James L. Maino

Reconciling theories for metabolic scaling

Metabolic theory specifies constraints on the metabolic organisation of individual organisms. These constraints have important implications for biological processes ranging from the scale of molecules all the way to the level of populations, communities and ecosystems, with their application to the latter emerging as the field of metabolic ecology. While ecologists continue to use individual metabolism to identify constraints in ecological processes, the topic of metabolic scaling remains controversial. Much of the current interest and controversy in metabolic theory relates to recent ideas about the role of supply networks in constraining energy supply to cells. We show that an alternative explanation for physicochemical constraints on individual metabolism, as formalised by dynamic energy budget (DEB) theory, can contribute to the theoretical underpinning of metabolic ecology, while increasing coherence between intra- and interspecific scaling relationships. In particular, we emphasise how the DEB theory considers constraints on the storage and use of assimilated nutrients and derive an equation for the scaling of metabolic rate for adult heterotrophs without relying on optimisation arguments or implying cellular nutrient supply limitation. Using realistic data on growth and reproduction from the literature, we parameterise the curve for respiration and compare the a priori prediction against a mammalian data set for respiration. Because the DEB theory mechanism for metabolic scaling is based on the universal process of acquiring and using pools of stored metabolites (a basal feature of life), it applies to all organisms irrespective of the nature of metabolic transport to cells. Although the DEB mechanism does not necessarily contradict insight from transport-based models, the mechanism offers an explanation for differences between the intra- and interspecific scaling of biological rates with mass, suggesting novel tests of the respective hypotheses.

A dynamic energy budget for the whole life-cycle of holometabolous insects

Alterations of the amount and quality of food consumed during ontogeny can affect different life-history traits, such as growth rate, developmental time, survival, adult size, and fitness. Understanding the dynamics of such metabolic and energetic pathways and investments is particularly challenging in the case of holometabolous insects due to their strikingly different life stages. We show how whole life-cycle energy and mass budgets can be achieved for holometabolic insects through dynamic energy budget (DEB) theory, permitting the fate of acquired and stored nutrients to be followed over a complete life-cycle. We applied the DEB theory to model the whole life-cycle energetics of an endoparasitic wasp, Venturia canescens (Hymenoptera: Ichneumonidae). Data on embryo, larval, and pupal dry mass, imago longevity, and fecundity were used for assessing the goodness of fit of the model. Our model predicted the growth curves of the larval and pupal stages, the number of eggs laid by the imago through time, and lifespan events, such as the different developmental times of the parasitoid. The model enabled us to distinguish and follow the energy invested in eggs through income and capital reserves. The mechanisms leading to the double costs of being small (a shorter life under starving conditions and fewer eggs) were identified by running the model for varying amounts of food eaten early in life, according to host sizes. The final larval instar harvests around 60 times the energy of a recently hatched larva. Around 90% of this energy is then used during pupation to build the structure of the imago and to pay maintenance. Imagoes, therefore, emerge with only a small percentage of the energy stored by the last instar larvae. Our study shows that, despite being small, this percentage of energy stored during the parasitoid development has a great impact on adult fitness, the loss of which cannot be compensated for by a rich adult environment. Our model is generic and has applications for a wide range of applied and theoretical questions about insect energetics, from population dynamics in multitrophic systems to responses to climate change and life-history strategies.

Ontogenetic and Interspecific Metabolic Scaling in Insects

Design constraints imposed by increasing size cause metabolic rate in animals to increase more slowly than mass. This ubiquitous biological phenomenon is referred to as metabolic scaling. However, mechanistic explanations for interspecific metabolic scaling do not apply to ontogenetic size changes within a species, implying different mechanisms for scaling phenomena. Here, we show that the dynamic energy budget theory approach of compartmentalizing biomass into reserve and structural components provides a unified framework for understanding ontogenetic and interspecific metabolic scaling. We formulate the theory for insects and show that it can account for ontogenetic metabolic scaling during the embryonic and larval phases, as well as the U-shaped respiration curve during pupation. After correcting for the predicted ontogenetic scaling effects, which we show to follow universal curves, the scaling of respiration between species is approximated by a three-quarters power law, supporting past empirical studies on insect metabolic scaling and our theoretical predictions. The ability to explain ontogenetic and interspecific metabolic scaling effects under one consistent framework suggests that the partitioning of biomass into reserve and structure is a necessary foundation to a general metabolic theory.

Mechanistic models for predicting insect responses to climate change

Mechanistic models of the impacts of climate change on insects can be seen as very specific hypotheses about the connections between microclimate, ecophysiology and vital rates. These models must adequately capture stage-specific responses, carry-over effects between successive stages, and the evolutionary potential of the functional traits involved in complex insect life-cycles. Here we highlight key considerations for current approaches to mechanistic modelling of insect responses to climate change. We illustrate these considerations within a general mechanistic framework incorporating the thermodynamic linkages between microclimate and heat, water and nutrient exchange throughout the life-cycle under different climate scenarios. We emphasise how such a holistic perspective will provide increasingly robust insights into how insects adapt and respond to changing climates.

