The response of temperate aquatic ecosystems to global warming: novel insights from a multidisciplinary project

This article serves as an introduction to this special issue of Marine Biology, but also as a review of the key findings of the AQUASHIFT research program which is the source of the articles published in this issue. AQUASHIFT is an interdisciplinary research program targeted to analyze the response of temperate zone aquatic ecosystems (both marine and freshwater) to global warming. The main conclusions of AQUASHIFT relate to (a) shifts in geographic distribution, (b) shifts in seasonality, (c) temporal mismatch in food chains, (d) biomass responses to warming, (e) responses of body size, (f) harmful bloom intensity, (f), changes of biodiversity, and (g) the dependence of shifts to temperature changes during critical seasonal windows.     

The anti-predator behaviour of wild white-handed gibbons (<Emphasis Type="Italic">Hylobates lar</Emphasis>)

Predation on gibbons is rarely observed in the wild. However, the gibbons' moderate body size and relatively small social groups suggest high vulnerability to predation. To assess the role of predation and to study their anti-predator behaviour, we presented visual predator models to nine groups of wild white-handed gibbons at Khao Yai National Park, Thailand. We measured subjects' immediate and delayed responses to four potential predators: tiger, clouded leopard, crested serpent eagle and reticulated python. Subjects reliably approached all four predators. In response to tigers and leopards, they additionally produced predator-specific songs and defecated copiously. In terms of delayed responses, distance between mated adults decreased, but only after exposure to the tiger model. In response to eagles and pythons, gibbons consistently vocalised, but this did not always include predator singing, and we found no long-term effects in overall activity or strata use. However, during 6 of 26 predator encounters, the gibbons produced songs with a structure that was intermediate between a duet song and a predator song more than 20 min after the predator encounter, indicating a long-term effect on their vocal behaviour. This study demonstrates that gibbons discriminate between different potential predators and respond to them with adaptive anti-predator behaviour, which include predator-specific vocal responses. We conclude that gibbons are not immune to predation and that terrestrial predators elicit consistent immediate and delayed anti-predation responses.     

A simple Lagrangian model to simulate temporal variability of algae in the Elbe River

We present a five-year (1997–2001) numerical simulation of daily mean chlorophyll a concentrations at station Geesthacht Weir on the lower Elbe River (Germany) using an extremely simple Lagrangian model driven by (a) water discharge, global radiation, water temperature, and (b) silica observations at station Schmilka in the upper reach of the Elbe River. Notwithstanding the lack of many mechanistic details, the model is able to reproduce observed chlorophyll a variability surprisingly well, including a number of sharp valleys and ascents/descents in the observed time series. The model's success is based on the assumption of three key effects: prevailing light conditions, sporadic limitation of algal growth due to lack of silica and algae loss rates that increase above an empirically specified temperature threshold of 20 °C. Trimmed-down model versions are studied to analyse the model's success in terms of these mechanisms.In each of the five years the model consistently fails, however, to properly simulate characteristic steep increases of chlorophyll a concentrations after pronounced spring minima. Curing this model deficiency by global model re-calibration was found to be impossible. However, suspension of silica consumption by algae for up to 10 days in spring is shown to serve as a successful placeholder for processes that are disregarded in the model but apparently play an important role in the distinctly marked period of model failure. For the remainder of the year the very simple model was found to be adequate.     

Terpenoids tame aggressors: role of chemicals in stingless bee communal nesting

Social insects aggressively defend their nest and surrounding against non-nestmates, which they recognize by an unfamiliar profile of aliphatic hydrocarbons on the cuticle. Prominent exceptions are communal nest aggregations of stingless bees. Stingless bees (Apidae: Meliponini) are also unique in possessing cuticular terpenes which are derived from tree resins and have not yet been reported for any other insect. We showed experimentally that sesquiterpenes from the body surface of the communal nesting bee Tetragonilla collina reduced aggression in otherwise aggressive bees which did not have sesquiterpenes themselves. In the field, bee species nesting in aggregations with T. collina often lack sesquiterpenes in their own cuticular profiles. These species show little aggression towards T. collina, whereas it can be heavily attacked by non-aggregated species that also possess cuticular sesquiterpenes. We conclude that appeasement by sesquiterpenes represents a novel mechanism to achieve interspecific tolerance in social insects.     

