SAFETY FACTORS OF TROPICAL VERSUS TEMPERATE LIMPET SHELLS: MULTIPLE SELECTION PRESSURES ON A SINGLE STRUCTURE

A comparison of the safety factors of tropical and temperate limpet shells in the eastern Pacific yielded two results of significance. A safety factor was defined as shell strength/maximum tenacity, where maximum tenacity (force required to detach foot) determines the maximum prying force that a crab or bird predator can exert on the shell. 1) On average, shell strength and foot tenacity for the tropical limpets were twice those for the temperate limpets. In contrast, the average safety factors for the two groups were approximately equal. This comparatively narrow range of safety factors was due to a highly significant association of greater shell strengths with greater foot tenacities. The implication of this result is that selection has acted to closely link the mechanical performances of these two rather independent structures, the shell and the foot. 2) The presence of an additional class of predators which feed on the tropical limpets was reflected in the safety factors of their shells. Whereas the shells of both tropical and temperate limpets are exposed to predator-induced prying forces, the shells of the tropical group are also exposed to lateral crushing forces generated by fish predators. This additional selection pressure was associated with several deviations from a regression of safety factor versus variability in shell strength which had been calculated previously for the temperate limpets. As predicted, the magnitudes of these deviations were correlated with the degree of exposure to this additional selection pressure. Hence, the presence of more than one selection pressure appears to have influenced the precision with which the shells of these species have become adapted to a single selection pressure. The use of safety factor analysis provides a very useful methodology for identifying additional selection pressures or adaptive constraints on biological structures.     

Adaptive design of locomotion and foot form in prosobranch gastropods

A comparison of the locomotor types, speed, tenacity, and foot form of nearly 300 species in 52 families of marine prosobranchs has revealed that foot size and shape and even subtle variations of locomotion affect the speed and strength of adhesion to the substratum.Gastropods inhabiting soft substrata move primarily by pedal cilia or by discontinuous locomotion in which shell and foot move alternately. Both types of movement are accompanied by low tenacity. A specialized type of discontinuous locomotion, namely, leaping, surpasses all other methods of movement in speed. Species with ciliary locomotion have a very large foot while those with discontinuous movement have an exceedingly small foot relative to shell size.The majority of prosobranchs inhabit hard substrata, move by continuous pedal muscular gliding, and have moderately high tenacity during movement. Arhythmic pedal locomotion yields lower maximum speeds and tenacities than do rhythmic pedal waves. Foot size and shape relative to shell length in species with arhythmic locomotion vary from very short and broad to long and narrow. Studies of transects at several temperate and tropical marine littoral stations showed that these species are confined to low littoral or sublittoral habitats that are sheltered from heavy wave action. High speed and tenacity are simultaneously attained only by species with rhythmic pedal waves.Speed and tenacity do not represent competing selective pressures on the size and shape of the foot. Speed increases among species as the foot approaches or exceeds shell length and is highest if the foot is also broad; the greatest tenacities are attained by species with a long, broad foot whose dimensions do not exceed that of the shell. The optimal shape for both high tenacity and speed is a broad foot somewhat shorter than the shell; neither speed nor tenacity are much compromised by this form. In general, only species with rhythmic pedal waves whose foot size and shape approximate the optimal form for high tenacity and speed are found in habitats exposed to much wave action. Long rhythmic waves, moving a large proportion of foot area at once, are in theory energetically more economical than small, very rapid waves resulting in the same overall speed, but experiments showed that tenacity is significantly reduced in gastropods which increase speed by enlarging the waves. The optimal wave pattern of a species should be a balance between the demand for speed with the least expenditure of energy, favored by a pattern of many large waves at once, and the demand for tenacity, favored by a pattern of few and small waves.Retrograde ditaxic waves of elongation are the most common pattern encountered among prosobranchs, and are associated with a large range of foot sizes and shapes. Such waves are at least one third as long as the foot, while direct waves and other waves of compression are frequently much smaller. The range of foot forms of species with waves of compression is restricted, tending to be optimal for high tenacity or to be long and narrow. Waves of compression appear to be a specialization with the potential for maintaining high tenacity even at high speeds since the waves can be very small, and for giving superior speed since they can travel very rapidly.     

