Empirical test on the relative climatic sensitivity between individuals of narrowly and broadly distributed species Iara Lacher,1,3,† and Mark W. Schwartz1,2 1Department 2John
of Environmental Science and Policy, University of California, Davis, Davis, California 95616 USA Muir Institute of the Environment, University of California, Davis, Davis, California 95616 USA
Citation: Lacher, I., and M. W. Schwartz. 2016. Empirical test on the relative climatic sensitivity between individuals of narrowly and broadly distributed species. Ecosphere 7(3):e01227. 10.1002/ecs2.1227
Abstract. Climate change is already influencing global ecology, exacerbating human-induced biodiver-
sity loss with potentially devastating results. A first step to addressing climate change impacts on conservation is to better understand how and to what extent species will be affected. Species with smaller geographic distributions are commonly perceived to be at highest risk of extinction. However, estimates of species vulnerability are frequently based on simplifying assumptions regarding climatic tolerance, usually arrived at through the use of models that associate mean spatial or temporal climate values with species distributions. Model estimated climatic tolerances may be improved by incorporating either finer spatial or temporal resolutions and/or additional distribution-limiting factors like dispersal, habitat connectivity, and species interactions. However, the underlying assumption that species-level climatic reflect individual tolerances can skew vulnerability estimates toward over-or underestimation. We use empirically derived fitness reaction norms of biomass and seed pod count to estimate the relative sensitivity of individuals of broadly distributed (BD) and narrowly distributed (ND) species across temperature and water gradients. Temperature and water treatments were based on local climate station data and IPCC projections of climatic change. On the basis of fitness reaction norms, we infer relative vulnerability to examine the assumption that ND species are relatively more vulnerable to climatic change than BD species. Study species included the BD Mimulus guttatus and Clarkia purpurea and the ND Mimulus nudatus and Clarkia gracilis ssp. tracyi. Compared to M. nudatus (ND), individuals of M. guttatus (BD) exhibited biomass responses that were significantly more sensitive to temperature and seed pod count responses that were significantly more sensitive to water and temperature. Conversely, compared to C. purpurea (BD), C. gracilis ssp. tracyi (ND) individuals exhibited biomass and seed pod count responses that were significantly more sensitive to temperature. In addition, we measured unexpected positive responses from both Clarkia species to increases in temperature. Our results support the idea that, when examined at a local scale, the size of a species’ geographic distribution does not necessarily correlate to climate change vulnerability. Key words: Clarkia gracilis ssp. tracyi; Clarkia purpurea; climate change; Mimulus guttatus; Mimulus nudatus; range size; sensitivity; species distribution models; vulnerability. Received 17 June 2015; revised 16 August 2015; accepted 18 August 2015. Corresponding Editor: D. P. C. Peters. Copyright: © 2016 Lacher et al. This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. 3 Present address: Smithsonian Conservation Biology Institute, 1500 Remount Rd, Front Royal, Virginia 22630 USA. † E-mail:
[email protected]
Introduction
et al. 2008, Dawson et al. 2011), making research on climate change impacts a top priority in biodiversity conservation (Sutherland et al. 2009). To effectively protect global biodiversity, resource managers must prioritize species according to their relative extinction risk as well as
Climate change is expected to have large negative impacts on biodiversity (Purvis et al. 2000, Jones et al. 2003, Parmesan and Yohe 2003, Thomas et al. 2004, Schwartz et al. 2006, Loarie v www.esajournals.org
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the feasibility and expected success of management actions. Therefore, identifying species that are most vulnerable to the negative influences of climate change is of primary concern (Oliver et al. 2012). Several studies estimate that narrowly distributed (ND) species are generally more vulnerable to climatic change than broadly distributed (BD) species (Thuiller et al. 2005, Broennimann et al. 2006, Ohlemüller et al. 2008, Ledig et al. 2010, Slatyer et al. 2013) because it is often untenable to assume that they can adapt or migrate in pace with the expected degree and velocity of climate change (Thuiller et al. 2005, Loarie et al. 2009). If ND species are, in fact, more vulnerable to climate change than BD species, the outcome for global biodiversity is unfavorable (e.g., Thomas et al. 2004), especially given that the majority of species have narrow geographic distributions (Gaston 1996). If, however, ND species are less vulnerable than estimated, skewed prioritizations may divert resources away from where they are actually needed (Loiselle et al. 2003, Bottrill et al. 2008, Lawler 2009, Atkins and Travis 2010, Schwartz 2012). Species distribution models (SDMs) have gained traction as a tool for estimating species vulnerability to climate change (Anderson 2013, Frances et al. 2015), but they are not without their limitations. Assumptions guiding how SDMs estimate climatic tolerance can result in projections that over or under estimate climatic tolerance and thus vulnerability to climate change. In their most basic form, SDMs assume that species are at equilibrium with their environments (Elith and Leathwick 2009) and associate species occurrences with climatic attributes such as temperature and precipitation to define a range of climatic conditions within which the species can tolerate (Wiens et al. 2009, Nicotra et al. 2010). As broader geographic distributions are statistically more likely to encompass a broader range of climatic conditions than narrower geographic distributions (Birand et al. 2012), SDMs frequently assign broader climatic tolerances and lower relative vulnerability for BD species relative to ND species. As this pattern is an artifact of the size of the geographic distribution, and additional factors aside from climate limit species’ distributions (e.g., dispersal, habitat connectivity, and species interactions), modeled estimates v www.esajournals.org
