Per-stage growth rates of head and body sizes in scarab larvae (Coleoptera: Scarabaeidae) decrease across ontogeny following a species-specific pattern

It has been widely assumed that the stepwise increase in the exoskeleton size of larval insects approximately follows a geometric progression from instar to instar, known as Dyar's Rule. However, it is not clear whether the per-instar increase in body size follows this rule. In insects, Dyar's Rule has been identified either by regressing the log-scaled size on the instar number (log-linear regression analysis) or by comparing the postmolt/premolt size ratio between instars (growth rate analysis). A previous study on the body mass of caterpillars showed the methodological pitfall that Dyar's Rule was statistically supported by log-linear regression analysis, but not at all by growth rates analysis. I considered this concern here by examining the per-stage growth rates of head and body sizes for larvae of the beetle Trypoxylus dichotomus using both methods and compared the resulting growth rates for body size within and between taxonomic orders. Dyar's Rule was statistically supported by the log-linear regression analysis but not by growth rate analysis for both the head and body sizes in T. dichotomus. The body size growth rate in T. dichotomus decreased as the instar progressed. This developmental pattern was also found in reported data for the other six scarabs, but not in data for Lepidoptera or Hymenoptera. These findings confirm that the per-stage growth rate of body size does not follow Dyar's Rule in a wide range of insects, and suggest that developmental change in the body size growth rate varies among insect groups.     

Dyar's Rule and the Investment Principle: optimal moulting strategies if feeding rate is size-dependent and growth is discontinuous

We consider animals whose feeding rate depends on the size of structures that grow only by moulting (e.g. spiders'' legs). Our Investment Principle predicts optimum size increases at each moult; under simplifying assumptions these are a function of the scaling of feeding rate with size, the efficiency of moulting and the optimum size increase at the preceding moult. We show how to test this quantitatively, and make the qualitative prediction that size increases and instar durations change monotonically through development. Thus, this version of the model does not predict that proportional size increases necessarily remain constant, which is the pattern described by Dyar''s Rule. A literature survey shows that in nature size increases tend to decline and instar durations to increase, but exceptions to monotonicity occur frequently: we consider how relaxing certain assumptions of the model could explain this. Having specified various functions relating fitness to adult size and time of emergence, we calculate (using dynamic programming) the effect of manipulating food availability, time of hatching and size of the initial (or some intermediate) instar. The associated norms of reaction depend on the fitness function and differ from those when growth follows Dyar''s Rule or is continuous. We go on to consider optimization of the number of instars. The Investment Principle then predicts upper and lower limits to observed size increases and explains why increases usually change little or decline through development. This is thus a new adaptive explanation for Dyar''s Rule and for the most common deviation from the Rule.     

Does the ‘investment principle’ model explain moulting strategies in lepidopteran larvae?

Abstract.  The aim of the present study was to evaluate the applicability of a general optimality model of insect development in the case of lepidopteran larvae. According to the model, larvae moult mainly to increase the size of mouthparts, which is assumed to limit consumption rates. The assumptions of this model being met, one should expect a dependence of growth rates on head capsule size, constancy of absolute growth rates within an instar and higher growth rates in older instars. The validity of these predictions is tested on two species of lymantriid moths. Head capsule size has only a weak effect on growth rates in one of the species, and no effect in the other. Absolute growth rates tend to increase during the development within an instar. Higher growth rates of older instar larvae are explainable by an allometric relationship that extrapolates from growth within the preceding instar. Thus, there is no evidence of an extra increase in growth performance attributable to moulting into the subsequent instar. These results support the idea that growth rates of lepidopteran larvae are limited by nutrient absorption rates rather than by the rates of consumption. There is a considerable cost of moulting in terms of lost growing time: the larvae would double their weights during an instar if they were able to develop without the premoult decrease in growth rates. The investment principle model does not appear to be directly usable to explain moulting strategies in the lepidopteran larvae studied. However, it may well be applicable after some adjustment (i.e. assuming that larvae should moult before consumption rates become limiting).     

