Bamfield Marine Sciences Centre

Because of its simplicity, the binary-switch nature of left-right asymmetry permits meaningful comparisons among many different organisms. Phylogenetic analyses of asymmetry variation, inheritance, and molecular mechanisms reveal unexpected insights into how development evolves. First, directional asymmetry, an evolutionary novelty, arose from nonheritable origins almost as often as from mutations, implying that genetic assimilation ("phenotype precedes genotype") is a common mode of evolution. Second, the molecular pathway directing hearts leftward-the nodal cascade-varies considerably among vertebrates (homology of form does not require homology of development) and was possibly co-opted from a preexisting asymmetrical chordate organ system. Finally, declining frequencies of spontaneous asymmetry reversal throughout vertebrate evolution suggest that heart development has become more canalized.

▪ Abstract Selective reporting—e.g., the preferential publication of results that are statistically significant, or consistent with theory or expectation—presents a challenge to meta-analysis and seriously undermines the quest for generalizations. Funnel graphs (scatterplots of effect size vs. sample size) help reveal the extent of selective reporting. They also allow the strength of biological effects to be judged easily, and they reaffirm the value of graphical presentations of data over statistical summaries. Funnel graphs of published results, including: (a) sex-ratio variation in birds, (b) field estimates of heritabilities, and (c) relations between fluctuating asymmetry and individual attractiveness or fitness, suggest selective reporting is widespread and raise doubts about the true magnitude of these phenomena. Quasireplication—the “replication” of previous studies using different species or systems—has almost completely supplanted replicative research in ecology and evolution. Without incentives for formal replicative studies, which could come from changes to editorial policies, graduate training programs, and research funding priorities, the contract of error will continue to thwart attempts at robust generalizations. “For as knowledges are now delivered, there is a kind of contract of error between the deliverer and the receiver: for he that delivereth knowledge desireth to deliver it in such a form as may be best believed, and not as may be best examined; and he that receiveth knowledge desireth rather present satisfaction than expectant inquiry; and so rather not to doubt than not to err: glory making the author not to lay open his weakness, and sloth making the disciple not to know his strength.” The Advancement of Learning, Francis Bacon, 1605 ( 8 :170–171)

Individuals of the morphologically variable, rocky intertidal gastropod Thais (or Nucella) lamellosa developed larger apertural teeth when held in the presence of the predatory crab Cancer productus than when held in its absence, regardless of whether snails were fed or not. In addition, among fed snails larger apertural teeth were produced in the presence of crabs fed conspecific snails than in the presence of crabs fed frozen fish. Because all snails were held in containers through which water flowed from physically separated aquaria holding the crabs, these results indicate that water-soluble chemical cues released by this predatory crab and by damaged conspecifics induced T. lamellosa to improve the defense effectiveness of their shells. Finally, when allowed access to food, snails exposed to these stimuli ate fewer barnacles and grew less than those in the controls.

The ability of an organism to acquire O(2) from its environment is key to survival and can play an important role in dictating a species' ecological distribution. This study is the first, to our knowledge, to show a tight, phylogenetically independent correlation between hypoxia tolerance, traits involved in dictating O(2) extraction capacity and the distribution of a group of closely related fish species, sculpins from the family Cottidae, along the nearshore marine environment. Sculpins with higher hypoxia tolerance, measured as low critical O(2) tensions (P(crit)), inhabit the O2 variable intertidal zones, while species with lower hypoxia tolerance inhabit the more O(2) stable subtidal zone or freshwater. Hypoxia tolerance is phylogenetically independently associated with an enhanced O(2) extraction capacity, with three principal components accounting for 75 per cent of the variation in P(crit): routine O(2) consumption rate; mass-specific gill surface area; and whole blood haemoglobin (Hb)- O(2)-binding affinity (P(50)). Variation in whole blood Hb-O(2)P(50) is strongly correlated with the intrinsic O(2)-binding properties of the purified Hb while the differences in the concentration of the allosteric Hb modulators, ATP and GTP, provide a Hb system with substantial plasticity for survival in a highly O(2) variable environment.

