Climate and Fishing Drive Regime Shifts in Consumer-Mediated Nutrient

3180 | PETERS ET al.

(Early et al., 2016; Mack et al., 2000), habitat degradation (Lotze, have drawn attention to the potential importance of CND in con- 2006; McCauley et al., 2015), and anthropogenic climate change tributing to macrophyte productivity in temperate systems (Bracken (Hoegh-Guldberg & Bruno, 2010). To date, the vast majority of re- & Nielsen, 2004; Bray et al., 1988; Bray, Purcell, & Miller, 1986; search on the importance of animals in structuring ecosystems has Hepburn & Hurd, 2005), the extent to which changes in consumer focused on their role as consumers in influencing food web structure, abundance alter nutrient dynamics in these systems has received lit- trophic interactions, and energy flow (Estes et al., 2011; Terborgh, tle attention. 2015). Yet, as consumers, animals also serve as important media- Like most coastal ecosystems, fishing has drastically reshaped the tors of biogeochemical cycles through their excretion and egestion abundance and size structure of important consumers in kelp forests of essential nutrients (Elser et al., 2007; Elser & Urabe, 1999; Vanni, worldwide (Dayton, Tegner, Edwards, & Riser, 1998; Ling, Johnson, 2002). Consequently, widespread changes in consumer populations Frusher, & Ridgway, 2009; Salomon, Shears, Langlois, & Babcock, have the potential to fundamentally disrupt community dynamics, 2008; Steneck et al., 2002; Tegner, 2000). These impacts from fish- primary production, and other important functions as they mediate ing are being mitigated in part by the increased use of no-take ma- bottom-up as well as top-down regulation of ecosystems (Burkepile rine protected areas (MPAs) as tools for fishery management, and et al., 2013; Polis, 1999). for promoting and protecting ecosystem conservation (Edgar et al., Consumer-mediated nutrient dynamics (herein CND) is a critical 2014; Gell & Roberts, 2003; Lester et al., 2009). The use of MPAs in component of biogeochemical cycling in a wide range of terrestrial kelp forests has been particularly effective in restoring populations and aquatic systems, and the degree to which changes in consumer of top predators (Goñi, Quetglas, & Reñones, 2006; Kay, Lenihan, populations alter nutrient cycling is becoming increasingly recog- Guenther, et al., 2012; Kelly, Scott, MacDiarmid, & Babcock, 2000; nized (see reviews by Allgeier, Burkepile, & Layman, 2017; Atkinson, Lipcius, Stockhausen, & Eggleston, 2001), which can have cascading Capps, Rugenski, & Vanni, 2017; Sitters et al., 2017). Importantly, effects on primary producers (Caselle, Davis, & Marks, 2018; Shears disruptions to CND can diminish the provisioning of important eco- & Babcock, 2003). Ocean warming is another pervasive threat to kelp system services by animals such as fisheries, carbon sequestration, forest consumers and has been linked to large changes in their abun- and ecotourism (Hammerschlag et al., 2019; Schmitz, Hawlena, & dance and distribution, exacerbating the adverse effects of increased Trussell, 2010). CND may be especially important in hard bottom temperature on forest macrophytes worldwide (Pessarrodona et al., marine systems where the capacity to store nutrients is limited due 2019; Vergés et al., 2016; Wernberg et al., 2016). Moreover, over- to the absence of sediments. Such is the case for oligotrophic coral fishing of predators and high ocean temperature have been linked reefs where aggregations of fish serve as biogeochemical hotspots to outbreaks of infectious disease (Harvell, 1999; Lafferty, Porter, & concentrating nutrients that otherwise limit primary production Ford, 2004), which have led to dramatic population declines in im- (Layman, Allgeier, Yeager, & Stoner, 2013; Meyer, Schultz, & Helfman, portant consumers such as sea urchins and sea stars (Eisenlord et al., 1983; Shantz, Ladd, Schrack, & Burkepile, 2015). Moreover, de- 2016; Lafferty, 2004; Lester, Tobin, & Behrens, 2007). How fishing clines in reef fish populations due to fishing can significantly reduce pressure, disease, and climate change interact to disrupt CND in kelp the supply of nutrients to coral symbionts and reef macrophytes forests is entirely unknown, despite the potentially adverse conse- (Layman, Allgeier, Rosemond, Dahlgren, & Yeager, 2011) and lead to quences of their synergistic effects on the populations of many spe- decreases in primary production (Layman et al., 2013). cies (Lafferty, 2004; Ling et al., 2009). Unlike coral reefs in the tropics, shallow reefs in temperate seas In this study, we examined CND of benthic macroinvertebrates are typically dominated by forests of large brown macroalgae, that inhabiting giant kelp (Macrocystis pyrifera, Linnaeus) forests of south- is, kelps, whose net primary production rivals that of the most pro- ern California, where year-round kelp growth coupled with extended ductive ecosystems on Earth (Mann, 1973; Reed & Brzezinksi, 2009). periods of low concentrations of seawater nitrate and limited nitro- Nitrate is often considered to be the major form of nitrogen that fuels gen storage is the norm (Brzezinski et al., 2013). Our 18-year time this high productivity, yet its availability in many temperate reef sys- series of macroinvertebrate biomass spanned the most extreme tems varies greatly among seasons and years (Brzezinksi et al., 2013; warming event on record (Bond, Cronin, Freeland, & Mantua, 2015; Chapman & Craigie, 1977; Jackson, 1977; van Tussenbroek, 1989). Di Lorenzo & Mantua, 2016; Peterson, Robert, & Bond, 2015), dis- Despite this high variability and the limited capacity for some kelps ease outbreaks that led to mass mortalities of an important con- to store nitrogen for less than a few weeks (Gerard, 1982b), mea- sumer guild (Hewson et al., 2014), and the establishment of no-take surable growth occurs year-round in many kelp systems (Hepburn, MPAs at two of our five long-term study sites (Gleason et al., 2013). Holborow, Wing, Frew, & Hurd, 2007; Kirkman, 1989; Pessarrodona, We coupled species-specific estimates of ammonium excretion rates Foggo, & Smale, 2019; Reed, Rassweiler, & Arkema, 2008; Vadas, measured in the field to our biomass time series to (a) assess the Beal, Wright, Nickl, & Emerson, 2004; van Tussenbroek, 1989). Such contributions of benthic invertebrates to the supply of recycled observations have prompted suggestions that recycled forms of ni- nitrogen, (b) characterize CND of kelp forest macroinvertebrates trogen (e.g., ammonium and urea) are important in sustaining kelp across a wide range of environmental conditions, and (c) determine growth during extended periods of low nitrate availability (Brzezinksi how anomalous ocean warming, disease outbreaks, and fishing al- et al., 2013; Hepburn & Hurd, 2005; Smith, Brzezinski, Melack, Miller, tered CND through losses of top consumers and shifts in community & Reed, 2018; Wheeler & Druehl, 1986). While several investigators structure. PETERS ET al. | 3181

