Grazing rates of organic matter and living fungal biomass of decaying Spartina alterniflora by three species of salt-marsh invertebrates

 The pathway for the flow of salt-marsh grass production into marsh food-webs is still not well defined. We compared the abilities of three marsh macroinvertebrates [salt marsh periwinkles, Littoraria irrorata (Say) (=Littorina irrorata), salt-marsh coffee-bean snails, Melampus bidentatus (Say); and a talitrid amphipod, Uhlorchestia spartinophila Bounsfield and Heard] to access standing-dead leaves of smooth cordgrass (Spartina alterniflora Loisel). The invertebrates were incubated with naturally-decaying leaves, and the rates of removal of organic matter and living fungal biomass (ergosterol) were measured. The impact of invertebrate activity upon fungal growth rates was measured as rates of fungal-membrane synthesis (incorporation of radioacetate into ergosterol). The removal rates of organic leaf biomass per mg individual biomass were highest for amphipods (700 μg mg⁻¹ d⁻¹) and lowest for periwinkles (90 μg mg⁻¹ d⁻¹), but the relatively large biomass of the snails made their removal rates per individual greater than those of amphipods. Net removal of ergosterol by all three invertebrates was >50% for yellow-brown (early-decay) leaf blades. For fully-brown (advanced-decay) blades, >50% removal of ergosterol was found only for periwinkles; exposure to coffee-bean snails and amphipods resulted in a net ergosterol reduction of ≤20%. The lower net reduction of living fungal biomass by coffee-bean snails and amphipods may have been due to fungal-growth stimulation (2.3-fold stimulation in coffee-bean snails and 1.5-fold stimulation in amphipods). Grazing by periwinkles did not stimulate fungal growth, possibly because of its high intensity. Grazing by these three salt-marsh shredders may affect marsh-grass shoot-decay in different ways. Periwinkles may abbreviate the period of fungal production, and incorporate the decaying material relatively quickly into snail biomass and fecal-pellet rain to the sediments. Coffee-bean snails and amphipods may enhance and prolong fungal production, along with the formation of fecal-pellet rain. All three invertebrates fed preferentially on leaf blades rather than leaf sheaths, and feeding rates of gastropods were higher during the night than during the day. Received: 25 November 1998 / Accepted: 4 November 1999     

Uptake of organic material by aquatic invertebrates

Neanthes arenaceodentata (Moore) accumulates glycine –C¹⁴ from a dilute solution of seawater. After a 30 min exposure, 5 to 102 times as much radioactivity per unit volume is found in the animals (depending on the size and feeding stage of the worm) as is present in the medium. The relation between the log of cpm and log of weight is linear over 4 orders of magnitude variation in size. The rates of uptake were more variable in non-feeding stages of the life cycle. Non-feeding larvae showed rates of glycine accumulation which were significantly higher than those predicted from data on feeding stages.This work was supported in part by PHS Grant GM 12889 to the University of California, Irvine.     

Photosynthesis and respiration of exposed salt-marsh fucoids

Photosynthesis and respiration of the salt-marsh fucoids Ascophyllum nodosum ecad scorpioides and Fucus vesiculosus were investigated using an infrared CO₂ gas analyzer under a variety of light intensities, temperatures, and levels of desiccation while the algae were exposed to the atmosphere. Results indicated that net photosynthesis (0.5 to 2.0 mg C/g dry weight/h) saturated rapidly at light intensities (0.1 to 0.2 g cal/cm²/min) which were approximately 10 to 50% of the daily summer maximum intensities for algae found under phanerogam (Spartina alterniflora) canopies. Desiccation exhibited the most pronounced effect on photosynthesis, which increases slightly between 0 and 25% water loss, levels off, and decreases sharply at water losses greater than 50%. Dark respiration (0.1 to 0.3 mg C/g dry weight/h) is also inhibited by desiccation. Both species of algae appear to be broadly adapted to all three parameters investigated.This research was supported by research grants AG-375 and BO 38018 from the National Science Foundation and, in part, by the State University of New York Research Foundation and the Energy Research and Development Administration (ERDA).Communicated by M.R. Tripp, Newark     

