Franco Teixeira-de Mello

Impacts of climate warming on lake fish community structure and potential effects on ecosystem function

Fish play a key role in the trophic dynamics of lakes, not least in shallow systems. With climate warming, complex changes in fish community structure may be expected owing to the direct and indirect effects of temperature, and indirect effects of eutrophication, water-level changes and salinisation on fish metabolism, biotic interactions and geographical distribution. We review published and new data supporting the hypotheses that, with a warming climate, there will be changes in: fish community structure (e.g. higher or lower richness depending on local conditions); life history traits (e.g. smaller body size, shorter life span, earlier and less synchronised reproduction); feeding mode (i.e. increased omnivory and herbivory); behaviour (i.e. stronger association with littoral areas and a greater proportion of benthivores); and winter survival. All these changes imply higher predation on zooplankton and macroinvertebrates with increasing temperatures, suggesting that the changes in the fish communities partly resemble, and may intensify, the effects triggered by eutrophication. Modulating factors identified in cold and temperate systems, such as the presence of submerged plants and winter ice cover, seem to be weaker or non-existent in warm(ing) lakes. Consequently, in the future lower nutrient thresholds may be needed to obtain clear-water conditions and good ecological status in the future in currently cold or temperate lakes. Although examples are still scarce and more research is needed, we foresee biomanipulation to be a less successful restoration tool in warm(ing) lakes without a strong reduction of the nutrient load.

Environmental Warming in Shallow Lakes: A Review of Potential Changes in Community Structure as Evidenced from Space-for-Time Substitution Approaches

Abstract Shallow lakes, one of the most widespread water bodies in the world landscape, are very sensitive to climate change. Several theories predict changes in community traits, relevant for ecosystem functioning, with higher temperature. The space-for-time substitution approach (SFTS) provides one of the most plausible empirical evaluations for these theories, helping to elucidate the long-term consequences of changes in climate. Here, we reviewed the changes at the community level for the main freshwater taxa and assemblages (i.e. fishes, macroinvertebrates, zooplankton, macrophytes, phytoplankton, periphyton and bacterioplankton), under different climates. We analyzed data obtained from latitudinal and altitudinal gradients and cross-comparison (i.e. SFTS) studies, supplemented by an analysis of published geographically dispersed data for those communities or traits not covered in the SFTS literature. We found only partial empirical evidence supporting the theoretical predictions. The prediction of higher richness at warmer locations was supported for fishes, phytoplankton and periphyton, while the opposite was true for macroinvertebrates and zooplankton. With decreasing latitude, the biomass of cladoceran zooplankton and periphyton and the density of zooplankton and macroinvertebrates declined (opposite for fishes for both biomass and density variables). Fishes and cladoceran zooplankton showed the expected reduction in body size with higher temperature. Life history changes in fish and zooplankton and stronger trophic interactions at intermediate positions in the food web (fish predation on zooplankton and macroinvertebrates) were evident, but also a weaker grazing pressure of zooplankton on phytoplankton occurred with increasing temperatures. The potential impacts of lake productivity, fish predation and other factors, such as salinity, were often stronger than those of temperature itself. Additionally, shallow lakes may shift between alternative states, complicating theoretical predictions of warming effects. SFTS and meta-analyses approaches have their shortcomings, but in combination with experimental and model studies that help reveal mechanisms, the “field situation” is indispensable to understand the potential effects of warming.

Phytoplankton community structure in five subtropical shallow lakes with different trophic status (Uruguay): a morphology-based approach

Phytoplankton abundance and biomass can be explained as a result of spatial and temporal changes in physical and biological variables, and also by the externally imposed or self-generated spatial segregation. In the present study, we analyzed contrasting-season changes in the phytoplankton communities of five subtropical shallow lakes, covering a nutrient gradient from oligo-mesotrophy to hypereutrophy, using a morphologically based functional approach to cluster the species. Six environmental variables accounted for 46% of the total phytoplankton morphological groups variance, i.e., turbidity (Secchi disk), conductivity, total phosphorus, total nitrogen, total zooplankton abundance, and herbivorous meso:microzooplankton density ratio. The differences in resource availability and zooplankton abundance among the systems were related with important changes in phytoplankton composition and structure. Within phytoplankton assemblages, adaptations to improve both light and phosphorus/nitrogen uptake were important in nutrient-poor systems; while grazing-avoidance mechanisms, such as colonial forms or bigger individuals, seemed relatively important only in eutrophic Lake Blanca, where light was not a limiting factor. However, this was not observed in the nutrient-rich Lake Cisne, where low light availability (due to clay resuspension and dark water color) was identified as the main structuring factor. Our results suggest that the composition of phytoplankton morphologically based functional groups appear to reliably describe the trophic sate of the lakes. However, other factors, such as nonbiological turbid condition, or zooplankton composition, may interact rendering interpretations difficult, and therefore, deserve further studies and evaluation.

