Welcome: We study the ecology of marine benthic invertebrates
Book chapters in:
Role of trait combinations, habitat matrix, and network topology in metapopulation recovery from regional extinction
Luis Giménez, Peter Robins, Stuart R. Jenkins
We studied the role of oceanographic conditions and life history strategies on recovery after extinction in a metapopulation of marine organisms dispersing as pelagic larvae. We combined an age‐structured model with scenarios defined by realistic oceanographic conditions and species distribution along the Irish Sea coast (North Europe). Species life history strategies were modeled combining the dispersal behaviors with two levels of fecundity. Recovery times were quantified after simulating extinction in four regions. Two alternative strategies (high fecundity or larval tidal transport) led to short recovery times, irrespective of the effects of other drivers. Other strategies and low larval survival exacerbated the effects of oceanographic conditions on recovery times: longer times were associated with for example the presence of frontal zones isolating regions of extinction. Recovery times were well explained by the connectivity of each focal population with those located outside the area of extinction (which was higher in the so‐called small world topologies), but not by subsidies (direct connections with populations located nearby). Our work highlights the complexities involved in population recovery: specific trait combinations may blur the effects of the habitat matrix on recovery times; K‐strategists (i.e., with low fecundities) may achieve quick recovery if they possess the appropriate dispersal traits. High larval mortality can exacerbate the effect of oceanographic conditions and lead to heterogeneity in recovery times. Overall, processes driving whole network topologies rather than conditions surrounding local populations are the key to understand patterns of recovery.
Franziska Spitzner,Luis Giménez, Rebecca Meth, Steffen Harzsch,Gabriela Torres
Understanding organismal responses to environmental drivers is relevant to predict species capacities to respond to climate change. However, the scarce information available on intraspecific variation in the responses oversimplifies our view of the actual species capacities. We studied intraspecific variation in survival and larval development of a marine coastal invertebrate (shore crab Carcinus maenas) in response to two key environmental drivers (temperature and salinity) characterising coastal habitats. On average, survival of early larval stages (up to zoea IV) exhibited an antagonistic response by which negative effects of low salinity were mitigated at increased temperatures. Such response would be adaptive for species inhabiting coastal regions of freshwater influence under summer conditions and moderate warming. Average responses of developmental time were also antagonistic and may be categorised as a form of thermal mitigation of osmotic stress. The capacity for thermal mitigation of low-salinity stress varied among larvae produced by different females. For survival in particular, deviations did not only consist of variations in the magnitude of the mitigation effect; instead, the range of responses varied from strong effects to no effects of salinity across the thermal range tested. Quantifying intraspecific variation of such capacity is a critical step in understanding responses to climate change: it points towards either an important potential for selection or a critical role of environmental change, operating in the parental environment and leading to stress responses in larvae.
Incorporating the geometry of dispersal and migration to understand spatial patterns of species distribution
Dispersal and migration can be important drivers of species distributions. Because the paths followed by individuals of many species are curvilinear, spatial statistical models based on rectilinear coordinates systems would fail to predict population connectivity or the ecological consequences of migration or species invasions. I propose that we view migration/dispersal as if organisms were moving along curvilinear geometrical objects called smooth manifolds. In that view, the curvilinear pathways become the “shortest realised paths” arising from the necessity to minimise mortality risks and energy costs. One can then define curvilinear coordinate systems on such manifolds. I describe a procedure to incorporate manifolds and define appropriate coordinate systems, with focus on trajectories (1D manifolds), as parts of mechanistic ecological models. I show how a statistical method, known as “manifold learning”, enables one to define the manifold and the appropriate coordinate systems needed to calculate population connectivity or study the effects of migrations (e.g. in aquatic invertebrates, fish, insects and birds). This approach may help in the design of networks of protected areas, in studying the consequences of invasion, range expansions, or transfer of parasites/diseases. Overall, a geometrical view to animal movement gives a novel perspective to the understanding of the ecological role of dispersal and migration.
