Long-term marine protection enhances kelp forest ecosystem stability.

Trophic downgrading destabilizes ecosystems and can drive large-scale shifts in ecosystem state. While restoring predatory interactions in marine reserves can reverse anthropogenic-driven shifts, empirical evidence of increased ecosystem stability and persistence in the presence of predators is scant. We compared temporal variation in rocky reef ecosystem state in New Zealand's oldest marine reserve to nearby fished reefs to examine whether protection of predators led to more persistent and stable reef ecosystem states in the marine reserve. Contrasting ecosystem states were found between reserve and fished sites, and this persisted over the 22-year study period. Fished sites were predominantly urchin barrens but occasionally fluctuated to short-lived turfs and mixed algal forests, while reserve sites displayed unidirectional successional trajectories toward stable kelp forests (Ecklonia radiata) taking up to three decades following protection. This provides empirical evidence that long-term protection of predators facilitates kelp forest recovery, resists shifts to denuded alternate states, and enhances kelp forest stability.

Marine heat waves drive bleaching and necrosis of temperate sponges.

Marine heat waves (MHWs) are extended periods of excessively warm water1 that are increasing in frequency, duration, intensity, and impact, and they likely represent a greater threat to marine ecosystems than the more gradual increases in sea surface temperature.2,3,4 Sponges are major and important components of global benthic marine communities,5,6,7 with earlier studies identifying tropical sponges as potential climate change "winners."8,9,10,11 In contrast, cold-water sponges may be less tolerant to predicted ocean warming and concurrent MHWs. Here, we report how a series of unprecedented MHWs in New Zealand have impacted millions of sponges at a spatial scale far greater than previously reported anywhere in the world. We reported sponge tissue necrosis12 and bleaching (symbiont loss/dysfunction),13 which have been previously associated with temperature stress,6,12,14 for three common sponge species across multiple biogeographical regions, with the severity of impact being correlated with MHW intensity. Given the ecological importance of sponges,15 their loss from these rocky temperate reefs will likely have important ecosystem-level consequences.

Coastal darkening substantially limits the contribution of kelp to coastal carbon cycles.

Macroalgal-dominated habitats are rapidly gaining recognition as important contributors to marine carbon cycles and sequestration. Despite this recognition, relatively little is known about the production and fate of carbon originating from these highly productive ecosystems, or how anthropogenic- and climate-related stressors affect the role of macroalgae in marine carbon cycles. Here, we examine the impact of increasing turbidity on carbon storage, fixation and loss in southern hemisphere kelp forests. We quantified net primary production (NPP) and biomass accumulation (BA), and estimated carbon release via detritus and dissolved organic carbon (DOC) across a large-scale turbidity gradient. We show that increased turbidity, resulting in a 63% reduction in light, can result in a 95% reduction in kelp productivity. When averaged annually, estimates of NPP and BA per plant at high-light sites were nearly six and two times greater than those at low-light sites, respectively. Furthermore, the quantity of carbon fixed annually by kelp forests was up to 4.7 times greater than that stored as average annual standing stock. At low-light sites, the majority of C goes directly into tissue growth and is subsequently eroded. In contrast, excess production at high-light sites accounts for up to 39% of the total carbon fixed and is likely released as DOC. Turbidity is expected to increase in response to climate change and our results suggest this will have significant impacts on the capacity of kelp forests to contribute to carbon sequestration pathways. In addition to demonstrating that turbidity significantly reduces the quantity of carbon fixed by kelp forests, and subsequently released as detritus, our results highlight the negative impacts of turbidity on a large source of previously unaccounted for carbon.

Grazer behaviour can regulate large-scale patterning of community states.

Ecosystem patterning can arise from environmental heterogeneity, biological feedbacks that produce multiple persistent ecological states, or their interaction. One source of feedbacks is density-dependent changes in behaviour that regulate species interactions. By fitting state-space models to large-scale (~500 km) surveys on temperate rocky reefs, we find that behavioural feedbacks best explain why kelp and urchin barrens form either reef-wide patches or local mosaics. Best-supported models in California include feedbacks where starvation intensifies grazing across entire reefs create reef-scale, alternatively stable kelp- and urchin-dominated states (32% of reefs). Best-fitting models in New Zealand include the feedback of urchins avoiding dense kelp stands that can increase abrasion and predation risk, which drives a transition from shallower urchin-dominated to deeper kelp-dominated zones, with patchiness at 3-8 m depths with intermediate wave stress. Connecting locally studied processes with region-wide data, we highlight how behaviour can explain community patterning and why some systems exhibit community-wide alternative stable states.

