Alexandra H. Campbell

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.

Global patterns in the impact of marine herbivores on benthic primary producers

Despite the importance of consumers in structuring communities, and the widespread assumption that consumption is strongest at low latitudes, empirical tests for global scale patterns in the magnitude of consumer impacts are limited. In marine systems, the long tradition of experimentally excluding herbivores in their natural environments allows consumer impacts to be quantified on global scales using consistent methodology. We present a quantitative synthesis of 613 marine herbivore exclusion experiments to test the influence of consumer traits, producer traits and the environment on the strength of herbivore impacts on benthic producers. Across the globe, marine herbivores profoundly reduced producer abundance (by 68% on average), with strongest effects in rocky intertidal habitats and the weakest effects on habitats dominated by vascular plants. Unexpectedly, we found little or no influence of latitude or mean annual water temperature. Instead, herbivore impacts differed most consistently among producer taxonomic and morphological groups. Our results show that grazing impacts on plant abundance are better predicted by producer traits than by large-scale variation in habitat or mean temperature, and that there is a previously unrecognised degree of phylogenetic conservatism in producer susceptibility to consumption.

Temperature induced bacterial virulence and bleaching disease in a chemically defended marine macroalga

Host-pathogen interactions have been widely studied in humans and terrestrial plants, but are much less well explored in marine systems. Here we show that a marine macroalga, Delisea pulchra, utilizes a chemical defence - furanones - to inhibit colonization and infection by a novel bacterial pathogen, Ruegeria sp. R11, and that infection by R11 is temperature dependent. Ruegeria sp. R11 formed biofilms, invaded and bleached furanone-free, but not furanone-producing D. pulchra thalli, at high (24°C) but not low (19°C) temperatures. Bleaching is commonly observed in natural populations of D. pulchra near Sydney, Australia, during the austral summer when ocean temperatures are at their peak and the chemical defences of the alga are reduced. Furanones, produced by D. pulchra as a chemical defence, inhibit quorum sensing (QS) in bacteria, and this may play a role in furanone inhibition of R11 infection of furanone-free thalli as R11 produces QS signals. This interplay between temperature, an algal chemical defence mechanism and bacterial virulence demonstrates the complex impact environmental change can have on an ecosystem.

Long-term empirical evidence of ocean warming leading to tropicalization of fish communities, increased herbivory, and loss of kelp

Significance Most studies of the impact of global warming focus on the direct physiological impacts of climate change. However, global warming is shifting the distribution of many species and leading to novel interactions between previously separated species that have the potential to transform entire ecological communities. This study shows that an increase in the proportion of warmwater species (“tropicalization”) as oceans warm is increasing fish herbivory in kelp forests, contributing to their decline and subsequent persistence in alternate “kelp-free” states. These tropical and subtropical herbivores are increasingly impacting temperate algal communities worldwide, posing a significant threat to the long-term stability of these iconic ecosystems and the valuable services they provide. Some of the most profound effects of climate change on ecological communities are due to alterations in species interactions rather than direct physiological effects of changing environmental conditions. Empirical evidence of historical changes in species interactions within climate-impacted communities is, however, rare and difficult to obtain. Here, we demonstrate the recent disappearance of key habitat-forming kelp forests from a warming tropical–temperate transition zone in eastern Australia. Using a 10-y video dataset encompassing a 0.6 °C warming period, we show how herbivory increased as kelp gradually declined and then disappeared. Concurrently, fish communities from sites where kelp was originally abundant but subsequently disappeared became increasingly dominated by tropical herbivores. Feeding assays identified two key tropical/subtropical herbivores that consumed transplanted kelp within hours at these sites. There was also a distinct increase in the abundance of fishes that consume epilithic algae, and much higher bite rates by this group at sites without kelp, suggesting a key role for these fishes in maintaining reefs in kelp-free states by removing kelp recruits. Changes in kelp abundance showed no direct relationship to seawater temperatures over the decade and were also unrelated to other measured abiotic factors (nutrients and storms). Our results show that warming-mediated increases in fish herbivory pose a significant threat to kelp-dominated ecosystems in Australia and, potentially, globally.

