Antifouling adaptations of caridean shrimps: Cleaning of the antennal flagellum and general body grooming

Structural specializations of chelipeds used by caridean shrimp in two kinds of grooming activity are described. In general body grooming, the chelipeds, and in some species, the last walking legs, nip, pick or brush material from the exoskeleton. When the cleaning chelipeds are the second pair, the carpal segment is multisegmented, increasing distal flexibility which aids in grooming. Tufts of compound setae and setal chela locks are characteristic of cleaning chelae. In representatives from 13 of 15 caridean families surveyed, brushes of serrate setae surround the carpal-propodal joint of the first cheliped. This setal structure is used in the specific task of cleaning the chemotactile antennal flagellum. Cleaning brushes on the last walking legs of some species are involved in general body cleaning. Experiments on Heptacarpus pictus showed that when the cleaning chelipeds were ablated, body parts became fouled with epizoites and particulate debris in experimental shrimps, while control shrimps showed little fouling. Suggestions on the adaptive role of general body cleaning in these natant animals are discussed. A survey of cleaning characters in representatives from 15 caridean families suggest that such characters are rather constant within a family. A possible correlation between the taxonomic success of a family and the degree of development of general body cleaning is suggested.     

Effects of disc and arm loss on regeneration byMicrophiopholis gracillima (Echinodermata: Ophiuroidea) in nutrient-free seawater

Clibanarius longitarsus (De Haan), a hermit crab, feeds by means of both micro- and macrofeeding. Microfeeding is of two types: filter feeding and deposit feeding. In macrofeeding, the animal depends mainly on green algae, barnacles and some worms, etc. In filter feeding, the hermit crab uses its paired antennules for trapping microorganisms drawn into the water current created by the second and third maxillipeds; the antennae do not play any role in filter feeding. In deposit feeding, the hermit crab uses its chelae as well as pereiopods for toughing and obtaining detritus food material. In macrofeeding, the organism employs sharp chelae to collect small pieces of muscle from barnacles and then transfer them to the inner mouth parts. In algal feeding, the chelae as well as maxillipeds help in collecting and moving food material towards the mouth. In this investigation functional organisation ofC. longitarsus mouth parts was studied in detail with reference to the various feeding mechanisms, in specimens collected from the intertidal region of Bheemunipatnam, Andra Pradesh, India, in 1988 and 1989.     

Structure and function of the third maxillipeds of the banana prawn Penaeus merguiensis

The functions of the third maxilliped of Penaeus merguiensis de Man are described. It has a 6-segmented endopodite which is used in feeding, grooming and possible pheromone reception. In feeding, large pieces of food are gripped by the stout spines on inner borders of the ischia which hold them to the mouth so that particles can be torn off and ingested. All the distal segments have long setae used in grooming chelate pereiopods and the antennules. In mature males there is a tuft of about 300 slender setae at the end of the propus, but its function remains obscure.     

Locomotion,feeding, grooming and the behavioural responses to gravity,light and hydrostatic pressure in the stage I zoea larvae of Ebalia tuberosa (Crustacea: Decapoda: Leucosiidae)

The stage I zoeae of Ebalia tuberosa swam by sculling with the exopodites of the 1st and 2nd maxillipeds and flexed the abdomen to brake or change direction. The larvae gained depth by stopping all natatory movements and sinking passively at rates of 6 mm s^-1. The zoeae refused both living and dead nauplii of Artemia spp., as well as two species of diatoms, but fed readily on detritic material on the bottom which they scooped up using the endopodites of the maxillipeds and pressed against the mouthparts using the telson. The setae on the posterior border of the telson were used for grooming the maxillipeds and the anterior mouthparts. Day-old stage I zoeae were negatively geotactic, positively phototactic and responded to pressure increases by swimming upwards and by high barokinesis. By the third day some larvae had become positively geotactic but were photopositive, and the majority responded to pressure increases as in the day-old larvae. Five-day old larvae were still photopositive but the majority had become positively geotactic and fewer himbers responded to pressure. Seven-day old larvae failed to respond to any of the stimuli used and assumed a predominantly benthic lifestyle. It is suggested that this anomalous behaviour is related to the dispersal of the larvae and to the specialized habitat requirements of the adults while the rather unusual morphology of the larvae is related to their feeding behaviour and semi-benthic lifestyle.     