2 | MATERIALS AND METHODS Animals that could easily be collected by divers were brought to the surface and immediately transferred into 0.1 to 8.0 L acid-washed 2.1 | Study system clear plastic bags (depending on animal size) with known volumes of prefiltered (0.35 µm Whatman GF filter), UV-sterilized seawater. We focused our study on giant kelp forests located on shallow reefs Bags with animals were paired with control bags without animals (4–11 m depth) off the mainland coast of the Santa Barbara Channel, (filtered seawater only) and allowed to incubate for 30–150 min (de- CA, USA. Kelp forests in this region support diverse assemblages of pending on animal size) in a closed cooler with ice packs to maintain benthic invertebrates, fish, and other macroalgae that rely strongly on ambient temperatures. Water collected from each bag at the end of physical modification of habitat (e.g., light, space, temperature) by M. the incubation period was filtered (0.45 µm Whatman GF) into 60 ml pyrifera (Byrnes et al., 2011; Castorani, Reed, & Miller, 2018; Miller et amber HDPE bottles and placed on ice for transport to the labora- al., 2018). Data were collected at five kelp forests spanning ~75 km of tory at UCSB for ammonium analysis. Animals used in incubations coast: Arroyo Quemado (AQUE; 120.07°W, 34.28°N), Naples (NAPL; were also transported to the laboratory where they were weighed 119.57°W, 34.25°N), Isla Vista (IVEE; 119.51°W, 34.24°N), Mohawk wet for subsequent conversion to SFDM using species-specific rela- (MOHK; 119.43°W, 34.23°N), and Carpinteria (CARP; 119.32°W, tionships developed by Reed, Nelson, et al. (2016). 34.23°N). Between January 2014 and December 2015, prolonged We performed in situ incubations for the anemone Anthopleura warming of bottom waters occurred throughout much of the sola (Brandt, 1835) and the boring piddock clams Chaceia ovoidea Northeastern Pacific (Di Lorenzo & Mantua, 2016), including our study (Gould, 1851) and Parapholas californica (Conrad, 1837) because they sites where daily and monthly bottom temperature anomalies as high were difficult for divers to collect without causing them excessive as +5.8°C and +4.6°C, respectively, were recorded (Reed, Washburn, physiological stress or physical harm. Incubations for these species et al., 2016). Coinciding with this warming event were epidemic disease consisted of placing a clear polypropylene chamber over the speci- outbreaks that caused populations of sea stars to decline by >90% and men for 60 min. Chambers (0.7 L volume) had an open bottom (6 cm sea urchins by ~50% (Reed, Washburn, et al., 2016). In addition, a net- diameter) and were sealed to seafloor with a rubber gasket and a work of no-take MPAs was established in southern California in 2012 weighted flexible rubber skirt. Trials using rhodamine dye indicated that included two of our study sites (NAPL and IVEE), which provided the seal was effective and prevented water from flowing into or out us with an opportunity to assess the impacts of fishing on CND. of the chamber (J.R. Peters, personal observation). Incubation chambers were paired with control chambers (ambient seawater only). 2.2 | Data collection and time series procedures Following incubation, water samples for ammonium analysis were drawn from each chamber and the study specimen was collected. 2.2.1 | Time series of invertebrate biomass Water samples and animal specimens were transported to the labo-

