Spatial patterns and predictors of trophic control in marine ecosystems

A key question in ecology is under which conditions ecosystem structure tends to be controlled by resource availability vs. consumer pressure. Several hypotheses derived from theory, experiments and observational field studies have been advanced, yet a unified explanation remains elusive. Here, we identify common predictors of trophic control in a synthetic analysis of 52 observational field studies conducted within marine ecosystems across the Northern Hemisphere and published between 1951 and 2014. Spatial regression analysis of 45 candidate variables revealed temperature to be the dominant predictor, with unimodal effects on trophic control operating both directly (r² = 0.32; P < 0.0001) and indirectly through influences on turnover rate and quality of primary production, biodiversity and omnivory. These findings indicate that temperature is an overarching determinant of the trophic dynamics of marine ecosystems, and that variation in ocean temperature will affect the trophic structure of marine ecosystems through both direct and indirect mechanisms.     

The diversity of small eukaryotic phytoplankton (< or =3 microm) in marine ecosystems

Small cells dominate photosynthetic biomass and primary production in many marine ecosystems. Traditionally, picoplankton refers to cells ≤2 μm. Here we extend the size range of the organisms considered to 3 μm, a threshold often used operationally in field studies. While the prokaryotic component of picophytoplankton is dominated by two genera, Prochlorococcus and Synechococcus , the eukaryotic fraction is much more diverse. Since the discovery of the ubiquitous Micromonas pusilla in the early 1950s, just over 70 species that can be <3 μm have been described. In fact, most algal classes contain such species. Less than a decade ago, culture-independent approaches (in particular, cloning and sequencing, denaturing gradient gel electrophoresis, FISH) have demonstrated that the diversity of eukaryotic picoplankton is much more extensive than could be assumed from described taxa alone. These approaches revealed the importance of certain classes such as the Prasinophyceae but also unearthed novel divisions such as the recently described picobiliphytes. In the last couple of years, the first genomes of photosynthetic picoplankton have become available, providing key information on their physiological capabilities. In this paper, we discuss the range of methods that can be used to assess small phytoplankton diversity, present the species described to date, review the existing molecular data obtained on field populations, and end up by looking at the promises offered by genomics.     

The functional role of biodiversity in ecosystems: incorporating trophic complexity

Understanding how biodiversity affects functioning of ecosystems requires integrating diversity within trophic levels (horizontal diversity) and across trophic levels (vertical diversity, including food chain length and omnivory). We review theoretical and experimental progress toward this goal. Generally, experiments show that biomass and resource use increase similarly with horizontal diversity of either producers or consumers. Among prey, higher diversity often increases resistance to predation, due to increased probability of including inedible species and reduced efficiency of specialist predators confronted with diverse prey. Among predators, changing diversity can cascade to affect plant biomass, but the strength and sign of this effect depend on the degree of omnivory and prey behaviour. Horizontal and vertical diversity also interact: adding a trophic level can qualitatively change diversity effects at adjacent levels. Multitrophic interactions produce a richer variety of diversity-functioning relationships than the monotonic changes predicted for single trophic levels. This complexity depends on the degree of consumer dietary generalism, trade-offs between competitive ability and resistance to predation, intraguild predation and openness to migration. Although complementarity and selection effects occur in both animals and plants, few studies have conclusively documented the mechanisms mediating diversity effects. Understanding how biodiversity affects functioning of complex ecosystems will benefit from integrating theory and experiments with simulations and network-based approaches.     

Damped trophic cascades driven by fishing in model marine ecosystems

The largest perturbation on upper trophic levels of many marine ecosystems stems from fishing. The reaction of the ecosystem goes beyond the trophic levels directly targeted by the fishery. This reaction has been described either as a change in slope of the overall size spectrum or as a trophic cascade triggered by the removal of top predators. Here we use a novel size- and trait-based model to explore how marine ecosystems might react to perturbations from different types of fishing pressure. The model explicitly resolves the whole life history of fish, from larvae to adults. The results show that fishing does not change the overall slope of the size spectrum, but depletes the largest individuals and induces trophic cascades. A trophic cascade can propagate both up and down in trophic levels driven by a combination of changes in predation mortality and food limitation. The cascade is damped as it comes further away from the perturbed trophic level. Fishing on several trophic levels leads to a disappearance of the signature of the trophic cascade. Differences in fishing patterns among ecosystems might influence whether a trophic cascade is observed.     

