Phenotypic plasticity and optimal timing of metamorphosis under uncertain time constraints

Life-history theory suggests that optimal timing of metamorphosis should depend on growth conditions and time constraints under which individuals develop. Current models cannot make reliable predictions for species in ephemeral habitats where individuals often face an increasing mortality risk over time because these models assume time-invariant mortality rates (i.e., daily mortality rates remain constant) and fixed seasons. We examined the plasticity of growth, development, and body mass at metamorphosis in tadpoles of the tree-hole breeding frog Phrynobatrachus guineensis in relation to an unpredictable time constraint in the field and in controlled experiments along a fixed density and food gradient. Mean mass and age at metamorphosis of sibships were positively correlated with per capita food level. Based on our results, we developed a simple model of the optimal timing of metamorphosis under time-dependent mortality rates showing that development rates are not only adjusted to growth conditions but also to time-variant mortality rates. The increasing mortality rate represents a time constraint that favors a reduced larval period, but because it is based on probabilities of survival it allows a trade-off between development time and mass. We extend this model to different types of time constraints and show that it can predict the range of documented reaction norms. Differences between species in␣the correlation of age and mass at metamorphosis may have evolved due to differences in their time-variant mortality rates.     

Linking movement and oviposition behaviour to spatial population distribution in the tree hole mosquito Ochlerotatus triseriatus

1. Researchers often use the spatial distribution of insect offspring as a measure of adult oviposition preferences, and then make conclusions about the consequences of these preferences for population growth and the relationship between life-history traits (e.g. oviposition preference and offspring performance). However, several processes other than oviposition preference can generate spatial patterns of offspring density (e.g. dispersal limitations, spatially heterogeneous mortality rates). Incorrectly assuming that offspring distributions reflect oviposition preferences may therefore compromise our ability to understand the mechanisms determining population distributions and the relationship between life-history traits. 2. The purpose of this study was to perform an empirical study at the whole-system scale to examine the movement and oviposition behaviours of the eastern tree hole mosquito Ochlerotatus triseriatus (Say) and test the importance of these behaviours in determining population distribution relative to other mechanisms. 3. A mark-release-recapture experiment was performed to distinguish among the following alternative hypotheses that may explain a previously observed aggregated distribution of tree hole mosquito offspring: (H(1)) mosquitoes prefer habitats with particular vegetation characteristics and these preferences determine the distribution of their offspring; (H(2)) mosquitoes distribute their eggs randomly or evenly throughout their environment, but spatial differences in developmental success generate an aggregated pattern of larval density; (H(3)) mosquitoes randomly colonize habitats, but have limited dispersal capability causing them to distribute offspring where founder populations were established; (H(4)) wind or other environmental factors may lead to passive aggregation, or spatial heterogeneity in adult mortality (H(5)), rather than dispersal, generates clumped offspring distributions. 4. Results indicate that the distribution of tree hole mosquito larvae is determined in part by adult habitat selection (H(1)), but do not exclude additional effects from passive aggregation (H(4)), or spatial patterns in adult mortality (H(5)). 5. This research illustrates the importance of studying oviposition behaviour at the population scale to better evaluate its relative importance in determining population distribution and dynamics. Moreover, this study demonstrates the importance of linking behavioural and population dynamics for understanding evolutionary relationships among life-history traits (e.g. preference and offspring performance) and predicting when behaviour will be important in determining population phenomena.     

Natural infection of the tree hole breeding mosquito Aedes triseriatus (Diptera: Culicidae) with the fungus Funicularius triseriatus

In the course of a study of the population of Aedes triseriatus, a female adults was found to be infected with a fungus. The fungus, Funicularius triseriatus, is described as a new genus and species of the class Hyphomycetes (form-class Deuteromycetes). F. triseriatus is characterized by thallic arthrospores produced on conidiophores arising from hyphae which are funiculose in habit. This is the first report of the natural occurrence of a fungus on A. triseriatus adults.     

