Biofluorescence as a survey tool for cryptic marine species

As ecosystems come under increasing anthropogenic pressure, rare species face the highest risk of extinction. Paradoxically, data necessary to evaluate the conservation status of rare species are often lacking because of the challenges of detecting species with low abundance. One group of fishes subject to this undersampling bias are those with cryptic body patterns. Twenty‐one percent of cryptic fish species assessed for their extinction risk (International Union for Conservation of Nature [IUCN]) are data deficient. We developed a nondestructive method for surveying cryptically patterned marine fishes based on the presence of biofluorescence (underwater biofluorescence census, UBC). Blue LED torches were used to investigate how widespread biofluorescence was in cryptic reef fishes in the Coral Triangle region. The effectiveness of UBC to generate abundance data was tested on a data‐deficient pygmy seahorse species (Hippocampus bargibanti) and compared with data obtained from standard underwater visual census (UVC) surveys. We recorded 95 reef fish species displaying biofluorescence, 73 of which had not been previously described as biofluorescent. Of those fish with cryptic patterns, 87% were biofluorescent compared with 9% for noncryptic fishes. The probability of species displaying biofluorescence was 70.9 times greater for cryptic species than for noncryptic species. Almost twice the number of H. bargibanti was counted using the UBC compared with UVC. For 2 triplefin species (Ucla xenogrammus, Enneapterygius tutuilae), the abundance detected with UBC was triple that detected with UVC. The UBC method was effective at finding cryptic species that would otherwise be difficult to detect and thus will reduce interobserver variability inherent to UVC surveys. Biofluorescence is ubiquitous in cryptic fishes, making this method applicable across a wide range of species. Data collected using UBC could be used with multiple IUCN criteria to assess the extinction risk of cryptic species. Adopting this technique will enhance researchers’ ability to survey cryptic species and facilitate management and conservation of cryptic marine species.     

Algal plating as a tool for investigating allelopathy among marine microalgae

Chemical interactions among marine microalgae were studied in cultures of pennate diatoms on agar plates. Nine marine and freshwater pennate diatoms were surveyed as potential bioassay organisms; Cylindrotheca fusiformis was most favourable for assays because of its rapid and even growth on agar. Diatom and bacterial bioassays were used to screen cell and filtrate extracts of 14 microalgal cultures. A number of these algal species, which were grown axenically, produced extractable, intracellular and/or extracellular substances that inhibited the growth of C. fusiformis. Our results suggest that the culturing of pennate diatoms on a solid medium can provide a simple bioassay for screening algal extracts which potentially contain growth inhibitors involved in microalgal allelopathy.     

Incorporating multidimensional behavior into a risk management tool for a critically endangered and migratory species

Conservation of migratory species exhibiting wide-ranging and multidimensional behaviors is challenged by management efforts that only utilize horizontal movements or produce static spatial–temporal products. For the deep-diving, critically endangered eastern Pacific leatherback turtle, tools that predict where turtles have high risks of fisheries interactions are urgently needed to prevent further population decline. We incorporated horizontal–vertical movement model results with spatial–temporal kernel density estimates and threat data (gear-specific fishing) to develop monthly maps of spatial risk. Specifically, we applied multistate hidden Markov models to a biotelemetry data set (n = 28 leatherback tracks, 2004–2007). Tracks with dive information were used to characterize turtle behavior as belonging to 1 of 3 states (transiting, residential with mixed diving, and residential with deep diving). Recent fishing effort data from Global Fishing Watch were integrated with predicted behaviors and monthly space-use estimates to create maps of relative risk of turtle–fisheries interactions. Drifting (pelagic) longline fishing gear had the highest average monthly fishing effort in the study region, and risk indices showed this gear to also have the greatest potential for high-risk interactions with turtles in a residential, deep-diving behavioral state. Monthly relative risk surfaces for all gears and behaviors were added to South Pacific TurtleWatch (SPTW) ( https://www.upwell.org/sptw ), a dynamic management tool for this leatherback population. These modifications will refine SPTW's capability to provide important predictions of potential high-risk bycatch areas for turtles undertaking specific behaviors. Our results demonstrate how multidimensional movement data, spatial–temporal density estimates, and threat data can be used to create a unique conservation tool. These methods serve as a framework for incorporating behavior into similar tools for other aquatic, aerial, and terrestrial taxa with multidimensional movement behaviors.     

