A. Richard Palmer

Fluctuating asymmetry analyses: a primer

The developmental stability of an organism is reflected in its ability to produce an ‘ideal’ form under a particular set of conditions (Zakharov, 1992). The lower its stability, the greater the likelihood it will depart from this ‘ideal’ form. Ideal forms are rarely known a priori. However, bilateral structures in bilaterally symmetrical organisms offer a precise ideal, perfect symmetry, against which departures may be compared (Palmer & Strobeck, 1986). Thus they provide a very convenient method for assessing deviations from the norm, and studying the factors that might influence such deviations.

Detecting publication bias in meta-analyses: A case study of fluctuating asymmetry and sexual selection

Those familiar with human nature and the publication process acknowledge that biases due to selective reporting of results are likely widespread in all fields of academic inquiry that depend on tools of statistical inference (e.g., see Begg and Berlin 1988; Iyengar and Greenhouse 1988; and the extensive discussion following each). However, although qualitative and quantitative methods exist for assessing the prevalence of selective reporting, and selective reporting has been studied in the medical and social sciences (Begg 1994, and references therein), the issue has received little attention in recent meta-analyses of ecological and evolutionary patterns. Clearly, “if publication bias is present, and if it operates in the same direction for all studies (as is likely), then [meta-analysis] is likely not only to produce biased summary estimates but also to produce estimates which are apparently precise and accurate leading to conclusions which may not only be wrong but appear convincing” (Begg and Berlin 1988, p. 437). To biologists unacquainted with the formal study of publication patterns, the terms “selective reporting” (statistical significance of an outcome influences its likelihood of being reported or published) and “publication bias” (the inflation of average effect size due to selective reporting) may imply a conscious intent to deceive, but this

FISH PREDATION AND THE EVOLUTION OF GASTROPOD SHELL SCULPTURE: EXPERIMENTAL AND GEOGRAPHIC EVIDENCE

Marine gastropod molluscs exhibit a wide range of shell forms, many of which are believed to provide some defense against predation. Vermeij (1974) has suggested that narrow or occluded apertures, low spires, thickened shells and strong sculpture act in various ways to deter the attacks of shell-breaking or shell-entering predators. In addition, Vermeij (1976, 1977a) has presented evidence suggesting that inter-oceanic differences in crab predation intensity may have been responsible for the evolution of less vulnerable shells among Indo-West Pacific gastropods when compared with Eastern Pacific and Tropical Atlantic ones. Similarly, one might expect regional differences in the intensity of a particular mode of predation to lead to geographic variation in the frequencies and degree of development of a mode-specific morphological defense. Crabs and fishes are almost certainly the most important shell-breaking predators on lower intertidal and subtidal gastropods. Their modes of feeding, however, are rather different. Crabs are able to manipulate shells more precisely and can apply their chelae to a shell in a variety of ways. They should be less deterred by strong external sculpture than by thickened shells, reduced spires, or reinforced or occluded apertures, except when shells are small relative to chelae. On the other hand, fishes that crush gastropods must use their jaws and hence can only apply stress to very restricted portions of a shell in a restricted manner. They should be more effectively deterred by certain types of strong external sculpture than by thickened lips or restrictive apertures. More specifically, stout spines or nodes appear to reduce susceptibility to being crushed by fish. Such sculpture may act in at least four ways (Fig. 1): 1) it increases the effective diameter of the shell, thus decreasing the mechanical advantage of the predators crushing apparatus; 2) it distributes the stress over a larger area of the shell; 3) it localizes the stress at the thickest parts of the shell; and 4) it focuses the applied force to a very restricted area of the crushing surface, increasing the chance of damage to the predator. The structural similarity of strong axial ribbing suggests it should perform in a similar manner. Shell thickness and to some degree overall shell shape may also affect susceptibility to crushing. In this paper I directly test the importance of stout spines as a potential defense against crushing by fish. Observations on the type of damage inflicted by crushing fishes serve as the basis for some speculation about how other morphologies might also reduce vulnerability. Finally I consider the geographic distribution of stout spinose sculpture and how it relates to the distribution of shell-destroying fishes. Experimental studies that examine the importance of gastropod shells as a defense against predation have almost exclusively employed crabs as predators (Ebling et al., 1964; Kitching et al., 1966; Kitching and Lockwood, 1974; Vermeij, 1976; Zipser and Vermeij, 1978; but see Ivlevs 1961 study of freshwater carp, roach and perch on Limnaea ovata of different shell thicknesses, p. 102). The present study represents the first experimental examination of the types of shell morphologies that offer an effective defense against shell-crushing fishes and rays. Although I have only

