Small mammal cycles

TREE vol. 2, no. 6, June 1987

formation is now very much with us. AI1 of the taxonomic tools available to the palaeontologist, including the study of morphology alone, have particular strengths and weaknesses; taken in combination, molecular and morphological, living and fossil, they will be a potent measure of taxonomic relationships. The real interest, and fun, and perhaps even a real advance in evolutionary understanding, will come when major discrepancies occur between the various techniques! Acknowledgements I am grateful to Matthew 1. Collins for his comments on an early draft of this article.

References M.A. (1985) Geochemistry ofMarine Humic Compounds, Springer-Verlag 2 Ourisson, G., Albrecht, A. and Rohmer, M. I I9841 Sci. Am. 25 I, 34-4 I 3 Lowenstam, H.A. and Weiner, S. I19831 in Biomineralisation and Biological Metal Accumulation (Westbroek, P. and De long, E.W.. eds). pp. 191-203, Reidel 4 Hoering, T.C. ( I9801 in Biogeodemistry of Amino Acids (Hare, P.E. Hoering. T.C. and King, K., edsl, pp. 193-201, John Wiley&Sons 5 Armstrong, W.G., Halstead, L.B.. Reed, F.B. and Wood, L. 119831 Philos. Trans. R. Sot.

1 Rashid.

London Ser. B 301,301-343 6 Wyckoff, R.W.G. ( 19721 The Biochemistry of Animal Fossils, Scientechnica 7 Akiyama, M. ( 1971 I Biomineralization 3,65-70 8 Akiyami, M. and Wyckoff, R.W.G. ( I9701 Proc. Nat/ Atad.Sti. USA 67, 1097-I 100 9 Voss-Fouchart, M.F. and CrCgoire, C. ( 1971 Bull. Inst. R. Sti. Nat. Belg. 72,86-93 IO Weiner, S. and Lowenstam, H.A. II9801 in Acids (Hare, P.E., Biogeothemistry ofAmirzo Hoering, T.C. and King, K., edsl, pp. 95-l 14, John Wiley&Sons I I Schroeder, R.A. and Bada, 1.L. (19761 Earth Sci. Rev. I2,347-39 I 12 Voss-Fouchart, M.F. and Gri‘goire, C. I I9751 Arch. Internat. Physio/. Biochim 83, 43-52 I3 Tissot, B.P. and Welte, D.H. ( 1984) Petroleum Formation and Occurrence. SpringerVerlag 14 Abelson, P.H. (1954) Carnegie Inst. Washington Year&. 53,97-I01 15 Abelson, P.H. (1955) Carnegie Inst. Washington Yeah. 54, 107-l 09 16 Mycke, B., Narjes, F. and Michaelis, W. (19871 Nature 326, 179-181 17 Muyzer, G., Westbroek, P., De Vrind, I.P.M., Tanke, I., Vriiheid, T.. De long, E.W., Bruning, J.W. and Wehmiller, I.F. I I9841 Org. Geothem. 6,847-855 I8 Lowenstein. J.M. (I981 1Phi/. Trans. R. Sot. London Ser. B 292, 143-149 I9 De long, E., Westbroek, P., Westbroek, I.F. and Bruning, I.W. (1974) Nature 252,63-64 20 Westbroek, P., Van der Meide. P.H. Van der Wey-Kloppers, J.S., Van der Sluis. R.J., de Leeuw, j.W. and De long, E.W. II9791 Paleobiology 5, 151-167 21 Lowenstein. J.M. I I9801 Natt,,rwissenscha/ten 67,343-346

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22 Westbroek, P., Tanke-Visser, j., De Vrind, I.P.M., Spuy, R., Van der Pal. W. and De long, E.W. I 1983) in Biomineralisation and Biologica/ Metal Accumulation (Westbroek. P. and De long, E.W., edsl, pp. 249-253, Reidel 23 Treibs, A. (1934) Ann. Gem. 5 IO, 42-62 24 Eglinton. G. and Calvin, M. (1967) Sri. Am 216,32-43 25 Mackenzie, A.S., Brassell, SC., Eglinton, C and Maxwell, I.R. ( I982 I Science 2 I 7.49 l-504 26 Robson, J.N. and Rowland, S.I. f 1986) Nature 324,561-563 27 Brassell, S.C., Eglinton, C., Marlowe, I.T. Pflaumann, U. and Sarnthein. M. 11986) Nature 320, 129-l 33 28 lope, M. ( 1980) in Biogeochemistry of Amino Acids IHare, P.E., Hoering, T.C. and King, K., edst, pp. 83-94, lohn Wiley & Sons 29 Kolesnikov, C.M. and.Prosorovskaya. E.L. I I9861 in Les Brachiopodes Fossiles et Actuels IBiostratigraphie du Paleozoique 41. IRacheboeuf, P.R. and Emig, CC.. edsl. pp. I 13-l 20, Brest 30 Wilson, AC., Carlson, S.S.and White, T.I. II9771 Annu. Rev. Biochem. 46, 573-639 31 Maxson, R.d. and Maxson, L.R. 11986) Mol. Biol. Evol. 3, 375-388 32 Runnegar. B. ( 19861 Palaeontology 29, l-24 33 Weiner, S., Lowenstam, H.A. and Hood, L. ( 1976) Proc. Nat/ Atad. Sri. USA 73, 25 14-2545 34 Weiner, S., Lowenstam, H.A., Taborek, B. and Hood, L. (I9791 Paleobiology 5, 144-150 35 Cohen, B.L., Curry, G.B. and Balfe, P. I I9861 in Les Brathiopodes Fossiles et Actue/s IBiostratigraphi~ du Paleozoique 41 (Racheboeuf. P.R. and Emig, C.C.. edsl, pp 54-64, Brest 36 Curry, C.B. and Ansell, A.D 11986) in Les Brachiopodes Fossiles etA&e/s I Biostratigraphie du Paleozoique 4) Racheboeuf, P.R and Emig, C.C. edsl, pp. 23 l-242, Brest

