Rafting of benthic macrofauna: important factors determining the temporal succession of the assemblage on detached macroalgae

Rafting on biotic and abiotic substrata has been reported for many benthic marine invertebrates. Here, I describe important characteristics of common floating substrata and review published studies examining the succession of the assemblage on detached macroalgae to identify the most important factors determining this succession. Floating substrata differ in survival time (i.e. before they disintegrate) and in food value, with abiotic materials having high survival times but low food value and some biotic substrata (seagrasses, fresh wood) having high food values but short survival times. Large macroalgae with pneumatocysts may combine high survival times and high food values. Substratum survival and food value have consequences for the species composition of the rafting macrofauna. In general, suspension feeders dominate rafting assemblages on abiotic substrata, while grazing and boring species abound on macroalgae and wood. The succession of the rafting assemblage can be subdivided into three phases during which different processes predominate. During the initial phase some of the original colonizers (if present) disappear from the substratum, either due to active emigration or predation. This short, initial phase is followed immediately by the colonization phase, during which new organisms colonize the rafting substratum. Colonization may be rapid and intense in the beginning but then slows down. Towards the end of the colonization phase, some rafting organisms may reproduce and their offspring recruit within the parental raft. Results from two long-term studies confirmed that the proportion of species with direct development increased with duration of rafting. These successional changes will be most pronounced for large biotic substrata, rendering these particularly suitable for long-distance dispersal of organisms with direct development.     

Hitch-hiking on floating marine debris: macrobenthic species in the Western Mediterranean Sea

Marine litter has been defined as solid materials of human origin discarded at sea, or reaching the sea through waterways. The effect of marine debris on wildlife, tourism and human health is well documented and there is considerable scientific literature about plastic litter in the sea and over the seabed, mostly highlighting the possible impact on marine mammals and tourism. Dispersal of marine and terrestrial organisms on floating objects has biogeographical and ecological interest. For some species, extension of their geographical range is more likely to be related to transport of mature individuals on floating rafts than to the active or passive dispersal of reproductive propagules. Variability and variety of rafting materials has increased dramatically in recent years and marine litter has been used widely as a raft by ‘hitch-hiking’ species. This paper reports on the benthic invertebrates living on marine debris transported by wind and surface currents over the western Mediterranean Sea. Plastics accounted for the major item of debris because of poor degradability, however glass, cans, fishing nets and polyurethane containers, were also found. Macro-benthos living on raft material comprised mainly molluscs, polychaetes and bryozoans. Large fish were found commonly below large plastic bags. Estimations of the distances that may be covered by hitch-hiking species and the contribution of rafting to the theoretical dispersal of species is provided.     

Substratum preferences of settling larvae of marine fishes reared in the laboratory

Various species of marine fish larvae were reared in the laboratory to allow observation of the substratum preferences of newly settling fish. The range of preferences for settling larvae of intertidal species corresponded to the adult niche breadth. The preferred substratum was always an element of the adult habitat, although not necessarily the same substratum preferred by the adults. Experiments with artificial substrata indicated that settlement preferences are based on tactile cues and light transmission. Depending upon the species, other factors such as current speed or salinity can also influence settlement.     

In situ infrared spectroscopic investigation of Perna canaliculus mussel larvae primary settlement

The adhesion of Perna canaliculus mussel larvae on a germanium (Ge) prism in filtered seawater at 16 degrees C has been investigated by in situ attenuated total reflection infrared (ATR-IR) spectroscopy. The adhesive from the mussel larvae was spectrally monitored over 2 h and the IR spectrum showed its glycoproteinaceous nature with sulphated and carboxylated moieties. The adhesive from the mussel larvae differs from that of the adults, resembling the mucus secretion found in other benthic marine species at a larval stage. To date, this appears to be the first work describing the main chemical features of secreted adhesive associated with the primary settlement of mussel larvae. The acquired knowledge on the larval adhesive features may lead to enhanced settling methods in aquaculture or to antibiofouling strategies. The ATR-IR approach under temperature control is potentially useful for such studies on other small benthic organisms in both marine and freshwater environments.     

