Modelling and interpreting fish bioenergetics: a role for behaviour, life-history traits and survival trade-offs.

Bioenergetics is used as the mechanistic foundation of many models of fishes. As the context of a model gradually extends beyond pure bioenergetics to include behaviour, life-history traits and function and performance of the entire organism, so does the need for complementing bioenergetic measurements with trade-offs, particularly those dealing with survival. Such a broadening of focus revitalized and expanded the domain of behavioural ecology in the 1980s. This review makes the case that a similar change of perspective is required for physiology to contribute to the types of predictions society currently demands, e.g. regarding climate change and other anthropogenic stressors.

Eco-evolutionary dynamics induced by massive mortality events.

An eco-genetic model tuned on a population of marble trout Salmo marmoratus subject to periodic flood events was used to explore how the evolution of growth rates interacting with density-dependent processes can modify size at age and population structure and in turn influence the resilience of populations. Fish with greater growth potential were assumed to have higher mortality rates. The results of simulations were compared between two scenarios, one in which populations may evolve growth rates and the other one in which the distribution of growth rates within a population is kept fixed. Evolving populations had a greater proportion of age 1 year individuals in the population, greater median length at age 3 years (the typical age at sexual maturity for S. marmoratus) and lower population sizes. The slightly smaller population sizes did not affect realized extinction risk. Resilience, defined as the number of years necessary to rebound from flood-induced population collapse, was on average from 2 to 3 years in both scenarios, with no significant difference between them. Moderate heritability of growth, relaxation of density-dependent processes at low densities and rapid recovery to a safe population size combine to limit the capacity to evolve faster recovery after flood-induced population collapses via changing growth rates.

Using scale characteristics and water temperature to reconstruct growth rates of juvenile steelhead Oncorhynchus mykiss.

Juvenile steelhead Oncorhynchus mykiss from a northern California Central Valley population were reared in a controlled laboratory experiment. Significantly different rates of growth were observed among fish reared under two ration treatments and three temperature treatments (8, 14 and 20°C). Wider circulus spacing and faster deposition was associated with faster growth. For the same growth rate, however, circulus spacing was two-fold wider and deposited 36% less frequently in the cold compared to the hot temperature treatment. In a multiple linear regression, median circulus spacing and water temperature accounted for 68% of the variation in observed O. mykiss growth. These results corroborate previous research on scale characteristics and growth, while providing novel evidence that highlights the importance of water temperature in these relationships. Thus, this study establishes the utility of using scale analysis as a relatively non-invasive method for inferring growth in salmonids.

Top-down and bottom-up control of life-history strategies in coho salmon (Oncorhynchus kisutch).

Sexual maturation profoundly affects population dynamics, but the degrees to which genetic, top-down, and bottom-up controls affect age at maturity are unclear. Salmonid fishes have plastic age at maturity, and we consider genetic and environmental effects on this trait by developing fitness functions for coho salmon (Oncorhynchus kisutch). The functions are based on size-specific survival and reproductive success, where reproductive success is the product of fecundity and ability to defend nests (females) or the product of sperm volume and ability to mate (males). We model genetic and bottom-up controls (e.g., food availability) with an environmentally explicit growth function and top-down control (predation mortality) with survival functions that consider both size-dependent and size-independent mortality. For females, we predict that early maturation rarely maximizes fitness, but males can maximize fitness by maturing early if they grow well in freshwater. We predict that early maturation is most affected by the bottom-up effects of resource distribution at sea, followed by bottom-up and genotypic effects in freshwater. Top-down processes are predicted to have strong effects on the likelihood of delayed maturation.

The shape of things to come: using models with physiological structure to predict mortality trajectories.

