Pagurus Bernhardus Research Articles

Wave of mutilation: Scavenging hermit crabs use social information to locate carcasses

AbstractCarcasses are patchily distributed and often short‐lived resources, placing scavenging animals under pressure to locate them before they rot or are depleted by competitors. Scavengers may search for carcasses directly, or indirectly, using social information. Aggregations of feeding animals and their conspicuous competitive behaviour may be more readily detectable to searching scavengers than the carcass itself. Moreover, the actions of attendant scavengers upon the carcass, breaking it apart and releasing odour or chemical cues, may further enhance its detectability to others foraging nearby. Here we test this idea. In the first of two experiments performed in the field, we found that hermit crabs (Pagurus bernhardus) were attracted to shelled mussels (Mytilus edulis) that other hermit crabs were already feeding on. They showed no strong tendency to approach aggregations of conspecifics in the absence of food, nor conspecifics that were confined close to mussels but prevented from feeding on them. We speculated that through breaking up the carcass, the feeding hermit crabs released chemical cues and drifting particles of mussel tissue that further attracted other hermit crabs. We tested this in a second experiment, finding that finely chopped mussels attracted significantly more hermit crabs than did intact mussels. We suggest that scavenger feeding action upon carcasses makes these more detectable to others by releasing odour and particle plumes, a form of inadvertently produced social information.

Gut content metabarcoding of six crustaceans provides detailed diet description and insights into their roles as predators and scavengers

While many studies have analyzed the diet of marine consumers using traditional morphology-based methods, the integral diet of many species of functionally important groups such as benthic invertebrates remains poorly resolved. This hinders our ability to precisely establish trophic links among species, which is necessary to understand food webs and ecosystem dynamics. Here, we applied DNA metabarcoding to obtain a high resolution picture of the animal fraction of the diet of six species of crustaceans in the Bay of Biscay; the edible crab Cancer pagurus, the velvet crab Necora puber, the circular crab Atelecyclus undecimdentatus, the spider crab Maja brachydactyla, the shrimp Crangon crangon, and the hermit crab Pagurus bernhardus. We used two pairs of primers targeting the 18S rDNA (generalist) and 12S rDNA (fish-specific) regions to identify prey that makes up the animal fraction of the diet. Based on occurrence data, 54 prey taxa belonging to 5 different phylum mostly represented by teleost fishes and malacostracans were identified. Through a high-level of prey detection, results indicate a scavenging strategy across all consumers mostly based on the consumption of preys likely originating from fishing discards. This study also reveals patterns of niche overlaps among consumers differentiating C. crangon from others and suggesting high overlap in animal resource use between N. puber and M. brachydactyla as well as C. pagurus. High resolution diet description revealed the complexity of trophic interactions on a local scale.

Just a matter of size? Evaluating allometry and intersexual heterometry in Pagurus bernhardus using ratios and indices (Decapoda, Anomura).

Heterochely denotes the presence of dissimilarly sized chelipeds on opposite sides of the body, a prevalent occurrence in diverse crustaceans. Conversely, heterometry pertains to the quantifiable disparities in size between these chelipeds. Both chelipeds hold pivotal roles in activities such as foraging, mating, and defense. Consequently, individuals of both genders in heterochelic species exhibit this morphological pattern. Previous studies have identified sexual dimorphism in cheliped size, with males displaying larger major chelipeds compared to females, albeit solely relying on propodus length as a size proxy and focusing solely on the major cheliped. In our study, we meticulously examined 190 specimens of the common European hermit crab Pagurus bernhardus from two collections. We sought to elucidate allometric relationships and assess whether heterometry exhibited sex-based differences when adjusting for body size by using ratios. Our findings revealed that male chelipeds displayed hyperallometric growth relative to females, and all three calculated heterometry indices exhibited significant disparities between the sexes. Consequently, male specimens exhibited larger major and minor chelipeds, even when theoretically matched for body size with females. This phenomenon may be attributed, among other factors, to male-male contests. Should indirect mate selection favor males with larger chelipeds in proportion to their body size, this dynamic could potentiate sexual selection in their favor.

