Alfredo G. Nicieza

Variation in digestive performance between geographically disjunct populations of Atlantic salmon: countergradient in passage time and digestion rate

European Atlantic salmon (Salmo salar) populations inhabit rivers from northern Portugal to northern Norway across a wide spectrum of environmental variability. To address whether single physical factors might lead to genetic divergence of isolated populations, we compared the digestive performances total digestibility, relative nitrogen digestibility, passage time, and digestion rate (g dry matter · h−1) — of northern (Scotland) and southern (Asturias, northern Spain) populations at three temperature regimes (5, 12, and 20° C). Total dry matter digestibilities increased directly with temperature but were similar for both populations at each of the three trials. Relative nitrogen digestibility did not differ between populations nor among temperature regimes. In contrast, passage time was significantly longer for low-than for high-latitude fish at both 5 and 20° C. When the percentage of food digested and the passage time were integrated as digestion rates (food digested per unit time), a significant population × temperature interaction consistent with a genotype × environment interaction was detected in addition to the population and temperature effects. This implies that not only is the digestive performance of the high-latitude population higher throughout the range of temperatures examined, but moreover the difference is reinforced at high temperatures, where the digestion rate of high-latitude fish was 1.6 times greater. Taken together, these two results provide preliminary evidence for countergradient variation in digestive rates of salmonids in response to variation in growth opportunity. The data support our previous work on the same two populations showing differences in growth rates, and underlie one of the possible mechnisms leading to more rapid growth of the high-latitude fish when both populations are reared in a common environment.

Effects of induced variation in anuran larval development on postmetamorphic energy reserves and locomotion

Anuran larvae exhibit high levels of phenotypic plasticity in growth and developmental rates in response to variation in temperature and food availability. We tested the hypothesis that alteration of developmental pathways during the aquatic larval stage should affect the postmetamorphic performance of the Iberian painted frog (Discoglossus galganoi). We exposed tadpoles to different temperatures and food types (animal- vs. plant-based diets) to induce variation in the length of the larval period and body size at metamorphosis. In this species, larval period varied with temperature but was unaffected by diet composition. In contrast, size at metamorphosis was shaped by the interaction between food quality and temperature; tadpoles fed on an animal-based diet became bulkier metamorphs than those fed on plant-based food at high (22°C) but not at low (12°C) temperature. Body condition of newly metamorphosed frogs was unrelated to the temperature or food type experienced during the premetamorphic stage. Frogs maintained at high temperature during the larval period showed reduced jumping ability, especially when fed on the plant-based diet. However, when considering size-independent jumping ability, cold-reared individuals exhibited the lowest performance, and herbivores reared at 17°C the highest. Cold-reared (12°C) frogs accumulated larger amounts of energy reserves than individuals raised at 17°C or 22°C. This was still the case after correction for differences in body mass, thus indicating some size-independent effect of developmental temperature. Despite the higher lipid content of the carnivorous diet, the differences in energy reserves between herbivores and carnivores were relatively weak and associated with differences in body size. These results suggest that the consequences of environmental variation in the larval habitat can extend to the terrestrial phase and influence juvenile growth and survival.

Fish community variation along physical gradients in short streams of northern Spain and the disruptive effect of dams

Relationships between the fish community and selected habitat features were examined in a set of short temperate streams located at the northern end of the Iberian Peninsula. The fish fauna in these streams consists mostly of diadromous or estuarine species. Species richness and diversity increased with stream order, depth and width and decreased with elevation and distance from the sea. Stream order (positively) and elevation (negatively) were the two variables most highly correlated with species richness and diversity; higher order streams (order 3–4) showed greater values of species diversity than lower order ones (order 1) even when the elevation effect was removed. Addition of species in the downstream direction, but no replacement or loss was evidenced. We also compared the observed values of species diversity with those predicted from habitat features for a set of locations above unpassable dams. A great majority of the sites showed lower than predicted diversity values, which is an expected outcome for this mainly migratory fish fauna.

Compensatory response ‘defends’ energy levels but not growth trajectories in brown trout, Salmo trutta L.

