Brooding sea anemones (Cnidaria: Anthozoa: Actiniaria): paragons of diversity in mode,morphology, and maternity

Brooding has been reported in at least 57 species of sea anemone. More than three quarters (44/57) of the species that are known to brood have been described since the last comprehensive treatment of brooding in this lineage. Different authors focusing on different taxonomic groups within sea anemones over the last 115 years have collectively produced an imprecise and inconsistent set of terminology with respect to brooding in general and to the variety of conditions of brooding in particular. In this review, I characterize brooding as a behavior in which offspring are retained by the adult to at least the juvenile stage, in contrast with the more common release of eggs, embryos, or larvae. Brooding occurs in two primary modes, internal and external, in which offspring may be produced via sexual or asexual means. I categorize structures associated with external brooding in three types: pits, chambers, and grooves. Early inferences that external brooding has a primarily bipolar distribution continue to be supported with current data, but it is doubtful that small size and simultaneous hermaphroditism are correlated with brooding in sea anemones. Finally, I identify open questions about brooding in sea anemones and suggest future lines of research that will broaden our understanding of this phenomenon.     

Evidence of fostering in an internally brooding sea anemone

Evidence of alloparental care during the incubation stage has largely been demonstrated for species that incubate their offspring externally in a nest. Alloparental care in these species generally consists of the rearing of mixed broods which contain a low proportion of “foreign” young alongside the host's own offspring. However, many animals, including sea anemones, incubate offspring either on or within their bodies. The beadlet anemone Actinia equina incubate their young internally, and as many sea anemones are capable of reproducing both sexually and asexually, the origin of these internally brooded young has been the subject of much debate. While genetically identical young are brooded internally under the juvenile stage, it is thought that those produced sexually are released as larvae into the water and must return to the gastric cavity of an adult in order for metamorphosis to occur. As the likelihood of a planula larva finding its way back to its parent is slim, this suggests that alloparental care may play a role in the survival of juveniles in this species, a hypothesis first suggested a century ago but rarely tested. Here, using highly polymorphic microsatellite markers, we find evidence of alloparental care in A. equina. Our results indicate that while a high proportion of juveniles were genetically identical to their brooding adult, the remaining juveniles showed stark genetic differences to their brooding adult. These juveniles shared far fewer alleles with their “parent” than expected under sexual reproduction, indicating that they were not the adult's offspring. Furthermore, we found variation in the genetic composition of broods, which consisted either of (a) entirely genetically identical individuals, (b) a mix of unique individuals and clonemates or (c) entirely unique individuals, that is no shared genotype. Our results thus indicate that adult A. equina tolerate the presence of non-offspring within their gastric cavity and furthermore that they may incubate entirely “foreign” broods.     

The Social Structure of Inachus phalangium,a Spider Crab Associated with the Sea Anemone

The behaviour of the spider crab Inachus phalangium (Fabricius, 1775), which lives in association with the sea anemone Anemonia sulcata (Pennant), was studied in the field. The crab was found in the littoral zone of the Mediterranean Sea near Banyuls sur Mer, France, in the whole depth range studied (0.5–25 m). The crabs had a long-lasting association with individual Anemonia sulcata, occasionally with Aiptasia mutabilis. Most crabs were found in association with the same anemone for several days, some crabs were found in association with the same anemone for longer than one month. In the areas studied, on average 65 Inachus phalangium were found on 100 anemones. Crabs released in the vicinity of anemones moved towards them and entered them. Inachus phalangium could walk between the tentacles of Anemonia sulcata and Aiptasia mutabilis without eliciting feeding reactions of the anemone. The crabs left the anemones for moulting. After moulting masking material was removed from the exuvia and used again. The animals returned into an anemone while still soft. Material used for masking, usually algae, could be picked off the body and eaten. Masking material may be a food reservoir in addition to providing camouflage. Anemones were left only during night-time. The crabs left their anemone to moult, to feed in the vicinity, fleeing from larger conspecifics, and to migrate to a different anemone. Outside the anemone's protection Inachus was eaten by several species of fish. Individuals appeared to avoid each other. 57% of all animals were found alone on an anemone. Large males and females were more frequently found alone than were small males and females. Fights were observed between members of the same and of the opposite sex. During fights, legs and claws could be torn off. Adult males migrated more often between anemones and moved over larger distances when migrating than did adult females. Adult males probably migrated in search of sexually mature females. Such a roving strategy is evolutionarily stable only when the higher costs (in terms of energy expenditure and mortality) are compensated for by a higher number of offspring than produced in the alternative, pair-bonding strategy.     