Short-Term Microplastic Exposure Impairs Cognition in Hermit Crabs.

We tested whether acute microplastic exposure impacts information gathering and processing (cognition) in hermit crabs (Pagurus bernhardus). For five days, we kept 51 hermit crabs in tanks containing either polyethylene microspheres (n = 27) or no plastic (n = 24). We then transferred individuals into an intermediate-quality shell and presented them with two vials containing either a better or worse shell. Because touching both shell vials required an equivalent behavioural response, this design controlled for general activity. Plastic-exposed hermit crabs were less likely and slower than controls to touch the better shell vial, instead preferring the worse shell vial. Microplastics, therefore, impaired assessments and decision-making, providing direct evidence of acute microplastic exposure disrupting hermit crab cognition.

Under the influence of light: How light pollution disrupts personality and metabolism in hermit crabs

Anthropogenic disturbances are known to cause significant physiological and behavioural changes in animals and, thus, are the critical focus of numerous studies. Light pollution is an increasingly recognised source of disturbance that has the potential to impact animal physiology and behaviour. Here, we investigate the effect of constant light on a personality trait and metabolic rate in the European hermit crab Pagurus bernhardus. We used Bayesian mixed models to estimate average behavioural change (i.e. sample mean level behavioural plasticity) and between- and within-individual variation in boldness in response to laboratory light. Hermit crabs experiencing constant light were consistently less bold and had a higher metabolic rate than those kept under a standard laboratory light regime (12:12 h light/dark). However, there was no effect of light on individual consistency in behaviour. As boldness is associated with coping with risk, hermit crabs exposed to light pollution at night may experience increased perceived predation risk, adjusting their behaviour to compensate for the increased conspicuousness. However, reduced boldness could lead to lower rates of foraging and this, in combination with elevated metabolic rate, has the potential for a reduction in energy balance.

Sampling biases and reproducibility: experimental design decisions affect behavioural responses in hermit crabs

How important are sampling and experimental design decisions in shaping test subject behaviour under laboratory conditions? We examined the effects of circatidal rhythm, time held in captivity, sampling location (open or covered areas of habitat), acclimation period and water depth on activity and emergence latency in hermit crabs ( Pagurus bernhardus ). We found that subjects held in captivity for 1 month and those collected from the open were faster to emerge from their shells after disturbance compared, respectively, to those tested after 1 day in captivity or collected from beneath cover. We also found that subjects tested after shorter acclimation periods were more active than those tested following longer acclimation periods. Our findings reveal that sampling and study design decisions can have pronounced influences on subject behaviour measured under otherwise common conditions, with potentially important implications for interpretation and reproducibility of findings. As researchers we should take care to explicitly consider how sampling biases and effects arising from our experimental protocols might affect the behavioural responses of test subjects. Doing so can help us make more reasonable generalizations beyond our subject pool, draw better-informed comparisons between studies and achieve greater reproducibility of findings. • Do decisions we routinely make regarding experimental design affect outcomes? • Are animals we test representative of the wider populations we aim to understand? • We asked if subtle design decisions affected behaviour under laboratory conditions. • Time in captivity, acclimation time and location of collection affected behaviour. • We should declare and discuss potential for bias arising from experimental designs.

Does microplastic exposure and sex influence shell selection and motivation in the common European hermit crab, Pagurus bernhardus?

Microplastics (<5 mm) are a threat to marine biodiversity however their effects on animal cognition and behaviour are unclear. We investigated whether microplastic exposure affects shell selection behaviour and motivation in the common European hermit crab, Pagurus bernhardus. Subjects were maintained for 5 days in tanks containing either: polyethylene microplastic spheres (n = 40), or no plastic (n = 40). They were then placed in low-quality shells and presented with an alternative high-quality shell. When they first touched the high-quality shell, the hermit crabs were startled using visual and aural stimuli. We recorded the post-startle latency to re-contact the high-quality shell, quantifying motivation to explore and acquire a better shell. Plastic-exposed females were more likely to select the high-quality shell than control females. As hypothesised, female hermit crabs had longer initial contact latencies, startle durations, and shell entry latencies than males. We also found an interaction effect on shell investigation duration: females from the control treatment spent longer investigating the high-quality shell compared to males. This was absent in the microplastic treatment with females behaving similar to males. This controlled study serves as a starting point to investigate the effects of microplastics and sex differences on behaviour when under predatory threat, and demonstrated sex dependent sensitivity to an environmental pollutant of global concern.

