Modeling effects of climate change and phase ... - Wiley Online Library

Ecology, 95(3), 2014, pp. 763–774 Ó 2014 by the Ecological Society of America

Modeling effects of climate change and phase shifts on detrital production of a kelp bed KIRA A. KRUMHANSL,1,3 JEAN-SE´BASTIEN LAUZON-GUAY,2 2

AND

ROBERT E. SCHEIBLING1

1 Biology Department, Dalhousie University, Halifax, Nova Scotia B3H 4J1 Canada Fisheries and Oceans Canada, Institut Maurice-Lamontagne, Mont-Joli, Quebec G5H 3Z4 Canada

Abstract. The exchange of energy and nutrients between ecosystems (i.e., resource subsidies) plays a central role in ecological dynamics over a range of spatial and temporal scales. Little attention has been paid to the role of anthropogenic impacts on natural systems in altering the magnitude, timing, and quality of resource subsidies. Kelp ecosystems are highly productive on a local scale and export over 80% of kelp primary production as detritus, subsidizing consumers across broad spatial scales. Here, we generate a model of detrital production from a kelp bed in Nova Scotia to hindcast trends in detrital production based on temperature and wave height recorded in the study region from 1976 to 2009, and to project changes in detrital production that may result from future climate change. Historical and projected increases in temperature and wave height led to higher rates of detrital production through increased blade breakage and kelp dislodgment from the substratum, but this reduced kelp biomass and led to a decline in detrital production in the long term. We also used the model to demonstrate that the phase shift from a highly productive kelp bed to a lowproductivity barrens, driven by the grazing activity of sea urchins, reduces kelp detrital production by several orders of magnitude, an effect that would be exacerbated by projected increases in temperature and wave action. These results indicate that climate-mediated changes in ecological dynamics operating on local scales may alter the magnitude of resource subsidies to adjacent ecosystems, affecting ecological dynamics on regional scales. Key words: climate change; detrital production; invasive species; kelp ecosystems; ocean temperature; phase shifts; predictive modeling; resource subsidies; sea urchin grazing; wave action.

INTRODUCTION Resource subsidies, or the exchange of energy and nutrients between ecosystems, occur throughout marine, freshwater, and terrestrial habitats, and influence ecology from the level of species interactions (Spiller et al. 2010) and behavior (Harrold and Reed 1985) to food web properties (Huxel et al. 2002) and ecosystem productivity (Vetter 1995). Our understanding of ecological processes has expanded over time from those operating on a local scale (e.g., species interactions) to processes that operate on large scales (e.g., dispersal of organisms) to link communities and ecosystems in a landscape. There is growing recognition that resource subsidies are a form of connectivity between ecosystems that plays a key role in shaping ecological patterns and processes across a range of scales (Gravel et al. 2010, Marleau et al. 2010). Despite the ubiquity of resource subsidies in ecological systems, the impact of anthropogenic pressures and natural disturbance on the dynamics of resource exchange between ecosystems has only recently been considered (e.g., Greg et al. 2012). Manuscript received 6 February 2013; revised 2 August 2013; accepted 19 August 2013. Corresponding Editor: C. S. Thornber. 3 E-mail: [email protected]

Kelp beds or forests can be useful model systems for examining anthropogenic impacts on resource subsidies because of their strong linkage to adjacent marine and terrestrial systems through the transfer of detritus (Krumhansl and Scheibling 2012a). Kelps are a major source of productivity and biogenic habitat in temperate and polar coastal regions worldwide. The majority of kelp production enters detrital food webs (82% [Krumhansl and Scheibling 2012a]) within kelp beds (Duggins et al. 1989) and in adjacent sandy beach (Dugan et al. 2011), rocky intertidal (Bustamante et al. 1995), rocky and sandy subtidal (Lenanton et al. 1982, Wernberg et al. 2006, Filbee-Dexter and Scheibling 2012, Kelly et al. 2012) and deep-sea habitats (Vetter 1995, Vetter and Dayton 1999). Kelp detritus acts as a significant and, in many cases, primary source of food in these receiving habitats, fueling high rates of secondary production and determining the spatial organization of communities tens of meters to hundreds of kilometers from the source of kelp production (Krumhansl and Scheibling 2012a). Kelp detritus forms the base of food webs for many economically important species, including sea urchins, abalone, crab, lobster, and groundfish (Dayton et al. 1998, Steneck et al. 2002, Jack and Wing 2011, BrittonSimmons et al. 2012, Kelly et al. 2012), that live within kelp habitats and in adjacent habitats (Krumhansl and