The influence of resident adults on larval settlement: experiments with four species of ascidians

Residents within any community can affect the larval settlement of both their own and other species. In marine sessile communities resident adults can affect larval settlement by preying on settling larvae, removing or adding space for the larvae to colonize, or stimulating or prohibiting larval settlement on available substratum nearby. To examine those processes by which residents affect settlement, we exposed experimental substrata with three densities of adults of a single species at a site in eastern Long Island Sound, USA for a 24-h period. Four species of common ascidians, Botryllus schlosseri (Pallas), Botrylloides diegensis Ritter and Forsyth, Diplosoma macdonaldi Herdman, and Molgula manhattensis (De Kay), were used in 11 separate experiments. Few individuals of any species settling attached to the surfaces of these species and this resulted in the main effect of these residents being the usurpation of space and the restricting of settlement to unoccupied areas. A model is also presented to explain the apparent aggregated settlement of several species in open areas adjacent to the resident ascidians. From this model we suggest that the aggregated settlement can result from limited larval mobility such that some larvae that contact and reject the resident species as settlement sites may subsequently contact open surfaces of the same substratum and increase settlement densities there over those observed on control substrata. Finally, settlement data for several species indicate that Molgula may influence settlement by preying on larvae.     

Why Life Histories Evolve Differently in the Sea

Marine life histories differ from terrestrial life historiesbecause seawater is denser and more viscous than air, becausedesiccation is not a problem for organisms in water, and becausefood is abundant in suspension and solution. (1) Mating andcompetition for paternity in the sea often differs. Female gametesare often spawned freely. Passively dispersed spermatophorescould in some cases provide single paternity to an entire clutchof offspring. Penises of sessile animals reach far for copulation.There are no pollinators. (2) In many clades of benthic marineanimals, greater dispersal of offspring is associated with largeadult size, and greater parental care of offspring and reducedplanktonic larval periods are associated with small adult size.(3) Many benthic marine animals are colonies with modular construction,and these also commonly brood embryos and have short-lived larvae,in contrast to related solitary forms. (4) Unlike dispersalof terrestrial animals, larval dispersal of marine animals isoften obligate with sexual reproduction and often includes aprecompetent period during which larvae cannot settle at goodsites. Unlike terrestrial seeds, marine larvae have no clearadaptations for dispersal, often grow during dispersal, andoften leave bad sites. Feeding planktonic larvae are commonamong marine animals and rare among other aquatic animals, perhapsbecause of persistent aquatic routes between habitable sitesfor marine animals. Peculiarities in marine life histories mayinfluence many aspects of evolution in the sea. Closely relatedsedentary marine animals can differ greatly in larval dispersalwith consequences for recruitment to populations, genetic exchangebetween benthic populations, adaptation to local conditions,sex allocation, interaction with kin, speciation, and extinction.     

Less inhibited with age? Larval age modifies responses to natural settlement inhibitors

As larvae of marine invertebrates age, their response to settlement cues can change. This change can have significant consequences to both the ecology of these organisms, and to their response to antifouling coatings. This study examines how larval age affects the settlement response of larvae to two naturally derived settlement inhibitors, non-polar extracts from the algae Delisea pulchra and Dilophus marginatus, the former of which contains compounds that are in commercial development as antifoulants. Two species of marine invertebrates with non-feeding larvae were investigated: the bryozoans Watersipora subtorquata and Bugula neritina. Larval age strongly affected larval settlement, with older larvae settling at much higher rates than younger larvae. Despite having strong, inhibitory effects on young larvae, the non-polar extracts did not inhibit the settlement of older larvae to the same degree for both species studied. The results show that the effects of ecologically realistic settlement inhibitors are highly dependent on larval age. Given that the age of settling larvae is likely to be variable in the field, such age specific variation in settlement response of larvae may have important consequences for host-epibiont interactions in natural communities.     

Close encounters with eddies: oceanographic features increase growth of larval reef fishes during their journey to the reef

Like most benthic marine organisms, coral reef fishes produce larvae that traverse open ocean waters before settling and metamorphosing into juveniles. Where larvae are transported and how they survive is a central question in marine and fisheries ecology. While there is increasing success in modelling potential larval trajectories, our knowledge of the physical and biological processes contributing to larval survivorship during dispersal remains relatively poor. Mesoscale eddies (MEs) are ubiquitous throughout the world''s oceans and their propagation is often accompanied by upwelling and increased productivity. Enhanced production suggests that eddies may serve as important habitat for the larval stages of marine organisms, yet there is a lack of empirical data on the growth rates of larvae associated with these eddies. During three cruises in the Straits of Florida, we sampled larval fishes inside and outside five cyclonic MEs. Otolith microstructure analysis revealed that four of five species of reef fish examined had consistently faster growth inside these eddies. Because increased larval growth often leads to higher survivorship, larvae that encounter MEs during transit are more likely to contribute to reef populations. Successful dispersal in oligotrophic waters may rely on larval encounter with such oceanographic features.     

