Adaptations of Mustelinae to Adaptations of Mustelinae to WinterWinter

Or, They didn’t listen to Or, They didn’t listen to BergmannBergmann

Long Thin Body TypesLong Thin Body Types

Small and medium sizedSmall and medium sized

What about Bergmann’s rule?What about Bergmann’s rule?

Sheryn Olson, Winter Ecology, Spring 2005

Who are the Mustelinae?Who are the Mustelinae?

Texasferret.org

Subfamily MustelinaeSubfamily Mustelinae

SmallerSmaller weasels & stoatsweasels & stoats ferrets & ferrets &

polecatspolecats minkmink LargerLarger

martensmartens fishersfishers

Least weasel (Least weasel (Mustela Mustela nivalisnivalis))

Short Tailed Weasel or European Stoat (Mustela

erminea)

Long Tailed Weasel (Mustela frenata)

Smaller MustelinaeSmaller Mustelinae

Black Footed Black Footed FerretFerret

( (Mustela Mustela nigripesnigripes))

European Polecat (Mustela putorius

eversmanii)

American Mink Mustela vison

Smaller MustelinaeSmaller Mustelinae

Larger MustelinaeLarger Mustelinae

• MartensMartens

• FishersFishers

Larger MustelinaeLarger Mustelinae

Pine Marten Martes americana

• MartensMartens

• FishersFishers

Stone or Beech Marten Martes foines

Larger MustelinaeLarger Mustelinae

Fisher Fisher Martes pennantiMartes pennanti

• MartensMartens

• FishersFishers

What is Bergmann’s RuleWhat is Bergmann’s Rule

• A smaller surface to volume ratio A smaller surface to volume ratio means a lower rate of heat loss. means a lower rate of heat loss.

• The further north an endothermic The further north an endothermic species is distributed, the larger their species is distributed, the larger their body size. body size.

(Bergmann, 1847)(Bergmann, 1847)

Bergmann’s RuleBergmann’s Rule

• Is Bergmann’s rule valid? Is Bergmann’s rule valid?

• Methods of quantificationMethods of quantification

• Hypotheses to explain mechanismsHypotheses to explain mechanisms

• Six hypotheses Six hypotheses (Blackburn & Hawkins, 2004)(Blackburn & Hawkins, 2004)

Bergmann’s Rule Bergmann’s Rule and Mustelinaeand Mustelinae

• Is that species endothermic or Is that species endothermic or homeothermic? homeothermic?

(Rensch, 1938 and Mayr, 1956)(Rensch, 1938 and Mayr, 1956)

• Is a species distributed widely?Is a species distributed widely?

• Are comparisons inter- or intra- Are comparisons inter- or intra- specific? specific? (James, 1970 and Blackburn, et al, 1999)(James, 1970 and Blackburn, et al, 1999)

Bergmann’s Rule Bergmann’s Rule and Mustelinaeand Mustelinae

• Is a species distributed widely?Is a species distributed widely?

Mink

Lariviére, 1999

Bergmann’s Rule Bergmann’s Rule and Mustelinaeand Mustelinae

• Is a species distributed widely?Is a species distributed widely?

Long Tailed Weasel

Sheffield & Thomas, 1997

Bergmann’s Rule Bergmann’s Rule and Mustelinaeand Mustelinae

• Is a species distributed widely?Is a species distributed widely?

Short Tailed Weasel

King, 1983

Bergmann’s Rule Bergmann’s Rule and Mustelinaeand Mustelinae

• Is a species distributed widely?Is a species distributed widely?

Least WeaselM. nivalis

Sheffield & King, 1994

The FightThe Fight

  ForFor

Mayr, 1956, 1963Mayr, 1956, 1963

Rosenzweig, 1968Rosenzweig, 1968

Paterson, 1990Paterson, 1990

Ashton, 2000, Ashton, 2000, 20012001

Against Rensch, 1938Rensch, 1938McNab, 1971McNab, 1971Geist, 1987 Geist, 1987 Erlinge, 1987Erlinge, 1987Gould, 1997Gould, 1997Gaston, et. al., 1998Gaston, et. al., 1998

Meiri & Dayan, Meiri & Dayan, 20032003

Current StatusCurrent Status

• 2000, 2001: Ashton 2000, 2001: Ashton YES YES

• 2004: Blackburn & Hawkins2004: Blackburn & HawkinsMAYBEMAYBE

• 2004: Meiri, et al 2004: Meiri, et al MAYBEMAYBE

Questions for WeaselsQuestions for Weasels

• Why don’t weasels follow Why don’t weasels follow Bergmann’s Rule?Bergmann’s Rule?