Every year numerous ecological, biochemical, and physiological studies are performed using members of the order Laminariales. Despite the fact that kelp are some of the most intensely studied macroalgae in the world, there is significant debate over the classification within and among the three “derived” families, the Alariaceae, Laminariaceae, and Lessoniaceae (ALL). Molecular phylogenies published for the ALL families have generated hypotheses strongly at odds with the current morphological taxonomy; however, conflicting phylogenetic hypotheses and consistently low levels of support realized in all of these studies have resulted in conservative approaches to taxonomic revisions. In order to resolve relationships within this group we have sequenced over 6000 bp from regions in the nuclear, chloroplast, and mitochondrial genomes and included 42 taxa in Bayesian, neighbor‐joining, and parsimony analyses. The result is the first comprehensive and well‐supported molecular phylogeny for the ALL complex of the Laminariales. We maintain the three recognized families (Alariaceae, Laminariaceae, and Lessoniaceae), but with vastly different compositions, as well as propose the Costariaceae fam. nov. for Agarum , Costaria , Dictyoneurum , and Thalassiophyllum , the only genera in the Laminariales with flattened, occasionally terete, stipes and either a perforate or reticulate blade. In addition, our data strongly support a split of the genus Laminaria . We resurrect the genus Saccharina Stackhouse for the Laminaria clade that does not contain L. digitata (Hudson) J.V. Lamouroux, the type of the genus.

The onshore deposition of macroalgal and macrophyte wrack provides a potentially significant marine subsidy to intertidal and supratidal herbivore and decomposer communities. Based on the study of daily input loads to beaches, we estimated summer wrack deposition of up to 140 Mg (dry mass)/km shoreline in Barkley Sound, British Columbia. However, input rates were highly variable depending on beach type, nearshore hydrodynamics, and buoyancy characteristics of the wrack. Cobble beaches retained ∼10 times and 30 times more wrack than did gravel and sand beaches, respectively. Cobble and gravel beaches also differed in species composition of new (fresh) wrack input, with Macrocystis integrifolia being characteristic for the former and Nereocystis luetkeana for the latter, which we attribute to buoyancy characteristics of the floating debris. On sand beaches, Phyllospadix spp. and Enteromorpha spp. were the dominant wrack species. Species composition of freshly deposited wrack also depended on wave exposure, but predictability based on the species pool within a beach's catchment was restricted. Drift lines of aging wrack differed from freshly deposited wrack in species composition, probably due to wrack decomposition that results in fluxes of nutrients and energy between the adjacent marine and terrestrial habitats. We hold that the characteristics of a given beach, e.g., substratum and wave exposure, and their effects on wrack input, will have important ecological and biogeochemical implications for the marine–terrestrial ecotone.

Phylogenetic analyses of asymmetry variation offer a powerful tool for exploring the interplay between ontogeny and evolution because (i) conspicuous asymmetries exist in many higher metazoans with widely varying modes of development, (ii) patterns of bilateral variation within species may identify genetically and environmentally triggered asymmetries, and (iii) asymmetries arising at different times during development may be more sensitive to internal cytoplasmic inhomogeneities compared to external environmental stimuli. Using four broadly comparable asymmetry states (symmetry, antisymmetry, dextral, and sinistral), and two stages at which asymmetry appears developmentally (larval and postlarval), I evaluated relations between ontogenetic and phylogenetic patterns of asymmetry variation. Among 140 inferred phylogenetic transitions between asymmetry states, recorded from 11 classes in five phyla, directional asymmetry (dextral or sinistral) evolved directly from symmetrical ancestors proportionally more frequently among larval asymmetries. In contrast, antisymmetry, either as an end state or as a transitional stage preceding directional asymmetry, was confined primarily to postlarval asymmetries. The ontogenetic origin of asymmetry thus significantly influences its subsequent evolution. Furthermore, because antisymmetry typically signals an environmentally triggered asymmetry, the phylogenetic transition from antisymmetry to directional asymmetry suggests that many cases of laterally fixed asymmetries evolved via genetic assimilation.

Classic marine ecological paradigms view kelp forests as inherently temperate-boreal phenomena replaced by coral reefs in tropical waters. These paradigms hinge on the notion that tropical surface waters are too warm and nutrient-depleted to support kelp productivity and survival. We present a synthetic oceanographic and ecophysiological model that accurately identifies all known kelp populations and, by using the same criteria, predicts the existence of >23,500 km(2) unexplored submerged (30- to 200-m depth) tropical kelp habitats. Predicted tropical kelp habitats were most probable in regions where bathymetry and upwelling resulted in mixed-layer shoaling above the depth of minimum annual irradiance dose for kelp survival. Using model predictions, we discovered extensive new deep-water Eisenia galapagensis populations in the Galápagos that increased in abundance with increasing depth to >60 m, complete with cold-water flora and fauna of temperate affinities. The predictability of deep-water kelp habitat and the discovery of expansive deep-water Galápagos kelp forests validate the extent of deep-water tropical kelp refugia, with potential implications for regional productivity and biodiversity, tropical food web ecology, and understanding of the resilience of tropical marine systems to climate change.