Testing mechanistic models of growth in insects

Insects are typified by their small size, large numbers, impressive reproductive output and rapid growth. However, insect growth is not simply rapid; rather, insects follow a qualitatively distinct trajectory to many other animals. Here we present a mechanistic growth model for insects and show that increasing specific assimilation during the growth phase can explain the near-exponential growth trajectory of insects. The presented model is tested against growth data on 50 insects, and compared against other mechanistic growth models. Unlike the other mechanistic models, our growth model predicts energy reserves per biomass to increase with age, which implies a higher production efficiency and energy density of biomass in later instars. These predictions are tested against data compiled from the literature whereby it is confirmed that insects increase their production efficiency (by 24 percentage points) and energy density (by 4 J mg−1) between hatching and the attainment of full size. The model suggests that insects achieve greater production efficiencies and enhanced growth rates by increasing specific assimilation and increasing energy reserves per biomass, which are less costly to maintain than structural biomass. Our findings illustrate how the explanatory and predictive power of mechanistic growth models comes from their grounding in underlying biological processes.

The effect of egg size on hatch time and metabolic rate: theoretical and empirical insights on developing insect embryos

Summary Body size scaling relationships allow biologists to study ecological phenomena in terms of individual level metabolic processes. Recently, dynamic energy budget (DEB) theory has been shown to offer novel insights on the effect of body size on biological rates. We test whether DEB theory and its unique partitioning of biomass into reserve and structural components can explain the effect of egg size on hatch time and the time course of respiration in insect embryos. We find that without any parameterization (calibration), DEB theory is able to predict hatch time for eggs sizes spanning four orders of magnitude from fundamental biological processes. We find, however, that the standard DEB model poorly predicts the time course of respiration, particularly in early embryonic development where a strong effect of egg size is observed. Further, we show that other theoretical models also poorly predict early embryonic respiration. By modifying the assumption that a fresh egg is entirely reserve, we show that embryonic respiration and hatch time can be better predicted by the DEB model. Useful theories in metabolic ecology, such as DEB theory, can help explain universal scaling patterns in development times. However, simple theoretical models must be expanded if they are to capture the scaling of metabolic rate in insect eggs. A Lay Summary is available for this article.

A cryptic diapause strategy in Halotydeus destructor (Tucker) (Trombidiformes: Penthaleidae) induced by multiple cues: Unraveling summer diapause in redlegged earth mites

BACKGROUND The polyphagous mite pest, Halotydeus destructor, typically has three generations during the cool moist season in Australia and produces over-summering diapause eggs in spring. Diapause eggs have a distinct thick and dark chorion and can survive heat, desiccation and the application of pesticides. Farmers suppress mites producing diapause eggs by a carefully timed spring pesticide application using Timerite® , which predicts the onset of diapause egg production based largely on day length. We investigated the association between diapause induction and other environmental factors that may complicate diapause predictions. RESULTS Diapause in H. destructor induction was influenced by three interacting environmental factors, namely day length, temperature and soil moisture. A cryptic type of diapause egg that lacked a thick chorion and was instead morphologically similar to non-diapause eggs was also discovered. Like diapause eggs, this newly discovered egg type could also survive hot and dry summer conditions. CONCLUSIONS There is an opportunity to refine the Timerite® spring spray by incorporating knowledge of other environmental factors inducing diapause in H. destructor. Compared with typical diapause eggs, the production of cryptic diapause eggs could reflect a strategy to deal with diversifying environmental stresses and/or represent a bet-hedging strategy to adapt to unpredictable environments.

No longer a west-side story – pesticide resistance discovered in the eastern range of a major Australian crop pest, Halotydeus destructor (Acari: Penthaleidae)

Abstract. The redlegged earth mite, Halotydeus destructor (Tucker) (Acari: Penthaleidae), is an important pest of pastures, broad-acre crops, and vegetables across southern Australia. Populations of H. destructor in Western Australia have been known to be resistant to pyrethroid and organophosphorus pesticides since 2006 and 2014, respectively. Resistant populations are currently widespread across Western Australia’s southern growing region but have, until now, remained undetected in the large south-eastern Australian range of H. destructor, despite ongoing resistance screening since 2006. Following reports of a field control failure in the Upper South East district in South Australia in 2016, resistance testing determined this South Australian population was resistant to pyrethroid and organophosphorus pesticides. The levels of resistance discovered were similar to resistant H. destructor populations in Western Australia, which are associated with chemical control failures. This work confirms for the first-time that pesticide resistant populations of H. destructor are no longer isolated to Western Australia.

How China’s “Floating Population” Floats: Recent Patterns in Migrant Workers’ Spatial Mobility and Destination Choice

This chapter estimates the effect of individual and regional attributes on income and job prestige using an original data set containing detailed working histories of approximately 2,300 temporary rural-to-urban migrants. Migrant worker job transitions are examined through time, as well as associated changes in prestige scores. An augmented Mincer model is utilized to explore the extent to which personal characteristics and job history determine earnings. Returns to education and work experience are estimated and compared with data sets on urban resident. The results highlight gender segregation in occupational structure and patterns of change, but show no overall difference in the average perceived job prestige between men and women. While the notion of local-migrant wage disparities is supported by this study, returns to work experience and education of migrants and locals were comparable. It is found that rural work experience contributes very little to migrant worker earnings. Such findings contribute to a richer understanding of an important and diverse labour force too often mischaracterized as static and homogenous.