Biochemical differences between trail mucus and adhesive mucus from marsh periwinkle snails

The composition of the adhesive form of marsh periwinkle mucus was compared to the trail mucus used during locomotion. The trail mucus consists primarily of large, carbohydrate-rich molecules with some relatively small proteins. In contrast, the adhesive mucus has 2.7 times as much protein with no significant difference in carbohydrate concentration. The resulting gel has roughly equal amounts of protein and carbohydrate. This substantial increase in protein content is due to the additional presence of two proteins with molecular weights of 41 and 36 kD. These two proteins are absent from the trail mucus. Both proteins are glycosylated, have similar amino acid compositions, and have isoelectric points of 4.75. This change in composition corresponds to an order of magnitude increase in tenacity with little clear change in overall concentration. The difference between adhesive and non-adhesive mucus suggests that relatively small proteins are important for controlling the mechanics of periwinkle mucus.     

Alternation between attachment mechanisms by limpets in the field

The attachment mechanism used by limpets in the rocky, wave-swept intertidal zone of California was determined during high tide and low tide. The two mechanisms that limpets are known to use, suction and glue-like adhesion, were distinguished by measuring the limpets' attachment forces in shear and by staining for glue-like residues where the limpets had been attached. The results show that ≈ 73% of limpets at high tide use suction, while the rest use glue-like adhesion. Conversely, ≈ 75% of limpets at low tide use glue-like adhesion, while the rest use suction. The normal tenacity of limpets was also measured at high and low tide. The mean tenacity at high tide was significantly less than that at low tide. From these data it was estimated that the mean tenacity of glue-like adhesion is ≈ 0.23 MN·m⁻² and the mean tenacity of suction adhesion is ≈ 0.09 MN·m⁻². It is hypothesized that the cycle of alternating attachment mechanisms is linked to the limpets foraging cycles.     

Protection against lethal freezing temperatures by mucus in an Antarctic limpet

The antarctic limpet, Patinigera polaris, is sometimes caught in near-shore ice and exposed to temperatures substantially below ?2 °C. In-frozen animals always secrete an envelope of mucus which prevents extracellular ice propagation down to ?10 °C. Survival in limpets without mucus protection is significantly lower. Ice propagation through limpet mucus is retarded below its equilibrium freezing point in a manner similar to polar fishes. The capacity of mucus as a cryoprotectant has not previously been described.     

Underwater locomotion strategy by a benthic pennate diatom Navicula sp.

The mechanism of diatom locomotion has been widely researched but still remains a hypothesis. There are several questionable points on the prevailing model proposed by Edgar, and some of the observed phenomena cannot be completely explained by this model. In this paper, we undertook detailed investigations of cell structures, locomotion, secreted mucilage, and bending deformation for a benthic pennate diatom Navicula species. According to these broad evidences, an updated locomotion model is proposed. For Navicula sp., locomotion is realized via two or more pseudopods or stalks protruded out of the frustules. The adhesion can be produced due to the pull-off of one pseudopod or stalk from the substratum through extracellular polymeric substances. And the positive pressure is generated to balance the adhesion because of the push-down of another pseudopod or stalk onto the substratum. Because of the positive pressure, friction is generated, acting as a driving force of locomotion, and the other pseudopod or stalk can detach from the substratum, resulting in the locomotion. Furthermore, this model is validated by the force evaluation and can better explain observed phenomena. This updated model would provide a novel aspect on underwater locomotion strategy, hence can be useful in terms of artificial underwater locomotion devices.     

Depth gradients in shell morphology correlate with thermal limits for activity and ice disturbance in Antarctic limpets

