Prey nutritional quality and the effectiveness of chemical defenses against tropical reef fishes

Summary Many coral-reef seaweeds and sessile invertebrates produce both secondary chemicals and mineral or fibrous skeletal materials that can reduce their susceptibility to consumers. Although skeletal materials often have been assumed to function as physical defenses, their deterrent effectiveness may derive from their reduction of prey nutritional quality as well as from noxiousness of the skeletal material itself. To test the relative importance of prey nutritional quality and chemical defenses in susceptibility to predation, we offered reef fishes on Guam a choice of artificial foods varying in nutritional quality (4% versus 22% protein) and in secondary chemistry (spanning approximately natural concentration ranges). Field feeding assays were performed with pachydictyol A from the pantropical brown seaweed genus Dictyota, manoalide from the Micronesian sponge Luffariella variabilis, and a brominated diphenyl ether from the Micronesian sponge Dysidea sp. The results indicated that chemical defenses were less effective in high- than in low-quality foods. In paired assays with metabolite-free controls, all three compounds at natural concentrations significantly reduced feeding by reef fishes only in assays using low-quality food, and not in assays with high-quality food. When fishes were offered an array of artificial foods varying in both food quality and metabolite concentration, food quality significantly affected fish feeding in all three cases, while secondary chemistry was significant in only one. Thus differences in nutritional quality, within the natural range among reef organisms, can be comparable to or greater in importance than secondary chemistry in affecting feeding preferences of their consumers. Reduced nutritional quality may be an important selective advantage of producing indigestible structural materials, in addition to their roles as physical support and defense, in coral reef organisms.     

Sponge community structure and anti-predator defenses on temperate reefs of the South Atlantic Bight

Predator–prey interactions can play a significant role in shaping the structure of both terrestrial and marine communities. Sponges are major contributors to benthic community structure on temperate reefs and although several studies have investigated how abiotic processes control sponge distributions on these reefs, the role of predation is less clear. We investigated the relationship between sponge predators and the distribution of sponges on temperate reefs in the South Atlantic Bight (SAB), off Georgia, USA. We documented sponge species richness and abundance, spongivorous fish density, and examined the ability of 19 sponge species to chemically and structurally deter predation by fishes. We also conducted reciprocal transplant experiments to determine if predation by fishes contributes to the observed zonation of sponge species on these reefs. Our surveys revealed two distinct sponge assemblages: one characterized by amorphous and encrusting sponge morphotypes colonizing the vertical, rocky outcroppings (scarp sponge community), while the other consisted of pedunculate, digitate, and arborescent growth forms occurring on the sediment-laden reef top (plateau sponge community). Spongivorous fishes were more abundant on the scarp than the plateau and scarp sponges were found to be more effective than plateau sponges at chemically deterring generalist fishes. In contrast, plateau sponges were more reliant on structural defenses: a result consistent with the higher spicule content of their skeletons. Transplant experiments confirmed that predators prevent some plateau sponges from colonizing the scarp even though they possess structural defenses. Thus, predation appears to play a role in shaping sponge community structure on SAB reefs by restricting those species lacking adequate chemical defenses to habitats where there is a paucity of spongivores.     

Allocation of chemical and structural defenses in the sponge Melophlus sarasinorum

Sponges have evolved a variety of chemical and structural defense mechanisms to avoid predation. While chemical defense is well established in sponges, studies on structural defense are rare and with ambiguous results. We used field and laboratory experiments to investigate predation patterns and the anti-predatory defense mechanisms of the sponge Melophlus sarasinorum, a common inhabitant of Indo-pacific coral reefs. Specifically, we aimed to investigate whether M. sarasinorum is chemically or structurally defended against predation and if the defenses are expressed differently in the ectosomal and choanosomal tissue of the sponge. Chemical defense was measured as feeding deterrence, structural defense as feeding deterrence and toughness. Our results demonstrated that chemical defense is evenly distributed throughout the sponge and works in conjunction with a structurally defended ectosome to further reduce predation levels. The choanosome of the sponge contained higher protein levels, but revealed no structural defense. We conclude that the equal distribution of chemical defenses throughout M. sarasinorum is in accordance with Optimal Defense Theory (ODT) in regards to fish predation, while structural defense supports ODT by being restricted to the surface layer which experiences the highest predation risks from mesograzers.     