If mortality rate is viewed as the outcome of processes of behavior, growth and reproduction, then it should be possible to predict mortality rate as a result of those processes. We provide two examples of how this may be done. In the first, we use the method of linear chains to treat mortality that is the result of multiple physiological processes, some of which may have delays. In the second, we assume that mortality is the result of damage associated with growth and metabolism. Both approaches lead to a rich diversity of predicted mortality trajectories. Although many of these look Gompertzian at young ages, the behavior at older ages depends upon the details of the physiological models.

Complex adaptive systems, aging and longevity.

Mortality and reproduction are intimately entwined in the study of aging and longevity. I apply the modern theory of complex adaptive systems (nonlinear, stochastic, dynamic methods) to questions of aging and longevity. I begin by highlighting major questions that must be answered in order to obtain a deeper understanding of aging. These are: (i) What should (in an evolutionary sense) mortality trajectories look like? (ii) Why does caloric restriction slow aging? (iii) Why does reproduction cause delayed mortality? (iv) Why does compensatory growth cause delayed mortality? I show how dynamic state variable models based on stochastic dynamic programming (Clark & Mangel, 2000) can be used to embed genetic theories of senescence (either mutation accumulation or antagonistic pleiotropy) in the somatic environment, as George Williams called for in 1957, and how they make the disposable soma theory of aging operational. Such models will allow unification of genetic and phenotypic theories of aging.

Age and longevity in fish, with consideration of the ferox trout.

In the first part of this paper, we review the evolutionary aspects of age and longevity in fish and then summarize the theory of maturity due to Ray Beverton. This theory allows one to predict age at maturity (and thus a putative point for the onset of senescence) from information on growth rate and mortality rate. We illustrate the application of this theory with data on tilapia species and then discuss the limitations of the theory. In the second part of the paper, we develop an individual based model for the ferox trout. This is a morph of brown trout Salmo salar that is an exception to the common notion that caloric restriction extends lifespan, in the sense that ferox trout achieve long life by eating more, not less. The model allows one to identify the role that ecological and biochemical adaptations play in the longevity of the ferox trout.

Egg maturation, egg resorption and the costliness of transient egg limitation in insects.

Although there is widespread agreement that the cost of oviposition underlies selective oviposition in insects, there is no consensus regarding which factors mediate the cost of oviposition. Models have suggested that egg costs are often paramount in those insects that do not continue to mature eggs during the adult stage (pro-ovigenic insects). Here we address the hypothesis that egg costs are generally less significant in synovigenic insects, which can replenish oocyte supplies through continuous egg maturation. A dynamic optimization model based on the biology of a highly synovigenic parasitoid, Aphytis aonidiae, suggests that the maximum rate of egg maturation is insufficient to balance the depletion of eggs when opportunities to oviposit are abundant. Transient egg limitation therefore occurs, which imposes opportunity costs on reproducing females. Thus, whereas the most fundamental constraint acting on the lifetime reproductive success of pro-ovigenic species is the fixed total number of eggs that they carry at eclosion, the most fundamental constraint acting on a synovigenic species is the maximum rate of oocyte maturation. Furthermore, the ability of synovigenic species to reverse the flow of nutrients from the soma to oocytes (i.e. egg resorption) has a dramatic influence on the cost of oviposition. Whereas females in hostrich environments may experience oviposition-mediated egg limitation, females in host-poor environments may experience oosorption-mediated egg limitation. Both forms of egg limitation are costly. Contrary to initial expectations, the flexibility of resource allocation that typifies synovigenic reproduction actually appears to broaden the range of conditions under which costly egg limitation occurs. Egg costs appear to be fundamental in mediating the trade-off between current and future reproduction, and therefore are an important factor favouring selective insect oviposition.

Messages from mortality: the evolution of death rates in the old.

Ageing is an increase in mortality and/or decline in fertility with advancing age. Evolutionary theories predict that ageing will evolve in response to the pattern of externally imposed hazards to survival and fertility; a prediction confirmed in new empirical studies. Recent studies of large cohorts of experimental animals and of humans have revealed that mortality rates do not continue to accelerate at very advanced ages. It has been suggested that evolutionary theories cannot account for these mortality patterns; however, this challenge is more apparent than real. Heterogeneity between individuals can shape mortality trajectories for populations, and recent evolutionary theory can both account for such heterogeneity and accommodate late-age mortality patterns.