of climatic tolerance can underestimate the full range of climatic conditions a species can tolerate, or its fundamental niche (Nicotra et al. 2010). In addition, SDMs use climate values averaged across space and time, potentially further under- estimating the range of climatic conditions within which a species can tolerate. Local inter- annual variation in climate may be large or small relative to the climatic variation represented across the entire geographic distribution of the species. Considering this temporal variation can alter perceived estimates of climatic tolerance at different degrees for BD and ND species. Finally, and itself fundamental to the above assumptions, is the common assumption that the broad range of climatic conditions represented by a species- level geographic distributions captures variation in climatic tolerance inherent between its populations. Geographic distributions are not homogenous across a landscape, resulting in the potential for individuals within species’ populations to adapt to local climatic conditions. For BD species especially, this can result in overall climatic tolerances of populations that are much narrower and much more variable than that represented by the species’ geographic distribution as a whole (Atkins and Travis 2010, Kelly et al. 2012, Schiffers et al. 2013), making these populations relatively more vulnerable to climatic change than would be estimated otherwise. Individuals within single locations may fall along a spectrum of local adaptation and tight linkage to median climatic conditions such that individuals of a ND species may be less, more, or equally responsive to climate as a closely related individual of a BD species. Thus, even if we assume the range of climatic conditions represented by recorded occurrences captures a species’ fundamental niche, we may still overlook the role that individuals within species populations have on the vulnerability of the species as a whole. Understanding the relative capacity of individuals from ND and BD species’ populations to differ in response across climatic conditions is a crucial step in interpreting species vulnerabilities using SDMs. Here, we infer relative vulnerability of individuals from populations of spatially adjacent congeneric BD and ND Mimulus and Clarkia through fitness reaction norms across temperature and water gradients. Higher relative climatic sensitivity, and lower relative tolerance, is signaled 2
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Fig. 1. Focal species occurrences (gray points) and the location of the McLaughlin Natural Reserve (white points at center of distribution). Mimulus guttatus (a); M. nudatus (b); Clarkia purpurea (c); and Clarkia gracilis ssp. tracyi (d) (Calflora 2010).
Methods Research site and species
The 2808 ha McLaughlin Natural Reserve is a part of the University of California Reserve System and rests between 366 and 914 m in the California coast range. McLaughlin has a Mediterranean climate, characterized by cool, wet winters and hot, dry summers. Average temperatures range between 8 °C and 25 °C and average annual precipitation is 750 mm. For many plants the climate at McLaughlin translates into a winter growing season that begins as early as the first winter rains. We estimated total growing season precipitation from October through September. Our field observations suggested February as a typical month when the plants begin to grow, and so we used temperature and precipitation profiles v www.esajournals.org
(b) 180°W 160°W 140°W 120°W
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by greater proportional change in fitness across environmental gradients toward environments of relatively more stress (Simms 2001, Dawson et al. 2011, sensu Cleland et al. 2013). This research fills the need for empirical research on the relationship between geographic distributions and climatic tolerance (Slatyer et al. 2013, Grossenbacher et al. 2014). In addition, unlike related studies (Hughes et al. 2001, Wu et al. 2010, Sheth and Angert 2014), we employ three aspects of experimental design that increase our ability to relate our findings to the natural world. First, we evaluate sensitivity based on the entire natural life-span of individuals within each species. Second, we base temperature and water treatments off of local meteorological data to mimic natural climatic trends across the growing season. Finally, we incorporate future climatic conditions from future climate projections (Intergovernmental Panel on Climate Change 2007). We measure fitness using end of life total biomass and seedpod count. We use these fitness measures to test the null hypothesis of no differences in responsiveness of individuals to climate against the two tailed alternative hypothesis where individuals of either species, in each pair, might be more responsive to climate than the other. We then use these results to infer what this implies about climate change vulnerability of ND and BD species more generally.
