Biological benthic tools as indicators of coastal marine ecosystems health

Coastal marine ecosystems are increasingly subjected to environmental stress and degradation due to pollution. Several research programmes have addressed this problem and produced relevant data sets for specific areas, often including consistent sets of environmental and biological variables. The value of existing information gathered from these types of data can be largely increased by combining them into a common data set to determine globally applicable relationships. To perform this exercise, the Intergovernmental Oceanographic Commission (IOC) of UNESCO has recently formed the Ad hoc Study Group on Benthic Indicators (http://www.ioc.unesco.org/benthicindicators) with the aim of developing robust indicators of benthic health. In this paper, initial products and ongoing activities of this international initiative are described and discussed. An expansion of initial IOC/UNESCO research on benthic fauna-organic carbon relationships is also presented. As part of this follow-up research, the relationship between total organic carbon concentrations of sediment and abundance, biomass and species diversity of benthic macrofauna was evaluated using data sets from 2 different regions of the world comprising 3 different coastal marine environments. The ability of identifying threshold levels in selected variables that could serve as indicators of related adverse environmental conditions leading to stress in the benthos is envisaged within the frame of a larger joint analysis, carried out by the IOC/UNESCO Study Group on Benthic Indicators, of merged data sets from several coastal regions worldwide.     

Trophic state,ecosystem efficiency and biodiversity of transitional aquatic ecosystems: analysis of environmental quality based on different benthic indicators

Estuaries and coastal lagoons are characterized by a strong spatial and temporal variability of physicochemical characteristics and productivity patterns. In these environments, the magnitude and direction of the ecological responses to inorganic nutrient increase (i.e. eutrophication) are difficult to predict. In the framework of the project, New Indicators of Trophic state and environmental quality of marine coastal ecosystems and transitional environments (NITIDA), we analysed benthic indicators of trophic state, ecosystem efficiency, and environmental quality in four different transitional environments. The trophic state of the sediments was assessed in terms of quantity and bioavailability of sediment organic C pools; ecosystem efficiency was determined in terms of the prokaryote efficiency in exploiting enzymatycally degraded organic C; environmental quality was determined in terms of meiofaunal diversity. Here, we provide a synopsis of the results obtained and a meta-analysis of the scores assessments obtained using the different ecological indicators of environmental quality and demonstrate that trophic state, ecosystem efficiency, and biodiversity in transitional ecosystems are closely linked. We conclude that the assessment of the environmental quality of transitional ecosystems should be based upon a battery of trophic state indicators and ‘sensors’ of ecosystem functioning, efficiency, and quality.     

Trophic state, ecosystem efficiency and biodiversity of transitional aquatic ecosystems: analysis of environmental quality based on different benthic indicators

Estuaries and coastal lagoons are characterized by a strong spatial and temporal variability of physicochemical characteristics and productivity patterns. In these environments, the magnitude and direction of the ecological responses to inorganic nutrient increase (i.e. eutrophication) are difficult to predict. In the framework of the project, New Indicators of Trophic state and environmental quality of marine coastal ecosystems and transitional environments (NITIDA), we analysed benthic indicators of trophic state, ecosystem efficiency, and environmental quality in four different transitional environments. The trophic state of the sediments was assessed in terms of quantity and bioavailability of sediment organic C pools; ecosystem efficiency was determined in terms of the prokaryote efficiency in exploiting enzymatycally degraded organic C; environmental quality was determined in terms of meiofaunal diversity. Here, we provide a synopsis of the results obtained and a meta-analysis of the scores assessments obtained using the different ecological indicators of environmental quality and demonstrate that trophic state, ecosystem efficiency, and biodiversity in transitional ecosystems are closely linked. We conclude that the assessment of the environmental quality of transitional ecosystems should be based upon a battery of trophic state indicators and 'sensors' of ecosystem functioning, efficiency, and quality.     

