Linking stages of life history: How larval quality translates into juvenile performance for an intertidal barnacle (Balanus glandula)

Many marine invertebrates with complex life cycles produce planktoniclarvae that experience environmental conditions different fromthose encountered by adults. Factors such as temperature andfood, known to impact the larval period, can also affect larvalsize and consequently the size of newly settled juveniles. Afterdocumenting natural variation in the size of cyprids (the finallarval stage) of the barnacle Balanus glandula, we experimentallymanipulated temperature and food given to larvae to producecyprids of differing sizes but within the size range of cypridsfound in the field. In a set of trials in which larvae of B.glandula were raised on full or reduced rations in the laboratoryand subsequently outplanted into the field as newly metamorphosedjuveniles, we explored the effects of larval nutrition and sizeon juvenile performance. Larvae that received full rations throughouttheir feeding period produced larger cyprids (with more lipidand protein). These larger cyprids grew faster as juvenilesand sometimes survived better in the field than juveniles fromlarvae that had their food ration reduced in the last feedinginstar. For naturally settling barnacles brought into the laboratorywithin 2 days of settlement and fed, we found that initial juvenilesize was a good predictor of juvenile size even after 2 weeksof growth. By manipulating food given to juveniles that werederived from larvae fed either full or reduced rations, we foundthat larval nutritional effects persisted in juveniles for 2–3times the period that larvae experienced altered food rations.     

Plasticity of size and growth in fluctuating thermal environments: comparing reaction norms and performance curves

Ectothermic animals exhibit two distinct kinds of plasticityin response to temperature: Thermal performance curves (TPCs),in which an individual's performance (e.g., growth rate) variesin response to current temperature; and developmental reactionnorms (DRNs), in which the trait value (e.g., adult body sizeor development time) of a genotype varies in response to developmentaltemperatures experienced over some time period during development.Here we explore patterns of genetic variation and selectionon TPCs and DRNs for insects in fluctuating thermal environments.First, we describe two statistical methods for partitioningtotal genetic variation into variation for overall size or performanceand variation in plasticity, and apply these methods to availabledatasets on DRNs and TPCs for insect growth and size. Our resultsindicate that for the datasets we considered, genetic variationin plasticity represents a larger proportion of the total geneticvariation in TPCs compared to DRNs, for the available datasets.Simulations suggest that estimates of the genetic variationin plasticity are strongly affected by the number and rangeof temperatures considered, and by the degree of nonlinearityin the TPC or DRN. Second, we review a recent analysis of fieldselection studies which indicates that directional selectionfavoring increased overall size is common in many systems—thatbigger is frequently fitter. Third, we use a recent theoreticalmodel to examine how selection on thermal performance curvesrelates to environmental temperatures during selection. Themodel predicts that if selection acts primarily on adult sizeor development time, then selection on thermal performance curvesfor larval growth or development rates is directly related tothe frequency distribution of temperatures experienced duringlarval development. Using data on caterpillar temperatures inthe field, we show that the strength of directional selectionon growth rate is predicted to be greater at the modal (mostfrequent) temperatures, not at the mean temperature or at temperaturesat which growth rate is maximized. Our results illustrate someof the differences in genetic architecture and patterns of selectionbetween thermal performance curves and developmental reactionnorms.     

Larval development of the pedunculate barnacles Octolasmis angulata Aurivillius 1894 and Octolasmis cor Aurivillius 1892 (Cirripedia: Thoracica: Poecilasmatidae) from the gills of the mud crab,Scylla tranquebarica Fabricius, 1798

Detailed studies of larval development of Octolasmis angulata and Octolasmis cor are pivotal in understanding the larval morphological evolution as well as enhancing the functional ecology. Six planktotrophic naupliar stages and one non-feeding cyprid stage are documented in details for the first time for the two species of Octolasmis. Morphologically, the larvae of O. angulata and O. cor are similar in body size, setation patterns on the naupliar appendages, labrum, dorsal setae-pores, frontal horns, cyprid carapace, fronto-lateral gland pores, and lattice organs. Numbers of peculiarities were observed on the gnathobases of the antennae and mandible throughout the naupliar life-cycle. The setation pattern on the naupliar appendages are classified based on the segmentation on the naupliar appendages. The nauplius VI of both species undergoes a conspicuous change before metamorphosis into cyprid stage. The cyprid structures begin to form and modify beneath the naupliar body towards the end of stage VI. This study emphasises the importance of the pedunculate barnacle larval developmental studies not only to comprehend the larval morphological evolution but also to fill in the gaps in understanding the modification of the naupliar structures to adapt into the cyprid life-style.     