Size specific boldness associated with differences in resource requirements and habitat use: a cross-sectional study in hermit crabs.

Animal personality is often studied within compressed periods of observation that represent narrow windows in comparison to animal lifespans. Although much is known about the relations between repeatable personality traits and cross-situational behavioral plasticity, less is known about how such traits might differ across age classes or life history transitions. We conducted a cross-sectional study of startle response duration in 3 size classes of Pagurus bernhardus, the common European hermit crab. We defined size classes using transitions in the preferred species of gastropod shells that accompany growth, and this change in preference is in turn associated with a transition from intertidal to subtidal habitats. Compared with small- and medium-sized intertidal individuals the larger subtidal hermit crabs behaved cautiously by showing startle responses of greater duration following disturbance. Startle responses were also repeatable within all 3 size classes, confirming the presence of animal personality in intertidal hermit crabs and demonstrating that this pattern is retained within the largest size classes, which have undergone the transition from intertidal to subtidal habitat. Interestingly, there was a trend for the pattern of repeatable startle response durations to increase with size class, with the highest value for repeatability and the greatest range of startle response durations being present within the large subtidal population. The greater range of startle responses indicates that the longer startle response durations in some larger individuals are more likely due to developmental changes with age and habitat use than reflecting selection against the boldest individuals during earlier stages of life.

The angle of attack: rapping technique predicts skill in hermit crab contests

Skill, the ability to perform a challenging behaviour well, has been shown to be an important determinant of success in a variety of contexts, including human sports, animal courtship and, most recently, animal contests. Because skilful movement requires precise motor control, skill is assumed to be underpinned by traits that determine these abilities. However, while these traits determine an individual's potential to perform effective movements (known as technique), this potential may not translate into skilful fighting due to interference from the opponent. Here, we investigated the relationship between technique and skill using the European hermit crab, Pagurus bernhardus . By examining the spatial distribution of shell raps, we found that, on average, technique exhibited during a ‘training’ fight predicted the level of skill displayed in a real contest. However, our results also demonstrated substantial among-individual variation in the direction of change across the two fights, with some individuals exhibiting better technique than skill and others showing the opposite pattern. Finally, we found that winners, but not losers, progressively adapted their targeting of strikes when faced with a fully functional opponent. Our results indicate that skill is a combination of innate technique and the ability to adapt to an opponent's behaviour. • Skill has recently been shown to be a key determinant of fighting success. • Skill is assumed to rely on innate capacities for motor control (technique). • But opponent interference may impede an individual's ability to perform skilfully. • Here we show that innate technique is indicative of the ability to fight skilfully. • We also find that skilful fighting relies on the ability to adapt to your opponent.

Does Microplastic Exposure and Sex Influence Shell Selection and Motivation in the Common European Hermit Crab, Pagurus Bernhardus?

Does Microplastic Exposure and Sex Influence Shell Selection and Motivation in the Common European Hermit Crab, Pagurus Bernhardus?

Animal contests and microplastics: evidence of disrupted behaviour in hermit crabs Pagurus bernhardus.

Microplastics are ubiquitous in global marine systems and may have negative impacts on a vast range of species. Recently, microplastics were shown to impair shell selection assessments in hermit crabs, an essential behaviour for their survival. Hermit crabs also engage in ‘rapping’ contests over shells, based on cognitive assessments of shell quality and opponent fighting ability and, hence, are a useful model species for examining the effects of microplastics on fitness-relevant behaviour in marine systems. Here, we investigated how a 5-day microplastic exposure (25 microplastics/litre) affected the dynamics and outcome of 120 staged hermit crab contests. Using a 2 × 2 factorial design, we examined how microplastics (i.e. presence or absence) and contestant role (i.e. attacker or defender) affected various behavioural variables. Significantly higher raps per bout were needed to evict microplastic-treated defenders when attackers were pre-exposed to control conditions (i.e. no plastic). Also, significantly longer durations of rapping bouts were needed to evict control-treated defenders when attackers were pre-exposed to microplastics. We suggest that microplastics impaired defenders' ability to identify resource holding potential and also affected attackers’ rapping strength and intensity during contests. These impacts on animal contests indicate that microplastics have broader deleterious effects on marine biota than currently recognized.