Relationship between depth, sediment, latitude, and the structure of benthic infaunal assemblages on the mainland shelf of southern California

A regional benthic survey was conducted in 1994, and the data were used to assess the relationship among three habitat factors (depth, sediment grain size, and latitude) and the distribution of benthic infaunal assemblages on the southern California coastal shelf. Benthic samples were collected with a 0.1 m² Van Veen grab from 251 sites on the continental shelf (10–200 m deep) from Point Conception, California, to the United States–Mexico international border. The relationship between habitat and assemblages was investigated by conducting a Q-mode cluster analysis to define groups of stations with similar species composition and then examining whether differences were present in physical habitat attributes among those groups of stations. Analysis of data from 175 uncontaminated sites yielded four habitat-related benthic infaunal assemblages along the southern California coastal shelf: a shallow-water assemblage from 10–32 m, a mid-depth assemblage between 32 and 115 m, and two deep-water (115–200 m) assemblages, one in fine and one in coarse sediments. These empirically defined points in the depth and sediment grain size gradients can be used to define reference habitats for the development of biocriteria. Benthic abundance and diversity were greatest in the mid-depth assemblage, conforming to predictions for benthic assemblages in regions of upwelling. Within the 500 km of coastline examined, latitude was not an important factor in defining assemblages. Received: 3 December 1999 / Accepted: 9 October 2000     

137 Cs在我国滨海核电周边海洋生物的富集及生态风险研究

铯-137(~(137)Cs)是滨海核电站液态流出物中主要人工放射性核素和重要监控指标之一,易被水生生物累积,有关核电周边海域内海洋生物的核素富集状况备受关注。通过分析海洋生物富集放射性~(137)Cs的方式、生物富集系数的种群特征、人工放射性核素在生物体内的辐射剂量率状况,结果显示:1)滨海核电周边海域内~(137)Cs的放射性水平较低; 2)海洋生物对于~(137)Cs的富集未呈现显著的种群规律; 3)目前对放射性铯的富集能力较高的生物主要是底栖生物; 4)核电厂周边海域内海洋生物通常未达到可导致电离辐射损伤的辐射剂量率水平。随着滨海核电在我国的大力发展,对能够快速反映环境放射性状况的指示生物的筛选、生物放射性质量安全及其生态健康风险需进一步关注。     

The application of predicted habitat models to investigate the spatial ecology of demersal fish assemblages

Benthic habitats are known to influence the abundance and richness of demersal fish assemblages; however, little is known about how habitat structure and composition influences these distributions at very fine scales. We examined how the benthic environment structures marine fish assemblages using high-resolution bathymetry and accurate predicted benthic habitat maps. Areas characterised by a mosaic of habitat patches supported the highest richness of demersal fishes. A total of 37.4% of the variation in the distribution of the fish assemblage was attributed to 6 significant variables. Depth explained 23.0% of the variation, with the boulders explaining 12.6% and relief 1.4%. The remaining measures (seawhips, light/exposure and solid reef) provided a small (<1.0%) but significant contribution. Identifying components of the benthic environment important in structuring fish assemblages and understanding how they influence the spatial distribution of marine fishes is imperative for better management of demersal fish populations.     

Size,spatial, and bathymetrical distribution of the ascidian Halocynthia papillosa in Mediterranean coastal bottoms: benthic–pelagic coupling implications

Benthic suspension feeders are abundant in Mediterranean coastal environments, though most of them are threatened due to overexploitation, climate change impacts, and unregulated diving or fishing practices. Little is known about most of the coastal communities in terms of large-scale distribution and realistic benthic–pelagic coupling implications, which are keys to understand and manage those threatened ecosystems. The active suspension feeder Halocynthia papillosa (one of the most common ascidian species of the Mediterranean Sea) was selected as a model organism to help to understand the ecological role in benthic–pelagic coupling processes and its importance as a carbon sink (an essential ecosystem service). The spatial and bathymetrical distribution of this organism has been studied using remotely operated vehicle video transects. The species was distributed throughout the study area, with a maximum density of 4 specimens m^?2. The highest abundances and the biggest sizes were observed on the range of 20–50 m depth. The role as carbon and nitrogen sink of this suspension feeder has been quantified coupling distribution data with existing in situ studies of feeding and respiration. Along the 1.24 ha of the study area, H. papillosa yearly ingested 519.4 g C and 31.4 g N and retained 20.2 g C. As long as the physiological data are known, this new methodology could be very useful in assessing bentho–pelagic links and the capacity of being C and N sinks of a wide range of species. This new approach may be essential for the future management of benthic communities.     

Fine-scale habitat modeling of a top marine predator: do prey data improve predictive capacity?