To fully understand how species distributions will respond to changing environments it is essential to understand the mechanisms underlying variation in animal performance and the relative importance of different ecological and environmental factors. A performance measure that has previously been used as an indicator of thermal capacity of the Antarctic limpet (Nacella concinna) to cope with regional warming is the ability to right if removed from the substratum and turned upside down. As part of an on-going study into limpet genetics and phenotypic plasticity, we tested the temperature limits for 50% righting of limpets from 6 and 30 m depth. The 50% threshold for limpets collected from 6 m (4.7 °C) was higher than for those collected from 30 m (0.7 °C). This compares with a previously published limit of 2.2 °C for limpets collected from 12-15 m at the same location. These thermal limits positively correlated with a depth gradient in shell height to length ratio; thickness and strength. Flatter limpets, had a reduced thermal limit for righting than taller limpets which we hypothesise is related to increased energy requirements of flat limpets, which have to turn through a greater angle to right than tall limpets. Of the factors that cause morphological plasticity of gastropod shells, iceberg disturbance is the most likely cause of the sub-tidal gradient in N. concinna shell shape, and therefore the thermal limit for righting of limpets from 6 to 30 m depth, rather than environmental temperature.     

Experimental manipulation of shell color and morphology of the limpets Lottia asmi (Middendorff) and Lottia digitalis (Rathke) (Mollusca: Patellogastropoda)

We experimentally show that substratum can determine an individual patellogastropod's color and morphology. Lottia asmi (Middendorff), previously considered a high-domed, black stenotopic species on trochid gastropods, is similar to other northeastern Pacific limpet species with low profile and tessellated color patterns, when it is translocated to rock substrata. Lottia digitalis (Rathke), a highly variable species with at least two ecological variants that have been considered to be genetically determined, changes between these two forms when translocated from stalked barnacles to rocks. Color changes because the ingested pigments (algal, periostracal, etc.) and other materials (e.g., calcium carbonate) vary between substrata; morphological changes occur as responses to the topographical complexity and constraints of substrata. The geographical distribution of ecological variants of polytypic limpet species, and the ability to achieve cryptic coloration, may be determined by the geographic distributions of algae on which the limpets feed rather than by intrinsic characteristics of the limpets.     

What triggers the “bail out” behaviour in the limpet Lottia gigantea?

Manipulating objects (small rocks, mussel shells, etc.) to which limpets are clinging will cause many spontaneously to release their hold ("bail out"). Experiments demonstrated that in the owl limpet (Lottia gigantea) bail out was only triggered by rotation of the limpet around a horizontal axis at rates of 0.13 to 1.00rps. Limpets reattached more vigorously to a surface following a “bail out” than when they were forcibly removed from the substratum. In the field a variety of intertidal gastropods were observed to “bail out”. “Bail out” appears to be an adaptive response allowing an individual to abandon a dislodged substratum for a more stable one.     

Snails and their trails: the multiple functions of trail‐following in gastropods

Snails are highly unusual among multicellular animals in that they move on a layer of costly mucus, leaving behind a trail that can be followed and utilized for various purposes by themselves or by other animals. Here we review more than 40 years of experimental and theoretical research to try to understand the ecological and evolutionary rationales for trail‐following in gastropods. Data from over 30 genera are currently available, representing a broad taxonomic range living in both aquatic and terrestrial environments. The emerging picture is that the production of mucus trails, which initially was an adaptation to facilitate locomotion and/or habitat extension, has evolved to facilitate a multitude of additional functions. Trail‐following supports homing behaviours, and provides simple mechanisms for self‐organisation in groups of snails, promoting aggregation and thus relieving desiccation and predation pressures. In gastropods that copulate, trail‐following is an important component in mate‐searching, either as an alternative, or in addition to the release of water‐ or air‐borne pheromones. In some species, this includes a capacity of males not only to identify trails of conspecifics but also to discriminate between trails laid by females and males. Notably, trail discrimination seems important as a pre‐zygotic barrier to mating in some snail species. As production of a mucus trail is the most costly component of snail locomotion, it is also tempting to speculate that evolution has given rise to various ways to compensate for energy losses. Some snails, for example, increase energy intake by eating particles attached to the mucus of trails that they follow, whereas others save energy through reducing the production of their own mucus by moving over previously laid mucus trails. Trail‐following to locate a prey item or a mate is also a way to save energy. While the rationale for trail‐following in many cases appears clear, the basic mechanisms of trail discrimination, including the mechanisms by which many snails determine the polarity of the trail, are yet to be experimentally determined. Given the multiple functions of trail‐following we propose that future studies should adopt an integrated approach, taking into account the possibility of the simultaneous occurrence of many selectively advantageous roles of trail‐following behaviour in gastropods. We also believe that future opportunities to link phenotypic and genotypic traits will make possible a new generation of research projects in which gastropod trail‐following, its multitude of functions and evolutionary trade‐offs can be further elucidated.     

