets (Johnson 1996). Collecting baseline repro- ductive data from free-ranging moose popu- lations is difficult for a number of reasons: 1) they can occur at low density, 2) they often occupy dense and remote habitats that complicate survey or capture efforts, and 3) their large size makes inspection of live- captured or hunter-harvested individuals logistically difficult. Lacking requisite infor- mation to guide local management, biolo- gists often use baseline data collected elsewhere including pregnancy rate, twining rate, and sex ratio of calves. These data NORTH DAKOTA REPRODUCTIVE PARAMETERS – JENSEN ET AL. ALCES VOL. 54, 2018 28 provide helpful metrics and sideboards to consider a range of reproduction, productiv- ity, and population dynamics. Moose began recolonizing the Pembina Hills area of northeastern North Dakota, USA in the late 1950s. By the early 1960s, a small resident population was established and the first modern hunting season occurred in 1977 (Knue 1991). This pattern of pioneering new areas of North Dakota continued, and by 1984, a hunting season extended to western North Dakota. The population further expanded during the study period, establishing into drift prairie, non-traditional moose habitat (Jensen 2001). In contrast, moose have declined substantially in recent years within our study area in northeastern North Dakota. This decline appears related to adult mortal- ity resulting from parasitic diseases and localized overharvest (Maskey 2008). Despite recent closures in hunting seasons, the population remains low and continues to decline in this region. Here we summarize reproductive param- eters of the expanding moose population in northeastern North Dakota during 1978– 1986. We provide pregnancy rates, litter size, fecundity rates, and fetal sex ratios of this irruptive population. Our objective was to summarize and interpret the basic repro- ductive parameters of harvested female moose to establish baseline data useful to interpret expanding, declining, and stable moose populations in North Dakota. STUDY AREA The distribution of harvested animals was between 47.10 and 48.99 °N, and 97.14 and 100.41 °W (Fig. 1). Common vegetation included prairie junegrass (Koeleria mac- rantha), indiangrass (Sorghastrum nutans), needle and thread grass (Hesperostipa comata), brome (Bromus spp.), wheat grass (Agropyron spp.), and alfalfa (Medicago sativa). Common herbaceous species included sarsaparilla (Aralia nudicaulis), baneberry (Actea spp.), false lily-of-the- valley (Maianthemum canadensis), wild vetch (Vicia americana), and Virginia anem- one (Anemone virginiana). Common woody species included green ash (Fraxinus pennsylvanica), box elder (Acer negundo), American elm (Ulnus americana), Russian olive (Elaeagnus angustafolia), plum (Prunus spp.), apple (Malus spp.), choke- cherry (Prunus virginiana), willow (Salix spp.), paper birch (Betula papyrifera), and balsam popular (Populus balsamea) (Bakke 1980, North Dakota Forest Service 2003). Mean annual temperature in northeastern North Dakota was 3 oC and annual precipita- tion was 51 cm (Sealbloom et al. 2011). Cervids in the area included white-tailed deer (Odocoileus virginianus), moose, and occasionally elk (Cervus elaphus). The pred- ator base for cervids was limited to coyotes (Canis latrans) (Sealbloom et al. 2011). However, on rare occasions during this study (1978 to 1986), gray wolf (Canis lupus), Canada lynx (Lynx canadensis), bobcat (Lynx rufus), and black bear (Ursus ameri- canus) were observed in northeastern North Dakota (Sealbloom et al. 2011). METHODS We examined 54 cow moose harvested post-rut from 10 November to 12 December in 1978 - 1986. Hunters voluntarily brought their moose in whole to a check station (i.e., prior to