Plasticity in the timing of a major life‐history transition and resulting changes in the age structure of populations of the salamander Hynobius retardatus

Variation in age and size at life‐history transitions is a reflection of the diversifying influence of biotic or abiotic environmental change. Examples abound, but it is not well understood how such environmental changes influence the age structure of a population. I experimentally investigated the effects of water temperature and food type on age and body size at metamorphosis in larvae of the salamander Hynobius retardatus. In individuals grown at a cold temperature (15 °C) or given Chironomidae as prey, the time to metamorphosis was significantly prolonged, and body size at metamorphosis was significantly enlarged, compared with individuals grown at a warmer temperature (20 °C) or fed larvae. I also examined whether larval density (a possible indicator of cannibalism in natural habitats) generated variation in the age structure of natural populations in Hokkaido, Japan, where the climate is subarctic. Natural ponds in Hokkaido may contain larvae that have overwintered for 1 or 2 years, as well as larvae of the current year, and I found that the number of age classes was related to larval density. Although cool water temperatures prolong the larval period and induce later metamorphosis, in natural ponds diet‐based enhancement of development translated into a shorter larval duration and earlier metamorphosis. Geographic variation in the frequency of cannibalism resulted in population differences in metamorphic timing in H. retardatus larvae. It is important to understand how environmental effects are ultimately transduced through individual organisms into population‐level phenomena, with the population response arising as the summation of individual responses. Without a thorough comprehension of the mechanisms through which population and individual responses to environmental conditions are mediated, we cannot interpret the relationship between population‐level and individual‐level phenomena. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 100–114.     

Naupliar development of Acanthodiaptomus denticornis (wierzejski, 1887) and Arctodiaptomus alpinus (Imhof, 1885) (Copepoda: Calanoida) and a comparison with other Diaptomidae

The six naupliar instars of the two alpine species Aconthodiaptornusdenticornis and Arctodiaptomus alpinus are described and illustrated.Their external morphology is compared with that of all presentlyknown diaptomid nauplii in an attempt to provide usehl taxonomiccharacteristics to identify larval diaptomids. The larval stagesof the two species are remarkably similar in size and overallappearance, and show an identical pattern of limb setation throughoutthe whole development. Diagnostic characters are mainly relatedto the differentiation of antennules and caudal armature.     

Ontogenic phototactic behaviors of larval stages in intertidal barnacles

Hydrobiologia - During larval development of the intertidal barnacle Fistulobalanus albicostatus, larvae in the naupliar stages I and II (NI&II) possess a single naupliar eye, and later...     

The dynamics of sponge larvae assemblages from northwestern Mediterranean nearshore bottoms

In this study, we show for the first time the dynamics of spongelarvae assemblages from nearshore meroplankton. Plankton wascollected by SCUBA diving once or twice a week during a 2-yearperiod over a rocky artificial reef in the NW Mediterranean.Data on larval abundance were cross correlated with the valuesof environmental parameters (i.e. seawater temperature, solarradiation, wind speed and atmospheric pressure). In the laboratory,we recorded external features and main behaviors of larvae.We collected larvae belonging to 20 different taxa of sponges,which are among the most common in the sublittoral hard bottomcommunities of the NW Mediterranean and other temperate areas.There was a positive correlation between maximum abundance oflarvae and highest water temperatures. Maximum solar radiationpreceded the maximum of larval abundance. Wind speed showedno clear seasonal patterns and atmospheric pressure was overallthe lowest when larvae were most abundant. Two main patternsin the larval release periods were observed. One was shown byspecies releasing larvae in summer, right before the maximumwater temperatures (orders Dictyoceratida and Dendroceratida)and another by the species whose larvae release from the endof summer till autumn, when temperatures decrease (order Poecilosclerida).The larvae of Phorbas tenacior, Raphidoflus jolicoueri, Mycalerotalis, Tedania anhelans, Pleraplysilla spinifera, Aplysillasulfurea var. rosea and Chelonaplysilla noevus are describedfor the first time. The larvae collected mainly belonged tothe parenchymella type (except for the species Oscarella sp.and probably Cliona viridis) and showed different features andbehaviors: from the elongated parenchymellae of Scopalina lophyropoda(order Halichondrida), which show simple swimming behavior andno response to light, to the parenchymellae of Poeciloscleridaand Dictyoceratida orders with variable morphologies as adaptationsto complex swimming behaviors. Our database will hopefully contributeto the present knowledge of larval types in sponges and definitivelyhighlight the importance of this group in the dynamics of meroplanktonfrom nearshore bottoms.     