Effect of changes in resource level on age and size at metamorphosis in Hyla squirella

Recent experiments suggest that timing of metamorphosis is fixed during development in some anurans, insects, and freshwater invertebrates. Yet, these experiments do not exclude a growth rate optimization model for the timing of metamorphosis. I manipulated food resources available to larvae of squirrel treefrogs (Hyla squirella) to determine if there is a loss of plasticity in duration of larval period during development and to critically test growth rate models for the timing of metamorphosis. Size-specific resource levels for individual tadpoles were switched from low to high or high to low at three developmental stages spaced throughout larval development. The effects of changes in resource availability on larval period and mass at metamorphosis were measured. Switching food levels after late limb bud development did not significantly affect larval period in comparison to constant food level treatments. Therefore, developmental rate in H. squirella is better described by a fixed developmental rate model, rather than a growth rate optimization model. The timing of fixation of developmental rate in H. squirella is similar to that found in other anuran species, suggesting a taxonomically widespread developmental constraint on the plasticity of larval period duration. Mass at metamorphosis was not significantly affected by the timing of changes in food levels; the amount of food available later in development determined the size at metamorphosis. Larval period and mass at metamorphosis were negatively correlated in only one of two experiments, which contrasts with the common assumption of a phenotypic trade-off between decreased larval period and increased mass at metamorphosis. Received: 19 August 1996 / Accepted: 20 June 1997     

Interspecific variation in desiccation survival time of Aedes (Stegomyia) mosquito eggs is correlated with habitat and egg size

Summary Survival times of eggs under three humidity conditions (42%, 68%, 88% RH) were investigated among Aedes (Stegomyia) mosquitoes from temperate and tropical zones (5 species and 20 geographical strains). This subgenus tends to occupy small aquatic sites as larvae, where desiccation resistance of eggs is necessary during habitat drought. Interspecific comparison showed that the egg survival time was correlated with egg volume and dryness of source locality, and probably with habitat. Aedes aegypti is associated most with arid climate and human-disturbed habitats — its large eggs survived the longest periods at all humidities. Aedes albopictus ranges from tropics to temperate zones and inhabits both disturbed and forest habitats — its eggs were less desiccation-resistant than A. aegypti eggs. The survival times for forest species eggs (A. riversi, A. galloisi, A. flavopictus) were variable at high humidities but at the lowest humidity were consistently shorter than for eggs of A. aegypti and A. albopictus.     

Ecological constraints on amphibian metamorphosis: interactions of temperature and larval density with responses to changing food level

Phenotypic plasticity is adaptive for an organism inhabiting a variable environment if the optimal phenotype of a trait that affects fitness varies with environmental conditions, and if the organism can perceive environmental conditions and respond appropriately. Wilbur and Collins have proposed that amphibian larvae might respond adaptively to changes in their resource environment. If conditions for growth in the aquatic environment deteriorate, then a tadpole should metamorphose earlier and smaller than a tadpole under constant high growth conditions. Several experiments on a variety of species have tested this prediction, but only one demonstrated such a response. That experiment involved Couch's spadefoot toads (Scaphiopus couchii) and employed a gradual decrease in food level, whereas the others all used an abrupt switch from high to low food. The purpose of the present experiment was to examine the response of S. couchii to an abrupt change in food level, and to determine if the response depended on the level of two other factors, density and temperature, that also affect larval development. The average effects of the abrupt change in food level were similar to those seen in studies on other species: age at metamorphosis was primarily determined by the early food regime, and size at metamorphosis was determined by food level late in the larval period, suggesting that the effect of decreased food depends on how the food change is done. However, the response to even an abrupt food change depended on interactions with other environmental factors. At high temperature, high initial food, and low density, development was very rapid and tadpoles switched from high to low food metamorphosed at about the same time and size as those at constant high food. In contrast, under high temperature and high initial food conditions, but at high density, tadpoles switched to low food metamorphosed somewhat earlier and smaller, on average, than tadpoles kept at high food. At low temperature, the direction of response depended on density: tadpoles metamorphosed much smaller and slightly, but significantly, earlier at low density, but smaller and later at high density. The developmental response to increased food also varied with temperature. Larvae at high temperature metamorphosed earlier and larger than those at constant low food. At low temperature, larvae metamorphosed larger, but at nearly the same time as their counterparts at constant low food. The combination of high density and constant low food prevented any tadpoles from metamorphosing at high temperature, and allowed relatively few metamorphs at low temperature. Under conditions which impose either very rapid or retarded development, the opportunity to respond to altered food level may be limited. Interactions among environmental factors, therefore, may constrain responses to changing conditions, and may even prevent completion of development. Received: 3 February 1997 / Accepted: 2 October 1997     