Conceptual frameworks and key questions for assessing the contribution of marine protected areas to shark and ray conservation

Marine protected areas (MPAs) are key tools in addressing the global decline of sharks and rays, and marine parks and shark sanctuaries of various configurations have been established to conserve shark populations. However, assessments of their efficacy are compromised by inconsistent terminology, lack of standardized approaches to assess how MPAs contribute to shark and ray conservation, and ambiguity about how to integrate movement data in assessment processes. We devised a conceptual framework to standardize key terms (e.g., protection, contribution, potential impact, risk, threat) and used the concept of portfolio risk to identify key attributes of sharks and rays (assets), the threats they face (portfolio risk), and the specific role of MPAs in risk mitigation (insurance). Movement data can be integrated into the process by informing risk exposure and mitigation through MPAs. The framework is operationalized by posing 8 key questions that prompt practitioners to consider the assessment scope, MPA type and purpose, range of existing and potential threats, species biology and ecology, and management and operational contexts. Ultimately, MPA contributions to shark and ray conservation differ according to a complex set of human and natural factors and interactions that should be carefully considered in MPA design, implementation, and evaluation.     

Density surface modelling with line transect sampling as a tool for abundance estimation of marine benthic species: the <Emphasis Type="Italic">Pinna nobilis</Emphasis> example in a marine lake

Density estimation of marine benthic fauna is most often conducted with fishery surveys using dredges or trawls. These estimates are often unreliable due to low and variable efficiency and are inappropriate when dealing with rare or endangered species. In the marine Lake Vouliagmeni, a density surface modelling (DSM) approach using survey data from line transects, integrated with a Geographic Information System (GIS), was used to estimate the population density of the endangered fan mussel Pinna nobilis. This is the first time that such an approach has been applied for a marine benthic species. DSM was beneficial in relation to traditional distance sampling. Apart from providing a more precise total abundance estimate, it related the density of the species to spatial covariates of interest, gave a depiction of the species dispersion in the study area, and provided abundance estimates in any sub-region of the study area. In Lake Vouliagmeni, a marked zonation of P. nobilis distribution was revealed, with the species being restricted in the shallow peripheral zone at depths <22 m. Two density peaks were observed, a major peak at depths between 12 and 13 m and a secondary peak at ∼4 m. A main hotspot of high density was also observed in the northeastern part of the lake. Total abundance of the species was estimated to be 6,770 individuals with a 95% confidence interval of 5,460–8,393 individuals.     

Aspects of sodium regulation in a brackish-water and a marine species of the isopod genus Sphaeroma

Sodium and chloride concentrations of the haemolymph were determined in Sphaeroma rugicauda Leach and S. serratum Fabricius acclimatized to a range of salinities. Sodium loss and uptake (using ²²Na) were measured in salinities below 1.1 for S. rugicauda and 7.2 for S. serratum. Potential differences between haemolymph and medium indicate active uptake of both ions in certain salinities. The active-uptake component of total sodium-influx was found to be related non-linearly to the sodium concentration of the medium. Curves of were fitted to the activeuptake data. Km values indicate that, in S. rugicauda, the sodium uptake system has a greater affinity for sodium than in S. serratum. These findings are discussed in relation to the distribution of each species.     

Novel molecular fingerprinting of marine avian diet provides a tool for gaining insights into feeding ecology

C₂₅ highly branched isoprenoids (HBIs) are produced by a relatively small number of diatom species, yet are common constituents of almost all marine environments. Previously, detection of HBIs in a few aquatic Arctic animals has indicated the potential use of these lipids for providing novel ecological information. In the current study, analysis of lipid extracts of livers from Leach’s storm petrel (Oceanodroma leucorhoa) and Brunnich’s guillemot (Uria lomvia) facilitated identification and quantification of HBI isomers. HBIs were found in the tissues of all specimens with clear differences in the abundances and distributions of individual HBI isomers both between Atlantic as well as Arctic birds. These differences are consistent with contrasting oceanographic regimes and suggests that regional differences in HBIs are reflected in the tissues of consumers. Tissue-specific assessment of HBI distributions has also revealed the presence of these lipids in muscle for the first time. This study represents the first report of HBI lipids in birds and provides evidence that these lipids are transferred across trophic levels and extends their potential use as chemical tracers beyond the ecology of aquatic organisms.     