Locomotion and adhesion of neutrophil granulocytes : Effects of albumin, fibrinogen and gamma globulins studied by reflection contrast microscopy

Proteins as well as materials of low molecular weight have marked effects on the rate of locomotion, adhesion and cell shape of human neutrophil granulocytes in vitro. Plasma protein preparations differ qualitatively with respect to their chemokinetic activity. Human serum albumin (HSA), fibrinogen and acid-treated gamma globulin without polymers have a positive chemokinetic effect on neutrophils suspended in Gey's solution. Standard gamma globulin (SGG) or acid-treated gamma globulin with polymers have marked negative chemokinetic activity. Three different mechanisms are presumably responsible for the low rate of locomotion observed in Gey's solution alone, Gey's solution containing acid-treated gamma globulin with polymers or SGG, respectively: (a) too firm adhesion to the substratum; (b) lack of adhesion to the substratum; and (c) impaired capacity to perform shape changes. The relationship between attachment of cells to the substratum and the rate of neutrophil locomotion has been investigated. It appears that the pattern of adhesion rather than cell attachment as measured by the proportion of neutrophils adhering to the substratum is a meaningful correlate to locomotion. Two different patterns of adhesion can be distinguished by means of reflection-contrast microscopy: (a) the pattern characterized by uniform grey areas is compatible with efficient locomotion; (b) a pattern characterized by large black areas at the cell periphery. It is associated with neutrophils in Gey's solution which fail to displace themselves efficiently. This suggests that reflection-contrast microscopy may be helpful in distinguishing contacts allowing locomotion to occur from contacts impeding neutrophil locomotion.     

The interplay of physical and biological factors in maintaining mid-shore and low-shore assemblages on rocky coasts in the north-west Mediterranean

This study examined the interactive effects of grazing by limpets and inclination of the substratum in maintaining differences between mid-shore and low-shore assemblages of algae in the northwest Mediterranean, at different scales of space and through time. Alternative models leading to different predictions about these effects were proposed and tested. Limpets were excluded by fences from areas of the substratum at mid levels on the shore. The response of algal assemblages to this manipulation was compared with control and enclosure plots at the same level, and with unmanipulated plots in the low shore where limpets are less abundant. The effects of limpets were examined at several replicated sites (0.1–4 km apart) for each slope of the substratum (nearly horizontal vs vertical), at different locations (hundreds of kilometres apart) and at different times. Individual taxa responded differently to limpet exclusion. The percentage cover of the coarsely branched and filamentous algae increased significantly in exclosure plots, in some loser reaching values found on the low shore. These patterns, however, varied greatly from shore to shore and significant effects were found both on horizontal and vertical substrata. Multivariate analyses indicated that grazing by limpets accounted for about 20% of the differences between mid-shore and low-shore assemblages. This effect was independent of substratum inclination and was consistent in space and time, suggesting that physical conditions were not as stressful for macroalgae on vertical substrata as initially supposed. Variable recruitment of algae is proposed as a possible explanation for the lack of consistency in the effects of limpets at the scale of the shore. The results of this study emphasize the need for multiple-scale analyses of the interactive effects of physical and biological factors to understand the organization of natural assemblages. Received: 22 June 1999 / Accepted: 15 November 1999     

Factors affecting individual variation in resting site fidelity in the patellid limpet,Cellana toreuma (Reeve)

An investigation was made of individual variation in resting site fidelity in the limpet,Cellana toreuma, with special attention to the adaptiveness of its homing behaviour. Limpets resting in the higher part of the study site showed strong resting site fidelity while those in the middle part showed weaker fidelity and tended to shift their resting sites to higher parts. Limpets resting in the lower part where there were an abundant supply of food and high predation intensity, had the strongest resting site fidelity and always returned to fixed resting sites with mucous sheets. The resting site fidelity varied continuously among individuals. Four causes for shift of resting site were detected: fleeing from starfish,Coscinasterias acutispina, pushing contests for resting site, non-returning excursions following and without following other's trail. The frequency of shift of resting sites due to each of these causes varied among individuals. Estimation of energy budget during about half a month showed that the location of resting site and frequency of shift of the site considerably affected the growth of limpets through energy expenditure by respiration and stationary mucus secretion, and energy intake by foraging. These variations were proposed as being a result not of density dependent dispersal nor adaptation to a single factor such as desiccation, heavy wave impacts or predation, but being due to individual difference in a compromise between two conflicting factors, susceptibility to predation and accessibility to food resources.     

