Hydroid defenses against predators: the importance of secondary metabolites versus nematocysts

Marine hydroids are commonly thought to be defended by stinging organelles called nematocysts that penetrate predator tissues and inject proteinaceous venoms, but not all hydroids possess these nematocysts. Although an increasing number of bioactive secondary metabolites have been isolated from marine hydroids, ecological roles of these compounds are poorly known. To test the hypothesis that nematocysts and noxious secondary metabolites represent alternative defenses against predation, we examined hydroids from North Carolina, United States for: (1) the palatability of whole polyps before and after nematocysts had been deactivated; (2) the palatability of their chemical extracts; and (3) their nutritional value in terms of organic content, protein content, and levels of refractory structural material (chitin). All hydroids were avoided by a generalist predator, the pinfish Lagodon rhomboides, compared with palatable control foods. Two of these (Halocordyle disticha and Tubularia crocea) became palatable after being treated with potassium chloride to discharge their nematocysts, suggesting that these species rely on nematocysts for defenses against predators. Chemical extracts from nematocyst-defended species had no effect on fish feeding. The four species that remained unpalatable after nematocysts had been discharged (Corydendrium parasiticum, Eudendrium carneum, Hydractinia symbiolongicarpus, Tridentata marginata) possessed chemical extracts that deterred feeding by pinfish. We have isolated and characterized the structures of the deterrent metabolites in two of these species. We found no differences in nutritional content or levels of chitin between nematocyst-defended and chemically defended species, and no evidence that either of these played a role in the rejection of hydroids as prey. Our results suggest that, among hydroids, chemical defenses may be at least as common as nematocyst-based defenses and that the two may represent largely alternative defensive strategies. The four hydroid species with deterrent extracts represent four families and both sub-orders of hydroids, suggesting that chemical defenses in this group may be widespread and have multiple origins. Received: 25 May 1999 / Accepted: 1 February 2000     

Separation and analysis of different types of nematocysts from <Emphasis Type="Italic">Cyanea capillata</Emphasis> (L.) medusae

Medusae play an important role in marine ecosystems, as competitors of many invertebrate and fish species. Additionally, jellyfish stings can cause severe pain, inflammation of the affected skin, and allergic reactions in human. Climate and environmental changes are likely to affect the medusae, but it is not yet clear whether these will affect their distribution, physiology, and their toxicity. Very little is known about the effect of biotic and abiotic factors on the proliferation and the distribution of medusan nematocysts. In this study, we compared three types of nematocysts (euryteles and A- and O-isorhizas) and venoms of Cyanea capillata medusae (Scyphozoa) obtained from the North Sea and the Baltic Sea, which have different salinity and temperature ranges. Different types of nematocysts were separated by laser microdissection and pressure catapulting (LMPC), and the proteinaceous contents of the nematocysts were analyzed by matrix-assisted laser desorption ionization time-of-flight mass spectrometry (MALDI-TOF MS). Medusae from the brackish Baltic Sea possessed more euryteles than those from the North Sea. The O-isorhizas and A-isorhizas were smaller in the Baltic Sea sample compared to the North Sea samples and the length-to-width ratios were larger in the Baltic Sea sample. Moreover, the pattern of proteins (potential toxins) obtained from the separated nematocysts showed differences among samples and nematocyst types, but no clear pattern was observable. This study displays the novel LMPC/MALDI-TOF MS approach as a useful tool to investigate the function and venom of cnidarian nematocysts types.     

Active Nematocyst Isolation Via Nudibranchs

Cnidarian venoms are potentially valuable tools for biomedical research and drug development. They are contained within nematocysts, the stinging organelles of cnidarians. Several methods exist for the isolation of nematocysts from cnidarian tissues; most are tedious and target nematocysts from specific tissues. We have discovered that the isolated active nematocyst complement (cnidome) of several sea anemone (Cnidaria: Anthozoa) species is readily accessible. These nematocysts are isolated, concentrated, and released to the aqueous environment as a by-product of aeolid nudibranch Spurilla neapolitana cultures. S. neapolitana feed on venomous sea anemones laden with stinging nematocysts. The ingested stinging organelles of several sea anemone species are effectively excreted in the nudibranch feces. We succeeded in purifying the active organelles and inducing their discharge. Thus, our current study presents the attractive possibility of using nudibranchs to produce nematocysts for the investigation of novel marine compounds.     