• What are the advantages What are the advantages of a of a small, thin small, thin body in body in Northern Northern Latitudes? Latitudes?

Physiological AdaptationsPhysiological Adaptations

higher metabolic rate higher metabolic rate ((Mustela nivalis)Mustela nivalis) (Scholander, 1950)(Scholander, 1950)

delayed implantation of embryos delayed implantation of embryos M. frenataM. frenata and and M. ermineaM. erminea

pelagic color changespelagic color changes

fur length fur length (Sheffield & King, 1994)(Sheffield & King, 1994)

M. Erminea changing pelage

Behavioral AdaptationsBehavioral Adaptations switching daily activity patternsswitching daily activity patterns

(Zielinski, 2000)(Zielinski, 2000)

switching food sourcesswitching food sources(Danilov and Tumanov, 1976; Weber, 1990(Danilov and Tumanov, 1976; Weber, 1990Pandolfi, et al, 1996)Pandolfi, et al, 1996)

caching foodcaching food(Weeks, 1991; Henry, et al., 1990(Weeks, 1991; Henry, et al., 1990; ; KingKing, 1989;, 1989;

Oksanan, et al 1985)Oksanan, et al 1985)

fur lined nestsfur lined nests

Is Bergmann’s rule invalid?Is Bergmann’s rule invalid?

• Long and thin works year roundLong and thin works year round

• The better to prey on subnivean and The better to prey on subnivean and burrowing mammalsburrowing mammals

• The better to avoid predators by going The better to avoid predators by going undergroundunderground

• Other adaptations compensate: Behavioral Other adaptations compensate: Behavioral and Physiologicaland Physiological

MorphologyMorphology

DiscussionDiscussion

Small Mustelinae use other strategies Small Mustelinae use other strategies to maintain their energy balance in to maintain their energy balance in winter.winter.

Weasel species appear not to follow Weasel species appear not to follow Bergmann’s rule.Bergmann’s rule.

Or do they? Short Tailed Weasels…Or do they? Short Tailed Weasels…– (King, 1983)(King, 1983)

In ConclusionIn Conclusion

Mustelinae illustrate it is Mustelinae illustrate it is important to consider a important to consider a whole suite of adaptations.whole suite of adaptations.

When observing patterns, When observing patterns, don’t confuse them with don’t confuse them with mechanisms.mechanisms.

Selected References: The Bergmann’s Rule Controversy

Ashton, Kyle G. 2001. Are ecological and evolutionary rules being dismissed prematurely? Diversity and Distributions. 7: 289-295.

 Ashton, K.G., Tracy, M.C. & de Queiroz, A. 2000. Is Bergmann’s rule valid

for mammals? American Naturalist. 156:390 – 415. Bergmann, Carl. 1847. Ueber die Verhältnisse der Wärmeokonomie der

Thiere zu ihrer Grösse. Gottinger studien. 3:595-708 Blackburn, T.M. & Gaston, K.J. and Loder, N. 1999. Geographic gradients in

body size: a clarification of Bergmann’s rule. Diversity and Distributions. 5: 165-174.

Blackburn, T.M. & Hawkins, B.A. 2004. Bergmann’s rule and the mammal fauna of North America. Ecography. 27: 715-724.

Dayan, Tamar, Simberloff, Daniel, Tchernov, E. and Yoran YT. 1989. Inter- and intraspecific Character Displacement in Mustelids. Ecology. 70(5): 1526-1539

Erlinge, S. 1987. Why do European stoats not follow Bergmann’s Rule? Erlinge, S. 1987. Why do European stoats not follow Bergmann’s Rule? Holarctic Ecology. 10: 33-39Holarctic Ecology. 10: 33-39

 Gaston, K.J. Blackburn, T.M. & Spicer, J. 1998. Rapoport’s rule:Time for

an epitaph? Trends in Ecology and Evolution. 13: 70-74.

