- Open Access
Did British breeding birds move north in the late 20th century?
© The Author(s). 2016
- Received: 15 April 2016
- Accepted: 27 July 2016
- Published: 19 August 2016
Contemporary climate change is the biggest experiment ever conducted by humans on a planetary scale, and its impact on the redistribution of life is potentially huge (e.g., Barnosky et al. Nature 471:51–57, 2011, Pereira et al. Science 330:1496–1501, 2010). An accurate diagnosis of the effects of climate change on the distributions of species requires, firstly, that methods used for detection of distributional changes are able to distinguish between directional and non-directional changes and, secondly, that they are able to tease apart distributional changes driven by natural population dynamics from changes driven by external forcing (climatic or non-climatic). We ask how appropriate are methods commonly used to detect directional shifts on species range changes.
We compare a widely used range-shift detection method previously used to demonstrate that climate change caused British breeding bird distributions to move northwards with alternative approaches that more comprehensively examine directionality in range changes. We find that once range dynamics are examined across all geographical quadrants in Britain, and in contrast with previous reports, no clear directional patterns of range shift emerge for this period.
Some of the methods typically used for examining species range shifts are prone to false positive errors, whereby directional range shifts are detected when in fact they did not occur. Without entering the discussion of what is more important to avoid (false negative errors, whereby directional range shifts pass unnoticed by analysis, or false positive errors), we argue that methods exist to determine whether range changes are directional or non-directional (a prerequisite to discern the causes of range changes).
Several studies have reported that range margins of many species moved poleward, probably in response to recent climate warming (e.g., [1–3]). In a highly influential study, Thomas and Lennon  reported that distributions of many British breeding birds moved north between 1968–1972 (T1) and 1988–1991 (T2) in what appeared to be a clear and predictable response to climate warming. We reanalyzed the data using methods designed to effectively distinguish directional and non-directional shifts in species range changes. We found that range expansions and contractions were non-directional in the ca. 20 years period examined by Thomas and Lennon (T&L). With some exceptions, expanding species expanded distributional limits across all geographical quadrants and contracting species contracted distributional limits across all quadrants. Late 20th Century patterns of range change among British breeding birds seem to be consistent with meta-population theory that predicts extinctions and colonization events to occur mainly in ‘sink’ habitats within the periphery of species ranges ; an observation that had already been made using the same data but different analyses [6, 7].
Climate limits the distributions of species, both directly by causing changes in the abiotic environment in which a species lives and, indirectly, by causing changes in biotic interactions and feedbacks between biotic interactions and abiotic processes (e.g., [8, 9]). The direct impact of climate change on species distributions is often investigated with phenomenological estimates of species-climate relationships. Usually, such relationships are inferred by matching present-day species distributions with climate variables (e.g., ). Yet, determining whether given climate change exceeds species climatic tolerances using analysis of species range data is difficult because there are many non-climatic factors constraining species distributional limits (e.g., [11, 12]). Species distributional dynamics across a given time period can be also examined by comparison with climate change patterns for the same period (e.g., [13–15]). The general principle is that if species distributional limits are moving in the same direction as climate change, then one might reasonably conclude that climate change is involved. Several studies have used the latter approach to detect latitudinal (e.g., ) and altitudinal (e.g., [17, 18]) shifts in species distributional limits.
However, detecting directional changes in species distributions requires that changes are compared across all geographical quadrants rather than just northern and southern range limits (see also ). In the northern hemisphere, the critical question is whether species distributions are, on average, moving northward—as expected if expansions were driven by climate warming—, or evenly across distributional margins—as expected if expansions were driven by population dynamics (e.g., [6, 7, 20]) or by multiple drivers acting in several directions and causing range changes to be complex and seemingly idiosyncratic (e.g., [21, 22]). Likewise, one should ask if local extinctions are, on average, occurring mainly at southern margins or whether they are ubiquitous across all margins of the species range.