Chilled Galleria mellonella larvae: mechanism of supernumerary moulting

ABSTRACT. Supernumerary larval instars were produced when Galleria mellonella L. (Lepidoptera) larvae were chilled at 0°C. Although sensitivity to cooling stress of the last instar and younger larvae were generally the same, only penultimate and the last instar larvae showed a significant correlation between their age and the number of additional larval moults. Chilling stress induced a rapid and persistent increase in the JH titre of the last instar larvae. Severing the ventral nerve cord resulted in a predictable loss of the ability to produce supernumerary moults in chilled last instar larvae. The data suggest that sensory input stimulates allatotropic hormone secretion by the brain of chilled larvae. The possible mechanism controlling supernumerary moulting is discussed.     

Size compensation in moth larvae: attention to larval instars

Environmental perturbations such as starvation and poor diet often prevent animals from attaining their optimal sizes. When the perturbation has a transient character, compensatory responses are expected in terms of faster growth or a prolonged developmental period. In the case of insect larvae, details of such responses are insufficiently known at the proximate level. Attention to responses at the level of particular larval instars should promote an understanding of insect developmental plasticity also in a more general context. To provide an instar‐specific analysis of compensatory growth, larvae of the moth Orgyia antiqua (L.) are reared on inferior diet during one larval instar. Responses in growth parameters are recorded in the course of the manipulated instars, as well as at the level of the entire larval period. The negative relationship between development time and size in response to the inferior food quality, typical of the entire larval periods, is also observed within the manipulated instars taken separately. The manipulated larvae remain smaller than the larvae of the control group (significant in males only), even by the end of the subsequent instar during which all individuals are provided with superior host. In males, close to full size compensation by the time of pupation is achieved only by means of adding an extra larval instar. The inability of larvae to fully compensate during one and even two instars is considered as an indication of the presence of constraints on the within‐instar growth pattern. An alternative, adaptational explanation for the incomplete compensation could be based on the cost of prolonged development period. Given the ecological context of the species' life history, such an explanation appears less likely.     

THE ONTOGENY OF ASYMMETRY IN EARWIG FORCEPS

Fluctuating asymmetry may play an important role in the evolution of naturally selected and secondary sexual traits. However, very little is known about how asymmetries arise or how organisms maintain symmetry during development. Here I propose three mutually exclusive patterns for the development of asymmetries through consecutive growth stages: (1) compensatory growth, in which growth of the shorter side is greatest at the following growth stage; (2) persistent growth, in which growth of the longer side is greatest at the following growth stage; and (3) uncorrelated growth in which growth of the following stage is unrelated to the asymmetry at the previous one. I followed the growth in the forceps of male earwigs through four successive instars. Dyar's rule was used as a null model of insect growth. In the molt from the second to third instar, asymmetries increased through uncorrelated growth and with the magnitude but not the sign expected from Dyar's rule. However, following this, at the molts between instars 3–4 and 4–5, compensatory growth maintained asymmetries at a lower level than expected from Dyar's rule. Although there was no reduction in the absolute magnitude of asymmetry, relative asymmetry did decline. The net growth of forceps length did not follow Dyar's rule. The interpretation of patterns of growth were more sensitive and informative than the interpretation of the relations between asymmetries at consecutive instars.     

Number of flagellar segments and moulting in the amphipod Gammarus pulex

SUMMARY. The number of flagellar segments on the antennules of Gammarus pulex was quantitatively related to body size in animals from natural populations and to moulting and instar number of isolated animals grown from birth in the laboratory. The number of segments was 5.0 at birth increasing to means of 19–20 in females and 21–22 in males at sexual maturity or c. 5 mg wet wt reached after nine or ten moults. Addition of segments to the paired flagellae of juveniles was not regular and the number of segments cannot be used to identify particular instars of individuals or to determine their age. The mean interval (days) between moults progressively increased in the later juvenile instars and was exponentially related to moult number, age and the number of flagellar segments; the moult interval is also exponentially related to these variables in adults.     