Crabs grown experimentally on fully shelled prey developed larger and stronger claws than those raised on nutritionally equivalent unshelled prey. When one claw was immobilized, claws also became asymmetrical. These use-induced changes differ from skeletal remodelling in vertebrates and many invertebrates because changes in the rigid exoskeleton can occur only after molting, and claw muscle mass must be reduced substantially before the molt. Such short-term adaptive responses to environmental stimuli, if heritable, could yield long-term evolutionary changes in claw size and, if combined with behavioral biases toward one side (handedness), could also promote the evolution of claw dimorphism.

By combining data from a variety of sources we explore patterns of evolution and speciation in Nucella, a widely studied genus of shallow-water marine neogastropods. We present a hypothesis of phylogenetic relationships for all of the currently recognized species of northern hemisphere Nucella, based on an analysis of 718 base pairs of nucleotide sequence from the mitochondrial cytochrome b gene. The order of appearance of species in the fossil record is congruent with this hypothesis. The topology of the inferred phylogeny of Nucella, coupled with ecological, morphological, and fossil evidence, was used to address three main questions: (1) At what time and by which route was the North Atlantic invaded from the North Pacific compared to prior studies of the trans-Arctic interchange? (2) Do patterns of molecular variation within species corroborate the importance of climatic cycles in driving speciation in north temperate marine animals? (3) Was radiation in the direction of increased or decreased ecological specialization, body size, or vulnerability to predation? Molecular evidence confirmed that the sole North Atlantic species, N. lapillus, arose from a North Pacific ancestor. Biogeographic and paleontological evidence supported the dispersal of Nucella, and perhaps other interchange species, via the Eurasian Arctic. Rather intriguingly, the linkage of N. lapillus to a western as opposed to eastern Pacific clade, and the biogeographic origins of the eastern Pacific species, parallel closely similar patterns observed in another genus of rocky-shore gastropods, Littorina. This congruence, in conjunction with information on the climatic and geographic histories of the region, as well as the geographic arrangement of mtDNA haplotypes within Nucella species, supports a model of speciation in Nucella driven by cycles of climatic amelioration and deterioration that began during the Miocene. Calibrations from the fossil record of Nucella suggest that third position transitions and transversions accrue at a rate of 3-4% and 0.5% respectively per million yr. This supports an early participation by Nucella in the trans-Arctic interchange, as suggested by paleobiogeographic studies. Consistent with the unstable taxonomic history of species of Nucella, we found few nonmolecular traits to be phylogenetically informative. Among North Pacific species, more recently derived species (N. canaliculata and the N. emarginata clade) were more ecologically specialized (narrower diet and habitat range). Consistent with extensive intraspecific variation, shell traits were quite labile evolutionarily: neither overall size nor development of antipredatory traits exhibited consistent evolutionary trends over the history of the genus. Nurse eggs (unfertilized eggs consumed by developing embryos) were an ancestral trait that was lost evolutionarily in the two clades that also exhibited increased body size, suggesting that these two life-history traits may be coupled. The reduced number of chromosomes in N. lapillus is clearly a derived state and is consistent with White's (1978) observations on chromosome evolution in other clades.

The Arctic is entering a new ecological state, with alarming consequences for humanity. Animal-borne sensors offer a window into these changes. Although substantial animal tracking data from the Arctic and subarctic exist, most are difficult to discover and access. Here, we present the new Arctic Animal Movement Archive (AAMA), a growing collection of more than 200 standardized terrestrial and marine animal tracking studies from 1991 to the present. The AAMA supports public data discovery, preserves fundamental baseline data for the future, and facilitates efficient, collaborative data analysis. With AAMA-based case studies, we document climatic influences on the migration phenology of eagles, geographic differences in the adaptive response of caribou reproductive phenology to climate change, and species-specific changes in terrestrial mammal movement rates in response to increasing temperature.

