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Aposematism and crypsis in a rodent: antipredator defence of the Norwegian lemming

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Abstract

Aposematism is unusual in herbivorous mammals, and exceptions help clarify its ecology and evolution. The Norwegian lemming differs from other rodents in colouration and behaviour. One hypothesis is that its black, yellow and white colours, loud calls and ferocious defence reduce predation by conspicuous aposematism. Another hypothesis is that the colouration is cryptic. These alternatives are tested in a detectability experiment comparing lemmings and sympatric grey-sided voles. All 18 observers detected a higher proportion of the lemmings, corroborating conspicuousness. Unlike smaller rodents, Norwegian lemmings often call from a distance at predators. The aposematism hypothesis predicts that cryptically coloured Alaskan brown lemmings will not call. In the field, Norwegian lemmings gave antipredator calls at a human observer in 36 of 110 encounters, but brown lemmings did so in only 1 of 39 cases. Most Norwegian lemmings called if surprised within a few metres but froze or fled silently farther away, relying on crypsis against distant predators. Small juveniles called as often as adults, a possible case of auto-mimicry. In an earlier experiment, Norwegian lemmings, in contrast with grey-sided voles, aggressively resisted attacks by a major avian predator of rodents. The tests corroborate the hypotheses that (1) distinctive, contrast-rich colouration, antipredator calls and threat postures of the Norwegian lemming form a multimodal suit of aposematic traits, warning predators that this is a more dangerous prey than the smaller sympatric voles, and (2) discriminability from undefended species is an important adaptive reason for conspicuous distinctness of many aposematic signals.

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References

  • Agresti I (2002) Categorical data analysis, 2nd edn. Wiley, Hoboken

    Book  Google Scholar 

  • Andersson M (1976a) Lemmus lemmus: a possible case of aposematic coloration and behavior. J Mammal 57:461–469

    Article  Google Scholar 

  • Andersson M (1976b) Population ecology of the long-tailed skua (Stercorarius longicaudus). J Anim Ecol 45:537–559

    Article  Google Scholar 

  • Andersson M (1977) Fjällämmeln – en nordisk särling. (English summary: The lemming (Lemmus lemmus) – an aberrant rodent). Fauna Och Flora 1977:182–188

    Google Scholar 

  • Andersson M (1981) Reproductive tactics of the long-tailed skua. Oikos 37:287–294

    Article  Google Scholar 

  • Andersson M, Jonasson S (1986) Rodent cycles in relation to food on an alpine heath. Oikos 46:93–106

    Article  Google Scholar 

  • Angerbjörn A, Tannerfeldt M, Erlinge S (1999) Predator–prey relationships: arctic foxes and lemmings. J Anim Ecol 68:34–49

    Article  Google Scholar 

  • Arvola A, Ilmén M, Koponen T (1962) On the aggressive behaviour of the Norwegian lemming (Lemmus lemmus) with special reference to the sounds produced. Arch Soc Zool Bot Fenn ‘Vanamo’ 17:80–101

    Google Scholar 

  • Barth L, Angerbjörn A, Tannerfeldt M (2000) Are Norwegian lemmings Lemmus lemmus avoided by arctic Alopex lagopus or red foxes Vulpes vulpes? A feeding experiment. Wildlife Biol 6:101–109

    Google Scholar 

  • Batzli GO, Pitelka FA, Cameron GN (1983) Habitat use by lemmings near Barrow, Alaska. Holarct Ecol 6:255–262

    Google Scholar 

  • Bergström U (1967) Observations on Norwegian lemmings, Lemmus lemmus (L.), in the autumn of 1963 and the spring of 1964. Ark Zool Ser 2 20:321–363

    Google Scholar 

  • Bohlin T, Tullberg B, Merilaita S (2008) The effect of signal appearance and distance on detection risk in an aposematic butterfly larva (Parnassius apollo). Anim Behav 76:577–584

    Article  Google Scholar 

  • Bohlin T, Gamberale-Stille G, Merilaita S, Exnerova A, Stys P, Tullberg BS (2012) The detectability of the colour pattern in the aposematic firebug, Pyrrhocoris apterus: an image-based experiment with human ‘predators’. Biol J Linn Soc 105:806–816

    Article  Google Scholar 

  • Caro T (2005) Antipredator defenses in birds and mammals. Univ Chicago Press, Chicago