Developmental variation in the forest tent caterpillar: life history consequences of a threshold size for pupation

In insects, size and age at adult emergence depend on larval growth that occurs in discrete steps or instars. Understanding the mechanisms controlling stepwise larval growth and the onset of metamorphosis is essential to the study of insect life history. We examined the patterns of growth of forest tent caterpillars Malacosoma disstria to quantify variation in the number of instars that larvae undergo before pupation, to identify the mechanisms underlying variation in larval development, and to evaluate the life history consequences of this variation. All caterpillars were reared under the same conditions; at each molt, the date, the head capsule width and the mass of the freshly molted insect were recorded. Logistic regression analysis showed that a threshold size (measured either as mass or head capsule width) must be reached at the beginning of a stadium for pupation to occur at the next molt. This threshold size was higher for females than for males, and as a result, females attained a higher pupal mass than males. To achieve this larger size, females often required more instars than males, despite a higher growth ratio (size increase within an instar). Within each sex, slow growing individuals exhibited more larval instars and longer larval development time, but attained the same pupal mass as faster growing individuals. The combination of a threshold size for pupation, discrete growth steps and variation in the number of these steps can thus complicate relationships between growth rate, pupal mass and larval development time. In our study, growth ratio and number of instars were correlated with development time but not with pupal mass, and no relationship was observed between development time and pupal mass. These findings imply that, in species with variable instar number, one cannot extrapolate overall larval growth from growth during a single instar. Given the constraints of discrete larval growth, variation in instar number provides greater flexibility for insects to compensate for poor growing conditions. In this case, inferior larval growth conditions don't necessarily lead to smaller adult size.     

Reduction of Delia radicum attack in field brassicas using a vertical barrier

According to life‐history theory, longer development time may result in bigger adults. However, reaction norms describing age and size at maturity often follow an L‐shaped form. This relationship is attributable to the simple notion that slowly growing individuals may not lengthen their development excessively after the maturation decision has been made, for example, when development is time limited in seasonal environments. In arthropods, growth occurs within instars, and thus the optimal growth strategy might be mediated by the phenotypic adjustment of instar numbers. We studied the relationship between age and size at maturity of a lichen‐feeding moth, Eilema depressum (Esper) (Lepidoptera: Arctiidae: Lithosiinae), and the variability of instar numbers in relation to achieved adult body mass and time used for maturation. A positive relationship between age and size at maturity was found across developmental pathways and a negative one within the developmental pathways. Directly developing larvae had higher growth rates, attained smaller pupal mass, and passed fewer instars than larvae maturing after overwintering. Host quality did not affect whether larvae matured during the remaining or the next season. High variation in the number of instars together with variable growth rates indicates high plasticity in adaptation to varying environmental conditions. Our results also confirm previous results that instar number variability may be a key characteristic mediating age and size at maturity in insects.     

Evergreen foliage allows early hatching in a pine processionary moth and escape from predation

1. Seasonal variation in leaf quality and climate conditions often imposes constraints on the temporal occurrence of tree‐feeding insect larvae, but the seasonal effects of predation have received limited attention. In temperate climate zones, both the abundance and activity of predators can be expected to vary over time. 2. The study reported herein examined the impact of temporal variation in predator activity levels on the life history of an herbivorous insect feeding on a constant food source: previous‐year needles of Scots pine (Pinus sylvestris L.). In field experiments, the survival and growth rates of colonies of Thaumetopoea pinivora Treitschke larvae that had been manipulated to hatch at three different dates were compared. Eggs of T. pinivora usually hatch by mid‐April in southern Sweden, which is earlier than most other herbivorous insects that overwinter as eggs in this region. 3. Predator exclusion experiments indicated that larvae which hatched later than April experienced a higher level of predator activity, mainly by ants. The final larval size and the timing of pupation were not affected by hatching date. First instar larvae were more extensively preyed on than second instars. 4. The life history of herbivore species can be affected by seasonal variation in predation pressures. This study suggests that early hatching in a lepidopteran species can allow a temporal escape from predation during the vulnerable early life stages.     