Orientation in the intertidal salt-marsh collembolan Anurida maritima

We investigated the cues used by the intertidal insect Anurida maritima (Apterygota: Collembola) to orient to the appropriate zone in which to seek shelter during high tide. Our experiments clearly ruled out any significant role for magnetic, local topographic, slope or celestial cues. Instead, we suggest that the difference between the appearance of the up-shore and the down-shore horizon is the major cue used by the collembolans. When a mirror was used to duplicate either of the two horizons, the insects were not able to orient. The insects moved towards an artificially dark horizon (the reverse of the mirror) placed down-shore, the opposite of their usual direction of movement. The insects had an endogenous circatidal rhythm of phototactic behaviour: most of the population was always negatively phototactic, but between 2 and 7 h after low tide, a significant proportion of the population became positively phototactic. This is the first demonstration of an endogenous tidal rhythm of orientation in an insect. Received: 31 May 1999 / Received in revised form: 1 February 2000 / Accepted: 19 February 2000     

Reproductive patterns of three intertidal salt-marsh gammaridean amphipods

Among three sympatric species of epibenthic amphipods found at different tide marks at Jamaica Bay, New York (USA), the length of time juveniles spend with the mother increases and the number of juveniles per brood decreases as tidal height increases. Each brood has two developmental periods: (1) the embryonic period, from ovulation to hatching; (2) the juvenile period, from hatching to emergence from the marsupium. Gammarus palustris, found at the high-tide mark, has a mean juvenile period of 1.7 days and a mean brood size of 12.4 offspring; G. mucronatus, found at mean-tide mark, has a mean juvenile period of 0.8 days and a mean brood size of 27.4 offspring; Melita nitida, found at low-tide mark, has a mean juvenile period of 0.5 days and a mean brood size of 30.0 offspring. Further, the range of days that a juvenile may emerge is widest for G. palustris (0 to 8 days after hatching) and narrowest for M. nitida (0 to 2 days).This work was submitted in partial fulfillment of the requirements for the Ph.D. at the City University of New York.     

Uptake and metabolism of two amino acids by anaerobic microorganisms in four diverse salt-marsh soils

The anaerobic microbial uptake of alanine and aspartic acid was determined in 4 diverse salt-marsh soils (tall and short Spartina alterniflora, creek bank, and mud flat). Uptake in soil slurries was determined by the radioisotopic tracer technique at one substrate concentration (<250 pmoles cm^-3). Dissolved free alanine and aspartic acid concentrations in the interstitial nutrient pool ranged from approximately 1 to 500 pmoles cm^-3. In the short S. alterniflora soil, maximum microbial uptake of alanine was found at a depth of 10 cm (8.32 pmoles cm^-3 h^-1); in the tall S. alterniflora soil maximum uptake was at 20 cm (23.4 pmoles cm^-3 h^-1). The utilization of aspartic acid appeared constant over the depth interval investigated (0 to 60 cm). The turnover times of alanine and aspartic acid in the tall and short S. alterniflora soils ranged from 5 to 25 h and 40 to 100 h, respectively. The percent of the labeled alanine and aspartic acid taken up that was mineralized by tall and short s. alterniflora microbenthos ranged from 20 to 50% and 5 to 20%, respectively.     

Effects of chronic oil pollution on a salt-marsh grass community

A small, naturally defined saltmarsh in Chesapeake Bay (USA) was repeatedly dosed with a No. 2 fuel oil. The production, decay rates, physical characteristics and hydrocarbon content of the dominant grass species present in the marsh were routinely monitored. Spartina alterniflora was the only grass species displaying effects of the oil dosing; this is attributed to the grass's location in the marsh. A substantial portion of the S. alterniflora in the marsh was killed by the oil dosing; the remaining portion evidenced sublethal effects including delayed development in the spring, increased density, and reduced mean weight per stem. The second annual cohort of shoots, usually produced in late summer and early fall, was suppressed almost entirely. Decay rates of S. alterniflora in the oiled marsh were higher and peaked later than decay rates in a control marsh. Oil which entered the roots and rhizomes of dead S. alterniflora was retained in a relatively undergraded state for at least 7 months after dosing stopped.Virginia Institute of Marine Science Contribution No. 945     