Multi-level trophic cascades in a heavily exploited open marine ecosystem

Anthropogenic disturbances intertwined with climatic changes can have a large impact on the upper trophic levels of marine ecosystems, which may cascade down the food web. So far it has been difficult to demonstrate multi-level trophic cascades in pelagic marine environments. Using field data collected during a 33-year period, we show for the first time a four-level community-wide trophic cascade in the open Baltic Sea. The dramatic reduction of the cod (Gadus morhua) population directly affected its main prey, the zooplanktivorous sprat (Sprattus sprattus), and indirectly the summer biomass of zooplankton and phytoplankton (top-down processes). Bottom-up processes and climate-hydrological forces had a weaker influence on sprat and zooplankton, whereas phytoplankton variation was explained solely by top-down mechanisms. Our results suggest that in order to dampen the occasionally harmful algal blooms of the Baltic, effort should be addressed not only to control anthropogenic nutrient inputs but also to preserve structure and functioning of higher trophic levels.     

Biomass diversity and stability of food webs in aquatic ecosystems

The diversity–stability hypothesis in ecology asserts that biodiversity begets stability of ecological systems. This hypothesis has been supported by field studies on primary producers in grasslands, in which the interaction between species is mostly competition. As to ecosystems with multitrophic predatory interaction, however, no definite consensus has been arrived at for the relation between trophic diversity and ecosystem stability. The stability index suitable to ecosystems with predatory interaction is given by MacArthurs idea of stability and its formulation by Rutledge et al. More suitable indices of stability (relative conditional entropy) are proposed in this study for the comparison of different ecosystems, and the validity of the diversity–stability hypothesis for food webs (networks of predation) with many trophic compartments in natural aquatic ecosystems is examined. Results reveal that an increase in the biomass diversity of trophic compartments causes an increase in the whole systemic stability of food webs in aquatic ecosystems. Hence, evidence of the whole systemic validity of the diversity–stability hypothesis for natural aquatic ecosystems with ubiquitous multitrophic predatory interaction was obtained for the first time.     

Climate change alters stability and species potential interactions in a large marine ecosystem

We have little empirical evidence of how large‐scale overlaps between large numbers of marine species may have altered in response to human impacts. Here, we synthesized all available distribution data (>1 million records) since 1992 for 61 species of the East Australian marine ecosystem, a global hot spot of ocean warming and continuing fisheries exploitation. Using a novel approach, we constructed networks of the annual changes in geographical overlaps between species. Using indices of changes in species overlap, we quantified changes in the ecosystem stability, species robustness, species sensitivity and structural keystone species. We then compared the species overlap indices with environmental and fisheries data to identify potential factors leading to the changes in distributional overlaps between species. We found that the structure of the ecosystem has changed with a decrease in asymmetrical geographical overlaps between species. This suggests that the ecosystem has become less stable and potentially more susceptible to environmental perturbations. Most species have shown a decrease in overlaps with other species. The greatest decrease in species overlap robustness and sensitivity to the loss of other species has occurred in the pelagic community. Some demersal species have become more robust and less sensitive. Pelagic structural keystone species, predominately the tunas and billfish, have been replaced by demersal fish species. The changes in species overlap were strongly correlated with regional oceanographic changes, in particular increasing ocean warming and the southward transport of warmer and saltier water with the East Australian Current, but less correlated with fisheries catch. Our study illustrates how large‐scale multispecies distribution changes can help identify structural changes in marine ecosystems associated with climate change.     

