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.     

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.     

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.     

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.     

Precise tuning of barnacle leg length to coastal wave action

Both spatial and temporal variation in environmental conditions can favour intraspecific plasticity in animal form. But how precise is such environmental modulation? Individual Balanus glandula Darwin, a common northeastern Pacific barnacle, produce longer feeding legs in still water than in moving water. We report here that, on the west coast of Vancouver Island, Canada, the magnitude and the precision of this phenotypic variation is impressive. First, the feeding legs of barnacles from protected bays were nearly twice as long (for the same body mass) as those from open ocean shores. Second, leg length varied surprisingly precisely with wave exposure: the average maximum velocities of breaking waves recorded in situ explained 95.6-99.5% of the variation in average leg length observed over a threefold range of wave exposure. The decline in leg length with increasing wave action was less than predicted due to simple scaling, perhaps due to changes in leg shape or material properties. Nonetheless, the precision of this relationship reveals a remarkably close coupling between growth environment and adult form, and suggests that between-population differences in barnacle leg length may be used for estimating differences in average wave exposure easily and accurately in studies of coastal ecology.     

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.     

ADAPTIVE PLASTICITY OF THE PENIS IN A SIMULTANEOUS HERMAPHRODITE

Acorn barnacles are important model organisms for the study of sex allocation. They are sessile, nonselfing hermaphrodites that copulate with penises that have been suggested to be phenotypically plastic. On wave-exposed shores, Semibalanus balanoides develop penises with relatively greater diameter whereas in wave-protected sites they are thinner. A reciprocal transplant experiment between wave-exposed and protected sites tested whether these exposure-specific morphologies have adaptive value. Mating success was compared over a range of distances to compare the ability of barnacles to reach mates. Barnacles that grew in the wave-protected site and mated in the wave-protected site fertilized more broods at increasing distances than those transplanted to the wave-exposed site. For barnacles that developed in the wave-exposed site, there was no difference in the ability to fertilize neighbors between sites of differing exposure. This study demonstrates the adaptive value of plasticity in penis morphology. The results suggest a trade-off between development of a penis adapted to wave exposure and the ability to fertilize distant mates. Barnacles in different physical environments are limited by different factors, which may limit numbers of potential mates, constrain optimal sex allocation strategies and alter reproductive behavior.     

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.     

Normally occurring intersexuality and testosterone induced plasticity in the copulatory system of adult leopard geckos

The copulatory neuromuscular system of lizards is highly sexually dimorphic. Adult males possess bilateral penises called hemipenes, which are independently controlled by two muscles, the retractor penis magnus (RPM) and transversus penis (TPN). These structures are not obvious in adult females. However, in adult female leopard geckos (Eublepharis macularius), testosterone induces hemipene growth. We investigated whether these structures develop de novo in adulthood or are histologically present as rudimentary structures in the female leopard gecko. We also investigated the extent of sexual dimorphisms and plasticity in the associated neuromuscular components. To do this, we compared copulatory morphology (sizes of hemipenes, RPM and TPN muscle fibers, and associated motoneurons, as well as motoneuron and RPM fiber number) in adult females treated with testosterone, control females, and control males. All of the geckos possessed hemipenes, RPMs and TPNs, but these structures were indeed vestigial in control females. Testosterone induced striking increases in hemipene and copulatory muscle fiber size in females, but not to levels equivalent to control males. In parallel, males with increased levels of androgenic activity had larger hemipenes, suggesting naturally occurring steroid-induced plasticity. Copulatory motoneurons were not sexually dimorphic in size or number, and these measures did not respond to testosterone. The data demonstrate that the copulatory system of leopard geckos, in which gonadal sex is determined by egg incubation temperature, differs from that of many species (both reptilian and mammalian) with genotypic sex determination. Indeed, the system is remarkable in that adult females have normally occurring intersex characteristics and they exhibit substantial steroid-induced morphological plasticity in adulthood.     

