Diet,food preference,and algal availability for fishes and crabs on intertidal reef communities in southern California

Synopsis Herbivory by wide-ranging fishes is common over tropical reefs, but rare in temperate latitudes where the effects of herbivorous fishes are thought to be minimal. Along the west coast of North America, herbivory by fishes on nearshore reefs is largely restricted to a few members of the Kyphosidae, distributed south of Pt. Conception. This paper presents information on natural diets and results from feeding choice experiments for two abundant kyphosids from intertidal habitats in San Diego, California —Girella nigricans andHermosilla azurea, and similar data for the lined shore crab,Pachygrapsus crassipes, which also forages over intertidal reefs. These results are compared with the availability of algae in intertidal habitats measured during summer and winter, on both disturbed and undisturbed habitats. The diets of juveniles ofG. nigricans andH. azurea collected from nearshore habitats were dominated by animal prey (mainly amphipods), but adults of these fishes, andP. crassipes, consumed algae nearly exclusively, with 26, 10, and 14 taxa of algae identified fromG. nigricans, H. azurea, andP. crassipes, respectively. Algae with sheet-like morphologies (e.g.Ulva sp.,Enteromorpha sp., members of the Delesseriaceae) were the principal algae in the diets of the fishes, and calcareous algae (e.g.Corallina sp.,Lithothrix aspergillum) and sheet-like algae (Enteromorpha sp.) comprised the greatest identifiable portion of the shore crab's diet. Feeding choice experiments indicated that the fishes preferred filamentous algae (e.g.Centroceras clavulatum, Polysiphonia sp.,Chondria californica) and sheet-like algae (e.g.Enteromorpha sp.,Ulva sp.,Cryptopleura crispa) over other algal morphologies, whereas the shore crab chose jointed calcareous algae (e.g.Lithothrix aspergillum, Corallina vancouveriensis, Jania sp.) most frequently. The diets and preferences for algae by the fishes were generally most similar to the assemblage of algae available in early successional (disturbed) habitats during summer when sheet-like and filamentous algae are abundant. The shore crab exhibited the opposite trend with a diet more similar to late successional (undisturbed) habitats.     

Interaction mechanisms between Gracilaria chilensis (Rhodophyta) and epiphytes

Epiphytes can have a considerable effect on Gracilaria production, and Ulva is one of the commonest algal species identified as an epiphyte, reaching loads of 60% (g of epiphytes per g of Gracilaria) in the intertidal cultures of southern Chile. This study evaluates the relative importance of light reduction, addition of weight to the host thalli and nutrient depletion, as mechanisms determining the interaction effects of Ulva epiphytes on Gracilaria cultivation. Using field experiments undertaken during the main Gracilaria growth season (spring), we evaluate the mechanisms of epiphyte-host algae interaction by manipulating artificial epiphytes. The results indicate that Ulva can significantly depress Gracilaria biomass production and that the addition of weight to the host algae and the consequent dislodgement increase, appear to be the main mechanisms involved in the Ulva-Gracilaria interaction. However, the light reduction caused by the epiphytes can also partially explain the reduction in Gracilaria production. Nutrients depletion would not appear to fully account for the detrimental effects of Ulva over Gracilaria in intertidal farming areas of southern Chile.     

Acidity enhances the effectiveness of active chemical defensive secretions of sea hares, <Emphasis Type="Italic">Aplysia californica</Emphasis>, against spiny lobsters, <Emphasis Type="Italic">Panulirus interruptus</Emphasis>

Sea hares such as Aplysia californica, gastropod molluscs lacking a protective shell, can release a purple cloud of chemicals when vigorously attacked by predators. This active chemical defense is composed of two glandular secretions, ink and opaline, both of which contain an array of compounds. This secretion defends sea hares against predators such as California spiny lobsters Panulirus interruptus via multiple mechanisms, one of which is phagomimicry, in which secretions containing feeding chemicals attract and distract predators toward the secretion and away from the sea hare. We show here that ink and opaline are highly acidic, both having a pH of ∼5. We examined if the acidity of ink and opaline affects their phagomimetic properties. We tested behavioral and electrophysiological responses of chemoreceptor neurons in the olfactory and gustatory organs of P. interruptus, to ink and opaline of A. californica within their natural range of pH values, from ∼5 to 8. Both behavioral and electrophysiological responses to ink and opaline were enhanced at low pH, and low pH alone accounted for most of this effect. Our data suggest that acidity enhances the phagomimetic chemical defense of sea hares.     