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Scheibling 2012a). Provisioning of detrital food webs is a significant ecosystem service supplied by kelps. Kelp biomass is being lost throughout the world through direct and indirect effects of changes in climate. Extreme warming and storm events have caused largescale losses of kelp (Vasquez et al. 2006, Reed et al. 2008, Foster and Schiel 2010, Filbee-Dexter and Scheibling 2012, Wernberg et al. 2013), the effects of which may be exacerbated by a decrease in kelp resilience at the upper limits of thermal tolerance (Wernberg et al. 2010). Increasing water temperatures in Nova Scotia and Norway are causing outbreaks of epibionts on kelp blades (Scheibling and Gagnon 2009, Andersen et al. 2011), which increase drag and reduce the strength of kelp tissues (Duggins et al. 2001, Krumhansl et al. 2011, de Bettignies et al. 2012), causing canopy loss and kelp mortality, particularly during periods of high wave action (Krumhansl and Scheibling 2011b, de Bettignies et al. 2012). Kelp ecosystems also undergo phase shifts that are defined by a marked reduction in kelp productivity and biomass. Phase shifts often occur through the destructive grazing of sea urchins in aggregations known as fronts (Lawrence 1975, Scheibling and Hatcher 2007). They also can result from kelp replacement by turf and other algal species following mortalities due to warming events, pollution, or outbreaks of epibionts (Scheibling and Gagnon 2006, Connell et al. 2008, Moy and Christie 2012, Wernberg et al. 2013). Phase-shift dynamics are tightly linked to seawater temperatures and storm frequency and intensity (Ling et al. 2009, Scheibling and Lauzon-Guay 2010). Climate change and sea urchin-mediated phase shifts have the potential to greatly influence detrital production and subsidy from kelp systems. Detrital production can be predicted to increase with warming seawater temperatures and increasing storm activity that cause kelp breakage and dislodgment, but will decline in the long term as kelp biomass is reduced. To explore this possibility, we develop a mathematical model to hindcast patterns of interannual variation in detrital production in relation to varying environmental conditions in a Nova Scotian kelp bed. We then use this model to predict impacts of climate change on detrital production rates by simulating increases in temperature and storm intensity at levels predicted in the next 10, 20, and 30 years. We also model detrital production during a sea urchin-mediated phase shift from a kelp bed to an urchin barrens. We then increase temperature and storm intensity during the transition to simulate the combined effects of environmental stressors and destructive grazing on kelp detrital production. We demonstrate that local changes in kelp biomass due to anthropogenic stressors and natural disturbance alter the magnitude of resource subsidies to adjacent ecosystems, which could have wide-ranging and profound impacts in subsidized communities.

Ecology, Vol. 95, No. 3

MATERIALS

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METHODS

Model description Detrital production was modeled based on an actual kelp bed at Splitnose Point (44828.609 0 N, 63832.741 0 W), a wave-exposed site located 17 km south of Halifax, Nova Scotia, Canada. This site was selected because the rocky subtidal community there periodically transitions between a highly productive kelp bed and a lowproductivity urchin barrens. Splitnose Point is representative of highly wave-exposed regions of the coastline, and generally has a higher biomass of kelps than more protected locations (Krumhansl and Scheibling 2011b). Kelp detrital production increases linearly with kelp biomass (Krumhansl and Scheibling 2011b), so detrital production estimates produced by our model likely represent the high end of the range for Nova Scotia. During the kelp bed state at Splitnose Point, the two dominant kelp species, Saccharina latissima and Laminaria digitata, form a dense canopy over an understory of foliose, filamentous, and turf-forming algae. The invasive bryozoan Membranipora membranacea encrusts kelp blades at this site, causing seasonal losses of kelp canopy through blade weakening and breakage (Scheibling and Gagnon 2009, Krumhansl et al. 2011). Grazing damage by the snail Lacuna vincta also weakens kelp tissues and causes increased rates of kelp blade breakage during fall storms (Krumhansl et al. 2011, Krumhansl and Scheibling 2011a, b). Urchin barrens are dominated by coralline algae and inhabited by broadly distributed sea urchins (Strongylocentrotus droebachiensis). The granitic substratum slopes gradually to a depth of 35 m, where it grades to sand (Kelly et al. 2012). See Lauzon-Guay and Scheibling (2007) for a detailed description of the site, and the dynamics of a shift from the kelp bed to the barrens state through destructive grazing by a sea urchin front. We used a series of spatial difference equations to model the biomass of each kelp species (S. latissima or L. digitata) at Splitnose Point (details provided in Appendices A–C). At each time step of one day, biomass increased through kelp production and decreased through erosion of kelp tissues, kelp dislodgment and mortality, and grazing by a sea urchin front. The spatial domain of the model comprises a 1 m wide band that extends offshore from 3 to 14 m depth. The domain was separated into 154 cells of 1 3 1 m, representing the along-bottom distance across the depth range, each with an associated depth. A conceptual diagram of interactions between biological processes and environmental variables (temperature and wave action) that determine kelp biomass and detrital production, upon which we based our model, is given in Fig. 1. Kelp production was modeled using a Ricker population growth model (Turchin 2003), which incorporated a negative effect of encrustation by the invasive bryozoan Membranipora membranacea on rate of kelp