removal of viscera, hide, head, or legs). Whole carcass and dressed weight were measured (Jensen et al. 2013), and when possible, uteri were examined to deter- mine reproductive status. We used incisor eruption (Peterson 1955) to identify calves (≤ 6 months), and estimated age of older moose via cementum annuli analysis of a front incisor (Matson’s Laboratory, Milltown, Montana, USA). ALCES VOL. 54, 2018 NORTH DAKOTA REPRODUCTIVE PARAMETERS – JENSEN ET AL. 29 After 1980, North Dakota Game and Fish Department (NDGFD) personnel performed these measurements (Gasaway et al. 1978, Haagenrud 1978). We also classified 5 adult cows based on their field dressed weight (≥ 290 kg; Jensen et al. 2013). To examine reproductive parameters, we separated cows into 3 age classes (calves, 1.5 years, ≥ 2.5 years; Boer 1992). We classified moose as pregnant if we observed ≥ 1 fetus upon uteral examination. McKenzie (1989) measured body mass (0.1 g) and crown-rump length (CR: point of intersection of the coronal and sagittal sutures of the skull to the tuberosity of the ischium to the nearest mm; Armstrong 1950, Morrison et al. 1959) of 52 fetuses from 30 dams. We recorded fetal sex when genitalia were sufficiently developed, which usually occurred by 6 to 8 weeks of age (n = 41 fetuses from 24 dams). We determined fetal age using the linear equations of Markgren (1969) and Crichton (1992), and then estimated conception date by backdating fetal age from the harvest date. We calculated twinning rate, fetal sex ratios, and fecundity rates (calculated as total fetuses/dam and female fetuses/dam; Caughley 1977, Johnson 1996). We used a chi-square goodness of fit test to examine whether the observed fetal sex ratio differed from 50:50. Additionally, Jensen et al. (2013) reported that moose in North Dakota do not reach peak body mass until 5.5 years old. Thus, moose ≤ 4.5 years may have less energy to allocate towards reproduction because they are still investing resources towards somatic growth. To examine whether this occurred, we separated known- age cows into 2 age classes (1.5–4.5 years, and ≥ 5.5 years) and compared twinning Fig. 1. Study area and locations where female moose were harvested in northeastern North Dakota, USA from 1978 to 1986. NORTH DAKOTA REPRODUCTIVE PARAMETERS – JENSEN ET AL. ALCES VOL. 54, 2018 30 rates between classes with a χ2 test for independence. Finally, we constructed a multiple logis- tic regression model using the glm function in Program R (R Core Team 2014; version 3.1) to examine if the odds of producing at least one male calf increased with dam age or total body mass. The model also contained a covariate for litter size to control for its effect on the response variable, and evalu- ated with the age, total weight, and sex of fetus data from 21 known dams. We calcu- lated the area under the receiver operating characteristic curve (AUC) for the model and evaluated its significance by comparing it to an intercept-only model with a likeli- hood ratio test. We considered results sig- nificant at α = 0.05. RESULTS We collected data from 54 females rang- ing in age from ≤ 6 months to 10.5 years. Pregnancy rates were 0%, 100%, and 95.1% for calves (n = 7), yearlings (1.5 years, n = 6), and adults (≥ 2.5 year, n = 41), respec- tively. One of 2 non-pregnant cows was severely emaciated with a large beaver trap on its front leg; it was clear that the trap had impacted estrus and/or conception. The mean conception date of 45 cows was 2 October ± 8.0 d (SD; range = 3 September to 21 October). Mean litter size of 45 cows was 1.76  0.07 (SE). Mean litter size was 1.0 ± 0.0 for yearlings (n = 6) and 1.85 ± 0.07 for adults (n = 39); one adult (4.5 years) had triplets (2 female, 1 male). The combined twinning rate