Interspecific variation in chemical defenses in the sea hares (Opisthobranchia: Anaspidea)

Most species of sea hares (Opisthobranchia: Anaspidea) sequester secondary metabolites from their algal diets in their digestive glands. Aplysia Juliana Quoy and Gaimard, 1832, a sea hare that feeds on Ulva spp. and Enteromorpha spp., algae with few or no secondary metabolites, were compared with the sympatric sea hares A. oculifera Adams and Reeve, 1850, A. kurodai (Baba, 1937), and Dolabella auricularia (Solander, 1786), all of which eat chemically rich algae, to see if sequestered secondary metabolites afford protection to sea hares from potential predators. Organic extracts of whole A. Juliana stimulated, and organic extracts of whole D. auricularia deterred feeding by crabs. However, tests with organic extracts of individual body parts indicated that this pattern was due almost exclusively to unpalatability of extracts of D. auricularia digestive glands. Tests with pieces of tissue from the exterior of the animals, or with extracts of such tissues, showed no consistent patterns indicating that A. Juliana were more palatable than other sea hares. Sea hare egg masses do not appear to contain diet-derived secondary metabolites. However, pieces of egg masses of A. Juliana and D. auricularia were universally rejected by crabs and reef fish, and extracts of A. Juliana egg masses deterred feeding by some reef fish. Finally, both opaline secretion of A. Juliana and ink of A. kurodai, but not ink of D. auricularia, none of which appear to contain diet-derived secondary metabolites, deterred feeding by crabs. Opaline secretion from A. Juliana, but not ink from A. kurodai, induced avoidance behavior in crabs. Although sequestered secondary metabolites clearly can affect the palatability of the digestive gland, there is little evidence that they affect the palatibility of the ink, opaline secretion, eggs, or skin, suggesting that sequestered secondary metabolites may not play a key role in anti-predator defense of sea hares.     

Testing for defensive synergy in Caribbean sponges: Bad taste or glass spicules?

Chemical and physical defenses of sessile organisms against consumers are well described for both terrestrial and marine systems. However, previous studies have focused on chemical or physical defenses in isolation, and have not considered their interaction. Marine sponges provide a model system for testing this interaction. Some sponge species produce secondary metabolites that deter predation; they may also contain siliceous spicules, but previous studies have provided little evidence that spicules in isolation offer any defense against generalist fish predators. To determine whether the two components have an additive, antagonistic, or synergistic interaction, crude organic extracts and spicules from individuals of 8 Caribbean sponge species were isolated and tested in laboratory feeding assays. These included one chemically defended reef sponge (Agelas clathrodes) and seven known to be intermediately deterrent: six from reef habitats (Cinachyrella alloclada, Clathria virgultosa, Cribrochalina infundibulum, Niphates digitalis, Svenzea zeai, and Xestospongia muta) and one from mangrove habitats (Tedania ignis). Extracts and spicules were assayed at various concentrations, both individually and in combination, in laboratory feeding assays with the bluehead wrasse, Thalassoma bifasciatum. A SAS based GENMOD procedure based on an isobolographic analysis model was used for statistical comparisons. Four sponges (A. clathrodes, C. alloclada, C. virgultosa, and one of three individuals of X. muta) showed evidence of synergisms. Of these, synergy in C. alloclada, C. virgultosa, and X. muta was caused by approximately natural concentrations of extracts and spicules. The extract of A. clathrodes was deterrent, but combination assays required nearly a 3-fold reduction in extract concentration and an 8-fold increase in spicule concentration to show the synergistic effect. Contrary to previous findings, spicules from C. infundibulum and two of three individuals of X. muta were deterrent at natural concentrations. Sponge spicules may be defensive in isolation, or may enhance chemical defenses against consumers, but the lack of synergisms for individuals in 4 of 7 species with intermediate levels of chemical defense suggests that defensive synergy is not the general rule and, when present, may be an example of an exaptation.     