Thomas and Lennon  measured distributional changes within the northern and the southern margins of species. Since distributional dynamics were expected to be different for southerly and northerly-distributed species, T&L grouped species based on their average geographical position within Britain. Consistent with the hypothesis that climate warming drove changes in the distributions of birds, they found that the northern margins of southerly-distributed species that increased ranges shifted northwards, while the northern margins of many southerly-distributed species that declined overall shifted southwards. In contrast, the southern margins of northerly-distributed species that increased ranges generally shifted southwards, whereas the southern margins of most of the northerly-distributed species that declined shifted northwards. In addition, they found that the northern margins of southerly-distributed species with no overall change in range size had a northward shift of 18.9 km, while no systematic distributional shift towards north or south was detected for northerly-distributed species. Gillings and colleagues  examined range dynamics more broadly and confirmed the general trend reported by T&L, while also detecting the existence of complex, multi-directional shifts that passed unnoticed in the original 1999 analysis.
We reanalyzed the data [23, 24] using two different analytical approaches that more explicitly seek to distinguish directional shifts from non-directional ones (see Additional file 1), and then asked whether late 20th Century changes in distributional limits of British breeding birds were significantly different across geographical quadrants. We assumed that if distributional changes of birds were not significantly different among quadrants (a question not addressed in previous studies), warming of temperatures should not be immediately invoked as the key candidate driver of such changes (see Additional file 2: Figure S1).
The northern limits of southerly distributed species that did not show an overall change in their range sizes (the interpretation of the x = 0 intercept in Fig. 1a) moved 22.35 km north on average, which is comparable with the 18.9 km northward shift reported by T&L (but P = 0.545). These species also shifted 5.96, 4.92 and 12.78 km inward, on average, along the southern, eastern and western margins of their ranges respectively (P <0.001, P = 0.091 and P < 0.001). The margins of northerly-distributed species followed similar patterns (P < 0.001) except along the western margins for which no meaningful range shift was detected (P = 0.712).
In the second analysis, we used a novel approach that counts the number of local expansion and contraction events in each geographical quadrant relative to the available land area (Additional file 2: Figure S1C). We found that the proportion of contracting and expanding marginal cells within each quadrant was not significantly different between quadrants for contracting and expanding species (Wilcoxon signed-rank test; P > 0.05) (Fig. 1b). An exception was recorded for southerly distributed species, whose patterns of range contraction were generally greater in the northern quadrant compared to the eastern one (P = 0.021). Overal, given these multiple significant tests across the four geographical quadrants we can argue that shifts were not significant at the level 0.05.
Several analysis and meta-analysis have reported pole-ward and elevation-ward shifts in distributional limits of species without contrasting them with distributional changes across their full range. Whether range shifts provide evidence that climate change is acting on them depends on the congruence of the range shifts patterns with climate change patterns . If range dynamics for expanding species are measured at only a single range edge, then, the likelihood is great that an expansion will be detected and erroneous conclusions could be made. But if range shifts, or pulses of range expansion and contraction, are ubiquitous across the range, then natural population dynamics, or non-linear interactions between climate and non-climatic vectors, such as biological invasions (e.g., ), land use (e.g., ), and/or disease (e.g., ), might be reasonably invoked as alternative driving forces of change.
There is a consensus that attribution of climate change effects to species range shifts should, ideally, be based on multiple lines of evidence (e.g., ). We agree. However, whenever inferences of climate change effects on range dynamics are based on statistical analysis of species range change data, it is crucial that tests are able to adequately distinguish directional and non-directional shifts (see also ). Such comparisons between observed species distributional patterns and expected distributional patterns under absence of process are the underlying principle of null models , and are becoming standard practice in different sub-fields of ecology (e.g., [31, 32]), biogeography (e.g., [33, 34]), conservation and global change biology (e.g., [35, 36]). Failure to undertake such comparisons in studies examining species range changes can lead to inflation of false positive errors by equivocally concluding for the existence of directional range shifts when they are no different from the null expectation.
Raising the bar of evidence in studies attributing climate change effects on species range changes is important to reduce errors of interpretation that could lead to erroneous management decisions. For example, if particular change in land-use practices causes a given species to contract its range, attributing the effect to climate change might lead to inappropriate management actions and inefficient allocation of funds to conservation in the short term. In the long term, failing to adhere to high standards could have the consequence of decreasing of confidence in climate change attribution studies as well as models, which would bring about the risk of neglecting important climate change impacts in management decisions.