Comparative effects of indole derivatives as antifouling agents on the growth of two marine diatom species

Antifouling agents, used to prevent biofouling, need to be assessed for their impacts on marine organisms and environment before the application. Diatoms are one of the main components of fouling biofilms, which play important roles in the formation of biofouling. Particularly, diatoms are also the important ingredients of primary production and present interest as ecotoxicological models in marine environment. In this study, two benthic diatoms Nitzschia closterium f. minutissima and Navicula climacospheniae, widely distributed in fouling biofilm, were used as models for screening the activities of potential antifoulants. Nine indole derivatives were tested and CuSO₄ was used as a reference. Indole derivatives showed significant anti-algal activities and the EC₅₀ values of most indole derivatives were lower than that of CuSO₄. Halogen substituent enhanced the anti-algal activities of compounds, and the most efficient compounds for N. closterium f. minutissima were gramine and 7-chloroindole with the EC₅₀ values of 1.94 and 2.1?mg/L, while for N. climacospheniae, 7-chloroindole and 6-bromoindole were the most efficient and the EC₅₀ values were 3.91 and 4.25?mg/L, respectively. In conclusion, indole derivatives would be one of the promising candidates as antifoulants and our results strengthened the need to perform antifouling activity assays and environment-friendly evaluations.     

Multivariate statistics as a tool for model-based prediction of floodplain vegetation and fauna

Robust prediction models for the spatial distribution of grassland vegetation, molluscs and carabids in a study area at the Middle Elbe (Germany) had to be generated by means of multivariate statistical methods. An appropriate study design has been developed. Data of all three taxons as well as numerous parameters of the abiotic environment were ascertained. Canonical correspondence analysis (CCA) detected clear dependencies between the occurrence of biotic objects and mainly hydrological parameters. By use of Arc/Info applications CANOGEN and CANORES, it was possible to extrapolate the models from the sample plots to the whole study area. The predicted spatial distribution of nearly all in the field studies examined species could be depicted with these instruments. Comparison between investigated and predicted distribution of species showed high correspondence.Robustness of the models was proved by interchanging model parameters for different study years and also in applying models at a second study area located 40 km upstream of the original study area.As a second method for further investigation, logistic regression was used to build generalised linear models (GLM) for potential indicator species in the study area.     

Swimming behavior of the marine copepodOithona davisae: internal control and search for environment

The swimming behavior of the marine cyclopoid copepodOithona davisae Ferrari and Orsi, collected in Tokyo Bay, Japan, between 1980 and 1983, was studied after acclimation to various food concentrations. Males and females exhibited forward and circular swimming movements. Males search mainly for mates, not for food. Their circular swimming behavior may serve for the mate search. The spiraling movement during mate-pursuit is peculiar to males. Circular swimming in females may function as a spontaneous search behavior for rich food areas and less crowded conditions. Females acclimated to a low food concentration, with net production about zero, responded sensitively to the increased food concentration by decreasing their swimming distance per unit time. Females acclimated to higher levels also responded similarly, but less sensitively. On the other hand, females kept without food exhibited no changes in swimming behavior and exhibited a stereotyped behavior at every food level. Females, when exposed to a low food level, may prefer to search for richer areas rather than capture food. The combined effect of the degree of internal activity (DIA) and the intensity of external stimulus (IES) determines the behavior pattern ofO. davisae. The behavioral response to IES depends on DIA.     

Assessing the current state of ecological connectivity in a large marine protected area system

The establishment of marine protected areas (MPAs) is a critical step in ensuring the continued persistence of marine biodiversity. Although the area protected in MPAs is growing, the movement of individuals (or larvae) among MPAs, termed connectivity, has only recently been included as an objective of many MPAs. As such, assessing connectivity is often neglected or oversimplified in the planning process. For promoting population persistence, it is important to ensure that protected areas in a system are functionally connected through dispersal or adult movement. We devised a multi-species model of larval dispersal for the Australian marine environment to evaluate how much local scale connectivity is protected in MPAs and determine whether the extensive system of MPAs truly functions as a network. We focused on non-migratory species with simplified larval behaviors (i.e., passive larval dispersal) (e.g., no explicit vertical migration) as an illustration. Of all the MPAs analyzed (approximately 2.7 million km²), outside the Great Barrier Reef and Ningaloo Reef, <50% of MPAs (46-80% of total MPA area depending on the species considered) were functionally connected. Our results suggest that Australia's MPA system cannot be referred to as a single network, but rather a collection of numerous smaller networks delineated by natural breaks in the connectivity of reef habitat. Depending on the dispersal capacity of the taxa of interest, there may be between 25 and 47 individual ecological networks distributed across the Australian marine environment. The need to first assess the underlying natural connectivity of a study system prior to implementing new MPAs represents a key research priority for strategically enlarging MPA networks. Our findings highlight the benefits of integrating multi-species connectivity into conservation planning to identify opportunities to better incorporate connectivity into the design of MPA systems and thus to increase their capacity to support long-term, sustainable biodiversity outcomes.     

