Brian J. Zgliczynski

Lytic to temperate switching of viral communities

Microbial viruses can control host abundances via density-dependent lytic predator–prey dynamics. Less clear is how temperate viruses, which coexist and replicate with their host, influence microbial communities. Here we show that virus-like particles are relatively less abundant at high host densities. This suggests suppressed lysis where established models predict lytic dynamics are favoured. Meta-analysis of published viral and microbial densities showed that this trend was widespread in diverse ecosystems ranging from soil to freshwater to human lungs. Experimental manipulations showed viral densities more consistent with temperate than lytic life cycles at increasing microbial abundance. An analysis of 24 coral reef viromes showed a relative increase in the abundance of hallmark genes encoded by temperate viruses with increased microbial abundance. Based on these four lines of evidence, we propose the Piggyback-the-Winner model wherein temperate dynamics become increasingly important in ecosystems with high microbial densities; thus ‘more microbes, fewer viruses’.

Re-Creating Missing Population Baselines for Pacific Reef Sharks

Summary Abstract Sharks and other large predators are scarce on most coral reefs, but studies of their historical ecology provide qualitative evidence that predators were once numerous in these ecosystems. Quantifying density of sharks in the absence of humans (baseline) is, however, hindered by a paucity of pertinent time-series data. Recently researchers have used underwater visual surveys, primarily of limited spatial extent or nonstandard design, to infer negative associations between reef shark abundance and human populations. We analyzed data from 1607 towed-diver surveys (>1 ha transects surveyed by observers towed behind a boat) conducted at 46 reefs in the central-western Pacific Ocean, reefs that included some of the worlds most pristine coral reefs. Estimates of shark density from towed-diver surveys were substantially lower (<10%) than published estimates from surveys along small transects (<0.02 ha), which is not consistent with inverted biomass pyramids (predator biomass greater than prey biomass) reported by other researchers for pristine reefs. We examined the relation between the density of reef sharks observed in towed-diver surveys and human population in models that accounted for the influence of oceanic primary productivity, sea surface temperature, reef area, and reef physical complexity. We used these models to estimate the density of sharks in the absence of humans. Densities of gray reef sharks (Carcharhinus amblyrhynchos), whitetip reef sharks (Triaenodon obesus), and the group “all reef sharks” increased substantially as human population decreased and as primary productivity and minimum sea surface temperature (or reef area, which was highly correlated with temperature) increased. Simulated baseline densities of reef sharks under the absence of humans were 1.1–2.4/ha for the main Hawaiian Islands, 1.2–2.4/ha for inhabited islands of American Samoa, and 0.9–2.1/ha for inhabited islands in the Mariana Archipelago, which suggests that density of reef sharks has declined to 3–10% of baseline levels in these areas. Resumen Los tiburones y otros depredadores mayores son escasos en la mayoría de los arrecifes de coral, pero estudios de su ecología histórica proporcionan evidencia cualitativa de que los depredadores una vez fueron numerosos en estos ecosistemas. Sin embargo, la cuantificación de la densidad de tiburones en ausencia de humanos (línea de base) es obstaculizada por la falta de datos de series de tiempo pertinentes. Recientemente, los investigadores han utilizado muestreos visuales submarinos, de extensión espacial limitada o de diseño no estándar, para inferir asociaciones negativas entre la abundancia de tiburones de arrecife y las poblaciones humanas. Analizamos datos de 1607 muestreos por remolque de buzos (transectos >1ha muestreados por observadores remolcados por una lancha) realizados en 46 arrecifes en el Océano Pacífico centro-occidental, arrecifes que incluyeron algunos de los más prístinos del mundo. Las estimaciones de densidad de tiburones fue sustancialmente menor (<10%) que estimaciones publicadas a partir de muestreos a lo largo de transectos pequeños (<0.02 ha), lo cual no es consistente con las pirámides de biomasa invertidas (la biomasa de depredadores es mayor que la biomasa de presas) reportadas para arrecifes prístinos por otros autores. Examinamos la relación entre la densidad de tiburones de arrecife observados en los muestreos por remolque de buzos y la población humana en modelos y consideramos la influencia de la productividad oceánica primaria, la temperatura de la superficie del mar, la superficie del arrecife y su complejidad física. Utilizamos estos modelos para estimar la densidad de tiburones en ausencia de humanos. Las densidades de Carcharhinus amblyrhynchos, Triaenodon obesus y el grupo de “tiburones estrictamente arrecifales” incrementó sustancialmente a medida que disminuyó la población humana y que incrementó la productividad primaria y la temperatura de la superficie del mar (o superficie del arrecife, que estaba altamente correlacionada con la temperatura. Las densidades basales simuladas de tiburones arrecifales en ausencia de humanos fueron 1.1–2.4/ha para las Islas Hawaianas, 1.2–2.4/ha en islas deshabitadas de Samoa Americana y 0.9–2.1/ha e islas deshabitadas del Archipiélago Mariana, lo que sugiere que la densidad de tiburones arrecifales ha declinado entre 3 -10% en relación con los niveles basales en esas áreas.