Predators and prey assort themselves relative to each other, the availability of resources and refuges, and the temporal and spatial scale of their interaction. Predictive models of predator distributions often rely on these relationships by incorporating data on environmental variability and prey availability to determine predator habitat selection patterns. This approach to predictive modeling holds true in marine systems where observations of predators are logistically difficult, emphasizing the need for accurate models. In this paper, we ask whether including prey distribution data in fine-scale predictive models of bottlenose dolphin (Tursiops truncatus) habitat selection in Florida Bay, Florida, U.S.A., improves predictive capacity. Environmental characteristics are often used as predictor variables in habitat models of top marine predators with the assumption that they act as proxies of prey distribution. We examine the validity of this assumption by comparing the response of dolphin distribution and fish catch rates to the same environmental variables. Next, the predictive capacities of four models, with and without prey distribution data, are tested to determine whether dolphin habitat selection can be predicted without recourse to describing the distribution of their prey. The final analysis determines the accuracy of predictive maps of dolphin distribution produced by modeling areas of high fish catch based on significant environmental characteristics. We use spatial analysis and independent data sets to train and test the models. Our results indicate that, due to high habitat heterogeneity and the spatial variability of prey patches, fine-scale models of dolphin habitat selection in coastal habitats will be more successful if environmental variables are used as predictor variables of predator distributions rather than relying on prey data as explanatory variables. However, predictive modeling of prey distribution as the response variable based on environmental variability did produce high predictive performance of dolphin habitat selection, particularly foraging habitat.     

A decision-support system in ICZM for protecting the ecosystems: integration with the habitat directive

This paper describes a decision-support system based on landscape ecology and focused on the study of ecosystems’ health. System capabilities are illustrated with three cases of integrated coastal zone management (ICZM), in the Adriatic Sea (Italy): the lagoon of Venice and the Rimini and Ancona coastal areas. Indicators and indices are developed with a focus on sub-regional and local problems in coastal management, with a multi-scale approach based on landscape and seascape ecology. Land-use changes of the coastal areas were detected by analyzing two sets of satellite images. Indices combining satellite imagery, socio-economic and environmental indicators, and landscape and seascape maps were created, showing ecological changes, habitat loss and gaps in conservation policy. The approach used provides means for the identification of conflicts and for the assessment of sustainability. Results show that the lagoon of Venice plays an important role in mitigating and compensating the impacts of human activities, and needs to be protected and restored. The Rimini area shows high ecological footprint and development-intensity and low biocapacity. The Ancona area needs the protection of its natural coastal space from potential sources of anthropogenic impacts to maintain its sustainability. A model of environment changes is critical for formulating effective environmental policies and management strategies. The developed decision-support system provides a suitability map per each area analyzed, which can be used in order to maximize different policy objectives and reduce coastal conflicts.     

Population distribution and structure of the free-living nematodes of Long Island Sound

The distribution and structure of nematode populations in 4 sedimentary environments (muds, muddy sands, fine sands and medium-coarse sands) in Long Island Sound were studied. Mean population densities were highest in muds and muddy sands. Cluster analysis suggested the presence of two basic faunistic units; a mud unit characterized by high species dominance, low species diversity and low species endemism, and a sand unit characterized by low species dominance, high species diversity and high species endemism. Species diversity in all habitats was a direct function of both species richness and equitability. Limited niche separation among deposit feeders, usually the dominant nematode trophic type in muddy sediments, is proposed as the cause for the high species dominance so often characteristic of shallow marine muds. The study afforded the opportunity to examine the quantitative and qualitative aspects of population structure in relation to environmental impact (as indicated by large differences in the heavy metal and organic carbon concentrations within each of the 4 sedimentary regimes). Within each sediment type no differences in population densities, species composition or species diversity of nematodes existed between heavily impacted and apparently non-impacted sediments, or between Long Island Sound and similar coastal regions. These findings cast doubt on (1) the use of heavy metal and organic carbon concentrations as indicators of environmental stress for marine nematodes; (2) the use of diversity indices alone as indicators of environmental deterioration; and (3) the usefulness of field monitoring studies alone for the assessment of pollution impact on marine nematodes.Contribution no. 100 from the Institute of Marine and Atmospheric Sciences, City College of New YorkCommunicated by M.R. Tripp, Newark     