    Google Scholar 

  • Caro T (2009) Contrasting coloration in terrestrial mammals. Philos T Roy Soc B 364:537–548

    Article  Google Scholar 

  • Caro T (2011) The functions of black-and-white coloration in mammals: review and synthesis. In: Stevens M, Merilaita S (eds) Animal camouflage. Cambridge University Press, Cambridge, pp 298–329

    Chapter  Google Scholar 

  • Charnov EL, Finerty JP (1980) Vole population cycles: a case for kin-selection? Oecologia 45:1–2

    Article  Google Scholar 

  • Cott HC (1940) Adaptive coloration in animals. Methuen, London

    Google Scholar 

  • Davies NB, Krebs JR, West SA (2012) An introduction to behavioural ecology, 4th edn. Wiley-Blackwell, Chichester

    Google Scholar 

  • Edmunds M (1974) Defence in animals. Longman, Essex

    Google Scholar 

  • Eibl-Eibesfeld I (1954) Zur Ethologie des Hamsters (Cricetus cricetus L.). Z Tierpsychol 10:204–254

    Google Scholar 

  • Erlinge S, Danell K, Frodin PK, Hasselquist D, Nilsson P, Olofsson EB, Svensson M (1999) Asynchronous population dynamics of Siberian lemmings across the Palaearctic tundra. Oecologia 119:493–500

    Article  Google Scholar 

  • Fedorov VB (1999) Contrasting mitochondrial DNA diversity estimates in two sympatric genera of Arctic lemmings (Dicrostonyx: Lemmus) indicate different responses to Quaternary environmental fluctuations. Proc R Soc Lond B 266:621–626

    Article  Google Scholar 

  • Fedorov VB, Stenseth NC (2001) Glacial survival of the Norwegian lemming (Lemmus lemmus) in Scandinavia: inference from mitochondrial DNA variation. Proc R Soc Lond B 268:809–814

    Article  CAS  Google Scholar 

  • Frafjord K (1995) Summer food habits of arctic foxes in the alpine region of southern Scandinavia, with a note on sympatric red foxes. Ann Zool Fenn 32:111–116

    Google Scholar 

  • Framstad E, Stenseth NC (1993) Habitat use of Lemmus lemmus in an alpine habitat. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 197–211

    Google Scholar 

  • Franks DW, Ruxton GD, Sherratt TN (2009) Warning signals evolve to disengage Batesian mimics. Evolution 63:256–267

    Article  PubMed  Google Scholar 

  • Fredga K, Fedorov V, Jarrell G, Jonsson L (1999) Genetic diversity in Arctic lemmings. Ambio 28:261–269

    Google Scholar 

  • Furness RW (1987) The skuas. T & AD Poyser, Calton

    Google Scholar 

  • Futuyma D (2013) Evolution, 3rd edn. Sinauer, Sunderland

    Google Scholar 

  • Gamberale G, Tullberg BS (1998) Aposematism and gregariousness: the combined effect of group size and coloration on signal repellence. Proc R Soc Lond B 265:889–894

    Article  Google Scholar 

  • Gamberale-Stille G, Bragée C, Tullberg BS (2009) Higher survival of aposematic prey in close encounters with predators: an experimental study of detection distance. Anim Behav 78:110–116

    Article  Google Scholar 

  • Götmark F (1992) Anti-predator effect of conspicuous plumage in a male bird. Anim Behav 44:51–55

    Article  Google Scholar 

  • Guilford T (1988) The evolution of conspicuous coloration. Am Nat 131:S7–S21

    Article  Google Scholar 

  • Hagen Y (1952) Rovfuglene og Viltpleien. Gyldendal norsk forlag, Oslo

    Google Scholar 

  • Halpin CG, Skelhorn J, Rowe C (2014) Increased predation of nutrient-enriched aposematic prey. Proc R Soc Lond B 281:20133255

    Article  Google Scholar 

  • Hellström P, Nyström J, Angerbjörn A (2014) Functional responses of the rough-legged buzzard in a multi-prey system. Oecologia 174:1241–1254

    Article  PubMed  Google Scholar 

  • Henttonen H, Kaikusalo A (1993) Lemming movements. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 157–186

    Google Scholar 

  • Henttonen H, Kaikusalo A, Tast J, Viitala J (1977) Interspecific competition between small rodents in subarctic and boreal ecosystems. Oikos 29:581–590