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FIG. 1. Conceptual interactions considered in the model. Boxes contain biological components of the model, while circles contain environmental components. Lines indicate effects, with arrowheads denoting effects in the positive direction and solid circles denoting effects in the negative direction.

production, modeled using field data from Krumhansl and Scheibling (2011b). Erosion of tissues from kelp blades increased with significant wave height (defined as the mean wave height of the highest one-third of waves), temperature, percentage of total blade area covered by M. membranacea, and the percentage of the distal third of kelp blades grazed by L. vincta (Krumhansl and Scheibling 2011b). The percentage of the distal third of blade area that was grazed by L. vincta increased with kelp biomass (measured as kilograms per square meter) and temperature (Krumhansl and Scheibling 2011a). The percentage of the total kelp blade area covered by M. membranacea was predicted from the thermal integral for the previous three months (degree-days) (Scheibling and Gagnon 2009). Kelp dislodgment is defined as the loss of individual kelp thalli that occurs during large wave events. Dislodgment rates and threshold values of wave height for dislodgment were estimated for each kelp species based on observed losses of individual thalli (Krumhansl and Scheibling 2011a) or canopy cover (Filbee-Dexter and Scheibling 2012) at Splitnose Point. Daily kelp mortality rate due to senescence (0.14%) was calculated from Chapman (1993). Model estimates of erosion, dislodgment, and mortality of kelps, and fecal production by sea urchins during destructive grazing of kelp were summed to estimate total detrital production. Individual sea urchin grazing rate was wave-adjusted according to depth, and multiplied by sea urchin density to determine the total biomass of kelp consumed by sea urchins in each cell. At the beginning of a destructive grazing event, sea urchins accumulated at the lower depth limit of kelp in the model domain, and remained there until the biomass of kelp reached 0, at which point sea urchins moved to an adjacent, shallower cell (see Lauzon-Guay et al. 2009 for details). Large quantities of

feces are produced when sea urchins destructively graze kelps, which contribute to the detrital pool (Sauchyn and Scheibling 2009a, b). Fecal production by sea urchins in dry mass (grams per day) was calculated by multiplying the dry mass of kelp consumed by the percentage of consumed material that is defecated (35.2% [Sauchyn et al. 2011]). If kelp biomass reached 0 in any cell that had not been grazed by sea urchins, it was set at 25 g at the beginning of the next time step to represent kelp recruitment (Lauzon-Guay et al. 2009). We assumed that a background density of sea urchins behind the front would consume kelp recruits in the barrens and prevent kelp recovery. Environmental parameters Seawater temperature from 1976 to 2009 was obtained from the Coastal Time Series (CTS) database, recorded as the average daily temperature from thermographs at 0–10 m depth. Thermographs were located within a polygon that is 5 km offshore and extends from Halifax Harbour (44839 0 N, 63834 0 W) to Lunenburg Bay (44815 0 N, 64814 0 W). Temperature was assumed to be constant across depths in the model domain. Significant wave height was obtained from meterological buoys located at Osbourne Head (1976–2001, buoy ID No. MEDS037, 44830 0 N, 6384 0 W) and Halifax Harbour (2001–2009, buoy ID No. C44258, 44830 0 N, 63824 0 W), located ;10 km from Splitnose Point. A wave attenuation function was applied to predict the impact of wave height at all depths (Holthuijsen 2007). Model runs To hindcast kelp biomass, kelp production, and detrital production (erosion, dislodgment and mortality of kelp) from 1976 to 2009, the model was run using temperature and wave height data recorded for this