T&L, Thomas & Lennon
We thank Chris Thomas for comments on an early version of this manuscript, and Carsten Rahbek and Camille Parmesan for discussion. We also thank the tens of thousands of volunteers who recorded the data for the British breeding bird atlases.
This research was partly supported by the Danish National Research Foundation Grant attributed to the Center for Macroecology, Evolution and Climate. MBA also acknowledges support from CIBIO-UID/BIA/50027/2013 (POCI-01-0145-FEDER-006821), and the Spanish National Research Council.
ST, BN, and MBA designed the analysis. ST led the analysis with important contributions from BN. MBA wrote the article with contributions from all authors. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
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- Parmesan C, Yohe G. A globally coherent fingerprint of climate change impacts across natural systems. Nature. 2003;421:37–42.View ArticlePubMedGoogle Scholar
- Root TL, Price JT, Hall KR, Schneider SH, Rosenzweig C, Pounds JA. Fingerprints of global warming on wild animals and plants. Nature. 2003;421:57–60.View ArticlePubMedGoogle Scholar
- Chen I-C, Hill JK, Ohlemüller R, Roy DB, Thomas CD. Rapid range shifts of species associated with high levels of climate warming. Science. 2011;333(6045):1024–6.View ArticlePubMedGoogle Scholar
- Thomas CD, Lennon JJ. Birds extend their ranges northwards. Nature. 1999;399:213.View ArticleGoogle Scholar
- Pulliam HR. Sources, sinks, and population regulation. Am Nat. 1988;132(5):652–61.View ArticleGoogle Scholar
- Donald PF, Greenwood JJD. Spatial patterns of range contraction in British breeding birds. IBIS. 2001;143:593–601.View ArticleGoogle Scholar
- Araújo MB, Williams PH, Fuller RJ. Dynamics of extinction and the selection of nature reserves. Proc R Soc London, Ser B. 2002;269:1971–80.View ArticleGoogle Scholar
- Ottersen G, Planque B, Belgrano A, Post E, Reid PC, Stenseth NC. Ecological effects of the North Atlantic Oscillation. Oecologia. 2001;128(1):1–14.View ArticleGoogle Scholar
- Post E. Ecology of climate change. Princeton: Princeton University Press; 2012.Google Scholar
- Peterson AT, Soberón J, Pearson RG, Anderson RP, Nakamura M, Martinez-Meyer E, Araújo MB. Ecological niches and geographical distributions. New Jersey: Princeton University Press; 2011.Google Scholar
- Araújo MB, Ferri-Yáñez F, Bozinovic F, Marquet PA, Valladares F, Chown SL. Heat freezes niche evolution. Ecol Lett. 2013;16(9):1206–19.View ArticlePubMedGoogle Scholar
- García-Valdés R, Zavala MA, Araújo MB, Purves DW, Gibson D. Chasing a moving target: projecting climate change-induced shifts in non-equilibrial tree species distributions. J Ecol. 2013;101(2):441–53.View ArticleGoogle Scholar
- Thomas CD. Climate, climate change and range boundaries. Divers Distrib. 2010;16(3):488–95.View ArticleGoogle Scholar
- Root T. Energy constraints on avian distributions and abundances. Ecology. 1988;69(2):330–9.View ArticleGoogle Scholar
- Gaston KJ. Geographic range limits: achieving synthesis. Proc R Soc B Biol Sci. 2009;276(1661):1395–406.View ArticleGoogle Scholar
- Walther G-R, Berger S, Sykes MT. An ecological ‘footprint’ of climate change. Proc R Soc Lond Ser B. 2005;272:1427–32.View ArticleGoogle Scholar
- Colwell RK, Brehm G, Cardelús CL, Gilman AC, Longino JT. Global warming, elevational range shifts, and lowland biotic attrition in the wet tropics. Science. 2008;322(5899):258–61.View ArticlePubMedGoogle Scholar