Effects of anemonefish on giant sea anemones: expansion behavior,growth, and survival

The symbiosis between giant sea anemones and anemonefish on coral reefs is well known, but little information exists on impacts of this interaction on the sea anemone host. On a coral reef at Eilat, northern Red Sea, individuals of the sea anemone Entacmaea quadricolor that possessed endemic anemonefish Amphiprion bicinctus expanded their tentacles significantly more frequently than did those lacking anemonefish. When anemonefish were experimentally removed, sea anemone hosts contracted partially. Within 1–4 h in most cases, individuals of the butterflyfish Chaetodon fasciatus arrived and attacked the sea anemones, causing them to contract completely into reef holes. Upon the experimental return of anemonefish, the anemone hosts re-expanded. The long-term growth rate and survival of the sea anemones depended on the size and number of their anemonefish. Over several years, sea anemones possessing small or no fish exhibited negative growth (shrinkage) and eventually disappeared, while those with at least one large fish survived and grew. We conclude that host sea anemones sense the presence of symbiotic anemonefish via chemical and/or mechanical cues, and react by altering their expansion behavior. Host sea anemones that lack anemonefish large enough to defend them against predation may remain contracted in reef holes, unable to feed or expose their tentacles for photosynthesis, resulting in their shrinkage and eventual death.     

Ammonia flux,physiological parameters,and <Emphasis Type="Italic">Symbiodinium</Emphasis> diversity in the anemonefish symbiosis on Red Sea coral reefs

Despite the ecological importance of anemonefish symbioses, little is known about how nutritional contributions from anemonefish interact with sea anemone physiology and Symbiodinium (endosymbiotic dinoflagellate) genetic identity under field conditions. On Red Sea coral reefs, we measured variation in ammonia concentrations near anemones, excretion rates of anemonefish, physiological parameters of anemones and Symbiodinium, and genetic identity of Symbiodinium within anemones. Ammonia concentrations among anemone tentacles were up to 49% above background levels, and anemonefish excreted ammonia significantly more rapidly after diurnal feeding than they did after nocturnal rest, similar to their excretion patterns under laboratory conditions. Levels of 4 physiological parameters (anemone protein content, and Symbiodinium abundance, chlorophyll a concentration, and division rate) were similar to those known for laboratory-cultured anemones, and in the field did not depend on the number of anemonefish per anemone or depth below sea surface. Symbiodinium abundance varied significantly with irradiance in the shaded reef microhabitats occupied by anemones. Most anemones at all depths harbored a novel Symbiodinium 18S rDNA variant within internal transcribed spacer region 2 (ITS2) type C1, while the rest hosted known ITS2 type C1. Association with Symbiodinium Clade C is consistent with the symbiotic pattern of these anemones on other Indo-Pacific reefs, but the C1 variant of Symbiodinium identified here has not been described previously. We conclude that in the field, anemonefish excrete ammonia at rapid rates that correlate with elevated concentrations among host anemone tentacles. Limited natural variation in anemonefish abundance may contribute to consistently high levels of physiological parameters in both anemones and Symbiodinium, in contrast to laboratory manipulations where removal of fish causes anemones to shrink and Symbiodinium to become less abundant.     

