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Are Animals Shrinking Due to Climate Change? Temperature-Mediated

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Are Animals Shrinking Due to Climate Change? Temperature-Mediated Are animals shrinking due to climate change? Temperature-mediated selection on body mass in mountain wagtails January 30, 2019 Jorinde Prokosch1, Zephne Bernitz2, Herman Bernitz3, Birgit Erni4, Res Altwegg4;5 1. Department of Mathematical Sciences, Norwegian University of Science and Technology, 7034 Trondheim, Norway 2. Veterinary Consultant, Middelburg MPU, South Africa 3. Department of Oral Pathology and Oral Biology, School of Dentistry, University of Pretoria, Pretoria, South Africa 4. Statistics in Ecology, Environment and Conservation, Department of Statistical Sciences, Uni- versity of Cape Town, Rondebosch 7701, South Africa 5. African Climate and Development Initiative, University of Cape Town, Rondebosch 7701, South Africa Author Contributions ZB, HB and RA conceptualized this study based on ideas of the late Steven Piper. ZB and HB collected data. JP, RA and BE analysed the data. JP and RA wrote the manuscript. All authors contributed to revisions. 1 Abstract Climate change appears to affect body size of animals whose optimal size in part depends on temperature. However, attribution of observed body size changes to climate change requires an understanding of the selective pressures acting on body size under different temperatures. We examined the link between temperature and body mass in a population of mountain wagtails (Motacilla clara) in KwaZulu-Natal, South Africa, between 1976 and 1999, where temperature increased by 0.18◦C. The wagtails became lighter by 0.035g per year. Partitioning this trend, we found that only a quarter of the effect (0.009g / year) was due to individuals losing weight and three quarters (0.027g / year) was due to lighter individuals replacing heavier ones. Only the latter component was statistically significant. Apparently, the wagtails were reacting to selection for reduced weight. Examining survival, we found that selection was temperature- mediated, i.e. lighter individuals survived better under high temperatures whereas heavier individuals survived better under low temperatures. Our results thus support the hypothesis that temperature drove the decline in body mass in this wagtail population and provides one of the first demonstrations of the selective forces underlying such trends. Key-words: body mass; climate change; survival; Motacilla clara; Bergmann’s rule 2 Introduction Climate change is having fundamental impacts on ecosystems around the globe (Walther et al., 2002; Parmesan & Yohe, 2003). One of the main components of climate change is temperature, which has increased globally by approximately 0.9◦C over the past 100 years (Blunden & Arndt, 2017). This change has affected many aspects of biological organisation (Parmesan, 2006), including range shifts (Thomas & Lennon, 1999), changes in phenology (Both & te Marvelde, 2007) and species interactions (Visser et al., 2004). An intriguing idea is that rising temperature could lead to changes in animals’ body sizes (Yom-Tov, 2001). The idea rests on the observation, known as Bergmann’s rule, that endothermic animals tend to be smaller in size in warmer environments than in colder regions (Bergmann, 1847). Bergmann’s rule appears to hold broadly at least across mammals and birds (Ashton et al., 2000; Ashton, 2002) but the mechanism responsible for this pattern is debated (reviewed in Blackburn et al., 1999; Watt et al., 2010). Bergmann’s explanation for his observations was based on heat conservation (Bergmann, 1847). He argued that homoeothermic animals living in relatively cold environments would profit from a relatively smaller surface area-to-volume ratio in order to radiate less of their body heat. How- ever, McNab (1971) pointed out that larger individuals have a larger surface and lose more heat in absolute terms. In a resource-limited environment, being large is therefore not necessarily ad- vantageous. More recent evidence shows that animals living in hot environments can be limited by the speed at which they can dissipate their body heat and higher area-to-volume ratios allow them to maintain higher activity levels without overheating (Speakman & Król, 2010). According to this theory, Bergmann’s rule could be the result of selection for small size in hot environments. Alternatively, Bergmann’s rule may not be directly temperature driven. For example, larger indi- viduals could be more starvation tolerant during cold seasons with low food availability (Lindstedt & Boyce, 1985; Goodman et al., 2012). The role of temperature in driving patterns of body size is not clear (but see van Gils et al., 2016). Given the importance of body size for the organisation of biological systems (Calder, 1983; Werner & Gilliam, 1984) climate-change induced selection on body size could have important effects on community dynamics. If temperature is a direct driver of body size, we would expect 3 temperature-dependent selection on body size to be common. In a recent comprehensive review, Teplitsky & Millien (2014) concluded that there is no