    Article  Google Scholar 

  • Heske EJ, Jensen PM (1993) Social structure in Lemmus lemmus during the breeding season. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 387–395

    Google Scholar 

  • Heske EJ, Ims RA, Steen H (1993) Four experiments on a Norwegian subalpine microtine rodent assemblage during a summer decline. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 411–424

    Google Scholar 

  • Honkavaara J, Koivula M, Korpimäki E, Siitari H, Viitala J (2002) Ultraviolet vision and foraging in terrestrial vertebrates. Oikos 98:505–511

    Article  Google Scholar 

  • Hoogland JL (1996) Why do Gunnison’s prairie dogs give anti-predator calls? Anim Behav 51:871–880

    Article  Google Scholar 

  • Hörnfeldt B (2012) Miljöövervakning av smågnagare, Naturvårdsverket, http://www2.vfm.slu.se/projects/Hornfeldt/index3.html

  • Ims RA, Yoccoz NG, Killengreen ST (2011) Determinants of lemming outbreaks. Proc Natl Acad Sci U S A 108:1970–1974

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jarrell GO, Fredga K (1993) How many kinds of lemmings? A taxonomic overview. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 45–57

    Google Scholar 

  • Kausrud KL, Mysterud A, Steen H, Vik JO, Østbye E, Cazelles B, Framstad E, Eikeset AM, Mysterud I, Solhøy T, Stenseth NC (2008) Linking climate change to lemming cycles. Nature 456:93–97

    Article  CAS  PubMed  Google Scholar 

  • Killengreen ST, Lecomte N, Ehrich D, Schott T, Yoccoz NG, Ims RA (2011) The importance of marine vs. human-induced subsidies in the maintenance of an expanding mesocarnivore in the arctic tundra. J Anim Ecol 80:1049–1060

    Article  PubMed  Google Scholar 

  • Kingdon J, Agwanda B, Kinnaird M, O’Brien T, Holland C, Gheysens T, Boulet-Audet M, Vollrath F (2012) A poisonous surprise under the coat of the African crested rat. Proc R Soc Lond B 279:675–680

    Article  Google Scholar 

  • Koponen T (1964) The sequence of pelages in the Norwegian lemming, Lemmus lemmus (L.). Arch Soc Zool Bot Fenn ‘Vanamo’ 18:260–278

    Google Scholar 

  • Koponen T, Kokkonen A, Kalela O (1961) On a case of spring migration in the Norwegian lemming, Lemmus lemmus (L.), at Kilpisjärvi in 1960. Ann Acad Sci Fenn A IV Biol 52:1–30

    Google Scholar 

  • Lagerholm VK, Sandovall-Castellanos E, Ehrich D, Abramson NI, Nadachowski A, Kalthoff DC, Germonpré M, Angerbjörn A, Stewart JR, Dalén L (2014) On the origin of the Norwegian lemming. Mol Ecol 23:2060–2071

    Article  PubMed  Google Scholar 

  • Lee TJ, Marples NM, Speed MP (2010) Can dietary conservatism explain the primary evolution of aposematism? Anim Behav 79:63–74

    Article  Google Scholar 

  • Mappes J, Marples N, Endler JA (2005) The complex business of survival by aposematism. Trends Ecol Evol 20:598–603

    Article  PubMed  Google Scholar 

  • Marsden W (1964) The lemming year. Chatto and Windus, London

    Google Scholar 

  • Merilaita S, Kaitala V (2002) Community structure and the evolution of aposematic coloration. Ecol Lett 5:495–501

    Article  Google Scholar 

  • Merilaita S, Ruxton GD (2007) Aposematic signals and the relationship between conspicuousness and distinctiveness. J Theor Biol 245:268–277

    Article  PubMed  Google Scholar 

  • Myllymäki A, Aho J, Lind EA, Tast J (1962) Behaviour and daily activity of the Norwegian lemming, Lemmus lemmus (L.), during autumn migration. Ann Zool Soc ‘Vanamo’ 24:1–31

    Google Scholar 

  • Newman C, Buesching CD, Wolff JO (2005) The function of facial masks in “midguild” carnivores. Oikos 108:623–633

    Article  Google Scholar 

  • Oksanen T (1993) Does predation prevent Norwegian lemmings from establishing permanent populations in lowland forests? In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 425–437

