The selective advantage of host feminization: a case study of the green crab Carcinus maenas and the parasitic barnacle Sacculina carcini

Male crabs infected by parasitic barnacles (Rhizocephala) are known to be morphologically feminized. Here, we investigate morphological chances in green crabs, Carcinus maenas, induced by the parasitic barnacle Sacculina carcini. Infected males acquire a broader, longer and segmented abdomen, fringed with marginal setae. Copulatory appendages and pereopods are reduced in length, and the chelae become smaller. The feminization show great individual variation. Males with scars from lost externae, the parasites reproductive organ situated under the abdomen, are less modified than males carrying an externa, and the feminization is more pronounced in smaller than in larger males. No super-feminization is evident in female crabs that remain morphologically unaffected by infection. The protective value of a parasitically induced enlargement of the male abdomen may constitute an adaptation that increases parasite longevity. The additional effects on male morphology are viewed as pleiotropic side effects of the main adaptive value of enlarging the abdomen.     

Almost royal: incomplete suppression of host worker ovarian development by a social parasite wasp

Insect social parasites, like other parasites, may benefit from inhibiting their host from reproducing (complete or partial parasitic castration) because they can then exploit more of the host’s resources for their own reproduction. In particular, social parasites that kill or expel the host queen need to prevent host workers from reproducing; this is a common worker response to the absence of their queen. Indeed, host workers would benefit from detecting the presence of the parasite and investing in direct and indirect fitness. Studying whether and how social parasites control host worker reproduction can provide information about the degree of integration of the parasite in the host colony and help identify factors regulating workers’ reproductive decisions in social insects. We investigated whether the paper wasp social parasite, Polistes sulcifer, suppresses Polistes dominula (host) worker reproduction as efficiently as the dominant host female does in queen-right colonies by comparing worker reproductive efforts in parasitized and non-parasitized (control) colonies. Our results show that 6 weeks after usurpation of their colony by the social parasite, parasitized workers (1) had more developed ovaries than control workers and (2) laid more eggs as soon as the opportunity arose. This reproductive readiness of parasitized workers was not apparent 2 weeks after colony usurpation. This suggests that P. dominula workers have evolved means to react to social parasitism, as occurs in some ants, and that the parasite has only limited control over host reproduction.     

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.     

How hot for how long? The potential role of heat intensity and duration in moderating the beneficial effects of an ecosystem engineer on rocky shores

Studies of the importance of ecosystem engineers have focused on their benefit to biodiversity through ameliorating environmental stress, without understanding the exact benefits gained by associated organisms. On monsoonal tropical shores, species experience strong seasonality in environmental conditions from almost temperate winters to tropical summers when mass mortalities can occur during daytime emersion. The limpet, Cellana grata, associates with an ecosystem engineer, the barnacle Tetraclita japonica, in summer, but not in winter. To understand the benefits of this association, physiological responses (heart rates and osmotic responses) of the limpet either amongst Tetraclita or on open rock surfaces were investigated under three environmental conditions in a laboratory mesocosm: awash (non-stressed), low (30 °C) and high thermal stress (40 °C) of varying durations (3 or 6 h). In general, at 30 °C, limpets showed similar physiological responses under all conditions for both exposure durations. After 6 h at 40 °C, however, all limpets on open rock surfaces died, whereas those associated with barnacles survived. The surviving limpets experienced similar levels of stress as those exposed to 40 °C on open rock surfaces for half the time (3 h), showing that both the level and duration of stress were important. Limpets, therefore, gain benefits from engineering species when conditions are extreme or stress is prolonged. Under low temperatures or for short durations (e.g. winter), associating with barnacles does not provide physiological benefits. Understanding how, and to what extent, associates benefit from ecosystem engineers highlights how close the margin between survival and mortality can be when conditions are extreme.     