Ulva (Chlorophyta,Ulvales) Biodiversity in the North Adriatic Sea (Mediterranean,Italy): Cryptic Species and New Introductions

Ulva Linnaeus (Ulvophyceae, Ulvales) is a genus of green algae widespread in different aquatic environments. Members of this genus show a very simple morphology and a certain degree of phenotypic plasticity, heavily influenced by environmental conditions, making difficult the delineation of species by morphological features alone. Most studies dealing with Ulva biodiversity in Mediterranean waters have been based only on morphological characters and a modern taxonomic revision of this genus in the Mediterranean is not available. We report here the results of an investigation on the diversity of Ulva in the North Adriatic Sea based on molecular analyses. Collections from three areas, two of which subject to intense shipping traffic, were examined, as well as historical collections of Ulva stored in the Herbarium Patavinum of the University of Padova, Italy. Molecular analyses based on partial sequences of the rbcL and tufA genes revealed the presence of six different species, often with overlapping morphologies: U. californica Wille, U. flexuosa Wulfen, U. rigida C. Agardh, U. compressa Linnaeus, U. pertusa Kjellman, and one probable new taxon. U. californica is a new record for the Mediterranean and U. pertusa is a new record for the Adriatic. Partial sequences obtained from historical collections show that most of the old specimens are referable to U. rigida. No specimens referable to the two alien species were found among the old herbarium specimens. The results indicate that the number of introduced seaweed species and their impact on Mediterranean communities have been underestimated, due to the difficulties in species identification of morphologically simple taxa as Ulva.     

In vitro recruitment of Ulva sp. and Enteromorpha sp. on gametophytic and tetrasporophytic thalli of four populations of Chondracanthuschamissoi from Chile

Chondracanthus chamissoi is a red alga which is acquiring an increasing economic importance in Chile and becoming a target species for cultivation. Because epiphytism is a major problem in the mariculture of seaweeds, the recruitment of Ulva sp. and Enteromorpha sp. on gametophytic (cystocarpic) and tetrasporophytic thalli of C. chamissoi was tested in vitro on four populations from different locations in Chile. For Ulva sp., the density, cover and length of the recruits varied between the reproductive phases of the host and among the studied populations of C. chamissoi. In most experiments, a larger number of epiphytic thalli was observed on gametophytic plants of C. chamissoi; populations from Calderilla and Lechagua had a higher resistance to epiphytism. For Enteromorpha sp., its ability to grow epiphytically on both phases of the host showed a greater variability, but was inferior to that of Ulva sp. The differential resistance to epiphytism in both reproductive phases and in plant origin indicates the possibility of obtaining selected strains of C. chamissoi with lower susceptibility to epiphytism that could be utilized in planning maricultural programs.     

Differential Parasitism of Native and Introduced Snails: Replacement of a Parasite Fauna

The role of parasites in a marine invasion was assessed by first examining regional patterns of trematode parasitism in the introduced Japanese mud snail, Batillaria cumingi (= B. attramentaria), in nearly all of its introduced range along the Pacific Coast of North America. Only one parasite species, which was itself a non-native species, Cercaria batillariae was recovered. Its prevalence ranged from 3 to 86%. Trematode diversity and prevalence in B. cumingi and a native sympatric mud snail, Cerithidea californica, were also compared in Bolinas Lagoon, California. Prevalence of larval trematodes infecting snails as first intermediate hosts was not significantly different (14% in B. cumingi vs 15% in C. californica). However, while the non-native snail was parasitized only by one introduced trematode species, the native snail was parasitized by 10 native trematode species. Furthermore, only the native, C. californica, was infected as a second intermediate host, by Acanthoparyphium spinulosum(78% prevalence). Given the high host specificity of trematodes for first intermediate hosts, in marshes where B. cumingi is competitively excluding C. californica, 10 or more native trematodes will also become locally extinct.     

