Cuticle and muscle variation underlying phenotypic plasticity in barnacle feeding leg and penis form

Many aspects of barnacle body form are known to be developmentally plastic. Perhaps the most striking examples of such plasticity occur in their feeding legs and unusually long penises, the sizes and shapes of which can change dramatically and adaptively with changes in conspecific density and local water flow conditions. However, whether variation in overall appendage form is mirrored by structural responses in cuticle and muscle is not known. In order to determine how structural variation underlies phenotypic plasticity in barnacle appendages, we examined barnacles occurring at low and high population densities from one wave‐protected and one wave‐exposed site. We used histological sectioning and fluorescence microscopy of feeding legs and penises to compare cuticle thickness, muscle thickness, and muscle organization, and artificial penis inflation to compare penis extensibility. We observed striking differences in cuticle thickness, muscle thickness, and muscle organization between sites that differed in water velocity, but we found no clear differences associated with variation in conspecific density. Penis extensibility also did not differ consistently between sites. These results are consistent with an adaptive explanation for much of the remarkable and complex variation in barnacle feeding leg and penis morphology among sites that differ in water velocity.     

Feeding in flow extremes: dependence of cirrus form on wave-exposure in four barnacle species

Wave-exposure influences the form of many organisms. Curiously, the impact of flow extremes on feeding structures has received little attention. Barnacles extend feather-like legs to feed, and prior work revealed a highly precise association between leg length and water velocity in one species. To assess the generality of this flow-dependence, we quantified variation in four leg traits (ramus length, ramus diameter, seta length, and intersetal spacing) in four intertidal barnacles (Balanus glandula, Chthamalus dalli, Semibalanus cariosus, Pollicipes polymerus) over a wave-exposure gradient in the North-Eastern Pacific. All species exhibited a negative allometric relation between leg length and body mass. Proportionally longer feeding legs may permit smaller barnacles to avoid lower flow and particle flux associated with boundary layers. Although coefficients of allometry did not vary with wave-exposure, form differences among wave-exposures were substantial. Depending on the species, acorn barnacles of the same size from protected shores had feeding legs that were 37-80% longer and 18-25% thinner, and setae that were 36-50% longer and up to 25% more closely spaced, than those from exposed shores. Differences were less pronounced for the gooseneck barnacle, P. polymerus. Moreover, in situ water velocity explained an impressive percentage of overall leg-length variation: 92% in B. glandula, 67% in C. dalli, 91% in S. cariosus, and 92% in P. polymerus. Clearly, both size and shape of barnacle feeding legs respond to local flow conditions. This response appears widespread--across two orders of thoracican barnacles, Pedunculata and Sessilia, and two superfamilies of acorn barnacles (Balanoidea and Chthamaloidea)--and likely adaptive. Longer rami and setae would yield a larger feeding area in low flow, whereas shorter, stouter rami with shorter setae would be less vulnerable to damage in high flow. Finally, the proportionally most variable species was abundant in the widest range of habitats, suggesting that increased plasticity may permit a wider niche breadth.     

Dramatic phenotypic plasticity in barnacle legs (Balanus glandula Darwin): magnitude,age dependence,and speed of response

Abstract.— The precise dependence of barnacle leg form on flow suggests the wave-swept environment imposes strong selection on suspension feeding limbs. I conducted three experiments to determine the mechanism, age dependence, and response time of cirrus variation in the acorn barnacle Balanus glandula . (1) To test whether cirrus variation arises via genetic or environmental mechanisms, I transplanted juvenile barnacles from one wave-exposed and one protected population into high and low flow conditions. Both populations exhibited similar abilities to modify cirri in response to experimental velocities: transplanted barnacles grew legs up to 84% longer in low flow. A small (up to 24%), but significant difference between source populations suggested slight genetic divergence in leg form. (2) Because flow is heterogeneous over space and time, I tested whether cirrus plasticity was limited to juveniles by transplanting both juveniles and adults from exposed and protected shores into quiet water. Remarkably, both juveniles and adults from the wave-exposed population produced legs over 100% longer than the original population, whereas protected barnacles remained unchanged. (3) A third transplant of adults into quiet water demonstrated that wave-exposed B. glandula modified cirrus form very quickly-within 18 days, or one to two molts. Results from these experiments suggest that variation in cirrus form is largely environmentally induced, but genetic differences may account for some variation observed among field populations; spatial and temporal flow heterogeneity appear to have selected for extreme flexibility of feeding form throughout a barnacle's life; and flow heterogeneity in the wave-swept environment appears to have selected for rapid ecophenotypic responses in the form of feeding structures.     