Assessment of factors affecting heart rate of the limpet Patella vulgata on the natural shore

 Heart rate variations of a population of the limpet Patella vulgata were monitored in the natural environment (Lough Hyne, southern Ireland) by non-invasive, optoelectronic recording. The heart rates of 145 limpets of different sizes, living on vertical and horizontal substrata, were measured both in air and water at different environmental temperatures, while the animals were inactive on their home scars. The heart rates of emersed, inactive limpets were positively related to air temperature and negatively related to limpet size. These relationships were similar for limpets on vertical and horizontal substrates. In contrast, no significant relationship between heart rate and temperature was found in submerged limpets, probably due to the narrow thermal range of the water during the study period. During submersion, a significant negative relationship between heart rate and size was evident for limpets on vertical surfaces but not for limpets on horizontal surfaces. In general, submerged limpets had a higher heart rate, 1.16 times that of limpets exposed to air. Moreover, the heart rates of nine animals were recorded while they were moving and while inactive on their home scars. Active limpets had a faster heart rate, 1.6 times that of limpets resting on their home scars. The dependence of heart rate on environmental temperature, size, respiratory medium and activity, as observed in limpets on the shore, agrees well with laboratory data and with previous findings of the correlation of oxygen consumption with the same factors. Such in situ measurements may, therefore, prove useful in attempts to determine natural levels of energy expenditure in models on the behaviour of foraging molluscs. Received: 5 September 1999 / Accepted: 17 April 2000     

Shell parameters in relation to zonation in mediterranean limpets

The relation of shell form to habitat in the Mediterranean limpets Patella caerulea (L.) and P. lusitanica (Gmelin) was investigated. P. caerulea shells were significantly longer, broader, but lower in height than P. lusitanica shells. The regression of the ratio (length plus breadth)/2 on the height of the shell was found to characterize the two limpet populations, with a small degree of overlap reflecting the distribution of the two limpets on the shore.     

Scarred limpets at hydrothermal vents: evidence of predation by deep-sea whelks

The chaotic physical and chemical environment at deep-sea hydrothermal vents has been associated with an ecosystem with few predators, arguably allowing the habitat to provide refuge for vulnerable species. The dominance of endemic limpets with thin, open-coiled shells at north Pacific vents may support this view. To test their vulnerability to predation, the incidence of healed repair scars, which are argued to reflect non-lethal encounters with predators, were examined on the shells of over 5,800 vent limpets of Lepetodrilus fucensis McLean (1988) that were collected from 13 to 18 August 1996. Three vent fields on the Juan de Fuca Ridge at ca. 2,200 m depth were sampled, two within 70 m of 47°56.87′N 129°05.91′W, and one at 47°57.85′N 129°05.15′W with the conspicuous potential limpet predators, the zoarcid fish Pachycara gymninium Anderson and Peden (1988), the galatheid crab Munidopsis alvisca Williams (1988), and the buccinid snail Buccinum thermophilum Harasewych and Kantor (2002). Limpets from the predator-rich vent were most often scarred, a significant difference created by the high incidence of scars on small (<4 mm long) limpets in this sample. Collected with the limpets were small (median shell diameter 4.4 mm) buccinids. They, rather than the larger, more conspicuous mobile fishes and crabs are argued to be the shell-damaging predator. Electronic supplementary material The online version of this article (doi:) contains supplementary material, which is available to authorized users.     

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.     

Effect of acanthocephalan parasites on the behaviour and coloration of the mud crab Macrophthalmus hirtipes (Brachyura: Ocypodidae)

In the field, the numbers of cystacanths of the parasitic acanthocephalan Profilicollis spp. harboured by crabs are relatively high and correlate with carapace width. In a field experiment, the responses of crabs to the simulated approach of a bird predator (the parasite's definitive host) was not influenced by the number of acanthocephalans they harboured. Crabs that were exposed at the surface of the sediments during receding high tide, however, tended to harbour more parasites than nearby crabs hidden in burrows. An analysis of colour patterns on the carapace of crabs showed that infection levels did not influence carapace pigmentation, and thus did not affect the conspicuousness of a crab relative to the background environment. However, the likelihood of a male crab winning a ritualized fight against a conspecific in the field was associated with its infection level, but in a way that suggests that this finding is a consequence of pathology rather than an adaptation of the parasite to increase its transmission rate. Although only weak evidence was found indicating that Profilicollis manipulates the behaviour or colour of its host to its own benefit, the high infection levels observed suggest that the crab population acts as a major reservoir for larval stages of this parasite that are infective to birds.     