Morphology of grooming limbs in species of Petrolisthes and Pachycheles (Crustacea: Decapoda: Anomura: Porcellanidae): a scanning electron microscopy study

The morphology of the grooming limbs, the 5th pair of pereiopods, was studied by scanning electron microscopy in six species of porcellanid crabs, Petrolisthes cabrilloi, P. cinctipes, P. armatus, P. galathinus, Pachycheles monilifer, and Pachycheles rudis, and their function was inferred by comparison with findings from previous studies. Grooming limb morphology was almost identical among the four Petrolisthes species and differed little compared to that of the two Pachycheles species. The 5th pereiopods bore a basal tuft of mechanoreceptive setae, three different types of grooming setae armed with setules or denticles, two types of smooth sensilla for location and identification of fouling objects, and a terminal, toothed chela for picking firmly attached objects off the gills and body. The grooming limb was extremely flexible and could reach most parts of the body, including the gill chamber on the opposite side. The grooming limb morphology in Petrolisthes cabrilloi is consistent with its wellknown effectiveness in preventing parasitism by the rhizocephalan Lernaeodiscus porcellanae. Grooming setae remove recently attached cyprids, while the chela can grip and remove the much smaller, firmly attached kentrogons. Porcellanid crabs not known to host rhizocephalans, however, had grooming limbs almost identical to those of Petrolisthes cabrilloi despite their previously demonstrated failure to prevent settlement and infestation by L. porcellanae larvae. The effectiveness of P. cabrilloi in removing kentrogons, therefore, seems also to depend on behavioral adaptations whereby this species recognizes the parasite larvae as high-threat objects.     

Microbial activities as a function of water depth in the Ligurian Sea: an autoradiographic study

Fourteen species of sergestid shrimps were collected in the Sargasso Sea between the surface and 1500 m near Bermuda on 4 cruises. The vertical distribution and feeding activity of the most abundant species are discussed in relation to interspecific competition and the adaptive significance of vertical migration. Each species lives within a narrow depth range and exhibits a diel vertical migration. Sergestes splendens migrated as much as 825 m, while S. japonicus migrated less than 100 m. Neither the seasonal nor permanent thermocline influenced the migration range. The only species which occurred together both day and night were S. pectinatus with S. vigilax and S. pectinatus with S. sargassi. Morphological differences in the third maxillipeds of these species suggest differences in feeding. Although most species eat a variety of organisms, the foreguts of S. grandis, S. corniculum, and S. splendens contained euphausiids more often than those of other species, and S. grandis and S. robustus fed more frequently on fishes. In contrast, S. japonicus appears to feed on detritus. Food was found in the foreguts of most species less frequently during the day than night, but no species fed only at night. S. sargassi and S. pectinatus fed equally day and night.     

Cleaning symbiosis in an obligate goby–shrimp association

Shrimps from the genus Alpheidae had never been considered as a cleaner organism. In the present study, we demonstrate for the first time, Alpheus rapax engaging in cleaning symbiosis with its gobiid fish associate Myersina macrostoma. Within 450 min of observation time, 9 instances totalling 546 s of cleaning behaviour were recorded. Cleaning behaviour was always preceded by physical contact between the shrimps and their goby associates. The shrimps initiated all cleaning incidents, but these were always terminated by the gobies. Cleaning sessions were observed to occur mostly in the tail region (60.8 %) and followed by the head region (26.2 %). In one instance, a shrimp was observed to clean the gills of its goby associate. The gobies appear to exert some control as to where they were being cleaned by repositioning themselves during a cleaning session.     