Leaf-litter processing by invertebrates in a mangrove forest in Queensland

The way leaf shredders handle and shred leaves under laboratory conditions and in the mangrove forest at Myora Springs, Queensland, Australia, was investigated during the period 1980 to 1984. Field observations on the behaviour of the crab Sesarma erythrodactyla during low tide revealed that this species spends most of its time foraging over mud. S. erythrodactyla eats mangrove leaves where they fall or drags them into burrows or hollow logs. Through their feeding activities, crabs (S. erythrodactyla, Metopograpsus frontalis, Helice leachii, Clistocoeloma merguiensis, Leptograpsus variegatus, Paragrapsus laevis, Ilyograpsus paludicula), isopods (Exospaeroma alata, Campaecopia sp.) amphipods (Orchestia sp., Melita sp.), and a capitellid polychaete (Capitellides sp.), break down whole mangrove leaves into small particles. The way in which a leaf is broken down by leaf-shredders influences the size and composition of the particulate organic matter (POM) in the environment. The POM egested by leaf-shredders varies from 32 to 1171 m. POM in this size range occurs in the guts of 38 invertebrate species which feed on mud, suggesting that they depend on the plant detritus produced by leafshredders as a source of food. Leaf-shredders therefore constitute a primary link in the marine food web of mangrove forests.     

Modification of sediment permeability and shear strength by two burrowing invertebrates

Laboratory experiments have been conducted on the effects of bioturbation by the amphipod Corophium volutator (Pallas) and the polychaete Nereis diversicolor (O.F. Müller) on the physical properties of estuarine muddy sand. Invertebrates and muddy sediment were collected from Langbank, Firth of Clyde, Scotland. Sediment columns were seeded with low, medium and high densities of invertebrates in single-and mixed-species experiments. Permeability decreased with increasing density of C. volutator, but increased with increasing density of N. diversicolor. Water content decreased with increasing density of both species. Shear strength increased with increasing density of both species, but more so with C. volutator than with N. diversicolor. Mixed-species effects on shear strength were additive, but some of the permeabilities were lower than predicted. Bivariate and multivariate correlation, and partial correlation analyses were applied to the data. Shear strength was negatively correlated with water content. The correlations between shear strength and permeability and between permeability and water content were affected differently by the two species. There were few partial correlations between the variables.     

In situ assessment of modification of sediment properties by burrowing invertebrates

Benthic organisms can significantly alter the physical properties of marine sediments, but it has hitherto been difficult to assess and quantify the effects of bioturbation. In situ geophysical techniques offer new methods for measuring these effects: measurement of acoustic shear-wave velocity and electrical resistivity allows nondestructive assessment of the properties of the grain framework and pore-fluid matrix, respectively, of the seabed sediment. The influence of burrowing invertebrates on the structural properties of sandy sediments at intertidal locations on the coast of Wales (UK) was investigated during the periol 1986–1987 using these techniques. Three species (Arenicola marina, Corophium arenarium and Lanice conchilega) were selected on the basis of their contrasting styles of burrow construction. All three species produced measurable and significant, although different, changes in bed properties. They modified shear-wave propagation through the bed by changing bed rigidity: while A. marina and C. arenarium decreased rigidity by creating open burrows, L. conchilega increased rigidity by building shell-lined tubes. All produced a decrease in electrical resistivity by altering porosity and/or tortuosity, which implies an increase in permeability; these changes were attributable not only to the presence of the burrows but also to modification of the between-burrow sediment texture and bed properties.     