Female great tits do not alter their yolk androgen deposition when infested with a low-transmittable ectoparasite

In birds as in many other taxa, parasites can have deleterious effects on offspring development. Therefore, avian mothers have evolved responses to counteract parasite virulence in offspring via transgenerational defense mechanisms that is the transfer of immune-enhancing substances such as antibodies to their eggs. Another maternal pathway is suggested by the finding that infested great tit mothers produced eggs with lower androgens, since these yolk androgens are immunosuppressive and potentially affect parasite susceptibility of the nestlings. However, whether this pathway is a specific adaptation to infestation with parasites that affect the offspring or an epiphenomenon of lower androgen production in the female due to the parasite effects on the mother itself is as yet unclear. In this study we infested female great tits (Parus major) with sheep ticks (Ixodes ricinus), which are nonnidicolous ectoparasites with low vertical transmission capability, and evaluated the effects on yolk androgen deposition. Tick-infested females did not significantly reduce their deposition of androgens (androstenedione (A₄) and testosterone) compared to tick-reduced females, which is in contrast to a previous study showing a lowered deposition of A₄ and testosterone when females were exposed to the nidicolous hen flea. Thus, females alter their hormone deposition, and thus likely offspring phenotype, when exposed to parasites that also form the parasitic environment of their offspring, but not when temporarily infested with the field-dwelling sheep ticks with low transmission capability. This suggests that selection favored the evolution of an adaptive transgenerational effect by acting mainly on the parasite-induced maternal effect.     

Mineralization of major lateral teeth in the radula of a deep-sea hydrothermal vent limpet (Gastropoda:Neolepetopsidae)

Radular teeth of a neolepetopsid patellogastropod limpet, Paralepetopsis ferrugivora, from a deep-sea hydrothermal vent site have similar elemental composition (O, Si, P, S, Cl, K and Fe) to radular teeth of the shallow-waters patellogastropod limpets. However, in contrast to shallow waters limpets, the fully mature teeth of P. ferrugivora do not show any crystalline phases. Amorphous silica was found in the cusp of the teeth and amorphous iron oxide in the junction zone and base of the teeth. Ferritin-rich vesicles were observed in cells adjacent to the junction zone of the early mature teeth, suggesting that these vesicles can mediate the delivery of iron to the tooth matrix. The similarity in the elemental composition between the hydrothermal limpet P. ferrugivora and shallow-waters patellogastropod limpets shows that the extreme hydrothermal environment did not alter the elemental composition of the radular teeth in the deep-sea species.Communicated by P. W. Sammarco, Chauvin     

Foraging and homing behaviour in the high-shore, crevice-dwelling limpet Helcion pectunculus (Prosobranchia: Patellidae)

The foraging activity of the high-shore, crevice-dwelling limpet Helcion pectunculus (Gmelin, 1791) (Prosobranchia: Patellidae) from an exposed shore on the eastern Cape coast of South Africa was monitored. Activity was compared during spring and neap tides and between spring, summer, autumn and winter. Rhythms of activity in this limpet varied depending upon microhabitat; individuals inhabiting both east- and west-facing rock surfaces were active during nocturnal low tides, but limpets on west-facing rock surfaces were also active during daytime low tides, whilst in the shade. Individuals travelled further during foraging excursions in winter (xˉ=85.53 cm) than in either spring (xˉ=55.7 cm) or summer (xˉ=48.8 cm) and also during spring low tides (xˉ=89.8 cm) compared with neaps (xˉ=40.9 cm). H. pectunculus exhibited rigid homing to a fixed scar within a crevice, and feeding excursions were found to consist of three distinct phases: a relatively rapid outward phase, a much slower foraging phase and a rapid homeward phase. Whether or not these limpets graze throughout an excursion is not known. Foraging was always highly directional, with a mean vector which took limpets onto an area of the rock face with the highest microalgal biomass. The fact that H. pectunculus took advantage of optimal feeding areas and memorized their location to enable return visits suggests a learning component in herbivorous gastropod foraging behaviour. Received: 29 December 1997 / Accepted: 8 May 1998     