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period. We then modeled the advance of a sea urchin grazing front to examine the reduction of kelp biomass, kelp production, and detrital production (erosion, dislodgment, and mortality of kelps; fecal production by sea urchins) associated with the transition from a kelp bed to an urchin barrens state. To do so, each year of environmental data was repeated 34 times independently to simulate a 34-year period over which this transition occurs and results in a stable barrens state. Kelp production, biomass, erosion, dislodgment, and mortality; sea urchin fecal production; and total detrital production were then averaged over all 34 model runs to generate mean values based on past variation in environmental conditions. To examine the potential impact of climate change on kelp biomass, kelp production, and detrital production, temperature and significant wave height were increased in the model at three levels based on projected changes to these climatic variables in 10, 20, and 30 years. Projected mean global increase in sea surface temperature is 0.0228C/yr (IPCC Fourth Assessment Report: Climate Change 2007, scenario A1B [IPCC 2007]). In model runs simulating the expected temperature increase in 10 years, a 0.228C increase was applied to all years in the 34-year data set. Each year of environmental data was then repeated for 12 years in the model. This is the period over which a phase shift from a kelp bed to barrens state occurs in our model, and is used to compare predictions under a stable kelp bed state vs. during a phase shift. Kelp production, erosion, dislodgment, mortality, and total detrital production were then summed separately over this 12-year period, and biomass was averaged. The proportional change in each measure was then calculated by subtracting the total or average over the 12-year period under normal conditions from the total or average during the 12-year period of simulated temperature increase, and divided by values under normal conditions. This was repeated for temperature increases of 0.448C (20-year simulation), and 0.668C (30-year simulation). Scheibling and Lauzon-Guay (2010) conducted a trend analysis of the 95th quantile of wind data over the past 30 years, detecting an annual increase of 0.5%. Assuming that the 95th quantile of waves increases at the same rate, we apply a 5%, 10%, and 15% increase in significant wave height to simulate expected conditions in 10, 20, and 30 years. This increase was applied to the model in the same way as for temperature. In a third set of simulations, both temperature and significant wave height were increased simultaneously at conditions predicted for each variable in 10, 20, and 30 years (i.e., 0.228C increase in temperature and 5% increase in significant wave height in 10 years, and so on). These nine climate simulations were then run with the advance of a sea urchin grazing front to predict the combined effects of losses of kelp biomass and climate change for detrital production. Proportional changes in each measure were calculated in the same manner.


RESULTS Hindcasted interannual trends in model parameters (1976–2009) Kelp biomass; annual rates of kelp production, erosion, dislodgment, and mortality; and total detrital production varied among years in our model (Fig. 2) in relation to interannual variation in environmental conditions and levels of grazing by L. vincta or blade encrustation by M. membranacea (Fig. 3). Mean and maximum water temperature increased from 1976 to 2009. Accordingly, our model predicted that mean and maximum levels of grazing by L. vincta also increased over this period, and that cover by M. membranacea on kelp blades was low or absent prior to 1983. After 1983, the cover of M. membranacea fluctuated interannually throughout the modeled period. Mean significant wave height varied little among years, but annual maxima varied widely, with peaks in 1993, 1995, and 1998. Erosion of kelp blades and total detrital production fluctuated interannually in our model (77–150 kg/yr and 191–260 kg/yr in the model domain, respectively), but increased over the 34-year period along with temperature and grazing by L. vincta (Figs. 2 and 3). The sharp increase in erosion in 1983 coincided with the appearance of M. membranacea in the model. Subsequent interannual variation in erosion of kelp and total detrital production reflected variation in the cover of M. membranacea. The model predicted the highest rate of erosion and cover of M. membranacea in 1990, when water temperature and grazing by L. vincta also were high. Dislodgment also fluctuated interannually in the model, and contributed an order of magnitude less kelp material to the detrital pool (4–27 kg/yr in the model domain) than erosion (77–150 kg/yr) or mortality (94– 104 kg/yr) (Fig. 2). The model predicted the highest rate of dislodgment in 1993, when the maximum significant wave height also was greatest among all years. Biomass decreased over time in the model as water temperature, erosion, total detrital production, and grazing damage by L. vincta increased, with the exception of a temporary increase from 2002 to 2004 when cover by M. membranacea was low (Figs. 2 and 3). Biomass decreased sharply in years in the model with high erosion rates (e.g., 1984, 1990, 1999). Mortality, which is a function of biomass in the model, followed a similar pattern as biomass from 1976 to 2009, and contributed less to the detrital pool than erosion after 1983. Kelp production increased over time in the model as kelp biomass decreased relative to the population carrying capacity. Our model also predicted spatial (with depth) and intra-annual (by month) patterns in detrital production, not presented here, that are strongly concordant with field measurements at Splitnose Point. For example, the model predicted an annual erosion rate at 5 m depth (1.62 kg/m2) that is comparable to that measured in the