The significance of moulting in Ecdysozoan evolution

SUMMARY Three major bilaterian clades first appear in the Early Cambrian fossil record: Deuterostomia, Lophotrochozoa, and Ecdysozoa. The taxa placed in Ecdysozoa are characterized by a moulting habit, unknown in the other major clades. The origin and consequences of moulting are of fundamental importance to the history of the ecdysozoan clade, chiefly because moulting precludes motile ectodermal cilia. Moulting may have originated as an adaptation to permit the enlargement, during growth, of secreted cuticular spines, flanges, and other structures used as ancillary locomotory devices. A combination of phylogenetic and fossil evidence suggests that the early members of these clades were small vermiform paracoelomates that likely lacked indirect-developing planktotrophic larvae. Thus, the evolution of planktotrophic larvae may have been independently achieved at least three times within Bilateria. The nonmoulting clades evolved larvae that swim and feed via ciliated tufts and bands, presumably intercalating these forms within their early developmental systems. Within Ecdysozoa, feeding larvae lacked ciliary feeding tracts and evolved by modification of early instars, employing limbs or setae to generate feeding currents. The setting aside during larval life of cells that give rise to adult features is probably an adaptation associated with metamorphosis.     

Food quality effects on instar‐specific life histories of a holometabolous insect

1. It is a long‐standing challenge to understand how changes in food resources impact consumer life history traits and, in turn, impact how organisms interact with their environment. To characterize food quality effects on life history, most studies follow organisms throughout their life cycle and quantify major life events, such as age at maturity or fecundity. From these studies, we know that food quality generally impacts body size, juvenile development, and life span. Importantly, throughout juvenile development, many organisms develop through several stages of growth that can have different interactions with their environment. For example, some parasitoids typically attack larger instars, whereas larval insect predators typically attack smaller instars. Interestingly, most studies lump all juvenile stages together, which ignores these ecological changes over juvenile development.
2. We combine a cross‐sectional experimental approach with a stage‐structured population model to estimate instar‐specific vital rates in the bean weevil, Callosobruchus maculatus across a food quality gradient. We characterize food quality effects on the bean weevil's life history traits throughout its juvenile ontogeny to test how food quality impacts instar‐specific vital rates.
3. Vital rates differed across food quality treatments within each instar; however, their effect differed with instar. Weevils consuming low‐quality food spent 38%, 37%, and 18% more time, and were 34%, 53%, and 63% smaller than weevils consuming high‐quality food in the second, third, and fourth instars, respectively. Overall, our results show that consuming poor food quality means slower growth, but that food quality effects on vital rates, growth and development are not equal across instars. Differences in life history traits over juvenile ontogeny in response to food quality may impact how organisms interact with their environment, including how susceptible they are to predation, parasitism, and their competitive ability.

     

Photoperiod and larval body size: integrated factors controlling onset of the moulting cycle in Heliconius melpomene (Lepidoptera)

In Heliconius melpomene , ecdysis to each stadium is asynchronous in continuous light, but is synchronized with respect to the time of day in an LD 12:12 photoperiod regime-generally occurring during the early part of the photophase. This is a consequence of synchronism in the time of day of onset of the moulting cycle, which occurs approximately 24 hours before ecdysis. There is variation in the number of days taken to complete an instar, however. Onset of the moulting cycle is gated by photoperiod, and occurs at the first gate following attainment by the larvae of a certain threshold size, indicated by weight. By depriving larvae of food, the time at which threshold size is obtained can be delayed; this results in a delay in the time of onset of the moulting cycle. Possible biological advantages in the wild of the existence of a threshold size for onset of the moulting cycle, and of synchronism in the time of day of ecdysis, have been suggested.     

Dyar's rule and multivariate allometric growth in nine species of waterstriders (Heteroptera: Gerridae)

The constancy of postmoult/premoult ratios of measures of linear size during ontogeny in insect and other arthropods is widely known as Dyar's rule. We tested this rule in nine species of the waterstrider genera Gerris and Aquarius (Heteroptera: Gerridae), using two size variables: head width and a multivariate measure derived from the pattern of multivariate allometry common to the species considered. Allometric patterns were similar in two independent datasets of laboratory-reared and field-caught specimens. Although our data strictly followed Dyar's rule injust a few instances, all growth ratios varied within a limited range only. Growth ratios for head width differed more between moults than those for multivariate size. The relationship between growth ratios for the two size measures conformed to the predictions based on allometry. We discuss hypotheses of the possible adaptive significance of growth ratios, such as their relation to mobility and systematic differences between hemimetabolous and holometabolous insects, and emphasize the importance of allometry. Since Dyar's rule is consistent with available evidence of physiological mechanisms underlying growth and moulting control of insects and crustaceans, it can be used as a general frame of reference to test alternative growth models.     