Letters to the Editor: Small Mammal

Cycles

The idea that all populations of small mammals are cyclic is indeed dead, as pointed out by Hanski in his recent news article in Trends in Ecology and Evolution’. However, the statement that ‘recent work may change our discouragement about population cycles of small mammals’ I find unfounded. The data backing up this statement are not only difficult to interpret but also mostly nonexistent. Clearly, something exceptional is happening in northern Fennoscandinavia. Henttonen’s* 1 g-year data series on the synchronous cycles of six rodent species from Pallasjarvi, Finland, are amazing but not unique. There is similar data series (15 years) for three rodent species from Ume4 in northern Sweden (B. Hijrnfeldt, pers. commun., and Ref. 3). Howthat ever, Hanski’s assertion Clethrionomys does not cycle in North America or shows less regular multiannual cyclicity may not necessarily be true. It is not Taitt and Krebs4 that claim that the genus Clethrionomys does not cycle in North America, as stated by Hanski, but rather Henttonen et aI.= and

Hansson and HenttonenG. In any event, this is a tentative conclusion because it is based on only two studies of C. gapperi and three studies of C. rutilus. Surely more data are needed. Hanski points out that there is a gradient from central Europe to northern Fennoscandia with an increase in regularity, amplitude and synchronicity of the rodent cycle7e8. A correlation with those factors and latitude says nothing about causality. Nor does it mean that truly cyclic populations of rodents (whatever true cyclicity really is) cannot be found outside of northern Fennoscandia. What is important in the ‘rodent cycle’ is the regular occurrence of a particular demographic pattern characterized by an increase in density, and then a rapid crash which is often followed by an extended low (one year). This is what needs to be explained. This kind of population dynamics is also found in several other geographical regions. There are two issues: (I) the cause of the crash in rodent density, and (2) the cause of the synchrony in density pattern among several populations of rodents in northern Fennoscandia. Hanski acknowledges

that we know little about the cause of the crash but feels that we are on the verge of understanding the synchrony. However, Hanski confuses these two issues in his article. For example, in the comparison between the effect of predators on populations of rodents from southern Sweden with populations of rodents from northern Fennoscandia the issue is the cause of the crash, not synchrony. Synchrony cannot be an issue in southern Sweden where the populations of rodents are not cyclic. Hanski proposes two extrinsic factors that could ‘play a crucial role in the vole cycle in northern Fennoscandia’: food and predators. It is essential to remember that the issue is the cause of the synchrony and not the cause of the crash. Hanski dismissed food in a few lines, giving three reasons. (1) different microtine rodent species eat partly or mostly different foods. The Clethrionomys. group may eat different foods but these different foods often come from the same species of plants (e.g. leaves, bark and berries of Vaccinium myrti//us)g. Also, the finding that there appears to be a natural cycle in the productivity of some plant 165

TREE vol. 2, no. 6, June 1987

species in northern Finlandlo,” is not mentioned. (2) Rodents in the boreal forests in Fennoscandia do not have a dramatic impact on their food resource. It is true that no obvious impact on the vegetation can be seen, but the effects of consumption of nutrients and secondary compounds are not always easy to observe. Recent work has shown that nutrients and secondary compounds did not vary with the cycle of C. rufocanus12f13. Studies of the effect of plant secondary compounds usually concentrate on toxic compounds. However, nontoxic compounds with a hormonal effect, such as phytoestrogens, could be more important. Not until there is experimental evidence, from the use of animals as biological assays of nutrition and secondary compounds, can the role of nutrition and secondary compounds be discounted. (3) Shrews, which are insectivores, should not fluctuate in synchrony with the rodents if food plays a crucial role in the vole cycle. Shrews may crash with the voles but they often recover in density during the year after the crash when voles remain low (G.A. Sonerud, unpublished). If predators were extending the low phase of the rodent cycle why should these predators not also keep the density of shrews low? What is the evidence for predators synchronizing the crash among several populations of rodents? Erlinge has indeed shown that a diverse predator community in southern Sweden switching among prey types may be responsible for keeping rodent numbers low and varying annually14. However, this is not proof that a few specialist predators are responsible for the synchronous cyclic nature of the rodents in northern Fennoscandia. A theoretical model shows that habitat heterogeneity alone, without predators, will result in stable density dynamics in a rodent populationls. There are few data on simultaneous density changes in cyclic rodent populations and mustelid predators. No systematic censusing of mustelid predators (stoats and least weasels) was done in Henttonen’s study area before 1981, and then the data are based only on track counts2. The last peak in density discussed by Henttonen2 was unusual in that it extended from 1980 to 1985. From 1981 to 1985, the estimated number of stoats and least weasels visiting the study area (2 km*) varied from 0 to 5 and 0 to 2 respectively, but what these numbers mean is difficult to interpret. These data are used to argue that predators failed to 166