Les recherches sur les lépidoptères foreurs des graminées et leurs antagonistes : bilan et perspectives

Ancistrocerus, Discoelius and Symmorphus are xylicolous predatory wasps, the former two genera hunting caterpillars, the last one using both caterpillars and larvae of Chrysomelidae beetles. One of the aims of this study was to compare the stinging pattern of species from these genera with the ancestral “complete four-sting pattern” (C4SP) and reduced “two-sting pattern” (C2SP). Another aim was to clarify whether stinging pattern of predatory wasps depends mostly on the prey type or on the systematic position of the wasp. Sting traces on 6123 paralysed prey specimens, taken from 409 fresh wasp nests made by 10 wasp species in reed (Phragmites australis) trap-nests in three localities of Lithuania, were studied. The total number of stings applied to a prey specimen, the number and the share of stings directed to its body segments and the probability of stinging the segments were considered. The main conclusions of the study are: (1) the total number of stings delivered to a prey is species-specific, in some cases it may be used to distinguish fresh nests of related wasp species, as those of Symmorphus crassicornis and S. murarius and those of Discoelius dufourii and D. zonalis. (2) The distribution of stings is significantly different from the basic patterns C4SP and C2SP in all ten studied wasps; however, four caterpillar-hunting species have the distribution close to the C2SP The stinging pattern of three Symmorphus species hunting Chrysomelidae larvae included regular stings to the throat, three thoracic and the first abdominal segment; it could be abbreviated as C5SP (a complete five-sting pattern). (3) The distribution of stings among the segments of prey was found to be more dependent on the taxonomic position of the wasp species than on the prey type, thus it might be used as a behavioural character in comparative and phylogenetic studies. (4) The stinging pattern depended on the prey type as well: in the caterpillar-hunting S. debilitatus, it was quite different from the stinging pattern of the Symmorphus that hunt Chrysomelidae larvae.     

Morphology of the nematocysts of the medusae of two scyphozoans, Catostylus mosaicus and Phyllorhiza punctata (Rhizostomeae): implications for capture of prey

Abstract. We examined the cnidomes (total complement of nematocysts) of medusae of the zooxanthellate and azooxanthellate jellyfishes Phyllorhiza punctata and Catostylus mosaicus (Rhizostomeae, Scyphozoa), and compared the assemblage of zooplankton captured on the oral arms of each species to determine whether differences in the types or amount of zooplankton captured were consistent with possible differences in the cnidomes. Cnidomes were described using light and scanning electron microscopy. Each species had a distinct cnidome and, in general, specimens of P. punctata appeared to have far fewer nematocysts than those of C. mosaicus. Four types of nematocysts were identified in medusae of C. mosaicus; 2 types of holotrichous isorhizae, rhopaloids, and birhopaloids. In C. mosaicus, the oral arms and bell margins possessed all of these types, but the cnidomes of the 2 regions differed in relative abundances and sizes of isorhizae and rhopaloids. Five types of nematocysts were identified in medusae of P. punctata, although not all types were found in all specimens. Round holotrichous isorhizae were found only in the bell, while oval holotrichous isorhizae, rhopaloids of 2 distinct size ranges, and birhopaloids were found in the bell and oral arms. Cnidomes of the bell and oral arms in specimens of P. punctata also differed in the relative abundance and sizes of oval isorhizae and rhopaloids. Although there were clear differences in the overall cnidomes and absolute abundances of nematocysts in each species, the oral arms (feeding appendages) of specimens of both C. mosaicus and P. punctata had similar types and relative abundances of nematocysts. Zooplankton sampled from the oral arms of each species showed that both species preyed predominantly on copepod nauplii and larvae of gastropods and bivalves. Medusae of C. mosaicus captured ～10 × more gastropod larvae and 5 × more bivalve larvae than those of P. punctata. Specimens of P. punctata captured approximately twice as many copepod nauplii as those of C. mosaicus. Differences in the relative abundance of types of zooplankton captured by each species could not be adequately explained by differences in the cnidomes of the oral arms.     

Hydroid nematophores: morphological,structural, and behavioural variety from old knowledge and new data