Larval development of Lynceus brachyurus (Crustacea, Branchiopoda, Laevicaudata): redescription of unusual crustacean nauplii, with special attention to the molt between last nauplius and first juvenile

The larval development of "conchostracans" has received only scattered attention. Here I present the results of a study on the larval (naupliar) development and the metamorphosis of Lynceus brachyurus, a member of the bivalved branchiopod order the Laevicaudata. Lynceus brachyurus is the only species of the "Conchostraca" in Denmark. The phylogenetic position of the Laevicaudata has traditionally been a source of controversy, and this study does not solve the question completely. This work focuses on features potentially important for phylogeny. The general appearance of the larvae of L. brachyurus has been known for more than a century and a half, and some of its unique features include a large, larval dorsal shield; a huge, plate-like labrum; and a pair of immovable, horn-like antennules. However, many details relating to limb morphology, potentially important for phylogeny, have not been studied previously. Based on size categories, five or six larval stages can be recognized. The larvae approximately double their length and width during development (length: 230-520 microm). Most morphological features stay largely unchanged during development, but the antennal coxal masticatory spines are significant exceptions: they become bifid after one of the first molts. In all larval stages only the antennae and the mandibles actively move. In late naupliar stages the trunk limbs become visible as rows of laterally placed, undeveloped, and still immovable lobes. Swimming is performed by the antennae, whereas the mandibles appear to be involved mainly in feeding, as in other branchiopod larvae. The last naupliar stage undergoes a small metamorphosis to the first juvenile stage, the details of which in part were studied by following the premolt juvenile condition through the cuticle of the last stage nauplius. Among other changes there is a characteristic change in the shape and morphology of the univalved dorsal naupliar shield to a bivalved juvenile carapace. The general morphologies of the antennae and the mandibles are very similar to those of other branchiopod larvae and fall well within the "branchiopod naupliar feeding apparatus" recognized as a branchiopod synapomorphy by Olesen (2003), but some specific features shared with the larvae of other "conchostracans" are also identified. These special "conchostracan" features include: 1) a similar antennular setation; 2) a similar comb-like setulation of the bifid antennal coxal processes; and 3) mandibular palpsetae with setules condensed. In light of recent suggestions concerning branchiopod phylogeny (Cyclestheria as a sister group to the Cladocera), these similarities probably do not support a monophyletic "Conchostraca" but rather are symplesiomorphies of this taxon. A final decision must await a phylogenetic analysis of a more complete set of characters.     

Study and modelling of the development of Euterpina acutifrons (Copepoda: harpacticoida)

The larval development of populations initially composed ofnauplii Nl of Euterpina acurifrons (Copepoda: Harpacticoida)is studied in the laboratory. A first experiment in which temperatureis the only varying parameter allows an assessment of inherentvariability of development. A simple mathematical model thenaccounts for the effect of temperature on development. We findresidence times to be almost identical for all developmentalstages, and higher mortality rates in the case of stages N6and Cl. The model also accounts for latency times observed inthe development of populations including larval stages. A secondexperiment, run at constant temperature, shows that a deficientfood supply increases the average residence time of early stages,as well as their variance. Data obtained on a population bredin tanks under unregulated trophic and temperature conditionsshow that the variation with time of the stage composition ofthe population modulates the effect of external factors on thegrowth of the population.     