Right-handed penises of the earwig Labidura riparia (Insecta, Dermaptera, Labiduridae): evolutionary relationships between structural and behavioral asymmetries

The number of penises vary in the insect suborder Forficulina (order Dermaptera; earwigs). Males of the families Diplatyidae, Pigidicranidae, Anisolabididae, Apachyidae, and Labiduridae have two penises (right and left), while those of the Spongipohridae, Chelisochidae, and Forficulidae have a single penis. The proposed phylogenetic relationships among these families suggest that the single‐penis families evolved from an ancestor possessing two penises. To date, examinations of double‐penis earwig species have found that only a single penis is used per single copulation. These diversities in structural and behavioral aspects of genitalia raises the following intriguing questions: How are the two penises used? Why did a penis degenerate in several earwig families, and which one was lost? To address these questions, structural and behavioral asymmetries were examined in detail for a representative species Labidura riparia (Labiduridae). Although there was no detectable morphological differentiation between the right and left penises, male L. riparia predominantly used the right one for insemination. This significant “right‐handedness” developed without any experience of mating and was also manifested in the resting postures of the two penises when not engaged in copulation. However, surgical ablation of the right penis did not influence the insemination capacity of males. In wild‐caught males, only about 10% were left‐handed; within this group, abnormalities were frequently observed in the right penis. These lines of evidence indicate that the left penis is merely a spare intromittent organ, which most L. riparia males are likely never to use. Additional observations of five species of single‐penis families revealed that the left penis degenerated in the common ancestor of this group. Considering the proposed sister relationship between the Labiduridae and the single‐penis families, it is possible that such behavioral asymmetries in penis' use, as observed in L. riparia, are parental to the evolutionary degeneration of the infrequently used left penis. J. Morphol., 2006. © 2006 Wiley‐Liss, Inc.     

Leaf traits and water relations of 12 evergreen species in Costa Rican wet and dry forests: patterns of intra-specific variation across forests and seasons

This study examined variation in leaf traits and water relations in 12 evergreen and semideciduous woody species that occur in both seasonal wet and dry forests in Costa Rica and compared intra-specific leaf–trait correlations to those found in inter-specific global studies. The following traits were measured in both forests across seasons for 2 years: leaf nitrogen (N), leaf carbon (C), specific leaf area (SLA), toughness, cuticle thickness, leaf thickness, and leaf lifespan (LLS). Leaf water potential (LWP) and water content (LWC) were measured as indices of plant available water. Canopy openness, soil moisture, and herbivory were also measured to compare environmental variation across sites. Although species contributed the greatest amount to variation in traits, season, forest, and their interaction had a large influence on patterns of intra-specific leaf–trait variation. Leaf traits that contributed most to variation across sites were C, LWP, leaf thickness, and SLA. Traits that contributed most to variation across seasons were leaf toughness, LWP, and LWC. Furthermore, leaf traits were more correlated (i.e., number and strength of correlations) in the dry than in the wet forest. In contrast to results from global literature syntheses, there was no correlation between LLS and N, or LLS and SLA. Both light and water availability vary seasonally and may be causing variation in a number of leaf traits, specifically those that relate to water relations and leaf economics. Strong seasonality may cause leaf–trait relationships at the local scale to differ from those documented in continental and global-scale studies.     

When dwarf males and hermaphrodites copulate: first record of mating behaviour in a dwarf male using the androdioecious barnacle <Emphasis Type="Italic">Scalpellum scalpellum</Emphasis> (Crustacea: Cirripedia: Thoracica)

Mating behaviour between a dwarf male and its hermaphrodite partner was observed for the first time in cirripedes using the androdioecious barnacle Scalpellum scalpellum. Mating between hermaphrodites was also observed. The dwarf males are located on the rim of the mantle cavity of the hermaphrodite partner. When mating, the male extends the penis, which is four times longer than its body. The penis first assumes a straight stance where it is waved around in a searching mode. Upon touching the cirri of the hermaphrodite, the penis and the cirri engage in prolonged contact during which hermaphrodite feeding is suspended. Thereafter the penis assumes a U-bend to reach into the brood chamber, where after the mantle valves are closed tightly around the penis. The nearly transparent penis is a tube of very thin cuticle, equipped with pairs of side branches but not containing any visible tissue. The penis enables the minute male, situated outside the brood chamber, to securely deposit sperm into its partner. Adjacently situated hermaphrodites interact socially in between feeding sessions by reorienting themselves on the peduncle to touch each other with their cirri. This can be followed by precopulatory behaviour, where one or both individuals extend the penis to touch their partner, leading again to actual copulation where the penis of one individual is inserted into the other. We discuss the results in the context of the diverse reproductive strategies found in cirripede barnacles.     