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FIG. 2. Modeled mean kelp biomass, kelp production, erosion, dislodgment and mortality, and total detrital production in the model domain (154 m2) based on environmental conditions recorded in the study region from 1976–2009.

field (1.71 kg/m2 [Krumhansl and Scheibling 2011a]). Similarly, predicted increases in detrital production rates in fall, coinciding with decreases in kelp biomass, mirrored seasonal patterns recorded at this site (Krumhansl and Scheibling 2011b). Trends with sea urchin grazing The transition from kelp bed to urchin barrens occurred over a 12-year period in the model (Fig. 4). During this transition, mean kelp biomass and kelp production decreased linearly from 185 to 15 kg and from 229 to 47 kg/yr, respectively, in the model domain (Fig. 4). Mortality also decreased linearly (from 94 to 8 kg/yr) as a proportion of kelp biomass. Erosion decreased from 117 to 25 kg/yr, with the greatest rate of decline when the grazing front was between 5 and 7 m. Dislodgment was consistently low (16 to 13 kg/yr) during the transition. Sea urchin fecal production contributed least to detrital production, and was greatest when the front was between 8 and 13 m (7.8 kg/yr), declining rapidly to 0 as the front grazed kelps shallower than 8 m. Total detrital production declined

from 235 to 48 kg/yr over the 12-year transition, mainly due to decreases in erosion and mortality. Climate change simulations Increases in temperature and significant wave height, applied either independently or concurrently in our model simulations, predict a decline in biomass relative to historical levels of these environmental factors (1976– 2009) in 10, 20, and 30 more years (i.e., by 2020, 2040, and 2050) (Fig. 5). The magnitude of biomass loss is greatest for simulations in which both temperature and significant wave height are increased. Increasing temperature alone and with significant wave height in the model result in an increase in grazing by L. vincta and encrustation by M. membranacea in all three projections, which cause an increase in erosion and total detrital production (Fig. 5). Erosion and total detrital production decrease along with grazing by L. vincta when significant wave height alone is increased in the model. Dislodgment increases when significant wave height is increased alone and with temperature, but decreases when only temperature is increased (Fig. 5). Kelp

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height independently or concurrently with temperature causes a decline in erosion, as biomass is lost to grazing (Fig. 6). Sea urchin feeding fronts advanced more rapidly in all climate change simulations compared to historical environmental conditions. This effect was greatest in simulations with a combined increase in temperature and significant wave height (Fig. 6). DISCUSSION

FIG. 3. Modeled mean and maximum blade area grazed by Lacuna vincta and cover by Membranipora membranacea, and recorded water temperature and significant wave height for each year in the model from 1976 to 2009.

production follows a similar pattern to that of erosion and total detrital production in all simulations (Fig. 5). In climate change simulations with destructive grazing by sea urchins, kelp biomass, total detrital production (including fecal production), and kelp production decline with increases in temperature and/or significant wave height in each of the three projections based on our model (Fig. 6). This decrease in biomass is greater than that predicted in climate change simulations without sea urchins (Fig. 5). Erosion increases with temperature in a similar manner as in simulations without urchins, but to a lesser degree (Fig. 6). Increasing significant wave