Eclosion rate, development and survivorship of Aedes albopictus (Skuse)(Diptera: Culicidae) under different water temperatures

In tropical areas, where vector insects populations are particularly numerous, temperature usually range between 25 degrees C and 35 degrees C. Considering the importance of such temperature variation in determining mosquitoes population dynamics, in this work the developmental, eclosion and survival rates of the immature stages of Aedes albopictus (Skuse) were compared under constant 25, 30 and 35 degrees C (using acclimatized chambers) and environmental (25 degrees C to 29 degrees C) temperatures. The hatching rate was considered as total number of larvae recovered after 24h. The development period as well as larval and pupal survival rate were evaluated daily. Eclosion rate was significantly higher under environmental temperature than under the studied constant temperatures, suggesting that temperature variation may be an eclosion-stimulating factor. The mean eclosion time increased with the temperature, ranging from 2.8h (25 degrees C) to 5.2h (35 degrees C). The larval period was greatly variable inside each group, although it did not differ significantly amongst groups (11.0 +/- 4.19 days), with individuals showing longer larval stages in water at 35 degrees C (12.0 +/- 4.95 days) and environmental temperature (13.6 +/- 5.98 days). Oppositely, survival was strongly affected by the higher temperature, where only one individual lived through to adult phase. The results suggest that population of Ae. albopictus from Recife may be adapting to increasing of environmental temperatures and that the limiting temperature to larval development is around 35 degrees C.     

Natural variability in size and condition at settlement of 3 species of marine invertebrates

Experimental studies have demonstrated that for many marineinvertebrate species, variability in larval condition or qualityat settlement may have important effects on post-settlement,early juvenile performance. Relatively few studies, however,explicitly examine natural variability in larval condition atsettlement. This study examines natural variability in larvalattributes (size and lipid index) at settlement for terminal-stagelarvae of intertidal mussels (Mytilus sp.) and barnacles (Pollicipespolymerus and Chthamalus dalli) from southern California. Despitesignificant differences among cohorts in larval attributes,for all 3 species a greater percentage of the variance in larvallength (80–100%) and lipids (58–83%) occurred amongindividuals within a cohort, rather than among cohorts. Forall 3 species, coefficients of variation within a cohort forlength were much smaller (3–8%) than those for lipid index(30–93%), suggesting that lipid storage is a much moreplastic attribute than size for larvae. For mussels, settlementintensity and larval attributes were decoupled, such that averagelarval condition of a cohort was not related to the number oflarvae that settled. At the cohort level, Mytilus and Pollicipessettling together across 3 dates showed similar trends of decreasinglipid index over time, suggesting that environmental conditionsmay influence co-occurring planktonic larvae similarly acrossspecies. This work highlights the need for further experimentsin the field on the effects of larval history on recruitmentsuccess in natural populations, and further studies to determinewhat factors influence larval attributes for planktonic larvaein the field.     

The genetic basis of altitudinal variation in the wood frog Rana sylvatica II. An experimental analysis of larval development

Summary The variation in larval developmental patterns in the wood frog, Rana sylvatica, along an elevation gradient of 1,000 m was experimentally studied. Larval populations at high elevation ponds had lower growth rates, developmental rates and were larger at all stages (including metamorphic climax) than larval populations developing in low elevation ponds. There was considerable variation among ponds within each elevation in both the length of the larval period and size at metamorphic climax. Reciprocal transplant experiments and controlled laboratory experiments revealed that most of the observed variation between high and low elevation populations could be explained by the effects of temperature induction during ontogeny. Significant genetic differences in growth rates and non-genetic maternal effects on developmental rates between larvae of mountain origin and lowland origin were also demonstrated. Selection in both environments has acted to minimize the prevailing environmental effect of pond temperature on developmental rates, but has accentuated the prevailing environmental effects on larval body size. As a consequence mountain larvae were capable of completing metamorphosis sooner and at a larger size in all environments than lowland larvae.     