Tissue-specific palatability and chemical defenses against macropredators and pathogens in the common articulate brachiopod Liothyrella uva from the Antarctic Peninsula

The punctate terebratulid brachiopod Liothyrella uva is the most common brachiopod species in Antarctica. Whole brachiopods, either live or freeze dried and ground into a powder and suspended in alginate, were unpalatable to the sympatric macropredators Odontaster validus (an abundant, omnivorous sea star) and Notothenia coriiceps (an abundant, omnivorous, epibenthic fish). The unpalatability of these ground tissues coupled with that of lipophilic extracts of whole L. uva presented in alginate pellets to O. validus, suggests an involvement of chemical defenses. Several isolated brachiopod tissues were also unpalatable to O. validus after being freeze dried, ground and suspended in alginate, but only the pedicle was unpalatable in such preparations to both O. validus and N. coriiceps. This observation is consistent with the Optimal Defense Theory since the pedicle is the only tissue not protected inside the brachiopod shell. There was, however, no correlation between the energetic content and unpalatability of any of the individual tissues. Organic extracts of tissues involved in feeding (lophophore and intestine–stomach) had relatively strong antimicrobial activity when assayed against several strains of Antarctic bacteria. However, the lophophore was palatable to both macropredators, suggesting nonoverlapping chemical defenses are involved in protection against predators and pathogens.     

Anti-predatory chemical defenses of ascidians: secondary metabolites or inorganic acids?

Both secondary metabolites and inorganic acids have been hypothesized to protect adult ascidians from predation, raising the possibility of alternative defensive strategies in these sessile, soft-bodied, benthic invertebrates. The objective of this investigation was to determine if ascidian species from the Western Atlantic have these chemical defenses against fish predators, and if so, to determine their location within the body of the ascidian. The palatability of crude organic extracts of whole ascidians, as well as the dissected tunics, viscera, and gonads (when possible) were determined at natural volumetric concentrations using laboratory feeding assays with the bluehead wrasse, Thalassoma bifasciatum. Acidified food pellets were also assayed to determine the effect of lowered pH on predation. Sixteen of the 17 species tested had deterrent organic extracts from some region of the body (Aplidium constellatum, Aplidium stellatum, Ascidia interrupta, Ascidia nigra, Botrylloides sp., Clavellina picta, Didemnum candidum, Didemnum vanderhosti, Diplosoma listerianum, Ecteinascidia turbinata, Eudistoma capsulatum, Eudistoma hepaticum, Rhopalaea abdominalis, Styela plicata, Symplegma rubra, and Trididemnum solidum). The location of the deterrent secondary metabolites was isolated in the gonad in all three solitary species, raising the possibility that these defenses are passed on to eggs or larvae. Nine ascidian species sequestered acid in their tunics (A. interrupta, A. nigra, A. stellatum, D. candidum, D. vanderhosti, E. capsulatum, E. hepaticum, R. abdominalis, and T. solidum) at levels that were effective in deterring fish predation (pH≤3.0). Only one species (Botrylloides nigrum) had neither chemical defense. Results of this study indicate that there is not a clear trade-off between the presence of secondary metabolites and inorganic acid defenses in ascidians, suggesting that these defenses are redundant, or that alternative chemical defenses may have evolved for different predators or for different stages in the life history of the ascidians producing them.     