Data on the size and abundances of common sessile and mobile reef ratory and processed as described above. macroinvertebrate species were collected annually in summer (July– The ammonium concentrations of all water samples were deter- August) from 2001 to 2018 within 80-m2 fixed plots (n = 2–8 plots mined within 12 hr of collection following fluorometric methods out- per site) by the Santa Barbara Coastal Long-Term Ecological Research lined by Taylor et al. (2007). Concentrations were converted to per capita ammonium excretion rates (µmol NH + h−1 individual−1) by factor- program (Reed, 2018). Sizes and abundances of all species were 4 converted into shell-free dry mass (herein SFDM) using species-spe- ing the bag/chamber volume (L) and incubation time (min) of each indi- cific power functions developed by Reed, Nelson, Harrer, and Miller vidual. Mass-specific ammonium excretion rates were calculated as the excretion rate divided by individual SFDM (µmol NH + h−1 dry g−1). We (2016). This 18-year time series of invertebrate biomass was cou- 4 pled with species-specific ammonium excretion rates (see below) to adjusted excretion rates by subtracting ammonium concentrations mea- model population- and community-level ammonium excretion rates. sured in filtered and ambient seawater as well as changes within control Beginning in summer 2012, additional surveys with a larger plot size bags/chambers paired with samples during the same incubation period. (1,200 m2) were conducted for the California spiny lobster, Panulirus interruptus, to obtain more accurate population estimates for this 2.2.3 | Time series of excretion rates highly mobile kelp forest predator (Reed, 2019). Lobster excretion models based on this 7-year time series were used to assess popula- Species-specific excretion data were used to develop generalized tion-level responses to no-take reserves and warming. linear models to assess the relationship between the ammonium excretion rate and the SFDM of an individual. Because they had similar excretion rates, species of sea urchins (Strongylocentrotus purpuratus 2.2.2 | Ammonium excretion rates (Stimpson, 1857) and Mesocentrotus franciscanus (Agassiz, 1863)) and We measured ammonium excretion rates from 351 individuals of 14 boring clams (C. ovoidea and P. californica) were pooled into their own common benthic macroinvertebrate species (Table 1) in late sum- respective models. Regressions were performed on log-transformed mer and early fall of 2017 and 2018. Excretion was measured for variables to estimate the slope, intercept, and root mean square a representative size range of each species following the methods error for each model (Appendix S1), and residuals were visually in- of Layman et al. (2011) and Allgeier, Yeager, and Layman (2013). spected to ensure assumptions of normality and homoscedasticity. 3182 | PETERS ET al.

TABLE 1 Mean excretion rates (mass-specific, per capita, and areal) of common kelp forest macroinvertebrates

Mass‐specific Per capita Areal excretion excretion excretion + + + (µmol NH4 (µmol NH4 (µmol NH4 Wet mass (g) dry g−1 hr−1) ind−1 hr−1) m−2 hr−1)

Species Common name n Range Mean ± SE Mean ± SE Mean ± SE

Panulirus interruptus California spiny lobster 71 77.82–1,511.15 3.41 ± 0.18 188.84 ± 9.31 0.91 ± 0.71 Pisaster giganteus Giant sea star 10 85.27–297.8 1.52 ± 0.12 22.41 ± 2.89 3.03 ± 1.27 Patiria miniata Bat star 11 10.27–116.84 0.48 ± 0.04 3.28 ± 0.39 1.06 ± 1.20 Muricea californica California golden gorgonian 18 6.26–69.96 0.27 ± 0.02 0.86 ± 0.09 0.15 ± 0.14 Megathura crenulata Giant keyhole limpet 28 47.62–199.39 0.27 ± 0.01 4.52 ± 0.13 0.42 ± 0.21 Norrisia norrisii Norris's top snail 13 34.00–80.78 0.15 ± 0.01 0.9 ± 0.1 0.002 ± 0.003 Styela montereyensi Stalked tunicate 11 5.51–17.6 0.14 ± 0.01 0.23 ± 0.03 0.22 ± 0.19 Kelletia kelletii Kellet's whelk 30 4.18–341.46 0.1 ± 0.01 0.2 ± 0.06 0.04 ± 0.03 Mesocentrotus Red urchin 30 60.31–357.69 0.08 ± 0.003 1.55 ± 0.11 0.76 ± 0.37 franciscanus Stronglyocentrotus Purple urchin 32 52.04–155.52 0.07 ± 0.01 0.75 ± 0.07 2.23 ± 0.98 purpuratus Megastraea undosa Wavy turban snail 36 3.58–507.40 0.07 ± 0.01 0.48 ± 0.11 0.08 ± 0.08 Chaceia ovoidea Wartneck piddock 31 153.6–331.09 0.03 ± 0.002 0.61 ± 0.08 1.05 ± 0.76 Parapholas californica Scale-sided piddock 15 92.51–178.94 0.01 ± 0.001 0.12 ± 0.02 0.38 ± 0.25 Anthopleura sola Starburst anemone 15 4.92–43.73 0.01 ± 0.001 0.04 ± 0.01 0.06 ± 0.02

Note: Mass-specific excretion rates were calculated as total ammonium excretion divided by the dry mass (g) of an individual. Per capita excretion rates were averaged over all sizes measured for that species. Areal excretion rates were averaged across all sites and years. Species arranged in order of decreasing mass-specific excretion rates. Size ranges n = sample size of incubated individuals.