平原河网地区大型底栖动物群落结构及其与环境因子的关系

大型底栖无脊椎动物是河流生态系统的重要组成生物,具有活动范围相对固定、生命周期较长、生活习性相对稳定等特点,可有效指示河流水质和水生态系统健康状况。有关大型底栖生物群落结构特征及其与水环境之间的关系研究一直是河流生态系统的研究热点。底栖动物具有较强的地域性,其群落结构特征受当地的自然环境特征和社会经济发展程度的双重因素影响。为研究典型平原河网地区的底栖动物群落结构及对水环境状况的响应特征,在上海市选取了83个河道断面进行大型底栖动物采样分析,共获取底栖动物20个分类单位（种）,其中软体动物10种,环节动物6种,节肢动物4种。上海河道底栖动物群落结构总体呈现结构单一、物种丰富度低、高度耐污性等显著特征,环节动物的栖息密度和出现频率均最高。城市化水平的空间差异性直接影响底栖动物空间分布的异质性,由市区至近郊、远郊,物种数从11种逐渐上升至15种,而栖息密度则由8 776.3个/m2下降至690.3个/m2。底栖动物群落结构的空间分布特征与水质理化指标的空间分布特征具有良好的对应性,水质空间变化导致环节动物和软体动物、节肢动物的空间分布存在一定交错性,耐污性较强的环节动物主要分布在有机污染重、溶解氧低的市区河道断面,而喜清洁环境的软体动物和节肢动物主要分布在水质较好的郊区断面。寡毛纲物种的栖息密度与溶解氧质量浓度呈显著负相关性。     

江苏省不同营养状况湖泊底栖动物群落结构与多样性比较

为了解江苏省湖泊底栖动物群落结构和多样性并研究其对水环境质量变化的响应,于2012年春秋两季对江苏省16个湖泊51个采样点湖泊底栖动物群落结构与多样性以及湖泊综合营养状态指数进行调查,分析水质指标与底栖动物指数间Pearson相关关系。结果表明,江苏省16个湖泊营养状态指数范围为35.5~66.4,其中约81.2%的湖泊处于轻度-中度富营养状态,表明水质从好到中度污染;湖泊底栖动物优势种为寡毛类的霍甫水丝蚓(Limnodrilus hoffmeisteri),优势度为13.0%;香浓多样性指数(Shannon-Wiener diversity index)范围为0.00~2.20,级别范围由极贫乏到较丰富状态,表明水质污染程度从重度到轻度污染。从全省尺度看,水质评价结果与生物学(香浓多样性指数、Pielou均匀度指数和Biotic Index(BI)指数)评价结果存在一定差异。与历史数据相比,江苏省湖泊底栖动物清洁敏感物种减少甚至消失,总体群落结构趋于小型化。16个湖泊水体总氮和总磷与底栖动物密度呈显著负相关,而综合营养状态指数与底栖动物指数(香浓多样性指数、Pielou均匀度指数和BI指数)间关系不显著。上述研究结果表明综合营养状态指数无法完全客观反映湖泊水生态健康状况,因此需要综合水质、水文、水生生物、生境状况等因素发展新的评价指标体系。     

Response of benthic foraminifera to heavy metal contamination in marine sediments (Sicilian coasts,Mediterranean Sea)

To examine the suitability of benthic foraminifera and their test deformations as bioindicators of pollution in coastal marine environments, we studied foraminifera and metal concentrations in 72 marine sediment samples, collected from the inner shelf along the Sicilian coast (Gulfs of Palermo and Termini) and on the south-eastern coast of Lampedusa Island. These areas are characterised by different environmental conditions. On the basis of pollution sources and foraminiferal assemblages, we recognised different zones in the Gulf of Palermo. The most polluted zones showed high metal concentrations, and low diversity of benthic foraminifera with species typical of stressed environments. By contrast, the lowest polluted zones showed a high population density and the highest percentages of epiphytes. Epiphytes were abundant where a Posidonia oceanica meadow was present and decreased in the most polluted zones. Sediments of the Gulf of Termini and Lampedusa exhibited high percentages of benthic foraminifera typical of well-oxygenated waters and low concentrations of metals, with the exception of sites located near sewage outfalls and harbour areas. Furthermore, even though deformed tests are commonly known in natural stressed environmental conditions, this study shows that in the most polluted zones, benthic foraminifera were characterised by the highest percentages of deformed individuals.     

Add-on conservation benefits of marine territorial user rights fishery policies in central Chile.