Seasonal and spatial variation in photosynthetic response of the kelp Ecklonia radiata across a turbidity gradient.

Understanding the photoacclimation response of macroalgae across broad spatial and temporal scales is necessary for predicting their vulnerability to environmental changes and quantifying their contribution to coastal primary production. This study investigated how the photosynthesis-irradiance response and photosynthetic pigment content of the kelp Ecklonia radiata varies both spatially and seasonally among seven sites located across a turbidity gradient in the Hauraki Gulf, north-eastern New Zealand. Photosynthesis-irradiance curves were derived under laboratory conditions for whole adult E. radiata using photorespirometry chambers. Lab-derived photosynthesis-irradiance curves in summer were also compared with in situ measurements made on kelp at each of the seven study sites. Photosynthetic parameters and pigments showed clear seasonal patterns across all sites as demonstrated by higher photosynthetic pigment levels and photosynthetic efficiency occurring in autumn and winter, and higher maximum rates of photosynthesis and respiration occurring in summer. Lamina biomass was similar across sites, yet thalli exhibited a clear photokinetic response to increasing turbidity. At turbid sites photosynthetic pigment levels and photosynthetic efficiency was higher, and respiration and saturation and compensation irradiances lower, compared to high-light sites. The results presented here further our understanding of low-light acclimation strategies in kelp and highlight the degree of seasonality in photosynthetic parameters. Though E. radiata demonstrates a clear capacity to photoacclimate to a degrading light environment, further research is needed to investigate the extent to which the observed acclimation can offset the likely negative effects of increasing turbidity on kelp forest primary production.

Quality of a fished resource: Assessing spatial and temporal dynamics.

Understanding spatio-temporal variability in the demography of harvested species is essential to improve sustainability, especially if there is large geographic variation in demography. Reproductive patterns commonly vary spatially, which is particularly important for management of "roe"-based fisheries, since profits depend on both the number and reproductive condition of individuals. The red sea urchin, Mesocentrotus franciscanus, is harvested in California for its roe (gonad), which is sold to domestic and international sushi markets. The primary driver of price within this multi-million-dollar industry is gonad quality. A relatively simple measure of the fraction of the body mass that is gonad, the gonadosomatic index (GSI), provides important insight into the ecological and environmental factors associated with variability in reproductive quality, and hence value within the industry. We identified the seasonality of the reproductive cycle and determined whether it varied within a heavily fished region. We found that fishermen were predictable both temporally and spatially in collecting urchins according to the reproductive dynamics of urchins. We demonstrated the use of red sea urchin GSI as a simple, quantitative tool to predict quality, effort, landings, price, and value of the fishery. We found that current management is not effectively realizing some objectives for the southern California fishery, since the reproductive cycle does not match the cycle in northern California, where these management guidelines were originally shaped. Although regulations may not be meeting initial management goals, the scheme may in fact provide conservation benefits by curtailing effort during part of the high-quality fishing season right before spawning.

Half a century of coastal temperature records reveal complex warming trends in western boundary currents.

Accelerated warming of western boundary currents due to the strengthening of subtropical gyres has had cascading effects on coastal ecosystems and is widely expected to result in further tropicalization of temperate regions. Predicting how species and ecosystems will respond requires a better understanding of the variability in ocean warming in complex boundary current regions. Using three ≥50 year temperature records we demonstrate high variability in the magnitude and seasonality of warming in the Southwest Pacific boundary current region. The greatest rate of warming was evident off eastern Tasmania (0.20 °C decade-1), followed by southern New Zealand (0.10 °C decade-1), while there was no evidence of annual warming in northeastern New Zealand. This regional variability in coastal warming was also evident in the satellite record and is consistent with expected changes in regional-scale circulation resulting from increased wind stress curl in the South Pacific subtropical gyre. Warming trends over the satellite era (1982-2016) were considerably greater than the longer-term trends, highlighting the importance of long-term temperature records in understanding climate change in coastal regions. Our findings demonstrate the spatial and temporal complexity of warming patterns in boundary current regions and challenge widespread expectations of tropicalization in temperate regions under future climate change.

