Major primary stages of biomineralization in radular teeth of the limpet Lottia gigantea

The radula (feeding organ) of the limpet Lottia gigantea is a membraneous ribbon to which are attached up to 150 transverse rows of teeth. The organic matrix of the teeth is impregnated with inorganic salts (Fe, Si, Ca). In its posterior end, the radula originates from a radular gland which is coiled dorsally, where long odontoblast cells secrete the tooth and the radular membrane. Teeth mature gradually. The organic matrix of this complex was stained homogeneously in the first five rows (hematoxylin-eosin). From Row 6 onward, the tooth became demarcated from the radular membrane by forming segments within the matrix of the radular membrane. The cusp's organic matrix milieu was histologically divided into two main domains, internal and external, each one consisting of fibrillar milieu. Teeth are embedded within the tall columnar superior epithelium, which superimposes the cusps. Iron-bearing granules started to appear in these cells beginning at Rows 7 to 10, increasing in number to Row 20 and continuing to at least Row 65. Iron proceeded to infiltrate first into the internal part of the cusp at Row 15. The outer part of the cusp was mineralized beginning at Rows 22 to 27. At about Row 30, the cusp was heavily mineralized by iron. Calcium was deposited into the radular membrane and tooth bases from the most posterior part. It is concluded that radula biomineralization is subject to highly complex but precisely controlled cytological-biochemical processes and that different parts of each young tooth are subjected simultaneously to different biomineralization pathways. Specimens used in this study were collected in 1984 from the intertidal zone at La Jolla, California.     

Ecological impacts on the limpet Lottia gigantea populations: human pressure over a broad scale on island and mainland intertidal zones

Here long-term monitoring data taken at 33 sites in southern and central California coast and islands were used to evaluate the size structure of the large intertidal limpet, Lottia gigantea in restricted-access and in easily accessible intertidal zones that encompass a wide range of ecological variables. Using multi-dimensional analysis of population size structures, we found that sites on islands and strictly protected mainland sites have significantly larger median limpet sizes and a greater range of limpet sizes than unprotected mainland sites, while no pattern occurs in latitudinal or regional comparison of sites. Although intertidal predators such as oystercatchers were not the primary focus of the monitoring efforts, extensive natural history notes taken during sampling visits support the argument that predation was not a primary cause for the size structure differences. Finally, substratum differences were determined not to have biased the observation of larger limpets in protected sites. In regard to human interactions with limpets, we conclude that the degree of enforcement against poaching is the better predictor of limpet size structure than proximity to population centers or visitation to intertidal sites.     

Population structure,northern range limit,and recruitment variation in the intertidal limpet Lottia scabra

The northern range limit of the intertidal limpet Lottia scabra is Cape Arago, Oregon (43°N), where adult survival is excellent, the population is small (<300), and recruitment is low; the range limit may be set by limited recruitment. Between June 2012 and March 2013, 25 sites from the middle of the species range (33°N) to Cape Arago were sampled and population size frequency distributions, densities, and nearest neighbor distances were compared to the amount of rocky and sandy shore and kelp bed size. North and south of 37°N, the densities of new recruits averaged 22 and 86 m^?2, respectively. This shift was associated with the range limit of Macrocystis pyrifera kelp beds; we hypothesize that slower currents in M. pyrifera beds may limit larval dispersal leading to higher recruitment. North and south of 40°N, adult density averaged <1 and 458 m^?2, respectively, with the species absent from many sites to the north. This shift was associated with a sharp drop in the amount of rocky shoreline and an increase in uninhabitable sandy shore. Near the northern range limit, >80 % of the individuals were solitary and may be unable to spawn successfully. Recruitment at Cape Arago was infrequent and likely due to self-recruitment. This study suggests that the range limit was set by the absence of M. pyrifera and too little rocky shore leading to high larval wastage, low settlement, low population densities, and, due to an Allee effect, very small effective population sizes.     