Growth and development of Calanus chilensis nauplii reared under laboratory conditions: testing the effects of temperature and food resources

We assessed growth and development of naupliar stages of Calanus chilensis Brodsky 1959, under a combination of three temperatures and two food levels in laboratory conditions. Both food supply and temperature significantly affected naupliar growth and development. High food, measured as chlorophyll a (Chl a) concentration, was 40 μg l⁻¹, on average, and yielded temperature-dependent growth rates in the range of 0.13-0.17 day⁻¹. Low food was about 1.2 μg chlorophyll a l⁻¹ and retarded or arrested development and drastically reduced the growth rate to the range of 0.05-0.09 day⁻¹. To test whether these experimental results were consistent with field data, we used published information on temperature and chlorophyll a variability in northern Chile and developed a combined temperature/food-dependent model to diagnose naupliar growth in the field through a 2-year seasonal cycle including the 1997-1998 El Niño conditions. We concluded that in the upwelling region off northern Chile, C. chilensis might seldom encounter conditions of food shortage, as those applied in the laboratory. Thus, naupliar growth of this species may be primarily controlled by environmental temperature and this might also be the case for the dynamics of the entire population inhabiting the coastal upwelling zone.     

粟穗螟滞育的形成和解除与环境条件的关系

粟穗螟Manpava bipunctella Ragonot在川南地区为二化性兼性滞育的昆虫。光周期是诱发滞育的主导因素,在中位温度下,滞育与否主要取决于幼虫发育期间的每日光照时数。在2s℃恒温下,临界光周期为14小时38分。幼虫对光照刺激反应的敏感期为低龄期。 温度和食料效应只发生在每天14小时以上的长光照下,低温有抵销长光照抑制滞育的作用,高温影响不显著;取食玉米的幼虫滞育率比高粱的高,并随寄主生育阶段的发展而增高。该虫滞育解除必需每天14-15小时的长光照;不利于滞育发育和解除,适宜温度为10一25℃。本文最后讨论了该虫滞育形成和解除的特点对发生规律的作用及在测报上的意义。     

Embryonic and naupliar development of Eudiaptomus gracilis and Eudiaptomus graciloides at different temperatures: comments on individual variability

Eudiaptomus gracilis and Eudiaptomus graciloides are amongstthe most common calanoid copepods in Europe and co-occur inmany lakes. To understand their ecological dynamics, it is essentialto know their responses to environmental variation. The findingthat E. graciloides exhibits diapause in winter, whereas E.gracilis reproduces throughout the year indicates that the twospecies might differ in their temperature responses. We measuredembryonic and naupliar development times, clutch size (numberof eggs per sac), hatching percentage and body length of thefirst copepodid stage (CI) of both species under non-limitingfood conditions at different temperatures. Special attentionwas given to individual variability on development times andto the use of the gamma density function (GDF) for fitting theprobability of moulting. Results show that E. gracilis exhibitsjust slightly faster development times, lower individual variability,higher hatching percentage and larger clutches than E. graciloidesand that extreme temperatures affected E. gracilis less intenselythan E. graciloides. GDF was a good tool for estimating individualvariability in the different experiments.     

Relative tolerance of cirripede larval stages to acute thermal shock: A laboratory study

(1) Meroplankters drawn into once-through cooling circuits of coastal power plants are subjected to transient thermal stress. The effect of such acute thermal shock on the development of barnacle larvae was studied in the laboratory.

(2) The response of the barnacle larvae (naupliar and cyprid stages) to elevated temperature was dependent on exposure time and their stage of development.

(3) Among the stages tested, N-6 larvae showed maximum tolerance. Exposure to 37°C did not affect larval survival, but delayed development of N-2 larva to cypris by one day.

(4) Exposure at 40°C delayed, hastened or did not affect the development time of N-2 and N-4 larvae through cypris, depending on exposure time.

(5) Ten mins exposure at 43°C proved lethal to all larval stages with mortality ranging from 20 to 86%.

(6) Development success of the surviving larvae, measured in terms of cypris yield, showed no significant difference from controls, at temperatures below 40°C.

(7) Settlement activity was significantly affected in only those cyprid larvae which were exposed to 43°C for 10 min.

(8) Results of the present study indicate that thermal stress experienced in the once-through cooling system does not have significant impact on survival and development of the barnacle larvae at temperatures of 37–40°C.     