Effects of time limitation and egg limitation on lifetime reproductive success of a parasitoid in the field.

We used field observations of freely foraging Aphytis aonidiae parasitoids in conjunction with results of laboratory studies of A. aonidiae and other Aphytis species to simulate lifetime patterns of behavior and reproduction. Field observations provided estimates of encounter rates with three classes of hosts, the mortality rate from predation on adult parasitoids, and host-handling times for oviposition and host feeding by adult wasps. A series of physiological parameters, including the egg maturation rate and the value of host-feeding meals, were estimated from previously published studies. Plasticity in parasitoid behavior was incorporated in two ways. For one set of simulations we used a behavioral rule derived empirically from observations of parasitoids made in the field, and for another we used a dynamic state-variable model to generate a set of behavioral rules that maximize lifetime reproductive success. As was expected, the empirically derived rule led to better matches with field observations than did simulations using the output of the dynamic model. Projections of lifetime reproductive success in the field ranged between three and 37 eggs within the 95% confidence intervals of the mortality rate and host encounter rate and depending on which behavioral rule was used. Lifetime reproductive success from the simulation with central estimates of the mortality and host encounter rates that incorporated the empirical rule was 6.25 eggs. Using the empirical versus the theoretical rule in the simulations led to a 10%-30% decline in projections of lifetime reproductive success, depending on mortality and host encounter rates. Regardless of the behavioral rule, the simulations underscored the observation that the host encounter rate was greater than the egg maturation rate. The overall oviposition rate was sufficiently high to lead to daily episodes of temporary egg limitation during which parasitoids must mature an egg before being able to oviposit.

A new look at relationships between size at maturity and asymptotic size.

Comparative studies have revealed positive correlations between size at maturity and asymptotic size in several taxa with asymptotic growth after maturity. Using a simple growth model, we show that positive correlations between size at maturity and asymptotic size are predicted for different individuals in the same species if growth costs of reproduction are inversely related to size at maturity. Several processes might lead to higher growth costs of reproduction for smaller individuals; these include effects of body size on competition for resources required for breeding, on the space available within the body cavity for food processing in gravid individuals, and on the costs of transporting eggs or young in relation to the total energy budget. We confirm several key elements of the growth model using data from female Iguana iguana lizards, including the novel assumption that instantaneous growth rates of adults of the same length will be positively related to their length at maturity. These analyses suggest a simple and possibly general explanation for positive correlations between size at maturity and asymptotic size within-and perhaps also among-species that continue to grow after maturity.

Predation on adult Aphytis parasitoids in the field.

We report on predation on adult females of the parasitoids Aphytis aonidiae and A. vandenboschi (Hymenoptera: Aphelinidae) foraging in the field. During 89.6 h of observation, we witnessed 18 encounters with predators, 6 of which resulted in parasitoid capture. Three classes of generalist predators attacked Aphytis: spiders (unidentified Salticidae and Thomisidae), workers of the Argentine ant, Linepithema humile, and nymphs of the assassin bug Zelus renardii (Hemiptera: Reduviidae). Although observations were conducted during most months of the year, encounters with predators occurred only during September, October and November. During these months, encounters with predators occurred on average every 3.2 h of observation, with one in three encounters resulting in parasitoid capture. Peaks in predation coincided with population peaks of A. aonidiae, but were unrelated to population dynamics of any of the predators. We compare these results with previously published laboratory studies on longevity of Aphytis parasitoids, and conclude that predation pressure has the potential to severely limit parasitoid fitness in the field.

When can a clonal organism escape senescence?