RQ of benthic marine invertebrates

This study investigated an incubation method which employed simultaneous measurement of CO₂ production and O₂ consumption rates to calculate the RQ (respiratory quotient; CO₂ production rate: O₂ consumption rate) of individual benthic marine invertebrates. Carbon dioxide production rates were calculated from changes in CO₂ concentration determined using seawater pH. O₂ consumption rates were calculated from changes in O₂ concentration with a correction applied for O₂ flux across the air/water interface due to gaseous exchange. Species examined were Triphyllozoon sp. cf. moniliferum (MacGillivray 1860), a bryozoan; Herdmania momus (Savigny), a solitary ascidian; Poneroplax albida (Blainville 1825), a chiton; and Haliotis roei (Gray 1826), an abalone. Six individuals of each were collected on 14 November 1985 from the limestone walls of a cave in a nearshore reef off Marmion, Western Australia. After acclimation for 6 h in experimental conditions, rates of CO₂ production and O₂ consumption were measured. A minimum period of 4 h was required to obtain consistent RQ values for each species. The standard error (SE) of the (calculated) RQ ratio was 14 to 33% of the mean in incubations of 4 h, and less than 14% in incubations of 4 to 12 h. The RQ is commonly used as an indicator of unknown catabolic substrates by comparing it with biochemically determined limits for known substrates. This study provides a strong argument against using the RQ of individual animals to draw any conclusions about catabolic substrates. Unexplained variation in the components of the RQ of an individual, measured over short time periods, and the potential involvement of stored reserves in catabolism, over longer time periods, obscure the relationship between the RQ of individual animals and the ratio's biochemically determined limits.     

On predation of pelagic larvae and early juveniles of marine bottom invertebrates by adult benthic invertebrates and their passing alive through their predators

The dynamic quantitative balance between prey and predator invertebrate species inhabiting the same shallow-shelf (sublittoral level bottom) benthic communities was first discussed by Thorson (1953). Thorson considered the exact timing of larval settlement of prey and predator species possessing pelagic development and temporal supression of the adult predators' feeding activities during reproduction at the time of the preys' settlement to constitute the major factors which facilitate survival of the prey species in such communities. However, information obtained demonstrates that Thorson's “mechanism of balance between predator and prey species of benthic communities” is not always effective in securing survival from predation not only of the prey's spat but even sometimes of the predator's spat also. Because of this, the “mechanism” can not be rated as universally effective in all situations. Analysis of the data so far published demonstrates that, in marine benthic communities, especially in shallow-shelf waters, it is not uncommon for gametes, larvae, or early juveniles of different prey species to pass alive through suspension (filter)-feeding and deposit-feeding adult invertebrates preying on them. Sometimes development can even continue after excretion by predators. The hypothesis of Voskresensky (1948) and Goycher (1949) of the importance of this phenomenon for the maintenance and recruitment of the mussel Mytilus edulis and other filter-feeding lamellibranchs of nearshore waters preying on their own and other lamellibranch pelagic larvae must be rejected on the basis of accumulated data on their feeding and general biology and on the adverse influence of the mucous of their faecal pellets and pseudofaeces on the larvae excreted by them alive. The data considered here demonstrate that, although the passing alive of larvae and spat of benthic invertebrates through benthic predators is not uncommon in shallow-shelf bottom-communities, it plays no important role in the processes of maintenance and recruitment of the species and communities involved nor of the marine benthos as a whole. The actual ecological significance of predation on pelagic larvae and bottom spat of benthic invertebrate prey species by all three main trophic groups of marine benthos (suspension or filter-feeders, deposit-feeders, carnivores) and its importance to predator-prey dynamics in marine benthic communities remains open to debate until more reliable quantitative data become available.     

Growth,production and energy transformations in the salt-marsh killifish Fundulus heteroclitus

Populations of Fundulus heteroclitus (L.) at the beginning of a growth season in a New England salt marsh consist of 3 yearly age classes, with the 1-year-old class contributing most of the biomass. Calculation of production rates revealed that the young fish were the most active part of the population and that females were more productive than males. The entire population spent equal amounts of energy in growth and in metabolism. Including the young of the year, we obtained total production of 160 kg dry weight/ha, a value among the highest obtained for natural fish populations. About 5 to 15% of the production is available to predators. Rates of food consumption by F. heteroclitus are high enough to turn over the population of prey relatively often. Popululations of F. heteroclitus are thus capable of exerting an important influence on the abundance and distribution of their prey.Contribution No. 3721 from the Woods Hole Oceanographic Institution.     