Information indices as a tool for quantifying development of below-ground terrestrial ecosystems

Information indices from ecosystem network analysis (ENA) describe the size and organization of an ecosystem and are claimed to quantify ecosystem development [Ulanowicz, R.E., 1986, Growth and Development, Springler-Verslag, New York, 203 pp.]. To date, these indices were not used to describe a gradient of ecosystem development for a field situation. Here we used information indices to quantify soil succession with soils of different age on the island Schiermonnikoog, The Netherlands. We evaluated whether information indices describe ecosystem development as predicted by ENA.For the Island of Schiermonnikoog the biomasses of soil organisms and roots were measured on four stages of succession (0, 10, 25 and 100 years old soils). Organisms were grouped based on their feeding characteristics. With these data consumption, respiration, excretion, external input and output flows to, from and between groups were calculated. These flows, in turn, were used to calculate the information indices. Relative information indices describe the organization of an ecosystem; i.e. level of organisation (specialization of flows), diversity and evenness of flows, and disorganisation. Absolute indices describe both size (in terms of energy flow) and organisation of the system. System size is used to scale the absolute indices and will be analysed separately as well.We found that the absolute indices increased when succession processed, as predicted by theory. This pattern could have been due to the build-up of biomass, which apparently did not level off. Because the succession gradient deals mostly with young soils (0, 10 and 25 years old) and only one older field (100 years old), the gradient should include more soils of around 100 years old and older to exclude this possibility. Relative indices, on the other hand, increased initially, but then levelled off. We think that this was due to the strong aggregation of functional groups, especially at lower trophic levels, because information in some functional groups showed (expected) trends.Our results suggest that the absolute indices are able to describe ecological succession of terrestrial below-ground ecosystems. The relative indices, in contrast, appeared to be insensitive to subtle succesional changes.     

Intertype mark correlation function: A new tool for the analysis of species interactions

The spatial pattern of the different species in complex ecosystems reflects the underlying ecological processes. In this paper a second order moment function is proposed and tested to analyse the spatial distribution of a mark, which could be a tree characteristic such as diameter or height, between two different types of points, which could be two different tree species. The proposed function was a conditional density function based on the intertype K_rs(d) function, incorporating as test function the correlation of the marks between pairs composed of points of different types. The results obtained in simulated and real plots prove that the function is capable of revealing the scale at which spatial correlation of the mark between two types of points exists. The proposed function allows the spatial association between individuals of different species at different life stages to be identified. This analysis may reveal information on species ecology and interspecific interactions in forest ecosystems.     

Kelp as a trophic resource for marine suspension feeders: a review of isotope-based evidence

Kelp forests are enormously productive, and they and adjacent habitats support large populations of suspension feeders. What do these suspension feeders eat? Intuitively, we might expect that kelp primary production is a key form of trophic support for these animals. Indeed, a large and growing number of studies using carbon stable isotope data, typically collected over short time periods, have asserted that detritus from kelps is an important, and in some cases the main, food source for coastal benthic suspension feeders. This view has been incorporated into several textbooks and review papers covering kelp forest ecosystems, and loss of trophic support for benthic suspension feeders is now often invoked as an ecosystem consequence of top-down or other impacts on kelp forests. More direct evidence, however, suggests that these animals mainly eat phytoplankton and, in some cases, bacteria or zooplankton. Because isotope values of pure coastal phytoplankton, uncontaminated with detritus, are difficult to obtain, present studies have largely relied on single measurements from offshore environments or from the literature, which typically reflects offshore values. We review the evidence showing that phytoplankton isotope values can, and are expected to, vary widely in coastal waters and that inshore phytoplankton may often be enriched in ¹³C compared to offshore phytoplankton. This unaccounted-for variation may have systematically biased the results of such trophic studies toward finding large contributions of kelp detritus to suspension-feeder diets. We review some key stable isotope studies and put forth evidence for alternative explanations of the isotope patterns presented. Finally, we make recommendations for future isotope studies and describe several approaches for progress in this area. New techniques, particularly flow cytometry and compound-specific stable isotope analysis, provide ways to shed light on this interesting and important ecological issue.     

