James J. Leichter

Effects of Coral Reef Benthic Primary Producers on Dissolved Organic Carbon and Microbial Activity

Benthic primary producers in marine ecosystems may significantly alter biogeochemical cycling and microbial processes in their surrounding environment. To examine these interactions, we studied dissolved organic matter release by dominant benthic taxa and subsequent microbial remineralization in the lagoonal reefs of Moorea, French Polynesia. Rates of photosynthesis, respiration, and dissolved organic carbon (DOC) release were assessed for several common benthic reef organisms from the backreef habitat. We assessed microbial community response to dissolved exudates of each benthic producer by measuring bacterioplankton growth, respiration, and DOC drawdown in two-day dark dilution culture incubations. Experiments were conducted for six benthic producers: three species of macroalgae (each representing a different algal phylum: Turbinaria ornata – Ochrophyta; Amansia rhodantha – Rhodophyta; Halimeda opuntia – Chlorophyta), a mixed assemblage of turf algae, a species of crustose coralline algae (Hydrolithon reinboldii) and a dominant hermatypic coral (Porites lobata). Our results show that all five types of algae, but not the coral, exuded significant amounts of labile DOC into their surrounding environment. In general, primary producers with the highest rates of photosynthesis released the most DOC and yielded the greatest bacterioplankton growth; turf algae produced nearly twice as much DOC per unit surface area than the other benthic producers (14.0±2.8 µmol h−1 dm−2), stimulating rapid bacterioplankton growth (0.044±0.002 log10 cells h−1) and concomitant oxygen drawdown (0.16±0.05 µmol L−1 h−1 dm−2). Our results demonstrate that benthic reef algae can release a significant fraction of their photosynthetically-fixed carbon as DOC, these release rates vary by species, and this DOC is available to and consumed by reef associated microbes. These data provide compelling evidence that benthic primary producers differentially influence reef microbial dynamics and biogeochemical parameters (i.e., DOC and oxygen availability, bacterial abundance and metabolism) in coral reef communities.

Variation beneath the surface: Quantifying complex thermal environments on coral reefs in the Caribbean, Bahamas and Florida

Analysis of in situ temperature records collected on six coral reefs in the Caribbean, Bahamas, and Florida Keys reveal significant variability across a range of temporal and spatial scales from minutes to seasons, across depths, and among sites. Subsurface variability occurring at daily and faster frequencies is prevalent across the region, likely driven by combinations of diurnal heating and cooling, wind driven advection, and internal waves at tidal and faster frequencies. This high frequency variability is not detected in records of remotely-sensed sea surface temperature alone. Diurnal variability likely caused by diurnal solar heating and cooling and possibly by advection associated with diurnal winds (daily sea breeze) was significant at all sites and showed greatest magnitude of variation at shallowest depths. Temperature fluctuations at tidal and faster frequencies were common at 5 out of the 6 sites. The magnitude of this variability is not well explained by measured vertical temperature stratification combined with oscillations of the water column associated with barotropic surface tides. Rather, the magnitude and nature of the temperature changes point to the presence of internal waves generated at tidal and faster frequencies. Power spectra calculated seasonally show greatest variability within both diurnal and semi-diurnal frequency bands in Spring and Summer at Florida, Bahamas, Jamaica, and St. Croix. Variability within the semi-diurnal frequency band at Belize and Bonaire was greatest in Winter. Warming in Summer estimated as degree-hours per day above 29.0°C increased with increasing latitude and varied significantly among sites and depths in a manner not predictable from remotely sensed SST data alone. Site latitude was directly related to the amplitude of the seasonal thermal variability, but was not tightly related to variability at daily and faster frequencies which was greatest at the highest and lowest latitude sites. The interactions of depth, site, and season across the study region are associated with distinct signals of thermal variability, and have significant implications for the physiology and ecology of corals and other reef organisms.

Spatial and Temporal Variability of Internal Wave Forcing on a Coral Reef

The deployment of a dense spatial array of temperature sensors on a coral reef in the Florida Keys provided a unique view of the interaction of cool water incursions generated by internal waves with the three-dimensional reef bathymetry. Water temperature on the reef surface was sampled every 5 s at 100 points on a 100 m by 150 m grid with concomitant measurements of water column velocity and temperature from mid-May through mid-August 2003. Episodic incursions of cool, subsurface water were driven by periods of strong semidiurnal internal tide and higher-frequency internal wave activity. For every time step in the data record the mean profile of temperature as a function of depth is calculated with a 3-m vertical averaging length scale. Subtracting this mean profile from the raw record yields a within depth, horizontal temperature anomaly. Visualization through time of the anomaly mapped onto the measured reef bathymetry reveals episodic variability of thermal patchiness across the reef as well as persistent features associated with reef bathymetry. Variation in the nature of the cooling and resulting thermal heterogeneity among events and seasons suggests multiple modes of cool water incursion ranging from unbroken, tidal period internal waves to packets of higher-frequency, energetic, broken internal bores.