was 73.3% (0% of yearlings, 82% of adults; Table 1, Fig. 2). Twinning rates of 1.5 – 4.5 year-olds (0.68, n = 28) and ≥ 5.5 year- olds (0.85, n = 13) were not different (χ2 1 = 1.27, P = 0.26). We determined sex of 43 (21 male and 22 female) fetuses collected from 24 adults. Fetal sex ratio did not differ from a 50:50 ratio (χ2 1 = 0.5, P = 0.88; Table 2, Fig. 2). Mean fecundity (# fetuses per cow) was 1.0 ± 0.0 for yearlings (n = 6), 1.76 ± 0.31 for adults (n = 41), and 1.66 ± 0.07 for all cows combined (n = 47). Mean fecundity of female fetuses was 0.67 ± 0.33 for yearlings (n = 3), 0.87 ± 0.17 for adults (n = 23), and 0.85 ± 0.15 for all cows combined (n = 26) (Fig. 2). The probability of producing at least one male calf increased with age (β = 1.8, Odds Ratio = 6.0, AUC = 0.89, P = 0.03, n = 21 dams), but not weight (β = -0.02, P = 0.35) or litter size (β = -0.49, P = 0.68; Table 3). DISCUSSION North American moose populations have varied dramatically through time (Peterson 1999, Post et al. 2002, Lenarz et al. 2010), with highest densities within a relatively narrow band of primary habitat roughly 300 to 750 km wide stretching from central Alaska across the central portion of the prairie provinces to the upper Great Lakes, to the northeastern states and Maritime provinces. Although this area composes about 30% of overall moose range Table 1. Reproductive parameters for 54 harvested cow moose in North Dakota, USA from 1978–1986. Age (yr) n % Pregnant % Twinning Mean Litter Size (SE) 0.5 7 0 0 0 1.5 6 100.0 0 1.00 (0.00) ≥2.5 41 95.1 85.0 1.87 (0.07) all (≥ 1.5) 47 95.7 73.3 1.76 (0.07) ALCES VOL. 54, 2018 NORTH DAKOTA REPRODUCTIVE PARAMETERS – JENSEN ET AL. 31 Fig. 2. Reproductive parameters for harvested cow moose in North Dakota from 1978 to 1986. A) Twinning rate of 45 cow moose; * indicates classification as adult but without exact age estimate. B) Proportion of litters comprised of female fetuses (n = 24 cows). C) Fecundity (total fetuses/cow) of 47 cow moose; * indicates classification as adult but without exact age estimate. D) Fecundity (female fetuses/cow) based on the examination of 26 cow moose; * indicates classification as adult but without exact age estimate. Table 2. Sex ratios of fetuses recovered from 24 known-age moose in North Dakota, USA from 1978–1986. Age (yr) n Sex of Fetus % Female Male Female 1.5 3 1 2 66.7 ≥2.5 21 20 20 50.0 All 24 21 22 51.2 Table 3. Statistics associated with the multiple logistic regression used to examine the relationships between male calf production and dam age, dam body weight, and litter size for 21 dams (≥ 1.5 yr) sampled from 1981–1985 in North Dakota, USA. Variable β SE Odds Ratio P Model Significance AUC age 1.8 0.84 6.0 0.03 χ 3 2 = 10.0, P = 0.02 0.89 body weight -0.02 0.02 0.98 0.35 litter size -0.49 1.2 0.61 0.68 NORTH DAKOTA REPRODUCTIVE PARAMETERS – JENSEN ET AL. ALCES VOL. 54, 2018 32 in North America, an estimated 89% of the North American population is found within this band of primary habitat (Jensen et al. 2018). Moose evolved as a pioneering species that disperses into recently created disturbed areas, such as those created by fire or timber operations (Peek 1974, 1998). Moose dispersing into new areas of North Dakota thus represent novel populations and provide a valuable opportunity to study reproductive rates of irrupting populations. Pregnancy and twinning rates vary amongst moose populations. For example, in his summary, Boer (1992) found that adult pregnancy rate averaged 84.2% for North American moose, whereas Ruprecht et al. (2016) reported a rate of 74.1% for moose along the southern extent of moose range. Similar pregnancy rates are reported for populations in Alaska (76–97%; Schwartz 1998), Quebec (87-90%; Ferguson et al. 