Abstract
Intraspecific body mass in ungulates has often been shown to increase with latitude. The biological basis for such latitudinal gradients is, however, poorly known. Here we examined whether satellite-derived indices of environmental phenology, based on the normalised difference vegetation index (NDVI), as well as variables derived from meteorological stations, altitude, and population density, can explain latitudinal gradients and regional variation in body mass of Norwegian moose. The best model gave a considerably better fit than latitude alone, and included all explanatory environmental variables. Accordingly, heavy moose were found in areas with short and intense summers that were followed by long, cold winters, at low altitude relative to the tree-limit, and with low population density relative to the available plant biomass. This relationship was stronger for yearlings than for calves, except for the effect of population density. This indicates that differences in the characteristics of the vegetation quality and environmental phenology, as well as winter harshness and population density, are important factors that shape both the latitudinal and other geographical gradients in moose body mass.
Similar content being viewed by others
References
Albon SD, Langvatn R (1992) Plant phenology and the benefits of migration in a temperate ungulate. Oikos 65:502–513
Andersen R (1991) Habitat deterioration and the migratory behaviour of moose (Alces alces L.) in Norway. J Appl Ecol 28:102–108
Arft AM, Walker MD, Gurevitch J, Alatalo JM, Bret-Harte MS, Dale M, Diemer M, Gugerli F, Henry GHR, Jones MH, Hollister RD, Jónsdóttir IS, Laine K, Lévesque E, Marion GM, Molau U, Mølgaard P, Nordenhäll U, Raszhivin V, Robinson CH, Starr G, Stenström A, Stenström M, Totland Ø, Turner PL, Walker LJ, Webber PJ, Welker JM, Wookey PA (1999) Responses of tundra plants to experimental warming: meta-analysis of the International Tundra Experiment. Ecol Monogr 69:491–511
Ashton KG, Tracy MC, de Queiroz A (2000) Is Bergmann’s rule valid for mammals? Am Nat 156:390–415
Bliss LC (1962) Adaptation of arctic and alpine plants to environmental conditions. Arctic 15:117–144
Bø S, Hjeljord O (1991) Do continental moose ranges improve during cloudy summers? Can J Zool 69:1875–1879
Boelman NT, Stieglitz M, Rueth HM, Sommerkorn M, Griffin KL, Shaver GR, Gamon JA (2003) Response of NDVI, biomass, and ecosystem gas exchange to long-term warming and fertilization in wet sedge tundra. Oecologia 135:414–421
Burnham KP, Anderson DR (2002) Model selection and multimodel inference. A practical information-theoretic approach, 2nd edn. Springer, Berlin Heidelberg New York
Cederlund GN, Sand HKG, Pehrson Å (1991) Body mass dynamics of moose calves in relation to winter severity. J Wildl Manage 55:675–681
Cook RD (1977) Detection of influential observation in linear regression. Technometrics 19:15–18
Côte SD, Rooney TP, Tremblay J-P, Dussault C, Waller DM (2004) Ecological impacts of deer overabundance. Annu Rev Ecol Syst 35:113–147
Deinum B (1984) Chemical composition and nutritive value of herbage in relation to climate. In: Riley H, Skjelvåg AO (eds) The impact of climate on grass production and quality, vol. 10. Norwegian State Agricultural Research Stations, Ås, pp 338–350
Dong J, Kaufmann RK, Myneni RB, Tucker CJ, Kauppi PE, Liski J, Buermann W, Alexeyev V, Hughes MK (2003) Remote sensing estimates of boreal and temperate forest woody biomass: carbon pools, sources and sinks. Remote Sens Environ 84:393–418
Ericsson G, Wallin K (1999) Hunter observations as an index of moose Alces alces population parameters. Wildl Biol 5:177–185
Ericsson G, Ball JP, Danell K (2002) Body mass of moose calves along an altitudinal gradient. J Wildl Manage 66:91–97
ESRI (2005) ArcDoc version 9.1. Environmental Systems Research Institute, Inc. Redlands, CA
Gaillard J-M, Delorme D, Boutin J-M, Van Laere G, Boisaubert B (1996) Body mass of roe deer fawns during winter in two contrasting populations. J Wildl Manage 60:29–36
Garel M, Solberg EJ, Sæther B-E, Herfindal I, Høgda K-A (2006) The length of growing season and adult sex ratio affect sexual size dimorphism in moose. Ecology 87:745–758