Climate-driven changes in ecosystem state have significant impacts on local community structure and productivity. Our model indicates that historical and predicted future changes in climate and phase shifts reduce kelp biomass, and in turn detrital production rates. Kelp detritus subsidizes coastal and deep-sea ecosystems over large scales (Krumhansl and Scheibling 2012a). Anthropogenic impacts and phase-shift dynamics have traditionally been viewed from the perspective of impacts on community dynamics on a local scale. Our modeling results suggest that impacts may extend to regional scales as the magnitude of detrital subsidies to adjacent systems is reduced. Our model predicts that detrital production increased between 1976 and 2009 as a result of warming seawater temperatures over this period through a combination of direct and indirect processes. High water temperature directly reduces the quality and toughness of kelp blade tissues by causing degradation (Rothausler et al. 2009), leading to an increase in erosion rate. Reduced tissue toughness also facilitates grazing by mesograzers such as L. vincta (Molis et al. 2010), which reduces the strength of kelp tissues and increases the incidence of blade breakage and canopy loss (Krumhansl et al. 2011, Krumhansl and Scheibling 2011a, b, de Bettignies et al. 2012). Erosion and total detrital production increased significantly following the appearance of the invasive bryozoan M. membranacea in the model in 1983. Average annual temperature rose by 0.58–4.88C after 1983 over those recorded from 1977 to 1982, with the exception of 1988, when our model predicted no blade coverage by M. membranacea. In reality, M. membranacea was first reported in the Gulf of Maine, USA, in 1987 (Lambert et al. 1992) and along the Atlantic coast of Nova Scotia in 1992 (Scheibling et al. 1999). Our model suggests that temperature conditions prior to 1983 may have been unsuitable for recruitment and high rates of growth of the invasive bryozoan on kelps, if it had been present in the region. This is consistent with a population dynamics model for M. membranacea on kelps in Nova Scotia, which predicts a near complete loss of blade coverage when daily water temperatures from January to August (2005–2008) are reduced by 18– 28C (Saunders et al. 2010). These results indicate that a historical increase in temperature may have fundamentally altered seasonal dynamics of detrital production in kelp beds in Nova Scotia, leading to a predicted longterm decline of kelp biomass and concomitant detrital subsidy.

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FIG. 4. Modeled kelp biomass, kelp production, erosion, dislodgment and mortality, total detrital production, the depth of the urchin front, and urchin fecal production during destructive grazing by sea urchins in the model domain (154 m2). The black line denotes the mean of model runs that repeat each year of environmental data 34 times. Gray shaded area indicates maximum and minimum values.

Physical processes and biological interactions similar to those included in our model also regulate detrital production rates in other temperate kelp systems (Krumhansl and Scheibling 2012a). High kelp blade erosion rates have been reported in other regions in late summer and fall when water temperature, irradiance, sedimentation, and fouling by encrusting and grazing epibionts are high (Gunnill 1985, Brown et al. 1997, Andersen et al. 2011), suggesting increases in detrital production rates and declines in kelp biomass with increasing water temperatures. Large wave events are a common cause of biomass loss in kelp ecosystems globally, but higher drag on larger canopy kelp species

such as Macrocystis and Nereocystis may make them more prone to dislodgment than smaller prostrate forms such as Laminaria and Saccharina. This could result in a more direct positive effect of significant wave height on detrital production, and negative effect on biomass, for these large kelp species than predicted by our model. Interestingly, loss of blade tissue resulting from blade damage by mesograzers may enhance survivorship of some kelp species by reducing blade area and drag, enabling them to persist under increasing wave conditions (de Bettignies et al. 2012, 2013). Sea urchin-mediated phase shifts are common in kelp beds and forests throughout their temperate range, and

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FIG. 5. The relative change (%) in mean kelp biomass, kelp production, erosion, and dislodgment, kelp blade area grazed by Lacuna vincta, encrustation by Membranipora membranacea, and total detrital production relative to historical conditions during a simulated absolute increase in temperature and relative increase in significant wave height (SWH; defined as the mean wave height of the highest one-third of waves) at levels predicted after 10 years (0.228C, 5% wave height), 20 years (0.448C, 10%), and 30 years (0.668C, 15%), and a combined increase of temperature and significant wave height at these levels. The error bars show maximum and minimum values.