    Google Scholar 

  • Olofsson J, Tømmervik H, Callaghan TV (2012) Vole and lemming activity observed from space. Nat Clim Change 2:880–883

    Article  Google Scholar 

  • Østbye E, Engh CE, Lien L, Mysterud I, Østbye K, Pedersen O, Semb-Johansen A (1993) Regional distribution of lemmings (Lemmus lemmus) during cyclic highs in the Hallingdalen Valley, southern Norway, 1966–1985. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 187–196

    Google Scholar 

  • Ottosson U, Ottvall R, Elmberg J, Green M, Gustafsson R, Haas F, Holmqvist N, Lindström Å, Nilsson L, Svensson M, Svensson S, Tjernberg M (2012) Fåglarna i Sverige – antal och förekomst. SOF, Halmstad

    Google Scholar 

  • Petzsch H (1950) Über Warn– und Drohreaktionen, Imponiergehaben, Schreckstellung und Flucht des Hamsters (Cricetus cricetus L.). Z Tierpsychol 7:293–295

    Article  Google Scholar 

  • Poulton EB (1890) The colours of animals: their meaning and use especially considered in the case of insects. Keegan Paul, London

    Book  Google Scholar 

  • Rausch R (1950) Observations on a cyclic decline of lemmings (Lemmus) on the arctic coast of Alaska during the spring of 1949. Arctic 3:166–177

    Article  Google Scholar 

  • Roper TJ (1990) Responses of domestic chicks to artificially coloured insect prey: effects of previous experience and background colour. Anim Behav 39:466–473

    Article  Google Scholar 

  • Rowe C, Halpin C (2013) Why are warning displays multimodal? Behav Ecol Sociobiol 67:1425–1439

    Article  Google Scholar 

  • Ruffino L, Oksanen T (2014) Co-evolution of jaegers (Stercorarius spp.) and arctic lemmings (Dicrostonyx spp. and Lemmus spp.) and the formation of the jaeger guild: a hypothesis. Evol Ecol Res 16:121–132

    Google Scholar 

  • Ruxton GD, Sherratt TN (2006) Aggregation, defence and warning signals: the evolutionary relationship. Proc R Soc Lond B 273:2417–2424

    Article  Google Scholar 

  • Ruxton GD, Sherratt TN, Speed MP (2004) Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. Oxford University Press, Oxford

    Book  Google Scholar 

  • Schuler W, Hesse E (1985) On the function of warning coloration—a black and yellow pattern inhibits prey attack by naïve domestic chicks. Behav Ecol Sociobiol 16:249–255

    Article  Google Scholar 

  • Sherratt TN (2002) The coevolution of warning signals. Proc R Soc Lond B 269:741–746

    Article  Google Scholar 

  • Sherratt TN, Beatty CD (2003) The evolution of warning signals as reliable indicators of prey defence. Am Nat 162:377–389

    Article  PubMed  Google Scholar 

  • Sherratt TN, Franks DW (2005) Do unprofitable prey evolve traits that profitable prey find difficult to exploit? Proc R Soc Lond B 272:2441–2447

    Article  Google Scholar 

  • Stankowich T, Caro T, Cox M (2011) Bold coloration and the evolution of aposematism in terrestrial carnivores. Evolution 65:3090–3099

    Article  PubMed  Google Scholar 

  • Stankowich T, Haverkamp PJ, Caro T (2014) Ecological drivers of antipredator defenses in carnivores. Evolution 68:1415–1425

    Article  PubMed  Google Scholar 

  • Steen H, Holst JC, Solhøy T, Bjerga M, Klaussen E, Prestegard I, Sundt RC, Johannesen Ø (1997) Mortality of lemmings, Lemmus lemmus, at peak density in a mountainous area of Norway. J Zool 243:831–835

    Article  Google Scholar 

  • Stenseth NC, Ims RA (eds) (1993a) The biology of lemmings. Academic, London

    Google Scholar 

  • Stenseth NC, Ims RA (1993b) The history of lemming research. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 3–34

    Google Scholar 

  • Stenseth NC, Ims RA (1993c) Population dynamics of lemmings: temporal and spatial variation—an introduction. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 61–96

    Google Scholar 

  • Stenseth NC, Ims RA (1993d) Intra- and interspecific relations—an introduction. In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 339–354