Within-plant variation in seaweed palatability and chemical defenses: optimal defense theory versus the growth-differentiation balance hypothesis

Within-plant variation in the concentration of secondary metabolites, nutritive value, toughness, and susceptibility to herbivory was assessed for the brown alga Dictyota ciliolata. When young apices and older tissue from the same plant were offered in equal abundance to the herbivorous amphipod Ampithoe longimana and the sea urchin Arbacia punctulata, young apices were consumed about 2 times more than older tissue. Compared to young apices, the less preferred older tissue had a less palatable lipophilic extract, significantly higher concentrations of two secondary metabolites (another secondary metabolite did not differ significantly), 33% more soluble protein, and was 233% tougher. Higher levels of chemical defenses in older tissues, and not tissue toughness or nutritive value, appear to be responsible for the preference of Ampithoe longimana for young apices. The pattern of lower levels of chemical defenses in young than older tissues of D. ciliolata is the opposite of the pattern observed in coenocytic seaweeds and most vascular terrestrial and marine plants, all of which have translocation systems for moving materials among plant portions. Unlike these other plants, which preferentially allocate chemical defenses to young tissues, D. ciliolata cannot readily translocate secondary metabolites. The growth-differentiation balance hypothesis suggests that actively dividing and expanding cells are less able to produce secondary metabolites. This hypothesis may help explain why older tissues are better defended than young, rapidly growing apices.     

Chemical profile of adults and buds of the chemically defended marine sponge Tethya maza

Several adults and the corresponding larvae of marine sponges are known as rich sources of secondary metabolites. In this paper we will show the chemical profile of adults and buds of the sponge Tethya maza. Cholesterol, ergost-5,22-dienol-3, stigmast-5,24-dienol-3, cholest-5,22-dienol-3, cholest-5-enol-3-one-7, and stigmast-5,24(28)-dien-3-ol were the major compounds detected, two of them being detected only in crude extracts of the adults while one was present only in the buds. Due to this high similarity it is supposed that buds could be chemically protected with regards to predation as well as the adult individuals of T. maza. This is the first report of chemicals present in the structures (buds) of sponges produced by asexual reproduction.     

The biogeography of polyphenolic compounds in marine macroalgae: temperate brown algal defenses deter feeding by tropical herbivorous fishes

Summary Many tropical brown algae have low levels of polyphenolic compounds and are readily consumed by herbivorous fish. In contrast, temperate brown algae often produce large quantities of phenolic compounds causing them to be distasteful to herbivorous gastropods and sea urchins. We hypothesized that tropical brown algae do not use phenolic compounds as antiherbivore defenses because these compounds are not effective deterrents against tropical fish. To test our hypothesis, we assessed the ability of extracts from 8 tropical and 13 temperate algae with a broad range of phenolic levels to deter feeding by herbivorous fishes on Guam. Extracts of the high-phenolic (>2% d.w.) temperate brown algae consistently deterred feeding by herbivorous fishes, whereas extracts from low phenolic (<2% d.w.) temperate and 6 of 8 low-phenolic tropical brown algae did not. Thus, phenolic compounds could be effective feeding deterrents towards herbivorous fishes on Guam, but for unknown reasons they are not used by Guamanian brown algae.     

Density-dependent effects of prey defenses and predator offenses

Defenses protect prey, while offenses arm predators. Some defenses and offenses are constitutive (e.g. tortoise shells), while others are phenotypically plastic and not always expressed (e.g. neckteeth in water fleas). All of them are costly and only adaptive at certain prey densities. Here, I analyse such density-dependent effects, applying a functional response model to categorize defenses and offenses and qualitatively predict at which prey densities each category should evolve (if it is constitutive) or be expressed (if it is phenotypically plastic). The categories refer to the step of the predation cycle that a defense or offense affects: (1) search, (2) encounter, (3) detection, (4) attack, or (5) meal. For example, prey warning signals such as red coloration prevent predator attacks and are hence step 4 defenses, while sharp predator eyes enhance detection and are step 3 offenses. My theoretical analyses predict that step 1 defenses, which prevent predators from searching for their next meal (e.g. toxic substances), evolve or are expressed at intermediate prey densities. Other defenses, however, should be most beneficial at low prey densities. Regarding predators, step 1 offenses (e.g. immunity against prey toxins) are predicted to evolve or be expressed at high prey densities, other offenses at intermediate densities. I provide evidence from the literature that supports these predictions.     