2000), and Norway (60%; Solberg et al. 2002). The pregnancy rate (95.1%) of adults in our study is as high as reported elsewhere, but that of North Dakota yearlings (100%; albeit only 6 animals) is higher than reported by Ruprecht et al. (2016; 0%) and Boer (1992) (range = 17.7–64.5%). Our results are more similar to a population that expanded (irrupted) nearly simultaneously in New Hampshire where ovulation rates of yearlings (n = 187) and adults (n > 500) were 63 and >90%, respectively, during the first 10 years of harvest (Adams and Pekins 1995, Bergeron et al. 2013). Similarly, the overall twinning rate of 82% (including one litter of triplets) for females ≥ 2.5 years old was considerably higher than reported in other North American populations in Alaska (17–65%; Schwartz 1998), Minnesota (32-58%; Severud et al. 2014, 2015), New Hampshire (6-21%; Musante et al. 2010), and various Canadian provinces (41-49%; Ferguson et al. 2000). We also found no trade-off between reproduction and somatic growth as twinning rates were similar for 1.5–4.5 and ≥ 5.5 year- olds. Boer (1992) reported that moose popu- lations below carrying capacity display yearling pregnancy rates of 64.5%, adult pregnancy rates of 84.2%, and adult twin- ning rates of 44.1%. We found up to 35% higher values in our study population that was below carrying capacity on high-quality habitat, arguably values representative of an expanding, irruptive population. Our mean fecundity rates were also similar to those measured in other studies with a few notable exceptions. For example, mean fecundity was 0.97 female calves/adult (≥ 4.5 years) in south-central Alaska (Testa 2004), and 0.93 - 1.35 for multiparous (i.e., calved previously) adults in Norway (Saether et al. 1996). However, these popu- lations and data were unique as the Alaskan females first reproduced at 3-years of age, and the Norwegian sample only included multiparous females; we could not control for prior reproductive status. The mean preg- nancy and fecundity rates of our adults were considerably higher than reported for many populations along the southern range bound- ary of moose (Ruprecht et al. 2016), as well as populations found at more northern lati- tudes; albeit, summary data rarely account for the specific dynamics of populations. Nonetheless, our fecundity rates clearly indicate that the study population was highly productive, if not maximal, and reflective of an irruptive population. Although older dams were more likely to produce litters that included males, multi- ple intrinsic and extrinsic factors influence the sex ratio of offspring in several species. Intrinsic factors such as maternal body mass and maternal body condition affect offspring sex ratio (Verme 1969, 1983, Schwartz and Hundertmark 1993, Cameron 2004, Sheldon and West 2004, Cameron and Linklater 2007, Borowik and Jędrzejewska 2016). ALCES VOL. 54, 2018 NORTH DAKOTA REPRODUCTIVE PARAMETERS – JENSEN ET AL. 33 Extrinsic factors such as weather during gestation (Post et al. 1999) and timing of conception (Holand et al. 2006, Veeroja et al. 2010) are also influential, and may act individually or in concert making it difficult to detect general patterns in the offspring sex ratio of moose (Boer 1992). Regardless, we found a relationship between fetal sex ratio and maternal age structure (more male calves with age) which could possibly influence population dynamics, as measurable shifts in the sex ratio can alter population growth rates of moose (Reuterwall 1981). However, our analysis was of limited sample size (n = 21 across age classes) and we recom- mend further monitoring before considering any management strategy to alter the age structure of the population (Schwartz and Hundertmark 1993). These reproductive