Selected References: The Bergmann’s Rule Controversy

Geist, V. 1987. Bergmann’s rule is invalid. Canadian Journal of Zoology. 65: 1035-1038.

Geist, V. 1990. Bergmann’s rule is invalid: a reply to J.D. Paterson. Canadian Journal of Zoology. 68: 1613-1615.

Gould, S.H. 1997. Cope’s rule as psychological artifact. Nature. 385: 199-200.

 Meiri S, Dayan T., Simberloff, D. 2004. Carnivores, biases and

Bergmann’s rule . Biological Journal of the Linnean Society. 81 (4): 579-588.

Mayr, Ernst. 1956. Geographical character gradients and climatic adaptation. Evolution. 10: 105-108.

 Mayr, Ernst. 1963. Animal Species and Evolution. Harvard University Press,

Cambridge, Mass. Paterson, J.D. 1990. Comment – Bergmann’s rule is invalid: a reply to V.

Geist. Canadian Journal of Zoology 68: 1610 – 1612. Rensch, B. 1938. Some problems of geographical variation and species-

formation. Proceedings of the Linnean Society of London. 150: 275- 285 Rosenzweig, M.L. 1995. Species diversity in space and time. Cambridge

University Press, Cambridge.  

References CitedReferences Cited Ashton, Kyle G. 2001. Are ecological and evolutionary rules being

dismissed prematurely? Diversity and Distributions. 7: 289-295.

Ashton, K.G., Tracy, M.C. & de Queiroz, A. 2000. Is Bergmann’s rule valid for mammals? American Naturalist. 156:390 – 415.

Bergmann, Carl. 1847. Ueber die Verhältnisse der Wärmeokonomie der Thiere zu ihrer Grösse. Gottinger studien. 3:595-708

 Blackburn, T.M. & Gaston, K.J. and Loder, N. 1999. Geographic gradients

in body size: a clarification of Bergmann’s rule. Diversity and Distributions. 5: 165-174.

 Blackburn, T.M. & Hawkins, B.A. 2004. Bergmann’s rule and the

mammal fauna of North America. Ecography. 27: 715-724. Danilov, P.I. and I.L Tuminov. 1976. Mustelids of northwestern USSR.

Institut Biologii, Karelskii Filial, Akademii Nauk SSSR, Leningrad, 256 pp. (in Russian)

References CitedReferences Cited  

Dayan, Tamar, Simberloff, Daniel, Tchernov, E. and Yoran YT. 1989. Inter- and intraspecific Character Displacement in Mustelids. Ecology. 70(5): 1526-1539

Erlinge, S. 1987. Why do European stoats not follow Bergmann’s Rule? Holarctic Erlinge, S. 1987. Why do European stoats not follow Bergmann’s Rule? Holarctic Ecology. 10: 33-39Ecology. 10: 33-39

 Geist, V. 1987. Bergmann’s rule is invalid. Canadian Journal of Zoology. 65:

1035-1038. Geist, V. 1990. Bergmann’s rule is invalid: a reply to J.D. Paterson. Canadian

Journal of Zoology. 68: 1613-1615. Hall, ER. 1951. American Weasels. Univ of Kansas Publication Museum of Natural

History. 4:1-466. Henry SE, Raphael MG, Ruggiero LF. 1990. Food caching and handling by

marten. Great Basin Nat 50:381-383

 James, F. C. 1970. Geographic size variation in birds and its relationship to climate. Ecology 51: 365-390.

King, Carolyn M. 1983. Mustela erminea. Mammalian Species. 197, pp. 1-8.  Lariviére, Serge.  1999.  Mustela vison. Mammalian Species. American Society of

Mammalogists. No. 608. pp. 1-9. 3 fig. Distribution map of mink. 