Sensitivity to near-future CO2 conditions in marine crabs depends on their compensatory capacities for salinity change
Whiteley NM, Suckling CC, Ciotti BJ, Brown J, McCarthy ID, Gimenez L, Hauton C
Marine crabs inhabit shallow coastal/estuarine habitats particularly sensitive to climate change, and yet we know very little about the diversity of their responses to environmental change. We report the effects of a rarely studied, but increasingly prevalent, combination of environmental factors, that of near-future pCO2 (~1000 µatm) and a physiologically relevant 20% reduction in salinity. We focused on two crab species with differing abilities to cope with natural salinity change, and revealed via physiological and molecular studies that salinity had an overriding effect on ion exchange in the osmoregulating shore crab, Carcinus maenas. This species was unaffected by elevated CO2, and was able to hyper-osmoregulate and maintain haemolymph pH homeostasis for at least one year. By contrast, the commercially important edible crab, Cancer pagurus, an osmoconformer, had limited ion-transporting capacities, which were unresponsive to dilute seawater. Elevated CO2 disrupted haemolymph pH homeostasis, but there was some respite in dilute seawater due to a salinity-induced metabolic alkalosis (increase in HCO3− at constant pCO2). Ultimately, Cancer pagurus was poorly equipped to compensate for change, and exposures were limited to 9 months. Failure to understand the full spectrum of species-related vulnerabilities could lead to erroneous predictions of the impacts of a changing marine climate.
Hatching rhythm and larval release in Leptodius exaratus (H.) (Decapoda: Brachyura: Xanthidae) from rocky shores in Kuwait
Zainab Al-Wazzan, Lewis Le Vay, Manaf Behbehani, Luis Giménez
Journal of Crustacean Biology
The hatching rhythm and larval release patterns of the rocky shore crab Leptodius exaratus (H. Milne Edwards, 1834) in relation to the tidal cycle, the time of the day, and lunar cycle were investigated in the laboratory. A total of 263 ovigerous females were collected at six sites in Kuwait between April and July 2014. The pattern of larval release was monitored in relation to local tidal and diel cycles. Larval release was synchronized with local neap tide events with a significant correlation between hatching frequency and the predicted tidal height. This pattern changed towards the second half of the spawning season, and females released larvae during spring and neap tides. It was found that this species has a nocturnal hatching rhythm with larvae being released at early night during neap tides and at late night during spring tides (later in the season) as a correspondent to the expected ebb tide. The results of the laboratory experiments suggest that the hatching rhythm of L. exaratus is endogenous. These results contribute to further understand how intertidal species adjust the time of their reproduction to maximise larval survival.
Influence of temperature and light regime on the larval
development of the common spider crab Maja brachydactyla
Balss, 1922 (Brachyura: Majidae)
Diego Castejón, Guiomar Rotllant, Luis Giménez, Gabriela Torres, Guillermo Guerao
Aquaculture Research 49:3548-3558
Temperature and light are important factors affecting production in the aquaculture industry, as they can drive behaviour and physiological responses of free‐swimming larval stages. However, the influence of light on crustacean farming has received little consideration. The common spider crab Maja brachydactyla Balss, 1922 has a great potential for aquaculture because of the easy maintenance, high fecundity, and short larval development. In order to optimize larval culture techniques, we quantified the influence of temperature and light on larval survival, development, and elemental (carbon and nitrogen) body composition. Constant darkness resulted in longer developmental time as compared with daily light photoperiod (6–16 light hours). Larvae reared under constant darkness showed also reduced dry mass, carbon and nitrogen content, and C:N ratio. We also found carry‐over effects of light conditions: constant darkness experienced during the zoeal stage led to increased developmental time in the megalopa stage. Temperature and light showed additive effects. We optimized the larval culture of M. brachydactyla requiring around 14 days from hatch to first juvenile by keeping cultures under 21 ± 1°C and light sources simulating the daily light cycle.