Patterns of natural selection on size at metamorphosis in water frogs

Strategies for optimal metamorphosis are key adaptations in organisms with complex life cycles, and the components of the larval growth environment causing variation in this trait are well studied empirically and theoretically. However, when relating these findings to a broader evolutionary or ecological context, usually the following assumptions are made: (1) size at metamorphosis positively relates to future fitness, and (2) the larval growth environment affects fitness mainly through its effect on timing of and size at metamorphosis. These assumptions remain poorly tested, because data on postmetamorphic fitness components are still rare. We created variation in timing of and size at metamorphosis by manipulating larval competition, nonlethal presence of predators, pond drying, and onset of larval development, and measured the consequences for subsequent terrestrial survival and growth in 1564 individually marked water frogs (Rana lessonae and R. esculenta), raised in enclosures in their natural environment. Individuals metamorphosing at a large size had an increased chance of survival during the following terrestrial stage (mean linear selection gradient: 0.09), grew faster and were larger at maturity than individuals metamorphosing at smaller sizes. Late metamorphosing individuals had a lower survival rate (mean linear selection gradient: -0.03) and grew more slowly than early metamorphosing ones. We found these patterns to be consistent over the three years of the study and the two species, and the results did not depend on the nature of the larval growth manipulation. Furthermore, individuals did not compensate for a small size at metamorphosis by enhancing their postmetamorphic growth. Thus, we found simple relationships between larval growth and postmetamorphic fitness components, and support for this frequently made assumption. Our results suggest postmetamorphic selection for fast larval growth and provide a quantitative estimate for the water frog example.     

Effect of leaf litter and density on fitness and population performance of the hole mosquito Aedes triseriatus

Abstract.

• 1 We tested the effects of food, in the form of leaf litter, and density on population growth and fitness correlates of the tree hole mosquito Aedes triseriatus. Our field experiment used a 2 x 2 randomized block design, with three holes as blocks. In cages within three holes, we manipulated densities of Aedes triseriatus larvae, and presence of leaf litter. Our laboratory experiment used a 2 x 3 factorial design in which we also manipulated densities of larvae and availability of leaf litter within similar cages (inside, outside, or absent). For both experiments we determined effects on survival, days to and mass at eclosion of both sexes, and a composite index of population performance λ′, that estimates finite rate of increase.
• 2 In the field experiment, we found significant and large effects of leaf litter and of density on the performance of A. triseriatus. The effect of density did not depend on leaf litter availability. We documented significant variation among tree holes for most correlates of fitness. Often, the effects of treatments varied significantly depending on the tree hole tested.
• 3 In the laboratory experiment we found significant effects of density and litter, and that direct browsing on leaf litter is necessary for the effect of litter on performance of A. triseriatus. In the laboratory, the negative effect of increased density was dependent on leaf litter availability.
• 4 Our results demonstrate that leaf litter has important effects on population performance of tree hole mosquitoes in natural tree holes. Direct browsing on the surface of leaf litter is the most likely mechanism by which litter enhances population growth. The impact of litter on populations varies among tree holes.

     

Costs of reproduction and geographic variation in the reproductive tactics of the mosquito Aedes triseriatus