The relationship between omnivory and stability has been the subject of a longstanding debate in ecology. Early theory predicted that omnivory would decrease the probability of food webs being stable. While early empirical data appeared to support the prediction that omnivory should be rare, detailed study of food webs later revealed that omnivory is ubiquitous across ecosystems and taxa. Recent years have seen renewed interest in the omnivory‐stability debate, and advances in mechanistic non‐equilibrium models demonstrated that omnivory can both increase and decrease stability. Current efforts have therefore focused on identifying biological mechanisms that promote the persistence of food webs with omnivory. We synthesize recent evidence that omnivory often stabilizes food webs when it occurs as life‐history omnivory, when prey experience reduced predation rates due to refuges or adaptive antipredator defences, and when omnivores interfere with each other or feed adaptively. Empirical research has lagged behind theory and there remains a shortage of studies directly measuring the stability of diverse natural communities that vary in the number and strength of omnivorous interactions. Early microcosm experiments indicated a narrow range of conditions for the persistence of simple omnivorous modules, while studies of omnivory embedded within larger natural networks have demonstrated its stabilizing effects. These new findings alter our view of food web dynamics and show that rather than looking for a simple and general omnivory‐stability relationship, we should focus on identifying conditions under which omnivory is a stabilizing feature of more complex natural systems.

This study investigates wasting disease in the northeast Pacific keystone predatory sea star Pisaster ochraceus on the outer west coast of Vancouver Island (British Columbia, Canada). To quantify the effects of temperature, season and locality on the vulnerability of P. ochraceus to wasting disease, we conducted surveys and experiments in early and late summer. To test the prediction that a small increase in temperature would result in heightened infection intensities, we housed sea stars at different temperatures in the laboratory and caged sea stars subtidally at 2 depths. Prevalence and infection intensity were always higher in warm temperature treatments and did not differ between the sexes or with increasing size. Disease effects also varied with season and locality. Specimens held in aquaria displayed significantly higher disease prevalence and infection intensity in June versus August. Furthermore, sea stars from a sheltered inlet showed markedly higher prevalence of the disease in late summer, while wave-exposed sites had consistently low disease prevalence. Seasonal changes in reproductive potential, host condition and/or physiological acclimation, as well as differences in environmental regime among localities, may impact the dynamics of wasting disease. These results demonstrate that small increases in temperature could drive mass mortalities of Pisaster due to wasting disease, with vulnerability possibly reaching a peak in spring and in populations from sheltered localities. This is the most northern report of wasting disease in the class Asteroidea on the west coast of North America.

We investigated the consequences of feeding for acid-base balance, nitrogen excretion, blood metabolites and osmoregulation in the Pacific spiny dogfish. Sharks that had been starved for 7 days were surgically fitted with indwelling stomach tubes for gastric feeding and blood catheters for repetitive blood sampling and were confined in chambers, allowing measurement of ammonia-N and urea-N fluxes. The experimental meal infused via the stomach tube consisted of flatfish muscle (2% of body mass) suspended in saline (4% of body mass total volume). Control animals received only saline (4% of body mass). Feeding resulted in a marked rise in both arterial and venous pH and HCO3- concentrations at 3-9 h after the meal, with attenuation by 17 h. Venous P(O2) also fell. As there were negligible changes in P(CO2), the response was interpreted as an alkaline tide without respiratory compensation, associated with elevated gastric acid secretion. Urea-N excretion, which comprised >90% of the total, was unaffected, while ammonia-N excretion was very slightly elevated, amounting to <3% of the total-N in the meal over 45 h. Plasma ammonia-N rose slightly. Plasma urea-N, TMAO-N and glucose concentrations remained unchanged, while free amino acid and beta-hydroxybutyrate levels exhibited modest declines. Plasma osmolality was persistently elevated after the meal relative to controls, partially explained by a significant rise in plasma Cl-. This marked post-prandial conservation of nitrogen is interpreted as reflecting the needs for urea synthesis for osmoregulation and protein growth in animals that are severely N-limited due to their sporadic and opportunistic feeding lifestyle in nature.

Niche theory in its various forms is based on those environmental factors that permit species persistence, but less work has focused on defining the extent, or size, of a species' environment: the area that explains a species' presence at a point in space. We proposed that this habitat extent is identifiable from a characteristic scale of habitat selection, the spatial scale at which habitat best explains species' occurrence. We hypothesized that this scale is predicted by body size. We tested this hypothesis on 12 sympatric terrestrial mammal species in the Canadian Rocky Mountains. For each species, habitat models varied across the 20 spatial scales tested. For six species, we found a characteristic scale; this scale was explained by species' body mass in a quadratic relationship. Habitat measured at large scales best-predicted habitat selection in both large and small species, and small scales predict habitat extent in medium-sized species. The relationship between body size and habitat selection scale implies evolutionary adaptation to landscape heterogeneity as the driver of scale-dependent habitat selection.