Construction of chimaeric gardens through fungal intercropping: a symbiont choice experiment in the leafcutter ant Atta texana (Attini, Formicidae)

Interspecies or intraspecies cooperation can be stabilized evolutionarily if choosing partners favor beneficial partners and discriminate against non-beneficial partners. We quantified such partner choice (symbiont choice) in the leafcutter ant Atta texana (Attini, Formicidae) by presenting the ants in a cafeteria-style preference assay with genotypically distinct fungal cultivars from A. texana and Acromyrmex versicolor. Symbiont choice was measured as the ants' tendency to choose one or more cultivar(s) from several pure (axenic) cultivar fragments and convert a given fungal fragment into a garden. Microsatellite DNA fingerprinting enabled us to identify the cultivars chosen by the ants for their gardens. In 91% of the choice tests, A. texana workers combined multiple cultivars into a single intercropped, chimaeric garden, and the cultivars coexisted in such chimaeric gardens for as long as 4 months. Coexistence of distinct fungal genotypes in chimaeric gardens appears to contradict a recent model of cultivar competition postulating that each cultivar secretes incompatibility compounds harming other cultivars, which presumably would preclude the intercropped polyculture observed in our experiments. Although we found no clear evidence of novel, recombinant genotypes in the experimental chimaeric gardens, the intercropping of cultivar genotypes may occasionally lead under natural conditions to exchange of genetic material between coexisting cultivars, thus introducing novel cultivar genotypes into the leafcutter symbiosis. Symbiont choice by ants and any competition between coexisting cultivar strains in chimaeric gardens do not appear to operate fast enough in our laboratory assay to convert chimaeric gardens into the monocultures observed for A. texana under natural conditions.     

Change of magnetic properties due to fluctuations of hydrocarbon contaminated groundwater in unconsolidated sediments

Sediments affected by fluctuations of hydrocarbon contaminated groundwater were studied at a former military site. Due to remediation, groundwater table fluctuation (GWTF) extends over approximately one meter. Three cores were collected, penetrating through the GWTF zone. Magnetic parameters, sediment properties and hydrocarbon content were measured. We discovered that magnetic concentration parameters increased towards the top of the GWTF zone. Magnetite is responsible for this enhancement; rock magnetic parameters indicate that the newly formed magnetite is in a single domain rather than a superparamagnetic state. The presence of hydrocarbons is apparently essential for magnetite to form, as there is clearly less magnetic enhancement in the core, which is outside of the strongly contaminated area. From our results we conclude that the top of the fluctuation zone has the most intensive geomicrobiological activity probably responsible for magnetite formation. This finding could be relevant for developing methods for simply and quickly detecting oil spills.     

Determination of lindane leachability in soil-biosolid systems and its bioavailability in wheat plants

The leachability of lindane from different biosolid amended soils was determined and compared to its bioavailability. Sand, soil, and a mixture of soil-sand (1:1 w/w) were spiked with lindane, blended with different amounts of biosolids, and subjected to a leaching process with water that lasted for 1-28 d. This procedure is in accordance with ISO/TS 21268-1: 2007. After these batch tests, lindane was extracted from the leachates using three different solvent-free microextraction techniques, including solid phase microextraction (SPME), stir-bar sorptive extraction (SBSE), and silicone rod extraction (SRE). The amount of lindane was determined with thermal desorption and gas chromatography coupled to mass spectrometry (GC-MS). The efficiencies of the three microextraction techniques were statistically different, and the efficiency could be related to the amount of polydimethylsiloxane (PDMS) in each extraction device. However, all of the techniques provide data that shows that the leachability of lindane is dependent on the amount of organic matter contained in the matrix.The results of the lindane leachability assay were compared to the bioavailability of lindane, which was determined by measuring the amount of lindane that accumulated in the roots of wheat plants grown in similar soil-biosolid systems.It was confirmed that the amount of organic matter in the matrix is a determining factor for lindane immobilization. The presence of biosolids decreases the mobility of lindane in all of the systems under study. Similarly, increasing biosolid concentrations in the soil significantly decreased the bioavailability of lindane and, consequently, plant absorption.The good correlation (R² = 0.997) between the leachability of lindane from the matrix and plant absorption of lindane indicates that the proposed biomimetic methodology can predict the bioavailability of lindane in a time period as short as 7 d.The results of this work confirm that amending contaminated soils with biosolids is beneficial for immobilizing lindane and helps prevent the percolation of lindane through the soil profile and into groundwater.     