Patterns in the production of antiherbivore chemical defenses in plant communities

The diversity of chemical identity and mode of action of toxic substances present in plants is suggested to be partially the result of generalist herbivore grazing pressure, while convergence in digestibility-reducing substances and their method of function is due primarily to specialist herbivore. Analysis of alkaloid patterns from herbaceous and woody perennials show that most species differ in their alkaloid composition and many sympatric species and subspecies show unique patterns. The high degree of functional convergence in digestibility-reducing substances is supported by convergent patterns in tannins among woody perennials.     

Ecological factors influencing the evolution of insects' chemical defenses

How insect defense chemicals have evolved has remained relativelyunderstudied, compared with the evolution of aposematic signalsof such defenses. Because there is mounting evidence that chemicaldefenses can generally be expected to be costly, understandingthe evolution of such defenses and their maintenance in theface of the potential for automimicry (signaling by individualsthat do not invest in defense) is nontrivial. One potentialexplanation is that chemically defended insects suffer lessfrom predation than those that do not invest in chemical defenses.Here, we use a series of models to explore aspects of the evolutionof such costly chemical defenses. Our models predict that investmentin costly defenses can occur across a wide range of predationintensities; however, if predation intensity is low, then thedefense has to be very effective to be selected, unless thedefense is very cheap. Furthermore, the evolution of antipredatorydefenses will be relatively insensitive to the severity of anymechanism, whereby prey pay a cost every time they use theirdefense against an attacking predator even if they survive theattack, but sensitive to the form of the relationship betweeninitial investment in constituting the defense and survivalbenefit. Once defense becomes common in the prey population,prey may get a frequency-dependent benefit if predators learnto avoid prey of this type after several attacks. Finally, wepredict that increasing the rate of avoidance learning by predatorsencourages reduced investment in antipredatory defenses by prey.The potential for these predictions to be tested empiricallyis discussed.     

Assessing early recruitment dynamics and its demographic consequences among tropical reef fishes: Accommodating variation in recruitment seasonally and longevity

Abstract When settlement of pelagic juveniles of reef fishes is highly and predictably seasonal, annual, end-of-season surveys of surviving recruits (which are commonly used on the Great Barrier Reef) are useful for assessing recruitment dynamics and their demographic effects. However, when settlement is continuous or weakly seasonal, with patterns that vary both between species and within species among years, regular, sometimes year-round, recruitment surveys at intervals linked to short-term settlement dynamics are needed to quantify fluctuations in recruitment strength. Monthly recruitment surveys may be appropriate in the tropical northwest Atlantic, where settlement is often both lunar periodic, and broadly and variably seasonal. Use of a variety of recruit-census methods impedes comparisons of recruitment patterns and their demographic effects, because recruit densities and recruit:adult ratios cannot be directly compared when recruits (because they have widely varying post-settlement ages) have experienced very different levels of early post-settlement mortality. Examining the relationship between changes in adult populations and annual, end-of-season recruitment may be satisfactory for long-lived species with strong settlement seasonality and maturation times of approximately 1 year. However, it is inappropriate for short-lived, rapidly maturing species, particularly those that have broad and variable settlement seasons and whose populations fluctuate substantially throughout the year in response to short-term fluctuations in recruitment. Comparisons of demographic effects of recruitment among species with different longevity require the use of non-arbitrary time scales, such as the time to maturity and the adult half-life.     