References CitedReferences Cited  

Loso, H. 1999. "Mustela erminea" (On-line), Animal Diversity Web. Accessed February 24, 2005 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Mustela_erminea.html.

 Mayr, Ernst. 1956. Geographical character gradients and climatic

adaptation. Evolution. 10: 105-108. Mayr, Ernst. 1963. Animal Species and Evolution. Harvard University Press,

Cambridge, Mass. McNab, Brian K. 1971. On the Ecological Significance of Bergmann's Rule.

Ecology: Vol. 52, No. 5, pp. 845–854. Meiri S, Dayan T., Simberloff, D. 2004. Carnivores, biases and Bergmann’s

rule . Biological Journal of the Linnean Society. 81 (4): 579-588. Oksanan, T, Oksanen, L, Fretwell SD. 1985. Surplus killing in the hunting

strategy of small predators. Am Nat 126:328-346. Meiri S, Dayan T., Simberloff, D. 2004. Carnivores, biases and Bergmann’s

rule. Biological Journal of the Linnean Society. 81 (4): 579-588. 

References CitedReferences Cited  

Pandolfi M, Demarinas AM & Petrov I. 1996. Fruit as a winter feeding resource in the diet of stone marten (Martes foina) in east-central Italy. Z. Säugetierk. 61 : 215-220.

 Paterson, J.D. 1990. Comment – Bergmann’s rule is invalid: a reply to V.

Geist. Canadian Journal of Zoology 68: 1610 – 1612. Rensch, B. 1938. Some problems of geographical variation and species-

formation. Proceedings of the Linnean Society of London. 150: 275- 285 Rosenzweig, M.L. 1995. Species diversity in space and time. Cambridge

University Press, Cambridge. Sheffield, Steven R. and King, Carolyn M. 1994. Mustela nivalis. Mammalian

Species. 454, pp. 1-10.  Sheffield, SR. and Thomas, HH. 1997. Mustela frenata. Mammalian Species.

570:1-9.  Scholander, PF., V Walters, WR Hock, L Irving. 1950. Body insulation of some

arctic and tropical mammals and birds. Biol. Bull 99:225-236. 

References CitedReferences Cited  

Stevens, G. C. 1989. The latitudinal gradient in geographical range: how so many species co-exist in the tropics. Am. Nat. 133:240-256.

Weeks, HP. 1991. Arboreal caching of prey by long-tailed weasel. The Prairie Naturalist. 25:39-42.

 Weber J. M. 1990. Seasonal exploitation of amphibians by otters (Lutra lutra )

in north-east Scotland. J. Zool. Lond. 220, 641-651. Zielinski, William J. 2000. Weasels and Martens – Carnivores in Northern

Latitudes. Chapter 5, pp. 95-118 in Activity Patterns in Small Mammals. Ecological Studies. Vol. 141. S. Halle, N.C. Stenseth (Editors)

 http://www.inhs.uiuc.edu/dnr/fur/species/weasel.html Global Invasive Species List:

http://www.issg.org/database/species/distribution.asp?si=98&fr=1&sts=sss# (for M. erminea)

 http://www.washington.edu/burkemuseum/collections/mammalogy/mamwash/muer.html - distribution and maps of M. erminea

Texasferret.org: http://www.texasferret.org/news/199901.shtml Family Tree

University of Michigan Museum of Zoology Animal Diversity Web: http://animaldiversity.ummz.umich.edu/site/accounts/information/Mustelidae.html

 Zoo page from Yugoslavia http://www.nrtonline.co.yu/zoopage/klas/mesojedi.htm– many photos.

 

Black Footed FerretsBlack Footed Ferrets

Black-footed Ferret Timeline ------- http://www.blackfootedferret.org 1851: The black-footed ferret is reported and described by John James Audubon. No one will report seeing a ferret again for another 26 years.

1964: A female ferret and kits are found in Mellette County in western South Dakota. They are considered perhaps the last black-footed ferrets in the world.

1967: The black-footed ferret is put on the Endangered Species list.

1971: Executive Order 11643 is implemented, banning the use of poisons with secondary hazards on public lands.