Intraspecific host discrimination is widespread in solitary parasitoids whose adult females forage for and evaluate host suitability, whereas interspecific discrimination is less common. In some parasitoid species, mostly Diptera and Coleoptera, the larva performs the last step of host searching. It has been suggested that host discrimination will rarely occur in such host-seeking larvae because their low mobility results in a low host encounter rate. We determined the extent to which the larvae of Aleochara bilineata Gyllenhal (Coleoptera: Staphylinidae), a solitary parasitoid of aggregated Diptera pupae: (1) discriminated between unparasitized hosts and hosts parasitized by conspecifics; (2) used semiochemical cues to discriminate; (3) were influenced by life expectancy, presence of conspecifics and host availability in their host acceptance decision; and the extent to which (4) A. bilineata and A. bipustulata L., a species exploiting the same hosts and occurring sympatrically, showed interspecific host discrimination. A. bilineata larvae were able to discriminate between unparasitized hosts and hosts parasitized by conspecifics in a choice experiment. Such behavior has never previously been described for a coleopteran parasitoid or for a parasitoid species whose larvae perform host searching. Host discrimination in this species was not based on the presence of visual or tactile cues (e.g., entrance holes) but rather on chemical cues. The life expectancy of A. bilineata larvae was significantly shorter in the presence than in absence of hosts, and older larvae had lower parasitism success than young larvae in a 24-h experiment. However, the host acceptance decision of A. bilineata larvae was not influenced by larval age or the presence of conspecifics when the ratio of hosts per larva was greater than or equal to 1. When hosts were scarce, the degree of superparasitism increased significantly with the number of foraging conspecifics and the age of the larvae. Both species of Aleochara showed intra- and interspecific host discrimination in a choice experiment. In contrast to A. bipustulata, A. bilineata larvae more frequently parasitized hosts parasitized by A. bipustulata than those parasitized by conspecifics. We suggest that host discrimination will be frequent in solitary parasitoids with host-seeking larvae when hosts are aggregated. Received: 4 June 1998 / Accepted: 1 September 1998     

Sequential predator effects across three life stages of the African tree frog, <Emphasis Type="Italic">Hyperolius spinigularis</Emphasis>

While theoretical studies of the timing of key switch points in complex life cycles such as hatching and metamorphosis have stressed the importance of considering multiple stages, most empirical work has focused on a single life stage. However, the relationship between the fitness components of different life stages may be complex. Ontogenetic switch points such as hatching and metamorphosis do not represent new beginnings—carryover effects across stages can arise when environmental effects on the density and/or traits of early ontogenetic stages subsequently alter mortality or growth in later stages. In this study, I examine the effects of egg- and larval-stage predators on larval performance, size at metamorphosis, and post-metamorphic predation in the African tree frog Hyperolius spinigularis. I monitored the density and survival of arboreal H. spinigularis clutches in the field to estimate how much egg-stage predation reduced the input of tadpoles into the pond. I then conducted experiments to determine: (1) how reductions in initial larval density due to egg predators affect larval survival and mass and age at metamorphosis in the presence and absence of aquatic larval predators, dragonfly larvae, and (2) how differences in mass or age at metamorphosis arising from predation in the embryonic and larval environments affect encounters with post-metamorphic predators, fishing spiders. Reduction in larval densities due to egg predation tended to increase per capita larval survival, decrease larval duration and increase mass at metamorphosis. Larval predators decreased larval survival and had density-dependent effects on larval duration and mass at metamorphosis. The combined effects of embryonic and larval-stage predators increased mass at metamorphosis of survivors by 91%. Larger mass at metamorphosis may have immediate fitness benefits, as larger metamorphs had higher survival in encounters with fishing spiders. Thus, the effects of predators early in ontogeny can alter predation risk even two life stages later.     

Pre-hatching exposure to water mold reduces size at metamorphosis in the moor frog

Developmental plasticity is increasingly recognized as important for ecological and evolutionary processes. However, few studies consider the potential for delayed effects of early environments. Here, we show that tadpoles hatching from clutches exposed to water mold (Saprolegnia) have 20% decreased mass at metamorphosis, despite no further exposure subsequent to hatching. The effects were consistent across four populations that have previously been shown to vary in their resistance to infection during embryonic development. Contrary to expectations, time to hatching or metamorphosis was not affected, suggesting that the results do not reflect an evolved escape strategy from infected waters triggered by embryonic conditions. Instead, decreased mass at metamorphosis may arise from carry-over effects of impaired embryo development. Such strong links across developmental stages have potential consequences for the evolution of plasticity and the responses of populations to emergent infections.     