Intertidal invertebrates locally enhance primary production

The contribution of autochthonous vs. allochthonous inputs to productivity is an important determinant of ecosystem function across multiple habitats. In coastal marine systems, nutrients are thought to come primarily from the upwelling of deep, nutrient-rich water. Using experimental manipulations of a dominant tide pool animal, the mussel Mytilus californianus, I show that the presence of mussels greatly increases the supply of inorganic nitrogen and phosphorus. Mussels further had a direct effect on productivity: benthic microalgal abundance increased by a factor of 4-8, while the growth of a red alga was four times greater in the presence of mussels. The increase in nitrite and nitrate associated with mussels further suggests nitrifying activity by microbes. These findings have broad implications for coastal marine systems, including that regenerated nutrients may contribute more to productivity than previously recognized and that the presence of animal-generated nutrients sets the stage for numerous positive interactions.     

Causes and consequences of salt-marsh erosion in an Atlantic estuary in SW Spain

This study reports on the quantification of horizontal erosion by undermining of slopes in the atlantic mesotidal salt marshes of Odiel, SW Spain, and analyses its causes and consequences. Horizontal erosion has produced considerable losses of salt marsh area, including zones of mature salt marsh. Human pressure, such as from water-borne traffic or the exploitation of the slopes for the capture of bait, increases the natural erosion processes. The role of vegetation in protecting the slopes against erosion is studied. Channel banks covered with plants, many of which belong to species with long-living, above-ground creeping stems, were less eroded than those without vegetation cover. The enormous volume of sediments moved (ca. 7000m³ in one year) could contribute to the silting-up of the navigable channels of the estuary, so that continual dredging is necessary to allow access to shipping. These sediments are highly contaminated, and dredging exposes them more directly to the trophic network of the estuary. There is a considerable loss of natural resources. Finally, the integrated management of this coastal ecosystem is discussed.     

A trophic cascade triggers collapse of a salt-marsh ecosystem with intensive recreational fishing

Overexploitation of predators has been linked to the collapse of a growing number of shallow-water marine ecosystems. However, salt-marsh ecosystems are often viewed and managed as systems controlled by physical processes, despite recent evidence for herbivore-driven die-off of marsh vegetation. Here we use field observations, experiments, and historical records at 14 sites to examine whether the recently reported die-off of northwestern Atlantic salt marshes is associated with the cascading effects of predator dynamics and intensive recreational fishing activity. We found that the localized depletion of top predators at sites accessible to recreational anglers has triggered the proliferation of herbivorous crabs, which in turn results in runaway consumption of marsh vegetation. This suggests that overfishing may be a general mechanism underlying the consumer-driven die-off of salt marshes spreading throughout the western Atlantic. Our findings support the emerging realization that consumers play a dominant role in regulating marine plant communities and can lead to ecosystem collapse when their impacts are amplified by human activities, including recreational fishing.     

Seasonal variations in salt-marsh macroalgae photosynthesis. I. Ascophyllum nodosum ecad scorpioides

Photosynthesis in whole plants of the intertidal alga Ascophyllum nodosum ecad scorpiodes was evaluated by measuring ¹⁴C-uptake under a variety of light intensities and approximately monthly intervals during a 15 month study. Photosynthetic rates were determined in terms of dry weight, pigment content and uptake into ethanolsoluble and insoluble fractions. The specimens, naturally acclimated to in situ light intensities and temperatures, exhibited photosynthetic responses to light intensity which differed with time of year. Maximum photosynthetic potential occurred during the spring months and minimum potential occurred during late summer and winter months. Variations in photosynthetic potential were closely related to seasonal changes in field biomass. Both photosynthetic potential and biomass were inversely related to growth patterns of the salt-marsh phanerogam Spartina alternilora.This research was supported by Research Grant AG-375 from the National Science Foundation and, in part, by the State University of New York Research Foundation and the Energy Research and Development Administration (ERDA).     