From cells to colonies: at what levels of body organization does the ‘temperature‐size rule’ apply?

SUMMARY An inverse relationship between temperature during ontogeny and final body size is widespread in ectotherms, but poorly understood. Evidence suggests that within organs, this “temperature‐size rule” (TSR) may also apply to cell size with no change in numbers. So how closely do reductions in size and number of cells and other repeated structures correlate with size reduction at higher levels of organization? We examine this in the context of a proposal that size and/or number changes at various organizational levels are adaptive responses to temperature‐ and size‐dependent oxygen supply. We subjected two clones of the modular colonial bryozoan, Celleporella hyalina, to orthogonal combinations of two temperatures and two oxygen concentrations during ontogeny, observing effects on sizes of colonies and larvae, and sizes and numbers of cells, tentacles, and modules (autozooids). We found that the size:number responses varied among cell types and among structures at different levels of organization, with the inverse temperature‐size relationship applying only to larval parenchymal cells and colony modules. Using our findings and other evidence we propose a unifying adaptive hypothesis that predicts how temperature affects the sizes of mitochondria, cells, organs, modules and organisms, and their relationships with processes that determine the functional capacity of aerobic metabolism.     

Effects of repeated haemolymph withdrawals on haemocyte counts and moulting in lemon-butterfly, Papilio demoleus L

Total and differential haemocyte counts following repeated haemolymph withdrawals were made in V instar larvae of P. demoleus. While total count showed a steady reduction reaching its lowest in prepupal stage, much variation was observed in the relative percentage of various cell types. Further, the repeated removals of haemolymph from V instar larvae and pupae affected imaginal moulting and lengths of body and wings in adult butterflies.     

Induction of supernumerary larval moulting in the tobacco hornworm Manduca sexta: interaction of bisacylhydrazine ecdysteroid agonists with endogenous Juvenile Hormone

Abstract When given in a critical dietary dose range, the insecticidal bisacylhydrazine ecdysteroid agonists RH‐5849 or tebufenozide (RH‐5992) cause fifth stage Manduca sexta (L.) larvae to moult to a supernumerary sixth‐stage giant larva. The effect is dependent on exposure to the chemicals immediately after the previous ecdysis. Previous removal of the corpora allata does not interfere with the induction of premature moulting by RH‐5849 but completely prevents the formation of supernumerary larvae. The juvenilizing effect is therefore due to the interaction of the moult‐promoting effect of the ecdysteroid agonists with the high titre of endogenous Juvenile Hormone that is present just after ecdysis to the fifth stage in this insect. The ecdysteroid agonists themselves appear to have no intrinsic Juvenile Hormone‐agonist properties. Sixth‐stage larvae resulting from exposure to critical dietary concentrations of RH‐5849 are morphologically completely larval in character. When transferred to diet without the ecdysteroid agonist, they feed normally and gain weight, growing much larger than control fifth stage insects. At the end of the supernumerary stage, they cease to feed, wander in the usual way, and form a normal pupal cuticle but then die as pharate pupae without shedding the sixth‐stage larval cuticle.     