Differences in reef fish assemblages between populated and remote reefs spanning multiple archipelagos across the central and western Pacific

Comparable information on the status of natural resources across large geographic and human impact scales provides invaluable context to ecosystem-based management and insights into processes driving differences among areas. Data on fish assemblages at 39 US flag coral reef-areas distributed across the Pacific are presented. Total reef fish biomass varied by more than an order of magnitude: lowest at densely-populated islands and highest on reefs distant from human populations. Remote reefs (<50 people within 100 km) averaged ~4 times the biomass of “all fishes” and 15 times the biomass of piscivores compared to reefs near populated areas. Greatest within-archipelagic differences were found in Hawaiian and Mariana Archipelagos, where differences were consistent with, but likely not exclusively driven by, higher fishing pressure around populated areas. Results highlight the importance of the extremely remote reefs now contained within the system of Pacific Marine National Monuments as ecological reference areas.

Global assessment of the status of coral reef herbivorous fishes: evidence for fishing effects

On coral reefs, herbivorous fishes consume benthic primary producers and regulate competition between fleshy algae and reef-building corals. Many of these species are also important fishery targets, yet little is known about their global status. Using a large-scale synthesis of peer-reviewed and unpublished data, we examine variability in abundance and biomass of herbivorous reef fishes and explore evidence for fishing impacts globally and within regions. We show that biomass is more than twice as high in locations not accessible to fisheries relative to fisheries-accessible locations. Although there are large biogeographic differences in total biomass, the effects of fishing are consistent in nearly all regions. We also show that exposure to fishing alters the structure of the herbivore community by disproportionately reducing biomass of large-bodied functional groups (scraper/excavators, browsers, grazer/detritivores), while increasing biomass and abundance of territorial algal-farming damselfishes (Pomacentridae). The browser functional group that consumes macroalgae and can help to prevent coral–macroalgal phase shifts appears to be most susceptible to fishing. This fishing down the herbivore guild probably alters the effectiveness of these fishes in regulating algal abundance on reefs. Finally, data from remote and unfished locations provide important baselines for setting management and conservation targets for this important group of fishes.