Control and Consequences of Alternative Developmental Modes in a Poecilogonous Polychaete

SYNOPSIS. The poecilogonous polychaete Streblospio benedicti(Webster) exhibits both planktotrophic and lecithotrophic modesof larval development. The alternative trophic modes are associatedwith differences in age and size at maturation, offspring number,size and energetic investment, larval planktonic period, morphologyand survivorship. This paper reviews a decade of research intothe control and consequences of the traits associated with planktotrophyand lecithotrophy in S. benedicti. The dominant control on reproductiveand developmental characters is genetic. Significant additivegenetic variance has been detected for egg diameter, fecundity,larval planktonic period and aspects of larval morphology. However,environmental factors such as temperature, food quality andphotoperiod, and intrinsic factors such as maternal age, exertconsiderable influence on non-trophic developmental traits (e.g.,offspring number, size and energy content). Demographic consequencesof development mode are reviewed for field and laboratory demesof S. benedicti dominated by individuals exhibiting either planktotrophyor lecithotrophy. Similar population size structure, fluctuationsin abundance, P: B ratios, and estimated population growth ratesare achieved through trade-offs between survivorship and fecundity. Development mode may best be viewed as a complex set of traitsthat are intimately linked developmentally and evolutionarilyto other aspects of an organism's life history. Greater insightinto the control and consequences of development mode shouldresult from further investigation of these linkages     

Growth, development and condition of Dendraster excentricus (Eschscholtz) larvae reared on natural and laboratory diets

Feeding invertebrate larvae may be food limited while developingin the ocean. If they are, then their time in the plankton isprolonged, which likely increases mortality. Food limitationcould be due to the quantity and/or quality of the food available.In an effort to answer how food type influences larval nutrition,we compared growth, development and lipid deposition for Dendrasterexcentricus larvae reared in natural seawater from two depths(1 and 20 m) and in filtered seawater on a monoculture laboratorydiet of 6 cells µL^–1 of the green alga Dunaliellatertiolecta (Butcher). Five days post-fertilization, larvaereared on the laboratory diet had developed to the latest stage,were the largest and had lipid deposits. Larvae reared on naturalsurface water were intermediate in size and developmental stage,and larvae reared in the water from 20 m depth were the smallestand developed the slowest. This trend continued at 8 days post-fertilizationwhen surface water diet larvae were similar in size to laboratorydiet larvae, but their juvenile rudiments were significantlysmaller. To assess food availability in each food treatment,we compared the concentration of chlorophyll (Chl) a, b andc in natural seawater from each depth and in D. tertiolectaculture in filtered seawater. Natural seawater collected fromthe surface had the highest concentration of Chl a and c, whereasChl b was not significantly different between treatments. IncreasedChl concentrations in the surface water are likely due to higherconcentrations of diatoms and dinoflagellates, which are typicallynot high-quality food items for echinoid larvae. Our resultssupport a hypothesis that echinoid larvae in the water columnmay be limited by food quality.     

The Nauplius Larva of Crustaceans: Functional Diversity and the Phylotypic Stage

SYNOPSIS. The crustacean nauplius larva is a development stagecharacterized by the presence of three pairs of head appendages.All crustaceans pass through the naupliar stage whether embryonicallyor as freeliving larvae. The nauplius is thought to be the phylotypicstage and represent a fundamental developmental constraint incrustaceans. However, free-living nauplii are primitive andI present evidence that this form is functionally plastic, e.g.,locomotory modes are diverse even in closely related species.I argue that this functional plasticity allowed the persistenceof nauplii in the early evolution of crustaceans and, as a consequence,naupliar development became a deep-seated feature of crustaceans.Thus, we see nauplii as phylotypic. This suggests that, in spiteof the presence of phylotypic stages in various phyla, phylotypyitself may not represent a similar, underlying developmentalconstraint in every case.     

Nauplii of the copepod, Calanus pacificus, off southern California in the El Nino winter-spring of 1992, and implications for larval fish

Female and naupliar Calanus were rarer in winter and springof 1992, an El Niño period, than in 1989. The ratio ofabundances, nauplius III (NIII) female^-1 (a composite surrogatefor reproduction and survival), did not differ between yearsand was not consistently correlated with concurrently measuredchlorophyll (a measure of food). Survival from egg to NIII wasnegatively correlated with biomass of macrozooplankton (a measureof predators). Survival from NIV to NVI was less variable thanthat of younger states; it was poorer in winter of 1992 thanin winter of 1989, but did not differ in median magnitude betweenthe two springs, although it was least variable spatially inspring of 1992. Survival of these feeding stages was not correlatedwith chlorophyll. The relative ranty of nauplii was equivalentto a reduction of 30% in this source of food for larval fish.