Evol Ecol (2013) 27:1033–1044 DOI 10.1007/s10682-012-9615-x ORIGINAL PAPER
Maternal investment during pregnancy in wild meerkats Stuart P. Sharp • Sinead English • Tim H. Clutton-Brock
Received: 4 May 2012 / Accepted: 20 October 2012 / Published online: 31 October 2012 Ó Springer Science+Business Media Dordrecht 2012
Abstract Maternal investment in offspring development is a major determinant of the survival and future reproductive success of both the mother and her young. Mothers might therefore be expected to adjust their investment according to ecological conditions in order to maximise their lifetime fitness. In cooperatively breeding species, where helpers assist breeders with offspring care, the size of the group may also influence maternal investment strategies because the costs of reproduction are shared between breeders and helpers. Here, we use longitudinal records of body mass and life history traits from a wild population of meerkats (Suricata suricatta) to explore the pattern of growth in pregnant females and investigate how the rate of growth varies with characteristics of the litter, environmental conditions, maternal traits and group size. Gestational growth was slight during the first half of pregnancy but was marked and linear from the midpoint of gestation until birth. The rate of gestational growth in the second half of pregnancy increased with litter size, maternal age and body mass, and was higher for litters conceived during the peak of the breeding season when it is hot and wet. Gestational growth rate was lower in larger groups, especially when litter size was small. These results suggest that there are ecological and physiological constraints on gestational growth in meerkats, and that females may also be able to strategically adjust their prenatal investment in offspring according to the likely fitness costs and benefits of a particular breeding attempt. Mothers in larger groups may benefit from reducing their investment because having more helpers might allow them to lower reproductive costs without decreasing breeding success. Keywords Cooperative breeding Foetal growth Gestation Load-lightening Maternal investment Meerkat Electronic supplementary material The online version of this article (doi:10.1007/s10682-012-9615-x) contains supplementary material, which is available to authorized users. S. P. Sharp S. English T. H. Clutton-Brock Department of Zoology, University of Cambridge, Downing Street, Cambridge CB2 3EJ, UK S. P. Sharp (&) Lancaster Environment Centre, Lancaster University, Lancaster LA1 4YQ, UK e-mail:
[email protected]
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Introduction Maternal investment in the development of offspring has a profound impact on the survival and future reproductive success of both the mother and her young (Mousseau and Fox 1998; Roff 2002; Maestripieri and Mateo 2009). It has been shown in a wide range of taxa from invertebrates to humans that the level of investment covaries with the mother’s age (e.g. Berkeley et al. 2004; Plaistow et al. 2007) and condition (e.g. Fairbanks and McGuire 1995; Warner et al. 2007), the quality of her mate (e.g. Wedell 1996; Cunningham and Russell 2000) and the environment that she experiences during various stages of the reproductive cycle (e.g. Kaplan and Phillips 2006; Roseboom et al. 2006). Furthermore, the size and growth of offspring are not only constrained by maternal phenotype and environmental conditions, but mothers may strategically adjust the amount of resources that they allocate to their young in order to maximise their own lifetime fitness (Mousseau and Fox 1998; Marshall and Uller 2007; Maestripieri and Mateo 2009). However, the extent to which mothers are able to make these adjustments according to predictions about the future quality of the environment remains a source of debate in evolutionary and biomedical research (Wells 2007; Gluckman et al. 2008; Monaghan 2008). Cooperatively breeding species, in which parents receive assistance with the care of their offspring from one or more ‘helpers’, are useful model systems for investigating maternal investment strategies (Russell and Lummaa 2009). The number of helpers and their effect on maternal and offspring fitness vary considerably both between and within species (Wilson 1971; Bourke 1999; Solomon and French 1997; Dickinson and Hatchwell 2004; Russell 2004), making group size an important and predictable source of environmental heterogeneity that may influence the extent to which mothers invest in a given reproductive attempt (Russell and Lummaa 2009). Reduced maternal care of offspring in the presence of helpers, or ‘load-lightening’, has been reported in many species and can be associated with an increase in maternal condition, survival or productivity (Wilson 1971; Hatchwell 1999; Heinsohn 2004; Russell 2004). However, the majority of research has focused on birds or insects and, with the exception of work on humans (Sear and Mace 2008; Hrdy 2009; Kramer 2010), there have been relatively few studies of how alloparental care impacts on maternal investment in mammals (Russell 2004). In particular, prenatal investment has rarely been investigated (Russell and Lummaa 2009), despite good evidence from other vertebrates that mothers adjust their allocation of resources to eggs