Water flow over subtidal rock walls: relation to distributions and growth rates of sessile suspension feeders in the Gulf of Maine Water flow and growth rates

Abstract Moving water delivers food resources to sessile suspension feeding invertebrates and the interaction between water motion and substrate topography may dramatically influence the ecology of these animals. Growth rates of two species of sessile suspension feeders were compared between positions within individual 1.5-m high rock walls at an offshore site at 30-m depth in the Gulf of Maine, USA. The site is characterized by strong, highly variable water flow. Growth rates for the active suspension feeding mussel Mytilus edulis (Linnaeus), were greater at upper than at lower wall positions, while growth rates for the facultatively-active suspension feeding sponge Halichondria panicea (Pallas) showed the opposite pattern, with higher rates at lower than upper wall positions. Mussel and sponge growth rates were related both to patterns of bulk fluid flux across the walls and to naturally occurring distributions of sessile suspension feeders. Dissolution of alabaster and plaster solids indicated that upper wall positions experienced significantly higher bulk fluid flux than lower wall positions. Distribution data show non-random suspension feeder abundances across a series of small rock walls at two offshore sites. The abundance of passive suspension feeders was greatest near the top edges, while active and facultatively-active suspension feeders occur in greatest densities at lower wall positions. The results show that the interaction of small scale, abrupt, topographic features with variable local flow conditions can lead to physical gradients within rock walls. These gradients significantly affect the growth of suspension feeders, and may influence the structure sessile of invertebrate communities on subtidal rock walls.

Marine reserve design: optimal size, habitats, species affinities, diversity, and ocean microclimate

The design of marine reserves is complex and fraught with uncertainty. However, protection of critical habitat is of paramount importance for reserve design. We present a case study as an example of a reserve design based on fine-scale habitats, the affinities of exploited species to these habitats, adult mobility, and the physical forcing affecting the dynamics of the habitats. These factors and their interaction are integrated in an algorithm that determines the optimal size and location of a marine reserve for a set of 20 exploited species within five different habitats inside a large kelp forest in southern California. The result is a reserve that encompasses approximately 42% of the kelp forest. Our approach differs fundamentally from many other marine reserve siting methods in which goals of area, diversity, or biomass are targeted a priori. Rather, our method was developed to determine how large a reserve must be within a specific area to protect a self-sustaining assemblage of exploited species. The algorithm is applicable across different ecosystems, spatial scales, and for any number of species. The result is a reserve in which habitat value is optimized for a predetermined set of exploited species against the area left open to exploitation. The importance of fine-scale habitat definitions for the exploited species off La Jolla is exemplified by the spatial pattern of habitats and the stability of these habitats within the kelp forest, both of which appear to be determined by ocean microclimate.

Influence of coral and algal exudates on microbially mediated reef metabolism.

Benthic primary producers in tropical reef ecosystems can alter biogeochemical cycling and microbial processes in the surrounding seawater. In order to quantify these influences, we measured rates of photosynthesis, respiration, and dissolved organic carbon (DOC) exudate release by the dominant benthic primary producers (calcifying and non-calcifying macroalgae, turf-algae and corals) on reefs of Mo‘orea French Polynesia. Subsequently, we examined planktonic and benthic microbial community response to these dissolved exudates by measuring bacterial growth rates and oxygen and DOC fluxes in dark and daylight incubation experiments. All benthic primary producers exuded significant quantities of DOC (roughly 10% of their daily fixed carbon) into the surrounding water over a diurnal cycle. The microbial community responses were dependent upon the source of the exudates and whether the inoculum of microbes included planktonic or planktonic plus benthic communities. The planktonic and benthic microbial communities in the unamended control treatments exhibited opposing influences on DO concentration where respiration dominated in treatments comprised solely of plankton and autotrophy dominated in treatments with benthic plus plankon microbial communities. Coral exudates (and associated inorganic nutrients) caused a shift towards a net autotrophic microbial metabolism by increasing the net production of oxygen by the benthic and decreasing the net consumption of oxygen by the planktonic microbial community. In contrast, the addition of algal exudates decreased the net primary production by the benthic communities and increased the net consumption of oxygen by the planktonic microbial community thereby resulting in a shift towards net heterotrophic community metabolism. When scaled up to the reef habitat, exudate-induced effects on microbial respiration did not outweigh the high oxygen production rates of benthic algae, such that reef areas dominated with benthic primary producers were always estimated to be net autotrophic. However, estimates of microbial consumption of DOC at the reef scale surpassed the DOC exudation rates suggesting net consumption of DOC at the reef-scale. In situ mesocosm experiments using custom-made benthic chambers placed over different types of benthic communities exhibited identical trends to those found in incubation experiments. Here we provide the first comprehensive dataset examining direct primary producer-induced, and indirect microbially mediated alterations of elemental cycling in both benthic and planktonic reef environments over diurnal cycles. Our results highlight the variability of the influence of different benthic primary producers on microbial metabolism in reef ecosystems and the potential implications for energy transfer to higher trophic levels during shifts from coral to algal dominance on reefs.