Recruitment in the intertidal limpet Lottia digitalis (Patellogastropoda: Lottiidae) may be driven by settlement cues associated with adult habitat

The ribbed limpet, Lottia digitalis, is found high in rocky intertidal habitat throughout its geographic range. In order to identify likely natural settlement locations for larvae of this species, laboratory-reared larvae were settled onto substrata collected from within and near an adult L. digitalis habitat. Of larvae exposed to rock chiseled from within high-intertidal adult habitat, 31.0% and 23.3% underwent metamorphosis during two separate experiments. Similarly, an unidentified filamentous green alga that was isolated from this rock induced metamorphosis in 26.6% and 8.7% of larvae during additional experiments. In contrast, larvae did not metamorphose upon bare rocks or upon rocks encrusted with a crustose corraline alga (CCA) that were collected from lower intertidal zones, nor did they metamorphose upon the macroalgae Ulva sp., Enteromorpha contorta, Alaria marginata, or Polysiphonia sp. The presence of mucus from adult conspecifics during these experiments did not enhance metamorphosis onto rock taken from adult habitat, but it did induce metamorphosis in an average of 13.5% and 7.0% of larvae introduced to the mid-intertidal bare rock and CCA substrata, respectively. Finally, 38.0% and 34.4% of larvae from two experiments underwent metamorphosis when exposed to the high-intertidal barnacle Pollicipes polymerus. These results suggest that larval settlement, rather than differential post-settlement mortality and/or migration, drives recruitment of L. digitalis in high-intertidal habitats.     

Behavioral responses of territorial red squirrels to natural and experimental variation in population density

The relative scarcity of studies at the intersection of behavioral and population ecology is surprising given the presumed importance of behavior in density-dependent population regulation. Here we tested whether North American red squirrels (Tamiasciurus hudsonicus) adjust their behavior in response to local population density and whether they use rates of territorial vocalizations in their local neighborhood to assess density. We examined these relationships using 18?years of live trapping and 20?years of behavioral data that were collected across natural variation in local population density. To disentangle the effects of population density on behavior from those due to changes in per capita food abundance or changes in the frequency of antagonistic interactions with neighbors, we also experimentally manipulated population density with long-term food supplementation as well as perceived population density with long-term playbacks of territorial vocalizations. The frequency with which squirrels emitted territorial vocalizations was positively associated with local population density. In contrast, antagonistic physical interactions observed between squirrels and territorial intrusions were rare and the frequency of intrusions was weakly and negatively, not positively, associated with population density. Squirrels experiencing naturally and experimentally high density conditions spent less time in the nest and feeding but more time being vigilant. Similar density-dependent changes in behavior were observed in response to our manipulations of perceived population density, indicating that vocalization rates and not physical interactions or food abundance were the mechanism by which squirrels assessed and responded behaviorally to changes in local density.     

Population structure and sex-change in the coral-inhabiting snailCoralliophila violacea at Hsiao-Liuchiu,Taiwan

Surveys of the coral-inhabiting snailCoralliophila violacea (Lamarck) (=C. neritoidea Kiener) were made on shallow fringing reefs (<8 m deep) around Hsiao-Liuchiu, Taiwan, between July and October 1990. The snails were aggregated into patches on the surface of massive poritid coral colonies. Coral colonies >40 cm in diameter were more likely to bear patches of snails than smaller colonies, and also to have more snails. The coralliophilids ranged from 5 to 30 mm in aperture length. The sex ratio of the population was biased toward males (539:279), with only a few small individuals of indistinguishable sex. Snails between 6 and 10 mm were all males, while most snails with aperture lengths 20 mm were females. Judging from the distinct size ranges of males and females within patches and from the observed degeneration of the penis, the snails may have changed sex from male to female with increasing size. Sex-change may occur across a wide size range (10 to 20 mm). The correlation of smallest female size and largest male size among patches indicates that snail size at sex-change is peculiar to each individual patch. Those females in patches with a single female (but many males) were significantly smaller than females in multiple-female patches. It is likely that in the absence of females males change sex at a smaller size, whereas in the presence of large females males delay sexchange until they have reached a larger size. The plasticity of size at sex-change may be adaptive and a result of natural selection at the individual level.     