Ecological studies on a tropical limpet Cellana radiata

Some aspects of the habitat zones, distribution pattern, and population density with reference to tidal levels of the tropical limpet Cellana radiata (Born) are presented. Observations have also been made on the homing behaviour of the limpet. Unlike the temperate limpets, no migration to different tidal levels during different seasons was observed in C. radiata.     

Brood mate eviction or brood mate acceptance by brood parasitic nestlings? An experimental study with the non-evictor great spotted cuckoo and its magpie host

Some avian brood parasitic nestlings are highly virulent, destroying all host eggs or nestmates, while others accept growing up together with host nestmates. The traditional idea was that all brood parasitic nestlings would benefit from being alone in the host nest. Thus, why do nestlings of some brood parasitic species accept the company of host offspring in the nest? The trade-off hypothesis suggests that brood parasites must balance the costs and benefits of killing host young because of two major potential costs: risk of nest desertion and loss of begging assistance. Here, we test this hypothesis in a non-evictor cuckoo species, the great spotted cuckoo Clamator glandarius and its main host, the magpie Pica pica, by manipulating brood size (1–3 nestlings) and brood composition (only cuckoo, only magpie or mixed) during three consecutive breeding seasons. None of the broods were abandoned by host parents, and cuckoo nestlings alone in the nest tended to grow faster (i.e. wing length). Thus, none of the predictions of the two potential costs on which the trade-off hypothesis is based apply to the great spotted cuckoo–magpie system. Our experimental study could not directly test why chick killing has not evolved in great spotted cuckoos, but the results point in the direction of several possibilities. We suggest that chick killing in great spotted cuckoos may not be adaptive mainly because another, less costly strategy (i.e. outcompeting host nestmates for food), is efficient for successful parasitism of magpie hosts.     

Predation by the nemertean Carcinonemertes errans on eggs of the Dungeness crab Cancer magister

The nemertean Carcinonemertes errans is an important predator on the eggs of its host, the Dungeness crab Cancer magister. Each nemertean consumes an average of approximately 70 crab eggs during the host brooding period. The nemerteans, which apparently consume no other food during the host brooding period, convert crab egg tissue to worm tissue with an efficiency of 28.9% on a caloric basis. Epidemic levels of Carcinonemertes errans on the central California Dungeness crab population have resulted in the direct mortality of an average of 55% of the eggs produced by that population over the last 5 years, making C. errans probably the most numerically significant predator on these crabs.     

Shiny cowbirds share foster mothers but not true mothers in multiply parasitized mockingbird nests

Obligate brood parasitic birds, such as cowbirds, evade parental care duties by laying their eggs in the nests of other species. Cowbirds are assumed to avoid laying repeatedly in the same nest so as to prevent intrabrood competition between their offspring. However, because searching for host nests requires time and energy, laying more than one egg per nest might be favoured where hosts are large and can readily rear multiple parasites per brood. Such ‘repeat parasitism’ by females would have important consequences for parasite evolution because young parasites would then incur indirect fitness costs from behaving selfishly. We investigated shiny cowbird (Molothrus bonariensis) parasitism of a large host, the chalk-browed mockingbird (Mimus saturninus), in a population where over 70 % of the parasitized mockingbird nests receive multiple cowbird eggs. We assessed egg maternity directly, using cameras at nests to film the laying of individually-marked females. We also supplemented video data with evidence from egg morphology, after confirming that each female lays eggs of a consistent appearance. From 133 eggs laid, we found that less than 5 % were followed by the same female visiting the nest to lay again or to puncture eggs. Multiple eggs in mockingbird nests were instead the result of different females, with up to eight individuals parasitizing a single brood. Thus, while cowbird chicks regularly share mockingbird nests with conspecifics, these are unlikely to be their maternal siblings. Our results are consistent with shiny cowbird females following a one-egg-per-nest rule, even where hosts can rear multiple parasitic young.     