Aerial exposure and body temperature of the intertidal sea anemone Anthopleura elegantissima

The sea anemone Anthopleura elegantissima is a common member of intertidal communities along the west coast of North America, and can experience extended periods of increased temperature during summertime low tides. Internal body temperatures of emersed individuals of A. elegantissima were monitored in a laboratory wind tunnel and in the field, and factors influencing the anemones’ thermal experience were examined. Larger body size and aggregation with conspecifics slowed body temperature increases in controlled wind tunnel conditions. In the field, anemones in the interior of an aggregation stayed cooler than those on the edges, and microhabitat features related to light exposure and surface orientation overshadowed any direct effects of body size. In the warmest month only (July), aggregations of A. elegantissima were significantly larger at the upper limit of their distribution than they were at the mid and lower limits, suggesting aggregation in high intertidal zones may be a behavioral response to desiccation and temperature stress. As this sea anemone can host multiple species of symbiotic algae with different thermal tolerances, the ability to slow body heating may affect the type of algae hosted and thus the potential contribution of this abundant anemone to primary production in the intertidal zone.     

Postural Shifts During Egg‐Brooding and Their Impact on Egg Water Balance in Children’s Pythons (Antaresia childreni)

Parental care typically consists of distinct behavioral components that are balanced to address the multiple needs of offspring. Female pythons exhibit post‐oviposition parental care in which they coil around their parchment‐shelled eggs throughout incubation (40–80 d). Subtle postural shifts during egg‐brooding facilitate embryonic gas exchange but may entail hydric costs to the clutch. This study used a simple behavioral model to (1) further quantify the costs and benefits of specific parental behaviors to developing offspring and (2) determine the influence that developmental stage and relative clutch mass have on parental behavior. Although previous research has demonstrated that egg‐brooding as a whole reduces clutch water loss, we hypothesized that egg‐brooding female pythons specifically adopt a tightly coiled posture to conserve embryonic water, but must make postural adjustments to enhance gas exchange between the clutch and nest environments at the cost of increased clutch water loss. We measured rates of water loss in brooding Children’s pythons (Antaresia childreni) and their respective clutches (i.e., brooding units) and monitored changes in brooding posture. We conducted serial trials to elucidate the effect of developmental stage on postural adjustments and water loss. Results demonstrated that the proportion of time females spent in a tightly coiled posture was inversely related to mean water loss from the brooding unit. Analyses indicated that slight adjustments in posture led to bursts in brooding unit water loss. Indeed, brooding unit water loss during postural adjustments was significantly higher than during tight coiling. These findings imply that python egg‐brooding provides an adjustable diffusive barrier that leads to discontinuous gas exchange, which minimizes clutch water loss. Because females with larger relative clutch masses spent more time tightly coiled, egg‐brooding female pythons may use a ‘water first’ strategy in which they intentionally conserve clutch water at the cost of reduced embryonic respiratory gas exchange.     

Body size and symbiotic status influence gonad development in <Emphasis Type="Italic">Aiptasia pallida</Emphasis> anemones

Pale anemones (Aiptasia pallida) coexist with dinoflagellates (primarily Symbiodinium minutum) in a mutualistic relationship. The purpose of this study was to investigate the role of these symbionts in gonad development of anemone hosts. Symbiotic and aposymbiotic anemones were subjected to light cycles that induced gametogenesis. These anemones were then sampled weekly for nine weeks, and gonad development was analyzed histologically. Anemone size was measured as mean body column diameter, and oocytes or sperm follicles were counted for each anemone. Generalized linear models were used to evaluate the influence of body size and symbiotic status on whether gonads were present and on the number of oocytes or sperm follicles produced. Body size predicted whether gonads were present, with larger anemones being more likely than smaller anemones to develop gonads. Both body size and symbiotic status predicted gonad size, such that larger and symbiotic anemones produced more oocytes and sperm follicles than smaller and aposymbiotic anemones. Overall, only 22 % of aposymbiotic females produced oocytes, whereas 63 % of symbiotic females produced oocytes. Similarly, 6 % of aposymbiotic males produced sperm follicles, whereas 60 % of symbiotic males produced sperm follicles. Thus, while gonads were present in 62 % of symbiotic anemones, they were present in only 11 % of aposymbiotic anemones. These results indicate that dinoflagellate symbionts influence gonad development and thus sexual maturation in both female and male Aiptasia pallida anemones. This finding substantiates and expands our current understanding of the importance of symbionts in the development and physiology of cnidarian hosts.     