    Google Scholar 

  • Stevens M, Merilaita S (eds) (2011) Animal camouflage: mechanisms and function. Cambridge University Press, Cambridge

    Google Scholar 

  • Svennungsen TO, Holen ØH (2007) The evolutionary stability of automimicry. Proc R Soc Lond B 274:2055–2062

    Article  Google Scholar 

  • Taitt MJ (1993) Adaptive colouration in Lemmus lemmus: why aren’t Norwegian lemmings brown? In: Stenseth NC, Ims RA (eds) The biology of lemmings. Academic, London, pp 440–445

    Google Scholar 

  • Taylor JR (1997) An introduction to error analysis, 2nd edn. University Science, Sausalito

    Google Scholar 

  • Thompson DQ (1955) The 1953 lemming emigration at Point Barrow, Alaska. Arctic 8:37–45

    Article  Google Scholar 

  • Tullberg BS, Merilaita S, Wiklund C (2005) Aposematism and crypsis combined as a result of distance dependence: functional versatility of the colour pattern in the swallowtail butterfly larva. Proc R Soc Lond B 272:1315–1321

    Article  Google Scholar 

  • Wallace AR (1867) Proceedings of the entomological society of London. March 4:lxxx-lxxxi

  • Wiklund CG, Angerbjörn A, Isakson E, Kjellén N, Tannerfeldt M (1999) Lemming predators on the Siberian tundra. Ambio 28:281–286

    Google Scholar 

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Acknowledgments

I thank the Swedish Research Council, Christer Jonasson and the Abisko Scientific Research Station for research grants, and the Naval Arctic Research Laboratory, Barrow, Alaska, for fieldwork facilities. I am grateful to my field companions, in particular Sven Jonasson and Jan Uddén; to Nils Åke Andersson, Anders Angerbjörn, Lars Baer, Sven Jakobsson, Heikki Henttonen, Birger Hörnfeldt and Johan Wallander for information about lemming abundance; to Staffan Andersson, Donald Blomqvist and Gabriella Gamberale-Stille for helpful discussions; to Anders Angerbjörn, Tim Caro, Alecia Carter, Frank Götmark, Rolf Ims, Sami Merilaita, Joacim Näslund, Birgitta Tullberg and anonymous referees for constructive suggestions on the manuscript; and to Peter Myers and Larry Underwood for valuable help at Barrow. Alexander Rydén kindly provided the video clip of a Norwegian lemming. The Abisko experiment was kindly made possible with short notice by Urban Emanuelsson and his biology student group.

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Appendix

Appendix

To measure my step length and its precision, I counted steps to each of 50 targets in heath habitat, also measuring each distance to the nearest 0.1 m with a tape. The average step length, 0.80 m, was obtained as the sum of distances (722.4 m) divided by the sum of steps (902). One way of checking the precision (relative or fractional uncertainty, Taylor 1997) and consistency of the step-based estimate is plotting it against the distance measured by tape (Fig. 4). With its higher precision (usually less than 1 % error), the tape measure is here used as the real distance with which to compare the less accurate step-based estimate (see Taylor 1997). Taking the absolute value of the difference between a tape measurement and the corresponding step-based estimate, and dividing by the tape measurement, gives the relative error of the step-based estimate. The 50 distances thus estimated to the nearest m (number of steps x 0.8) differed on average by 6.3 % from the tape measurements (see Fig. 4). The step-based measure is therefore adequate for exploring the distance trend in lemming calls at encounters, which spans a range of 0–38 m (Fig. 2).

Fig. 4
figure 4

Relationship between 50 measured distances and the corresponding estimates based on steps (see “Appendix” text). The average relative error of the step-based estimate compared to the measured distance (solid line) is 6.3 %

Further support for the step-based measure is a test in Alaskan coastal tundra, counting my steps 5 times along a 100-m distance measured by tape, giving an average of 124.6 steps (SD = 0.9), i.e. a step length of 0.80 m. Although the identity with the step length estimated here is a coincidence, the similarity supports the usefulness in the wild of a step-based distance measure (which may of course vary between individuals and habitats, owing to differences in e.g. stature and topography).

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Andersson, M. Aposematism and crypsis in a rodent: antipredator defence of the Norwegian lemming. Behav Ecol Sociobiol 69, 571–581 (2015). https://doi.org/10.1007/s00265-014-1868-7

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