Locomotion and adhesion of polymorphonuclear leukocytes. Effects of the supporting substratum

Contact angle measurements have been used to correlate surface hydrophobicity of a supporting substratum with adhesion and locomotion of polymorphonuclear leukocytes. The binding of human serum albumin, a well-known chemokinetic substance, to hydrophilic glass slides gave rise to hydrophobic surfaces with adhesive properties conductive to cell polarization, thus allowing cell locomotion. Parallel contact angle and cell adhesion measurements suggested that albumin modified the cell-substratum interaction by increasing the van der Waals forces of attraction and reducing the electrostatic forces. By allowing cells to adhere to a hydrophobic surface (siliconized glass), it was found that protein could be omitted from in vitro test systems for leukocyte locomotion. It is suggested that quantitatively equal cell adhesion values may, depending on the type of attraction forces working in adhesion to the substratum, result in different locomotion patterns.     

Locomotion and adhesion of polymorphonuclear leukocytes effects of the supporting substratum

Contact angle measurements have been used to correlate surface hydrophobicity of a supporting substratum with adhesion and locomotion of polymorphonuclear leukocytes. The binding of human serum albumin, a well-known chemokinetic substance, to hydrophilic glass slides gave rise to hydrophobic surfaces with adhesive properties conducive, to cell polarization thus allowing cell locomotion. Parallel contact angle and cell adhesion measurements suggested that albumin modified the cellsubstratum interaction by increasing the van der Waals forces of attraction and reducing the electrostatic forces. By allowing cells to adhere to a hydrophobic surface (siliconized glass), it was found that protein could be omitted from in vitro test systems for leukocyte locomotion. It is suggested that quantitatively equal cell adhesion values may, depending on the type of attraction forces working in adhesion to the substratum, result in different locomotion patterns.     

Desiccation of intertidal limpets: Effects of shell size,fit to substratum,and shape

For undisturbed, field populations of the northeast Pacific, intertidal limpet Collisella pelta (Rathke), water loss was found to be proportional to apertural circumference rather than mantle cavity surface area. This contrasts with previous laboratory measurements for other limpet species and emphasizes the importance of the fit of shell to substratum for non-homing limpets. This close fit maintained a meniscus of water between the edge of the shell and the substratum, thereby reducing evaporative surface area and increasing the advantage of large size for reducing the rate of water loss. Shell-raising behavior eliminated the meniscus, increasing the rate of desiccation, and water loss appeared to become proportional to mantle cavity surface area. Indirect evidence suggests that C. pelta may utilize shell-raising behavior for evaporative cooling under thermally stressful conditions in the field.Both shell size and shape affect the ratio of water stores (proportional to internal shell volume) to evaporative surface area (proportional to apertural circumference) and per cent water loss is, potentially, a function of this ratio. Shape, however, (when defined as volume/circumference) exhibits an average allometric increase with increasing size (volume) for C. pelta, as well as for three other sympatric limpet species: C. Paradigitalis (Fritchman), C. Digitalis (Rathke), and Notoacmea scutum (Rathke). An independent measure of shape is, therefore, required to separate shape effects on desiccation from size effects; this measure was obtained by rearranging the allometry equation. In contrast to significant size effects, no measurable effect of shape on desiccation was detected. Variation in limpet shell shape may be partially or wholly maintained by factors other than an adaptational response to desiccation.     