Predators indirectly induce stronger prey through a trophic cascade.

Many prey species induce defences in direct response to predation cues. However, prey defences could also be enhanced by predators indirectly via mechanisms that increase resource availability to prey, e.g. trophic cascades. We evaluated the relative impacts of these direct and indirect effects on the mechanical strength of the New Zealand sea urchin Evechinus chloroticus We measured crush-resistance of sea urchin tests (skeletons) in (i) two marine reserves, where predators of sea urchins are relatively common and have initiated a trophic cascade resulting in abundant food for surviving urchins in the form of kelp, and (ii) two adjacent fished areas where predators and kelps are rare. Sea urchins inhabiting protected rocky reefs with abundant predators and food had more crush-resistant tests than individuals on nearby fished reefs where predators and food were relatively rare. A six-month long mesocosm experiment showed that while both food supply and predator cues increased crush-resistance, the positive effect of food supply on crush-resistance was greater. Our results demonstrate a novel mechanism whereby a putative morphological defence in a prey species is indirectly strengthened by predators via cascading predator effects on resource availability. This potentially represents an important mechanism that promotes prey persistence in the presence of predators.

Warmer temperatures reduce the influence of an important keystone predator.

Predator-prey interactions may be strongly influenced by temperature variations in marine ecosystems. Consequently, climate change may alter the importance of predators with repercussions for ecosystem functioning and structure. In North-eastern Pacific kelp forests, the starfish Pycnopodia helianthoides is known to be an important predator of the purple sea urchin Strongylocentrotus purpuratus. Here we investigated the influence of water temperature on this predator-prey interaction by: (i) assessing the spatial distribution and temporal dynamics of both species across a temperature gradient in the northern Channel Islands, California, and (ii) investigating how the feeding rate of P. helianthoides on S. purpuratus is affected by temperature in laboratory tests. On average, at sites where mean annual temperatures were <14 °C, P. helianthoides were common, S. purpuratus was rare and kelp was persistent, whereas where mean annual temperatures exceeded 14 °C, P. helianthoides and kelp were rare and S. purpuratus abundant. Temperature was found to be the primary environmental factor influencing P. helianthoides abundance, and in turn P. helianthoides was the primary determinant of S. purpuratus abundance. In the laboratory, temperatures >16 °C (equivalent to summer temperatures at sites where P. helianthoides were rare) reduced predation rates regardless of predator and prey sizes, although larger sea urchins were consumed only by large starfishes. These results clearly demonstrate that the effect of P. helianthoides on S. purpuratus is strongly mediated by temperature, and that the local abundance and predation rate of P. helianthoides on sea urchins will likely decrease with future warming. A reduction in top-down control on sea urchins, combined with other expected impacts of climate change on kelp, poses significant risks for the persistence of kelp forests in the future.

Predation cues rather than resource availability promote cryptic behaviour in a habitat-forming sea urchin.

It is well known that predators often influence the foraging behaviour of prey through the so-called "fear effect". However, it is also possible that predators could change prey behaviour indirectly by altering the prey's food supply through a trophic cascade. The predator-sea urchin-kelp trophic cascade is widely assumed to be driven by the removal of sea urchins by predators, but changes in sea urchin behaviour in response to predators or increased food availability could also play an important role. We tested whether increased crevice occupancy by herbivorous sea urchins in the presence of abundant predatory fishes and lobsters is a response to the increased risk of predation, or an indirect response to higher kelp abundances. Inside two New Zealand marine reserves with abundant predators and kelp, individuals of the sea urchin Evechinus chloroticus were rarer and remained cryptic (i.e. found in crevices) to larger sizes than on adjacent fished coasts where predators and kelp are rare. In a mesocosm experiment, cryptic behaviour was induced by simulated predation (the addition of crushed conspecifics), but the addition of food in the form of drift kelp did not induce cryptic behaviour. These findings demonstrate that the 'fear' of predators is more important than food availability in promoting sea urchin cryptic behaviour and suggest that both density- and behaviourally mediated interactions are important in the predator-sea urchin-kelp trophic cascade.

Global patterns of kelp forest change over the past half-century.