海洋生物多样性损害与沿海地区经济增长关系实证研究

海洋生物多样性是海洋生态系统服务的基础,保护海洋生物多样性不仅对维持地球生态系统的功能至关重要,也与人类福祉密切相关。基于沿海11个省区生态系统亚健康程度指标和物种多样性损害指标,运用面板回归模型对中国沿海地区经济增长与海洋生物多样性损害的关系进行实证考察。研究结果表明：(1)海洋生态系统亚健康程度与沿海地区经济增长之间存在显著的线性关系,随着经济增长,典型海洋生态系统亚健康状态占比呈现出持续上升趋势。此外,实施排污费制度和建立海洋自然保护区有利于抑制海洋生态系统的恶化。(2)海洋物种多样性损害与沿海地区经济增长之间存在显著“倒U”型关系,随着经济增长,海洋物种多样性损害呈现先上升后下降的态势,转折点为人均GDP 45145元,目前海南省、广西壮族自治区、河北省未跨过转折点。此外,排污费制度有利于抑制海洋物种多样性损害,而沿海地区目前的产业结构加重了海洋物种多样性损害。根据实证分析结果,海洋生态系统健康尚未出现拐点,沿海地区经济增长如果建立在对生态环境破坏的基础上,则势必会造成生物多样性的损害。因此从规范海域利用方式,完善海岸生态保护红线划定,加强生态系统的监测与管理,保持绿色可持续的...     

Management strategies for sustainable invertebrate fisheries in coastal ecosystems of Galicia (NW Spain)

Artisanal coastal invertebrate fisheries in Galicia are socio-economically important and ecologically relevant. Their management, however, has been based on models of fish population dynamics appropriate for highly mobile demersal or pelagic resources and for industrial fisheries. These management systems focus on regulating fishing effort, but in coastal ecosystems activities that change or destruct key habitats may have a greater effect on population abundance than does fishing mortality. The Golfo Artabro was analysed as a representative example of a coastal ecosystem in Galicia, and the spider crab Maja squinado used as a model of an exploited coastal invertebrate, for which shallow coastal areas are key habitats for juvenile stages. The commercial legal gillnet fishery for the spider crab harvests adults during their reproductive migrations to deep waters and in their wintering habitats. Illegal fisheries operate in shallow waters. The annual rate of exploitation is >90%, and <10% of the primiparous females reproduce effectively at least once. A simple spatially-explicit cohort model was constructed to simulate the population dynamics of spider crab females. Yield- and egg-per-recruit analyses corresponding to different exploitation regimes were performed to compare management policies directed to control the fishing effort or to protect key habitats. It was found that the protection of juvenile habitats could allow increases in yield and reproductive effort higher than in the present system, with such protection based in the control of the fishing effort of the legal fishery. Additionally, there is an urgent need for alternative research and management strategies in artisanal coastal fisheries based on the implementation of a system of territorial use rights for fishers, the integration of the fishers into assessment and management processes, and the protection of key habitats (marine reserves) as a basic tool for the regulation of the fisheries.     

Potential consequences of climate change for primary production and fish production in large marine ecosystems

Existing methods to predict the effects of climate change on the biomass and production of marine communities are predicated on modelling the interactions and dynamics of individual species, a very challenging approach when interactions and distributions are changing and little is known about the ecological mechanisms driving the responses of many species. An informative parallel approach is to develop size-based methods. These capture the properties of food webs that describe energy flux and production at a particular size, independent of species'' ecology. We couple a physical–biogeochemical model with a dynamic, size-based food web model to predict the future effects of climate change on fish biomass and production in 11 large regional shelf seas, with and without fishing effects. Changes in potential fish production are shown to most strongly mirror changes in phytoplankton production. We project declines of 30–60% in potential fish production across some important areas of tropical shelf and upwelling seas, most notably in the eastern Indo-Pacific, the northern Humboldt and the North Canary Current. Conversely, in some areas of the high latitude shelf seas, the production of pelagic predators was projected to increase by 28–89%.     