Effect of crab effluent and scent of damaged conspecifics on feeding, growth, and shell morphology of the Atlantic dogwhelk Nucella lapillus (L.)

Juvenile Nucella lapillus of two different shell phenotypes, exposed shore and protected shore, were maintained in running seawater under each of three experimental conditions for 94 d: a) laboratory control, b) exposed to the effluent of crabs (Cancer pagurus) fed frozen fish (‘fish-crab’), and c) exposed to the effluent of crabs fed live conspecific snails (‘snail-crab’). Rates of barnacle consumption and rates of body weight change varied significantly between phenotypes and among experimental conditions. Individuals from the protected-shore consumed consistently fewer barnacles and grew consistently less than those from the exposed shore. Body weight increases in the fish-crab treatments were from 25 to 50% less than those in the controls and body weights in the snail-crab treatment either did not change or actually decreased. The perceived risk of predation thus appears to have a dramatic effect on the rates of feeding and growth of N. lapillus.

Evolutionary history of Northern Hemisphere Nucella (Gastropoda, Muricidae) : Molecular, morphological, ecological, and paleontological evidence

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?

Elevated CO2 affects shell dissolution rate but not calcification rate in a marine snail

As CO2 levels increase in the atmosphere, so too do they in the sea. Although direct effects of moderately elevated CO2 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 CO2 on deposition and dissolution rates are not known for many large-bodied organisms. We therefore tested the effects of increased CO2 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 CO2 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.

Prey selection by thaidid gastropods: some observational and experimental field tests of foraging models

SummaryField observations and experiments revealed that predatory intertidal gastropods of the genus Thais (or Nucella) were able both to recognize the expected food value of encountered prey (expected energy or growth potential gained per unit handling time) and to monitor their average yield over time (average energy or growth potential gained per unit foraging time). They appeared to discriminate not only among prey species, but also among different sized individuals of the same prey species. The evidence supporting these interpretations included: 1) field observations of snails feeding preferentially on prey types of higher expected food value even though lower value prey types were available and abundant, 2) a very limited number of direct underwater observations of foraging snails rejecting encountered items that were either of lower expected value than the item finally eaten or not measurably different from it, and 3) field (=‘arena’) experiments in which both average yield, and the distribution and abundance of potential prey were controlled: snails conditioned at a high average yield fed preferentially on high value items, while those animals conditioned at a low yield consumed prey in the proportions that they were encountered. These behaviors are all consistent with a prey-selection decision motivated by energetic considerations. Further, the field experiments indicated that these predatory gastropods could select items from a diverse array of prey so as to maximize growth in their natural environment. The behaviors were not consistent with three alternative foraging hypotheses: non-selective foraging, frequency-dependent foraging on prey types (here, sizes of particular prey species), and frequency-dependent foraging on prey species. Deviations from some of the quantitative predictions of optimal foraging theory appeared related to learning and risk.