Optimal Mate Searching Strategy in the Symbiotic Spider Crab Inachus phalangium (Decapoda)

The reproductive strategy of the symbiotic spider crab, Inachus phalangium was studied from 1981 to 1983 in the natural environment. Main study focus was the efficiency of males in search of mates. I. phalangium females are site-constant, and live in the protection of one anemone or group. Males travel frequently between anemones harbouring females due to spawn; they copulate and guard the females until spawning, after which the male leaves again. A male operates in a patrol area containing 3–8 anemone groups and up to 8 females, visiting each female in turn repeatedly just before it is due to spawn. Patrol areas of different males may overlap, with resulting competition to fertilize a female's next brood. Large males have higher reproductive success than small ones. Females live up to 8 months after the moult of puberty and hatch up to six broods, and males live up to 7 months as adults. A male could fertilize a calculated 26,000 eggs, whilst a female's reproductive potential is ca. 4,200 eggs. Mortality risks are higher for males than for females, probably because of increased predation while leaving the protection of anemones in order to visit females. Males learn the positions of anemones harbouring females in their patrol areas, and when these are due to spawn. This allows a male to travel with a target and arrive punctually to fertilize the next brood due in his circuit. I. phalangium is the first marine invertebrate reported to use a “schedule” of localities and times for visiting prespawning females. In this way males minimize searching time and mortality risk, and maximize the number of broods fertilized.     

Mobility of Stichodactyla Gigantea Sea Anemones and Implications for Resident False Clown Anemonefish, Amphiprion Ocellaris

For reef fishes that do not move between habitat patches following settlement, habitat selection is expected during settlement. Although false clown anemonefish, Amphiprion ocellaris, are sedentary following settlement, they are not especially discriminating during settlement, and are commonly found occupying anemones at which no apparent nest site exists. In this study I report on mobility of Stichodactyla gigantea sea anemones, including anemones with resident false clowns. I argue that anemone mobility can help explain why settling false clowns are not more discriminating: although the per annum probability of an anemone moving is low, the probability of that anemone moving over the course of a resident's life is considerably higher. Therefore, an anemone's current microhabitat may not be a good predictor of its microhabitat and suitability as a host in the future.     

Mothers influence offspring body size through post-oviposition maternal effects in the redbacked salamander, Plethodon cinereus

In the terrestrial salamander (Plethodon cinereus), previous work has shown that mothers body size is positively correlated to offspring size at the time of hatching even after controlling for the effects of egg size. This study was designed to determine whether maternal body size affects offspring size via pre-oviposition factors (e.g., yolk quality, jelly coat composition, or maternal genes) or post-oviposition factors (e.g., parental care behaviors, parental modification of environment). Gravid females were captured and induced to lay eggs in experimental chambers in which the environment was standardized. Fifteen clutches were exchanged, or cross-fostered, between female pairs differing in body size. Ten females whose eggs were taken away and then returned served as controls for the crossing treatment. Foster mothers did not significantly differ from control mothers in the time spent with eggs, body position, or number of egg movements during brooding. Average egg mass measured midway through development was not significantly correlated to the body size of either the genetic or foster mother, but was correlated to pre-oviposition oocyte size. At hatching, offspring body length was positively correlated to egg size and the foster mothers body size. This correlation suggests that in P. cinereus post-oviposition maternal effects have a greater impact on offspring size than other maternal factors incorporated into the egg prior to oviposition. While our study showed that larger mothers moved their eggs less often and tended to spend more time in contact with their eggs, further work needs to be done to identify the specific mechanisms through which larger mothers influence the body size of their offspring. This is the first experimental demonstration of post-oviposition maternal effects for any amphibian with parental care.     