Host plant density and territorial behavior of the seed bug,Neacoryphus bicrucis (Hemiptera: Lygaeidae)

Summary Adults of the seed bug, Neacoryphus bicrucis, are most numerous in large host plant patches and where host plants are most dense within patches. Males patrol small territories composed of host plants and expel other males and unreceptive females. Larger males aggressively exclude smaller males from high quality territories where both host plants and females are most dense. Consequently, large males mate more frequently than small males. Males remain for longer time in areas where host plants are more dense. However, mating experience influences tenure within a host plant patch such that males tend to remain where they have recently mated. Courtship is aggressive and male territorial behavior is similar to courtship behavior. Preference for territories in areas of high host plant density appears to have been selected to increase the rate of encounter with females which preferentially oviposit in areas of high host plant density.     

Morphological and habitat divergence in the intertidal limpet Patelloida pygmaea

In the intertidal limpet Patelloida pygmaea, two distinctive morphs, the forms pygmaea and conulus, have been recorded. The former possesses a flat elongated shell, and the latter has an extremely high round shell. It has been observed in the field that pygmaea is found on oyster shells Crassostrea gigas. The form conulus uses an unusual substrate for attachment. It is found on the living shells of the intertidal gastropod Batillaria cumingi. Although conulus is normally found only on shells of Batillaria, it can also be found on oyster shells when pygmaea and Batillaria shells are not present in nature. An electrophoretic analysis of allozymes showed that these two forms are reproductively isolated from each other and coexist without gene exchange on the same mudflat. Laboratory experiments showed that pygmaea prefers oyster shells and conulus prefers Batillaria shells as substrates for attachment when both oyster and Batillaria shells are present. The form pygmaea did not attach to Batillaria shells, even when only Batillaria shells were available. However, conulus also attached to oyster shells when Batillaria shells were not available. The proportion of individuals of conulus that attached to oyster shells decreased significantly when pygmaea was attaching to the oyster shells. These results suggest that pygmaea is ecologically more specialized to living on oyster shells than conulus.     

Analyses of limpet defense and predator offense in the field

Between November 1982 and August 1984 diving observations of two intertidal limpets' defensive behaviours in response to two predatory species were made near the Seto Marine Biological Laboratory of Kyoto University, in Wakayama Prefecture, Japan, for over 800 h. The focus of the observations was a simple isolated rock, 0.9 m² in area with an inclination of 75°. The pulmonate homing limpet Siphonaria sirius responded by fleeing from its home in response to the whelk Thais clavigera and by calmping tightly to its home scar in response to the starfish Coscinasterias acutispina. Both behaviours were successful for avoiding predation. After a whelk moved far away, limpets returned to their homes. The patellid limpet Cellana toreuma showed mantle folding behaviour or fled for an average distance of 8 cm vertically upwards in response to the whelk and for an average distance of 21 cm vertically upwards in response to the starfish. The amount of time predators spent foraging increased in the low intertidal zone relative to the mid and high zones, and most predator attacks were observed during the limpets' resting periods (submersion in late afternoon or nighttime). The upward directional flight displayed by C. toreuma was related to the upward orientation of the limpets' heads when they are in a resting position. Half of the limpets observed fleeing downward away from a starfish, a movement elicited by a downward attack, received a second attack. These limpets were preyed upon at the second encounter 67% of the time. The upward fleeing behaviour of C. toreuma resulted in the shifting of its resting site higher up the study site where fewer attacks occurred and where the mortality rate was at its lowest. It is suggested that the homing behaviour of S. sirius and the upward fleeing behaviour of C. toreuma are mechanisms by means of which interspecific competition between limpets is reduced and coexistence on a small rock surface is maintained.     