according to the number of helpers in their group (e.g. birds: Russell et al. 2007; fish: Taborsky et al. 2007). Unique among vertebrates, gestation in mammals is an extended period of maternal investment and one of the most energetically costly stages of reproduction for females (Gittleman and Thompson 1988). This generates a strong link between a mother’s condition and her offspring’s size and growth, making gestation a likely time for environmental and social factors to influence maternal investment strategies (Maestripieri and Mateo 2009). The rate of foetal growth provides a useful measure of gestational investment that, across species, correlates with various life history traits (Frazer and Huggett 1974; McKeown et al. 1976; Martin and MacLarnon 1985; Pontier et al. 1993), but most studies of intraspecific variation have measured the length of the gestation period rather than the rate of foetal growth itself. Gestation length has been shown to correlate with maternal age or state (e.g. Silk et al. 1993; Mysterud et al. 2009), environmental conditions (e.g. Byers and Hogg 1995; Boyd 1996) or offspring sex (e.g. Byers and Hogg 1995; Mysterud et al. 2009), but further work is needed to determine how these factors affect foetal growth rate,
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especially in polytocous species where mothers may trade off the per capita investment in foetal development against litter size (Frazer and Huggett 1974; McKeown et al. 1976; Pontier et al. 1993). Moreover, while social effects on gestation length have been described in one cooperatively breeding species (banded mongooses, Mungos mungo: Cant 2000; Hodge et al. 2011), we know of no study that has investigated whether the presence or number of helpers impacts on maternal investment in foetal growth rate. One major impediment to studying foetal growth is the difficulty of obtaining sequential measures of the mass of foetuses. As yet, most estimates of foetal growth rate are either derived from measures of gestation length and birth mass (Frazer and Huggett 1974; Martin and MacLarnon 1985) or are based on samples of mothers culled at different stages of gestation (Trites 1991; Yunker et al. 2005). Very few studies have been able to track the development of individual foetuses (see Hildebrandt et al. 2007 for an exception), but it is sometimes possible to repeatedly weigh individual mothers throughout pregnancy and, thus, to explore the ecological and life history correlates of the rate of increase in maternal mass (Boyd 1985; Urison and Buffenstein 1995; Long and Ebensperger 2010). Although growth of the placentae and other maternal tissues contributes to the gain in mass, the rate of increase is likely to be strongly correlated with foetal growth rate (Boyd 1985). Furthermore, placental development is an important but often overlooked component of a mother’s energetic investment during pregnancy (Gittleman and Thompson 1988). Investigating the combined gestational growth of maternal and foetal tissues therefore provides important insights into maternal investment, but existing studies of cooperatively breeding species are entirely restricted to captive or domesticated populations and have not directly investigated the influence of group size (Urison and Buffenstein 1995; Long and Ebensperger 2010). Here, we investigate gestational growth in a wild population of Kalahari meerkats (Suricata suricatta, Desmarest). Meerkats are cooperatively breeding mongooses that live in cohesive social groups of up to 50 individuals. Within these groups, reproduction is monopolised by a single female who is behaviourally dominant to all other female group members (Doolan and Macdonald 1997; Griffin et al. 2003; Clutton-Brock et al. 2008). Vacant dominant positions are filled by the oldest subordinate in the group or, where there is no age difference among the oldest females present, by the heaviest (Hodge et al. 2008). The dominant female produces one to four litters per year, each consisting of up to seven pups which are raised by all members of the group (Clutton-Brock et al. 2001, 2004; Hodge et al. 2008). Maternal age and body mass are important determinants of both investment in postnatal care and breeding success in dominant females (Russell et al. 2003; Hodge et al. 2008; Sharp and Clutton-Brock 2010), and the postnatal growth rate and survival of pups are higher in larger groups (Russell et al. 2002; Hodge et al. 2008; but see Sharp and Clutton-Brock 2010) despite reduced contributions to offspring care by dominant females (Clutton-Brock et al. 2004). However, the influence of maternal characteristics and group size on maternal investment during gestation has never been investigated. In this study, we use longitudinal records of body mass and life history to: (1) describe the pattern of gestational growth in dominant females; (2) measure the rate of gestational growth during the linear growth phase; and (3) investigate how gestational growth rate varies with characteristics of the litter, environmental conditions, maternal traits and group size. In particular, we test the prediction that growth rates are lower in larger groups because mothers are able to reduce their prenatal investment when they are likely to have more helpers providing postnatal care to compensate for this.