Compensatory growth is an organisms reaction to buffer deviations from targeted trajectories. We explored the compensatory patterns of juvenile brown trout under field and laboratory conditions. Divergence of size and condition trajectories was induced by manipulating food levels in the laboratory and then releasing the trout into a river. In the stream, the length trajectories of food-restricted and control fish were parallel, but food-restricted fish exhibited partial compensation for mass and rapid recovery of condition. A laboratory experiment on similar sized fish did not provide evidence for compensatory growth in length or mass. In contrast, data matched the compensatory patterns shown in the stream: length trajectories were parallel and the convergence of mass trajectories ceased as soon as food-restricted fish recovered condition to the level of controls. These results show that (i) brown trout did not compensate for depression in structural growth and (ii) mass recovery was targeted to reinstate condition or energy reserves, but not size at a given age. This does not support the common view that compensatory growth can be a general response to growth depression. Rather, compensation in other salmonids could be related to size thresholds associated with developmental switches at the onset of sexual maturation and migration.

Morphological variation between geographically disjunct populations of Atlantic salmon: the effects of ontogeny and habitat shift

Summary 1. Previous studies suggest that morphological divergence among populations is a widespread result of reproductive isolation and local adaptation. In this paper I test the hypothesis that morphological differentiation should be reduced when individuals shift from a geographically heterogeneous habitat (benthic, fresh water) to a relatively uniform habitat (pelagic, open ocean). 2. Juvenile Atlantic Salmon Salmo salar from two disjunct populations but reared under the same environmental conditions differed in a number of morphometric traits and general body shape in both the freshwater and the premigratory stage associated with the oceanic phase. 3. Relative to the premigratory phase, the riverine forms of these populations differed in a larger number of variables, the discriminant functions correctly assigned a larger proportion of individuals to their source population and morphological distances between population centroids were also greater. 4. Morphometric distances between the centroids of stages within populations were greater than distances between populations within stages. 5. Though preliminary, these results suggest that, for some traits, isolated populations may diverge in a determined stage but converge in another, especially in species that undergo a habitat shift.

Statistical analysis of structural compensatory growth: how can we reduce the rate of false detection?

Compensatory growth (CG) is a key issue in work aiming at a full understanding of the adaptive significance of growth plasticity and its carryover effects on life-history. The number of studies addressing evolutionary explanations for CG has increased rapidly during the last few years, but there has not been a parallel gain in our understanding of the methodological difficulties associated with the analysis of CG. We point out two features of growth that can have serious consequences for detecting CG: (1) size dependence of growth rates, which causes nonlinearity of growth trajectories, and; (2) temporal overlapping of structural growth and replenishment of energy reserves after a period of famine. We show that the currently used methods can be prone to spurious detection of CG (Type I error) under conditions of nonlinear growth, and therefore lead to the accumulation of a significant amount of false “empirical support.” True and simulated growth data provided consistent results suggesting that a substantial fraction of the existing evidence for CG may be spurious. A small curvature in the growth trajectory can lead to spurious “detection” of CG when control and manipulated trajectories are compared over the same time interval (the “simultaneous” approach). We present a novel, robust method (the “asynchronous” approach) based on the accurate selection of control trajectories and comparison of control and treatment growth rates at different times. This method enables a reliable test to be performed for compensation under asymptotic growth. While the general results of our simulations do not support the application of conventional methods to the general case of nonlinear growth trajectories under the simultaneous approach, simple methods may prove valid if the experimental design allows for asynchronous comparisons. We advocate an alternative approach to deal with “safe” detection of CG that overcomes the problems associated with the occurrence of nonlinear and asymptotic growth, and provide recommendations for improving CG study designs.

Trade-offs across life stages: does predator–induced hatching plasticity reduce anuran post-metamorphic performance?