Rapid experimental shift in host use traits of a polyphagous marine herbivore reveals fitness costs on alternative hosts

The host breadth of any particular herbivore reflects a compromise between evolutionary forces that promote specialism and those that promote polyphagy. Because most terrestrial herbivorous insects specialize, explorations of this evolutionary balance have focused largely on specialist than on polyphagous herbivores. Here, we experimentally tested whether fitness-based tradeoffs in utilizing alternative hosts can be detected within a polyphagous marine herbivore. The marine amphipod Ampithoe longimana occurs on multiple seaweeds year-round (especially the genera Sargassum, Ulva and Hypnea), but is particularly abundant on the diterpene-rich genus Dictyota during warmer summer months. If fitness-based tradeoffs in using these alternative hosts are present, A. longimana may experience fluctuating selection across seasons. To test this possibility, we performed a controlled natural-selection experiment in which amphipods were isolated on Dictyota or a mixed seaweed assemblage that did not include Dictyota. Within 15 weeks (less than five overlapping generations), Dictyota-lines had greater feeding tolerance for Dictyota and its secondary metabolites than did mixed-seaweed-lines. Dictyota-line females reproduced more quickly than did mixed-seaweed-line females on Dictyota, but mixed-seaweed-line juveniles had greater growth on Sargassum and Ulva and higher fecundity on all hosts than did Dictyota-line juveniles. While experimental shifts in preference and performance are likely genetically-mediated, our experimental protocol does not preclude a role for phenotypic plasticity. The presence of a fitness cost to evolving greater preference for Dictyota suggests that fluctuating selection may operate on feeding preference across seasons, but our test of this hypothesis was equivocal. We suggest that one reason that polyphagy persists within A. longimana and potentially other marine grazers is because polyphagy broadens resource use across seasons, and this benefit outweighs the fitness-based costs that can favor specialism. Our results also reinforce the notion that timescales of ecological and evolutionary dynamics can overlap.     

PRELIMINARY STUDIES OF SEASONALITY,ECOLOGY, AND SPECIES COMPOSITION OF ULVOID ALGAL BLOOMS IN WASHINGTON STATE

Blooms of green macroalgae can devastate important finfish and shellfish habitats. Ulvaria obscura, a relatively unstudied green alga, is a major contributor to these blooms in the San Juan Islands, Washington State, USA. The biomass and productivity of this and other ulvoid algae were measured seasonally for two years. Experiments comparing the growth rates, responses to desiccation, photoacclimation, and grazer preference of U. obscura and Ulva fenestrata were conducted. Ulvaria blooms tended to occur in the subtidal while Ulva blooms were often intertidal. Both genera bloomed between late June and September. Despite their superficial similarity, Ulvaria and Ulva display markedly different physiological and ecological responses. Ulva was capable of faster growth, had higher rates of photosynthesis, and was more desiccation tolerant than Ulvaria. Ulvaria, however, appears to be more resistant to grazing than Ulva.     

Dietary nitrogen availability in macroalgae enhances growth of the sea hare Aplysia californica (Opisthobranchia: Anaspidea)

Evidence suggests that marine herbivores select for prey items with elevated nitrogen content. We tested this hypothesis with experimental growth studies of the herbivorous gastropod Aplysia californica offered diets of the rhodophyte Gracilaria ferox with varying nitrogen content. A. californica had a sevenfold feeding preference by weight for G. ferox with higher tissue % N and % protein, and lower % C, % carbohydrate and carbon-to-nitrogen ratio (C/N) as compared to treatments with lower nitrogen and protein content. A. californica provided treatment diets of varying nitrogen availability (high, medium and low) also had significantly different growth rates within 30 days. The high N diet supported a two-fold higher growth rate than that of the medium N diet and four-fold higher than the low N treatment, with mean weights over the experiment reaching 20.4, 9.8, and 5.6 g, respectively. The evolutionary value of this dietary preference may facilitate faster growth to reproductive size, outgrowth of predators and sequestration of organic compounds from nitrogen-enriched macroalgae to deter predators. Despite recent attention, the importance of diet-derived compounds as anti-predatory chemical defenses in Aplysiids remains equivocal. Nitrogen-enriched macroalgal diets, however, may provide “primary metabolites” that serve as alternative defenses for Aplysiids.     