We generated an 18-year time series of ammonium excretion 2.3 | Data analyses rates at our study sites by populating species-specific models with the standing biomass of species with excretion data. Specifically, per To assess the contributions of benthic invertebrates to nitrogen re- + −1 −1 capita ammonium excretion rates (µmol NH4 individual hr ) were cycling, we ranked species in order of their mass-specific excretion calculated from the SFDM of an individual and multiplied by the mean rates and compared their mean per capita and areal N excretions + −2 −1 + density of a species to obtain areal N excretion (µmol NH4 m hr ) (Table 1). We then aggregated areal NH4 excretions and standing for each species in a plot (Allgeier et al., 2013; Burkepile et al., 2013). biomass estimates into the following functional groups based on Models developed for Pisaster giganteus (Stimpson, 1857) were used their contributions to total excretion and biomass: “Sea stars” (P. gi- as proxies for Pisaster brevispinus (Stimpson, 1857) due to the few ganetus, P. brevispinus, and Patiria miniata (Brandt, 1835)), “Urchins” P. brevispinus remaining at our sites. We applied this procedure to (S. purpuratus and M. franciscanus), “Boring clams” (C. ovoidea, P. cali- the more spatially comprehensive data collected for spiny lobster fornica), “Spiny lobsters” (P. interruptus), and “Other taxa” (M. califor- during 2012–2018 to better characterize the impacts of fishing on nica (Brandt, 1835), M. crenulata (Sowerby, 1825), N. norrisii (Sowerby, the excretion rates of this important predator. 1825), S. montereyensi (Dall, 1872), K. kelletii (Forbes, 1850), M. undosa Model prediction uncertainty was propagated into our final ex- (Wood, 1828), and A. sola). Both values were averaged across sites cretion rate estimates using a Monte Carlo procedure. Simulated within each year of the time series. Species in “Other taxa” supplied + species-specific model coefficients and their 95% confidence inter- <10% of total NH4 excretion and total biomass of invertebrates each vals were used to calculate per capita ammonium excretion rates year. Although we assessed the annual variability of areal N excretion 1,000 times at each site. Per capita rates were then converted to and standing biomass of each species (Appendices S2 and S3), we areal rates by multiplying by the density of each species. This Monte performed subsequent analyses of CND on these five groups. Carlo approach allowed us to propagate error in predicting individual We characterized kelp forest CND at the regional scale by assessing + rates into our estimates of mean areal N excretions for each species. the temporal variability of areal NH4 excretion and standing biomass We used the standard deviation of these values, which are normally of each functional group. Linear mixed models (LMMs) were fitted + distributed, to calculate the standard error of areal N excretion es- with either areal NH4 excretion/standing biomass as the response, timates. Monte Carlo iterations and modeling procedures were per- survey year as the explanatory variable, and sites included as a ran- formed using the arm package (Gelman & Hill, 2007) in R (R Core dom term to account for repeated sampling over time (lme4 package; Team, 2018). Bates, Mächler, Bolker, & Walker, 2014). We tested differences of both PETERS ET al. | 3183 response variables over time with Type-III one-way ANOVAs using 3 | RESULTS Kenward–Roger's method (lmerTest package; Kuznetsova, Brockhoff, & Christensen, 2017). Posthoc Tukey's pairwise contrasts were used to 3.1 | Invertebrate contributions to kelp forest further investigate which years drove differences (emmeans package; recycled nitrogen Lenth, 2018). Areal NH + excretions were square-root-transformed, 4 Mass-specific and per capita (averaged over all sizes) ammonium and biomass was log-transformed prior to model-fitting. Assumptions excretion rates varied substantially among invertebrate species and of normality and homoscedasticity were assessed through visual in- were highest in the California spiny lobster, P. interruptus (Table 1). spection of model residuals. This procedure was also applied to total Mass-specific excretion rates of P. interruptus were approximately areal NH + excretion/total standing biomass to compare interannual 4 two times higher than that of the sea star P. giganteus and approxi- differences among the entire assemblage. mately seven times that of P. miniata, whose excretion rates were We examined how warming, disease, and fishing affected CND the second and third highest. The sea urchins S. purpuratus and M. by comparing areal NH + excretion of each group of species at differ- 4 franciscanus and the boring clams C. ovoidea and P. californica had ent periods during the time series. For this purpose, we categorized relatively low mass-specific excretion rates (Table 1). When aver- the periods of the time series as prewarming (2001–2013), warming aged over the entire study period, areal NH + excretions were high- (2014–2015), and postwarming (2016–2018). Disease outbreaks re- 4 est for P. giganteus and S. purpuratus. Mean areal NH + excretion of sulting in high mortality of sea stars and sea urchins coincided with 4 P. interruptus was approximately three times lower than P. giganteus, the warm period. Therefore, we examined the consequence of dis- due to extremely low biomass densities for the first 13 years of the ease by comparing areal NH + excretions of these species during 4 study (Appendix S2). Collectively, benthic macroinvertebrates sup- warming and postwarming periods to the prewarming period using plied kelp forests in the region with an average total areal N excre- Welch's two-sample t tests of unequal variances. Areal NH + excre- 4 tion of (mean ± SE) 10.9 ± 1.0 µmol NH + m−2 hr−1, with rates ranging tions of P. interruptus, an intensively fished species, were compared 4 between 3.5 and 18.3 µmol NH + m−2 hr−1 over the study period. during the same periods to assess the effects of warming as well as 4 reduced fishing pressures in the two MPA sites between 2012 and 2018. Prior to t tests, areal excretion rates were square-root-trans- 3.2 | Patterns of kelp forest CND formed to meet normality assumptions. Using an ordination procedure, we further examined whether Over the study period, the 14 species that we examined (Table 1) warming, disease, and fishing were associated with major shifts at comprised 85%–97% of the total standing biomass of 84 species the community level. We calculated a Bray–Curtis dissimilarity ma- of benthic macroinvertebrates surveyed. Interannual fluctuations + trix of species-specific areal NH4 excretions, which were normalized in their total mean biomass were substantial (year: F17,68 = 6.7, using Wisconsin square-root transformation (Legendre & Gallagher, p < 0.001; Figure 1a), and declined fourfold from their maximum in 2001). We then used permutational multivariate analysis of variance 2001 to their minimum in 2015 (p < 0.001), which coincided with the (PERMANOVA) to detect changes in community structure across warming event. Fluctuations in the biomass of boring clams and sea sites and years (Anderson, 2017). Yearly differences in the commu- urchins drove these declines, as they comprised ~65% and ~20% of nity supply of recycled ammonium were displayed graphically using a the total biomass, respectively (Figure 1a). Despite their high bio- nonmetric multidimensional scaling plot with convex hulls depicting mass, boring clams contributed, on average, only ~14% of mean total + dispersion among sites. A species biplot was also generated to deter- areal NH4 excretions (Figure 1b), due to their low mass-specific mine correlations between species and ordination axes. Multivariate excretion rates (Table 1). In contrast, urchins contributed ~28% of + analyses and ordinations were conducted using the vegan package total areal NH4 excretions as their mass-specific rates were approx- (Oksanen et al., 2018). imately three times higher than boring clams (Table 1, Figure 1b). + We assessed how warming and the establishment of MPAs at Yet, areal NH4 excretion of urchins fluctuated over the study period + two of our five sites influenced lobster areal NH4 excretions with (year: F17,68 = 7.2, p < 0.001) as there were two periods (2001–2002 a LMM using the 2012–2018 lobster time series. In this analysis, re- and 2009–2014) with relatively high urchin biomass. serve status (MPA vs. non-MPA) and survey year were considered Sea stars and spiny lobsters both comprised <5% of the total fixed factors and site a random effect. We tested overall differences standing biomass of invertebrates (Figure 1a). Despite contributing + in the LMM with a Type-III two-way ANOVA using Satterthwaite's little to overall biomass, interannual patterns of total areal NH4 method (lmerTest package; Kuznetsova et al., 2017). Tukey's pair- excretion were driven primarily by their population dynamics, as wise contrasts were used to determine differences between reserve each group dominated invertebrate regimes of recycled ammonium status and year and their interaction. Lobster excretion rates were during two distinct periods of the study (sea stars: 2003–2013, spiny + square-root-transformed prior to model-fitting. To examine changes lobster: 2016–2018; Figure 1b). Total areal NH4 excretion varied in the population size structure of lobster over time, we fit kernel significantly between years (F17,68 = 6.9, p < 0.001), with rates as high + −2 −1 density estimates of carapace lengths (mm) for MPA and non-MPA as 18.3 ± 3.0 µmol NH4 m hr between 2009 and 2012, a period sites and plotted changes in their size distributions for each year. All when sea stars peaked in biomass and supplied ~60% of the total. + data analyses were performed using R (R Core Team, 2018). Total areal NH4 excretion decreased by ~81% between 2010 and 3184 | PETERS ET al.