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Materials and methods Study population and data collection A wild population of meerkats (S. suricatta) has been closely monitored at the Kuruman River Reserve in the South African Kalahari (26°580 S, 21°490 E) since January 1994. The present study used data collected up to November 2007, during which time more than 1,500 individuals in 35 social groups were habituated to observation from \2 m. All individuals were marked with subcutaneous transponder chips and could be identified in the field by unique dye marks applied to their fur. Groups were visited approximately once every 3 days to record all key life history events including changes in dominance or pregnancy status. More than 95 % of individuals were trained to climb onto an electronic balance and could be weighed (in g) most mornings before they went foraging. Dominance status was determined from established behavioural assays, and pregnancy could be identified by swelling of the abdomen and increases in body mass (Clutton-Brock et al. 1998; Hodge et al. 2008). Pregnancy in meerkats lasts around 70 days (Doolan and Macdonald 1997) and is usually first detected around the midpoint of this period. Litter mass prior to parturition typically comprises ca. 20 % of female body mass (Doolan and Macdonald 1997), so although pups are born in an underground burrow and remain there for around 3 weeks, birth dates could be established reliably from the sudden loss of body mass and abdomen distention in the mother (Clutton-Brock et al. 1998; Hodge et al. 2008). Conception dates were then estimated by backdating 70 days from birth, as behavioural signs of oestrus were rarely observed. The pattern of gestational growth In order to determine the pattern of growth throughout the gestation period, we plotted maternal body mass against time using data from all those pregnancies during which the mother was the dominant female in her group and had been weighed at least ten times between the estimated conception date (day 1) and the day before birth (day 70; n = 247 litters, 41 mothers, constituting over 70 % of all litters born to dominant females during the study period). Preliminary inspection of the data provided unequivocal evidence that the interbirth interval, and thus the gestation period, was \70 days in a small number of cases (\10 %). We therefore excluded measures of body mass taken in the first few days of the estimated gestation period if the female was pregnant with her previous litter. Calculation of gestational growth rate Preliminary examination of the data indicated that gestational growth was slight during the first half of pregnancy but marked and linear thereafter, and that litter size was the most important determinant of growth rate. We therefore calculated gestational growth rate (in g per day) for each pregnancy where litter size was known (see below) by obtaining the slope from a linear regression of maternal body mass against time from day 35 to day 70 of the gestation period. Analyses were restricted to those pregnancies for which the mother had been weighed at least ten times during this period (n = 137 pregnancies, 29 mothers). Litter size could only be determined once pups had emerged from their natal burrow, but previous ultrasound analyses have shown that few pups are lost between pregnancy and emergence unless the entire litter is killed: of those pups born to dominant mothers, 85 %
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survived to emergence and, in the few litters (17 %) where some but not all pups were lost prior to emergence, the mean number of pups per litter that died was 0.6 (Russell et al. 2003; AF Russell unpublished data). Litter size at emergence was therefore considered to be a reliable measure of litter size at birth. Factors associated with gestational growth rate Gestational growth rate was approximately normally distributed and therefore fitted as the response variable in a series of linear mixed effect models in order to investigate correlations with characteristics of the litter (litter size and litter sex ratio), environmental conditions (season), maternal traits (maternal age and initial body mass) and group size. Litter size was measured at emergence from the natal burrow as described above. Similarly, litter sex ratio was calculated for emerged pups only and measured as the number of males divided by the total number of pups in