data from the 1970s and 1980s are representative of an expand- ing and irruptive population that contrasts with the population currently declining in North Dakota (Timmermann and Rodgers 2017). They arguably represent maximal productivity of a moose population, and their interpretation are critical when compar- ing to like data from stable or fluctuating populations. Quantifying baseline reproduc- tive parameters such as pregnancy rates, twinning rates, fecundity, and fetal sex ratios is necessary to interpret population change and whether a given harvest prescription is sustainable. Given the recent decline of North Dakota moose, continued monitoring of these reproductive parameters and female age distribution is critical to best evaluate population dynamics and guide management strategies. ACKNOWLEDGMENTS We acknowledge J. C. and J. V. McKenzie for organizing and collecting much of the data on moose fetuses originating from 1978- 1986. We thank the following NDGFD personnel for collecting data at field stations: S. Allen, A. Anderson, B. Bitterman, S. Brashears, E. Dawson, G. Enyeart, A. Galle, J. Gulke, C. R. Grondahl, R. J. Gross, D. M. Grove, L. Johnson, M. Johnson, R. Knapp, G. Kobriger, A. Kreil, S. Kohn, M. Leer, G. Link, W. Lynott, M. McKenna, R. Patterson, G. Rankin, B. Renhowe, S. Richards, R. Rollings, J. Samuelson, W. Schmaltz, D. Schmidt, J. Schulz, R. Sohn, B. Stotts, D. Tibke, L. Tripp, L. Vetter, and J. Violett. We also thank N. DeCesare and 2 anonymous reviewers for comments on previous drafts of this manuscript. This work was federally funded by Pittman-Robertson research grants. REFERENCES AdAms, K. P., and P. J. PeKins. 1995. Growth patterns of New England moose: year- lings as indicators of population status. Alces 31: 53–59. Armstrong, R. A. 1950. Fetal development of the northern white-tailed deer (Odocoileus virginianus borealis Miller). American Midland Naturalist 43: 650–666. BAKKe, E. L. 1980. Movements and habitat use of ruffed grouse in the Turtle Mountains, North Dakota. M. Sc. Thesis, University of North Dakota, Grand Forks, North Dakota, USA. Bergeron, d. H., P. J. PeKins, and K. rines. 2013. Temporal assessment of physical characteristics and reproductive status of moose in New Hampshire. Alces 49: 39–48. Boer, A. H. 1992. Fecundity of North American moose. Alces Supplement 1: 1–10. BorowiK, T., and B. Jędrzejewska. 2016. Heavier females produce more sons in a low-density population of red deer. Journal of Zoology 302: 57–62. CAmeron, E. Z. 2004. Facultative adjust- ment of mammalian sex ratios in support of the Trivers Willard Hypothesis: evidence for a mechanism. Proceedings NORTH DAKOTA REPRODUCTIVE PARAMETERS – JENSEN ET AL. ALCES VOL. 54, 2018 34 of the Royal Society Biological Sciences 271: 1723–1728. CAmeron, E. Z., and W. L. LinKlAter. 2007. Extreme sex ratio variation in relation to change in condition around conception. Biology Letters 3: 395–397. CAugHley, G. 1977. Analysis of Vertebrate Populations. John Wiley & Sons. New York, New York, USA. CHitwood, M. C., M. A. LAsHley, J. C. Kilgo, C. E. MoormAn, and C. S. DePerno. 2015. White-tailed deer popu- lation dynamics and adult female sur- vival in the presence of a novel predator. Journal of Wildlife Management 79: 211–219. Coulson, T., E. A. CAtcHPole, S. D. AlBon, B. J. T. MorgAn, J. M. PemBerton, T. H. Clutton-BrocK, M. J. CrAwley, and B. T. Grenfell. 2001. Age, sex, density, winter weather, and population crashes in soay sheep. Science 292: 1528–1531. CricHton, V. 1992. Six year (1986/87- 1991/92) summary of in utero produc- tivity of moose in Manitoba, Canada. Alces 28: 203–214. Delgiudice, G. D., J. FieBerg, M. R. Riggs, M. C. Powell, and W. PAn. 2006. A long-term age-specific survival analysis of female white-tailed deer. Journal of Wildlife Management 70: 1556–1568. Ferguson, S. H., A. R. Bisset, and F. Messier. 