1972: A drowned ferret is discovered in a watering tank in Wyoming. No others are found.

Nine South Dakota ferrets are captured and taken to Patuxent Wildlife Research Center in Laurel, Maryland. It is hoped that these ferrets will produce kits, but every litter is dead at birth.

Black Footed FerretsBlack Footed Ferrets

Black-footed Ferret Timeline ------- http://www.blackfootedferret.org 1973: The Endangered Species Act is passed.

1979: The last Patuxent ferret dies. The black-footed ferret is declared extinct.

1981: September 25th -- A Wyoming ranch dog belonging to John and Lucille Hogg kills a black-footed ferret.

October 29th -- A live black-footed ferret is spotted near Meeteetse, Wyoming. Conservationists and researchers begin an intensive search and study of wild ferrets.

1984: The Meeteetse population is 129 black-footed ferrets. Plans are made to begin a captive breeding program.

1985: Outbreaks of sylvatic plague and canine distemper nearly wipe out the Meeteetse ferrets.

Black Footed FerretsBlack Footed FerretsBlack-footed Ferret Timeline ------- http://www.blackfootedferret.org

August 27th -- The US Fish & Wildlife Service and Wyoming Game and Fish Department decide to remove all known black-footed ferrets from their habitat in an effort to save the species. From October 1985-September 1986, 17 ferrets are taken into captivity.

1986: The IUCN--World Conservation Union's Conservation Breeding Specialist Group (CBSG) conducts a workshop to develop a recovery plan for captive breeding and reintroduction of black-footed ferrets.

1987: The last known ferret is captured at Meeteetse in February. These 18 captive black-footed ferrets are probably the rarest mammals on earth.

A captive breeding program is initiated by the US Fish & Wildlife Service, The Wyoming Game & Fish Department, and the American Zoo & Aquarium Association.

Two litters of ferret kits are born at Sybille Wildlife Research and Conservation Education Center, Wyoming to "Becky" and "Jenny". This brings the total number of black-footed ferrets in captivity to 25.

Black Footed FerretsBlack Footed FerretsBlack-footed Ferret Timeline -------

http://www.blackfootedferret.org 1988: In October, eight ferrets are flown to the National Zoological Park's Conservation and Research Center in Front Royal, VA to start a new breeding colony and to guard against catastrophic loss of the captive population. December, eight more ferrets are taken to the Henry Doorly Zoo in Omaha, NE.

"Conservation Biology of the Black-footed Ferret" (Seal et al.) is published.

The "Black-footed Ferret Recovery Plan" is drafted by the US Fish & Wildlife Service.

1989: 72 ferret kits are born at Sybille and 6 at Front Royal. The total ferret population is 120.

1990: The Cheyenne Mountain Zoo in Colorado Springs, Colorado joins the captive breeding program.

1991: Shirley Basin, in central Wyoming becomes the first black-footed ferret reintroduction site with the release of 49 juvenile ferrets.

Black Footed FerretsBlack Footed FerretsBlack-footed Ferret Timeline ------- http://www.blackfootedferret.org

1991: A Species Survival Plan (SSP) is developed in cooperation with the American Zoo and Aquarium Association to manage the genetic and demographic needs of the captive ferret population.

The Louisville Zoological Garden in Louisville, Kentucky and the Phoenix Zoo in Phoenix, AZ join the captive breeding program.

1992: Two litters of wild-born kits are reported in Shirley Basin--the first known kits born in the wild since the Meeteetse population was lost.

1993: Four wild-born litters are discovered in Shirley Basin.

The Toronto Zoo, Toronto, Canada joins the captive breeding program.

1994: The Charles M. Russell National Wildlife Refuge in Montana, and Badlands National Park, South Dakota receive ferrets for reintroduction.

An outbreak of plague spreads throughout the Shirley Basin release site and further reintroductions are postponed. A total of 228 ferrets released in Shirley Basin from 1991-1994. Small numbers of ferrets persist there today.

1995: The US Fish & Wildlife Services assumes responsibility for managing the Sybille, WY breeding facility and renames it the National Black-footed Ferret Conservation Center.