Effects of tidal height and wave exposure on cirrus and penis morphology of the acorn barnacle Tetraclita stalactifera

Exposure to wave action and other environmental factors can alter the morphology of intertidal barnacles. We tested several hypotheses on the causes of morphological variation in the cirri and penises of the barnacle Tetraclita stalactifera at sites differing in wave exposure, at different heights in the intertidal zone, and at different levels of population density. Unlike many other acorn barnacle species, cirrus and penis characteristics did not correspond to differences in wave exposure or crowding. However, barnacles from higher tidal elevations had thicker cirri and thicker penises than those from lower elevations. Because of reduced time submerged at higher elevations, increased thickness may be a means of compensating for reduced feeding and mating opportunity by allowing for continued feeding and mating attempts during periods of greater wave action. Our observations of differences in cirrus and penis morphology suggest that phenotypic plasticity in penis and cirrus characteristics are adaptations shared by the species T. stalactifera and other acorn barnacles, but that T. stalactifera responds differently to environmental stimuli than do other species.     

Limits to phenotypic plasticity: flow effects on barnacle feeding appendages

Phenotypic plasticity, the capacity of a given genotype to produce differing morphologies in response to the environment, is widespread among marine organisms (1). For example, acorn barnacles feed by extending specialized appendages (the cirral legs) into flow, and the length of the cirri is plastic: the higher the velocity, the shorter the feeding legs (2,3). However, this effect has been explored only for flows less than 4.6 m/s, slow compared to typical flows measured at sites on wave-exposed shores. What happens at faster speeds? Leg lengths of Balanus glandula Darwin, 1854, an acorn barnacle, were measured at 15 sites in Monterey, California, across flows ranging from 0.5 to 14.0 m/s. Similar to previous findings, a plastic response in leg length was noted for the four sites with water velocities less than 3 m/s. However, no plastic response was present at the 11 sites exposed to faster velocities, despite a 4-fold variation in speed. We conclude that the velocity at which the plastic response occurs has an upper limit of 2-4 m/s, a velocity commonly exceeded within the typical habitat of this species.     

Community-wide character displacement in barnacles: a new perspective for past observations

We tested for community‐wide character displacement of feeding leg length and shell morphology in two barnacle communities on the west coast of North America (southern California, USA and Vancouver Island, Canada). Neither community exhibited even displacement in shell morphology. Both barnacle communities, however, exhibited remarkably evenly displaced feeding leg length, despite large differences in geography and species composition (between the orders Pedunculata and Sessilia). Previous experiments suggest that this pattern results from competition, although the competitive mechanism remains unknown. Displacement of leg length may reflect dietary specialization, spatial competition, or both. In some cases the results from two null models differed, illustrating the importance of employing a null model that considers mean and variance, rather than character means alone. Overall, the observed pattern of character displacement provides a new perspective for re‐examining the complex relationship between morphology and interspecific competition among intertidal barnacles.     

Modular phenotypic plasticity: divergent responses of barnacle penis and feeding leg form to variation in density and wave-exposure

Traits can evolve both in response to direct selection and in response to indirect selection on other linked traits. Although the evolutionary significance of coupled traits (e.g., through shared components of developmental pathways, or through competition for shared developmental resources) is now well accepted, we know comparatively little about how developmental coupling may restrict the independent responses of two or more phenotypically plastic traits in response to conflicting environmental cues. Such studies are important because coupled development, if present, could act as an important limit to the evolution of functionally independent plasticity in multiple traits. I tested whether developmental coupling can restrict the direction of plastic responses by studying how penis form and leg form--both highly plastic traits of barnacles--varied in response to differences in conspecific density and water velocity. Penis length and leg length in Balanus glandula varied in parallel with variation in wave-exposure but varied in opposite directions with variation in conspecific density. This study represents one of the rare tests of developmental coupling between multiple (demonstrably adaptive) plastic traits: Barnacle legs and penises appear to exhibit modular development that can respond concurrently--yet in independent directions--to conflicting environmental cues.     