Negative effects of habitat drying and prior exploitation on the detritus resource in an ephemeral aquatic habitat

Ephemeral aquatic habitats are characterized by cycles of drying and subsequent inundation, and by production of sequential non-overlapping cohorts of organisms. Both processes may alter the quantity or quality of resources, and may therefore affect survival and development of cohorts that subsequently colonize ephemeral habitats. We examined these effects of habitat drying and non-overlapping cohorts on experimental cohorts of the tree hole mosquito Aedes triseriatus, testing specifically whether the value of leaf litter as a food resource is altered by cycles of inundation and drying, or by exploitation by a prior non-overlapping cohort. We created four treatments of leaf litter: (1) no prior cohort, continuously wet; (2) no prior cohort, one␣wet/dry cycle; (3) prior cohort, continuously wet, and (4) prior cohort, one wet/dry cycle, and tested for effects on individual fitness components (survivorship, mean dry mass at, and median days to eclosion) and on population growth (estimated finite rate of increase –λ′). Both resource drying and the presence of a prior cohort negatively affected individual fitness components in tires, increasing days to eclosion, and decreasing mean dry mass at eclosion for both sexes. Resource drying also negatively affected estimated rates of increase (λ′) in tree holes. A prior cohort had no significant effects on λ′. These results indicate that intraspecific interactions among mosquito larvae may include amensalistic effects of earlier, non-overlapping cohorts, and that resource drying reduces resource quality. The latter effect indicates that enhanced production of A. triseriatus from recently filled containers is not due to resource drying per se, and may result from more complex community-level effects of habitat drying. Extreme cycles of drying and inundation seem likely to increase intraspecific resource competition among drought-adapted species like A. triseriatus. Received: 5 May 1997 / Accepted: 20 January 1998     

Density-dependent effects of mortality on the optimal body size to shift habitat: Why smaller is better despite increased mortality risk

Many animal species across different taxa change their habitat during their development. An ontogenetic habitat shift enables the development of early vulnerable-to-predation stages in a safe “nursery” habitat with reduced predation mortality, whereas less vulnerable stages can exploit a more risky, rich feeding habitat. Therefore, the timing of the habitat shift is crucial for individual fitness. We investigate the effect that size selectivity in mortality in the rich feeding habitat has on the optimal body size at which to shift between habitats using a population model that incorporates density dependence. We show that when mortality risk is more size dependent, it is optimal to switch to the risky habitat at a smaller rather than larger body size, despite that individuals can avoid mortality by staying longer in the nursery habitat and growing to safety in size. When size selectivity in mortality is high, large reproducing individuals are abundant and produce numerous offspring that strongly compete in the nursery habitat. A smaller body size at habitat shift is therefore favored because strong competition reduces growth potential. Our results reveal the interdependence among population structure, density dependence, and life history traits, and highlight the need for integrating ecological feedbacks in the study of life history evolution.     

Phenotypic plasticity in response to nitrate supply of an inherently fast-growing species from a fertile habitat and an inherently slow-growing species from an infertile habitat

The aim of the present study was to investigate possible differences in plasticity between a potentially fast-growing and a potentially slow-growing grass species. To this end, Holcus lanatus (L.) and Deschampsia flexuosa (L.) Trin., associated with fertile and infertile habitats, respectively, were grown in sand at eight nitrate concentrations. When plants obtained a fresh weight of approximately 5 g, biomass allocation, specific leaf area, the rate of net photosynthesis, the organic nitrogen concentration of various plant parts and the root weight at different soil depths were determined. There were linear relationships between the morphological and physiological features studied and the In-transformed nitrate concentration supplied, except for the specific leaf area and root nitrogen concentration of H. lanatus, which did not respond to the nitrate concentration. The root biomass of H. lanatus was invariably distributed over the soil layers than that of D. flexuosa. However, D. flexuosa allocated more root biomass to lower soil depths with decreasing nitrate concentration, in contrast to H. lanatus, which did not respond. The relative response to nitrate supply, i.e. the value of a character at a certain nitrate level relative to the value of that character at the highest nitrate supply, was used as a measure for plasticity. For a number of parameters (leaf area ratio, root weight ratio, root nitrogen concentration, vertical root biomass distribution and rate of net photosynthesis per unit leaf weight) the potentially slow-growing D. flexuosa exhibited a higher phenotypic plasticity than the potentially fast-growing H. lanatus. These findings are in disagreement with current literature. Possible explanations for this discrepancy are discussed in terms of differences in experimental approach as well as fundamental differences in specific traits between fast- and slow-growing grasses.     