(a) FIGURE 1 Annual means (mean ± SE) 5 MPAs Warming of the (a) standing biomass and (b) areal established period ammonium excretions of kelp forest macroinvertebrates averaged across sites 4 (n = 5). Taxa in stacked bars are grouped in order of their contribution to total ) 2 areal excretions. Marine protected areas /m

3 (MPAs) established in 2012 (dashed line). Red band depicts the 2014–2015 warming period [Colour figure can be viewed at

2 wileyonlinelibrary.com] Biomass (wet kg

0 (b) 20 ) 1 h

2 m

15 + 4 mol NH µ 10

5 Areal N excretion ( Areal N excretion

0 20022004 20062008 2010 2012 2014 2016 2018 Year

Other taxa Boring clams Urchins Sea stars Spiny lobsters

2015, as the biomass of sea stars, and subsequently their excretion alterations were not detected until 2016 (prewarming vs. post- + rates, decreased by ~99%. Yet, total areal NH4 excretion increased warming: t = 4.5, p < 0.001, t = 2.8, p < 0.001, t = 2.9, p = 0.00, threefold between 2015 and 2018 as excretions from spiny lobster respectively; Figure 2). Panulirus interruptus was the only species + increased from 21% to 52% of the total (Figure 1b). During this pe- to show a significant increase in areal NH4 excretion rates during riod, we witnessed a 17-fold increase in lobster biomass (F17,68 = 3.2, and after the warming event (t = −2.8, p = 0.01, t = −3.5, p = 0.003, + p < 0.001) and 21-fold increase in their excretion rates (F17,68 = 3.3; respectively; Figure 2). Population-level areal NH4 excretion rates p < 0.001) across all of our sites (Figure 1a,b; Appendices S2 and S3). of boring clams and the seven species that comprised the “other taxa” group did not change appreciably between periods (Figure 2). Following sea star declines, spiny lobsters contributed the most to 3.3 | Effects of warming, disease, and fishing recycled ammonium. Community-level patterns in areal NH + excre- on CND 4 tions corroborate this as a significant shift occurred between 2013 and Impacts of warming and disease were most apparent in the sea stars 2014, coinciding with the onset of the warming event (PERMANOVA: 2 P. giganteus and P. brevispinus, both of which excreted substantial years: F17,68 = 6.0, R = 0.24; p < 0.001), though the magnitude of amounts of ammonium in prewarming years but went functionally community restructuring varied substantially by site (site: F4,68 = 63.7, extinct by 2014 (prewarming vs. warming: t = 4.7, p < 0.001, t = 3.2, R2 = 0.60; p < 0.001; Figure 3a). Relative dispersion between the p = 0.004 respectively, Figure 2). Outbreaks of disease resulted prewarming period (2001–2013) with the warming and postwarm- in declines in the areal excretions of the sea star P. miniata, and ing periods (2014–2018) was high for the two MPA sites (IVEE and the sea urchins S. purpuratus and M. franciscanus but significant NAPL) due to larger increases in lobster abundances following no-take PETERS ET al. | 3185