Latitudinal variation and coevolutionary diversification of sexually dimorphic traits in the false blister beetle Oedemera sexualis

Sexual traits are subject to evolutionary forces that maximize reproductive benefits and minimize survival costs, both of which can depend on environmental conditions. Latitude explains substantial variation in environmental conditions. However, little is known about the relationship between sexual trait variation and latitude, although body size often correlates with latitude. We examined latitudinal variation in male and female sexual traits in 22 populations of the false blister beetle Oedemera sexualis in the Japanese Archipelago. Males possess massive hind legs that function as a female‐grasping apparatus, while females possess slender hind legs that are used to dislodge mounting males. Morphometric analyses revealed that male and female body size (elytron length), length and width of the hind femur and tibia, and allometric slopes of these four hind leg dimensions differed significantly among populations. Of these, three traits showed latitudinal variation, namely, male hind femur was stouter; female hind tibia was slenderer, and female body was smaller at lower latitudes than at higher latitudes. Hind leg sizes and shapes, as measured by principal component analysis of these four hind leg dimensions in each sex, covaried significantly between sexes, suggesting coevolutionary diversification in sexual traits. Covariation between sexes was weaker when variation in these traits with latitude was removed. These results suggest that coevolutionary diversification between male and female sexual traits is mediated by environmental conditions that vary with latitude.     

Precisely proportioned: intertidal barnacles alter penis form to suit coastal wave action

For their size, barnacles possess the longest penis of any animal (up to eight times their body length). However, as one of few sessile animals to copulate, they face a trade-off between reaching more mates and controlling ever-longer penises in turbulent flow. We observed that penises of an intertidal barnacle (Balanus glandula) from wave-exposed shores were shorter than, stouter than, and more than twice as massive for their length as, those from nearby protected bays. In addition, penis shape variation was tightly correlated with maximum velocity of breaking waves, and, on all shores, larger barnacles had disproportionately stouter penises. Finally, field experiments confirmed that most of this variation was due to phenotypic plasticity: barnacles transplanted to a wave-exposed outer coast produced dramatically shorter and wider penises than counterparts moved to a protected harbour. Owing to the probable trade-off between penis length and ability to function in flow, and owing to the ever-changing wave conditions on rocky shores, intertidal barnacles appear to have acquired the capacity to change the size and shape of their penises to suit local hydrodynamic conditions. This dramatic plasticity in genital form is a valuable reminder that factors other than the usual drivers of genital diversification--female choice, sexual conflict and male-male competition--can influence genital form.     

Sexual selection,phenotypic variation,and allometry in genitalic and non‐genitalic traits in the sexually size‐dimorphic stick insect Micrarchus hystriculeus

The mobility hypothesis could explain the evolution of female‐biased size dimorphism if males with a smaller body size and longer legs have an advantage in scramble competition for mates. This hypothesis is tested by performing a selection analysis in the wild on Micrarchus hystriculeus (Westwood) (Phasmatodea), a sexually size dimorphic stick insect endemic to New Zealand. This analysis examined the form and strength of sexual selection on body size, leg lengths (front, mid and hind), and clasper size (a genitalic trait), and also quantified the degree of phenotypic variation and the allometric scaling pattern of these traits. By contrast to the mobility hypothesis, three lines of evidence were found to support significant stabilizing sexual selection on male hind leg length: a significant nonlinear selection gradient, negative static allometry, and a low degree of phenotypic variation. Hind leg length might be under stabilizing selection in males if having average‐sized legs facilitates female mounting or improves a male's ability to achieve the appropriate copulation position. As predicted, a negative allometric scaling pattern and low phenotypic variation of clasper size is suggestive of stabilizing selection and supports the ‘one‐size‐fits‐all’ hypothesis. Opposite to males, the mid and hind leg lengths of females showed positive static allometry. Relatively longer mid and hind leg lengths in larger females might benefit individuals via the better support of their larger abdomens. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 471–484.     