from February through August for our treatments. Our focal species were Mimulus guttatus (BD), M. nudatus (ND), Clarkia purpurea (BD), and C. gracilis ssp. tracyi (ND) (Fig. 1). We used annual plants due to short life histories that simplified both the measurement and interpretation of lifetime fitness measures. Annual life histories can also contribute to high intra- and inter- generational responsiveness to environmental variation (Salguero-Gómez et al. 2012, Cleland et al. 2013). We first selected ND species that were classified as either rare or uncommon in the Jepson Manual or listed as rare by the California Native Plant Society. Following Bevill and Louda 3
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(1999), we then paired these ND species with BD species that grow in close geographic proximity, have close phylogenetic relationships, and similar ecological traits. At McLaughlin, these species are found in low density chaparral or grasslands at elevations between 600 and 700 m. Mimulus guttatus (BD) and M. nudatus (ND) (Phrymaceae) can grow intermixed (personal observation) and have similar life histories, but differ in size and are more typically found in different micro-habitat types. Mimulus nudatus is much smaller in stature than M. guttatus. Mimulus guttatus shows a strong preference for wet soils (Hughes et al. 2001), even germinating and growing while still underwater (personal observation). Mimulus nudatus is frequently found on rocky serpentine seeps with very shallow to little soil. M. nudatus is a strict serpentine endemic, while M. guttatus is considered a soil generalist (Safford et al. 2005). However, at McLaughlin, Mimulus guttatus populations may be locally adapted to serpentine soil (Palm et al. 2012, and personal observation). Finally, the two species are reproductively isolated (Gardner and Macnair 2000) ensuring lack of hybridization. Clarkia purpurea (BD) and C. gracilis ssp. tracyi (ND) (Onagraceae) share similar life histories, habitats, and occasionally grow intermixed (personal observation). C. purpurea and C. gracilis are morphologically similar. Both C. purpurea and C. gracilis ssp. tracyi tend to grow in open grassland habitats alongside other native and non- native forbs and grasses. C. gracilis ssp. tracyi is considered to have an affinity to serpentine, while C. purpurea is considered a soil generalist (Safford et al. 2005). We collected seed for each of the four focal species from around one location (“research hill” at the McLaughlin Natural Reserve in the summers of 2009–2011), to minimize differences in soil and microclimate effects among species Mimulus seed was collected from individuals growing in serpentine or partially serpentine seeps and Clarkia seed from individuals in deeper, less serpentinitic soils. We collected approximately 50 seed pods from several individual plants per species across one site at McLaughlin where all four focal species occur in close proximity to each other. We took care not to remove more than 10% of total estimated seed per population. We also collected voucher specimens for each species. In addition v www.esajournals.org
to seed and plant material, we collected serpentine soil from an existing road cut at the reserve to avoid disturbing intact habitat. We germinated seeds collected from the field under identical conditions in greenhouses to reduce maternal effects of the environment on seeds used in the experiment and to amplify the number of available seed. Although both Mimulus species can self-pollinate, all species were hand-pollinated with paint brushes weekly during the seed magnification regardless of selfing ability and for both Clarkia species during the experiment. We germinated seed from all four species in shallow trays filled with peat and transferred seedlings into pots filled with a peat and sand mixture to grow and collect first generation greenhouse seed. Seeds from these plants were then germinated in the same peat mixture for use in the experiment. We selected a common soil for use in the experimental treatments based on described soil affinities of the species, field observations, and collection sites. We transplanted approximately 20 first generation individuals from each Mimulus species into 2 inch pots filled with a 50% serpentine/sand mixture and 20 individuals from each Clarkia species into 4 inch pots filled with a mixture composed of peat, sand, and perlite. We found that these soil mixtures reproduced plants of appropriate size and reproductive ability comparable to those in the field.