2000. The influences of density on growth and reproduction in moose Alces alces. Wildlife Biology 6: 31–39. GAsAwAy, W. C., D. B. HArKness, and R. A. Rausch. 1978. Accuracy of moose age determinations from incisor cementum layers. Journal of Wildlife Management 42: 558–563. HAAgenrud, H. 1978. Layers in secondary dentine of incisors as age criteria in moose (Alces alces). Journal of Mammalogy 59: 857–858. HolAnd, Ø., A. Mysterud, K. H. Røed, T. Coulson, H. GJøstein, R. B. WelAdJi, and M. Nieminen. 2006. Adaptive adjustment of offspring sex ratio and maternal reproductive effort in an iteroparous mammal. Proceedings of the Royal Society B 273: 293–299. Jensen, W. F. 2001. Lewis and Clark in North Dakota: wildlife then & now – a brief natural history of North Dakota, 1804 to present. Pages 10–19 in North Dakota Outdoors Magazine. North Dakota Game and Fish Department, Bismarck, North Dakota, USA. _____, J. R. Smith, M. Carstensen, C. E. Penner, B. M. Hosek, and J. J. Maskey. 2018. Epxanding GIS analyses to monitor and assess North American moose distri- bution and density. Alces 54: 71–80. _____, _____, J. J. MAsKey, Jr., J. V. McKenzie, and R. E. JoHnson. 2013. Mass, morphology, and growth rates of moose in North Dakota. Alces 49: 1–15. JoHnson, D. J. 1996. Population analysis. Pages 419–444 in T. A. Bookout, editor. Research and Management Techniques for Wildlife and Habitats. The Wildlife Society, Bethesda, Maryland, USA. JoHnson, H. E., L. S. Mills, T. R. StePHenson, and J. D. WeHAusen. 2010. Population- specific vital rate contributions influence management of an endangered ungulate. Ecological Applications 20: 1753–1765. Knue, J. 1991. Big Game in North Dakota: A Short History. North Dakota Game and Fish Department, Bismarck, North Dakota, USA. Lenarz, M. S., J. FieBerg, M. W. ScHrAge, and A. J. EdwArds. 2010. Living on the edge: viability of moose in northeastern Minnesota. Journal of Wildlife Management 74: 1013–1023. MArKgren, G. 1969. Reproduction of moose in Sweden. Viltrey 6: 127–299. MAsKey, J. J. 2008. Movements, resource selection, and risk analyses for parasitic disease in an expanding moose popula- tion in the northern Great Plains. Ph.D. Dissertation. University of North Dakota, Grand Forks, North Dakota, USA. McKenzie, J. C. 1989. Breeding season parameters of the moose (Alces alces) in North Dakota as determined from observed early developmental stage ALCES VOL. 54, 2018 NORTH DAKOTA REPRODUCTIVE PARAMETERS – JENSEN ET AL. 35 measurements. Supplemental Job. Moose and Elk Population Study No. 91. Pittman – Robertson Division Project W-67-R-29. North Dakota Game and Fish Department, Bismarck, North Dakota, USA. Morrison, J. A., C. E. TrAiner, and P. L. WrigHt. 1959. Breeding season in elk as determined from known-age embryos. Journal of Wildlife Management 23: 27–34. musAnte, A. r., P. J. PeKins, and d. l. scArPitti. 2010. Characteristics and dynamics of a regional moose Alces alces population in the northeastern United States. Wildlife Biology 16: 185–204. nortH dAKotA forest service. 2003. Legendary Forests: State Forests Guide. North Dakota Forest Service, Bottineau, North Dakota, USA. Olsson, O., and H. P. vAn der Jeugd. 2002. Survival in king penguins aptenodytes patagonicus: temporal and sex-specific effects of environmental variability. Oecologia 132: 509–516. PeeK, J. M. 1974. Initial response of moose to a forest fire in northeastern Minnesota. American Midland Naturalist 91: 435–438. _____. 