Host plant trichomes and the advantage of being big: progeny size variation of the pipevine swallowtail

1. Plants possess numerous traits that confer resistance against insect herbivores, and herbivores, in turn, can evolve traits to ameliorate the effectiveness of these traits. The pipevine swallowtail, Battus philenor, is an extreme specialist on plants in the genus Aristolochia. The only host plant available to the California population of B. philenor is A. californica. Aristolochia californica is distinct from most other B. philenor host plants in that it is pubescent. 2. The progeny of B. philenor are larger in California compared with populations examined in Texas. Size differences persist throughout larval development. 3. Regardless of maternal host plant, population differences in progeny size persist, and crosses between California (large progeny) and Texas (small progeny) B. philenor populations resulted in offspring producing intermediate sized progeny, indicating a heritable component to progeny size variation. 4. California neonate caterpillars more easily overcame the trichomes of A. californica compared with Texas neonates. When trichomes were removed from A. californica, time to feeding establishment was reduced for caterpillars from both populations. Texas caterpillars established feeding sites on A. californica with trichomes removed, in the same time required to establish feeding on their non‐pubescent host plant, A. erecta. 5. This study shows that plant trichomes might impose selection pressure on progeny size.     

The central nervous system of Bulla gouldiana: Peptide localization

In the present study, we describe the structure of the central nervous system (CNS) of the marine gastropod Bulla gouldiana, and compare it with the structure of the CNS of the related mollusc, Aplysia californica. In addition, we performed an immunohistochemical analysis of a series of peptides, and the synaptic vesicle protein, synapsin I, in the central nervous system of B. gouldiana. The most common peptide in the B. gouldiana nervous system is the molluscan cardioexcitatory peptide (FMRFamide), which is present in a significant proportion of B. gouldiana neurons. A smaller number of neurons exhibit immunoreactivity to antisera raised against the calcitonin gene related peptide, vasopressin, vasoactive intestinal peptide, cholecystokinin, galanin and enkephalin. In some instances there is colocalization of two or more peptides. Very few neurons or axons exhibit synapsin I-like immunoreactivity. The patterns of immunoreactivity to these antisera is quite similar to the patterns that have been described in other gastropods, including Lymnaea stagnalis and Aplysia californica. These observations emphasize the importance of FMRFamide-like compounds in phylogenetically old nervous systems and indicate that compounds similar to mammalian peptides are present in the gastropod. Thus, the production of a wide variety of peptide molecules and their use in neuronal function appears to be a highly conserved phylogenetic process.     

Spatial distribution of interacting insect predators: Possible roles of intraguild predation and the surrounding habitat

Predator foraging behaviour affects the outcome of enemy–enemy interactions. Using a combination of fieldwork and laboratory experiments, we show that intraguild predation may be important in the field distribution of generalist predators that share a common prey: the eggs (and larvae) of the leaf beetle Phratora vulgatissima, a major insect pest in coppicing willow plantations. We focused on a species from the hoverfly genus Parasyrphus (Syrphidae), which may exhibit large temporal and spatial variation in density. Predator and prey densities were quantified in 40 field plots in willow plantations. The likelihood of finding hoverfly eggs declined with increasing densities of two predatory mirids, Orthotylus marginalis and Closterotomus fulvomaculatus, which exhibit less mobile behaviour similar to that of hoverfly larvae. The density of a more mobile predatory bug species, the anthocorid Anthocoris nemorum, was not associated with hoverfly occurrence. These results corroborate the hypothesis that less mobile predators should be stronger intraguild predators than mobilepredators. Further partial support for this hypothesis was obtained in the laboratory study where individual predators were presented with clutches of P. vulgatissima eggs containing one hoverfly egg: the less mobile C. fulvomaculatus and O. marginalis tended to consume the hoverfly egg more readily than the more mobile A. nemorum. However, most individuals of all three bug species consumed the egg of the potential competitor – the syrphid – within 24 h. The field study also showed that hoverfly occurrence was positively associated with the density of their prey and with the presence of nearby forests. We conclude that intraguild predation, abundance of prey and the surrounding habitat affect the distribution of hoverflies in this system and should be considered when developing biological control methods.     