FIGURE 2 Areal ammonium excretion Prewarming Warming Postwarming rates of common kelp forest invertebrates Pisaster giganteus *** *** in prewarming (2001–2013), during Patiria miniata *** a warming (2014–2015), and postwarming Pisaster brevispinus ****** (2016–2018) years. Data are mean ± SE Panulirus interruptus ** *** averaged across sites and years within Strongylocentrotus purpuratus ** each period. Means during the warming Mesocentrotus franciscanus ** and postwarming periods were contrasted Chaceia ovoidea with those in the prewarming period Parapholas californica using pairwise t tests, and significant Megathura crenulata differences denoted by asterisks Styela montereyensis Muricea californica (***p < 0.001, **p < 0.01, *p < 0.05). Megastraea undosa aPisaster brevispinus areal excretion rates Anthopleura sola were estimated from the Pisaster giganteus Kelletia kelletii excretion model [Colour figure can be Norrisia norrisii viewed at wileyonlinelibrary.com] 1234 1 234 1 234 + 2 1 Areal N excretion (µmol NH4 m h ) protections designated in 2012 (Figure 3a). This effect was most pro- compensated in part by a concomitant increase in the abundance of nounced at IVEE as no lobsters were observed prior to 2012. Regime spiny lobster associated with synergies between warming and re- + shifts from sea stars to lobsters as the dominant NH4 recycler was ap- duced fishing pressure, resulting in a shift in recycled nutrient regimes parent across all sites, despite strong site-to-site variability (Figure 3a). (Figure 5). Climate extremes, disease outbreaks, and fishing pressure Indeed, all three sea star species were correlated with ordination axes increasingly affect coastal ecosystems. Our study provides a novel characterizing the 13 years preceding this event, while P. interrup- decadal-scale perspective of how changes in consumer abundances tus was correlated with the years following (2014–2018; Figure 3b). in response to these processes can affect ecosystem functioning. Further, several invertebrates unaffected by the warming event (e.g., Linked to a densovirus that has been present off the Pacific coast N. norrisii, M. undosa, Figure 2) were also strongly correlated with post- since 1979, the 2013–2015 epidemic of sea star wasting disease warming years, but effects were site-dependent (Figure 3b). (SSWD) was unprecedented in magnitude and scale given the num- While there were substantial yearly increases in areal N excre- ber of species affected and its broad geographical extent (Hewson et tion by lobsters since 2012, there were no prominent differences al., 2014). Although there is no strong evidence linking elevated sea- between MPAs and non-MPAs (two-way ANOVA: reserve status: water temperatures with the emergence of SSWD along the North

F1,3 = 0.22, p = 0.7; year: F6,18 = 8.0, p < 0.001; reserve status × year: Pacific Coast (Miner et al., 2018), anomalously warm ocean tempera-

F6,18 = 2.3, p = 0.08; Figure 4a). However, yearly changes in lobster tures have been implicated as the cause for sustaining its spread and population size structure were different between MPA and non- mortality rate in sea stars (Eisenlord et al., 2016) and are consistent MPAs, as more large-sized individuals were observed at MPAs in with temporal patterns observed at our sites (Reed, Washburn, et most years following designation (Figure 4b; note that 2012 data al., 2016). Before the onset of the 2014 warming period, sea star were collected before the fishing season in the year MPAs were es- populations were increasing in kelp forests along the Santa Barbara tablished). In 2014, we observed high densities of juvenile lobsters in coast. Yet, by 2015, their densities had declined to near zero. Mass MPA sites. Interestingly, in 2015, more small lobsters were observed mortalities of sea stars could have wide-reaching implications for at non-MPA sites than MPA sites. trophic dynamics and mediation of regime shifts through top-down control (Bonaviri, Graham, Gianguzza, & Shears, 2017; Burt et al., 2018; Menge et al., 2016). Our study highlights how sea stars may 4 | DISCUSSION also serve as “keystone recyclers” (Small, Pringle, Pyron, & Duff, 2011), further defining their role in regulating ecosystem processes. Our study revealed the impacts of climate anomalies, disease, and fish- Overfishing has important implications for coastal ecosystems ing pressure on kelp forest consumers and links changes in commu- as widespread removal of consumers disrupts trophic interactions nity composition with a regionwide shift in CND. Reef invertebrates (Dayton et al., 1998), reduces food web complexity (Jackson, 2001), contribute substantial amounts of ammonium to kelp forests through and restructures top-down regulation of primary producers (Tegner, their excretions; however, changes in the consumer community fol- 2000). Removing consumers also alters the supply and storage of lowing these events fundamentally altered this ecosystem function. nutrients, which are integral to energy flow in ecosystems (Allgeier Following a 2-year warming period coupled with disease outbreaks et al., 2017). Much of our knowledge of how fishing pressure impacts affecting sea stars and sea urchins, inputs of excreted ammonium ecosystems is inferred from the recovery of degraded states follow- from reef macroinvertebrates decreased by ~80%. Prior to their de- ing designation of no-take marine reserves (Cheng, Altieri, Torchin, mise, sea stars accounted for up to 62% of the ammonium excreted & Ruiz, 2019; Lester et al., 2009). Worldwide, species of spiny lob- by invertebrates. Yet the loss of this source of recycled nitrogen was ster have experienced significant population recoveries following 3186 | PETERS ET al.

(a) FIGURE 3 Nonmetric 0.8 2D Stress: 0.17 multidimensional scaling plots depicting 2D Stress: 0.17 (a) yearly assemblage-wide shifts in areal MPA non MPA ammonium excretion among sites and (b) family-level associations in excretion rates. Magnitude and direction of vectors 0.4 indicate strength of correlation with ordination axes [Colour figure can be NAPL viewed at wileyonlinelibrary.com] AQUE 0.0 MOHK IVEE CARP