respond numerically and thus permitted the extended cycle. However, without comparative data on predation during the other cycles of normal (short) duration, one cannot draw any conclusions. One can only speculate, that is, propose a hypothesis, and that is all that Henttonen has done16. One can take the hypothesis discussed by Hanski and lower it one trophic level. Diversity of plants in northern Fennoscandia is lower than in southern Fennoscandia17. The rodent cycle might be explained by the increased foraging pressure per plant species in northern Fennoscandia causing a mobilization of defence mechanisms in the plants, which may in turn cause the crash in the rodent populations and keep density low for a year or so. Predators may indeed ultimately prove to be intricately linked with the synchronous, high amplitude rodent cycle from northern Fennoscandia, but until there are data to test these ideas experimentally, we should not be misled into thinking that the small mammal cycle is on the threshold of being solved.

References 1 Hanski, I. (1987) Trends Ecol. Evol. 2, 55-56 2 Henttonen, H., Oksanen, T., Jortikka,A. and Haukisalmi, V. CJikos(in press) 3 Hernfeldt, H., Laefgren, 0. and Carlsson, B-G. (1986) Oecologia 68, 496-502 4 Taitt, M.J. and Krebs, C.J. (1985) in Biology of New World Microtines (Tamarin, R.H., ed.), pp. 567-620, American Society of Mammalogists 5 Henttonen, H., MC&ire, A.D. and Hansson L. (1985) Ann. Zoo/. Fenn. 22, 221-227 6 Hansson, L. and Henttonen, H. (1985) Ann. Zool. Fenn. 22,277-288 7 Hansson, L. and Henttonen, H. (1985)

Oecologia 67,394-402 6 Henttonen, H. and Hansson, L. Ho/arc. Ecol. (in press) 9 Hansson, L. (1985) Ann. Zoo/. Fenn. 315-318 10 Laine, K. and Henttonen, H. (1983) Oikos 40,407-41

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11 Tast, J. and Kalela, 0. (1971) Ann. Acad. Sci. Fenn. Ser. A4 186, l-l 4 12 Andersson, M. and Jonasson, S. (1986) Oikos 46,93-l 06 13 Jonasson, S., Bryant, J.P., Chapin, F.S., IV and Andersson, M. (1986) Am. Nat. 128,394-409 14 Erlinge, S., GBransson, G., Hansson, L.,

HGgsted, G., Liberg, 0.. Nilsson, I.N., von Shantz, T. and SylvBn, N. (1983) 0ikos40, 36-52 15 Bondrup-Nielsen, S. and Ims, R.A. Ssren Bondrup-Nielsen Oikos (in press) 16 Henttonen, H. Oikos (in press) Deptof Biology,DivisionofZoology,University of Oslo, 17 SjBrs, H. (1965) Acta Phytogeogr. Suet. Blindern,Box1050,N-0316.Oslo3, Norway. 50,48-63

Replyfrom I. Hanski Bondrup-Nielsen accuses me of wrongly endorsing the view that specialist predators, especially the small mustelids, might be the proximate cause of the exceptionally regular microtine rodent cycle in northern Fennoscandia, and of dismissing alternative views ‘in a few lines’. The purpose of my news item was not to review population cycles in small mammals in 1000 words but to draw readers’ attention to an interesting series of papers contributing new facts to the seemingly endless (and to many, fruitless) debate about small mammal cycles. I concluded that ‘geographical comparisons [due to Henttonen and Hansson, whose work1-3 was being discussed] have been helpful, and the results of synchronous declines are suggestive, but they do not remove the need for critical experiments, difficult as they are to carry out on a meaningful spatial scale’. The matters examined by Henttonen and Hansson were interspecific synchrony’ and geographi-

cal patterns in the amplitude and regularity of small mammal cycles1,3, and contrary to what BondrupNielsen believes the conclusions in these papers are based on extensive data sets from EuropelG2 and North America’. Bondrup-Nielsen may have failed to grasp the significance of synchronous crashes in syntopic species, when he wishes to keep ‘the cause of the crash in rodent density’ and ‘the cause of the synchrony in density pattern among several populations of rodents’ as two separate issues, which they can hardly be. He is simply wrong in suggesting that non-cyclic abundance changes cannot be synchronous in two or more species. Nobody has claimed that the predation hypothesis has already been shown to be correct in Fennoscandia; what has been said is that this hypothesis is consistent with the geographical and interspecific patterns documented by Henttonen and Hansson, and that it should be experimentally tested. Bondrup-