To combine the rational use of marine benthic resources and economic development of small-scale fishers, Chile passed legislation in 1991 establishing a comanagement policy that grants exclusive territorial user rights for fisheries (TURFs) to artisanal fisher organizations in well-defined inshore coastal areas, known as Management and Exploitation Areas for Benthic Resources (MEABRs). In general the policy has been proclaimed a management and economic success because benthic resource abundances have increased inside MEABRs in comparison with open-access areas. However, there is a lack of studies assessing the impact of this management policy on nontargeted subtidal species and community assemblages and the policy's implications for biodiversity and conservation. This study starts to fill this gap and links the allocation of TURFs for benthic resources with add-on conservation benefits for species that are not directly linked with the fishery policy. Comparative subtidal surveys inside vs. outside MEABRs were used to assess the effects of three MEABRs on managed targeted benthic species, biodiversity (species richness), and community assemblages in central Chile. Surveys focused exclusively on subtidal kelp forest habitats dominated by Lessonia trabeculata, spanning 4-12 m in depth and with similar levels of habitat complexity. The study comprised: (1) quantification of kelp forest complexity, (2) understory survey of sessile species, (3) quantification of conspicuous benthic macroinvertebrates, including those under management, and (4) quantification of reef-fish species inside the kelp habitat. Results showed population enhancement of target-managed invertebrates inside MEABRs. Moreover, reef-fish species were significantly more diverse and abundant inside MEABRs, and community assemblages of nontarget benthic invertebrates and reef fish were significantly different inside vs. outside MEABRs. The comanagement of inshore benthic resources in Chile, through MEABRs aims for the sustainability of invertebrate and algae stocks. However, our study shows that this management tool, which in practice restricts access to the entire management area, provides important conservation add-on effects for species that are not the focus of the management policies. Therefore, in Chile, the hundreds of already established MEABRs could represent an important ancillary network, which complements the biodiversity objectives of fully protected areas such as no-take marine protected areas or others.     

Applications of artificial neural networks for patterning and predicting aquatic insect species richness in running waters

Two artificial neural networks (ANNs), unsupervised and supervised learning algorithms, were applied to suggest practical approaches for the analysis of ecological data. Four major aquatic insect orders (Ephemeroptera, Plecoptera, Trichoptera, and Coleoptera, i.e. EPTC), and four environmental variables (elevation, stream order, distance from the source, and water temperature) were used to implement the models. The data were collected and measured at 155 sampling sites on streams of the Adour–Garonne drainage basin (South-western France). The modelling procedure was carried out following two steps. First, a self-organizing map (SOM), an unsupervised ANN, was applied to classify sampling sites using EPTC richness. Second, a backpropagation algorithm (BP), a supervised ANN, was applied to predict EPTC richness using a set of four environmental variables. The trained SOM classified sampling sites according to a gradient of EPTC richness, and the groups obtained corresponded to geographic regions of the drainage basin and characteristics of their environmental variables. The SOM showed its convenience to analyze relationships among sampling sites, biological attributes, and environmental variables. After accounting for the relationships in data sets, the BP used to predict the EPTC richness with a set of four environmental variables showed a high accuracy (r=0.91 and r=0.61 for training and test data sets respectively). The prediction of EPTC richness is thus a valuable tool to assess disturbances in given areas: by knowing what the EPTC richness should be, we can determine the degree to which disturbances have altered it. The results suggested that methodologies successively using two different neural networks are helpful to understand ecological data through ordination first, and then to predict target variables.     

Seasonal study of planktonic copepods and their benthic resting eggs in northern California coastal waters

Few investigations have examined the occurrence of zooplankton resting eggs in the sea bed of waters deeper than 20 m. In this study the distribution and abundance of planktonic copepods and their benthic resting eggs in coastal waters off northern California, U.S.A., were determined and related to environmental parameters (temperature, salinity, depth, and sediment grain size). Sediment cores, net tows, and CTD profiles were obtained in April and October 1989, and February, April, and October 1990. Water depths in the study area ranged from approximately 60 to 120 m. The mean abundance of eggs was as high as 1.2×10⁵ m^-2 for Acartia clausi Giesbrecht and 1.9×10⁵ m^-2 for Tortanus discaudatus Thompson and Scott. These egg concentrations are comparable to those reported previously for shallower more protected regions. The abundance of eggs in the sediments decreased with increasing depth of the water column. For the region as a whole, eggs were least abundant in muddy sediments. The mean abundance of eggs in the sea bed also varied seasonally and annully. Benthic resting eggs of A. clausi were more abundant in April 1989 than in April 1990, and adults of the species were never found in the plankton samples. The lack of adults is not unusual since results of previous studies indicate that A. clausi is a cold-water species, and in this region water temperatures are colder in summer, than in winter, due to upwelling. Temperature and salinity data indicated that the upwelling season had commenced by the time of the April 1990, but not the April 1989 sampling. Thus, the reduced abundance of benthic eggs in April 1990 may have been due to egg-hatching in response to reduced temperatures. The results suggest that the presence of A. clausi in coastal waters off northern California is linked to recruitment from benthic resting eggs.     