Estrogenic activity in extracts and exudates of cyanobacteria and green algae

Here is presented some of the first information on interactions of compounds produced by cyanobacteria and green algae with estrogen receptor signaling. Estrogenic potency of aqueous extracts and exudates (culture spent media with extracellular products) of seven species of cyanobacteria (10 different laboratory strains) and two algal species were assessed by use of in vitro trans-activation assays. Compounds produced by cyanobacteria and algae, and in particular those excreted from the cells, were estrogenic. Most exudates were estrogenic with potencies expressed at 50% of the maximum response under control of the estrogen receptor ranging from 0.2 to 7.2 ng 17β-estradiol (E₂) equivalents (EEQ)/L. The greatest estrogenic potency was observed for exudates of Microcystis aerigunosa, a common species that forms water blooms. Aqueous extracts of both green algae, but only one species of cyanobacteria (Aphanizomenon gracile) elicited significant estrogenicity with EEQ ranging from 15 to 280 ng 17β-estradiol (E₂)/g dry weight. Scenedesmus quadricauda exudates and extracts of Aphanizomenon flos-aquae were antagonistic to the ER when coexposed to E₂. The EEQ potency was not correlated with concentrations of cyanotoxins, such as microcystin and cylindrospermopsin, which suggests that the EEQ was comprised of other compounds. The study demonstrates some differences between the estrogenic potency of aqueous extracts prepared from the same species, but of different origin, while the effects of exudates were comparable within species. The observed estrogenic potencies are important namely in relation to the possible mass expansion of cyanobacteria and release of the active compounds into surrounding water.     

The predictive power of the elimination of dioxin-like pollutants from pigs: an in vivo study

Pigs accidentally given feed contaminated by dioxin-like pollutants are a serious public health issue. We have examined whether pigs with limited exposure during early periods of fattening would be categorized as non-compliant with the EU limit at slaughtering when growth-dilution, excretion and metabolism effects are considered. Sixteen female and sixteen castrated male weaned pigs were divided into four groups (e.g. DG0, DG1, DG2 and DG3) in week 2 after birth. From weeks 3 to 13, groups DG1, DG2, and DG3 pigs were fed with a polychlorinated dibenzo-p-dioxin/dibenzofuran (PCDD/F) and polychlorinated biphenyl (PCB) mixture at dosages of 1, 10 and 100 ng-toxic equivalent (TEQ) per kg dry mass feed in capsules, respectively. From weeks 13 to 23, the animals were nourished with clear feed. Control group DG0 was always fed with clear feed. Subcutaneous fat samples were collected at weeks 13, 18 and 23 by biopsies. The pollutant residues were analyzed by high resolution gas chromatography-high resolution mass spectrometry and quantified by a ¹³C-isotope dilution method. The results showed the following: (1) when slaughtered at week 23, the TEQ for DG1 pigs (0.66 ± 0.21 pg/g fat) was under the EU limit of 1 pg PCDD/F-TEQ/g fat; (2) PCDD/F congener-specific first-order elimination rates were linearly correlated with their toxicity equivalency factors (TEFs), and the rates were significantly dose-dependent for the more toxic congeners (TEF ≥ 0.1). Therefore, the pigs' exposure above the EU limit during the early fattening stage did not necessarily lead to their categorization as non-compliant pork; and the residual TEQ for pork can be predicted from early exposure concentrations based on the models established here.     

Concentrations of microcystins in tissues of several fish species from freshwater reservoirs and ponds

The aim of this study is to summarise the determination of concentrations of microcystins (MCs) in muscle and liver of freshwater fish species caught in stagnant waters of the Czech Republic. Within the years 2007–2009, 351 muscle samples and 291 liver samples of 16 freshwater fish species derived from four fishponds, and four water reservoirs were analysed. MCs were detected in 53 liver samples. The highest concentrations of microcystins were determined in liver samples of carnivorous fish species; 50.3 ng/g of fresh weight (FW) in perch (Perca fluviatilis) and 22.7 ng/g FW in pikeperch (Sander lucioperca). MCs in liver were detected in other five fish species; asp (Aspius aspius), pike (Esox lucius), common carp (Cyprinus carpio), grass carp (Ctenopharyngodon idella) and European eel (Anguilla anguilla). Concentrations of MCs in liver of nine fish species (European bream, whitefish, tench, silver carp, European catfish, roach, chub, crucian carp and rudd) were below the detection limit of 1.2–5.4 ng/g FW for different MC congeners. However, the concentrations of MCs in all muscle samples were below the detection limit. The assessment of MCs concentrations might be influenced by the detection method used. Due to the concentrations of MCs being below the detection limit in muscle samples of all fish species analysed, it seems that there might be a low potential threat for human health in case of fish muscle consumption.