Leg length and temperature determine the use of unipedal roosting in birds

The function of standing on one leg in birds has long been attributed to reducing heat loss from the unfeathered legs to the external environment. Whilst a handful of single‐species studies correlate the use of the behaviour with ambient temperature, the degree to which it is used across taxa is unknown. Given that leg‐length varies between species, the length of the leg (relative to body size) may mediate the use of this thermoregulatory behaviour, such that birds with longer legs should roost on one leg more than those with relatively shorter legs at any given ambient temperature. We tested this prediction through field observations and comparative analyses of nine shorebird species, with varying tarsi length relative to body size. Six of the nine species examined used unipedal standing more as temperatures decrease, indicating its role as a heat conservation behaviour. We also found that species with relatively longer legs roosted on one leg more frequently across a wide range of temperatures. Species with shorter leg lengths likely rely less on this posture to insulate the relatively smaller surface area of the legs. Our findings showed that the long accepted notion that birds stand on one leg more at colder temperatures holds, and that species with smaller relative leg length were less reliant on this behaviour to minimise heat loss from these bare appendages.     

The use of biocultural data in interpreting sex differences in body proportions among rural Amazonians

Variation in height and body proportions is relatively well-understood at the inter-population level, but less is known about intra-population variation. This study explores intra-population variation in body proportions among 172 (88 female; 84 male) adult rural Amazonians. We test the hypotheses that: (1) stunting is associated with changes in proportions and fatness; (2) the sexes express different proportions in response to similar environmental stress; and (3) female growth is negatively affected by the costs of reproduction. We examined height, sitting height, and total leg length in subsamples based on sex and nutritional status (stunted/nonstunted) in relation to biocultural factors including access to food and healthcare and female reproductive history parameters. Differences in proportions were examined using the Quick-Test (Tsutakawa and Hewett: Biometrics 33 (1977) 215-219); correlation analyses were used to detect associations between anthropometric data and body fatness, and female reproductive history parameters. We found significantly higher rates of stunting among females (X(2) = 5.31; P = 0.02; RR = 1.4). Stunted individuals exhibited relatively shorter legs than nonstunted individuals (P = 0.02), although this was not found in within-sex analyses. A significant negative correlation was found between leg length index and fatness (P < 0.01). Lastly, females exhibited relatively shorter legs than males (P = 0.0003) and, among females, height and leg length were significantly positively correlated with age-at-first-birth (P < 0.02) suggesting that adolescent pregnancy may negatively affect growth in this population. Our findings provide insights for the study of intra-population variation in body proportions and highlight the importance of biocultural data in interpreting the pattern of variation observed in living and past populations.     

The size–grain hypothesis: do macroarthropods see a fractal world?

Abstract.  1. In the size–grain hypothesis (a) long legs allow walking organisms to step over gaps and pores in substrate but prohibit them from entering those gaps; (b) the world is more rugose for small organisms; and (c) the relative cost of long legs increases as organisms grow smaller. The hypothesis predicts a positive allometry of leg length ( = mass ^b where b > 0.33 of isometry), a pattern that robustly holds for ants.
2. Toward testing for leg length allometries in other taxa, arthropods were extracted from the Panama leaf litter and measured. Three common taxa (spiders, diplopods, Coleoptera) yielded b s that exceeded 0.33 while three others (Acarina, Pseudoscorpiones, and Collembola) did not. The exponent b tended to increase ( P = 0.06, n = 7) with an arthropod taxon's average body mass.
3. Since leg length in cursorial organisms tends toward isometry in very small and very large taxa (i.e. mammals) this suggests that the size–grain hypothesis may best apply at a transition zone of intermediate body mass: the macroarthropods.
4. Body length was a robust predictor of mass in all groups despite variation in shape.     

Leg kinematics and muscle activity during treadmill running in the cockroach, Blaberus discoidalis : I. Slow running

We have combined high-speed video motion analysis of leg movements with electromyogram (EMG) recordings from leg muscles in cockroaches running on a treadmill. The mesothoracic (T2) and metathoracic (T3) legs have different kinematics. While in each leg the coxa-femur (CF) joint moves in unison with the femur-tibia (FT) joint, the relative joint excursions differ between T2 and T3 legs. In T3 legs, the two joints move through approximately the same excursion. In T2 legs, the FT joint moves through a narrower range of angles than the CF joint. In spite of these differences in motion, no differences between the T2 and T3 legs were seen in timing or qualitative patterns of depressor coxa and extensor tibia activity. The average firing frequencies of slow depressor coxa (Ds) and slow extensor tibia (SETi) motor neurons are directly proportional to the average angular velocity of their joints during stance. The average Ds and SETi firing frequency appears to be modulated on a cycle-by-cycle basis to control running speed and orientation. In contrast, while the frequency variations within Ds and SETi bursts were consistent across cycles, the variations within each burst did not parallel variations in the velocity of the relevant joints. Accepted: 24 May 1997     