Seasonal and diel changes in fish activity and potential cascading effects in subtropical shallow lakes with different water transparency

Fish play a key role in the functioning of shallow lakes. Simultaneously, fish are affected by physical in-lake factors, such as temperature and water transparency, with potential changes in their cascading effects on other communities. Here, we analysed the fish community structure and fish activity in four subtropical shallow lakes, varying in trophic state and water transparency, to assess changes promoted by temperature (i.e. summer and winter) and the light regime (i.e. day and night). We used a passive method (gillnets) during the day- and at night-time to detect changes in fish activity, but also sampled the littoral zone (during night) by point sample electrofishing to obtain a better description of the fish assemblage and habitat use. We observed different fish assemblages in the two seasons in all lakes. We captured more fish species and also obtained higher numbers (CPUE with nets) in summer. Contrary to our expectations, the visually oriented Characiformes were the most captured fish regardless of water transparency, at both day-time and night-time. We also found higher fish CPUE at night-time in all lakes. However, the differences between night and day decreased with decreasing transparency, being lower in the least clear lake, Lake Cisne. The nocturnal increase in fish CPUE (including visually oriented species) suggests that darkness serves as a good refuge for fish in shallow subtropical lakes, even at the likely cost of a lower feeding efficiency during the night. The importance of darkness seems to decrease with decreasing water transparency. We also argue that cascading effects of changes in the activity of piscivorous fish (seasonal changes in piscivores CPUE), when omni-planktivorous fish are indeed affected, may eventually reach the zooplankton, but may not be strong enough to reach the phytoplankton, regardless of water transparency.

Submerged macrophytes facilitate dominance of omnivorous fish in a subtropical shallow lake: implications for lake restoration

Biomanipulation based on removal of coarse fish, piscivorous fish stocking and sometimes also planting of submerged macrophytes has been used to restore temperate eutrophic shallow lakes. However, in warmer lakes, omnivorous fish are more abundant and apparently less well controlled by the piscivores. We investigated the food web structure and energy pathways of fish in the restored part of subtropical Lake Wuli, China, using gut contents analysis (GCA) and the IsoSource model based on stable isotope analysis (SIA) data. We found that omnivores dominated the fish community in terms of numbers. GCA showed that cyclopoid copepods constituted the main food item for the planktivores, while all adult omnivorous fish fed mainly on macrophytes. The IsoSource SIA model supported these results. Furthermore, piscivores consumed shrimps rather than juvenile omnivores, and the SIA analysis revealed no trophic links between piscivores and adult omnivores or zooplanktivores. We conclude that macrophytes constituted an important food item for omnivores, potentially promoting population growth of omnivores as control by piscivores was weak. This may yield a high predation pressure on both zooplankton and on macrophytes, possibly preventing the establishment of a stable macrophyte state following restoration of eutrophic lakes unless the fish density is regularly controlled.

Feeding habits and morphometry of Iheringichthys labrosus (Lütken, 1874) in the Uruguay River (Uruguay)

Body size and diet of organisms are fundamental attributes which determine their ecology and natural history. Iheringichthys labrosus is one of the most common fish species of the Uruguay River. However, its natural history is poorly known and there is little information about its diet and interactions with other species. This paper describes the feeding habits of this species, relating feeding patterns to the size classes and morphometry of individuals and to the temporal variations. Fishes were captured in May and November of 2006 in three zones of the lower Uruguay River. A total of 101 stomach contents was analyzed (standard length: 60-224 mm). The species exhibited a broad feeding spectrum with most items belonging to the benthic community. We found significant diet differences between size classes and studied months. However, we have not found a close relationship between changes in morphometric variables and diet shifts between size classes.

Stable isotope analysis confirms substantial differences between subtropical and temperate shallow lake food webs

Differences in trophic web structure in otherwise similar ecosystems as a consequence of direct or indirect effects of ambient temperature differences can lead to changes in ecosystem functioning. Based on nitrogen and carbon stable isotope analysis, we compared the food-web structure in a series of subtropical (Uruguay, 30–35°S) and temperate (Denmark, 55–57°N) shallow lakes. The food-web length was on average one trophic position shorter in the subtropical shallow lakes compared with their temperate counterparts. This may reflect the fact that the large majority of subtropical fish species are omnivores (i.e., feed on more than one trophic level) and have a strong degree of feeding niche overlap. The shapes of the food webs of the subtropical lakes (truncated and trapezoidal) suggest that they are fuelled by a combination of different energy pathways. In contrast, temperate lake food webs tended to be more triangular, likely as a result of more simple pathways with a top predator integrating different carbon sources. The effects of such differences on ecosystem functioning and stability, and the connection with ambient temperature as a major underlying factor, are, however, still incipiently known.

Potential drivers of seasonal shifts in fish omnivory in a subtropical stream

Abstract The trophic structure of fish assemblages often varies seasonally, following the changes in food availability and supposedly water temperature. To unveil potential drivers of trophic shifts, we studied changes in fish trophic structure at both whole-assemblage and species levels at contrasting food availability and water temperatures in a subtropical stream. We analysed the diet of the most abundant omnivorous species (Bryconamericus iheringii) monthly along the year, searching for relationships with environmental variables changing seasonally (i.e. temperature and water level) and with fish reproductive stage. We ran a single-species food choice field experiment with fixed animal and vegetal food availability in contrasting seasons to test food availability as driver of diet shifts. At the assemblage level, we found a higher consumption of vegetal during summer, reflecting the increased proportion of vegetal in the diet of omnivores, which dominated the assemblage. At the species level, the enhanced vegetal consumption was related to increases in temperature and reduction in water level. Moreover, fish selected for vegetal during summer and for animal food in winter under experimental conditions. Our findings support the role of temperature driving food web dynamics by increasing fish herbivory towards warmer scenarios, with potential strong implications for whole-assemblage trophic structure.