Abstract The field of left–right (LR) patterning—the study of molecular mechanisms that yield directed morphological asymmetries in otherwise symmetrical organisms—is in disarray. On one hand is the undeniably elegant hypothesis that rotary beating of inclined cilia is the primary symmetry‐breaking step: they create an asymmetric extracellular flow across the embryonic midline. On the other hand lurk many early symmetry‐breaking steps that, even in some vertebrates, precede the onset of ciliary flow. We highlight an intracellular model of LR patterning where gene expression is initiated by physiological asymmetries that arise from subcellular asymmetries (e.g. motor‐protein function along oriented cytoskeletal tracks). A survey of symmetry breaking in eukaryotes ranging from protists to vertebrates suggests that intracellular cytoskeletal elements are ancient and primary LR cues. Evolutionarily, quirky effectors like ciliary motion were likely added later in vertebrates. In some species (like mice), developmentally earlier cues may have been abandoned entirely. Late‐developing asymmetries pose a challenge to the intracellular model, but early mid‐plane determination in many groups increases its plausibility. Multiple experimental tests are possible. BioEssays 29: 271–287, 2007. © 2007 Wiley Periodicals, Inc.

As CO(2) levels increase in the atmosphere, so too do they in the sea. Although direct effects of moderately elevated CO(2) in sea water may be of little consequence, indirect effects may be profound. For example, lowered pH and calcium carbonate saturation states may influence both deposition and dissolution rates of mineralized skeletons in many marine organisms. The relative impact of elevated CO(2) on deposition and dissolution rates are not known for many large-bodied organisms. We therefore tested the effects of increased CO(2) levels--those forecast to occur in roughly 100 and 200 years--on both shell deposition rate and shell dissolution rate in a rocky intertidal snail, Nucella lamellosa. Shell weight gain per day in live snails decreased linearly with increasing CO(2) levels. However, this trend was paralleled by shell weight loss per day in empty shells, suggesting that these declines in shell weight gain observed in live snails were due to increased dissolution of existing shell material, rather than reduced production of new shell material. Ocean acidification may therefore have a greater effect on shell dissolution than on shell deposition, at least in temperate marine molluscs.

assisted in the field without compensation, and this assistance was of greatest value. Clarence R. Alien sacrificed his own research time to conduct seismic studies on the glacier which provided essential data on the thickness of ice and configuration of the bedrock channel. Kermit Jacobson, purchasing agent of the California Institute of Technology, took time from his regular duties to expedite the shipment

To study the mechanisms of branchial acid-base regulation, Pacific spiny dogfish were infused intravenously for 24 h with either HCl (495+/- 79 micromol kg(-1) h(-1)) or NaHCO(3) (981+/-235 micromol kg(-1) h(-1)). Infusion of HCl produced a transient reduction in blood pH. Despite continued infusion of acid, pH returned to normal by 12 h. Infusion of NaHCO(3) resulted in a new steady-state acid-base status at approximately 0.3 pH units higher than the controls. Immunostained serial sections of gill revealed the presence of separate vacuolar proton ATPase (V-H(+)-ATPase)-rich or sodium-potassium ATPase (Na(+)/K(+)-ATPase)-rich cells in all fish examined. A minority of the cells also labeled positive for both transporters. Gill cell membranes prepared from NaHCO(3)-infused fish showed significant increases in both V-H(+)-ATPase abundance (300+/-81%) and activity. In addition, we found that V-H(+)-ATPase subcellular localization was mainly cytoplasmic in control and HCl-infused fish, while NaHCO(3)-infused fish demonstrated a distinctly basolateral staining pattern. Western analysis in gill membranes from HCl-infused fish also revealed increased abundance of Na(+)/H(+) exchanger 2 (213+/-5%) and Na(+)/K(+)-ATPase (315+/-88%) compared to the control.

Mean size (volume) of the eggs of the starfish Solaster stirnpsonl was 0.406 mm3 (n = 658); this did not differ among 4 locations in Barkley Sound, on the west coast of Vancouver Island, Canada. However, there were significant differences in mean egg size among females at each location. The range of egg sizes among s i b h g s w i h n a single spawn was 28 and 39 % of the mean size for 2 females (n = 100 for each sample). Egg organic content (measured for individual eggs) was also variable. Mean content was 113.9 pg organic carbon egg-'. There were significant differences in egg organic content among locations and among females within a population. The range of sibling variation was 43 and 48% of the mean content. However, egg size was not a reliable predictor of egg content. Even the extreme egg sizes failed to yield significantly different predictions of egg content. Therefore the assumption that egg size is a reliable indicator of parental investment per offspring is not warranted in intraspecific life history studes.