Plasticity of hatching and the duration of planktonic development in marine invertebrates

Plasticity in hatching potentially adjusts risks of benthic and planktonic development for benthic marine invertebrates. The proportionate effect of hatching plasticity on duration of larval swimming is greatest for animals that can potentially brood or encapsulate offspring until hatching near metamorphic competence. As an example, early hatching of the nudibranch mollusk Phestilla sibogae is stimulated by scattering of encapsulated offspring, as by a predator feeding on the gelatinous egg ribbon. When egg ribbons are undisturbed, hatching is at or near metamorphic competence. Disturbance of an unguarded benthic egg mass can insert 4 or more days of obligate larval dispersal into the life history. As another example, the spionid annelid Boccardia proboscidea broods capsules, each with both cannibalistic and developmentally arrested planktivorous siblings plus nurse eggs. Early hatching produces mainly planktivorous larvae with a planktonic duration of 15 days. Late hatching produces mainly adelphophages who have eaten their planktivorous siblings and metamorphose with little or no period of swimming. Mothers actively hatch their offspring by tearing the capsules, and appeared to time hatching in response to their environment and not to the stage of development of their offspring. Higher temperature increased the variance of brooding time. Females appeared to hatch capsules at an earlier developmental stage at lower temperatures. Species that release gametes or zygotes directly into the plankton have less scope for plasticity in stage at hatching. Their embryos develop singly with little protection and hatch at early stages, often as blastulae or gastrulae. Time of hatching cannot be greatly advanced, and sensory capabilities of blastulae may be limited.     

Trends in the Diversity,Distribution and Life History Strategy of Arctic Hydrozoa (Cnidaria)

This is the first attempt to compile a comprehensive and updated species list for Hydrozoa in the Arctic, encompassing both hydroid and medusa stages and including Siphonophorae. We address the hypothesis that the presence of a pelagic stage (holo- or meroplanktonic) was not necessary to successfully recolonize the Arctic by Hydrozoa after the Last Glacial Maximum. Presence-absence data of Hydrozoa in the Arctic were prepared on the basis of historical and present-day literature. The Arctic was divided into ecoregions. Species were grouped into distributional categories according to their worldwide occurrences. Each species was classified according to life history strategy. The similarity of species composition among regions was calculated with the Bray-Curtis index. Average and variation in taxonomic distinctness were used to measure diversity at the taxonomic level. A total of 268 species were recorded. Arctic-boreal species were the most common and dominated each studied region. Nineteen percent of species were restricted to the Arctic. There was a predominance of benthic species over holo- and meroplanktonic species. Arctic, Arctic-Boreal and Boreal species were mostly benthic, while widely distributed species more frequently possessed a pelagic stage. Our results support hypothesis that the presence of a pelagic stage (holo- or meroplanktonic) was not necessary to successfully recolonize the Arctic. The predominance of benthic Hydrozoa suggests that the Arctic could have been colonised after the Last Glacial Maximum by hydroids rafting on floating substrata or recolonising from glacial refugia.     

Sampling multiple life stages significantly increases estimates of marine biodiversity

Biodiversity assessments are critical for setting conservation priorities, understanding ecosystem function and establishing a baseline to monitor change. Surveys of marine biodiversity that rely almost entirely on sampling adult organisms underestimate diversity because they tend to be limited to habitat types and individuals that can be easily surveyed. Many marine animals have planktonic larvae that can be sampled from the water column at shallow depths. This life stage often is overlooked in surveys but can be used to relatively rapidly document diversity, especially for the many species that are rare or live cryptically as adults. Using DNA barcode data from samples of nemertean worms collected in three biogeographical regions—Northeastern Pacific, the Caribbean Sea and Eastern Tropical Pacific—we found that most species were collected as either benthic adults or planktonic larvae but seldom in both stages. Randomization tests show that this deficit of operational taxonomic units collected as both adults and larvae is extremely unlikely if larvae and adults were drawn from the same pool of species. This effect persists even in well-studied faunas. These results suggest that sampling planktonic larvae offers access to a different subset of species and thus significantly increases estimates of biodiversity compared to sampling adults alone. Spanish abstract is available in the electronic supplementary material.     