Enrique González-Ortegón, Lewis Le Vay, Mark Edward Mackay Walton & Luis Giménez,
Offspring size variation in relation to maternal size and season is characteristic of a range of species living in seasonal environments. Little is known about the proximate mechanisms explaining the links between maternally driven variation in offspring phenotypes, for instance when mothers have different diets depending on their size or the season. Here, we use stable isotopes techniques to quantify size dependent and seasonal variations in diet in mothers of shrimp Palaemon serratus and explore possible links between maternal diet and phenotype of embryos and freshly hatched larvae. We found that larger females, which occur more frequently in winter, produce larvae with higher carbon and nitrogen content as well as higher percent carbon, than smaller mothers collected in winter. In addition, isotopic composition suggest that larger mothers collected in winter, were feeding at a higher trophic level, or on an enriched prey pool compared with smaller mothers collected in summer. Overall, there seems to be a strong association between offspring size and maternal diet, mediated by maternal size and/or season.
Response of estuarine free-living nematode assemblages to organic enrichment: an experimental approach
Noelia Kandratavicius, Catalina Pastor de Ward, Natalia Venturini, Luis Giménez, Marcel Rodriguez, Pablo Muniz
Organic enrichment, especially from anthropogenic sources, is one of the current threats to coastal marine biodiversity. Organic enrichment occurs mainly in sheltered soft bottoms, characterized by fine sediments, and results in multiple changes in the benthic habitat, including hypoxia and an increased concentration of compounds that are toxic to marine invertebrates. We report on the results of a microcosm-based experiment (duration= 30 d), quantifying the effects of organic enrichment on taxonomic and functional diversity of nematode assemblages from an open/closed coastal lagoon of South America (Rocha Lagoon, Uruguay). In open/closed lagoons, the input of organic matter becomes a major disturbance due the limitation in water renewal. In our experiment, enrichment led to reductions in abundance, richness and trophic diversity of the nematode assemblage. Rapid reductions in total abundance (after 4 d) were registered, while richness decreased only towards the end of the experiment (~ 30 d). Trophic changes were characterized by loss of predators/omnivores and dominance of selective deposit-feeders and epigrowth-feeders. By contrast, we did not find any selective effect of enrichment associated with life history traits (eg maturity index). Overall, these findings have 2 important implications for the conservation and monitoring of the health of coastal lagoons: first, monitoring of nematode assemblages at the genus level is sufficient to detect enrichment effects; second, an index of trophic diversity would be a good indicator of the effects of enrichment on natural communities.
Scale-dependent natural variation in larval nutritional reserves in a marine invertebrate: implications for recruitment and cross-ecosystem coupling
Luis Giménez, Gabriela Torres, Amanda Kate Pettersen, Michael Timothy Burrows,
Alicia Estevez & Stuart Rees Jenkins
Marine Ecology Progress Series 570: 141-155
In species with complex life cycles, laboratory studies show that variations in traits of settling larvae can affect post-settlement survival and can influence recruitment and benthic-pelagic coupling. However, we still know little about the magnitude and spatial scale of natural trait variation. We studied spatial variation in body size and nutritional reserves (carbon, nitrogen and lipids) of settled cyprids of the barnacle Semibalanus balanoides, along the coast of West Scotland. We quantified variation among regions (north vs south: range~ 700 km), locations (~50km), shores (~10 km) and within shores (~10 m). We also evaluated trait responses to gradients in chlorophyll and shore openness, and compared swimming vs. settled cyprids in order to infer the likely influence of costs of substratum search on trait variation. Variability between regions was large, with higher trait values (e.g. Carbon per cyprid: 35-50% higher) in the north. Most traits correlated negatively with pelagic chlorophyll-a (a proxy for larval/juvenile food availability); this counter-gradient pattern suggests an adaptive role of increased reserves, buffering benthic juveniles from low food availability during the critical early post-settlement period. Body size and nitrogen content correlated positively with shore openness; lower than expected carbon content suggest increased costs of substratum search on open shorelines. Higher nitrogen content but lower percent carbon was found in settled vs swimming larvae, suggesting costs of substratum search at the time of settlement. Overall, we uncovered the spatial scales at which trait variation, shaped by pelagic processes, can affect post-metamorphic survival, recruitment and benthic-pelagic coupling.