Encounters between Antarctic limpets, <Emphasis Type="Italic">Nacella concinna</Emphasis>, and predatory sea stars, <Emphasis Type="Italic">Lysasterias</Emphasis> sp., in laboratory and field experiments

Antarctic limpets, Nacella concinna, from the Admiralty Bay (King George Island, South Shetlands) for at least part of the year (austral winter) co-exist with predatory sea stars Lysasterias sp. Our laboratory and field experiments established that the presence of Lysasterias sp. or its odour had considerable influence upon their behaviour. Limpets’ responses, consisting of shell mushrooming, shell rotation and flight, were distinctly different from their reaction to other stimuli, such as food and conspecific odours, or mechanical stimulation. Moreover, a significant impact of sea star presence on limpets’ activity was observed, with limpets fleeing to a distance of 60 cm from the predator. Such reactions allow limpets to lower the incidence of sea star predation, but at the cost of presumptive disrupting of foraging and an additional energy expended for locomotion. A visible difference was noted between two limpet populations, with the rockpool limpets responding only after physical contact with being touched by a sea star, and the subtidal ones responding at a distance of up to 20 cm.     

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.     

Food webs and fishing affect parasitism of the sea urchin Eucidaris galapagensis in the Galápagos

In the Galápagos Islands, two eulimid snails parasitize the common pencil sea urchin, Eucidaris galapagensis. Past work in the Galápagos suggests that fishing reduces lobster and fish densities and, due to this relaxation of predation pressure, indirectly increases urchin densities, creating the potential for complex indirect interactions between fishing and parasitic snails. To measure indirect effects of fishing on these parasitic snails, we investigated the spatial relationships among urchins, parasitic snails, commensal crabs, and large urchin predators (hogfish and lobsters). Parasitic snails had higher densities at sites where urchins were abundant, probably due to increased resource availability. Commensal crabs that shelter under urchin spines, particularly the endemic Mithrax nodosus, preyed on the parasitic snails in aquaria, and snails were less abundant at field sites where these crabs were common. In aquaria, hogfish and lobsters readily ate crabs, but crabs were protected from predation under urchin spines, leading to a facultative mutualism between commensal crabs and urchins. In the field, fishing appeared to indirectly increase the abundance of urchins and their commensal crabs by reducing predation pressure from fish and lobsters. Fished sites had fewer snails per urchin, probably due to increased predation from commensal crabs. However, because fished sites also tended to have more urchins, there was no significant net effect of fishing on the number of snails per square meter. These results suggest that fishing can have complex indirect effects on parasites by altering food webs.     

Sewage discharges in oceanic islands: effects and recovery of eulittoral macrofauna assemblages

Sewage discharges are among the most common anthropogenic stressors on rocky shores. However, studies on benthic invertebrates’ responses to sewage pollution on insular assemblages are rare. In order to fulfil this gap, (i) the effects of sewage pollution and (ii) the recovery capacity of eulittoral insular assemblages were examined. The study was conducted on Terceira Island (Azorean Archipelago, Portugal), in four distinct areas: one impacted area (outfall in operation), one post-impacted area (decommissioned outfall) and two undisturbed reference areas. Results showed that the abundance of the dominant species changed between reference and impacted areas. More specifically, the abundance of limpets Patella candei, and barnacles Chthamalus stellatus decreased, while the abundance of littorinids Tectarius striatus and Melarhaphe neritoides increased near the sewage discharges. Seventeen months after removal of the outfall, limpet and barnacle populations had partially recovered, but littorinid populations had still not fully recovered. This study confirms the negative effects of sewage discharges on eulittoral assemblages, and provides information on the resilience of benthic species following the cessation of sewage disposal.