Ferrets are found to be highly susceptible to direct contact with plague.

1996: The US Fish & Wildlife Service establishes a Black-footed Ferret Recovery Implemen-tation Team to help guide recovery efforts. The BFFRIT includes representatives from federal and state governments, Native American tribes, zoos, and conservation organiza-tions.

The South Dakota ferret reintroduction effort expands onto the Buffalo Gap National Grasslands.

Arizona joins the reintroduction program by testing the use of on-site "preconditioning" pens for the first time at a release site in the Aubrey Valley in northwestern Arizona.

1997: Twenty-four on-site preconditioning pens are constructed by the US Forest Service on the Buffalo Gap National Grasslands. 1997 is the first year that all ferrets destined for reintroduction are preconditioned before release.

A new reintroduction effort begins on the Fort Belknap Indian Reservation, Montana.

1998: The captive breeding program experiences its best year ever with a record 452 ferrets born and 339 surviving to weaning. Eighteen of the weaned young are produced in on-site pens in Arizona--an important milestone.

The number of ferrets available for reintroduction exceeds all previous years with ap-proximately 210 kits released to the wild in Arizona, Montana, and South Dakota.

The pen breeding program expands with the addition of pen facilities built by the Turner Endangered Species Fund in New Mexico. Twenty pens are completed at a pending reintroduction site in northwest Colorado, and twenty pens are constructed at Bowdoin National Wildlife Refuge in Montana to support on-going release efforts in Montana.

The US Fish & Wildlife Service plans for construction of a new breeding facility near Fort Collins, Colorado to replace the current Wyoming facility.

Perhaps the most important milestone in 1998 is the fact that for the first time since the black-footed ferret recovery program began, there are more ferrets in the wild than in captivity. To date, more than 2600 ferrets have been produced in captivity.:

Black Footed FerretsBlack Footed FerretsBlack-footed Ferret Timeline -------

http://www.blackfootedferret.org 1995: The US Fish & Wildlife Services assumes responsibility for managing the Sybille, WY breeding facility and renames it the National Black-footed Ferret Conservation Center.

Ferrets are found to be highly susceptible to direct contact with plague.

1996: The US Fish & Wildlife Service establishes a Black-footed Ferret Recovery Implementation Team to help guide recovery efforts. The BFFRIT includes representatives from federal and state governments, Native American tribes, zoos, and conservation organizations.

The South Dakota ferret reintroduction effort expands onto the Buffalo Gap National Grasslands.

Arizona joins the reintroduction program by testing the use of on-site "preconditioning" pens for the first time at a release site in the Aubrey Valley in northwestern Arizona.

Black Footed FerretsBlack Footed FerretsBlack-footed Ferret Timeline -------

http://www.blackfootedferret.org 1997: Twenty-four on-site preconditioning pens are constructed by the US Forest Service on the Buffalo Gap National Grasslands. 1997 is the first year that all ferrets destined for reintroduction are preconditioned before release.

A new reintroduction effort begins on the Fort Belknap Indian Reservation, Montana.

1998: The captive breeding program experiences its best year ever with a record 452 ferrets born and 339 surviving to weaning. Eighteen of the weaned young are produced in on-site pens in Arizona--an important milestone.

The number of ferrets available for reintroduction exceeds all previous years with ap-proximately 210 kits released to the wild in Arizona, Montana, and South Dakota.

Black Footed FerretsBlack Footed FerretsBlack-footed Ferret Timeline -------

http://www.blackfootedferret.org 1998:

The pen breeding program expands with the addition of pen facilities built by the Turner Endangered Species Fund in New Mexico. Twenty pens are completed at a pending reintroduction site in northwest Colorado, and twenty pens are constructed at Bowdoin National Wildlife Refuge in Montana to support on-going release efforts in Montana.

The US Fish & Wildlife Service plans for construction of a new breeding facility near Fort Collins, Colorado to replace the current Wyoming facility.

Perhaps the most important milestone in 1998 is the fact that for the first time since the black-footed ferret recovery program began, there are more ferrets in the wild than in captivity. To date, more than 2600 ferrets have been produced in captivity.