Maternal brooding in the children’s python <Emphasis Type="Italic">(Antaresia childreni)</Emphasis> promotes egg water balance

Parental care provides considerable benefits to offspring and is widespread among animals, yet it is relatively uncommon among squamate reptiles (e.g., lizards and snakes). However, all pythonine snakes show extended maternal egg brooding with some species being facultatively endothermic. While facultative endothermy provides thermal benefits, the presence of brooding in non-endothermic species suggests other potential benefits of brooding. In this study we experimentally tested the functional significance of maternal brooding relative to water balance in the children’s python, Antaresia childreni, a small species that does not exhibit facultative endothermy. Clutch evaporative water loss (EWL) was positively correlated with clutch mass and was much lower than expected values based on individual eggs. The conglomerate clutch behaved as a single unit with a decreasing surface area to volume ratio as clutch size increased. Maternal brooding had a dramatic impact on evaporation from eggs, reducing and possibly eliminating clutch EWL. In a separate experiment, we found that viability of unattended eggs is highly affected by humidity level, even in the narrow range from 75 to 100% relative humidity at 30.5°C (20–33 mg m⁻³ absolute humidity). However, the presence of the brooding female ameliorated this sensitivity, as viability of brooded clutches at 75% relative humidity was higher than that of non-brooded eggs at either the same absolute humidity or at near-saturated conditions. Overall, these results demonstrate that brooding behavior strongly promotes egg water balance (and thus egg viability) in children’s pythons.     

Pycnogonid‐cnidarian trophic interactions in the deep Monterey Submarine Canyon

Abstract. Whale carcasses, sunken wood, and cold seeps provide organically enriched oases in the food‐limited deep‐sea benthos. At three such enriched habitats in Monterey Bay, CA, at a depth of nearly 3000 m, we observed pycnogonids (sea spiders) of at least two species, Colossendeis gigas and C. japonica, feeding on sea anemones that were commonly found there. Submersible remotely operated vehicles provided direct observations of feeding, as well as high definition video and photographic images. We recorded the co‐occurrence of both pycnogonids and prey anemones during ten of 12 visits during 2002–2006. Anemones and pycnogonids were conspicuously more abundant at these oases than in the surrounding benthos. The sedentary anemone Anthosactis pearseae was attached directly to whalebones while the pom‐pom anemone, Liponema brevicornis, was found resting on soft sediment, rolling in benthic currents, or accumulating where these currents were disrupted by topography, as at whale falls, wood falls, and clam fields. Both pycnogonid species were observed feeding on these anemones, either as predators or as micropredators.     

Exclusive Male Egg Care and Determinants of Brooding Success in a Millipede

The evolution of exclusive male parental care is a major and controversial issue in behavioural ecology. Although arthropods practicing paternal care are thought to be key taxa for investigating this issue, few studies have attempted to clarify the selection factors associated with male behaviour and fitness consequences in arthropods. In the millipede Brachycybe nodulosa, males curl their bodies around egg masses on the undersides of decaying logs. Male‐removal experiments in the laboratory strongly suggest that males defend the eggs against fungal infection. Orphaned eggs were soon covered by hyphae and no eggs hatched, whereas almost all eggs brooded by males successfully hatched. The egg‐brooding males showed no aggressive responses when disturbed. Only some mature males bred in the field. Furthermore, the number of eggs brooded varied greatly among the males. Selected generalized linear models revealed that males with a wide seventh body segment, which possesses gonopods (genital legs), tended to succeed in brooding; and males with a wider body also obtained more eggs. Colony attributes had no significant effects on male brooding. We discuss the possible sexual selection mechanisms that could accomplish this pattern of brooding success among male B. nodulosa.     

