Dan A. Smale

The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts

Climate-driven changes in biotic interactions can profoundly alter ecological communities, particularly when they impact foundation species. In marine systems, changes in herbivory and the consequent loss of dominant habitat forming species can result in dramatic community phase shifts, such as from coral to macroalgal dominance when tropical fish herbivory decreases, and from algal forests to ‘barrens’ when temperate urchin grazing increases. Here, we propose a novel phase-shift away from macroalgal dominance caused by tropical herbivores extending their range into temperate regions. We argue that this phase shift is facilitated by poleward-flowing boundary currents that are creating ocean warming hotspots around the globe, enabling the range expansion of tropical species and increasing their grazing rates in temperate areas. Overgrazing of temperate macroalgae by tropical herbivorous fishes has already occurred in Japan and the Mediterranean. Emerging evidence suggests similar phenomena are occurring in other temperate regions, with increasing occurrence of tropical fishes on temperate reefs.

Climate-driven regime shift of a temperate marine ecosystem

No turning back? Ecosystems over time have endured much disturbance, yet they tend to remain intact, a characteristic we call resilience. Though many systems have been lost and destroyed, for systems that remain physically intact, there is debate as to whether changing temperatures will result in shifts or collapses. Wernburg et al. show that extreme warming of a temperate kelp forest off Australia resulted not only in its collapse, but also in a shift in community composition that brought about an increase in herbivorous tropical fishes that prevent the reestablishment of kelp. Thus, many systems may not be resilient to the rapid climate change that we face. Science, this issue p. 169 Rapid warming tropicalizes a temperate kelp forest. Ecosystem reconfigurations arising from climate-driven changes in species distributions are expected to have profound ecological, social, and economic implications. Here we reveal a rapid climate-driven regime shift of Australian temperate reef communities, which lost their defining kelp forests and became dominated by persistent seaweed turfs. After decades of ocean warming, extreme marine heat waves forced a 100-kilometer range contraction of extensive kelp forests and saw temperate species replaced by seaweeds, invertebrates, corals, and fishes characteristic of subtropical and tropical waters. This community-wide tropicalization fundamentally altered key ecological processes, suppressing the recovery of kelp forests.

Extreme climatic event drives range contraction of a habitat-forming species

Species distributions have shifted in response to global warming in all major ecosystems on the Earth. Despite cogent evidence for these changes, the underlying mechanisms are poorly understood and currently imply gradual shifts. Yet there is an increasing appreciation of the role of discrete events in driving ecological change. We show how a marine heat wave (HW) eliminated a prominent habitat-forming seaweed, Scytothalia dorycarpa, at its warm distribution limit, causing a range contraction of approximately 100 km (approx. 5% of its global distribution). Seawater temperatures during the HW exceeded the seaweeds physiological threshold and caused extirpation of marginal populations, which are unlikely to recover owing to life-history traits and oceanographic processes. Scytothalia dorycarpa is an important canopy-forming seaweed in temperate Australia, and loss of the species at its range edge has caused structural changes at the community level and is likely to have ecosystem-level implications. We show that extreme warming events, which are increasing in magnitude and frequency, can force step-wise changes in species distributions in marine ecosystems. As such, return times of these events have major implications for projections of species distributions and ecosystem structure, which have typically been based on gradual warming trends.

Threats and knowledge gaps for ecosystem services provided by kelp forests: a northeast Atlantic perspective