in many regions are the result of overfishing of top predators that control sea urchin populations (Steneck et al. 2002, Ling et al. 2009). According to our model, detrital production is reduced by an order of magnitude (from 235 to 48 kg/yr) during the transition from a kelp bed to an urchin barrens. Phase shifts to turf and other algal-dominated assemblages (Connell et al. 2008, Andersen et al. 2011, Tanaka et al. 2012), or barrens dominated by other echinoderms (Rassweiler et al. 2010), also occur throughout the global range of kelp, and in many cases are attributed to or exacerbated by

anthropogenic impacts on kelp ecosystems (e.g., Ling et al. 2009). These phase shifts are characterized by largescale and persistent declines of kelp biomass, and are likely to be associated with similar losses of kelp detrital production, as predicted by our model. The ability to model key ecosystem processes is important for predicting the impacts of environmental change. Detrital pathways account for most of the material and energy flow from kelp primary production in kelp ecosystems (Krumhansl and Scheibling 2012a), and our model demonstrates that dynamics of detrital

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FIG. 6. The relative change in mean kelp biomass, kelp production, erosion, and dislodgment, kelp blade area grazed by Lacuna vincta; encrustation of kelp by Membranipora membranacea; and total detrital production relative to historical conditions during destructive grazing by sea urchins, and a simulated absolute increase in temperature and relative increase in significant wave height (SWH, defined as the mean wave height of the highest one-third of waves) at levels predicted in 10 years (0.228C, 5% wave height), 20 years (0.448C, 10%), and 30 years (0.668C, 15%), and a combined increase of temperature and significant wave height at these levels. Also shown is the relative position of the sea urchin grazing front (Front depth) in future climate simulations relative to simulated grazing during historical conditions. Error bars show maximum and minimum values.

production are linked to long-term variation in temperature and significant wave height. Increasing these environmental factors to levels predicted in 10, 20, and 30 years beyond the historical baseline (1976–2009) had complex direct and indirect effects on detrital production rates. Increasing temperature alone or together with significant wave height resulted in an increase in detrital production rates (particularly for temperature alone).

Dislodgment increased when significant wave height alone was increased, but this did not correspond to an increase in total detrital production rates in these simulations. Erosion is a more significant pathway of detrital production in this kelp system than dislodgment, so wave-mediated dislodgment of kelp individuals reduced the number of kelps that contribute detritus through erosion, and resulted in a decline in total

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detrital production. This decline was also attributed to a reduction in grazing intensity by L. vincta on kelps with increasing significant wave height. Kelp biomass was reduced by high rates of detrital production through erosion and dislodgment in all climate simulations, with the greatest decline when temperature and significant wave height were increased concurrently in the model. When a sea urchin grazing front was included in climate simulations, biomass decreased to a much greater degree, damping the positive effect of increasing temperature on total detrital production. These results suggest that increases in these environmental factors with climate change will increase detrital production in the short term, but will have long-term negative effects on kelp bed persistence and detrital production through a reduction in kelp biomass. The synergistic effects of changes in climate and phase shifts are predicted to cause the greatest reductions in detrital subsidies. The predicted global increase in mean SST (0.0228C/ yr) used in our model is based on the IPCC A1B (IPCC 2007) scenario of global economic growth and development, which is generally thought of as representing an ‘‘average’’ trajectory of temperature increase. The Northwest Atlantic has been warming more rapidly than other regions of the globe in the past century (Wu et al. 2012), which may be an indication that future warming in the region will exceed global averages. Recent studies have shown that the intensification of climatic extremes may cause more dramatic ecosystemscale changes than gradual rises in mean temperature (Trenberth 2012, Wernberg et al. 2013), suggesting that future changes in climate may cause greater declines in kelp biomass and detrital production than predicted by our model. Also, it is important to note that our model does not explicitly address the direct physiological effects of temperature on kelp production and growth. Even gradual increases in temperature are likely to decrease kelp production in cold-temperate kelp species (Staehr and Wernberg 2009, Bearham et al. 2013), resulting in a significant decrease in growth and productivity. The potential for anthropogenic changes to ecosystems to impact resource subsidies has largely been overlooked. Recent studies have shown that introduced species can alter both the magnitude of resource exchange between ecosystems through negative interactions with animals that act as vectors of resource transport (Croll et al. 2005, Fukami et al. 2006, Young et al. 2010), and the nutritional quality of resource subsidies through displacement of native macroalgae (Krumhansl and Scheibling 2012b). Warming temperatures also can effect the phenology and magnitude of cross-ecosystem exchanges of materials through species range shifts and changes in species abundance, primary production, and decomposition rates (Buzby and Perry 2000, Leberfinger et al. 2010, Larsen et al. 2011, Greg et al. 2012). Such changes can have profound impacts on global carbon cycling (Larsen et al. 2011), predator–prey