In species with complex life cycles hatching plasticity can provide an effective escape from egg predators, but theoretical studies predict a predation-risk trade-off across egg and larval stages. In this study, we examine whether the presence of an egg predator can alter the timing of hatching in an anuran, Rana temporaria, and the consequences of hatching plasticity after transition to the terrestrial habitat. Predator cues induced earlier hatching, and hatchlings were smaller, less developed and had relatively shorter and deeper tails than control hatchlings. The predator–induced differences in developmental time were compensated throughout the larval period; there was no predator effect on metamorph age or size. Surprisingly, the effects of egg predators were perceptible after metamorphosis. Juveniles emerging from the predator and the no-predator treatments differed in several size-adjusted morphological dimensions. Seemingly these morphological differences were not large enough to give rise to suboptimal growth or locomotor performance after metamorphosis. Thus, our results suggest only a short-term effect on juvenile phenotype, but not a trade-off between hatching time and juvenile performance.

Factors determining tadpole vulnerability to predators: can prior experience compensate for a suboptimal shape?

We investigated the role of constitutive morphology and previous experience in predator avoidance in two anuran species associated with different larval habitats. In Rana temporaria, deeper tails and larger body size conferred selective advantage against dragonfly predation. Previous experience with predators had a positive influence on the survival of R. temporaria tadpoles equivalent to predator selection. By contrast, survival in Bufo bufo seems unrelated to tail shape or experience. This suggests that B. bufo lacks constitutive morphological defenses against insect predators, and that morphological and behavioral defenses could result more effective than chemical deterrents for these insect predators. A key novelty of this study is the observation that Rana tadpoles having prior experience with predators have an enhanced success in further encounters, and this occurs before the morphological induced defense has been established. This induced modification for R. temporaria, and its lack of for B. bufo, may be an important determinant of larval survival.

Effects of angling on population structure of brown trout, Salmo trutta L., in mountain streams of Northern Spain

Effects of angling exploitation on brown trout populations were assessed by comparing fished sections with close ones unfished for at least 20 years, in mountain streams of Asturias (Northern Spain). Both the fish size and age structure significantly differed among sections in the expected direction according to their exploitation status. The main effects were a significant decrease in age structure complexity (diversity), life span, and percent individuals above the legal limit size in the exploited stocks versus the unexploited ones. Trout above the minimum length limit for fishing (18 cm) averaged 19.47% of the fish caught in the unfished sections (sd = 4.01; n = 5), and 4.72% (sd = 3.46; n = 4) in those subjected to angling. Furthermore, fish older than 4 years represented 39.84% (sd = 8.53) and 1.19% (sd = 1.60) of the catch, respectively. Effects on recruitment (density of young fishes) and growth rates (length at age 1 + to 3 +) were not absolutely consistent, though maximum values were associated with fished sections.

Time constraints and flexibility of growth strategies: geographic variation in catch-up growth responses in amphibian larvae

1. As size is tightly associated with fitness, compensatory strategies for growth loss can be vital for restoring individual fitness. However, immediate and delayed costs of compensatory responses may prevent their generalization, and the optimal strategy may depend on environmental conditions. Compensatory responses may be particularly important in high-latitude habitats with short growing seasons, and thus, high-latitude organisms might be more efficient at compensating after periods of unfavourable growth conditions than low-latitude organisms. 2. We investigated geographical differences in catch-up growth strategies of populations of the common frog (Rana temporaria) from southern and northern Sweden in two factorial common garden experiments involving predation risk and two different causes of growth arrest (nutritional stress and low temperatures) to evaluate how the compensatory strategies can be affected by context-dependent costs of compensation. Larval and metamorphic traits, and post-metamorphic performance were used as response variables. 3. Only northern tadpoles exposed to low food completely caught up in terms of metamorphic size, mainly by extending the larval period. Low food decreased survival and post-metamorphic jumping performance in southern, but not in northern tadpoles, suggesting that northern tadpoles have a better ability to compensate after periods of restricted food. 4. Both northern and southern tadpoles were able to metamorphose at the same size as control tadpoles after being exposed to low temperatures, indicating that consequences of variation in temperature and food availability differed for tadpoles. However, the combination of low temperatures and predation risk reduced survival in both southern and northern tadpoles. Also, predation risk decreased energy storage in both experiments. 5. Our results highlight the influence of climatic variation and the type of stressor as selective factors shaping compensatory strategies.