Assessing Coral Reefs on a Pacific-Wide Scale Using the Microbialization Score

The majority of the worlds coral reefs are in various stages of decline. While a suite of disturbances (overfishing, eutrophication, and global climate change) have been identified, the mechanism(s) of reef system decline remain elusive. Increased microbial and viral loading with higher percentages of opportunistic and specific microbial pathogens have been identified as potentially unifying features of coral reefs in decline. Due to their relative size and high per cell activity, a small change in microbial biomass may signal a large reallocation of available energy in an ecosystem; that is the microbialization of the coral reef. Our hypothesis was that human activities alter the energy budget of the reef system, specifically by altering the allocation of metabolic energy between microbes and macrobes. To determine if this is occurring on a regional scale, we calculated the basal metabolic rates for the fish and microbial communities at 99 sites on twenty-nine coral islands throughout the Pacific Ocean using previously established scaling relationships. From these metabolic rate predictions, we derived a new metric for assessing and comparing reef health called the microbialization score. The microbialization score represents the percentage of the combined fish and microbial predicted metabolic rate that is microbial. Our results demonstrate a strong positive correlation between reef microbialization scores and human impact. In contrast, microbialization scores did not significantly correlate with ocean net primary production, local chla concentrations, or the combined metabolic rate of the fish and microbial communities. These findings support the hypothesis that human activities are shifting energy to the microbes, at the expense of the macrobes. Regardless of oceanographic context, the microbialization score is a powerful metric for assessing the level of human impact a reef system is experiencing.

Fishing drives declines in fish parasite diversity and has variable effects on parasite abundance

Despite the ubiquity and ecological importance of parasites, relatively few studies have assessed their response to anthropogenic environmental change. Heuristic models have predicted both increases and decreases in parasite abundance in response to human disturbance, with empirical support for both. However, most studies focus on one or a few selected parasite species. Here, we assess the abundance of parasites of seven species of coral reef fishes collected from three fished and three unfished islands of the Line Islands archipelago in the central equatorial Pacific. Because we chose fish hosts that spanned different trophic levels, taxonomic groups, and body sizes, we were able to compare parasite responses across a broad cross section of the total parasite community in the presence and absence of fishing, a major human impact on marine ecosystems. We found that overall parasite species richness was substantially depressed on fished islands, but that the response of parasite abundance varied among parasite taxa: directly transmitted parasites were significantly more abundant on fished than on unfished islands, while the reverse was true for trophically transmitted parasites. This probably arises because trophically transmitted parasites require multiple host species, some of which are the top predators most sensitive to fishing impacts. The increase in directly transmitted parasites appeared to be due to fishing-driven compensatory increases in the abundance of their hosts. Together, these results provide support for the predictions of both heuristic models, and indicate that the direction of fishings impact on parasite abundance is mediated by parasite traits, notably parasite transmission strategies.

The Lagoon at Caroline/Millennium Atoll, Republic of Kiribati: Natural History of a Nearly Pristine Ecosystem

A series of surveys were carried out to characterize the physical and biological parameters of the Millennium Atoll lagoon during a research expedition in April of 2009. Millennium is a remote coral atoll in the Central Pacific belonging to the Republic of Kiribati, and a member of the Southern Line Islands chain. The atoll is among the few remaining coral reef ecosystems that are relatively pristine. The lagoon is highly enclosed, and was characterized by reticulate patch and line reefs throughout the center of the lagoon as well as perimeter reefs around the rim of the atoll. The depth reached a maximum of 33.3 m in the central region of the lagoon, and averaged between 8.8 and 13.7 m in most of the pools. The deepest areas were found to harbor large platforms of Favia matthaii, which presumably provided a base upon which the dominant corals (Acropora spp.) grew to form the reticulate reef structure. The benthic algal communities consisted mainly of crustose coralline algae (CCA), microfilamentous turf algae and isolated patches of Halimeda spp. and Caulerpa spp. Fish species richness in the lagoon was half of that observed on the adjacent fore reef. The lagoon is likely an important nursery habitat for a number of important fisheries species including the blacktip reef shark and Napoleon wrasse, which are heavily exploited elsewhere around the world but were common in the lagoon at Millennium. The lagoon also supports an abundance of giant clams (Tridacna maxima). Millennium lagoon provides an excellent reference of a relatively undisturbed coral atoll. As with most coral reefs around the world, the lagoon communities of Millennium may be threatened by climate change and associated warming, acidification and sea level rise, as well as sporadic local resource exploitation which is difficult to monitor and enforce because of the atolls remote location. While the remote nature of Millennium has allowed it to remain one of the few nearly pristine coral reef ecosystems in the world, it is imperative that this ecosystem receives protection so that it may survive for future generations.