Chronic parrotfish grazing impedes coral recovery after bleaching

Coral bleaching, in which corals become visibly pale and typically lose their endosymbiotic zooxanthellae (Symbiodinium spp.), increasingly threatens coral reefs worldwide. While the proximal environmental triggers of bleaching are reasonably well understood, considerably less is known concerning physiological and ecological factors that might exacerbate coral bleaching or delay recovery. We report a bleaching event in Belize during September 2004 in which Montastraea spp. corals that had been previously grazed by corallivorous parrotfishes showed a persistent reduction in symbiont density compared to intact colonies. Additionally, grazed corals exhibited greater diversity in the genetic composition of their symbiont communities, changing from uniform ITS2 type C7 Symbiodinium prior to bleaching to mixed assemblages of Symbiodinium types post-bleaching. These results suggest that chronic predation may exacerbate the influence of environmental stressors and, by altering the coral-zooxanthellae symbiosis, such abiotic-biotic interactions may contribute to spatial variation in bleaching processes.

Sea ice microbial production supports Ross Sea benthic communities: influence of a small but stable subsidy

Diversity in guilds of primary producers enhances temporal stability in provision of organic matter to consumers. In the Antarctic ecosystem, where temporal variability in phytoplankton production is high, sea ice contains a diatom and microbial community (SIMCO) that represents a pool of organic matter that is seasonally more consistent, although of relatively small magnitude. The fate of organic material produced by SIMCO in Antarctica is largely unknown but may represent an important link between sea ice dynamics and secondary production in nearshore food webs. We used whole tissue and compound-specific stable isotope analysis of consumers to test whether the sea ice microbial community is an important source of organic matter supporting nearshore communities in the Ross Sea. We found distinct gradients in delta13C and delta15N of SIMCO corresponding to differences in inorganic carbon and nitrogen acquisition among sites with different sea ice extent and persistence. Mass balance analysis of a suite of consumers demonstrated large fluxes of SIMCO into the nearshore food web, ranging from 5% to 100% of organic matter supplied to benthic species, and 0-10% of organic matter to upper water column or pelagic inhabitants. A delta13C analysis of nine fatty acids including two key biomarkers for diatoms, eicosapentaenoic acid (EPA, 20:5omega3), and docosahexaenoic acid (DHA, 22:6omega3), confirmed these patterns. We observed clear patterns in delta13C of fatty acids that are enriched in 13C for species that acquire a large fraction of their nutrition from SIMCO. These data demonstrate the key role of SIMCO in ecosystem functioning in Antarctica and strong linkages between sea ice extent and nearshore secondary productivity. While SIMCO provides a stabilizing subsidy of organic matter, changes to sea ice coverage associated with climate change would directly affect secondary production and stability of benthic food webs in Antarctica.

Anchor Ice and Benthic Disturbance in Shallow Antarctic Waters: Interspecific Variation in Initiation and Propagation of Ice Crystals

Sea ice typically forms at the ocean’s surface, but given a source of supercooled water, an unusual form of ice—anchor ice—can grow on objects in the water column or at the seafloor. For several decades, ecologists have considered anchor ice to be an important agent of disturbance in the shallow-water benthic communities of McMurdo Sound, Antarctica, and potentially elsewhere in polar seas. Divers have documented anchor ice in the McMurdo communities, and its presence coincides with reduced abundance of the sponge Homaxinella balfourensis, which provides habitat for a diverse assemblage of benthic organisms. However, the mechanism of this disturbance has not been explored. Here we show interspecific differences in anchor-ice formation and propagation characteristics for Antarctic benthic organisms. The sponges H. balfourensis and Suberites caminatus show increased incidence of formation and accelerated spread of ice crystals compared to urchins and sea stars. Anchor ice also forms readily on sediments, from which it can grow and adhere to organisms. Our results are consistent with, and provide a potential first step toward, an explanation for disturbance patterns observed in shallow polar benthic communities. Interspecific differences in ice formation raise questions about how surface tissue characteristics such as surface area, rugosity, and mucus coating affect ice formation on invertebrates.

Simulating social-ecological systems: the Island Digital Ecosystem Avatars (IDEA) consortium

Systems biology promises to revolutionize medicine, yet human wellbeing is also inherently linked to healthy societies and environments (sustainability). The IDEA Consortium is a systems ecology open science initiative to conduct the basic scientific research needed to build use-oriented simulations (avatars) of entire social-ecological systems. Islands are the most scientifically tractable places for these studies and we begin with one of the best known: Moorea, French Polynesia. The Moorea IDEA will be a sustainability simulator modeling links and feedbacks between climate, environment, biodiversity, and human activities across a coupled marine–terrestrial landscape. As a model system, the resulting knowledge and tools will improve our ability to predict human and natural change on Moorea and elsewhere at scales relevant to management/conservation actions.