Chemical Mediation of Ternary Interactions Between Marine Holobionts and Their Environment as Exemplified by the Red Alga Delisea pulchra

The need for animals and plants to control microbial colonization is important in the marine environment with its high densities of microscopic propagules and seawater that provides an ideal medium for their dispersal. In contrast to the traditional emphasis on antagonistic interactions of marine organisms with microbes, emerging studies lend support to the notion that health and performance of many marine organisms are functionally regulated and assisted by associated microbes, an ecological concept defined as a holobiont. While antimicrobial activities of marine secondary metabolites have been studied in great depth ex-situ, we are beginning to understand how some of these compounds function in an ecological context to maintain the performance of marine holobionts. The present article reviews two decades of our research on the red seaweed Delisea pulchra by addressing: the defense chemistry of this seaweed; chemically-mediated interactions between the seaweed and its natural enemies; and the negative influence of elevated seawater temperature on these interactions. Our understanding of these defense compounds and the functional roles they play for D. pulchra extends from molecular interactions with bacterial cell signaling molecules, to ecosystem-scale consequences of chemically-controlled disease and herbivory. Delisea pulchra produces halogenated furanones that antagonize the same receptor as acylated homoserine lactones (AHL)—a group of widespread intercellular communication signals among bacteria. Halogenated furanones compete with and inhibit bacterial cell-to-cell communication, and thus interfere with important bacterial communication-regulated processes, such as biofilm formation. In a predictable pattern that occurs at the ecological level of entire populations, environmental stress interferes with the production of halogenated furanones, causing downstream processes that ultimately result in disease of the algal holobiont.

Towards restoration of missing underwater forests.

Degradation of natural habitats due to urbanization is a major cause of biodiversity loss. Anthropogenic impacts can drive phase shifts from productive, complex ecosystems to less desirable, less diverse systems that provide fewer services. Macroalgae are the dominant habitat-forming organisms on temperate coastlines, providing habitat and food to entire communities. In recent decades, there has been a decline in macroalgal cover along some urbanised shorelines, leading to a shift from diverse algal forests to more simple turf algae or barren habitats. Phyllospora comosa, a major habitat forming macroalga in south-eastern Australia, has disappeared from the urban shores of Sydney. Its disappearance is coincident with heavy sewage outfall discharges along the metropolitan coast during 1970s and 1980s. Despite significant improvements in water-quality since that time, Phyllospora has not re-established. We experimentally transplanted adult Phyllospora into two rocky reefs in the Sydney metropolitan region to examine the model that Sydney is now suitable for the survival and recruitment of Phyllospora and thus assess the possibility of restoring Phyllospora back onto reefs where it was once abundant. Survival of transplanted individuals was high overall, but also spatially variable: at one site most individuals were grazed, while at the other site survival was similar to undisturbed algae and procedural controls. Transplanted algae reproduced and recruitment rates were higher than in natural populations at one experimental site, with high survival of new recruits after almost 18 months. Low supply and settlement success of propagules in the absence of adults and herbivory (in some places) emerge as three potential processes that may have been preventing natural re-establishment of this alga. Understanding of the processes and interactions that shape this system are necessary to provide ecologically sensible goals and the information needed to successfully restore these underwater forests.

Spatial variability of microbial assemblages associated with a dominant habitat-forming seaweed.

Macroalgal surfaces support abundant and diverse microorganisms within biofilms, which are often involved in fundamental functions relating to the health and defense of their seaweed hosts, including algal development, facilitation of spore release, and chemical antifouling. Given these intimate and important interactions, environmental changes have the potential to negatively impact macroalgae by disrupting seaweed–microbe interactions. We used the disappearance of the dominant canopy-forming fucoid Phyllospora comosa from the metropolitan coast of Sydney, NSW, Australia as a model system to study these interactions. We transplanted Phyllospora individuals from nearby, extant populations back onto reefs in Sydney to test whether bacterial assemblages associated with seaweed surfaces would be influenced by (i) the host itself, independently of where it occurs, (ii) the type of habitat where the host occurs, or (iii) site-specific differences. Analyses of bacterial DNA fingerprints (terminal fragment length polymorphisms) indicated that assemblages of bacteria on Phyllospora were not habitat-specific. Rather, they were primarily influenced by local, site-specific conditions with some evidence for host-specificity in some cases. This could suggest a lottery model of host-surface colonization, by which hosts are colonized by ‘suitable’ bacteria available in the local species pool, resulting in high variability in assemblage structure across sites, but where some species in the community are specific to the host and possibly influenced by differences in host traits.