Impacts of a reduction in seawater pH mimicking ocean acidification on the structure and diversity of mycoplankton communities.
Maris Reich Antje Wichels, Katrin Panzert, Evamaria Krause,Luis Giménez, Gunnar Gerdts
Aquatic Microbial Ecology 79:221-233
Increases in atmospheric carbon dioxide (CO2) change ocean chemistry, as dissolved CO2 leads to a reduction in the seawater pH. Many marine taxa have been shown to be affected by ocean acidification; however, information on marine fungi is lacking. We analyzed the effect of pH on mycoplankton communities. The pH of microcosms was adjusted to a value mimicking the predicted ocean acidification in the near future. Fungal communities were analyzed using a double-marker gene approach, allowing a more detailed analysis of their response using 454 pyrosequencing. Mycoplankton communities in microcosms with in situ and adjusted water pH values differed significantly in terms of structure and diversity. The differences were mainly abundance shifts among the dominant taxa, rather than the exclusion of fungal groups. A sensitivity to lower pH values was reported for several groups across the fungal kingdom and was not phylogenetically conserved. Some of the fungal species that dominated the communities of microcosms with a lower pH were known pathogenic fungi. With the increasing awareness of the significant role fungi play in marine systems, including performing a diverse range of symbiotic activities, our results highlight the importance of including fungi in further research projects studying and modeling biotic responses to the predicted ocean acidification.
Persistent and context-dependent effects of the larval feeding environment on post-metamorphic performance through the adult stage
Gabriela Torres, Luis Giménez, Amanda Kate Pettersen, Mathilde Bue,
Michael Timothy Burrows, Stuart Rees Jenkins
Marine Ecology Progress Series 545, 915–923
One of the central issues in ecology is the identification of processes affecting the population structure and dynamics of species with complex life cycles. In such species, variationin both the number of larvae that enter a population and their phenotype are important drivers of survival and growth after metamorphosis. Larval experience can have strong effects on key postmetamorphic traits, but the temporal scale of such ‘trait-mediated effects’ may be short, and their magnitude may depend on the environment experienced after metamorphosis. We used an intertidal barnacle to study the long-term consequences of trait-mediated effects under different postmetamorphic conditions by manipulating larval food concentration and monitoring patterns of survival and growth in juveniles at 2 intertidal levels over a 5 mo period. In 2 replicated experiments, higher food levels resulted in increased body size, mass and reserves (measured from elemental composition) in the settling larval stage and increased body size of newly metamorphosed juveniles. In Expt 1, high food concentration reduced juvenile mortality at low intertidal levels, while on the upper intertidal, mortality was high for all larval food concentrations. By contrast, in Expt 2, low larval food concentration decreased juvenile survival at both shore levels. When present, effects were established early (Weeks 1 or 2) and persisted for over 10 wk in Expt 1 and 22 wk in Expt 2. Interactive effects of the larval and juvenile environments can have importantimplications for population size: trait-mediated effects may persist for long periods, helping toexplain patterns of adult abundance.