Gracilaria conferta and its epiphytes: (2) Interrelationship between the red seaweed and Ulva cf. lactuca

Ulva cf. lactuca has been a disturbing competitor of experimental Gracilaria conferta outdoor cultures in Israel. The effect of environmental conditions on the competitive ability of Ulva versus Gracilaria, and the main limiting factors for which these seaweeds compete, were studied here. Single and biculture experiments of both seaweeds showed that Ulva outgrew and damaged Gracilaria under all irradiance and temperature combinations. The higher competitive ability of Ulva cf. lactuca in bicultures was not a result of responses to shading or nitrogen shortage, but rather to a shortage of available inorganic carbon, an increase in pH and apparent excretions of Ulva which inhibited the growth of Gracilaria.     

Systematics of green algae resembling Ulva conglobata,with a description of Ulva adhaerens sp. nov. (Ulvales,Ulvophyceae)

A phylogenetic and morphological study of green algae resembling Ulva conglobata from Japan was undertaken, along with morphological observations of the original material of U. conglobata Kjellman. The samples resembling U. conglobata included five genetically distinct species: U. fasciata, U. pertusa, U. tanneri, Ulva sp. 1 and Ulva sp. 2. The discovery of marginal denticulations in some of the original material of U. conglobata, made it possible to distinguish those species without denticulations: U. pertusa, U. tanneri and Ulva sp. 2. The morphological characteristics of Ulva sp. 1 matched those of U. conglobata, but Ulva sp. 1 was not clearly identified as U. conglobata owing to the lack of DNA sequence data of the original material. Ulva sp. 2 had lobes adhering to each other by rhizoids. This morphological feature is stable in Ulva sp. 2 and unique among Ulva species. In conjunction with the molecular data, Ulva sp. 2 was described as a new species, U. adhaerens sp. nov. This species features rhizoidal extensions in regions other than the base and an elaborate arrangement of the extensions used for adhesion. It thereby expands our knowledge of the morphogenesis of the morphologically simple genus Ulva.     

The effect of different nitrogen and carbon sources on amino acid synthesis in Ulva,Dictyota and Pterocladia

Summary This investigation includes a study of the effect of ammonium salt, nitrate and urea as nitrogen sources; vitamin B₆ as cofactor in transamination, and of acetate, pyruvate and glucose as carbon sources on the dry weight, total nitrogen and amino acid synthesis in Ulva, Dictyota and Pterocladia. The results showed that urea and to a lesser extent ammonium salt were better nitrogen sources for either Ulva or Pterocladia, while ammonium salt was best for Dictyota. Vitamin B₆ was effective in transaminations and resynthesis of amino acids in the three marine algae, especially Ulva. Pyruvate was a better carbon source than either acetate or glucose in increasing dry weights, total nitrogen and amino acid synthesis in Ulva and Dictyota, whereas acetate was best in Pterocladia.     

Biotic resistance experienced by an invasive crustacean in a temperate estuary

Communities high in species diversity tend to be more successful in resisting invaders than those low in species diversity. It has been proposed that the biotic resistance offered by native predators, competitors and disease organisms plays a role. In Yaquina Bay, Oregon, we observed very little overlap in the distribution of the invasive European green crab, Carcinus maenas, and the larger red rock crab, Cancer productus. C. productus dominates the more saline, cooler lower estuary and C. maenas, the less saline, warmer upper estuary. Because caged C. maenas survive well in the lower estuary, we decided to test the hypothesis that C. productus prey on C. maenas and thus contribute to their exclusion from the more physically benign lower estuary. A laboratory species interaction experiment was designed to determine whether C. productus preys on smaller C. maenas at a higher rate than on smaller crabs of their own species. Crabs of both species were collected and sorted by weight into three size classes: small, medium and large. Small and medium crabs of both species were paired with C. maenas and C. productus of various sizes. When conspecifics were paired, mortality was less than 14%, even in the presence of larger crabs. Smaller C. productus survived well in the presence of larger C. maenas, but the reverse was not true. When small C. maenas (60–67 mm carapace width) were matched with medium and large C. productus, their mortality increased to 52% and 76%, respectively. A less dramatic pattern was observed for medium C. maenas (73–80 mm) in the presence of medium and large C. productus. Thus on the West Coast of North America, the more aggressive red rock crab, C. productus, has the potential to reduce the abundance of C. maenas in the more saline and cooler lower estuaries.     