interactions (Harrold and Reed 1998, Nakano and Murakami 2001), community structure (Krumhansl and Scheibling 2012b), and productivity (Bustamante et al. 1995, Vetter 1995). Our model indicates that climate-mediated declines in biomass of a dominant primary producer on a local scale may reduce the magnitude of detrital subsidies, influencing dynamics on regional scales. This result can be generalized to any natural system with a dominant primary producer that supplies detrital food webs over a range of scales. Future research should attempt to quantify the effect of changes in resource subsidies that result from climate change, introduced species, and phase shifts on primary and secondary productivity and community organization in subsidized habitats. The impact of anthropogenic changes to ecosystems on cross-ecosystem exchange of resources should be considered more broadly. ACKNOWLEDGMENTS This research was funded by a Discovery Grant and a Strategic Networks Grant (Canadian Healthy Oceans Network) to R. E. Scheibling from the Natural Sciences and Engineering Research Council of Canada (NSERC). We thank two anonymous reviewers for the helpful comments on a previous draft of the manuscript. LITERATURE CITED Andersen, G. S., H. Steen, H. Christie, S. Fredriksen, and F. E. Moy. 2011. Seasonal patterns of sporophyte growth, fertility, fouling, and mortality of Saccharina latissima in Skagerrak, Norway: implications for forest recovery. Journal of Marine Biology 11:690375. Bearham, D., M. A. Vanderklift, and J. R. Gunson. 2013. Temperature and light explain spatial variation in growth and productivity of the kelp Ecklonia radiata. Marine Ecology Progress Series 476:59–70. Britton-Simmons, K. H., A. L. Rhoades, R. E. Pacunski, A. W. E. Galloway, A. T. Lowe, E. A. Sosik, M. N. Dethier, and D. O. Duggins. 2012. Habitat and bathymetry influence the landscape-scale distribution and abundance of drift macrophytes and associated invertebrates. Limnology and Oceanography 57:176–184. Brown, M. T., M. A. Nyman, J. A. Keogh, and N. K. M. Chin. 1997. Seasonal growth of the giant kelp Macrocystis pyrifera in New Zealand. Marine Biology 129:417–424. Bustamante, R. H., G. M. Branch, and S. Eekhout. 1995. Maintenance of an exceptional intertidal grazer biomass in South Africa: subsidy by subtidal kelps. Ecology 76:2314– 2329. Buzby, K. M., and S. A. Perry. 2000. Modeling the potential effects of climate change on leaf pack processing in central Appalachian streams. Canadian Journal of Fisheries and Aquatic Sciences 57:1773–1783. Chapman, A. R. O. 1993. ‘Hard’ data for matrix modeling of Laminaria difitata (Laminariales, Phaeophyta) populations. Hydrobiologia 260/261:263–267. Connell, S. D., B. D. Russell, D. J. Turner, S. A. Shepherd, T. Kildea, D. Miller, L. Airoldi, and A. Cheshire. 2008. Recovering a lost baseline: missing kelp forests from a metropolitan coast. Marine Ecology Progress Series 360:63– 72. Croll, D. A., J. L. Maron, J. A. Estes, E. M. Danner, and G. V. Byrd. 2005. Introduced predators transform subarctic islands from grassland to tundra. Science 307:1959–1961. Dayton, P. K., M. J. Tegner, P. B. Edwards, and K. L. Riser. 1998. Sliding baselines, ghosts, and reduced expectations in kelp forest communities. Ecological Applications 8:309–322.

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SUPPLEMENTAL MATERIAL Appendix A Detailed description of modeling methods and parameters (Ecological Archives E095-062-A1). Appendix B Parameter abbreviations used in the model (Ecological Archives E095-062-A2). Appendix C Parameter coefficients used in the model to predict erosion, kelp production, grazing damage by Lacuna vincta on kelp blades, and kelp blade coverage by Membranipora membranacea (Ecological Archives E095-062-A3).