Some clonal organisms may live for thousands of years and show no signs of senescence, while others consistently die after finite life spans. Using two models, we examined how stage-specific life-history rates of a clone's modules determine whether a genetic individual escapes senescence by replacing old modules with new ones. When the rates of clonal or sexual reproduction and survival of individual modules decline with age, clones are more likely to experience senescence. In addition, the models predict that there is a greater tendency to find senescence in terms of a decline in the rate of sexual reproduction with clone age than in terms of an increase in the probability of clone mortality, unless rates of sexual reproduction increase dramatically with module stage. Using a matrix model modified to represent the clonal lifestyle, we show how a trade-off between sexual and clonal reproduction could result in selection for or against clonal senescence. We also show that, in contrast to unitary organisms, the strength of selection on life-history traits can increase with the age of a clone even in a growing population, countering the evolution of senescence.

A simple direct method for finding persistence times of populations and application to conservation problems.

The computation of persistence times of populations has become a central focus in conservation biology. We describe a simple, direct method for finding the statistics of persistence times by assuming that there is a maximum population size. Thus, even though the population dynamics may be very complex for population sizes below the maximum, it is possible to write a finite set of equations from which the mean and second moment of the persistence time can be found by using simple, algebraic methods. We apply the method to compute the mean and coefficient of variation of persistence times of populations that suffer large decrements (catastrophes). Our results show that in the presence of catastrophes, the increase in mean persistence time with large populations is not nearly as rapid as other theories suggest and that catastrophes occurring at even modest rates can considerably increase the risk of extinction.

Parent-offspring conflict and life-history consequences in herbivorous insects.

We develop an evolutionarily stable strategy theory of parent-offspring conflict in insect herbivores for the case in which offspring can choose to leave host plants on which they have been deposited by their mother. We find that a fundamental parent-offspring conflict in larval leaving rates occurs because individual larvae are more related to themselves than to their siblings whereas mothers are equally related to each of their offspring. Several patterns emerge: (1) The optimal probability of movement from the mother's perspective, P*(mom), is always greater than or equal to the optimal probability of movement from the offspring's perspective, P*(off), (2) a consequence of this difference in optimal probabilities of movement is that the mother's fitness for a given clutch is always greater for P*(mom) than P*(off), (3) as the payoff for leaving a plant decreases, (i) the optimal movement rates decrease and (ii) clutches become smaller, (4) as relatedness increases, optimal movement probabilities increase and this causes an increase in optimal clutches, and (5) the clutch size that maximizes the mother's lifetime fitness will frequently diverge from that which the mother would produce were the offspring to move at her optimal rate (i.e., P*(mom)).

Dynamic information in uncertain and changing worlds.

A general theory for information processing by organisms living in uncertain and changing worlds is developed. The three fundamental properties of the theory are: (i) the use of a memory parameter that allows the organism to forget the more distant past, (ii) a succinct representation of encounters and information and (iii) flexibility in the estimates of parameters by including the uncertainty in these estimates in a consistent manner. The theory is developed using Bayesian methods (but can also be applied to maximum likelihood estimation) and is applied to the encounter models standardly used in ecology (Poisson, binomial, and negative binomial). Two applications are discussed: (i) patch selection and the matching rule and (ii) superparasitism by a parasitoid.

A dynamic habitat selection game.

A patch selection game is formulated and analyzed. Organisms can forage in one of H patches. Each patch is characterized by the cost of foraging, the density and value of food, the predation risk, and the density of conspecifics. The presence of conspecifics affects the finding and sharing of food, and the predation risk. Optimal foraging theory can be viewed as a "1-person" game against nature in which the optimal patch choice of a specific organism is analyzed assuming that the number of conspecifics in other patches is fixed. In the general game theoretic approach, the behavior of conspecifics is included in the determination of the distinguished organism's strategy. An iterative algorithm is used to compute the solution of the "n-person" game or dynamic ESS, which differs from the optimal foraging theory solution. Experiments to test the proposed theory using rodents and seed trays are briefly discussed.