COMPARISONS OF THE BIOLOGY OF THE INTERTIDAL SUBANTARCTIC LIMPETS NACELLA CONCINNA AND KERGUELENELLA LATERALIS

Two limpet species occur intertidally on subantarctic SouthGeorgia, the patellid Nacella concinna and the siphonarlid Kerguelenellalateralis. N. concinna is confined to the lower shore closeto LWS; K. lateralis occurs in middle shore pools, so theirdistributions do not overlap. N. concinna has a much narrowerthermal niche (–12.9°C to +15.6°C) than K. lateralis(–17.8°C to +31.8°C). Environmental data are presentedto show that the upper lethal temperature of N. concinna islow enough to prevent the limpet living higher on the shore.Both limpet species are slow-moving, but K. lateralis showsincreasing speed with rising temperature, peaking at 15–20°C.In contrast, N. concinna moves actively down to –1.9°C(when sea water freezes), but there is a steady decrease inspeed of locomotion above +2°C. Locomotion ceases at 14°Cin N. concinna (c.f. 30°C in K. lateralis). Both speciesexhibit very low tenacities, but in N. concinna tenacity decreaseswith increasing shell length. In K. lateralis there is no effectof temperature on tenacity. Both species show a positive allometricrelationship between foot area and shell length. N. concinnafeeds upon microbial films and microepiflora, but K. lateraliseats colonial diatoms and Enteromorpha bulbosa. Observationson shell middens of the kelp gull Larus dominicanus showed thatthe gulls did not eat K. lateralis, though they ate great quantitiesof the less accessible N. concinna. Gulls ate N. concinna assmall as 11 mm shell length (within the size range of K. lateralis).Experiments on gulls demonstrated an unwillingness to eat K.lateralis, probably because the siphonariid extrudes a viscidwhite mucus when the foot is touched. (Received 9 May 1996; accepted 8 July 1996)     

The mucus producing glands and the distribution of the cilia of the pulmonate slug Limax pseudoflavus

The gross anatomy and histochemistry of the mucus-producing glands of Limax pseudoflavus Evans were investigated. The body mucus can be divided into three areas. The dorsal body surface is covered with a sulphated acid mucopolysaccharide/protein mixture secreted largely by five cell types. The pedal mucus is a mixture of neutral mucopolysaccharide from the suprapedal gland. The dorsal and pedal mucus sheets are separated by the peripodal groove whose cells secrete a weakly acid mucus. The duct of the suprapedal gland, the epidermis around the pneumostome, the ventral surface of the peripodal groove and the centre of the underside of the foot are ciliated. The dorsal and pedal mucus remain stationary relative to the body and the substrate respectively and the only rejection currents seen in the mucus are around the pneumostome.
It is suggested that the pedal mucus is formed by the mixture of the products of the suprapedal gland and the mucoprotein secreting gland in the leading edge of the foot, thus producing a mucus suitable for locomotion. Many areas of the animal (e.g. the head, pneumostome, sole and the leading edge of the foot) are capable of producing both a fluid (neutral or weakly acid) and a viscous (acid) mucus. It is postulated that such an arrangement allows for both adhesion and lubrication at different times.     

Interactive effects of grazing and enrichment on diversity; conceptual implications of a rocky intertidal experiment

Understanding the ways in which consumers and productivity act and interact to yield differences in diversity is of primary conceptual and pragmatic importance in a world in which humans are simultaneously changing ecological communities and substantially altering the availability of nutrients. Here, I used macroalgal communities on rocky reefs to examine the effects of both limpet grazing and nutrient enrichment on algal diversity throughout almost two years of succession. The experimental design included three levels each of grazing and nutrients, with unglazed terracotta pots attached to the rock as replicate plots in a high intertidal limpet-macroalgal community. Grazing effects varied by year. During the first year, grazing effects were context-dependent with limpets resulting in lower species richness, especially at the highest level of limpet density. However, at this highest level of limpet density, high enrichment counteracted the negative effect of limpets such that diversity was similar to that in treatments with lower limpet densities. In the second year, grazing generally decreased richness, regardless of enrichment. The results of this experiment are partially consistent with the grazer-reversal hypothesis – grazing decreased richness in low nutrient conditions and this effect was neutralized (rather than reversed) under high enrichment. Inconsistencies with model predictions may be explained by the apparent unresponsiveness of algal productivity to experimental enrichment, the unique substrate-scraping feeding mechanisms of limpets, and potentially limited propagule supply.