Predation drives recurrent convergence of an interspecies mutualism

Mutualisms are important ecological interactions that underpin much of the world's biodiversity. Predation risk has been shown to regulate mutualism dynamics in species‐specific case studies; however, we lack studies which investigate whether predation can also explain broader patterns of mutualism evolution. We report that fish‐anemone mutualisms have evolved on at least 55 occasions across 16 fish families over the past 60 million years and that adult body size is associated with the ontogenetic stage of anemone mutualisms: larger‐bodied species partner with anemones as juveniles, while smaller‐bodied species partner with anemones throughout their lives. Field and laboratory studies show that predators target smaller prey, that smaller fishes associate more with anemones, and that these relationships confer protection to small fishes. Our results indicate that predation is likely driving the recurrent convergent evolution of fish‐anemone mutualisms and suggest that similar ecological processes may have selected convergence in interspecies interactions in other animal clades.     

Detrimental effects of host anemone bleaching on anemonefish populations

Coral bleaching and related reef degradation have caused significant declines in the abundance of reef-associated fishes. Most attention on the effects of bleaching has focused on corals, but bleaching is also prevalent in other cnidarians, including sea anemones. The consequences of anemone bleaching are unknown, and the demographic effects of bleaching on associated fish recruitment, survival, and reproduction are poorly understood. We examined the effect of habitat degradation including host anemone bleaching on fish abundance, egg production, and recruitment of the panda anemonefish (Amphiprion polymnus) near Port Moresby, Papua New Guinea. Following a high-temperature anomaly in shallow waters of the region, most shallow anemones to a depth of 6 m (approximately 35% of all the anemones in this area) were severely bleached. Anemone mortality was low but bleached anemones underwent a ~34% reduction in body size. Total numbers of A. polymnus were not affected by bleaching and reduction in shelter area. While egg production of females living in bleached anemones was reduced by ~38% in 2009 compared to 2008, egg production of females on unbleached anemones did not differ significantly between years. Total recruitment in 2009 was much lower than in 2008. However, we found no evidence of recruiting larvae avoiding bleached anemones at settlement suggesting that other factors or different chemical cues were more important in determining recruitment than habitat quality. These results provide the first field evidence of detrimental effects of climate-induced bleaching and habitat degradation on reproduction and recruitment of anemonefish.     

The maturity and breeding season of the bellybarred pipefish, <Emphasis Type="Italic">Hippichthys spicifer</Emphasis>, in Okinawa-jima Island rivers

We investigated the breeding season and size at maturation and described the morphology of newly released Hippichthys spicifer larvae collected from the estuaries of four rivers on northern Okinawa-jima Island, southern Japan. The minimum size of brooding males was 108 mm standard length (SL). The smallest mature female, as estimated from gonadosomatic index (GSI) analysis and histological observations of gonads, was about 100 mm SL. Histological observations showed the gonad of H. spicifer to be a cylindrical tube with a sequential pattern of follicle development and a single germinal ridge. We surmised that the breeding season is year-round, as shown by monthly changes in female GSI, gonad histology, and monthly changes in the occurrence of brooding males. The monthly changes in female GSI and proportions of brooding males were small in winter. The number of eggs in the male brood pouch ranged from 114 to 1,764 (604.4 ± 322.8, mean ± standard deviation; n = 25). The SL of the released larvae was 9.9 mm. All fins except the pectoral fins were formed, the body was elongated, and the developmental stage was similar to that of other Urophori species. The smallest individual present in the mangrove areas of estuaries was 78.0 mm SL.     

Morphological features,development and reproduction of Melittobia acasta on Bombus terrestris

Morphological features, development and reproduction behavior of the parasite Melittobia acasta (Walker) were studied when reared on the pupae of the bumblebee Bombus terrestris L. in the laboratory under 23°C, 50% relative humidity and 12 h light : 12 h dark conditions. The parasites laid transparent white and elongated eggs. Newly hatched larval size and shape were very similar to eggs but they were identified by their body segments. Larvae increased their body size through moulting and transformed into a vermiform shape. Male pupae were shiny brown with dots. The female pupae were distinguished by their black shiny color, shorter size and the presence of compound eyes. Adult male pupae were dark brown and dwarf‐winged, whereas female pupae were macropterous and brachypterous. Reproduction took place by fertilization and also parthenogenetically. Mean fecundity within 5 days by mated (47.9 ± 30.5 female^?1) and virgin (7.4 ± 6.8 female^?1) females were statistically different. Mated females laid fertilized eggs that produced adult males or females, whereas virgin females laid unfertilized eggs that produced males. Development durations of the virgin female originated eggs, larvae, pupae and adults were statistically identical with those of mated females. The parasites were female‐biased and foundress number did not affect offspring sex ratio. This study shows that both mated and virgin females of M. acasta can produce many offspring on B. terrestris pupae within a short period, indicating that they are dangerous parasites of the bumblebee in a mass rearing system.     