Competition for food and other niche-related studies of three species of salt-marsh foraminifera

The niches of 3 species of salt-marsh foraminifera, Allogromia laticollaris, Rosalina leei, and Spiroloculina hyalina were assessed in the laboratory. The 3 species reproduce within the following ranges: temperature (10° to 33°C), salinity (12 to 45‰) and pH (5 to 10). Competition for food among the 3 species was evaluated. S. hyalina did not compete with other species. Intraspecific competition (crowding) appears to be an important factor limiting the reproduction of A. laticollaris. Crowding seems to have little effect on the other 2 species. The feeding of foraminifera is affected by the quality and quantity of food organisms. The feeding rate of the species tested is directly related to concentration within a range of 10² to 10⁶ cells fed. S. hyalina is a bacterial feeder. A. laticollaris is a rare species which may become locally abundant when dominant species are missing. S. hyalina is also a rare species, which can bloom where the density of bacteria is relatively high and in the absence of competing species. R. leei is a stable, conspicuous species, whose moderate numbers are relatively unaffected by physical stress and competition. Some new laboratory data on Ammonia beccarii were obtained so that this species could be compared with the other studied. Differences in niches are graphically presented.     

Lactate and succinate oxidoreductases in marine invertebrates

Nineteen species of littoral marine invertebrates, representing Porifera, Cnidaria, Ctenophora, Brachiopoda, Mollusca, and Arthropoda, were studied with respect to the ability of tissue extracts to catalyze the lactate and succinate dehydrogenase reactions in both directions. Pyruvate reductase (PR) activity varied tremendously with species, from 0.014 mole/min/g of tissue in the etenophore Mnemiopsis leidyi to 145 -moles/min in leg muscle of the horseshoe crab Limulus polyphemus, a 10,000-fold range. Lactate dehydrogenase (LD) activity varied from 0.010 in the ctenophore to 2.91 in the squid Loligo pealei, a 300-fold range. The ratio PR/LD, indicating the probability of lactic acid production, was 1,968 in muscle of the flounder, the only vertebrate studied. It was very much lower in all invertebrates; in a brachiopod, Terebratulina septentrionalis, the ratio was only 0.68. Fumarate reductase (FR) and succinate dehydrogenase (SD) activities varied less widely. The extremes of the ratio FR/SD, indicating the probability of succinic acid production, were 0.24 in the clam Mercenaria mercenaria, and 7.6 in the oyster Crassostrea virginica. PR/LD appears related to the capacity for vigorous muscular activity, sustaining rapid movement of larger animals, and FR/SD appears related to tolerance of temporary anaerobiosis, such as found in sessile animals that close their valves tightly on exposure to air during low tide.     

Relevance of wound-activated compounds produced by diatoms as toxins and infochemicals for benthic invertebrates

Plants evolve the production of wound-activated compounds (WACs) to reduce grazing pressure. In addition, several plant-produced WACs are recognized by various invertebrates, playing the role of infochemicals. Due to co-evolutionary processes, some invertebrates recognize plant infochemicals and use them to identify possible prey, detect the presence of predators or identify algae containing various classes of toxic metabolites. Different metabolites present in the same algae can play the role of toxins, infochemicals or both simultaneously. We investigated the infochemical activity of compounds extracted from three diatoms epiphytes of the seagrass Posidonia oceanica, by conducting choice experiments on invertebrates living in the same community or in close proximity. Furthermore, the specific toxicity of the extracts obtained from the same algae was tested on sea urchin embryos using a standard bioassay procedure, to detect the presence of toxins. The comparison of the two effects demonstrated that invertebrates are subjected to diatom wound-activated toxicants when these algae are not associated with their own habitat, but they are able to recognize volatile infochemicals derived from diatoms associated with their habitats. The specific toxicity of WACs was shown to be inversely correlated to the perceptive ability of invertebrates towards volatile compounds liberated by the same algae. Hence, when the recognition of specific algae by a given invertebrate species evolves, their detrimental effects on the receiving organism may be lost.