Lars Gutow, Antonia Eckerlebe, Luis Giménez and Reinhard Saborowski
The ingestion of microplastics has been shown fora great variety of marine organisms. However, benthic marinemesoherbivores such as the common periwinkle Littorina littoreahave been largely disregarded in studies about the effects ofmicroplastics on the marine biota, probably because the pathwayfor microplastics to this functional group of organisms was notobvious. In laboratory experiments we showed that the seaweedFucus vesiculosus retains suspended microplastics on its surface.The numbers of microplastics that adhered to the algae correlatedwith the concentrations of suspended particles in the water. Inchoice feeding assays L. littorea did not distinguish between algaewith adherent microplastics and clean algae without microplastics,indicating that the snails do not recognize solid nonfoodparticles in the submillimeter size range as deleterious. In periwinkles that were feeding on contaminated algae, microplasticswere found in the stomach and in the gut. However, no microplastics were found in the midgut gland, which is the principledigestive organ of gastropods. Microplastics in the fecal pellets of the periwinkles indicate that the particles do not accumulaterapidly inside the animals but are mostly released with the feces. Our results provide the first evidence that seaweeds mayrepresent an efficient pathway for microplastics from the water to marine benthic herbivores.
The Effects of temperature and salinity on the survival, growth and duration of the larval development of the common spider crab Maja brachydactyla (Balss, 1922) (Brachyura: Majidae)
Castejon, D. Rotllant, G. Gimenez, L. Torres, G. and Guerao, G.
The effect of temperature and salinity on the larval development of the common spider crab Maja brachydactyla (Balss, 1922) were studied in the laboratory. Larvae were reared at different salinities (0-45) at constant temperature, and under six different combinations of temperature (18 and 21 degrees C) and salinity (30, 35, and 40). The survival and developmental time from newly hatched zoeae to the megalopa stage and from megalopa to the first juvenile stage was quantified; the 24 h median lethal salinity (LS50) for first zoeal stage was calculated. Dry mass (DM), elemental body composition (Carbon, Hydrogen, Nitrogen) and carbon: nitrogen ratio (C:N) were determined in both starved and nourished zoeae. The lower and upper LS50 for M. brachydactyla first zoea in 24 h were 19.9 and 56.0, respectively; similar to other marine stenohaline brachyuran larvae. The megalopa stage was reached in a salinity range from 30 to 40. The highest survival rates to the first juvenile stage were observed at salinity: 35 and temperature: 21 degrees C. Salinity was the key parameter for the survival to first juvenile, whereas the temperature had a higher effect over the duration of the larval development. The greatest loss of DM in starving and nourished zoeae was observed at low salinity (25). No differences were found in DM or C:N during the megalopa stage. The culture and ecological implications of the salinity tolerance of M. brachydactyla larvae are discussed.
Individual and mixture effects of selected pharmaceuticals on larval development of the estuarine shrimp Palaemon longirostris
E González-Ortegón, J Blasco, E Nieto, M Hampel, L Le Vay, L Giménez
Few ecotoxicological studies incorporate within the experimental design environmental variability and mixture effects when assessing the impact of pollutants on organisms. We have studied the combined effects of selected pharmaceutical compounds and environmental variability in terms of salinity and temperature on survival, development and body mass of larvae of the estuarine shrimp Palaemon longirostris. Drug residues found in coastal waters occur as mixture, and the evaluation of combined effects of simultaneously occurring compounds is indispensable for their environmental risk assessment. All larval stages of P. longirostris were exposed to the nonsteroidal antiinflammatory drug (NSAID) diclofenac sodium (DS: 40 and 750 μg L−1), the lipid regulator clofibric acid (CA: 17 and 361 μg L−1) and the fungicide clotrimazole (CLZ: 0.14 and 4 μg L−1). We observed no effect on larval survival of P. longirostris with the tested pharmaceuticals. However, and in contrast to previous studies on larvae of the related marine species Palaemon serratus, CA affected development through an increase in intermoult duration and reduced growth without affecting larval body mass. These developmental effects in P. longirostris larvae were similar to those observed in the mixture of DS and CA confirming the toxic effects of CA. In the case of CLZ, its effects were similar to those observed previously in P. serratus: high doses affected development altering intermoult duration, tended to reduce the number of larval instars and decreased significantly the growth rate. This study suggests that an inter-specific life histories approach should be taken into account to assess the effect of emergent compounds in coastal waters.