The IUCN Red List of Threatened Species: an assessment of coral reef fishes in the US Pacific Islands

Widespread declines among many coral reef fisheries have led scientists and managers to become increasingly concerned over the extinction risk facing some species. To aid in assessing the extinction risks facing coral reef fishes, large-scale censuses of the abundance and distribution of individual species are critically important. We use fisheries-independent data collected as part of the NOAA Pacific Reef Assessment and Monitoring Program from 2000 to 2009 to describe the range and density across the US Pacific of coral reef fishes included on The International Union for the Conservation of Nature’s (IUCN) 2011 Red List of Threatened Species. Forty-five species, including sharks, rays, groupers, humphead wrasse (Cheilinus undulatus), and bumphead parrotfish (Bolbometopon muricatum), included on the IUCN List, were recorded in the US Pacific Islands. Most species were generally rare in the US Pacific with the exception of a few species, principally small groupers and reef sharks. The greatest diversity and densities of IUCN-listed fishes were recorded at remote and uninhabited islands of the Pacific Remote Island Areas; in general, lower densities were observed at reefs of inhabited islands. Our findings complement IUCN assessment efforts, emphasize the efficacy of large-scale assessment and monitoring efforts in providing quantitative data on reef fish assemblages, and highlight the importance of protecting populations at remote and uninhabited islands where some species included on the IUCN Red List of Threatened Species can be observed in abundance.

Sequencing at sea: Challenges and experiences in Ion Torrent PGM sequencing during the 2013 Southern Line Islands Research Expedition

Genomics and metagenomics have revolutionized our understanding of marine microbial ecology and the importance of microbes in global geochemical cycles. However, the process of DNA sequencing has always been an abstract extension of the research expedition, completed once the samples were returned to the laboratory. During the 2013 Southern Line Islands Research Expedition, we started the first effort to bring next generation sequencing to some of the most remote locations on our planet. We successfully sequenced twenty six marine microbial genomes, and two marine microbial metagenomes using the Ion Torrent PGM platform on the Merchant Yacht Hanse Explorer. Onboard sequence assembly, annotation, and analysis enabled us to investigate the role of the microbes in the coral reef ecology of these islands and atolls. This analysis identified phosphonate as an important phosphorous source for microbes growing in the Line Islands and reinforced the importance of L-serine in marine microbial ecosystems. Sequencing in the field allowed us to propose hypotheses and conduct experiments and further sampling based on the sequences generated. By eliminating the delay between sampling and sequencing, we enhanced the productivity of the research expedition. By overcoming the hurdles associated with sequencing on a boat in the middle of the Pacific Ocean we proved the flexibility of the sequencing, annotation, and analysis pipelines.

Reef Fish Survey Techniques: Assessing the Potential for Standardizing Methodologies.

Dramatic changes in populations of fishes living on coral reefs have been documented globally and, in response, the research community has initiated efforts to assess and monitor reef fish assemblages. A variety of visual census techniques are employed, however results are often incomparable due to differential methodological performance. Although comparability of data may promote improved assessment of fish populations, and thus management of often critically important nearshore fisheries, to date no standardized and agreed-upon survey method has emerged. This study describes the use of methods across the research community and identifies potential drivers of method selection. An online survey was distributed to researchers from academic, governmental, and non-governmental organizations internationally. Although many methods were identified, 89% of survey-based projects employed one of three methods–belt transect, stationary point count, and some variation of the timed swim method. The selection of survey method was independent of the research design (i.e., assessment goal) and region of study, but was related to the researcher’s home institution. While some researchers expressed willingness to modify their current survey protocols to more standardized protocols (76%), their willingness decreased when methodologies were tied to long-term datasets spanning five or more years. Willingness to modify current methodologies was also less common among academic researchers than resource managers. By understanding both the current application of methods and the reported motivations for method selection, we hope to focus discussions towards increasing the comparability of quantitative reef fish survey data.