Intraspecific behaviors and major cheliped sexual dimorphism in three congeneric callianassid shrimp

Decapod callianassid shrimps are usually solitary occupants of their burrows. They are known to show distinct sexual dimorphism of the major cheliped, which is used as a weapon for intraspecific fighting. Three species of Nihonotrypaea occur in an estuary in southern Japan; they consist of two tidal flat species (N. harmandi; N. japonica) and one boulder beach species (N. petalura), with maximum population densities of 1,400, 340, and 12 m^–2, respectively. The major cheliped size and total length of shrimp were recorded from each population. The degrees of major cheliped sexual dimorphism were ordered as N. harmandi >N. japonica >N. petalura. In the laboratory, intra- and intersexual behaviors at forced encounters between two shrimps were recorded, for the former behavior throughout the year and the latter in the non-breeding season. At their intersected burrows, the shrimps either fought or retreated or filled the burrow crack. Males interacted aggressively with each other, with the intensity being N. petalura >N. harmandi N. japonica. Females of the tidal flat species were non-aggressive, while those of N. petalura were as aggressive with each other as were males. Intersexually, males of all species and females of N. petalura were much less aggressive than intrasexually. In N. petalura only, burrow-sharing behavior between sexes occasionally occurred. The interspecific difference in these behaviors is in parallel with the degree of major cheliped sexual dimorphism. Different intensities of intrasexual competition for mates could have been imposed by the different population densities of these species.Communicated by T. Ikeda, Hakodate     

Burrow structure, burrowing and feeding behaviour of Corallianassa longiventris and Pestarella tyrrhena (Crustacea, Thalassinidea, Callianassidae)

The behaviour of the Caribbean Corallianassa longiventris and the Mediterranean Pestarella tyrrhena, two burrowing thalassinideans, was studied in situ and in laboratory aquaria. Burrows of C. longiventris were closed most of the time; they consist of a deep U (down to 1.5 m) with upper and deeper chambers, some of them filled with macrophyte debris. The burrows of P. tyrrhena reached down to a maximum depth of 54 cm and consisted of a shallow U with a mound and a funnel, and a spiral shaft from which several, often debris-filled chambers branched off. The appearance of C. longiventris at the sediment surface to collect debris is strongly triggered by wave swell or odours from plant and animal juices; its burrows are opened within 10 min. The surface activity of P. tyrrhena was relatively less frequent and less predictable. Inside the burrows, both species exhibited different patterns of time allocated to 25 defined behavioural states. After being offered seagrass debris, P. tyrrhena spent relatively less time manipulating this debris, but it handled sediment more often than C. longiventris. During frequent mining events, both species showed sediment-sorting behaviour, which brought a parcel of sediment in close contact with the mouthparts; some of this sediment may be ingested because the fecal rods produced by both shrimps contain very fine sediment particles. Seagrass debris is irregularly tended by P. tyrrhena after its introduction into the chambers. Such material ultimately becomes buried. Corallianassa longiventris frequently returns to its debris chambers to pick up pieces of seagrass, which are subsequently cut with the chelae or ripped with the third maxilliped and then transported to another empty chamber nearby. Pieces become smaller with time and show curved cutting edges and bite marks. After 100 to 140 days, 2 to 6 g(dw) seagrass debris are consumed in this manner by individuals of this species. The debris-related behaviour of P. tyrrhena probably enriches the sediment around the burrow for stochastic encounters during later mining events. Such an indirect benefit may also be effective on a population level because other individuals may also encounter this buried nutrient source. Electronic Supplementary Material Supplementary material is available for this article at and is accessible for authorized users.     

Cleaner-client interactions on a Caribbean reef: influence of correlates of parasitism

We investigated the influence of known correlates of parasitism, namely fish density, body size and social behaviour, on three highly variable aspects of the interactions between cleaning gobies (Elacatinus spp.) and their clients, on a Barbadian coral reef. We specifically considered (1) variability in client visit rate to cleaning stations, (2) cleaning goby preference for specific clients and (3) variation in the time spent cleaning by cleaners. Using phylogenetically independent contrasts, we found that client species that were abundant on the reef visited cleaning stations more often than rarer client species. This could be due to the positive relationship between ectoparasite load and client density, or alternatively may simply reflect the frequency of contact between cleaners and clients. Cleaning gobies spent more time cleaning large-bodied clients, which usually have higher ectoparasite loads, although cleaning goby preference for clients was influenced by none of the correlates of client parasitism. Overall, factors assumed to correlate with ectoparasite load had a limited influence on the variability observed in the interactions between cleaning gobies and their clients. Received: 27 October 1999 / Received in revised form: 11 January 2000 / Accepted: 24 January 2000     