There is a rich old literature on nematothecae, which have been described from many species of nine families of thecate hydroids, but detailed knowledge of nematophores is from a very few species. Using both old data and new observations, information was gathered on species belonging to the genera Hydrodendron, Zygophylax, Antennella, Plumularia, Monotheca, Macrorhynchia, Gymnangium, and Thecocarpus. Specimens belonging to five families collected on the coral reefs of Réunion Island (SW Indian Ocean) were observed alive and videotaped to gather information on nematophores. Nematophores are classified and named here as belonging to three types. An amoeboid nematophore of the four plumularid families Kirchenpaueriidae, Halopterididae, Plumulariidae, and Aglaopheniidae usually consists of two parts, which are more separate in aglaophenids than in the others. The cnidostyle (or nematostyle) is fixed, is formed of ectoderm and endoderm, and includes a cluster of large nematocysts at its top. It is inferred to serve in defence because nematocysts inside the nematotheca can be fired when stimulated. The sarcostyle is a mobile amoeboid layer of ectoderm capable of considerable extension; those that are bilobed on top can extend in two directions at a time. The sarcostyle can emit small pseudopods on its edges that phagocytose particles at the surface of the perisarc. Its hypothesized function of cleaning the colony and providing nutrition in the form of small detrital particles and bacteria taken up by phagocytosis remains to be confirmed by experimentation. The cnidostyle-like nematophore of the Campanulinidae, Linolariidae, and Clathrozoidae is a fixed structure formed of a bilayered pedicel ending with a cluster of nematocysts able to fire while still inside the nematotheca, like the cnidostyle part of the amoeboid nematophore. It functions in defence as well. The tentacle-like nematophore of the Haleciidae and Lafoeidae, described here for the first time, is a single very extensible process provided with nematocysts that issue from the nematotheca and formed by a file of endodermal chordal cells surrounded by ectoderm. In halecids, nematocysts are not always gathered on the very top, forming what looks like a strongly capitate tentacle, as was previously thought, but can be more scattered, giving the structure a filiform appearance. This type has active movements, being able to twist and bend in all directions. Its prey capture function has not been demonstrated; a sensory function is more probable. Additional data have to be collected for more species to compare the types with more confidence, but they appear to have different origins for their considerably different morphologies, structures, and behaviour.     

Cryptic diets of forage fish: jellyfish consumption observed in the Celtic Sea and western English Channel

To establish if fishes’ consumption of jellyfish changes through the year, we conducted a molecular gut-content assessment on opportunistically sampled species from the Celtic Sea in October and compared these with samples previously collected in February and March from the Irish Sea. Mackerel Scomber scombrus were found to feed on hydrozoan jellyfish relatively frequently in autumn, with rare consumption also detected in sardine Sardina pilchardus and sprat Sprattus sprattus. By October, moon jellyfish Aurelia aurita appeared to have escaped predation, potentially through somatic growth and the development of stinging tentacles. This is in contrast with sampling in February and March where A. aurita ephyrae were heavily preyed upon. No significant change in predation rate was observed in S. sprattus, but jellyfish predation by S. scombrus feeding in autumn was significantly higher than that seen during winter. This increase in consumption appears to be driven by the consumption of different, smaller jellyfish species than were targeted during the winter.     

Fine structure of the nematocytes of Polypodium hydriforme Ussov (Cnidaria)

The fine structure of the stinging cells (nematocytes) and stinging capsules (nematocysts) is described for Polypodium hydriforme. a freshwater coclenterate with a prominent endoparasitie stage in its life cycle. All the nematocysts belong to the type of lesser glutinants (atrichous isorhiza) and fall into three size classes. The internal structure of the capsules is similar in the three classes. A novel type of organization of the cnidocil apparatus of the nematocysts is described. The cnidocil lacks a root fibre and its kinctosome sits directly on the operculum of the nematocyst, so that the entire cnidocil apparatus has a radial rather than bilateral symmetry. It is compared with that of other types of nematocytes and its similarity with the mechanoreccptors of the coelentcratcs is noted. The possible place of the Polypodium nematocytes in the evolution of the collar receptors of the Metazoa is discussed.     

Cnidarian internal stinging mechanism

Stinging mechanisms generally deliver venomous compounds to external targets. However, nematocysts, the microscopic stinging organelles that are common to all members of the phylum Cnidaria, occur and act in both external and internal tissue structures. This is the first report of such an internal piercing mechanism. This mechanism identifies prey items within the body cavity of the sea anemone and actively injects them with cytolytic venom compounds. Internal tissues isolated from sea anemones caused the degradation of live Artemia salina nauplii in vitro. When examined, the nauplii were found to be pierced by discharged nematocysts. This phenomenon is suggested to aid digestive phagocytic processes in a predator otherwise lacking the means to masticate its prey.     

Craniometrical variations among eastern Brazilian marmosets and their systematic relationships

The craniometrical variations among marmosets on the eastern coast of Brazil or theCallithrix jacchus group (C. jacchus, C. penicillata, C. kuhli, C. geoffroyi, C. flaviceps, andC. aurita) were analyzed to test various hypotheses for the arrangement of the species and phylogenetic relationships ofC. kuhli andC. flaviceps. Q-mode correlation coefficients and principal component analysis were employed to extract important shape factors from the craniometrical data. On this basis, the shape distances among the eastern Brazilian marmosets were found to be larger than those between the marmosets which are recognized as distinct species. This evidence supports the hypothesis that the members of theC. jacchus group are distinct species.C. kuhli shows the strongest resemblance toC. geoffroyi within theC. jacchus group.C. flaviceps is the most similar toC. aurita in its cranial shape. These findings indicate thatC. kuhli is most closely related toC. geoffroyi, whileC. flaviceps is toC. aurita.     