Competition for food and other niche-related studies of three species of salt-marsh foraminifera

The niches of 3 species of salt-marsh foraminifera, Allogromia laticollaris, Rosalina leei, and Spiroloculina hyalina were assessed in the laboratory. The 3 species reproduce within the following ranges: temperature (10° to 33°C), salinity (12 to 45‰) and pH (5 to 10). Competition for food among the 3 species was evaluated. S. hyalina did not compete with other species. Intraspecific competition (crowding) appears to be an important factor limiting the reproduction of A. laticollaris. Crowding seems to have little effect on the other 2 species. The feeding of foraminifera is affected by the quality and quantity of food organisms. The feeding rate of the species tested is directly related to concentration within a range of 10² to 10⁶ cells fed. S. hyalina is a bacterial feeder. A. laticollaris is a rare species which may become locally abundant when dominant species are missing. S. hyalina is also a rare species, which can bloom where the density of bacteria is relatively high and in the absence of competing species. R. leei is a stable, conspicuous species, whose moderate numbers are relatively unaffected by physical stress and competition. Some new laboratory data on Ammonia beccarii were obtained so that this species could be compared with the other studied. Differences in niches are graphically presented.     

Salinity effects on the coexistence of cryptic species: a case study on marine nematodes

The coexistence of four cryptic species of Rhabditis (Pellioditis) marina (Nematoda: Rhabditidae) at small geographical scale challenges ecological competition theory and was therefore studied in the laboratory at two different salinities, where their performance in combined cultures was compared with that in monospecies cultures. We found that three of the four cryptic species were able to coexist, but that interspecific interactions (competition and facilitation) were common. Salinity had an effect on these interactions, with a shift from contest to scramble competition. This shift may result from an increased population development of two of the four species at the lower salinity in the monospecific cultures. This experiment demonstrates that abiotic conditions may play an important role in achieving coexistence between cryptic species and can alter the interspecific interactions between them.     

Genetic mating system of the brown smoothhound shark (<Emphasis Type="Italic">Mustelus henlei</Emphasis>), including a literature review of multiple paternity in other elasmobranch species

Although an understanding of mating systems is thought to be an important component of long-term population management, these life history characteristics are poorly known in sharks. Here, we employ polymorphic microsatellite markers to test for the occurrence and prevalence of multiple paternity in a population of the brown smoothhound shark, Mustelus henlei. We analyzed litters from 14 females sampled from the Pacific coast of Baja California Sur. The minimum number of sires ranged from one to three with an average of 2.3 sires per litter. Regression analyses did not indicate a relationship between female body size and number of sires, or female body size and size of the litter. A review of the existing literature on genetic mating systems in sharks suggests that polyandry may be common and that reproductive behavior may have evolved from conflicting selection pressures between the sexes.     

Interaction and impacts of two introduced species on a soft-sediment marine assemblage in SE Tasmania

Introduced species are having major impacts in terrestrial, freshwater and marine ecosystems world-wide. It is increasingly recognised that effects of multiple species often cannot be predicted from the effect of each species alone, due to complex interactions, but most investigations of invasion impacts have examined only one non-native species at a time and have not addressed the interactive effects of multiple species. We conducted a field experiment to compare the individual and combined effects of two introduced marine predators, the northern Pacific seastar Asterias amurensis and the European green crab Carcinus maenas, on a soft-sediment invertebrate assemblage in Tasmania. Spatial overlap in the distribution of these invaders is just beginning in Tasmania, and appears imminent as their respective ranges expand, suggesting a strong overlap in food resources will result from the shared proclivity for bivalve prey. A. amurensis and C. maenas provide good models to test the interaction between multiple introduced predators, because they leave clear predator-specific traces of their predatory activity for a number of common prey taxa (bivalves and gastropods). Our experiments demonstrate that both predators had a major effect on the abundance of bivalves, reducing populations of the commercial bivalves Fulvia tenuicostata and Katelysia rhytiphora. The interaction between C. maenas and A. amurensis appears to be one of resource competition, resulting in partitioning of bivalves according to size between predators, with A. amurensis consuming the large and C. maenas the small bivalves. At a large spatial scale, we predict that the combined effect on bivalves may be greater than that due to each predator alone simply because their combined distribution is likely to cover a broader range of habitats. At a smaller scale, in the shallow subtidal, where spatial overlap is expected to be most extensive, our results indicate the individual effects of each predator are likely to be modified in the presence of the other as densities increase. These results further highlight the need to consider the interactive effects of introduced species, especially with continued increases in the number of established invasions.Communicated by M.S. Johnson, Crawley