Induction of metamorphosis in the sea urchin Holopneustes purpurascens by a metabolite complex from the algal host Delisea pulchra

Most benthic invertebrates have complex life cycles with planktonic larvae that return to the substratum to settle and metamorphose into a benthic stage. Although naturally produced chemical cues have long been thought to be important for the settlement or metamorphosis of invertebrate larvae, few ecologically relevant chemical cues have been clearly identified. The marine echinoid Holopneustes purpurascens has a complex life cycle, with a planktonic, nonfeeding dispersive larva that metamorphoses into a benthic stage that lives in the canopy of subtidal benthic algae such as the red alga Delisea pulchra and the kelp Ecklonia radiata. Recently recruited juveniles are found primarily on D. pulchra, and we hypothesized that this was in response to a chemical cue produced by this alga. Competent larvae metamorphosed in the presence of D. pulchra, or seawater surrounding this alga, but not in response to the presence of E. radiata or its extracts. A cue for metamorphosis was isolated and characterized from D. pulchra and found to be a water-soluble complex of the sugar floridoside and isethionic acid in a 1:1 molar ratio. The floridoside-isethionic acid complex also triggered settlement in H. purpurascens; however, this response was less specific than metamorphosis and was reversible. Larvae of H. purpurascens also metamorphosed in the presence of several other species of red, but not brown or green, algae from their habitat. Floridoside is found only in red algae, suggesting that the floridoside-isethionic acid complex may be acting as a cue for metamorphosis in other red algae as well as in D. pulchra.     

Population genetics at three spatial scales of a rare sponge living in fragmented habitats

Background  

Rare species have seldom been studied in marine habitats, mainly because it is difficult to formally assess the status of rare species, especially in patchy benthic organisms, for which samplings are often assumed to be incomplete and, thus, inappropriate for establishing the real abundance of the species. However, many marine benthic invertebrates can be considered rare, due to the fragmentation and rarity of suitable habitats. Consequently, studies on the genetic connectivity of rare species in fragmented habitats are basic for assessing their risk of extinction, especially in the context of increased habitat fragmentation by human activities. Sponges are suitable models for studying the intra- and inter-population genetic variation of rare invertebrates, as they produce lecitotrophic larvae and are often found in fragmented habitats.     

THERMOGEOGRAPHY OVER TIME CREATES BIOGEOGRAPHIC REGIONS: A TEMPERATURE/SPACE/TIME-INTEGRATED MODEL AND AN ABUNDANCE-WEIGHTED TEST FOR BENTHIC MARINE ALGAE

We developed a time-integrated thermogeographic model to demonstrate conditions under which benthic marine algal assemblages evolve biogeographic patterns in their distribution and abundance. The graphical model applies to rocky marine sublittoral zones in which seasonal temperatures, coastline area, isolation, and evolutionary time are primary factors. Time is treated by using the temperature/area/distributions for the present (interglacial period) integrated with that of 18,000 years before present (glacial period). These two alternate states characterize the global marine realm since the late Pliocene to Pleistocene time during which many extant species have evolved. The resulting abiotic "thermogeographic" model defines 20 regions that correspond with the cores of 24 recognized biogeographic regions and/or provinces determined by published distributions of organisms. Modern biogeographic regions conform closely with thermogeographic regions where temperature, area, and time are integrated. We also propose that biogeographic patterns should be determined by the abundance of species assemblages rather than presence and absence or percent endemism as is commonly done. We test the efficacy of thermogeographic regions with abundance-weighted patterns in the biogeography of crustose coralline red algae (Rhodophyta/Corallinales) in the colder part of the northern hemisphere. Based on abundance, rather than presence/absence, coralline red algal biogeographic regions correspond closely with the model's thermogeographic regions.     

Nonsignificant isolation by distance implies limited dispersal

Understanding the scale of dispersal is an important consideration in the conservation and management of many species. However, in species in which the high‐dispersal stage is characterized by tiny gametes or offspring, it may be difficult to estimate dispersal directly. This is the case for many marine species, whose pelagic larvae are dispersed by ocean currents by several days or weeks before beginning a benthic, more sedentary, adult stage. As consequence of the high‐dispersal larval stage, many marine species have low genetic structure on large spatial scales (Waples 1998 ; Hellberg 2007 ). Despite the high capacity for dispersal, some tagging studies have found that a surprising number of larvae recruit into the population they were released from (self‐recruitment). However, estimates of self‐recruitment are not informative about mean dispersal between subpopulations. To what extent are limited dispersal estimates from tagging studies compatible with high potential for dispersal and low genetic structure? In this issue, a study on five species of coral reef fish used isolation by distance (IBD) between individuals to estimate mean dispersal distances (Puebla et al. 2012 ). They found that mean dispersal was unexpectedly small (<50 km), given relatively low IBD slopes and long pelagic durations. This study demonstrates how low genetic structure is compatible with limited dispersal in marine species. A comprehensive understanding of dispersal in marine species will involve integrating methods that estimate dispersal over different spatial and temporal scales. Genomic data may increase power to resolve these issues but must be applied carefully to this question.     