Kelp forests (Order Laminariales) form key biogenic habitats in coastal regions of temperate and Arctic seas worldwide, providing ecosystem services valued in the range of billions of dollars annually. Although local evidence suggests that kelp forests are increasingly threatened by a variety of stressors, no comprehensive global analysis of change in kelp abundances currently exists. Here, we build and analyze a global database of kelp time series spanning the past half-century to assess regional and global trends in kelp abundances. We detected a high degree of geographic variation in trends, with regional variability in the direction and magnitude of change far exceeding a small global average decline (instantaneous rate of change = -0.018 y-1). Our analysis identified declines in 38% of ecoregions for which there are data (-0.015 to -0.18 y-1), increases in 27% of ecoregions (0.015 to 0.11 y-1), and no detectable change in 35% of ecoregions. These spatially variable trajectories reflected regional differences in the drivers of change, uncertainty in some regions owing to poor spatial and temporal data coverage, and the dynamic nature of kelp populations. We conclude that although global drivers could be affecting kelp forests at multiple scales, local stressors and regional variation in the effects of these drivers dominate kelp dynamics, in contrast to many other marine and terrestrial foundation species.

Canopy interactions and physical stress gradients in subtidal communities.

Species interactions are integral drivers of community structure and can change from competitive to facilitative with increasing environmental stress. In subtidal marine ecosystems, however, interactions along physical stress gradients have seldom been tested. We observed seaweed canopy interactions across depth and latitudinal gradients to test whether light and temperature stress structured interaction patterns. We also quantified interspecific and intraspecific interactions among nine subtidal canopy seaweed species across three continents to examine the general nature of interactions in subtidal systems under low consumer pressure. We reveal that positive and neutral interactions are widespread throughout global seaweed communities and the nature of interactions can change from competitive to facilitative with increasing light stress in shallow marine systems. These findings provide support for the stress gradient hypothesis within subtidal seaweed communities and highlight the importance of canopy interactions for the maintenance of subtidal marine habitats experiencing environmental stress.

Global conservation outcomes depend on marine protected areas with five key features.

In line with global targets agreed under the Convention on Biological Diversity, the number of marine protected areas (MPAs) is increasing rapidly, yet socio-economic benefits generated by MPAs remain difficult to predict and under debate. MPAs often fail to reach their full potential as a consequence of factors such as illegal harvesting, regulations that legally allow detrimental harvesting, or emigration of animals outside boundaries because of continuous habitat or inadequate size of reserve. Here we show that the conservation benefits of 87 MPAs investigated worldwide increase exponentially with the accumulation of five key features: no take, well enforced, old (>10 years), large (>100 km(2)), and isolated by deep water or sand. Using effective MPAs with four or five key features as an unfished standard, comparisons of underwater survey data from effective MPAs with predictions based on survey data from fished coasts indicate that total fish biomass has declined about two-thirds from historical baselines as a result of fishing. Effective MPAs also had twice as many large (>250 mm total length) fish species per transect, five times more large fish biomass, and fourteen times more shark biomass than fished areas. Most (59%) of the MPAs studied had only one or two key features and were not ecologically distinguishable from fished sites. Our results show that global conservation targets based on area alone will not optimize protection of marine biodiversity. More emphasis is needed on better MPA design, durable management and compliance to ensure that MPAs achieve their desired conservation value.

Toxic cascades: multiple anthropogenic stressors have complex and unanticipated interactive effects on temperate reefs.

In a changing environment multiple anthropogenic stressors can have novel and non-additive effects on interacting species. We investigated the interactive effects of fishing and harmful algal blooms on the predator-sea urchin-macroalgae trophic cascade. Fishing of urchin predators had indirect negative effects on macroalgae, whereas blooms of epi-benthic dinoflagellates (Ostreopsis siamensis) were found to have strong negative effects on urchins and indirect positive effects on macroalgae. Based on these opposing effects, blooms were expected to counteract the cascading effects of fishing. However, a large bloom of Ostreopsis led to greater divergence in macroalgae abundance between reserve and fished sites, as urchins declined at reserve sites but remained stable at fished sites. This resulted from enhanced predation rates on bloom-affected urchins at reserve sites rather than direct lethal effects of Ostreopsis on urchins. We argue that interacting stressors can facilitate or attenuate trophic cascades depending on stressor intensity and complex non-lethal interactions.