Geist V (1987) Bergmann’s rule is invalid. Can J Zool 65:1035–1038
Hansen AH, Jonasson S, Michelsen A, Julkunen-Tiitto R (2006) Long-therm experimental warming, shading and nutrient addition affect the concentration of phenolic compounds in arctic-alpine deciduous and evergreen dwarf shrubs. Oecologia 147:1–11
Herfindal I, Sæther B-E, Solberg EJ, Andersen R, Høgda KA (2006) Population characteristics predict responses in moose body mass to temporal variation in the environment. J Anim Ecol 75:1110–1118
Hjeljord O, Histøl T (1999) Range-body mass interactions of a northern ungulate—a test of hypothesis. Oecologia 119:326–339
Høgda KA, Karlsen SR, Solheim I (2001) Climatic change impact on growing season in Fennoscandia studied by a time series of NOAA AVHRR NDVI data. In: Proceedings of IGARSS, 9–13 July 2001, Sydney, Australia, vol. 3, pp 1338–1340
Kerr JT, Ostrovsky M (2003) From space to species: ecological applications for remote sensing. Trends Ecol Evol 18:299–305
Klein DR (1970) Tundra ranges north of the boreal forest. J Range Manage 23:8–14
Langvatn R, Albon SD (1986) Geographic clines in body weight of Norwegian red deer: a novel explanation of Bergmann’s rule. Holarct Ecol 9:285–293
Lavsund S, Nygrén T, Solberg EJ (2003) Status of moose populations and challenges to moose management in Fennoscandia. Alces 39:109–130
Lenart EA, Bowyer RT, Ver Hoef J, Ruess RW (2002) Climate change and caribou: effects of summer weather on forage. Can J Zool 80:664–678
Lindstedt SL, Boyce MS (1985) Seasonality, fasting endurance, and body size in mammals. Am Nat 125:873–878
Loison A, Langvatn R (1998) Short- and long-term effects of winter and spring weather on growth and survival of red deer in Norway. Oecologia 116:489–500
Loison A, Langvatn R, Solberg EJ (1999) Body mass and winter mortality in red deer calves: disentangling sex and climate effects. Ecography 22:20–30
Martínez M, Rodrígues-Vigal C, Jones OR, Coulson T, San Miguel A (2005) Different hunting strategies select for different weights in red deer. Biol Lett 1:353–356
McNab BK (1971) On the ecological significance of Bergmann’s rule. Ecology 52:845–854
Moen A (1999) National atlas of Norway: vegetation. Norwegian Mapping Authority, Hønefoss
Myneni RB, Hall FG, Sellers PJ, Marshak AL (1995) The interpretation of spectral vegetation indexes. IEEE Trans Geosci Remote Sens 33:481–486
Mysterud A, Langvatn R, Yoccoz NG, Stenseth NC (2001) Plant phenology, migration and geographical variation in body weight of a large herbivore: the effect of a variable topography. J Anim Ecol 70:915–923
Mysterud A, Langvatn R, Yoccoz NG, Stenseth NC (2002) Large-scale habitat variability, delayed density effects and red deer populations in Norway. J Anim Ecol 71:569–580
Nilsen EB, Solberg EJ (2006) Patterns of hunting mortality in Norwegian moose (Alces alces) populations. Eur J Wildl Res 52:153–163
Persson I-L, Danell K, Bergström R (2005) Different moose densities and accompanied changes in tree morphology and browse production. Ecol Appl 15:1296–1305
Pettorelli N, Gaillard J-M, Duncan P, Ouellet J-P, Van Laere G (2001) Population density and small-scale variation in habitat quality affect phenotypic quality in roe deer. Oecologia 128:400–405
Pettorelli N, Vik JO, Mysterud A, Gaillard J-M, Tucker CJ, Stenseth NC (2005) Using the satellite-derived NDVI to assess ecological responses to environmental change. Trends Ecol Evol 20:503–510
Potvin F, Beaupré P, Laprise G (2003) The eradication of balsam fir stands by white-tailed deer on Anticosti Island, Québec: A 150-year process. Ecoscience 10:487–495
R Development Core Team (2005). R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna
Reed BC, Brown JF, Darrel V, Loveland TR, Merchant JW, Ohlen DO (1994) Measuring phenological variability from satellite imagery. J Veg Sci 5:703–714
Sæther B-E (1985) Annual variation in carcass weight of Norwegian moose in relation to climate along a latitudinal gradient. J Wildl Manage 49:977–983
Sæther B-E (1997) Environmental stochasticity and population dynamics of large herbivores: a search for mechanisms. Trends Ecol Evol 12:143–149