Predation Risk Reduces a Female Preference for Heterospecific Males in the Green Swordtail

The presence of a predator can result in the alteration, loss or reversal of a mating preference. Under predation risk, females often change their initial preference for conspicuous males, favouring less flashy males to reduce the risk of being detected by predators. Previous studies on predator‐induced plasticity in mate preferences have given females a choice between more and less conspicuous conspecific males. However, in species that naturally hybridize, it is also possible that females might choose an inconspicuous heterospecific male over a conspicuous conspecific male under predation risk. Our study addresses this question using the green swordtail (Xiphophorus helleri) and the southern platyfish (Xiphophorus maculatus), which are sympatric in the wild. We hypothesized that X. helleri females would prefer the sworded conspecific males in the absence of a predator but favour the less conspicuous, swordless, heterospecific males in the presence of a predator. Contrary to our expectation, females associated more with the heterospecific male than the conspecific male in the control (no predator) treatment, and they were non‐choosy in the predator treatment. This might reflect that females were attracted to the novel male phenotype when there was no risk of predation but became more neophobic after predator exposure. Regardless of the underlying mechanism, our results suggest that predation pressure may affect female preferences for conspecific versus heterospecific males. We also found striking within‐population, between‐individual variation in behavioural plasticity: females differed in the strength and direction of their preferences, as well as in the extent to which they altered their preferences in response to changes in perceived predation risk. Such variation in female preferences for heterospecific males could potentially lead to temporal and spatial variation in hybridization rates in the wild.     

Continued functioning of the feeding apparatus during moulting of Boophilus microplus as an adaptation of one-host ticks

Nymphs of the 1-host cattle tick Boophilus microplus remain attached to the host during moulting, but this process is not uniform throughout the tick tissues. The muscles of the pharynx and salivarium remain attached to the cuticle and are functional while the cuticle of the legs has already separated from the underlying epidermis and muscle. The nymphs continue to feed for 2 days after the moulting process in the legs has begun, and they more than double their weight in this time. Mouth-part primordia of the adults develop while the nymphs are still feeding. These adaptations could be an advantage of a 1-host feeding strategy, as they decrease the non-feeding development time spent on the host. In the 3-host tick Haemaphysalis longicornis, which moults off the host, the pharynx, salivarium and legs all begin the moulting process at the same time.     

淮北相山恢复演替群落优势树种叶片的生态解剖

对淮北相山混交林5个优势种叶片的生态解剖学观察表明,其叶片结构具有一定的旱生特征:表皮具发达的表皮毛或角质层,全栅等面叶或具发达的栅栏组织,维管组织发达。牡荆(Vitex negundo var. cannabifolia)和酸枣(Ziziphus jujuba var. spinosa)作为两个广布优势树种,叶片结构表现出很大的可塑性:1)同一群落环境(混交林)中,叶片结构随着季节的变化表现出发育可塑性(5月初的叶片比9月中旬更具有阳生叶的特点);2)不同恢复演替阶段的群落中,叶片结构随着群落环境的变化表现出环境可塑性,其变化趋势为:灌草丛(旱生/阳生)-灌丛(旱生/阳生)-落叶疏林(中生/阳生)-人工侧柏(Platycladus orientalis)林(中生/阴生)。这种可塑性既是植物适应其异质生境的一种重要机制,同时又是不同群落环境的反映。非参数相关分析表明,牡荆和酸枣的叶片结构受多个生态因子综合影响,其中水分和风速是影响叶片结构的主导因子。叶片的上表皮角质层厚度、气孔器密度、栅栏组织厚度、叶片厚度、木质部厚度、韧皮部厚度、维管束厚度等性状均与土壤含水量和空气相对湿度呈显著负相关,与风速呈显著正相关。     