direct evidence that decreases in body size in birds and mammals are an evolutionarily adaptive response to climate change. However, most studies they reviewed simply examined trends in body mass. Once a trend is found, it can only either be consistent with warming (i.e. the animals became lighter) or not (the animals became heavier). Trends by themselves can therefore not provide a strong test of the hypothesis. Studies that examined adaptive responses of body size to climate warming either found no evidence for selection on body size or no genetic basis for the observed size trends (Teplitsky et al., 2008; Ozgul et al., 2009; Husby et al., 2011; Gardner et al., 2017). However, among migratory birds in North America, the observed trends in body size were apparently driven by selection on body size during the winter (Van Buskirk et al., 2010). If climate warming causes evolutionary changes in body size, we predict that: 1. the observed trends should be due to smaller individuals replacing larger individuals, rather than shrinking individuals, and that 2. there should be direct temperature mediated selection on an important fitness component, i.e. large individuals have a higher fitness under cold temperatures and small individuals have higher fitness under hot temperatures. Using body mass as a measure of size, we tested these predictions in a population of mountain wagtails (previously long-tailed wagtail, Motacilla clara) living along a river in KwaZulu Natal, South Africa. Between 1976 and 1999, average body mass in this population has decreased and temperature has increased. We show that the mass trend is due to lighter individuals replacing heavier ones. We further show that the effect of temperature on survival depends on body mass with lighter individuals surviving relatively better under hot conditions and heavier individuals surviving relatively better under cold conditions. Our results therefore confirm our predictions and are consistent with climate change being the driver of the observed mass changes in this population. 4 Methods Data collection The mountain wagtail (Motacilla clara) is a non-migratory passerine bird with a wide distribution across sub-Saharan Africa, including the east and south coast of South Africa. Mountain wagtails inhabit areas with small fast-flowing rivers in a largely arboreal environment. The birds hold life-long territories, which they rarely leave (Piper, 1990). We studied mountain wagtails along a 7 km stretch of the Palmiet River, Westville, KwaZulu- Natal (29◦490S30◦550E) in South Africa. From 1976 to 1999, we captured individuals with mist nets and ringed them with a numbered 3 mm steel ring and a unique combination of three or four color-rings (issued by SAFRING: South African Bird Ringing Unit, Animal Demography Unit, University of Cape Town). Body mass was measured to the nearest 0.1 g on a spring balance. This study used data on territorial adults. The sexes are morphologically similar and we were not able to distinguish them in these analyses. Each territory was systematically searched for surviving adults on a quarterly basis where the first quarter started in August (Q1: Aug-Oct (southern hemisphere spring), Q2: Nov-Jan (summer), Q3: Feb-Apr (autumn), Q4: May-Jul (winter)). The onset of breeding falls in the second half of August and generally runs through to about mid December. In our study, we therefore consider the Wagtail year to extend from August until July, starting at the beginning of the southern hemisphere spring. Only territorial birds breed and they tend to use the same nest sites every year. They lay between one and four eggs, but on average 1.55 fledglings were produced per pair per annum. Individuals were either recaptured or identified by reading their color rings (Piper, 2002). We obtained mean quarterly temperature and total rainfall (another important environmental driver in South Africa) from a weather station in Palmiet (29◦49035:900S30◦55039:000E). We also ex- plored minimum and maximum temperatures but they showed similar trends as mean temperature and we did not pursue these further. 5 Statistical analysis Climate We decomposed mean quarterly temperature and rainfall time series into trend and seasonal effects using a state-space model (Durbin & Koopman, 2012) with the following observation equation: 2 yt = xt + γt + et; et ∼ N(0; σe ) and state transition equations: 2 xt = xt−1 + βt + νt; νt ∼ N(0; σν ) 2 βt = βt − 1 + !t;!t ∼ N(0; σ!) t−1 X 2 γt = − γi + t; t ∼ N(0; σ ) i=t−4 Here yt is the observed temperature or rainfall value, xt is the underlying mean, which can change over time in this model, βt the slope or change in mean, and γt the seasonal effect. The last equation formulates an unstructured seasonal effect for four seasons. The et, νt, !t and t are 2 2 error terms (with associated variances σx) that we assumed to be independent. We set σv = 0, to obtain smoother trend estimates. We used R package dlm (Petris, 2010; Petris & Petrone, 2011) to fit these state-space models. The advantage of a state-space modelling approach is mainly that slope and seasonal effects are allowed to change over time (Durbin & Koopman, 2012).
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