Demographic consequences of disease in a habitat-forming seaweed and impacts on interactions between natural enemies.

Diseases affecting natural ecosystems are increasing in frequency and severity, but unless obviously catastrophic, the consequences of disease outbreaks are often overlooked, relative to other ecological processes (e.g., predation, competition). Disease can have profound effects on individuals and can also strongly influence interactions between infected hosts and their natural enemies. We investigated whether a novel bleaching disease affected the survival or performance of a habitat-forming red seaweed, Delisea pulchra. In addition, we investigated bidirectional, multipartite interactions between this seaweed host, its pathogens, and consumers. Although we found no negative impacts of disease on survival of D. pulchra, bleaching had substantial, negative consequences for affected individuals, including a dramatic drop in fecundity and a significant decrease in size. In the first direct demonstration of bacterial disease-mediated herbivory of seaweeds, herbivores generally preferred to consume bleached tissue in feeding trials, and we also found higher densities of herbivores on bleached than co-occurring, healthy algae at sites where herbivores were abundant. In a conceptually reciprocal test of the effects of herbivores on infection, we showed that simulated herbivory increased susceptibility to bleaching when algae were also exposed to cultures of a bacterial pathogen. Given the high proportions of D. pulchra affected by bleaching during peak periods, the impacts of this disease are likely to have important implications at the population level. This work highlights complex interactions between habitat-forming organisms and their natural enemies and further emphasizes the need to consider disease in ecological research.

Restoring seaweeds: does the declining fucoid Phyllospora comosa support different biodiversity than other habitats?

Degradation and loss of natural habitats due to human activities is a main cause of global biodiversity loss. In temperate systems, seaweeds are a main habitat former and support extremely diverse communities, including many economically important species. Coastal urbanisation is, however, causing significant declines of key habitat-forming seaweeds. To develop successful management strategies such as seaweed habitat restoration, it is necessary to first determine what additional ecosystem values are likely to be added through restoration and to provide baseline data against which goals can be established and success can be measured. The habitat-forming fucoid Phyllospora comosa was once common on shallow subtidal reefs around Sydney, Australia’s largest city, but disappeared in the 1980s, coincident with heavy sewage outfall discharges. To provide the baseline data necessary for restoring and managing Phyllospora in areas from where it has disappeared, we quantified the community composition and abundance of fish and large invertebrates (abalone and sea urchins) in healthy Phyllospora habitats and compared them to those in Ecklonia radiata (the other major habitat-forming kelp in the region) as well as other common shallow subtidal habitats. Fish assemblage structure was similar between Phyllospora vs Ecklonia beds, but Phyllospora supported much greater numbers of abalone and urchins than any other habitat. This suggests that, in terms of some components of the biodiversity it supports, Phyllospora is functionally unique and not a redundant species. Restoring this seaweed will, therefore, also contribute to biodiversity rehabilitation by restoring unique faunal assemblages that are supported by Phyllospora, including economically important species.

27 years of benthic and coral community dynamics on turbid, highly urbanised reefs off Singapore

Coral cover on reefs is declining globally due to coastal development, overfishing and climate change. Reefs isolated from direct human influence can recover from natural acute disturbances, but little is known about long term recovery of reefs experiencing chronic human disturbances. Here we investigate responses to acute bleaching disturbances on turbid reefs off Singapore, at two depths over a period of 27 years. Coral cover declined and there were marked changes in coral and benthic community structure during the first decade of monitoring at both depths. At shallower reef crest sites (3–4 m), benthic community structure recovered towards pre-disturbance states within a decade. In contrast, there was a net decline in coral cover and continuing shifts in community structure at deeper reef slope sites (6–7 m). There was no evidence of phase shifts to macroalgal dominance but coral habitats at deeper sites were replaced by unstable substrata such as fine sediments and rubble. The persistence of coral dominance at chronically disturbed shallow sites is likely due to an abundance of coral taxa which are tolerant to environmental stress. In addition, high turbidity may interact antagonistically with other disturbances to reduce the impact of thermal stress and limit macroalgal growth rates.