Waterborne chemical compounds in tropical macroalgae: positive and negative cues for larval settlement

Settlement sites of marine invertebrate larvae are frequently influenced by positive or negative cues, many of which are chemical in nature. Following from the observation that many shallow-water, Hawai'ian marine macroalgae are free of fouling by sessile invertebrates, we predicted that the algae are chemically protected and dependent on either surface-bound or continuously released soluble compounds to deter settling invertebrate larvae. To address the importance of waterborne algal compounds, we experimentally determined whether larvae of two of Hawai'i's dominant hard-surface fouling organisms, the polychaete tube worm Hydroides elegans and the bryozoan Bugula neritina, would settle in the presence of waters conditioned by 12 species of common Hawai'ian macroalgae (representing the Phaeophyta, Chlorophyta, Rhodophyta and Cyanophyta). The results included a full spectrum of biological responses by each larval species to waterborne algal compounds. Larval responses to conditioned water were consistent for each algal species, but the outcomes were not predictable based on the taxonomic relationships of the algae. For example, among the species of Phaeophyta examined, different conditioned waters were: (1) toxic, (2) inhibited settlement, (3) simulated settlement, or (4) had no effect, compared to larvae in control dishes containing filtered seawater. Additionally, larval responses to aged (24 h) conditioned waters could not be predicted from the results of assays run with conditioned waters utilized immediately after preparation. Finally, settlement by larvae of one species did not predict outcomes of tests for the other species. Four of 12 shallow-reef Hawai'ian macroalgae tested released compounds into surrounding waters that immediately killed or inhibited settlement by both H. elegans and B. neritina (toxic: Dictyota sandvicensis; inhibitory: Halimeda discoidea, Sphacelaria tribuloides, Ulva reticulata); the remaining 8 algal species prevented settlement by one of these fouling organisms but for the other had no effect or, in some cases, even stimulated settlement     

Mating behaviour of male Carcinus maenas in relation to a putative sex pheromone: behavioural changes in response to antennule restriction

Temporary suspension of the receptivity of the male antennules confirmed these organs as the site of putative pheromone detection in the crab Carcinus maenas. Comparative analysis of male performance in individual components of sexual behaviour failed to identify any difference between male crabs with antennules restricted and others without, when individuals from each group were placed in contact with receptive females. However, even though pheromone perception by males was not a prerequisite for the initiation of sexual behaviour, in its absence the control of normal sequence and duration of pairing behaviour was disrupted.     

<Emphasis Type="Italic">Octopus insularis</Emphasis> (Octopodidae), evidences of a specialized predator and a time-minimizing hunter

Shallow-water octopuses have been reported as major predators of motile species in benthonic marine communities, capturing their prey by different foraging techniques. This study assessed for the first time the feeding ecology, foraging behavior, and defensive strategy during foraging, including the use of body patterns, to construct a general octopus foraging strategy in a shallow water-reef system. Octopus insularis was studied in situ using visual observations and video recordings. The diet included at least 55 species of crustaceans (70%), bivalves (17.5%), and gastropods (12.5%); however, only four species accounted for half of the occurrences: the small crabs Pitho sp. (26.8%) and Mithrax forceps (23.9%), the bivalve Lima lima (5.3%), and the gastropod Pisania pusio (4.9%). Poke and crawl were most frequent foraging behaviors observed in the video recordings. The foraging behaviors were associated with environmental variables and octopus body size. The sequences of foraging behavior showed characteristics of a tactile saltatory searching predator, as well as a visual opportunist. Body patterns showed a relationship with foraging behavior, habitat variables, and octopus body size. Mottle was the most frequent pattern, especially during poke and crawl, in shallower depths. Dorsal light–ventral blue green was more frequent during swimming at mid-water, and Blotch was the normal pattern during web-over by large animals. The large proportion of two species of small crabs in den remains, the intense search for food during short hunting trips, and the intense use of cryptic body patterns during foraging trips, suggest that this species is a ‘time-minimizing’ forager instead of a ‘rate-maximizer’.     