Biochemical and energy changes during embryogenesis in the rock scallopCrassadoma gigantea

The biochemical composition of eggs spawned from rock scallopsCrassadoma gigantea (Gray) collected from Clayoquot Sound, Vancouver Island (British Columbia, Canada) in the winter of 1987 and the summer of 1988, differed significantly only in lipid and soluble-ash contents. Major macronutrients were catabolized simultaneously and linearly with time of embryogenesis. Total egg energy expended during development was 11.8 kJ g^–1 derived 46.7, 9.8 and 43.5%, from lipid, carbohydrate, and protein, respectively. Glucose in the egg was the dominant source of carbohydrate energy. Deposition of shell was linear with time of embryogenesis and the formation of 44.8% dry wt of shell in the early larval stage, referred to as the D-larva, consumed 64.4% of the total energy expended. Energy required for shell formation was 17.55 kJ g^–1. The RNA:DNA ratio declined exponentially from 18.6 in the egg to 2.21 in the D-larva, which was consistent with that of adult bivalves. Many changes in fatty acid composition were linear with time of embryogenesis, and the percentage ofn3- andn6-higher unsaturated fatty acids to total polyethylenic acids exhibited significant declining and increasing trends, respectively. The linear rate of catabolism of eicosapentaenoic acid, 20:5n3, and the constant level of docosahexaenoic acid, 22:6n3, illustrated an energy and a structural role, respectively, for these dominant acids in the embryonic development of the rock scallop.     

Genetic differentiation independent of intertidal gradients in the pulmonate limpet Siphonaria kurracheensis

The intertidal limpet Siphonaria kurracheensis (Reeve, 1856) has a bimodal vertical distribution of abundance on rocky shores at Rottnest Island, Western Australia. An electrophoretic study of 5 polymorphic enzymes revealed no consistent genetic differences between adults high and low on the shore. Contrasting with this absence of a detectable genetic response to the steep environmental gradients in the intertidal zone, there were genetic differences among low-shore adults from different sites, and between adults and recruits. This genetic differentiation could be due to either localized selection or temporal variation in the genetic makeup of recruits.Communicated by G. F. Humphrey, Sydney     

Intraspecific comb usurpation in the social wasp Polistes fuscatus

Summary Incidents of usurpation were observed in colonies of Polistes fuscatus nesting on farm buildings (1977–79) and in nestboxes (1980–84) in Johnson County, Iowa, USA. Most usurpations (84.8%) occurred in the latter half of the preworker phase of the colony cycle, which coincided with periods of high predation of combs by vertebrates. Usurpers were probably displaced single foundresses which did not join neighbors or refound colonies after comb loss. Most (89–100%) usurpers of known relatedness to the foundresses they replaced were cousins or less related to them. Usurpation was a significant source of nest loss (19.6%) among single foundresses, but was rare (2.2%) in multiple-foundress colonies and colonies with workers (3.5%). Usurpers often destroyed younger brood (eggs and larvae in instars 1–3) in host colonies, while older larvae and pupae were usually spared. Brood destruction was more pronounced in more advanced host combs. Usurper survivorship after workers eclosed was lower than than of queenright single foundresses (61.5% vs 87.0%). Reproductive success by usurpers was less than that of queenright single foundresses, but greater than that of foundresses which initiated colonies late in the preworker colony cycle.     

Comparison of allozyme and mitochondrial DNA spatial differentiation in the limpet Patella vulgata

Allozyme and restriction enzyme analysis of mtDNA was used to study variation in samples from British populations of the marine limpet Patella vulgata in two regions. South Wales and Northeast England. Allozyme analysis revealed significant differences in allele frequencies among samples. However F _ST (population differentiation) values were no higher between than within regions, indicating that genetic heterogeneity was localised and not related to geographic separation. For mtDNA, samples from South Wales exhibited higher haplotype diversity values than samples from Northeast England. In addition there were substantial differences in the haplotype distribution between regions. The value of , the haploid analogoue of F _ST , was low within regions (=0.09) but high between regions (=0.44). The estimated difference in migration rate for allozymes and mtDNA exceed the neutral expectation, unless it is assumed that there are influential differences in the magnitude of female and male gametic dispersal.     