Sæther B-E, Haagenrud H (1983) Life history of the moose (Alces alces): fecundity rates in relation to age and carcass weight. J Mammal 64:226–232
Sæther B-E, Haagenrud H (1985) Geographical variation in body weight and sexual size-dimorphism of Norwegian moose (Alces alces). J Zool 206:83–96
Sæther B-E, Andersen R, Hjeljord O, Heim M (1996) Ecological correlates of regional variation in life history of the moose Alces alces. Ecology 77:1493–1500
Sand H, Cederlund G, Danell K (1995) Geographical and latitudinal variation in growth patterns and adult body size of Swedish moose (Alces alces). Oecologia 102:433–442
Schloss AL, Kicklighter DW, Kaduk J, Wittenberg U (1999) Comparing global models of terrestrial net primary productivity (NPP): comparison of NPP to climate and the Normalized Difference Vegetation Index (NDVI). Global Change Biol 5:25–34
Skogland T (1990) Density dependence in a fluctuating wild reindeer herd; maternal vs. offspring effects. Oecologia 84:442–450
Solberg EJ, Sæther B-E (1994) Male traits as life-history variables: annual variation in body mass and antler size in moose (Alces alces). J Mammal 75:1069–1079
Solberg EJ, Sæther B-E (1999) Hunter observations of moose Alces alces as a management tool. Wild Biol 5:107–117
Solberg EJ, Heim M, Sæther B-E, Holmstrøm F (1997) Oppsummeringsrapport. Overvåkningsprogram for hjortevilt. Elg 1991–95. NINA Report 30:1–68
Solberg EJ, Sæther B-E, Strand O, Loison A (1999) Dynamics of a harvested moose population in a variable environment. J Anim Ecol 68:186–204
Solberg EJ, Loison A, Gaillard J-M, Heim M (2004) Lasting effects of conditions at birth on moose body mass. Ecography 27:677–687
Solberg EJ, Rolandsen CM, Heim M, Grøtan V, Garel M, Sæther B-E, Nilsen EB, Austrheim G, Herfindal I (2006) Elgen i Norge sett med jegerøyne—En analyse av jaktmaterialet fra overvåkingsprogrammet for elg og det samlede sett elg-materialet for perioden 1966–2004. NINA Report 125:1–197
Stewart KM, Bowyer RT, Dick BL, Johnson BK, Kie JG (2005) Density-dependent effects on physical condition and reproduction in North American elk: an experimental test. Oecologia 143:85–93
Stubsjøen T, Sæther B-E, Solberg EJ, Heim M, Rolandsen CM (2000) Moose (Alces alces) survival in three populations in northern Norway. Can J Zool 78:1822–1830
Tucker CJ, Fung IY, Keeling CD, Gammon RH (1986) Relationship between atmospheric CO2 variations and a satellite-derived vegetation index. Nature 319:195–199
Tucker CJ, Slayback DA, Pinzon JE, Los SO, Myneni RB, Taylor MG (2001) Higher northern latitude normalized difference vegetation index and growing season trends from 1982 to 1999. Int J Biometeorol 45:184–190
VanSoest PJ (1994) Nutritional ecology of the ruminant, 2nd edn. Cornell University Press, Ithaca, NY
Veroustraete F, Patyn J, Myneni RB (1996) Estimating net ecosystem exchange of carbon using the normalized difference vegetation index and an ecosystem model. Remote Sens Environ 58:115–130
White RG (1983) Foraging patterns and their multiplier effects on productivity of northern ungulates. Oikos 40:377–384
Zhou LM, Tucker CJ, Kaufmann RK, Slayback D, Shabanov NV, Myneni RB (2001) Variations in northern vegetation activity inferred from satellite data of vegetation index during 1981 to 1999. J Geophys Res D 106:20069–20083
Acknowledgments
We thank Compton J. Tucker at Goddard Space Flight Center, USA, for providing us with the GIMMS data set, and the thousands of Norwegian moose hunters and local moose managers for providing the moose data. We also thank Anne Loison, Marco Festa-Bianchet and one anonymous referee for valuable and helpful comments that greatly improved the manuscript, while John D.C. Linnell kindly improved the English of the manuscript. This project was funded by the Directorate for nature management and the Research Council of Norway (programmes NORKLIMA and Changing Landscapes).
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Jean-Michel Gaillard.
Rights and permissions
About this article
Cite this article
Herfindal, I., Solberg, E.J., Sæther, BE. et al. Environmental phenology and geographical gradients in moose body mass. Oecologia 150, 213–224 (2006). https://doi.org/10.1007/s00442-006-0519-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-006-0519-8