Chemosensory and feeding responses of the nudibranch Aeolidia papillosa to the symbiotic sea anemone Anthopleura elegantissima

Abstract. The aeolid nudibranch Aeolidia papillosa is an important predator on the sea anemone Anthopleura elegantissima , a host to two kinds of endosymbiotic algae: zooxanthellae and zoochlorellae. The possible influence of the algae on the nudibranch's predatory response to this anemone was examined in a laboratory study. In chemosensory experiments, the nudibranch detected and chose anemone scent over a seawater control, but in both chemosensory and feeding experiments showed no preference for zooxanthellate or zoochlorellate anemones. Ingestive conditioning on zooxanthellate or zoochlorellate anemones had no effect on choice of these two anemone types in chemosensory experiments. Comparisons of the productivity and photosynthetic pigments of algae obtained from nudibranch feces and from anemones show that both algae survive passage through the nudibranch gut. The productivity of fecal zooxanthellae was 1.6X greater than that of zooxanthellae freshly isolated from anemones, although the chlorophyll a content of fecal zooxanthellae was reduced. The productivity and amount of pigments were the same for zoochlorellae in nudibranch feces and freshly isolated from anemones. Comparing fecal and isolated algae, there was no significant difference in the percentage of zooxanthellae in the process of cell division. However, the percentage of dividing cells was 2.6X higher in fecal than in freshly isolated zoochlorellae (18% and 6.9% respectively). Although the endosymbiotic algae do not make their host more or less attractive to the nudibranch, this predator may play an important role in maintaining the symbiotic relationship of Anthopleura elegantissima with zooxanthellae and zoochlorellae by providing viable algae in its feces as a source for the anemone host.     

Testing the role of male–male competition in the evolution of sexual dimorphism: a comparison between two species of porcelain crabs

Theory predicts marked sexual dimorphism in terms of body size and body structures used as weapons (e.g. chelipeds) in gonochoric species with intense male sexual competition for receptive females and reduced or no sexual dimorphism in species where competition among males is trivial. We tested this hypothesis using a pair of closely‐related species of symbiotic porcelain crabs as a model. In one species that inhabits sea anemones solitarily, competition among males for receptive females is unimportant. In a second species that dwells as dense aggregations on sea urchins, male–male competition for sexual partners is recurrent. We expected considerable sexual dimorphism in body size and weaponry in the urchin‐dwelling crab and reduced sexual dimorphism in the anemone‐dwelling crab. In agreement with expectations, in the urchin‐dwelling crab, male body size was, on average, larger than that of females and males invested considerably more to cheliped length than females. Also supporting theoretical considerations, in the anemone‐dwelling crab, sexual dimorphism in terms of body size was not detected and differences between the sexes in investment to cheliped length were minor. Interestingly, chelipeds were more developed both in males and females of the anemone‐dwelling crab than in the urchin‐dwelling crab as a result of the importance of these structures for monopolization of their naturally scarce anemone hosts. Another difference between the studied species was the existence of two clearly distinguishable ontogenetic phases in males of the urchin‐dwelling crab but not in males of the anemone‐dwelling crab. Whether the two different male morphs display different male reproductive strategies in the urchin‐dwelling crab remains to be addressed. Other conditions that might additionally explain the observed differences in sexual dimorphism (e.g. female mate choice) between the studied species remain to be explored. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2012, 105 , 548–558.