The conflict between feeding and territorial defence in the great tit

Summary A field experiment investigated whether feeding and territorial defence competed for time in the activity budget of territorial male great tits during the spring. Feeding tables were placed on the territories of five males. Five other territorial males also fed at these tables, while ten additional males had no access to any feeding tables. A standardised intrusion using playback of territorial song and a stuffed mount of a male great tit was conducted on each of the twenty territories, and the response of the resident male measured. All of the males with access to a feeding table responded more vigorously to the intrusion than the males who received no extra food. These results are not attributable to the fact that males defended their territories more vigorously because of the addition of feeding tables, since males that gained extra food outside the boundaries of their own territories also defended more vigorously than birds with no access to a feeding table. The results support the conclusion that the provisioned males defended more vigorously because they could afford to take more time out from feeding.     

Temporal genetic variation in populations of the limpet Cellana grata from Hong Kong shores

Variations in the relative contributions of gene flow and spatial and temporal variation in recruitment are considered the major determinants of population genetic structure in marine organisms. Such variation can be assessed through repeated measures of the genetic structure of a species over time. To test the relative importance of these two phenomena, temporal variation in genetic composition was measured in the limpet Cellana grata, among four annual cohorts over 10 years at four rocky shores in Hong Kong. A total of 408 limpets, comprising individuals from 1998, 1999, 2006 and 2007 cohorts were screened for genetic variation using five microsatellite loci. Minor but significant genetic differentiation was detected among samples from the 1998/1999 collection (F _ST = 0.0023), but there was no significant differentiation among the 2006/2007 collection (F _ST = 0.0008). Partitioning of genetic variation among shores was also significant in 1998/1999 but not in the 2006/2007 collection, although there was no correlation between genetic and geographic distances. There was no significant difference between collections made in 1998/1999 and 2006/2007. This lack of clear structure implies a high level of gene flow, but differentiation with time may be the result of stochastic recruitment variation among shores. Estimates of effective population size were not high (599, 95% C.L. 352–11397), suggesting the potential susceptibility of the populations to genetic drift, although a significant bottleneck effect was not detected. These findings indicate that genetic structuring between populations of C. grata in space and time may result from spatio-temporal variation in recruitment, but the potential development of biologically significant differentiation is suppressed by a lack of consistency in recruitment variability and high connectivity among shores.     

The Wahlund effect and the geographical scale of variation in the intertidal limpet Siphonaria sp.

Samples of Siphonaria sp. were collected between 1978 and 1982 from sites covering its known geographic range, from Kalbarri, Western Australia to Port Robe, South Australia. Geographic variation of 7 polymorphic enzymes was examined in this intertidal pulmonate limpet, and was found to be consistently small, indicating a large-scale influence of gene flow due to planktonic dispersal. Despite this large-scale uniformity, there is fine-scale genetic patchiness, which is repeated, rather than accumulated, on the larger scale. Throughout its geographic range, Siphonaria sp. shows deficits of heterozygotes for all 7 loci. The consistency among loci indicates that the causes of the deficits are populational, rather than locus-specific. A Wahlund effect, the departure from Hardy-Weinberg equilibrium due to mixing of individuals from groups with different allelic frequencies, is the simplest explanation of such deficits. The limited geographic variation of allelic frequencies, however, is grossly inadequate to produce these deficits through a Wahlund effect. Similarly, temporal variation in allelic frequencies in recruits does not explain the deficits. The largest contributor to a Wahlund effect appears to be binomial sampling variance among small local breeding groups. Thus, mixing of larvae on a scale of metres, rather than among geographical areas, apparently produces the deficits of heterozygotes.     