Copepods act as a switch between alternative trophic cascades in marine pelagic food webs

A recent meta‐analysis indicates that trophic cascades (indirect effects of predators on plants via herbivores) are weak in marine plankton in striking contrast to freshwater plankton ( Shurin et al. 2002 , Ecol. Lett., 5, 785–791). Here we show that in a marine plankton community consisting of jellyfish, calanoid copepods and algae, jellyfish predation consistently reduced copepods but produced two distinct, opposite responses of algal biomass. Calanoid copepods act as a switch between alternative trophic cascades along food chains of different length and with counteracting effects on algal biomass. Copepods reduced large algae but simultaneously promoted small algae by feeding on ciliates. The net effect of jellyfish on total algal biomass was positive when large algae were initially abundant in the phytoplankton, negative when small algae were dominant, but zero when experiments were analysed in combination. In contrast to marine systems, major pathways of energy flow in Daphnia‐dominated freshwater systems are of similar chain length. Thus, differences in the length of alternative, parallel food chains may explain the apparent discrepancy in trophic cascade strength between freshwater and marine planktonic systems.     

Low functional redundancy in coastal marine assemblages

The relationship between species and functional diversity remains poorly understood for nearly all ecosystem types, yet determining this relationship is critically important for developing both a mechanistic understanding of community assembly and appropriate expectations and approaches to protecting and restoring biological communities. Here we use two distinct data sets, one from kelp forests in the Channel Islands, California, and one from a global synthesis of marine reserves, to directly test how variation in species diversity translates into changes in functional diversity. We find strong positive relationships between species and functional diversity, and increased functional diversity of fish assemblages coinciding with recovery of species diversity in marine reserves, independent of the method used for classifying species in functional groups. These results indicate that low levels of redundancy in functional species traits exist across a suite of marine systems, and that fishing tends to remove whole functional groups from coastal marine ecosystems.     

Heterogeneity of ecological patterns,processes, and funding of marine manipulative field experiments conducted in Southeastern Pacific coastal ecosystems

Ecological manipulative experiments conducted in marine coastal ecosystems have substantially improved ecological theory during the last decades and have provided useful knowledge for the management and conservation of coastal ecosystems. Although different studies report global trends in ecological patterns worldwide, Southeastern Pacific coastal ecosystems have been poorly considered. Given that the SE Pacific coast encompasses diverse coastal ecosystems, consideration of studies conducted along this range can shed light on the heterogeneity of processes regulating coastal communities. We reviewed the biotic interactions and habitat type considered, as well as the complexity in terms of spatial and temporal extent of manipulative field experimental studies conducted along the SE Pacific coast from 0°S to 56°S (Ecuador to Chile). We test the effect of funding reported by different studies as a main factor limiting experimental complexity. From field ecological studies published from 1970 to 2016, we found that 81 studies were truly manipulative, in which one or multiple factors were “manipulated.” Around 77% of these studies were located between 21°S and 40°S, and conducted in intertidal rocky habitats. An increase in experimental studies was observed between 2010 and 2015, especially focused on herbivore–alga interactions, although we found that both the temporal extent and spatial extent of these studies have shown a decrease in recent decades. Funding grant amount reported had a positive effect on elapsed time of field experiments, but no effect was observed on spatial extent or in the biotic interactions considered. Elapsed time of experiments was different among the main biotic interactions considered, that is, herbivory, predation, and competition. We suggest that to further progress in applied ecological knowledge, it will be necessary to consider pollution and urbanization processes explicitly using a field experimental framework. This information could improve our understanding of how ecosystems present along the SE Pacific coast respond to climate change and increased levels of human interventions.     

Oscillating trophic control induces community reorganization in a marine ecosystem

Understanding how climate regulates trophic control may help to elucidate the causes of transitions between alternate ecosystem states following climate regime shifts. We used a 34-year time series of the abundance of Pacific cod ( Gadus macrocephalus ) and five prey species to show that the nature of trophic control in a North Pacific ecosystem depends on climate state. Rapid warming in the 1970s caused an oscillation between bottom–up and top–down control. This shift to top–down control apparently contributed to the transition from an initial, prey-rich ecosystem state to the final, prey-poor state. However, top–down control could not be detected in the final state without reference to the initial state and transition period. Complete understanding of trophic control in ecosystems capable of transitions between alternate states may therefore require observations spanning more than one state.     