Effects of dredging on critical ecological processes for marine invertebrates,seagrasses and macroalgae,and the potential for management with environmental windows using Western Australia as a case study

Dredging can have significant impacts on benthic marine organisms through mechanisms such as sedimentation and reduction in light availability as a result of increased suspension of sediments. Phototrophic marine organisms and those with limited mobility are particularly at risk from the effects of dredging. The potential impacts of dredging on benthic species depend on biological processes including feeding mechanism, mobility, life history characteristics (LHCs), stage of development and environmental conditions. Environmental windows (EWs) are a management technique in which dredging activities are permitted during specific periods throughout the year; avoiding periods of increased vulnerability for particular organisms in specific locations. In this review we identify these critical ecological processes for temperate and tropical marine benthic organisms; and examine if EWs could be used to mitigate dredging impacts using Western Australia (WA) as a case study. We examined LHCs for a range of marine taxa and identified, where possible, their vulnerability to dredging. Large gaps in knowledge exist for the timing of LHCs for major species of marine invertebrates, seagrasses and macroalgae, increasing uncertainty around their vulnerability to an increase in suspended sediments or light attenuation. We conclude that there is currently insufficient scientific basis to justify the adoption of generic EWs for dredging operations in WA for any group of organisms other than corals and possibly for temperate seagrasses. This is due to; 1) the temporal and spatial variation in the timing of known critical life history stages of different species; and 2) our current level of knowledge and understanding of the critical life history stages and characteristics for most taxa and for most areas being largely inadequate to justify any meaningful EW selection. As such, we suggest that EWs are only considered on a case-by-case basis to protect ecologically or economically important species for which sufficient location-specific information is available, with consideration of probable exposures associated with a given mode of dredging.     

Biodiversity and functioning of polychaetes in benthic sediments

Polychaetes are well represented in most marine and estuarine environments, both in terms of number of individuals and species, and they typically contribute a significant percentage of the total macrofaunal diversity. They exhibit considerable variations in recruitment in both time and space, which is then often reflected in adult distributions. Whilst families and genera of polychaetes have wide distributions, normally species have discrete distributions. Polychaetes are often classified according to their diverse feeding guilds. They play a major role in the functioning of benthic communities, in terms of recycling and reworking of benthic sediments, bioturbating sediments and in the burial of organic matter. Some species form dense tubiculous colonies which can radically change recruitment patterns of other infaunal organisms. Polychaetes, by their burrowing and feeding activity, may considerably enhance various sedimentary processes. However, much remains to be learnt as to how benthic communities function, and how they may change in function as they are increasingly being impacted especially in coastal waters adjacent to centres of population.     

Rapid, long-distance dispersal by pumice rafting

Pumice is an extremely effective rafting agent that can dramatically increase the dispersal range of a variety of marine organisms and connect isolated shallow marine and coastal ecosystems. Here we report on a significant recent pumice rafting and long-distance dispersal event that occurred across the southwest Pacific following the 2006 explosive eruption of Home Reef Volcano in Tonga. We have constrained the trajectory, and rate, biomass and biodiversity of transfer, discovering more than 80 species and a substantial biomass underwent a >5000 km journey in 7-8 months. Differing microenvironmental conditions on the pumice, caused by relative stability of clasts at the sea surface, promoted diversity in biotic recruitment. Our findings emphasise pumice rafting as an important process facilitating the distribution of marine life, which have implications for colonisation processes and success, the management of sensitive marine environments, and invasive pest species.     

Offspring size effects in the marine environment: A field test for a colonial invertebrate

Abstract A central tenet of life‐history theory is the presence of a trade‐off between the size and number of offspring that a female can produce for a given clutch. A crucial assumption of this trade‐off is that larger offspring perform better than smaller offspring. Despite the importance of this assumption empirical, field‐based tests are rare, especially for marine organisms. We tested this assumption for the marine invertebrate, Diplosoma listerianum, a colonial ascidian that commonly occurs in temperate marine communities. Colonies that came from larger larvae had larger feeding structures than colonies that came from smaller larvae. Colonies that came from larger larvae also had higher survival and growth after 2 weeks in the field than colonies that came from smaller larvae. However, after 3 weeks in the field the colonies began to fragment and we could not detect an effect of larval size. We suggest that offspring size can have strong effects on the initial recruitment of D. listerianum but because of the tendency of this species to fragment, offspring size effects are less persistent in this species than in others.