Dynamic tuning of hair bundle mechanoreceptors in a sea anemone during predation

The sea anemone Haliplanella luciae (Cnidaria, Anthozoa) detects chemical and mechanical stimuli from prey. Hair bundle mechanoreceptors on the tentacles participate in regulating discharge of microbasic p-mastigophore nematocysts. Properly stimulated hair bundles sensitize the anemone to discharge nematocysts into objects that contact the tentacles. The hair bundle mechanoreceptors are composed of stereocilia derived from a multicellular complex. This complex consists of a single sensory neuron surrounded by two to four supporting cells. The mechanoreceptor is similar in many ways to vertebrate hair cells of the acousticolateralis system. However, anemone hair bundles are adjustable in structure and responsiveness according to the activity of two different chemoreceptors. One chemoreceptor binds N -acetylated sugars and the other binds amino compounds including proline. N -acetylated sugars induce lengthening of the hair bundle and a downward shift in frequencies that elicit maximal discharge of microbasic p-mastigophore nematocysts. Furthermore, N -acetylated sugars shift maximal discharge to smaller amplitude vibrations. Thus, N -acetylated sugars likely tune hair bundles so that small, swimming zooplankton stimulate maximal discharge. Proline leaks into the seawater from the hemolymph of wounded prey. Proline induces shortening of the hair bundle and shifts maximal discharge of nematocysts to higher frequencies and to larger amplitude vibrations. Thus, proline likely tunes hair bundles so that small, wounded, prey stimulate maximal discharge of nematocysts as they struggle to escape. Thus, suitably sized prey stimulate maximal discharge of microbasic p-mastigophore nematocysts upon first contacting the anemone tentacle and again upon attempting to escape.     

Occasional intraguild predation structuring small mammal assemblages: the marsupial Didelphis aurita in the Atlantic Forest of Brazil

The didelphid marsupial, Didelphis aurita, is suggested as an intraguild predator and as key‐species in small mammal assemblages of the Atlantic Forest of Brazil. The field experiments required to test this hypothesis are complex to implement, but the recent revival of regression methods offers a viable alternative. Here we use the dynamic and static regression methods to determine the importance of D. aurita as a competitor and intraguild predator. Capture–recapture data from two localities in the Rio de Janeiro State were used, Garrafão (municipality of Guapimirim), a coastal forest of the Serra do Mar, and Barra de Maricá, a costal sand dune vegetation. Population and microhabitat variables were monitored from April 1997 to April 2003 in Garrafão, and from January 1986 to July 1990 in Barra de Maricá. Microhabitat variables were related to Canopy, Plant, Litter and Rock covers, Obstruction from 0 to 1.5 m, and Number of logs. Exploitation competition was tested by the dynamic method, which models the effects of D. aurita on the per capita growth rate of a species. Interference by predation or competition was tested by the static method, where the abundance of D. aurita at trap stations was regressed against the abundance of other small mammals, after removal of any variation associated with microhabitat factors. Exploitation competition was not detected, but the interference of D. aurita was pervasive, affecting all small mammals studied in the two localities. The clear avoidance of D. aurita by all small mammals tested in two localities of different physiognomies indicates that it functions as an intraguild predator, even if actual predation by D. aurita is an occasional event.     

Attraction of Aurelia and Aequorea to prey

Previously it has been assumed that medusae make random contact with their prey. Medusae were tested in a flow-through aquarium with inflow at each end and a central outflow. Aurelia aurita and Aequorea victoria were attracted to either end of the chamber if Artemia prey were present in a screened compartment. A. aurita was also shown to be attracted to water conditioned by Artemia, and to ammonium chloride added to one or other of the inflow currents.     