1998. Habitat relationships. Pages 351–376 in A. W. Franzmann and C.C. Schwartz, editors. Ecology and Management of the North American Moose. The Wildlife Management Institute, Washington, D. C., USA. Peterson, R. L. 1955. North American Moose. University of Toronto Press, Toronto, Ontario, Canada. Peterson, R. O. 1999. Wolf-moose interac- tions on Isle Royale: the end of natural regulation? Ecological Applications 9: 10–16. Post, E., M. C. ForcHHAmmer, N. C. StensetH, and R. LAngvAtn. 1999. Extrinsic modification of vertebrate sex ratios by climatic variation. American Naturalist 154: 194–204. _____, N. C. StenetH, R. O. Peterson, J. A. VuceticH, and A. M. Elis. 2002. Phase dependence and population cycles in a large-mammal predator prey system. Ecology 83: 2997–3002. R Core Team. 2014. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. (accessed August 2017). RAitHel, J. D., M. J. KAuffmAn, and D. H. PletscHer. 2007. Impact of spatial and temporal variation in calf survival on the growth of elk popula- tions. Journal of Wildlife Management 71: 795–803. ReuterwAll, C. 1981. Temporal and spatial variability of calf sex ratio in Scandinavian moose Alces alces. Oikos 73: 39–45. RuPrecHt, J. S., K. R. Hersey, K. HAfen, K. L. MonteitH, N. J. DeCesAre, M. J. KAuffmAn, and D. R. MAcNulty. 2016. Reproduction in moose at their southern range limit. Journal of Mammalogy 97: 1355–1365. SAetHer, B. E., R. Andersen, L. HJelJord, and M. Heim. 1996. Ecological cor- relates of regional variation in life his- tory of the moose Alces alces. Ecology 77: 1493–1500. SeAlBloom, R. W., J. W. HogAnson, and W. F. Jensen. 2011. Mammals of North Dakota. North Dakota Institute for Regional Studies, North Dakota State University, Fargo, North Dakota, USA. Schwartz, C. C. 1998. Reproduction, natal- ity and growth. Pages 141–171 in A.W. Franzmann and C.C. Schwartz, editors. Ecology and Management of the North American Moose. The Wildlife Management Institute. Washington, D. C., USA. _____, and K. J. HundertmArK. 1993. Reproductive characteristics of Alaskan moose. Journal of Wildlife Management 57: 454–468. Severud, W. J., G. D. DelGiudice, T. R. OBermoller, T. A. EnrigHt, R. G. WrigHt, and J. D. Forester. 2015. Using GPS collars to determine parturition and http://www.R-project.org/> http://www.R-project.org/> NORTH DAKOTA REPRODUCTIVE PARAMETERS – JENSEN ET AL. ALCES VOL. 54, 2018 36 cause-specific mortality of moose calves. Wildlife Society Bulletin 39: 616–625. _____, _____, _____, K. J. FosHAy, and R. G. WrigHt. 2014. Using GPS collars to determine moose calving and cause- specific mortality of calves in northeast- ern Minnesota: progress report on second field season. Pages 40–56 in L. Cornicelli, M. Carstensen, M. D. Grund, M. A. Larson, and J. S. Lawrence, editors. Summaries of Wildlife Research Findings 2013. Minnesota Department of Natural Resources, St. Paul, Minnesota, USA. SHeldon, B. C., and S. A. West. 2004. Maternal dominance, maternal condition, and offspring sex ratio in ungulate mam- mals. American Naturalist 163: 40–54. SolBerg, E. J., A. Loison, T. H. RingsBy, B. E., SAetHer, and M. Heim. 2002. Biased adult sex ratio can affect fecundity in primiparous moose Alces alces. Wildlife Biology 8: 117–128. TestA, J. W. 2004. Population dynamics and life history trade-offs of moose (Alces alces) in south-central Alaska. Ecology 85: 1439–1452. TimmermAnn, H. R., and A. R. Rodgers. 2017. The status and management of moose in North America – circa 2015. Alces 53: 1–22. VeeroJA, R., A. KirK, V. TilgAr, S. Säde, M. KreitsBerg, and J. Tõnisson. 2010. Conception date affects litter type and foetal sex ratio in female moose in Estonia. Journal of Animal Ecology 79: 169–175. Verme, L. J. 1969. Reproductive patterns of white-tailed deer related to nutritional plane. Journal of Wildlife Management 33: 881–887. _____. 1983. Sex ratio in Odocoileus: a critical review. Journal of Wildlife Management 47: 573–582.