NMDS2 0.4 Year 2018

2013 0.8 2008

2003

1.2 (b) 0.8

P. miniata P. giganteus 0.4 P. brevispinus S. montereyensis

M. franciscanus 0.0 M. californica K. kelletii M. crenulata S. purpuratus P. californica C. ovoidea A. sola NMDS2 0.4

M. undosa N. norrisii 0.8

P. interruptus 1.2 1.0 0.5 0.0 0.5 1.0 NMDS1 protections via no-take reserves (Goñi et al., 2006; Kelly et al., 2000; Ruíz-Chavarría, González-Armas, Durazo, & Guzmán-del Proó, 2015) Lipcius et al., 2001). In California, populations of P. interruptus had as indicated by the high densities of juvenile lobsters recorded in our been severely reduced by commercial and recreational fishing pres- surveys during summer 2014. Lobsters serve an important trophic sures (Kay, Lenihan, Guenther, et al., 2012). Following the desig- role in kelp forests by regulating populations of sea urchins whose nation of a network of no-take reserves in California in 2012, and grazing can eliminate entire stands of kelp and associated understory the 2014–2015 warming event, we witnessed a 58-fold increase in algae (Breen & Mann, 1976; Ling et al., 2009; Shears & Babcock, lobster biomass across our sites, even in unprotected areas. This re- 2002). Our finding that lobsters excrete more nitrogen per gram of gionwide increase likely reflects synergies between increased pro- biomass than any other invertebrate in our study, with rates similar tections from fishing (Ling et al., 2009) and favorable conditions for to kelp forest fish (Bray et al., 1988, 1986), suggests they also have recruitment and growth associated with warming (Funes-Rodríguez, an important bottom-up role in kelp forest nutrient cycling. During PETERS ET al. | 3187

FIGURE 4 Annual trends in Palinurus interupptus (a) ammonium excretion (a) rates and (b) population size structures 10.0 (carapace length in mm) at marine protected area (MPA) and non-MPA ) sites following MPA designation. Values 1 MPA h

are means averaged over sites with the 2 non MPA

same MPA designation. Error bars in (a) m 7.5 represent ± 1 SE. Dashed line in panel B + 4 depicts the legal carapace length for take (83 mm) [Colour figure can be viewed at mol NH wileyonlinelibrary.com] µ 5.0

2.5 Areal N excretion ( Areal N excretion

0.0 (b) 2012 2013 2014 2015 2016 2017 2018 200

175 1

1 150

1 125

100

75 Carapace length (mm) 50

0.00 0.02 0.04 0.00 0.02 0.04 0.00 0.02 0.04 0.00 0.02 0.04 0.00 0.02 0.04 0.00 0.02 0.04 0.00 0.02 0.04 Density

our study, lobsters replaced sea stars as the dominant invertebrate Giant kelp has a limited capacity to store N (Gerard, 1982a), and its nitrogen recycler and are on a trajectory to fully compensate for the growth in southern California is sustained only when ambient N con- loss of ammonium recycled by sea stars. Predators with high mass- centrations are >1 µM (Gerard, 1982b). The supply of nitrate via up- specific excretion rates in other systems may also serve as keystone welling to our study sites off Santa Barbara easily meets these demands recyclers and widescale reductions in their biomass from global during winter and spring (McPhee-Shaw et al., 2007). Yet the growth change drivers, like those reported in our study, will undoubtedly and productivity of giant kelp and benthic understory algae are often reduce their contribution to bottom-up processes (Hammerschlag as high during summer and fall when available nitrate consistently falls et al., 2019; Schmitz et al., 2010). below 1 µM (Brzezinksi et al., 2013; Harrer, Reed, Miller, & Holbrook, Ammonium is one of the most available forms of nitrogen for ma- 2013; Rassweiler, Reed, Harrer, & Nelson, 2018). Our results show that rine primary producers (Mulholland & Lomas, 2008) and is readily taken benthic consumers supply substantial amounts of ammonium to kelp up by M. pyrifera (Bray et al., 1986; Hepburn & Hurd, 2005) and under- forests, and their excretion may be particularly important for primary story macroalgae (Haines & Wheeler, 1978; Pritchard, Hurd, Beardall, & production by reef macrophytes during the summer when available Hepburn, 2015; Thomas & Harrison, 1987; Young, Berges, & Dring, 2009). nitrate is low. 3188 | PETERS ET al.

FIGURE 5 Conceptual diagram depicting shifts in recycled nutrient regimes following the 2014–2015 Prewarming nutrient regime: Postwarming nutrient regime: + –2 –1 6 µmol NH + m–2h–1 13 µmol NH4 m h 4 warming period and designation of marine protected areas in 2012. Group percentages comprise the mean total Other taxa: 9% Other taxa: 12% areal ammonium excretion for pre- and postwarming periods [Colour figure can Sea stars: 50% Sea stars: 1% be viewed at wileyonlinelibrary.com]