Effect of grazing by isopods and amphipods on growth of Ulva spp. (Chlorophyta)

Eutrophication of shallow coastal waters often leads to blooms of macroalgae. Grazing by crustaceans, such as amphipods and isopods, can reduce macroalgal biomass accumulation. At the same time, growth of the macroalgae can be stimulated by epiphyte removal. The role of grazing by isopods and amphipods on Ulva spp. biomass development was investigated in the Veerse Meer, a brackish lagoon situated in the southwest Netherlands. Exclusion of grazing in the field did not stimulate Ulva spp. growth. In fact, growth rates were higher in exclosures that allowed grazers to enter. Edibility tests identified the amphipod Gammarus locusta, and the isopods Idotea chelipes and Sphaeroma hookeri as potential grazers on Ulva spp. However, when epiphytic diatoms were present on the Ulva spp. thalli, Gammarus and Sphaeroma grazed on ephiphytes and not on Ulva tissue. Only Idotea continued to graze on Ulva spp. A laboratory growth experiment revealed a positive effect of Gammarus presence on Ulva spp. growth, probably caused by preferential removal of epiphytic diatoms from the Ulva spp. thalli. The growth stimulation by epiphyte removing grazers such as Gammarus may explain the higher growth rates in the presence of grazers observed in the field. When determining the potential role of invertebrate grazers in controlling macroalgal biomass accumulation, it is important to include an assessment of the epiphyte abundance on the macroalgae, as preferential removal of epiphytes may stimulate growth and thus have the opposite effect.     

Some effects of pre-release host-plant on the biological control of Panonychus ulmi by the predatory mite Amblyseius fallacis

Amblyseius fallacis Garman has been selected for pyrethroid resistance and mass reared for experimental release as a biological control agent for tetranychid mites on a number of crops in Canada. Several releases of this predator onto apple and peach trees have failed to result in the establishment of A. fallacis, or in the biological control of Panonychus ulmi Koch. Here, we test the hypothesis that the change of host-plant at the time of release is a critical factor in the establishment of A. fallacis for biological control of P. ulmi. Functional and numerical response studies were undertaken on two populations of A. fallacis: a wild strain collected from the canopy foliage of an apple orchard near Vineland, Ontario; and a second strain reared on bean plants in a commercial insectary with Tetranychus urticae as prey. Each population consumed significantly more P. ulmi and produced significantly more eggs when on leaf disks from the plant species they were reared on, than on leaf disks from the novel host plant. A further experiment was conducted to determine if establishment and biological control of mass-reared A. fallacis could be affected by rearing a population for a short term on apple leaves prior to release on apple trees. Three release treatments were made into potted apple trees in a glasshouse, using predators commercially mass-reared on bean and T. urticae: A. fallacis released directly; A. fallacis reared in the laboratory for four weeks on bean and T. urticae; A. fallacis reared on apple leaves and T. urticae for four weeks. They were compared with a control treatment lacking predator release. Contrary to results of the functional and numerical response studies, no difference was observed between release treatments. All release treatments adding A. fallacis resulted in a similar, if limited, degree of biological control of P. ulmi. These results indicated that there may be short-term effects of host plant on the establishment of A. fallacis and biological control of P. ulmi, which in our study were observed as an initial reduction of the predatory response. However, in a test, the predators appeared to overcome these short-term effects and successfully established on the new host-plant to control P. ulmi.