the litter. In 23 of the litters, one or two pups died before they could be sexed; to avoid having to exclude these litters from the analyses, we calculated litter sex ratio for the sexed pups only as this was unlikely to bias the analyses. The season during which the litter was conceived was fitted in the models in order to account for environmental variation, as seasonality is thought to have a major influence on other aspects of growth in meerkats (Russell et al. 2002; English et al. 2012). The season was either the hot and wet ‘high’ season (October to April) or the cold and dry ‘low’ season (May to September; Doolan and Macdonald 1997; Russell et al. 2002). Most litters are conceived during the high season when food availability and long-term growth rates are relatively high (Doolan and Macdonald 1997; English et al. 2012). Maternal age was measured (in days) at the birth of the litter, and initial body mass was the mean maternal mass (in g) in the week after conception. Group size was calculated as the mean daily group size (excluding pups) in the week prior to conception. Finally, the identity of the mother and the cohort (the calendar year at conception) were fitted as random terms in the models to account for the non-independence of multiple litters from the same mother and interannual variation in seasonal conditions, respectively. Prior to analysis, we centred and standardised all variables (except season) to facilitate the direct comparison of parameter estimates and the appropriate interpretation of main effects involved in interactions (Schielzeth 2010). Colinearity between all explanatory variables was assessed by calculating correlations and variance inflation factors (VIFs), following Zuur et al. (2009). All variables were included in the analysis because pairwise correlations between them were weak (r \ 0.4 in all cases) and VIFs were small (\2 in all cases). We then used an information theoretical approach for model selection and parameter estimation (Burnham and Anderson 2002). Preliminary analyses suggested that the interaction between litter size and group size was the only one of all possible first-order interactions that was likely to explain variation in gestational growth rate. This interaction, together with the six explanatory variables described above, produced a set of 48 candidate models excluding those that did not contain litter size and those that contain the interaction but not the constituent main effects (see Supplementary Table S1); litter size was fitted in all models because it is likely to be the most significant determinant of gestational growth rate. All candidate models were fitted using the package ‘lme4’ (Bates et al. 2011) in the R environment, version 2.13.0 (R Development Core Team 2011). We then compared these models using AICc (the second order Akaike Information Criterion), and averaged the 95 % confidence set of models (Burnham and Anderson 2002) in the package MuMIn (Barton´ 2011). We validated these models by plotting the distribution of the residuals,
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the residuals versus the fitted values and the residuals versus each of the covariates (Zuur et al. 2009).
Results The pattern of gestational growth Gestational growth was found to be negligible during the first half of pregnancy but marked and approximately linear from the midpoint of gestation until birth (Fig. 1). Examining the data for each pregnancy separately showed that this overall pattern was consistent, but that the rate of linear growth varied between pregnancies, even for litters of the same size (Fig. 2). Factors associated with gestational growth rate
900 800 700 500
600
Maternal body mass (g)
1100
Gestational growth rate was most strongly correlated with litter size and season (Table 1; Table S1). The rate of growth increased with litter size (Fig. 3; Table 1) and was higher for litters conceived during the high season (Table 1). Although litter sex ratio appeared in the 95 % confidence set of models, the effect size was negligible and unlikely to be biologically meaningful (Table 1). Both the age and initial body mass of the mother were positively correlated with gestational growth rate, but there was a strong negative correlation between the rate of growth and group size (Fig. 3; Table 1); an interaction between litter size and group size revealed that this effect was stronger in smaller litters (Fig. 3; Table 1).