Sound production and pectoral spine locking in a Neotropical catfish (Iheringichthys labrosus, Pimelodidae)

Catfishes may have two sonic organs: pectoral spines for stridulation and swimbladder drumming muscles. The aim of this study was to characterize the sound production of the catfish Iheringichthys labrosus. The I. labrosus male and female emits two different types of sounds: stridulatory sounds (655.8 + 230 Hz) consisting of a train of pulses, and drumming sounds (220 + 46 Hz), which are composed of single-pulse harmonic signals. Stridulatory sounds are emitted during abduction of the pectoral spine. At the base of the spine there is a dorsal process that bears a series of ridges on its latero-ventral surface, and by pressing the ridges against the groove (with an unspecialized rough surface) during a fin sweep, the animal produce a series of short pulses. Drumming sound is produced by an extrinsic sonic muscle, originated on a flat tendon of the transverse process of the fourth vertebra and inserted on the rostral and ventral surface of the swimbladder. The sounds emitted by both mechanisms are emitted in distress situation. Distress was induced by manipulating fish in a laboratory tank while sounds were recorded. Our results indicate that the catfish initially emits a stridulatory sound, which is followed by a drumming sound. Simultaneous production of stridulatory and drumming sounds was also observed. The catfish drumming sounds were lower in dominant frequency than stridulatory sounds, and also exhibited a small degree of dominant frequency modulation. Another behaviour observed in this catfish was the pectoral spine locking. This reaction was always observed before the distress sound production. Like other authors outline, our results suggest that in the catfish I. labrosus stridulatory and drumming sounds may function primarily as a distress call. Bagres podem apresentar dois orgaos sonoros: o espinho peitoral para o som peitoral ou estridulatorio e o musculo sonoro da bexiga natatoria. O objetivo deste trabalho foi caracterizar a producao de som no bagre Iheringichthys labrosus. Essa especie emite dois sons diferentes, o som peitoral ou estridulatorio (655,8 + 230 Hz) que consiste numa serie de pulsos, e o som de tamboril (220 + 46 Hz) que e composto por sinais harmonicos de pulso simples. O som peitoral e emitido com o movimento do espinho da nadadeira peitoral. A base do espinho possui um processo dorsal que suporta uma serie de cristas na sua superficie lateroventral, e ao pressionar as cristas contra o sulco (com uma superficie rugosa nao especializada) durante o movimento de abertura da nadadeira, se produz uma serie de pulsos curtos. O som de tamboril e produzido por um musculo sonico extrinseco, originado em um tendao plano preso ao processo transversal da quarta vertebra e inserido nas superficies rostral e ventral da bexiga natatoria. Os sons sao emitidos por ambos os mecanismos em situacao de estresse, a qual foi induzida atraves da manipulacao dos peixes em um tanque no laboratorio, enquanto os sons eram gravados. Nossos resultados indicam que o bagre emite primeiro o som peitoral e em seguida o som de tamboril. Tambem foi observada a producao simultânea dos sons estridulatorio e de tamboril. O som de tamboril mostra uma frequencia dominante mais baixa do que o som peitoral, e tambem apresenta um grau menor de modulacao de frequencia dominante. Isso pode estar relacionado com um som de cortejo, como verificado em outros peixes teleosteos. Outro comportamento observado nessa especie de bagre e a capacidade de travar o espinho peitoral. Essa reacao foi observada imediatamente antes da producao do som. Como descrevem outros autores, nossos resultados sugerem que em I. labrosus o som de estridulacao e de tamboril funcionam como uma chamada de alarme.

What can resting egg banks tell about cladoceran diversity in a shallow subtropical lake

Dormant stages (“resting eggs”) produced by cladocerans can persist for long periods of time in sediments and restore populations once the environmental conditions become favorable again. Lake Blanca, a subtropical shallow eutrophic lake, hosts a cladoceran community dominated by small-sized species. Previous studies on zooplankton resting eggs suggested that the cladoceran genera Daphnia and Simocephalus were present, but they had never been found before in water samples. In the present study, we compared a biweekly active community sampling with the resting egg bank (passive cladoceran community) from littoral and pelagic zones. Moreover, we tested the amount of samples required to have a representative reconstruction of the diversity in both compartments (water and sediment). Lake Blanca showed a relatively high cladoceran species richness (24) in the water column, with rapid temporal replacement. Several species were present in water samples during short temporal windows; therefore, to detect these species a strong sampling effort in terms of temporal frequency and spatial distribution was required. Contrary to our expectations, resting egg community showed a lower diversity than the active community; however, we demonstrated that the analysis of resting egg bank composition can help detect general community structure patterns.