Growth rate as a measure of food value in thaidid gastropods: Assumptions and implications for prey morphology and distribution

Abstract Rates of body growth were measured for three species of rocky intertidal gastropods: Thais (or Nucella ) lamellosa (Gmelin), T . (or N .) canaliculata (Duclos), and T . (or N .) emarginata (Deshayes). Three size classes of each predator species were grown experimentally in cages at two tidal heights on four size classes of each prey species: Semibalanus cariosus (Pallas), Balanus glandula Darwin, and Mytilus edulis L. Growth was also assessed for Thais canaliculata feeding on Mytilus californianus Conrad, and Thais emarginata feeding on Chthamalus dalli Pilsbry. Rates of body growth varied as a function of predator size, prey size and prey species. With one exception (large Thais canaliculata ) intermediate sized Balanus glandula promoted the most rapid growth for all sizes of all three species of Thais ; thus these potentially competing predator species have the same highest ranked prey. Among prey promoting slower growth, those encountered commonly in the normal habitats of the predator promoted more rapid growth than those encountered rarely, suggesting that past evolutionary experience has influenced present food value (= growth potential) of prey. For some predators, the ranking of prey species changed with predator size; Chthamalus dalli and similar sized Balanus glandula promoted comparable growth in small Thais emarginata but Chthamalus dalli promoted much slower growth than similar sized Balanus glandula in larger Thais emarginata . Rank differences based on prey size in Balanus glandula became more pronounced and in some instances changed with increasing predator size; larger B. glandula promoted relatively faster growth for large snails than for small snails in all Thais species. Finally, growth rates were correlated with two important attributes of fitness in T. canaliculata and T. emarginata ; in general, prey promoting more rapid growth also resulted in an earlier age of first reproduction for initially immature snails and higher rate of egg capsule production for mature individuals. Thus, these growth rates provide a basis from which to examine quantitatively patterns of prey selection from an energy- or growth-maximization perspective. These patterns of predator growth also permit inferences about the possible influence of predation on the evolution of prey morphology, life-history, and microhabitat distribution. Size refuges from Thais predation were confirmed for both Semibalanus cariosus and Mytilus californianus . Both Balanus glandula and Mytilus edulis , on the other hand, were vulnerable to predation by all sizes of Thais examined (> 10 mm) regardless of prey size; thus, neither of these species achieves a size refuge. In addition, on rocky shores, vertical distributions of the prey species reflect general preference patterns of their predators: higher value prey species, i.e. those with less well developed defensive morphologies ( Balanus glandula, Mytilus edulis ), generally occur higher on the shore. This pattern would be expected if preferred prey are consumed first lower on the shore where they are more available.

SIZE-DEPENDENT ASYMMETRY: FLUCTUATING ASYMMETRY VERSUS ANTISYMMETRY AND ITS RELEVANCE TO CONDITION-DEPENDENT SIGNALING

Fluctuating asymmetry (FA) has received much recent attention in studies of the evolution of sexual signaling systems. Tests apparently showing that symmetry decreases as individual condition decreases have bolstered the view that FA plays a significant role in the evolution of sexual signals. However, a closer inspection of several examples of bilateral variation as a function of trait size (a correlate of condition) suggests a different pattern of variation. Rather than FA, these traits suggest a pattern of size‐dependent antisymmetry (a bimodal frequency distribution of R – L). We introduce some quantitative methods to test for condition‐ or size‐dependent FA. Our analyses reject pure FA for four of the five published datasets involving signals (the fifth is equivocal), but confirm the presence of size‐dependent FA in one nonsignaling trait. In the studies not conforming to FA, the data appear to fit more closely a pattern of antisymmetry in individuals with smaller signaling traits. Our results thus suggest that current discussions and conclusions about the role of FA in the evolution of signaling systems should be reconsidered. More specifically, we note that condition‐dependent antisymmetry offers a more reliable indicator than condition‐dependent FA. We caution, however, that additional work will be needed to determine whether the pattern is general and not an artifact. Our method of analysis could usefully be applied to studies of other continuous factors expected to be correlated with asymmetries, including heterozygosity, inbreeding, and environmental stress. Finally, we suggest that antisymmetry may have commonly been mistaken for FA in a variety of cases dealing with a variety of problems.

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.