A new method to determine in situ growth rates of decapod shrimp: a case study with brown shrimp Crangon crangon

Shrimps are economically and ecologically very important, yet a lack of ageing techniques and hence unknown growth rates often impairs analytical assessments and management. A new method for the determination of in situ growth rates of shrimps is presented, based on dry weight condition. Since this index oscillates from low values directly after moult to highest values prior to moult in constantly feeding shrimp, the lowest observed pre-moult condition followed by a moult was introduced as a reference value to separate growing and starving individuals in field data. Experiments with Crangon crangon confirmed that (1) post-moult condition varies in a narrow physiologically optimal range, regardless of recent growth increments, and (2) dry weight condition prior to moult is closely related to the subsequent length increment. The method was applied to estimate growth increments from in situ dry weight condition data of C. crangon. The new method can easily be applied to other related species, since the required data can be obtained from very simple short-term experiments.     

The near-bottom shrimp faunas (Decapoda: Natantia) at two abyssal sites in the Northeast Atlantic Ocean

Bottom and near-bottom decapod shrimp communities from two northeast Atlantic abyssal sites (ca. 4 040 and 5 440m) were examined in 1984 and 1985. In both cases, an increase in abundance was observed in the bottom 90 m of the water column, with the largest numbers of shrimps occurring closest to the sediment surface (10 to 25 m off the bottom). The benthopelagic communities were composed of species drawn from both pelagic and benthic habitats rather than being specific and discrete. Hymenodora glacialis was the dominant species at the shallower site but it was absent from the near-bottom samples at the deeper one. H. acanthitelsonis, however, occurred at both sites. Several new depth records have been established, and there are two recordings of species previously unknown to the eastern Atlantic basin. Vertical migration and differences in modes of reproduction are discussed.     

Importance of ectoparasites and mucus in cleaning interactions in the Mediterranean cleaner wrasse Symphodus melanocercus

In fish cleaning associations, the net benefits gained by clients and cleaners from cleaning have still not been clearly evaluated. In particular, the role of ectoparasitism and the importance of client mucus characteristics remain unclear for most cleaner fish species. This paper investigates the cleaning behaviour of the Mediterranean cleaner wrasse Symphodus melanocercus, based on observations, cleaner gut contents, client ectoparasites and mucus characteristics. We showed that this fish is a specialised cleaner fish, similar to some other tropical cleaner species. Gnathiid isopod larvae and caligid copepods represented a large proportion of the items preyed on by S. melanocercus. Although their feeding activity was related to their client ectoparasite load, it was also significantly linked to client mucus load, which would indicate that the cleaning behaviour of S. melanocercus is not purely altruistic. Finally, as client visit to cleaning stations is related to their ectoparasitism, we propose that ectoparasite removal is likely to be a benefit for the client fishes of S. melanocercus. Received: 28 July 2000 / Accepted: 8 November 2000     

Parasitism as a determinant of community structure on intertidal flats

The burrowing and movement ability of the New Zealand cockle Austrovenus stutchburyi is reduced when infected by echinostome trematodes. Previous experimental evidence from a single site suggests that this parasite-induced behavioural change of a key bivalve can affect the structure of the surrounding benthic community. By using multiple regression analyses on data collected from 17 intertidal flats, we here show that cockle parasitism is associated with macrozoobenthic community structure on a larger spatial scale. Regressions were performed for animal abundance, biomass, species diversity and species richness separately, entering cockle parasitism (infection intensity), presence/absence of ghost shrimps (Callianassa filholi), cockle density, primary producer abundance and organic content, particle size, sorting coefficient and gravel content of the substrate as predictors. Next to ghost shrimps, cockle parasitism was the best predictor of animal abundance by affecting (mainly positively) 8 of the 49 most widespread species significantly. Cockle parasitism was also associated with the biomass of anthozoans (positively), nemerteans (negatively) and bivalves (positively), whereas overall animal biomass was positively related to the sorting coefficient of the substrate. Species diversity was positively associated with cockle parasitism and gravel content of the substrate. Species richness was significantly associated with cockle parasitism (positively), ghost shrimps (negatively) and abundance of primary producers (positively) in combination. The impact of cockle parasitism on benthic community structure is believed governed directly or indirectly by (1) reduced sediment disturbance, (2) increased surface structural complexity and (3) availability of larval trematodes as an additional food source.     