Significance of ATP,carbon, and caloric content of meiobenthic nematodes in partitioning benthic biomass

Benthic, free-living marine nematodes from two stations, one subtidal, one intertidal, in the North Inlet Estuary, South Carolina, USA, have been characterized by measurement of adenosine triphosphate (ATP), carbon, caloric content, and ash-free dry weight. Two methods of extracting the organisms from the sediment were used. Resulting carbon to ATP ratios and population density data from ongoing North Inlet meiofauna studies show that the nematodes account for 0.11 to 6.33 g ATP per g dry weight of sediment, varying seasonally. The percentage of nematode ATP/g sediment is higher in the winter and lowest in the summer, and accounts for 68% to over 90% of the total sediment ATP. The findings of this study indicate that meiofauna, particularly nematodes, can no longer be overlooked as a separate entity in attempts to partition benthic systems.Contribution No. 173 from the Belle W. Baruch Institute for Marine Biology and Coastal Research. Research supported by Oceanography Section, National Science Foundation, NSF Grant DES 72-01573 AO1.     

Trophic structure of coastal Antarctic food webs associated with changes in sea ice and food supply

Predicting the dynamics of ecosystems requires an understanding of how trophic interactions respond to environmental change. In Antarctic marine ecosystems, food web dynamics are inextricably linked to sea ice conditions that affect the nature and magnitude of primary food sources available to higher trophic levels. Recent attention on the changing sea ice conditions in polar seas highlights the need to better understand how marine food webs respond to changes in such broad-scale environmental drivers. This study investigated the importance of sea ice and advected primary food sources to the structure of benthic food webs in coastal Antarctica. We compared the isotopic composition of several seafloor taxa (including primary producers and invertebrates with a variety of feeding modes) that are widely distributed in the Antarctic. We assessed shifts in the trophic role of numerically dominant benthic omnivores at five coastal Ross Sea locations. These locations vary in primary productivity and food availability, due to their different levels of sea ice cover, and proximity to polynyas and advected primary production. The delta15N signatures and isotope mixing model results for the bivalves Laternula elliptica and Adamussium colbecki and the urchin Sterechinus neumeyeri indicate a shift from consumption of a higher proportion of detritus at locations with more permanent sea ice in the south to more freshly produced algal material associated with proximity to ice-free water in the north and east. The detrital pathways utilized by many benthic species may act to dampen the impacts of large seasonal fluctuations in the availability of primary production. The limiting relationship between sea ice distribution and in situ primary productivity emphasizes the role of connectivity and spatial subsidies of organic matter in fueling the food web. Our results begin to provide a basis for predicting how benthic ecosystems will respond to changes in sea ice persistence and extent along environmental gradients in the high Antarctic.     

Intertidal invertebrates locally enhance primary production

The contribution of autochthonous vs. allochthonous inputs to productivity is an important determinant of ecosystem function across multiple habitats. In coastal marine systems, nutrients are thought to come primarily from the upwelling of deep, nutrient-rich water. Using experimental manipulations of a dominant tide pool animal, the mussel Mytilus californianus, I show that the presence of mussels greatly increases the supply of inorganic nitrogen and phosphorus. Mussels further had a direct effect on productivity: benthic microalgal abundance increased by a factor of 4-8, while the growth of a red alga was four times greater in the presence of mussels. The increase in nitrite and nitrate associated with mussels further suggests nitrifying activity by microbes. These findings have broad implications for coastal marine systems, including that regenerated nutrients may contribute more to productivity than previously recognized and that the presence of animal-generated nutrients sets the stage for numerous positive interactions.