0
10
20
30
40
50
60
70
Day of gestation Fig. 1 The pattern of gestational growth during pregnancy. The boxes show the medians, first and third quartiles and the whiskers show the ranges for all data from 247 pregnancies
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1100 1000 900 800 700
Maternal body mass (g)
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35
40
45
50
55
60
65
70
Day of gestation Fig. 2 The pattern of gestational growth during the second half of pregnancy. The scatter plot shows the raw data for three examples of pregnancies in different dominant females with a litter size of four (the median litter size across all litters) Table 1 The results of linear mixed effect models of the factors associated with gestational growth rate during the second half of pregnancy Fixed effect
Estimate
Unconditional standard error
Relative importance
Intercept
5.26
0.18
Litter size
0.89
0.12
1.00
Litter sex ratio
-0.05
0.11
0.23
Season (low relative to high)
-0.87
0.28
1.00
Maternal age
0.18
0.14
0.39
Initial body mass
0.17
0.13
0.41
Group size
-0.20
0.14
0.62
Litter size 9 group size
0.16
0.11
0.29
Random effect
Variance
Mother ID
0.06
Cohort
0.07
Residual
1.70
For details of the full set of models, see Supplementary Table S1 Details of the fixed effects were obtained by averaging the 95 % confidence set of models. Details of the random effects were obtained from the best-fitting model
Discussion The pattern of gestational growth in wild dominant female meerkats was broadly similar to that reported in captive studies of two social rodent species (naked mole-rats,
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10
8 6 4 2 0
Gestational growth rate (g per day)
12
1040
1
2
3
4
5
6
Litter size Fig. 3 Gestational growth rate during the second half of pregnancy for litters of different sizes and in groups of different sizes. The solid line shows the relationship predicted by the averaged model for a mother of mean age (1,724 days) and initial body mass (768.6 g) in a group of mean size (18) during the high season (when most pregnancies occur). The broken lines show the same relationship but for females in groups of size one standard deviation larger (dotted line) and smaller (dashed line) than the mean. The boxes show the medians, first and third quartiles and the whiskers show the ranges of the partial residuals for the main effect of litter size
Heterocephalus glaber: Urison and Buffenstein 1995; degus, Octodon degus: Long and Ebensperger 2010), with negligible or slow growth until approximately half way through the gestation period and marked linear growth thereafter. In contrast, a study of wild rabbits (Oryctolagus cuniculus) found that growth rate was approximately constant and linear throughout gestation (Boyd 1985). Gestational growth combines development of the foetuses, placentae, uterus and mammary tissue in addition to nutrient storage by the mother (Boyd 1985; Gittleman and Thompson 1988), and the relative investment in each of these is likely to differ between species (Gittleman and Thompson 1988). In smaller mammals, for example, mothers typically deposit proportionally less fat (Gittleman and Thompson 1988), and this may be especially true of species such as meerkats and degus that live in arid environments. Furthermore, the costs of lactation in both of these species are often shared between the mother and one or more allolactators (Scantlebury et al. 2002; Ebensperger et al. 2006), and mothers may therefore investment less in the development of mammary tissue or fat deposition. In either case, increases in maternal mass would be relatively small until the onset of significant foetal growth, which in many species occurs a considerable time after conception (McKeown et al. 1976; Trites 1991; Yunker et al. 2005). The rate of gestational growth during the second half of pregnancy increased significantly with litter size. This is to be expected in all polytocous mammals given that foetal growth typically accounts for the majority of maternal weight gain in pregnancy (Boyd 1985; Michener 1989). Interestingly, however, there was no clear evidence of a reduction in the per capita growth rate of foetuses in larger litters, and it may be that trade offs between pup quality and quantity are difficult to detect without measuring the body mass of
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individual foetuses or pups at birth. Alternatively, the potential for such a trade off may be complicated by the influence of group size on maternal investment. As predicted, the rate of gestational growth was lower in larger groups, and this supports the hypothesis that mothers are able to strategically adjust their level of prenatal investment according to the amount of assistance they are likely to receive with raising their young (Russell and Lummaa 2009). If postnatal offspring care by helpers compensates for reductions in maternal investment during gestation, then mothers may benefit from lowering reproductive costs without decreasing offspring fitness. Similar examples of prenatal ‘loadlightening’ have been found in birds (Russell et al. 2007) and fish (Taborsky et al. 2007), but we know of no mammalian studies. In meerkats, pup growth rates and survival are higher in larger groups (Russell et al. 2002; Hodge et al. 2008; but see Sharp and CluttonBrock 2010) despite reduced contributions to offspring care by dominant females (CluttonBrock et al. 2004). Further work is now needed to determine how variation in maternal investment during and after gestation impacts on the survival and reproductive success of dominant females in groups of different sizes. This would help to elucidate