Diurnal and nocturnal scavenger communities differ at two shallow-water depths in an Irish marine lough

We report on still/video photographic studies in 2018/9 of diurnal and nocturnal benthic scavenging on carrion in shallow water (2 m and 12 m depths) within Lough Hyne (a biodiverse Irish sea lough) using natural light during replicated 6 h daytime deployments and dim red light (630 nm) during 6 h deployments at night. In 2018 at 2 m depth in the North Basin, bait was present throughout day-time deployments, showing little evidence of scavenging; scavenger species' richness and abundance were low. At night, baits disappeared or were skeletonised; they were scavenged by a significantly more abundant and species-rich scavenger guild. At 12 m depth in the same basin, baits were removed or skeletonised during day and night. This confirmed our hypothesis that scavengers avoid well-lit very shallow water during the day, probably to avoid predation. Multivariate analysis of 2018/19 still photo data (12 m depth) revealed pronounced and statistically significant separate clustering of day, night and basin abundance/species data, although overall species' richness values did not differ significantly. These analyses together reflected differences in species’ compositions associated with contrasting sediments, flow regimes and night/day. Nephrops norvegicus, Pagurus bernhardus and Crangon crangon were only found in the low flow rate North Basin; Homarus gammarus, Trigla sp., Callionymus lyra, Agonus, Tritia reticulata and Marthasterias glacialis were only found in the high flow rate South Basin. Most scavenger species foraged in both day and night (though in different proportions). However, prawns (Palaemon serratus) only appeared at night. Small mobile scavenging fish, small crabs and prawns arrived at baits within seconds to minutes, as did locally-abundant slow movers (e.g. anemones (Anthopleura ballii), whelks (T. reticulata)). These times are shorter than recorded in earlier studies in deeper water. Larger crustaceans (e.g. Cancer pagurus, H. gammarus) took tens of minutes to hours before arrival; similar times have previously been recorded in deeper water. Large crustacean scavengers (C. pagurus, Maja squinado, H. gammarus) took substantial quantities of bait during long feeding bouts, but catsharks (Scyliorhinus canicula) often took similar quantities in a few seconds. All of the dominant scavenger species are broad-spectrum omnivores; only one obligate scavenger species (Tritia reticulata) was present (only in South Basin) and consumed negligible quantities of bait.

Plastic additive oleamide elicits hyperactivity in hermit crabs

Numerous studies have estimated the abundance of plastics in our oceans and warned of its threat to wildlife. However, mechanisms underlying its attractiveness to marine life remain unclear. Though visual similarities to food sources have been suggested, recent studies show that biofouled plastics release dimethyl sulfide which marine fauna mistake for food whilst foraging. Our study shows that the plastic additive oleamide (9-octadecenamide) attracts hermit crabs (Pagurus bernhardus). Respiration rate increases significantly in response to low concentrations of oleamide, and hermit crabs show a behavioral attraction comparable to their response to the feeding stimulant betaine. Oleamide has a striking resemblance to the necromone oleic acid, a chemical released by arthropods during decomposition. As scavengers, hermit crabs may misidentify oleamide as a food source, creating an olfactory trap. As such, our short communication demonstrates that additive leaching may play a significant role in the attraction of marine life to plastic.

Ocean Acidification Amplifies the Olfactory Response to 2-Phenylethylamine: Altered Cue Reception as a Mechanistic Pathway?