Variation in penis morphology and mating ability in the acorn barnacle, Semibalanus balanoides

I examined variation in penis morphology of the acorn barnacle, Semibalanus balanoides, at different aggregation densities and at different levels of wave exposure. Barnacles in sparse, un-crowded aggregations had significantly longer penises than those from densely crowded groups, suggesting a response to increase the chance of reaching distant mating partners. Barnacles exposed to oceanic waves had penises with significantly greater basal diameter, possibly to strengthen the penis and retain function in turbulent conditions. I compared the percentage of individual barnacles with fertilized broods over a range of distances to their nearest possible mate in sites exposed to or protected from waves. As neighbor distance increased, the proportion of individuals with fertilized egg masses decreased in both wave-exposed and protected sites. However, at greater mate distances in the wave exposed sites, the proportion of individuals with fertilized eggs was significantly lower than the proportion in protected sites, indicating that exposure to waves hinders mating with neighbors at increasing distances. These results suggest that the intensity of mate competition may differ for barnacles between environments with different levels of wave exposure. These differences in male ability are predicted to alter relative sex allocation to male and female function.     

Phenotypic variation for adhesive tenacity in the barnacle Balanus amphitrite

Silicone fouling-release coatings represent a non-toxic alternative to biocide-containing ship hull paints. These coatings allow fouling organisms to attach to the hull surface, but prevent firm adhesion. Adhesive tenacity to fouling-release materials varies both among and within species. We quantified broad-sense genetic and environmental sources of intraspecific variation in tenacity to two silicone substrata, for the barnacle Balanus amphitrite. For both materials tenacity varied over an order of magnitude; however, the partitioning of this variation differed between the substrata. For International Veridian, a commercially-available fouling-release coating, removal stress varied significantly among maternal families and replicate barnacle cultures. Variation among the maternal families was associated with previously observed differences among these families in the condition of the adhesive plaque. Additional experiments suggested that variation among the replicate cultures arose from heterogeneity between replicate coatings in properties that affect tenacity. We could not attribute variation in removal stress for Dow Corning Silastic T-2, a silicone rubber used for mold-making, to any of the genetic or environmental sources tested. Instead, variation may have been due to measurement error or heterogeneity within replicate coatings in properties affecting tenacity. Differences among maternal families in removal stress may stem from variation in the interaction between the adhesive and the substratum, or in the viscoelastic properties of the adhesive plaque.     

Regulation of sex-specific feeding behavior in fiddler crabs: physiological properties of chemoreceptor neurons in claws and legs of males and females

This study examined properties of chemoreceptor neurons in the claws and legs of the fiddler crabs Uca pugilator and U. pugnax. The primary goal was to establish the neural basis of previously observed greater female sensitivity to feeding stimulants, and secondarily to compare physiological properties of chemoreceptor neurons in these semi-terrestrial crustaceans with those of fully aquatic forms. Sensitivity of chemoreceptor neurons in claws and legs is sex-specific; individual neurons of females respond to lower stimulus concentrations than male chemoreceptor neurons, and equivalent concentrations elicit greater spiking in female vs male chemoreceptor neurons. Thus, the population of chemoreceptor neurons in females expresses lower thresholds and greater average sensitivity than in males. Greater sensitivity of claw neurons explains observations indicating that females continue to feed at food levels too low to stimulate males. Sensitivity differences in leg neurons of males vs females have no clear behavioral correlate, but suggest that females can orient to more dilute stimuli than males. Chemoreceptor neurons of fiddler crabs have low sensitivities and slow rates of adaptation compared to other crustaceans. Also, neurons in claws adapt less slowly than neurons in legs, which may reflect subtle differences in the chemical stimulus environment experienced by claws vs legs.     