Kelp forests along temperate and polar coastlines represent some of most diverse and productive habitats on the Earth. Here, we synthesize information from >60 years of research on the structure and functioning of kelp forest habitats in European waters, with particular emphasis on the coasts of UK and Ireland, which represents an important biogeographic transition zone that is subjected to multiple threats and stressors. We collated existing data on kelp distribution and abundance and reanalyzed these data to describe the structure of kelp forests along a spatial gradient spanning more than 10° of latitude. We then examined ecological goods and services provided by kelp forests, including elevated secondary production, nutrient cycling, energy capture and flow, coastal defense, direct applications, and biodiversity repositories, before discussing current and future threats posed to kelp forests and identifying key knowledge gaps. Recent evidence unequivocally demonstrates that the structure of kelp forests in the NE Atlantic is changing in response to climate- and non-climate-related stressors, which will have major implications for the structure and functioning of coastal ecosystems. However, kelp-dominated habitats along much of the NE Atlantic coastline have been chronically understudied over recent decades in comparison with other regions such as Australasia and North America. The paucity of field-based research currently impedes our ability to conserve and manage these important ecosystems. Targeted observational and experimental research conducted over large spatial and temporal scales is urgently needed to address these knowledge gaps.

Ice scour disturbance in Antarctic waters

The West Antarctic Peninsula is one of the fastest warming regions on Earth, and, as a consequence, most maritime glaciers and ice shelves in the region have significantly retreated over the past few decades. We collected a multiyear data set on ice scouring frequency from Antarctica by using unique experimental markers and scuba diving surveys. We show that the annual intensity of ice scouring is negatively correlated with the duration of the winter fast ice season. Because fast ice extent and duration is currently in decline in the region after recent rapid warming, it is likely that marine benthic communities are set for even more scouring in the near future.

Large-Scale Geographic Variation in Distribution and Abundance of Australian Deep-Water Kelp Forests

Despite the significance of marine habitat-forming organisms, little is known about their large-scale distribution and abundance in deeper waters, where they are difficult to access. Such information is necessary to develop sound conservation and management strategies. Kelps are main habitat-formers in temperate reefs worldwide; however, these habitats are highly sensitive to environmental change. The kelp Ecklonia radiate is the major habitat-forming organism on subtidal reefs in temperate Australia. Here, we provide large-scale ecological data encompassing the latitudinal distribution along the continent of these kelp forests, which is a necessary first step towards quantitative inferences about the effects of climatic change and other stressors on these valuable habitats. We used the Autonomous Underwater Vehicle (AUV) facility of Australia’s Integrated Marine Observing System (IMOS) to survey 157,000 m2 of seabed, of which ca 13,000 m2 were used to quantify kelp covers at multiple spatial scales (10–100 m to 100–1,000 km) and depths (15–60 m) across several regions ca 2–6° latitude apart along the East and West coast of Australia. We investigated the large-scale geographic variation in distribution and abundance of deep-water kelp (>15 m depth) and their relationships with physical variables. Kelp cover generally increased with latitude despite great variability at smaller spatial scales. Maximum depth of kelp occurrence was 40–50 m. Kelp latitudinal distribution along the continent was most strongly related to water temperature and substratum availability. This extensive survey data, coupled with ongoing AUV missions, will allow for the detection of long-term shifts in the distribution and abundance of habitat-forming kelp and the organisms they support on a continental scale, and provide information necessary for successful implementation and management of conservation reserves.

Ecological observations associated with an anomalous warming event at the Houtman Abrolhos Islands, Western Australia

Coral reefs and kelp beds are two of the most ecologically and economically important marine habitats on Earth. Coral reefs and kelp beds are usually biogeographically distinct, being associated with tropical and temperate to subpolar areas, respectively. However, at the Houtman Abrolhos Islands (28 43¢ 0† S, 113 47¢ 0† E), a group of small limestone protrusions some 60 km off Western Australia (WA), coral reefs and kelp beds are juxtaposed (Smale et al. 2010) (Fig. 1a). This unusual constellation is likely conditioned by the long environmental stability and unique oceanography of the region. The Houtman Abrolhos Islands experienced a marine ‘heat wave’ in 2011 driven, in part, by strong La Niña conditions, which increased the poleward flow of warm water along the coastline of WA (Pearce et al. 2011). Satellite-derived SSTs off WA were the highest on record during the event, while at the Houtman Abrolhos Islands temperature peaked at 28.7 C on March 1; 5 C higher than the long-term monthly mean (Pearce et al. 2011). Surveys of coral reefs and kelp beds (>5,600 m) were conducted with an AUV in April 2011 at multiple sites, between 15 and 25 m depth. Image analysis revealed extensive bleaching (up to 20% of coral cover per site), primarily of Montipora spp (Fig. 1b). Widespread coral bleaching has not been reported from this system previously, even during exposure at spring tides and during the global bleaching event of 1998 (Webster et al. 2002), and no bleaching was observed in previous AUV surveys. Furthermore, extensive epibiosis of the kelp Ecklonia radiata (most likely by encrusting coralline algae) was observed adjacent to bleached coral (Fig. 1c), which has also not been reported before and may be associated with elevated temperatures. The islands represent a temperate–tropical transition zone, with many key species found at the edge of their ranges, so that marine communities here may act as important indicators of climatic change.