With carbon dioxide (CO2) levels rising dramatically, climate change threatens marine environments. Due to increasing CO2 concentrations in the ocean, pH levels are expected to drop by 0.4 units by the end of the century. There is an urgent need to understand the impact of ocean acidification on chemical-ecological processes. To date, the extent and mechanisms by which the decreasing ocean pH influences chemical communication are unclear. Combining behaviour assays with computational chemistry, we explore the function of the predator related cue 2-phenylethylamine (PEA) for hermit crabs (Pagurus bernhardus) in current and end-of-the-century oceanic pH. Living in intertidal environments, hermit crabs face large pH fluctuations in their current habitat in addition to climate-change related ocean acidification. We demonstrate that the dietary predator cue PEA for mammals and sea lampreys is an attractant for hermit crabs, with the potency of the cue increasing with decreasing pH levels. In order to explain this increased potency, we assess changes to PEA’s conformational and charge-related properties as one potential mechanistic pathway. Using quantum chemical calculations validated by NMR spectroscopy, we characterise the different protonation states of PEA in water. We show how protonation of PEA could affect receptor-ligand binding, using a possible model receptor for PEA (human TAAR1). Investigating potential mechanisms of pH-dependent effects on olfactory perception of PEA and the respective behavioural response, our study advances the understanding of how ocean acidification interferes with the sense of smell and thereby might impact essential ecological interactions in marine ecosystems.

Context-dependent use of visual cues in the shell selection behaviour of the hermit crab Pagurus bernhardus

Animals avoid predator attack in different ways; some carry defensive structures to reduce predation, with the classic example being hermit crabs and their use of a mollusc shell as a portable refugium. During shell selection, various shell characteristics are investigated by the crab to determine their suitability. Here we consider the role of visual cues. Previous research suggests that some hermit crabs are more likely to initially choose a conspicuous shell but also to move to backgrounds against which they are less conspicuous, suggesting a short-term/long-term trade-off. Across experiments in which we manipulated shell and background colour, we show initially that Pagurus bernhardus prefer black shells over white but this preference was lost in the absence of visual cues. We then show that the strength of preference was dependent on background colour. We repeated this last experiment with red and yellow shells against red or yellow backgrounds to investigate whether this preference extended to chromatic hues. A preference for darker (red) shells was expressed, but preference alteration with background was not observed. P. bernhardus therefore discriminate between shells in terms of shell and background colour, and discrimination may be rooted in a preference for darker shaded shells.

Microplastic exposure increases predictability of predator avoidance strategies in hermit crabs

The contamination of natural systems with plastic debris has become one of the most pressing global environmental issues. Microplastics (MPs) are of particular concern because their ubiquity and small size make them available for ingestion by a range of aquatic biota. MP exposure studies are hence proliferating rapidly but are typically limited to the analyses of population-level responses in toxicity endpoints across treatments. Potential contaminant-induced alterations in behavioural patterns, however, could manifest on numerous levels of variation: at the population-level, between individuals and within individuals. Here, we used repeated measures on startle response durations – a risk-avoidance mechanism – in European hermit crabs, Pagurus bernhardus, to measure behavioural responses to MP exposure across multiple levels of variation. We found that MP exposure led to a significant decrease of startle duration at the population-level as well as a reduction of intra-individual variation. In other words, crabs became less risk averse on average and their behaviour became more predictable with increasing MP concentrations. Collectively, our findings indicate that MP pollution might increase susceptibility to predation in hermit crabs.

Evolutionary loss of threat display in more social species: phylogenetic comparisons, natural interactions in the wild, and experiments with models