Life‐history traits in a parasitoid dipteran species with free‐living and obligate parasitic immature stages

The robber fly Mallophora ruficauda Weidemann (Diptera: Asilidae) is an important pest of apiculture in the Pampas of Argentina. As adults, they prey on honey bees and other insects, whereas the larvae are ectoparasitoids of Scarabaeidae grubs. Females of M. ruficauda lay eggs in grassland where the larvae drop to the ground after being wind‐dispersed and burrow underground searching for their hosts. A temporal asynchrony exists between the appearance of the parasitoid larvae and the host, with the parasitoid appearing earlier than the host. The present study investigates whether a strategy of synchronization with the host exists in M. ruficauda and determines which of the larval instars are responsible for it. Survival patterns and duration of the immature stages of the parasitoid are investigated to determine whether there is a modulation in the development at any time that could reduce the asynchrony. Experiments are carried out to determine the survival and duration of free‐living larval stadia in the absence of cues associated with the host. It is established that the first instar is capable of moulting to the second instar without feeding and in the absence of any cues related to the host, a unique event for parasitoids. Also, the first instar of M. ruficauda moults to the second stage within a narrow temporal window, and the second instar never moults in the absence of the host. After parasitizing a host, the second instar has the longest lifespan and is the most variable with respect to survival compared with the rest of the instars. All larval instars, except for those in the last (fifth) stadium, have a similar rate of mortality to that of second‐instar larvae. Additionally, it is established that the host is killed during the fourth (parasitoid) stadium and that the first‐ and fifth‐larval instars develop independently of the host. Finally, possible mechanisms that could aid in compensating for the asynchrony between the parasitoid and the host, promoting the host–parasitoid encounter, are discussed.     

Non‐moulted primary coverts correlate with rapid primary moulting

Time constraint is a main factor which affects the moult strategies in passerines, mainly during the first year of life. The variability of moult strategies between species is associated with the extent of the moult. In the first year of life, the extent of the moult is highly variable between species and individuals. In most passerine species, juveniles only renew some of their feathers, but the factors that govern which feathers are renewed and which are retained have been largely overlooked. Here we examine the common pattern of non‐moulted primary coverts (PC) in passerines during the first‐year moult cycle (post‐juvenile and first‐year pre‐breeding moults). On the interspecific level we found that among 63 species of passerines, PCs are the least commonly moulted feather tract. For five species (Hirundo rustica, Pycnonotus xanthopygos, Prinia gracilis, Acrocephalus stentoreus and Passer moabiticus) which perform a complete post‐juvenile moult, we found that the PC moult occurs over a longer period than greater coverts (GCs) and is sequential (non‐simultaneous). At the intraspecific level, we found that the main difference between a partial and complete moult in Prinia gracilis is the moulting or non‐moulting of the PCs. We also demonstrate that for Prinia gracilis 1) juveniles which do not moult their PCs, moult their primaries at a higher speed than those which moult their PCs and 2) area/mass ratio of PCs is lower than of GCs. These two findings may explain why many passerines skip PC renewal during the first year of life. Because the PC moult lasts a long time, forgoing this moult enables long term resource savings that allow for dealing with time constraints. Our results highlight the adaptive advantages of non‐moulted PCs in cases of time constraints.     

A Novel Technique for Identifying the Instar of Field-Collected Insect Larvae

Many field studies of insects have focused on the adult stage alone, likely because immature stages are unknown in most insect species. Molecular species identification (e.g., DNA barcoding) has helped ascertain the immature stages of many insects, but larval developmental stages (instars) cannot be identified. The identification of the growth stages of collected individuals is indispensable from both ecological and taxonomic perspectives. Using a larval–adult body size relationship across species, I present a novel technique for identifying the instar of field-collected insect larvae that are identified by molecular species identification technique. This method is based on the assumption that classification functions derived from discriminant analyses, performed with larval instar as a response variable and adult and larval body sizes as explanatory variables, can be used to determine the instar of a given larval specimen that was not included in the original data set, even at the species level. This size relationship has been demonstrated in larval instars for many insects (Dyar’s rule), but no attempt has been made to include the adult stage. Analysis of a test data set derived from the beetle family Carabidae (Coleoptera) showed that classification functions obtained from data sets derived from related species had a correct classification rate of 81–100%. Given that no reliable method has been established to identify the instar of field-collected insect larvae, these values may have sufficient accuracy as an analytical method for field-collected samples. The chief advantage of this technique is that the instar can be identified even when only one specimen is available per species if classification functions are determined for groups to which the focal species belongs. Similar classification functions should be created for other insect groups. By using those functions together with molecular species identification, future studies could include larval stages as well as adults.