Beyond trophic morphology: stable isotopes reveal ubiquitous versatility in marine turtle trophic ecology

The idea that interspecific variation in trophic morphology among closely related species effectively permits resource partitioning has driven research on ecological radiation since Darwin first described variation in beak morphology among Geospiza. Marine turtles comprise an ecological radiation in which interspecific differences in trophic morphology have similarly been implicated as a pathway to ecopartition the marine realm, in both extant and extinct species. Because marine turtles are charismatic flagship species of conservation concern, their trophic ecology has been studied intensively using stable isotope analyses to gain insights into habitat use and diet, principally to inform conservation management. This legion of studies provides an unparalleled opportunity to examine ecological partitioning across numerous hierarchical levels that heretofore has not been applied to any other ecological radiation. Our contribution aims to provide a quantitative analysis of interspecific variation and a comprehensive review of intraspecific variation in trophic ecology across different hierarchical levels marshalling insights about realised trophic ecology derived from stable isotopes. We reviewed 113 stable isotope studies, mostly involving single species, and conducted a meta‐analysis of data from adults to elucidate differences in trophic ecology among species. Our study reveals a more intricate hierarchy of ecopartitioning by marine turtles than previously recognised based on trophic morphology and dietary analyses. We found strong statistical support for interspecific partitioning, as well as a continuum of intraspecific trophic sub‐specialisation in most species across several hierarchical levels. This ubiquity of trophic specialisation across many hierarchical levels exposes a far more complex view of trophic ecology and resource‐axis exploitation than suggested by species diversity alone. Not only do species segregate along many widely understood axes such as body size, macrohabitat, and trophic morphology but the general pattern revealed by isotopic studies is one of microhabitat segregation and variation in foraging behaviour within species, within populations, and among individuals. These findings are highly relevant to conservation management because they imply ecological non‐exchangeability, which introduces a new dimension beyond that of genetic stocks which drives current conservation planning. Perhaps the most remarkable finding from our data synthesis is that four of six marine turtle species forage across several trophic levels. This pattern is unlike that seen in other large marine predators, which forage at a single trophic level according to stable isotopes. This finding affirms suggestions that marine turtles are robust sentinels of ocean health and likely stabilise marine food webs. This insight has broader significance for studies of marine food webs and trophic ecology of large marine predators. Beyond insights concerning marine turtle ecology and conservation, our findings also have broader implications for the study of ecological radiations. Particularly, the unrecognised complexity of ecopartitioning beyond that predicted by trophic morphology suggests that this dominant approach in adaptive radiation research likely underestimates the degree of resource overlap and that interspecific disparities in trophic morphology may often over‐predict the degree of realised ecopartitioning. Hence, our findings suggest that stable isotopes can profitably be applied to study other ecological radiations and may reveal trophic variation beyond that reflected by trophic morphology.     

Geographical variation in the 'bottom-up' control of diversity: fleas and their small mammalian hosts