不同寄主上桃粉大尾蚜的取食偏好及形态变异研究

【目的】桃粉大尾蚜Hyalopterus pruni Geoffroy是一种常见的农业害虫,分布广泛。本文对采自上海地区粘核毛桃Amygdalus persica L.var.scleropersica(Reich.)Yüet Lu、紫叶李Prunus cerasifera Ehrhar f.atropurpurea(Jacq.)Rehd.和芦苇Phragmites australis(Cav.)Trin.ex Steud.3种植物上桃粉大尾蚜的取食偏好和形态变异进行了研究。【方法】通过叶碟法观测桃粉大尾蚜对3种寄主叶片的取食偏好,同时测量体长、体宽、触角各节长、喙末端长和宽、各足节长等30个形态指标,基于对形态数据的统计分析,包括主成分分析、聚类分析和判别分析,研究不同寄主植物上桃粉大尾蚜的形态变异。【结果】饲以3种寄主植物叶片时,来自粘核毛桃和芦苇上的桃粉大尾蚜对各寄主叶片的总体喜食程度依次为芦苇>粘核毛桃>紫叶李,来源于紫叶李上的个体对3种叶片的喜食程度为芦苇>粘核毛桃=紫叶李;形态数据分析发现粘核毛桃和紫叶李上的桃粉大尾蚜各指标间均无显著差异(P>0.05),但二者与芦苇上的个体在触角节Ⅱ、触角末节鞭部长、喙末端长和中足胫节的长度间差异显著(P<0.05),紫叶李与芦苇上的个体前足跗节Ⅰ长这一指标差异显著(P<0.05),此外,主成分分析筛选的体长、头宽、触角各节和各足长度等特征构成的前四个主成分对总体方差的累计贡献率达到66.206%,其中贡献率较高的特征为触角和各足节长度,系统聚类和典型判别分析的结果显示采自芦苇上的桃粉大尾蚜区别于粘核毛桃和紫叶李上的,归为一类,同为蔷薇科植物的紫叶李和粘核毛桃上的桃粉大尾蚜克隆有小部分重叠。【结论】禾本科植物上的桃粉大尾蚜种群形态特征与蔷薇科植物上的相比,触角节Ⅱ和末节鞭部、喙末端长、中足胫节的长度存在一定的分化,初步推测造成桃粉大尾蚜形态分化的原因主要为寄主植物营养成分及其表面特征,其种内变异的具体机制仍需进一步探索。     

Sexual dimorphism in leg length among orb-weaving spiders: a possible role for sexual cannibalism

The degree and direction of sexual dimorphism across different species is commonly attributed to differences in the selection pressures acting on males and females. The extent of these differences is especially apparent in species that practise sexual cannibalism, where the female attempts to capture and eat a courting male. Here, we investigate the relationship between sexual dimorphism in size and leg length, sexual cannibalism and courtship behaviour in three taxonomic groups of orb-weaving spiders, using morphological data from 249 species in 36 genera. Females are larger than males in all three taxonomic groups, and males have relatively longer legs than females in both the Araneinae and Tetragnathidae. Across genera within each taxonomic group, male body size is positively correlated with both female body size and male leg length, and female body size is positively correlated with female leg length. Sexual size dimorphism is negatively correlated with relative male leg length within the Araneinae, but not within either the Tetragnathidae or the Gasteracanthinae. There was no negative correlation between sexual size dimorphism and relative female leg length in any taxonomic group. We argue that the relationship between sexual size dimorphism and relative male leg length within the Araneinae may be the result of selection imposed by sexual cannibalism by females.     

Stance leg control: variation of leg parameters supports stable hopping

The spring-loaded inverted pendulum describes the planar center-of-mass dynamics of legged locomotion. This model features linear springs with constant parameters as legs. In biological systems, however, spring-like properties of limbs can change over time. Therefore, in this study, it is asked how variation of spring parameters during ground contact would affect the dynamics of the spring-mass model. Neglecting damping initially, it is found that decreasing stiffness and increasing rest length of the leg during a stance phase are required for orbitally stable hopping. With damping, stable hopping is found for a larger region of rest-length rates and stiffness rates. Here, also increasing stiffness and decreasing rest length can result in stable hopping. Within the predicted range of leg parameter variations for stable hopping, there is no need for precise parameter tuning. Since hopping gaits form a subset of the running gaits (with vanishing horizontal velocity), these results may help to improve leg design in robots and prostheses.