Boring clams: 14% Boring clams: 18%

Spiny lobster: 1% Urchins: 26% Spiny lobster: 46% Urchins: 23%

Research in kelp forests (Bray et al., 1988, 1986; Hepburn & that lead to variability in excretion rates by consumers such as diet Hurd, 2005) and temperate tidepools (Bracken, Dolecal, & Long, switching, feeding rate, time of day, and ambient water temperature 2014; Bracken & Nielsen, 2004) has shown that consumers enhance (Allgeier, Wenger, Rosemond, Schindler, & Layman, 2015). For ex- nutrient cycling and primary production. Bray et al. (1988) found ample, the extended warming event may have resulted in increased that benthic macroinvertebrates and fishes collectively supplied rates of N recycling in many species due to higher metabolic rates in + −2 −1 25–30 µmol NH4 m hr in kelp forests off Catalina Island, CA, these ectotherms. Additional research is needed to determine how similar to rates supplied by macroinvertebrates in our study system. these factors alter the supply of locally regenerated nitrogen to af- Similarly, mesozooplankton in temperate regions excrete between fect bottom-up processes in reef ecosystems. + −2 −1 29 and 45 µmol NH4 m hr (Hernández-León, Fraga, & Ikeda, Climate- and human-driven regime shifts are common in aquatic 2008). By comparison, measurements of excretion by reef fish in (Daskalov, Grishin, Rodionov, & Mihneva, 2007; deYoung et al., + −2 −1 tropical systems ranged between 82 and 96 µmol NH4 m hr 2008; Pessarrodona et al., 2019) and terrestrial (Ripple & Beschta, (Allgeier et al., 2013; Burkepile et al., 2013). Generally, excretion 2006; Romme et al., 2011) consumer communities, often resulting in rates from temperate and tropical reef macrofauna range between alteration of important ecosystem functions via modification of top- + −2 −1 10 and 500 µmol NH4 m hr (Bronk & Steinberg, 2008). Inputs down and bottom-up processes (Andersen, Carstensen, Hernández- of recycled nitrogen from sea birds and marine mammals can ex- García, & Duarte, 2009). Our study is unique in that it highlights how ceed this range (Roman & McCarthy, 2010) and are likely important anthropogenic defaunation can shift regimes of recycled nutrients sources for kelp forests, particularly those offshore from breed- and disrupt CND over annual or decadal scales. Many conclusions ing colonies and haul out areas (Bokhorst, Convey, & Aerts, 2019; about the importance of CND are based on studies taking place over Otero, Peña-Lastra, Pérez-Alberti, Ferreira, & Huerta-Diaz, 2018). one or two field seasons (Allgeier et al., 2013; Burkepile et al., 2013), Our estimates of invertebrate excretions seem low in comparison, which do not effectively characterize natural variation in consumer but they are based on an 18-year average estimated from a diverse populations or capture important disturbance events that impact array of sites that more appropriately depict temporal and spatial consumer communities. Indeed, we saw several major alterations to heterogeneity in animal biomass and therefore average rates of ex- CND in kelp forests over the course of this study and these tran- cretion. Indeed, total reef excretion rates had tremendous spatial sitions between different consumer regimes over time likely occur + −2 −1 variability with rates between 0.06 and 58.6 µmol NH4 m hr . in ecosystems worldwide (Folke et al., 2004). Extreme temperature And excretion rates in a given plot can vary by 20-fold over an 18- events, disease, and other global-scale impacts have widespread year period. negative impacts on consumer populations (Bellard, Bertelsmeier, We focused our study on benthic macroinvertebrates because Leadley, Thuiller, & Courchamp, 2012; Harvell et al., 2002; Smale they comprised the majority of animal biomass on reefs at our sites et al., 2019). Management practices such as the creation of MPAs (Miller, Page, & Reed, 2015; Reed, Nelson, et al., 2016), and as reef may help to minimize these impacts by reducing local losses to fish- residents, they have the potential to provide a consistent source of ing and enhancing spill over (via propagule supply or adult move- nitrogen to kelp forests. Similar to Bray et al. (1988), we hypothesize ment) into fished areas to increase regional abundances (Goñi et al., that hydrodynamic processes restrict the availability of ammonium 2006; Kay, Lenihan, Kotchen, & Miller, 2012; Lester et al., 2009). It is regenerated by benthic invertebrates to supporting primary produc- widely recognized that consumer regime shifts arising from environ- tion occurring on or near the benthos. The results from our 18-year mental change and human actions alter top-down control (Daskalov time series show that macroinvertebrates consistently provide am- et al., 2007; deYoung et al., 2008; Pessarrodona et al., 2019; Ripple monium to reef primary producers over a wide range of environmen- & Beschta, 2006; Romme et al., 2011). Our study is one of the first to tal conditions. However, we were unable to capture some factors demonstrate that they also impact inputs of limited nutrients needed PETERS ET al. | 3189 to sustain primary production. More data that describe shifts in the Bokhorst, S., Convey, P., & Aerts, R. (2019). Nitrogen inputs by marine regimes of recycled nutrients in other systems are needed to predict vertebrates drive abundance and richness in Antarctic terrestrial ecosystems. Current Biology, 29(10), 1721–1727.e3. https ://doi. how these impacts alter the functioning of natural systems and their org/10.1016/j.cub.2019.04.038 ecosystem services in a rapidly changing world. Bonaviri, C., Graham, M., Gianguzza, P., & Shears, N. T. (2017). Warmer temperatures reduce the influence of an important keystone predator. Journal of Animal Ecology, 86(3), 490–500. https://doi. ACKNOWLEDGEMENTS org/10.1111/1365-2656.12634 We thank the numerous graduate and undergraduate student volun- Bond, N. A., Cronin, M. F., Freeland, H., & Mantua, N. (2015). Causes and impacts of the 2014 warm anomaly in the NE Pacific. Geophysical teers who assisted data collection for this project. We owe special Research Letters, 42(9), 3414–3420. https ://doi.org/10.1002/2015G thanks to K. Munsterman, K. Landfield, J. Allgeier, C. Nelson, S. Harrer, L063306 L. Kui, and R. Miller for their suggestions with field logistics, experi- Bracken, M. E. S., Dolecal, R. E., & Long, J. D. (2014). Community mental design, and data analysis. We are also grateful to three anon- context mediates the top-down vs. bottom-up effects of graz- ers on rocky shores. Ecology, 95(6), 1458–1463. https ://doi. ymous reviewers whose comments improved the manuscript. This org/10.1890/13-2094.1 research was supported by the U.S. National Science Foundation's Bracken, M. E. S., & Nielsen, K. J. (2004). Diversity of intertidal macroal- Long-Term Ecological Research Program (OCE 9982105, 0620276, gae increases with nitrogen loading by invertebrates. Ecology, 85(10), & 1232779), by NSF CAREER Grant OCE-1547952 to D.E.B., and 2828–2836. https ://doi.org/10.1890/03-0651 Bray, R. N., Miller, A. C., Johnson, S., Krause, P. R., Robertson, D. L., & through the UC Santa Barbara Associated Students Coastal Fund Westcott, A. M. (1988). Ammonium excretion by macroinvertebrates to J.R.P. Images of species utilized in figures were provided as a and fishes on a subtidal rocky reef in southern California. 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