- Wilson RJ, Gutiérrez D, Martínez D, Agudo R, Monserrat VJ. Changes to the elevational limits and extent of species ranges associated with climate change. Ecol Lett. 2005;8:1138–46.View ArticlePubMedGoogle Scholar
- Gillings S, Balmer DE, Fuller RJ. Directionality of recent bird distribution shifts and climate change in Great Britain. Glob Chang Biol. 2015;21(6):2155–68.View ArticlePubMedGoogle Scholar
- Bradshaw CJ, Brook BW, Delean S, Fordham DA, Herrando-Perez S, Cassey P, Early R, Sekercioglu CH, Araujo MB. Predictors of contraction and expansion of area of occupancy for British birds. Proc Biol Sci 2014, 281(1786).Google Scholar
- VanDerWal J, Murphy HT, Kutt AS, Perkins GC, Bateman BL, Perry JJ, Reside AE. Focus on poleward shifts in species’ distribution underestimates the fingerprint of climate change. Nat Clim Chang. 2013;3(3):239–43.View ArticleGoogle Scholar
- Garcia RA, Cabeza M, Rahbek C, Araujo MB. Multiple dimensions of climate change and their implications for biodiversity. Science. 2014;344(6183):1247579.View ArticlePubMedGoogle Scholar
- Sharrock JTR. The atlas of breeding birds of Britain and Ireland. Berkhamsted: Poyser; 1976.Google Scholar
- Gibbons DW, Reid JB, Chapman RA. The new atlas of breeding birds in Britain and Ireland: 1988–1991. London: Poyser; 1993.Google Scholar
- Sax DF, Gaines SD. Species invasions and extinction: the future of native biodiversity on islands. Proc Natl Acad Sci. 2008;105(Supplement 1):11490–7.View ArticlePubMedPubMed CentralGoogle Scholar
- Jetz W, Wilcove DS, Dobson AP. Projected impacts of climate and land-use change on the global diversity of birds. PLoS Biol. 2007;5(6):e157.View ArticlePubMedPubMed CentralGoogle Scholar
- Hof C, Araújo MB, Jetz W, Rahbek C. Additive threats from pathogens, climate and land-use change for global amphibian diversity. Nature. 2011;480:516–9.PubMedGoogle Scholar
- Parmesan C, Burrows MT, Duarte CM, Poloczanska ES, Richardson AJ, Schoeman DS, Singer MC. Beyond climate change attribution in conservation and ecological research. Ecol Lett. 2013;16 Suppl 1:58–71.View ArticlePubMedGoogle Scholar
- O’connor MI, Holding JM, Kappel CV, Duarte CM, Brander K, Brown CJ, Bruno JF, Buckley L, Burrows MT, Halpern BS, et al. Strengthening confidence in climate change impact science. Glob Ecol Biogeogr. 2015;24(1):64–76.View ArticleGoogle Scholar
- Gotelli NJ, Graves GR. Null models in ecology. Washington: Smithsonian Institution Press; 1996.Google Scholar
- Cazelles K, Araújo MB, Mouquet N, Gravel D. A theory for species co-occurrence in interaction networks. Theor Ecol. 2015;9(1):39–48.View ArticleGoogle Scholar
- Gotelli NJ, Graves GR, Rahbek C. Macroecological signals of species interactions in the Danish avifauna. Proc Natl Acad Sci. 2010;107(11):5030–5.View ArticlePubMedPubMed CentralGoogle Scholar
- Rahbek C, Gotelli NJ, Colwell RK, Entsminger GL, Rangel TFLVB. Predicting continental-scale patterns of bird species richness with spatially explicit models. Proc R Soc Lond B Biol Sci. 2007;274:165–74.View ArticleGoogle Scholar
- Colwell RK, Lees DC. The mid-domain effect: geometric constraints on the geography of species rechness. Trends Ecol Evol. 2000;15:70–6.View ArticlePubMedGoogle Scholar
- Araújo MB, Alagador D, Cabeza M, Nogués-Bravo D, Thuiller W. Climate change threatens European conservation areas. Ecol Lett. 2011;14(5):484–92.View ArticlePubMedPubMed CentralGoogle Scholar
- Williams PH, Araújo MB. Apples, oranges, and probabilities: integrating multiple factors into biodiversity conservation with consistency. Environ Model Assess. 2002;7:139–51.View ArticleGoogle Scholar