Aim We searched for signs of the ‘bottom‐up’ diversity effect in the association between fleas (Siphonaptera) and their small mammalian hosts (Rodentia, Insectivora and Lagomorpha). We asked (1) whether a strong dependence of flea species richness on host species richness is characteristic for both Palaeoarctic and Nearctic realms; (2) if yes, whether the ratio of host species per flea species along the host diversity gradient is similar between the Palaeoarctic and Nearctic; and (3) whether factors other than host species richness (i.e. geographical position, climate and landscape) might better explain variation in flea species richness than host species richness. Location The study used previously published data on species richness of fleas and their small mammalian hosts from 26 Palaeoarctic and 19 Nearctic regions. Methods We regressed the number of flea species on the number of small mammal species across regions, separately for Palaeoarctic and Nearctic realms, using both non‐transformed data as well as data corrected for the confounding effects of host sampling effort and sampling area. To test whether flea species richness is determined by external factors unrelated to the host, we used stepwise multiple regressions of flea species richness against host species richness and parameters describing the geographical position, climate and relief of a region. Results When non‐transformed data were analysed, flea species richness was positively correlated with host species richness in both the Palaeoarctic and Nearctic, although the slopes of the two regressions differed significantly. After removal of the confounding effects of host sampling effort and sampling area, Palaeoarctic flea species richness remained strongly positively correlated with host species richness, whereas in the Nearctic, flea species richness appeared to be completely independent of host species richness. Results of the multiple regressions using corrected data demonstrated that in the Palaeoarctic, flea species richness was correlated with both the number of host species and the mean altitude of the region, whereas in the Nearctic, flea species richness only tended to be weakly correlated with latitude (however, this correlation turned out to be non‐significant after Bonferroni correction). Main conclusions We found evidence of bottom‐up control of flea diversity in the Palaeoarctic regions only, and not in the Nearctic. We explore several potential explanations for the different patterns observed in the two biogeographical realms, including differences in (1) levels of host specialization, (2) history of host–parasite associations and (3) landscape effects on flea diversification. We conclude that these factors combine to create different macroecological patterns in different biogeographical realms, and that diversity is not governed by the same forces everywhere.     

Gene flow and population history in high dispersal marine invertebrates: mitochondrial DNA analysis of Holothuria nobilis (Echinodermata: Holothuroidea) populations from the Indo-Pacific

The sea cucumber, Holothuria nobilis, has a long-lived planktotrophic larvae, and previous allozyme surveys have suggested that high dispersal is realized. In contrast, recent ecological studies indicate that dispersal is low. To reconcile these data, and to investigate the evolution of this Indo-Pacific species, we screened geographical variation in 559 bp of a mitochondrial gene (COI) in 360 samples from the Australasian region and La Réunion. Sequences from La Réunion differed by > 7% from others and may constitute another species. Haplotype diversity in other samples was high (0.942, SD = 0.007), but haplotypes were closely related (mean nucleotide diversity: 0.0075, SD = 0.0041). AMOVA, pairwise FST values and exact tests did not detect significant population structure. Nested clade analysis showed that one of two main clades was over-represented in west Australia, whereas the other was more common in the northern Great Barrier Reef. Isolation-by-distance was identified as the main determinant of population structure at several clade levels. Contiguous range expansion was inferred for evolutionary older clade levels and this may correspond to a late Pleistocene (88 000-193 000 years ago) population expansion inferred from haplotype mismatch distributions. Thus, the population genetic structures detected are likely to be formed prior to the last ice age, with some indications for high dispersal on shorter time scales.     

Population genetic structure of the biological control agent Macrolophus pygmaeus in Mediterranean agroecosystems

Biological control of agricultural pests relies on knowledge of agroecosystem functionality, particularly when affected by the use of mass‐produced biological agents. Incorporating pre‐ and/or post‐release information such as genetic diversity and structure on these agents using molecular‐based approaches could advance our knowledge of how they perform in agroecosystems. We evaluated the population genetics of Macrolophus pygmaeus, the most widely used predatory mirid against many arthropod pests of greenhouse crops in the Mediterranean region, using the mitochondrial Cytb sequence and microsatellite data, and population genetics and phylogeny approaches. We investigated commercially mass‐produced insects (i.e., commercial insects either mass‐reared in the laboratory for many generations, or purchased by farmers and released in the greenhouses) and “wild” insects (i.e., that occur naturally outside or are collected in nature for release in the greenhouses). The mirids were mainly collected in agroecosystems in which solanaceous plants are grown in northern Spain, southern France and Greece. Both molecular markers and approaches distinguished 2 genetically differentiated populations. The less genetically diverse population, hereafter named the “commercial” strain included all individuals from laboratory mass‐rearings and most releases of commercially bred individuals. The most genetically diverse population mainly comprised individuals originating from noncultivated environments, or from releases of “wild” individuals. Rare examples of hybridization between M. pygmaeus from the 2 populations were observed and asymmetric gene flow was revealed. These findings provide new insights into what happens to M. pygmaeus released in the agroecosystems we studied, and show that it is possible to monitor some commercial strains.