Life-history features of the marine intertidal limpet Notoacmea scutum (Gastropoda) in central California

Growth of individually marked specimens of Notoacmea scutum (Rathke) was followed for 15 months (April, 1978 to June, 1979) at a field site in central California, USA. Growth rates were highly seasonal, being highest from late spring through early summer and lowest during winter. Growth rate also varied significantly with intertidal height: limpets lower in the intertidal zone grew faster. Both relationships may have been related to the relative abundance of food or to the amount of time available for foraging. Recently settled limpets, which were present throughout the year, grew to approximately 17 mm in length by the end of their first year; by then, they had also reached the size at which mature gonads were consistently found (16 mm). Limpets were almost 26 mm long by the end of the second year. Substantial mortality occurred throughout the year, but it was particularly severe during winter, when a large portion of the reproductive population was lost. This pronounced winter mortality was probably not caused by invertebrate predators such as seastars. Most limpets at the study site were less than 2 yr old.     

Intraspecific aggression in the colour morphs of the anemone Phymactis clematis from Chile

The anemone Phymactis clematis exhibits intraspecific agression. An investigation into dominance relationships amongst the 3 colour morphs collected from Vna del Mar, Chile, during June, 1980, revealed them to be equally aggressive. The outcomes of experimental contests appeared to reside solely with size-dependent differences in the threshold for the release of agression. Contests were asymmetric and larger individuals displayed aggression earlier against smaller opponents, and won encounters. An analysis of times for the onset of aggression in contests showed that they were highly variable and were not a good indicator of the absolute aggressive ability of individuals as denoted by dominance rankings. It provided, however, evidence indicating a lack of assessment of opponent size during initial contact. This is discussed in relation to the evolution of aggression in anemones and to the concept of evolutionarily stable strategies in contest behaviour. It is concluded that future work on the apparent size-dependent threshold will most instructively be conducted at the neurophysiological level.     

Sex change in a giant endemic limpet,Patella kermadecensis,from the Kermadec Islands

Sex-ratios of the limpetPatella kermadecensis Pilsbry, collected at three times of the year during 1984 and 1985 at Raoul Island in the Kermadecs group, varied with the size of the limpets. Small limpets were predominantly male, while amongst larger ones about half were female. The presence of hermaphroditism inP. kermadecensis was confirmed by microscopic examination of gonad material from over 50 limpets, which revealed a high percentage of individuals with both male and female gametes in their gonads. It is postulated that protandric sex change occurs in this large limpet, and that this phenomenon is related to a change in habitat from the backs of large shells (limpets less than approximately 50 mm) to bedrock (larger limpets). The pattern of sex change inP. kermadecensis is compared with that in other species of limpet, and it is suggested that a reproductive system consisting of gonochoristic males and sequential hermaphrodites may be particularly advantageous for a large, slow-growing species that has a very restricted geographical range.     

Intraspecific nest parasitism in the swallow Hirundo rustica: the importance of neighbors

Summary Intraspecific nest parasitism in the swallow Hirundo rustica involves several parasite and anti-parasite tactics. Neighboring swallows breed asynchronously, perhaps because neighboring nests with overlapping egg-laying periods have higher frequency of intraspecific nest parasitims than neighboring nests with no such overlap. Since nest guarding prevents nest parasitism, the effect of nest guarding was removed by putting up old swallow nests. Such experimental nests were parasitized by swallows more often when the nests contained eggs, than when empty, and when the nests were far away from, rather than close to, an active neighboring nest. Close experimental nests with eggs were, however, parasitized less frequently if asynchronous (non-overlapping egg-laying periods), rather than synchronous, to active neighboring nests. Aggressive anti-parasite behavior of nest owners was determined from responses towards female intruders. Responses were more often aggressive before and especially during egg laying than during incubation. Nest owners also behaved aggressively more often when the intruder approached close to as compared to at some distance from their nest. Focal pairs behaved aggressively more often towards closely approaching intruders during the incubation period than towards distantly approaching intruders during the egg-laying period. Swallows reduce the frequency of intraspecific nest parasitism by nesting asynchronously with and close to a neighboring nest. Aggression by neighbors may reduce the success of potential parasitic swallows.