whether reduced investment by females with more helpers is a strategic adjustment or instead the result of constraints imposed by living in larger groups. For example, competition for food may increase with group size, or maintaining dominance may be more costly when the number of subordinate females in the group is higher (Clutton-Brock et al. 2008). The relationship between gestational growth rate and group size was weaker in larger litters. This may be because there are greater constraints on maternal investment when litter size is large. For example, if mothers reduce the per capita growth rate of foetuses in larger litters, as has been shown in other mammals (McKeown et al. 1976; Michener 1989), then further reductions according to group size may not be possible without compromising offspring fitness. Even if such trade offs do not occur, then mothers may be more likely to maximise investment in larger litters in order to offset the increased level of sibling competition. Arguably, the interaction between litter size and group size is more indicative of strategic investment than of investment constrained by competition within groups, as it is difficult to imagine why the effects of the latter would be more apparent when litter size was smaller. It is important to note that litter size was measured at emergence rather than at birth, and it is possible that the effects reported for litter size and its interaction with group size are misleading. However, very few pups die between birth and emergence unless the entire litter is killed (Russell et al. 2003; see also the ‘‘Materials and methods’’), so fitting litter size at birth to the models would be very unlikely to change the results presented here beyond minor differences in effect sizes. Similarly, the lack of any meaningful effect of litter sex ratio at emergence does not necessarily mean that the sex ratio in utero has no influence on foetal growth, but sex differences are more likely to occur in those species with a stronger degree of sexual size dimorphism or sex-biased variance in reproductive success than meerkats (Trites 1991; Byers and Hogg 1995; Mysterud et al. 2009). The season during which conception occurred was an important predictor of gestational growth rate. The rate of growth was higher between October and April, when temperature and rainfall are also higher, than between May and September, and similar relationships have been found between seasonality and other aspects of growth in meerkats (Russell et al. 2002; English et al. 2012). Several studies of other species have reported seasonal differences in gestation length or foetal growth rates (Byers and Hogg 1995; Boyd 1996; Yunker et al. 2005), and these differences may be particularly marked in arid environments, where even sporadic periods of rainfall can dramatically increase food availability and thus intake rate and growth (English et al. 2012). Further analysis of the relationship
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between gestational growth and rainfall at different stages of the reproductive cycle is needed to investigate whether mothers are able to adjust their prenatal investment according to the amount of food that is likely to be available during the postnatal period of offspring care. Similarly, the positive correlations between gestational growth rate and both maternal age and initial body mass support the findings from studies of other mammals, including humans, that a mother’s condition influences her prenatal investment (Michener 1989; Trites 1991; Silk et al. 1993; Scholl et al. 1997), but the extent to which these relationships result from condition-dependent constraints or strategic investment remains unclear (Monaghan 2008). In conclusion, the rate of gestational growth in dominant female meerkats varies according to characteristics of the litter, season, maternal traits and group size. These results suggest that there are ecological and physiological constraints on gestational growth, but also provide the first evidence from mammals that mothers may be able to strategically adjust their prenatal investment in offspring development according to environmental and social conditions. The idea that mothers are able to foresee what these conditions will be like during the lifetime of the offspring remains contentious (Wells 2007; Gluckman et al. 2008; Monaghan 2008) but, in cooperative breeders, the number of helpers in the group is one source of environmental heterogeneity that mothers may be able to reliably predict (Russell and Lummaa 2009). Regardless of the mechanism underlying variation in gestational growth rate, the results presented here indicate that differential investment during pregnancy may be an important but overlooked component of mammalian life history evolution. Acknowledgments We thank the Kotze family and Northern Cape Conservation for allowing us to conduct research in the Kalahari; the Mammal Research Institute at the University of Pretoria and Penny Roth for logistical support; and Marta Manser for her role in maintaining the Kalahari Meerkat Project. We are also extremely grateful to the many volunteers, field staff, postgraduate students and postdoctorates who assisted with data collection and to Shinichi Nakagawa and Andrew Bateman for statistical advice. Two anonymous reviewers provided feedback that greatly improved the paper. The Biotechnology and Biological Sciences Research Council, the Isaac Newton Trust, the Leverhulme Trust, the University of Cambridge, the Swiss National Science Foundation and the Earthwatch Institute provided financial support.
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