Nematocyst composition of the cubomedusan Chiropsalmus quadrigatuschanges with growth

The nematocysts of Chiropsalmus quadrigatus (Cubozoa; Cubomedusa; Chirodropidae) were examined to determine if their composition changes with an increase in body size. Fixed tentacles of specimens collected in Okinawa, Japan, were homogenized and their nematocysts were observed under a differential interference contrast microscope. Six nematocyst types were observed in medusae of all sizes microbasic mastigophores (MM), large and small trirhopaloids (lTR and sTR), holotrichous isorhizas (HI), ellipsoidal isorhizas (eI), and ovoid isorhizas (oI). Two other nematocysts, large ovoid isorhizas (loI) and microbasic euryteles (ME), were observed only in small individuals. There was also marked difference in proportion of tentacular nematocysts between small and large individuals. HI was the dominant type in small specimens, while MM and eI were predominant in large specimens. Nematocyst composition in the bell and pedalia also differed between small and large individuals. Bells of small medusae contained oI and sTR, while only oI were observed in most large individuals. The pedalia of small medusae had clusters of MM, ME, sTR, and oI. Such single clusters on pedalium bases were characteristic of small individuals. The pedalia of large individuals contained scattered oI. Tentacles of medusae are used for prey capture, so the changes in the major type of nematocysts in tentacles may reflect changes in prey type.     

Nematocysts of Rhopilema nomadica (Scyphozoa: Rhizostomeae), an immigrant jellyfish in the eastern mediterranean

Rhopilema nomadica—a recently discovered scyphomedusa in the eastern Mediterranean—is considered a lessepsian migrant. Its nematocysts were extracted from the scapular and mouth-arm tentacles and examined using light and electron microscopy techniques. The morphometric parameters of the nematocysts were measured before and after complete discharge. Three categories of nematocysts were identified: heterotrichous isorhiza haploneme, holotrichous isorhiza haploneme, and heterotrichous microbasic eurytele. The relative abundance of the nematocysts and their occurrence in tissues of the jellyfish were noted. A brief discussion concerning the classification of certain types of nematocysts is given. A comparison with the available data on other Rhopilema species revealed that the nematocyst categories of R. nomadica are more similar to those of the Atlantic R. verrilli than to those of the Western Pacific R. esculentum. A brief comparison of the injuries caused by these species is given. © 1995 Wiley-Liss, Inc.     

Realized trophic niche driven by apparent competition: an example with marsupials

According to apparent competition theory, the co‐occurrence of two species that share the same predators appears to affect each other's population growth and abundance. However, due to habitat loss and over‐hunting, top predators are being made rare worldwide. Considering that apparent competitors share similar resources, we would expect the absence of top predators to reflect in changes on prey realized trophic niches. To test our hypothesis, we developed a model to predict the abundance ratio of apparent competitor species based on changes in their realized trophic niches. We tested our model against field data on the Neotropical marsupials Didelphis aurita and Metachirus nudicaudatus. Our results revealed that D. aurita and M. nudicaudatus are two species under apparent competition and their realized trophic niche and diet overlap change according to the presence of top predators. The model was able to predict the actual relative abundances of D. aurita and M. nudicaudatus in the three empirical studies analyzed. Our study presents quantitative support to the apparent competition theory; however, the model's applications to other groups still need to be verified. Additionally, our study shows that the lack of top predators has consequences on the realized trophic niche of their prey, and therefore, we reinforce that conservation plans need to focus on the effects of top predator loss on ecosystems.     

Retention, capture and consumption of experimental prey by orb-web weaving spiders in coffee plantations of Southern Mexico

This study focuses on the predatory capacity of four sympatric species of web- building spiders that inhabit coffee plantations in Southern Mexico: Gasteracantha cancriformis, Cyclosa caroli, and the morphologically similar species pair Leucauge mariana and L. venusta which were considered as one species group. The retention capabilities of the webs of these species and the incidence of prey capture and consumption were measured using eight types of insect prey belonging to the orders Coleoptera (1 species), Hymenoptera (3), Diptera (2) Lepidoptera (1) and Homoptera (1). The different characteristics of each prey such as body weight, body size, defensive behaviour, etc., were recorded. The incidence of prey retention, capture and consumption were significantly higher in G. cancriformis than in any of the other species. The lowest rates of retention, capture and consumption were observed in C. caroli, while L. mariana/venusta were intermediate in their predatory capabilities. Significant negative correlations between prey size and percent consumption were detected in L. mariana/venusta and in G. cancriformis; in both cases, large prey were less likely to be immediately consumed than small prey items. The results can be interpreted in the light of the morphological characteristics of the spiders. G. cancriformis possesses long legs and a carapace and appeared to have few difficulties to manipulate all types of prey. In contrast, C. caroli showed lesser abilities to manipulate and subdue aggressive prey items, perhaps due to the short leg length and unprotected body of this species. The consumption of prey items may be related to the predatory strategy of each spider. G. cancriformis constructs a new web every morning and prey storage was never observed. The absence of prey storage behaviour could explain why this species consumes prey soon after capture. In contrast, C. caroli constructs a permanent web and stores captured prey on a stabilimentum that may explain the very low incidence of immediate consumption of prey observed in this species.