Temperature and water treatment development
We derived temperature and water treatments from temperature and precipitation data collected at the Knoxville Creek meteorological station, located approximately 550 m from the collection site (Western Regional Climate Center) and IPCC SRES scenarios A1B and B1 (Intergovernmental Panel on Climate Change 2007) and Global Circulation Models for the year 2080 (Table A1). We developed baseline temperature and water treatments from temperature and precipitation values collected from the Knoxville Creek meteorological station averaged across years 2000 to 2010. We based temperature treatments off of diurnal daily values at 2 week intervals and water treatments off of average monthly precipitation totals. The baseline temperature treatment follows temperature trends based off of daily values averaged across years. The baseline water treatment
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follows the rate of decline in mean monthly precipitation totals across years, under the assumption that precipitation amount reflects soil moisture. In addition to the baseline temperature treatment, we developed two additional, warmer treatments. These include a 1.4 °C rise in temperature, and a 3.8 °C rise in temperature (Table A2). These values were based on minimum and maximum temperature projections from a suite of 16 models for the year 2080 at McLaughlin (Maurer et al. 2007). As we based treatments on averages, temperature treatments are cooler than the hottest days, yet warmer than the coolest nights. However, temperature treatments also had values higher than the median maximum or lower than the minimum temperatures experienced by our focal species at McLaughlin in February through August of 2000–2010. In addition to the baseline water treatment, we developed three additional treatment representing 15%, 25%, and 50% drier conditions from the baseline and three additional treatments representing 15%, 25%, and 50% wetter conditions from the baseline (Tables A3 and A4). Minimum and maximum water treatments were based on the highest predicted departure in precipitation for the year 2080, from the same suite of 16 models used in developing the temperature treatments (Maurer et al. 2007). As is the case with the baseline water treatment, the six additional higher and lower water treatments decline in water amount as the experiment progresses (Tables A3 and A4). Natural variation in total precipitation during the years 2000–2010 exceeds both the 50% higher and lower watering treatments, suggesting water treatments were conservative. As precipitation at McLaughlin is heaviest early in the growing season, we assumed that the amount of water required to meet field capacity of potted soil represented early-season precipitation, or “peak water” (Tables A3 and A4). To find field capacity, we filled ten pots with soil and calculated the mean water volume that remained in the soil after 10 min of drainage. Due to differing pot sizes, this amount was 45 mL for Mimulus species and 250 mL for Clarkia species. To find water amounts in mL across the entire treatment, we calculated percent change in rainfall as the season progressed and multiplied this percentage by the mL of water needed to meet v www.esajournals.org
field capacity. We then applied this arithmetic across the remaining six treatments (Tables A3 and A4). As the amount of water exceeds field capacity in three water treatments and falls below in three others, treatments subject individuals to differing degrees of moisture stress at different periods in the growth cycle.
Growth chamber experiments
To ensure we had enough seedlings of comparable age and size, we germinated first generation seeds of all four focal species in trays of peat set in water in individual chambers of appropriate temperature. At 2 weeks, we planted randomly selected, similarly sized seedlings of Mimulus species into containers (3.8 cm diameter, 21 cm depth, and 164 mL volume) filled with a 50% serpentine/sand mixture and Clarkia species into containers (6.4 cm diameter, 25.4 cm depth, and 656 mL volume) filled with a mixture composed of peat, sand, and perlite. All temperature and water treatments were applied within Conviron growth chambers (model PGR15) located at the UC Davis controlled environment facility. Our experimental design consisted of three growth chambers each set to one of the three temperature treatments within which water treatments were manipulated by hand. In each chamber and for each of the seven water treatments, we placed ten replicates of each Clarkia species (n = 70) and fourteen replicates of each Mimulus species (n = 98). This resulted in a total of 210 individuals for each Clarkia species and 294 individuals for each Mimulus species. We increased day and night temperatures within each chamber at 2 week intervals to reflect diurnal cycles throughout the growing season for our focal species (S2). We rotated plants within and between chambers several times during the experiment to reduce potential chamber effects. We used pipettes with an accuracy of ±0.1 mL to water individuals three times a week according to values calculated in each of the seven treatments. In addition to temperature and water, we controlled for relative humidity and daylight hours using data from the Knoxville Meteorological Station as a guide. Furthermore, we applied a nutrient-enriched solution with an N-P-K ratio of 2:1:2 at 2 week intervals throughout the experiments. 5
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Fitness measures included total dry biomass and lifetime seed pod count. Destructive sampling for biomass occurred once individual plants died and once potentially viable seed stopped ripening. Plants were placed in individually labeled paper envelopes and dried at 70 °C for an additional week before weighing. We used seedpod count as a proxy for measuring lifetime seed production because it is a recognized method of determining the net fitness for plants with an annual life form (Kulheim et al. 2002).
and treatments (Figures 2 and 3). To ease interpretation of the relative effects of treatments on biomass and seedpod count between species, we calculated effect sizes based on centered models. We used the programming platform R v. 2.15 (R Core Team 2013) for all analyses.
Results Effect of treatments
Results from the linear regression on the biomass response for Mimulus and Clarkia suggest that both temperature and water treatments, including the interaction of temperature and water, had significant effects on biomass and seedpod count (Table A6 and A7). Higher water amounts significantly positively affected biomass for both Mimulus and Clarkia (β = 0.03, P