Syntaxin 1A modulates the sexual maturity rate and progeny egg size related to phase changes in locusts

The migratory locust (Locusta migratoria) exhibits clear phenotypic plasticity depending on its population density. Previous studies have explored the molecular mechanisms of body colour, behavior, immunity, and metabolism between high population density gregarious (G) and low population density solitarious (S) locusts. However, the molecular mechanisms underlying differences in reproductive traits remain unknown. G locusts reach sexual maturation much faster and lay larger eggs compared with S locusts. The traits of G locusts decreased significantly with isolation, whereas those of S locusts increased with crowding. Analysis of gene expression in female adults indicated that syntaxin 1A (Syx1A) was expressed significantly higher in G locusts than in S locusts. After silencing Syx1A expression in G locusts by RNA interference (RNAi), their sexual maturity rate and progeny egg size changed towards those of S locusts. Similarly, increment in the traits of S locusts with crowding was blocked by Syx1A interference. Changes in the traits were also confirmed by decrease in the level of vitellogenin, which is regulated by Syx1A. In conclusion, plasticity of the sexual maturity rate and progeny egg size of G and S locusts, which is beneficial for locusts to adapt to environmental changes, is regulated by Syx1A.     

Effects of leaf litter species on macroinvertebrate community properties and mosquito yield in Neotropical tree hole microcosms

Detritus quality and quantity affect macroinvertebrate productivity and distribution in many freshwater ecosystems. This study experimentally investigated the effects of leaf litter from Ceiba pentandra, Dipteryx panamensis, Ficus yoponensis, and Platypodium elegans on macroinvertebrate species composition, richness, and abundance in artificial water-filled tree holes in a lowland moist forest of Panama. Species composition was similar among treatments, but species richness and longevity differed among litter types and were consistently highest with Platypodium litter. Similar patterns were observed in natural tree holes of the focal tree species. The mosquito Culex mollis was the most abundant species in the field experiment. Average conductivity and dissolved oxygen concentration differed among leaf species, but pH did not. Leaf toughness was positively correlated with mean macroinvertebrate abundance and cumulative species richness. A laboratory experiment measured C. mollis yield and pupation time in tree hole microcosms containing the four litter species. Cumulative mosquito mass and time to pupation differed among leaf litter species, with Platypodium litter supporting the greatest yield. Pupation was slowest on Ceiba litter. Grazing by mosquito larvae facilitated leaf decomposition in all treatments. Results suggest that differences in macroinvertebrate species richness and mosquito yield can be attributed to differences in nutritional quality among litter species. Received: 14 October 1998 / Accepted: 21 February 1999     

Strong habitat selection and the development of population structure in a mosquito

Summary Remarkably simple and regular patterns of genic variation for two electrophoretically assayed loci are presented against a background of strong habitat selection, population isolation, and population structuring in the pitcher-plant mosquitoWyeomyia smithii. The genic variation assessed thus far comes from 29 local populations, all but one of which lie within the glaciated region of North America. Although the conclusions drawn from these patterns are still quite tentative, it appears that the fact that the same higher frequency electromorphs occurred everywhere for both loci may be due more to selection than drift. Drift or selection, acting alone or in concert may be responsible for the almost complete absence of electromorphs of intermediate frequency. A weak association was found between the two-locus genic variation and the well-studied diapause-development time variation in this species. It is suggested that a Wrightian interaction system and fluctuating-stabilizing selection might account for maintenance of the genic level polymorphism. The observations reported are circumstantially in accord with Wright's shifting balance process of evolution. Future studies in the older parts of the species range will put these hypotheses to a strong test.     

Life history reaction norms to time constraints in a damselfly: differential effects on size and mass

Optimality models predict that, under a time constraint, organisms should accelerate development, and preferably so by increasing growth rate, to keep size at emergence constant. Unfortunately, most tests did neglect genetic constraints and interchanged mass with body size which may explain mixed support for some of the models' predictions. We imposed time constraints on full sibling larvae of the damselfly Enallagma cyathigerum by manipulating day length regimes. Under a time constraint, larval development and growth rate based on size indeed were faster. This made it possible to keep size at emergence constant, despite the shorter development time. Interestingly, under a time constraint, growth rate based on mass was not increased and larvae had a lower mass at emergence. We see two reasons for this difference between body mass and size. First, size is fixed at emergence, while mass can still increase in many insects. Secondly, genetic constraints may have contributed to different responses for size and mass. In general, our results strongly suggest discriminating between size and mass when testing life history responses.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 83 , 187–196.