From fronds to fish: the use of indicators for ecological monitoring in marine benthic ecosystems, with case studies from temperate Western Australia

Ecological indicators are used for monitoring in marine habitats the world over. With the advent of Ecosystem Based Fisheries Management (EBFM), the need for cost effective indicators of environmental impacts and ecosystem condition has intensified. Here, we review the development, utilisation and analysis of indicators for monitoring in marine benthic habitats, and outline important advances made in recent years. We use the unique, speciose benthic system of Western Australia (WA) as a detailed case study, as the development of indicators for EBFM in this region is presently ongoing, and major environmental drivers (e.g. climate change) and fishing practices are currently influencing WA marine systems. As such, the work is biased towards, but not restricted to, indicators that may be important tools for EBFM, such as biodiversity surrogates and indicators of fishing pressure. The review aimed to: (1) provide a concise, up-to-date account of the use of ecological indicators in marine systems; (2) discuss the current, and potential, applications of indicators for ecological monitoring in WA; and (3) highlight priority areas for research and pressing knowledge gaps. We examined indicators derived from benthic primary producers, benthic invertebrates and fish to achieve these goals.

Climate-driven shifts in species' distributions may exacerbate the impacts of storm disturbances on North-east Atlantic kelp forests

Physical disturbance through wave action is a major determinant of kelp forest structure. The North-east Atlantic storm season of 2013–14 was unusually severe; the south coast of the UK was subjected to 6 of the 12 most intense storms recorded in the past 5 years. Inshore significant wave heights and periods exceeded 7m and 13s with two storms classified as ‘1-in-30 year’ events. We examined the impacts of the storm season on kelp canopies at three study sites. Monospecific canopies comprising Laminaria hyperborea were unaffected by storm disturbance. However, at one study site a mixed canopy comprising Laminaria ochroleuca, Saccharina latissima and L. hyperborea was significantly altered by the storms, due to decreased abundances of the former two species. Quantification of freshly severed stipes suggested that the ‘warm water’ kelp L. ochroleuca was more susceptible to storm damage than L. hyperborea. Overall, kelp canopies were highly resistant to storm disturbance because of the low vulnerability of L. hyperborea to intense wave action. However, if climate-driven shifts in kelp species distributions result in more mixed canopies, as predicted, then resistance to storm disturbance may be eroded.

Turning on the heat: ecological response to simulated warming in the sea.

Significant warming has been observed in every ocean, yet our ability to predict the consequences of oceanic warming on marine biodiversity remains poor. Experiments have been severely limited because, until now, it has not been possible to manipulate seawater temperature in a consistent manner across a range of marine habitats. We constructed a “hot-plate” system to directly examine ecological responses to elevated seawater temperature in a subtidal marine system. The substratum available for colonisation and overlying seawater boundary layer were warmed for 36 days, which resulted in greater biomass of marine organisms and a doubling of space coverage by a dominant colonial ascidian. The “hot-plate” system will facilitate complex manipulations of temperature and multiple stressors in the field to provide valuable information on the response of individuals, populations and communities to environmental change in any aquatic habitat.