Key features and context-dependence of fishery-induced trophic cascades.

Trophic cascades triggered by fishing have profound implications for marine ecosystems and the socioeconomic systems that depend on them. With the number of reported cases quickly growing, key features and commonalities have emerged. Fishery-induced trophic cascades often display differential response times and nonlinear trajectories among trophic levels and can be accompanied by shifts in alternative states. Furthermore, their magnitude appears to be context dependent, varying as a function of species diversity, regional oceanography, local physical disturbance, habitat complexity, and the nature of the fishery itself. To conserve and manage exploited marine ecosystems, there is a pressing need for an improved understanding of the conditions that promote or inhibit the cascading consequences of fishing. Future research should investigate how the trophic effects of fishing interact with other human disturbances, identify strongly interacting species and ecosystem features that confer resilience to exploitation, determine ranges of predator depletion that elicit trophic cascades, pinpoint antecedents that signal ecosystem state shifts, and quantify variation in trophic rates across oceanographic conditions. This information will advance predictive models designed to forecast the trophic effects of fishing and will allow managers to better anticipate and avoid fishery-induced trophic cascades.

Evaluation of biogeographic classification schemes for conservation planning: application to New Zealand's coastal marine environment.

For many regions worldwide, multiple and often contrasting biogeographic classifications exist that are derived from a variety of taxa and techniques. This presents a challenge for managers who must choose appropriate large-scale spatial frameworks for systematic conservation planning. We demonstrate how systematically collected community data can be used to evaluate existing biogeographic classifications, identify the most appropriate metric for biogeographic patterns seen in other taxonomic groups, and develop an independent biogeographic classification scheme for systematic conservation planning. We evaluated 6 existing biogeographic classifications for New Zealand's nearshore marine environment with community-similarity metrics derived from abundance and presence-absence data for macroalgae (107 species) and mobile macroinvertebrates (44 species). The concordance between community metrics and the previous classifications was high, as indicated by a high multivariate classification success (CS) (74.3-98.3%). Subsequently, we carried out an independent classification analysis on each community metric to identify biogeographic units within a hierarchical spatial framework. The classification derived from macroalgal presence-absence data achieved the highest CS and could be used as a mesoscale classification scheme in which 11 regional groupings (i.e., bioregions) (CS = 73.8-84.8%) are nested within northern and southern biogeographic provinces (CS = 90.3-98.7%). These techniques can be used in systematic conservation planning to inform the design of representative and comprehensive networks of marine protected areas through evaluation of the current coverage of marine reserves in each bioregion. Currently, 0.22% of the territorial sea around mainland New Zealand is protected in no-take marine protected areas in which 0-1.5% of each bioregion represented.

Context-dependent effects of fishing: variation in trophic cascades across environmental gradients.

Marine reserves provide a large-scale experimental framework to investigate the effects of fishing on food web dynamics and how they vary with environmental context. Because marine reserves promote the recovery of previously fished predators, spatial comparisons between reserve and fished sites are often made to infer such effects; however, alternative explanations for differences between reserve and fished sites are seldom tested (e.g., environmental variation among sites). We investigated the context dependency of the predator-urchin-kelp trophic cascade reported in northeastern New Zealand by comparing the abundance of herbivorous sea urchins (Evechinus chloroticus), the extent of urchin barrens habitat, and macroalgal biomass between reserve and fished sites within six locations that span an environmental gradient in wave exposure, sedimentation, and water clarity. At depths where differences in urchin abundance or macroalgal biomass were found between reserve and fished sites we used a model selection approach to identify which variables (fishing or environmental factors) best explained the variation among sites. Differences between reserve and fished sites were not ubiquitous across the locations examined and were highly depth specific. At sheltered locations, urchins were rare and barrens absent at both reserve and fished sites. At moderately exposed coastal locations, actively grazing urchins were most abundant at 4-6 m depth, and significant differences in macroalgal biomass between reserve and fished sites were observed. In contrast, at offshore island locations, urchins extended into deeper water, and differences between reserve and fished sites were found at 4-9 m depth. These differences could only be attributed to trophic cascades associated with protection from fishing in two of the six locations examined. In other cases, variation between reserve and fished sites was equally well explained by differences in sediment or wave exposure among sites. These results suggest that trophic cascades are not ubiquitous to northeastern New Zealand's subtidal reefs and the importance of sea urchins, and indirectly predators, in controlling macroalgal biomass will vary at local and regional scales in relation to abiotic factors. A better mechanistic understanding of how environmental variation affects the strength of species interactions across multiple spatial scales is needed to predict the ecosystem-level effects of fishing.