Host location by larvae of a parasitic barnacle: larval chemotaxis and plume tracking in flow

Numerous studies describe stimulation and/or enhancement oflarval settlement by distance chemoreception in response tochemical factors emitted by conspecific adults, host and preyspecies and microbial films. However, active upstream trackingof odor plumes, needed in order to locate specific, spatiallylimited settlement sites, has thus far received little scientificattention. This study examines host location in flow and stillwater by larvae of the parasitic barnacle Heterosaccus dollfusi,which inhabits the brachyuran crab Charybdis longicollis. Experimentsincluded analysis of larval motion patterns under four conditions:still water, in flow, in still water with waterborne host metabolitesand in flow with host metabolites. Our results show that H.dollfusi larvae are capable of actively and effectively locatingtheir host in still water and in flow, using chemotaxis andrheotaxis and modifying their swimming pattern, direction, velocity,determination and turning rate to accommodate efficient navigationin changing environmental conditions.     

Post‐eclosion temperature effects on insect cuticular hydrocarbon profiles

The insect cuticle is the interface between internal homeostasis and the often harsh external environment. Cuticular hydrocarbons (CHCs) are key constituents of this hard cuticle and are associated with a variety of functions including stress response and communication. CHC production and deposition on the insect cuticle vary among natural populations and are affected by developmental temperature; however, little is known about CHC plasticity in response to the environment experienced following eclosion, during which time the insect cuticle undergoes several crucial changes. We targeted this crucial to important phase and studied post‐eclosion temperature effects on CHC profiles in two natural populations of Drosophila melanogaster. A forty‐eight hour post‐eclosion exposure to three different temperatures (18, 25, and 30°C) significantly affected CHCs in both ancestral African and more recently derived North American populations of D. melanogaster. A clear shift from shorter to longer CHCs chain length was observed with increasing temperature, and the effects of post‐eclosion temperature varied across populations and between sexes. The quantitative differences in CHCs were associated with variation in desiccation tolerance among populations. Surprisingly, we did not detect any significant differences in water loss rate between African and North American populations. Overall, our results demonstrate strong genetic and plasticity effects in CHC profiles in response to environmental temperatures experienced at the adult stage as well as associations with desiccation tolerance, which is crucial in understanding holometabolan responses to stress.     

Exoskeleton anchoring to tendon cells and muscles in molting isopod crustaceans

Specialized mechanical connection between exoskeleton and underlying muscles in arthropods is a complex network of interconnected matrix constituents, junctions and associated cytoskeletal elements, which provides prominent mechanical attachment of the epidermis to the cuticle and transmits muscle tensions to the exoskeleton. This linkage involves anchoring of the complex extracellular matrix composing the cuticle to the apical membrane of tendon cells and linking of tendon cells to muscles basally. The ultrastructural arhitecture of these attachment complexes during molting is an important issue in relation to integument integrity maintenance in the course of cuticle replacement and in relation to movement ability. The aim of this work was to determine the ultrastructural organization of exoskeleton - muscles attachment complexes in the molting terrestrial isopod crustaceans, in the stage when integumental epithelium is covered by both, the newly forming cuticle and the old detached cuticle. We show that the old exoskeleton is extensively mechanically connected to the underlying epithelium in the regions of muscle attachment sites by massive arrays of fibers in adult premolt Ligia italica and in prehatching embryos and premolt marsupial mancas of Porcellio scaber. Fibers expand from the tendon cells, traverse the new cuticle and ecdysal space and protrude into the distal layers of the detached cuticle. They likely serve as final anchoring sites before exuviation and may be involved in animal movements in this stage. Tendon cells in the prehatching embryo and in marsupial mancas display a substantial apicobasally oriented transcellular arrays of microtubules, evidently engaged in myotendinous junctions and in apical anchoring of the cuticular matrix. The structural framework of musculoskeletal linkage is basically established in described intramarsupial developmental stages, suggesting its involvement in animal motility within the marsupium.