Hermaphroditism in brown shrimp: lessons from field data and modelling

This study was undertaken to further clarify whether the brown shrimp, Crangon crangon (Linnaeus 1758), is a gonochorist, a facultative or an obligate hermaphrodite. Juvenile shrimps were sampled from intertidal habitats along the German Wadden Sea coast with a push net and from a power plant water inlet to quantify the share of primary females. Length-based sex ratios were determined for about 27,000 individuals using external characteristics. Observed sex ratios were mainly female-biased, and also large males occurred regularly in the catch. This indicates that sex at hatch is not male as would be characteristic for an obligate protandric hermaphrodite and that not all male shrimps change sex. A cohort-based computer simulation, including sex-specific growth rates, mortality and seasonally varying recruitment, generated sex ratios comparable to the field. The observed decline in the proportion of males with increasing size can be explained solely by faster growth of females without involving hermaphroditism. Based on temperature-dependent growth and moult rates as well as length-specific numbers of eggs per female, the potential egg production of primary and secondary females was modelled, yielding contributions of secondary females of <1%. Sex change in C. crangon has previously been observed and may be interpreted as an evolutionary relict of this species having evolved in a habitat characterized by lower population densities, lower predation levels and increased longevity compared to today’s living conditions in North Sea coastal waters.     

Color patterns of the shrimps Heptacarpus pictus and H. paludicola (Caridea: Hippolytidae)

Color patterns of the shallow-water shrimps Heptacarpus pictus and H. paludicola are formed by chromatosomes (usually termed chromatophores) located beneath the translucent exoskeleton. Development of color patterns is related to size (age) and sex. The color expressed is determined by the chromatosome pigment dispersion, arrangement, and density. In populations with well-developed coloration (H. pictus from Cayucos, California, 1976–1978, H. paludicola from Argyle Channel, San Juan Island, Washington, June–July, 1978), prominent coloration was a characteristic of maturing females, breeding females, and some of the larger males. In the Morro Bay, California, population of H. paludicola (sampled 1976–1978), color patterns were poorly developed except in a few large females. In both species, most shrimp lose color at night because of pigment retraction in certain chromatosomes. In both species, there are 5 basic morphs: 1 transparent and 4 colored morphs. In the colored morphs, the color patterns are composed of bands, stripes, and spots which appear to disrupt the body outline. Each color morph also has a common environmental color in its color pattern, e.g the green of green algae, the whites and pinks of dead and living coralline algae, and various shades of tidepool litter. These shrimps are apparently under heavy predation pressure by fish, and it is suggested that the color patterns are camouflage against such visually-hunting predators.     

The kin recognition system of carpenter ants (Camponotus spp.)

Summary Hamilton's (1964) hypothesis linking haplodiploidy and eusociality in the Hymenoptera could be reconciled with the occurrence of polygyny and multiple insemination if workers are able to distinguish full (3/4 related) sisters from other familiar matri- and patrilines within the colony, and direct altruistic behavior toward them preferentially. We examined this possibility in small genetically mixed nests of the carpenter ant Camponotus floridanus, formed by the transfer of worker pupae from two unrelated source colonies. In 120 h of observation on 12 queenright and 12 queenless nests, more than 15,000 behavioral interactions were recorded. Workers antennated familiar nonkin significantly more frequently than familiar sisters. However, they failed to discriminate consistently between kin and non-kin in food exchanges and grooming. Aggressive behavior was occasionally observed in some queenless nests, but almost never in the presence of a queen. When aggression did occur, it was directed significantly more often toward non-kin. Though related adult workers did not cooperate preferentially, the biases in antennation and aggression do indicate an ability to discriminate familiar kin from familiar nonkin, which may be employed in other contexts such as the rearing of reproductive brood.