Cascading effects of fishing can alter carbon flow through a temperate coastal ecosystem.

Mounting evidence suggests that fishing can trigger trophic cascades and alter food web dynamics, yet its effects on ecosystem function remain largely unknown. We used the large-scale experimental framework of four marine reserves, spanning an oceanographic gradient in northeastern New Zealand, to test the extent to which the exploitation of reef predators can alter kelp carbon flux and secondary production. We provide evidence that the reduction of predatory snapper (Pagrus auratus) and lobster (Jasus edwardsii) can lead to an increase in sea urchins (Evechinus chloroticus) and indirect declines in kelp biomass in some locations but not others. Stable carbon isotope ratios (delta13C) of oysters (Crassostrea gigas) and mussels (Perna canaliculus) transplanted in reserve and fished sites within four locations revealed that fishing indirectly reduced the proportion of kelp-derived organic carbon assimilated by filter feeders in two locations where densities of actively grazing sea urchins were 23.7 and 8.3 times higher and kelp biomass was an order of magnitude lower than in non-fished reserve sites. In contrast, in the two locations where fishing had no effect on urchin density or kelp biomass, we detected no effect of fishing on the carbon signature of filter feeders. We show that the effects of fishing on nearshore trophic structure and carbon flux are context-dependent and hinge on large-scale, regional oceanographic factors. Where cascading effects of fishing on kelp biomass were documented, enhanced assimilation of kelp carbon did not result in the magnification of secondary production. Instead, a strong regional gradient in filter feeder growth emerged, best predicted by chlorophyll a. Estimates of kelp contribution to the diet of transplanted consumers averaged 56.9% +/- 6.2% (mean +/- SE) for mussels and 33.8% +/- 7.3% for oysters, suggesting that organic carbon fixed by kelp is an important food source fueling northeastern New Zealand's nearshore food webs. The importance of predators in mediating benthic primary production and organic carbon flux suggests that overfishing can have profound consequences on ecosystem functioning particularly where pelagic primary production is limiting. Our results underscore the broader ecosystem repercussions of overfishing and its context-dependent effects.

Marine reserves demonstrate top-down control of community structure on temperate reefs.

Replicated ecological studies in marine reserves and associated unprotected areas are valuable in examining top-down impacts on communities and the ecosystem-level effects of fishing. We carried out experimental studies in two temperate marine reserves to examine these top-down influences on shallow subtidal reef communities in northeastern New Zealand. Both reserves examined are known to support high densities of predators and tethering experiments showed that the chance of predation on the dominant sea urchin, Evechinus chloroticus, within both reserves was approximately 7 times higher relative to outside. Predation was most intense on the smallest size class (30-40 mm) of tethered urchins, the size at which urchins cease to exhibit cryptic behaviour. A high proportion of predation on large urchins could be attributed to the spiny lobster, Jasus edwardsii. Predation on the smaller classes was probably by both lobsters and predatory fish, predominantly the sparid Pagrus auratus. The density of adult Evechinus actively grazing the substratum in the urchin barrens habitat was found to be significantly lower at marine reserve sites (2.2±0.3 m-2) relative to non-reserve sites (5.5±0.4 m-2). There was no difference in the density of cryptic juveniles between reserve and non-reserve sites. Reserve populations were more bimodal, with urchins between 40 and 55 mm occurring at very low numbers. Experimental removal of Evechinus from the urchin barrens habitat over 12 months lead to a change from a crustose coralline algal habitat to a macroalgal dominated habitat. Such macroalgal habitats were found to be more extensive in both reserves, where urchin densities were lower, relative to the adjacent unprotected areas that were dominated by urchin barrens. The patterns observed provide evidence for a top-down role of predators in structuring shallow reef communities in northeastern New Zealand and demonstrate how marine reserves can reverse the indirect effects of fishing and re-establish community-level trophic cascades.