Biologic response to environmental stress in tropical reefs: Lessons from modern Polynesian coralgal atolls and Middle Permian sponge and Shamovella-microbe reefs (Capitan Limestone USA)

Despite prejudices that comparisons of paleoecological patterns in modern and fossil reef communities are of doubtful validity, we compare the biologic response of living coralgal reefs in French Polynesia to environmental stress with an exceptionally well exposed Middle Permian sponge reef and Shamovella-microbial reef of the Capitan Limestone in New Mexico. In the western Tuamotu Archipelago, reef margins are characterized by depth-related changes of biodiversity. The subtidal basic reefbuilding community contains the highest diversity (23 coral and 6 calcareous algal species). With decreasing water depth and increasing environmental stress, diversity reaches a minimum of five taxa on the reef flat. The Capitan consists of two reef stages. Reefbuilders of the lowermost exposed part of Stage 1 formed a cement-rich sponge reef with 42 taxa (28 sponge species). Decreasing water depth along the reef face is accompanied by loss of five taxa, variations in the gross morphology of sponges and changes in framework architecture. Stage 2, dominated by Shamovella obscura, one bryozoan species and microbes, is sandwiched between two unconformities suggesting much shallower water and higher environmental stress. Despite differences in shelf profile and taxonomy, both the modern and Permian reefbuilders respond to increasing environmental stress with diversity impoverishment and dominance of binders.     

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     

Aspects of the spawning of western Atlantic butterflyfishes (Pisces: Chaetodontidae)

Synopsis The status of knowledge of spawning among the five shallow waterChaetodon species in the western Atlantic is reviewed. Spawning has been observed for three species in Puerto Rico, St. Croix and the Bahamas, with possible courtship in a fourth.Chaetodon aculeatus spawned near the time of sunset over objects on the reef as single female/male pairs or as two females and one male, with pair spawning in rapid succession. Spawning occurred during much of the lunar month from February to April and it is uncertain whether any lunar periodicity to spawning exists. Male-male aggression was noted. Spawning sites (coral heads) were alternated daily and it is likely that females spawn only once every two days. A single female produced as many as 2090 eggs in a single spawning.Chaetodon capistratus spawned during much of the lunar month from February to April. It spawned about 5 min afterC. aculeatus, occasionally using the same sites, and alternated sites daily. A female produced as many as 3710 eggs in one spawning.Chaetodon striatus spawned from February to April but it is unknown if it has any lunar spawning cycle. No predation attempts by piscivores on spawning adults were seen. Predation byMelichthys niger on eggs ofC. striatus occurred. No egg predation was observed forC. aculeatus andC. capistratus. With an assumed four month reproductive season, alternate day spawning and observed egg production values,C. aculeatus andC. capistratus produce respectively about 100 000 and 200 000 eggs per large female per year. The reproductive strategy of smaller species may be to produce moderate numbers of eggs per day over a spawning season of at least a few months while larger species may produce more eggs per day for a shorter period.     

Condition dependence in biosynthesized chemical defenses of an aposematic and mimetic Heliconius butterfly

Aposematic animals advertise their toxicity or unpalatability with bright warning coloration. However, acquiring and maintaining chemical defenses can be energetically costly, and consequent associations with other important traits could shape chemical defense evolution. Here, we have tested whether chemical defenses are involved in energetic trade‐offs with other traits, or whether the levels of chemical defenses are condition dependent, by studying associations between biosynthesized cyanogenic toxicity and a suite of key life‐history and fitness traits in a Heliconius butterfly under a controlled laboratory setting. Heliconius butterflies are well known for the diversity of their warning color patterns and widespread mimicry and can both sequester the cyanogenic glucosides of their Passiflora host plants and biosynthesize these toxins de novo. We find energetically costly life‐history traits to be either unassociated or to show a general positive association with biosynthesized cyanogenic toxicity. More toxic individuals developed faster and had higher mass as adults and a tendency for increased lifespan and fecundity. These results thus indicate that toxicity level of adult butterflies may be dependent on individual condition, influenced by genetic background or earlier conditions, with maternal effects as one strong candidate mechanism. Additionally, toxicity was higher in older individuals, consistent with previous studies indicating accumulation of toxins with age. As toxicity level at death was independent of lifespan, cyanogenic glucoside compounds may have been recycled to release resources relevant for longevity in these long‐living butterflies. Understanding the origins and maintenance of variation in defenses is necessary in building a more complete picture of factors shaping the evolution of aposematic and mimetic systems.