Abstract Fitness can be increased dramatically by communication. So why, given the benefits of communication, would displays ever be completely lost evolutionarily? Threat displays, in particular, are relatively cheap to produce and are precursors of attack, so should be especially hard for both senders and receivers to lose completely. Here we explore an evolutionary transition in sociality, testing whether complete evolutionary loss of threat display has occurred in ‘more social’ hermit crab species, which interact more frequently with conspecifics. First, we synthesised literature and observations on the presence versus absence of threat display across hermit crab species, mapping this information onto a phylogenetic tree. We found that all ‘less social’ species — marine and terrestrial — produce threat displays, consistent with threat display being the ancestral state. But ‘more social’ terrestrial species, which are highly derived, do not produce a threat display, suggesting an evolutionary loss. Next, we contrasted natural interactions in the wild within a less social species (Pagurus bernhardus) versus within a more social species (Coenobita compressus), finding that the less social species, despite a lower rate of social encounter, had a higher rate of display per encounter (24%). In contrast, the more social species’ rate of display per encounter was negligible (&lt;1%), effectively indicating a loss in production. Finally, we experimentally reanimated threat display in the more social species, using postured models to test whether receivers retained any responsiveness to threat display. Starkly, receivers were not deterred by threat display, showing equal responsiveness across both threat and non-threat models, regardless of whether the models were stationary or dynamically moving. Our results thus reveal a case of complete collapse of communication involving threat display, implicating the social environment in this loss. In more social species, an extreme dependence on conspecific-derived shells likely drove a ‘desperado effect’, with threat displays being lost because they could not stop others from pursuing these valuable resources.

First insights into the phylogeography and demographic history of the common hermit crab Pagurus bernhardus (Linnaeus, 1758) (Decapoda: Anomura: Paguridae) across the Eastern Atlantic and North Sea

AbstractThe common hermit crab Pagurus bernhardus (Linnaeus, 1758) is an abundant and ecologically important benthic crustacean in the northeastern Atlantic Ocean. While this species has been intensively studied in terms of its ecology, physiology, behavior, and larval development, knowledge about its population structure and demographic history is still lacking. We examined, for the first time, the genetic variability of P. bernhardus by analyzing two mitochondrial gene fragments (CO1 and 16S) from more than 150 specimens collected from various locations from the Iberian Peninsula to Norway. Our results provide evidence for a significant genetic structure according to the sampled regions for both genetic markers. Furthermore, a comprehensive demographic history reconstruction, mainly based on neutrality tests and a Bayesian Skyline Plot (CO1), revealed a recent demographic expansion of P. bernhardus that preceded the Last Glacial Maximum. Such pattern of retrieved demographic trend could have been likely a successive process to historical contraction of the species into potential climate refugia within the surveyed geographic spectrum.

Microplastics disrupt hermit crab shell selection.

Microplastics (plastics < 5 mm) are a potential threat to marine biodiversity. However, the effects of microplastic pollution on animal behaviour and cognition are poorly understood. We used shell selection in common European hermit crabs (Pagurus bernhardus) as a model to test whether microplastic exposure impacts the essential survival behaviours of contacting, investigating and entering an optimal shell. We kept 64 female hermit crabs in tanks containing either polyethylene spheres (n = 35) or no plastic (n = 29) for 5 days. We then transferred subjects into suboptimal shells and placed them in an observation tank with an optimal alternative shell. Plastic-exposed hermit crabs showed impaired shell selection: they were less likely than controls to contact optimal shells or enter them. They also took longer to contact and enter the optimal shell. Plastic exposure did not affect time spent investigating the optimal shell. These results indicate that microplastics impair cognition (information-gathering and processing), disrupting an essential survival behaviour in hermit crabs.

The status of Clibanarius erythropus after a recent range expansion to Great Britain, with the highest latitude recording of a gravid individual

BackgroundIn 2016, the range of the hermit crab Clibanarius erythropus expanded to South West Britain for the second time. C. erythropus primarily lives in the Mediterranean and the Atlantic coast of Europe from the Bay of Biscay to Morocco. The species has now been recorded on both the north and south coast of the South West peninsula of the UK from Newtrain Bay, on the north coast of Cornwall, to Wembury, on the south coast of Devon. It is unknown if the crab’s reappearance in the UK has been caused by a one-off colonisation event or by a continued influx of larvae.ResultsThe population in the UK is made up of individual within a narrow size bracket, indicating a single colonisation event took place, and that the population is an ageing one. However, we also report the highest latitude recording of a gravid individual for the species.ConclusionA lack of gravid individuals was suggested to be why the species was unable to sustain its presence in the UK following a previous colonisation in 1960. This discovery hints that rising water temperatures may allow C. erythropus and other warm-water species to expand and sustain themselves in the UK. We also found crossover in shell utilisation between C. erythropus and the native hermit crab Pagurus bernhardus, suggesting that competition might occur between the two species.