Michael J. Keough

Responses of settling invertebrate larvae to bioorganic films: effects of different types of films

Abstract Larvae of benthic invertebrates are exposed to a variety of chemical cues, many of biological origin, as they near a potential settlement surface. One such cue is the bioorganic film that covers many surfaces, and some laboratory evidence suggests that larvae respond to the presence or absence of such films. Our earlier work has shown that, at two field sites in southeastern Australia, a variety of species recruit at higher densities to substrata bearing such a film, and here we begin to determine the specificity of those responses. Experimental substrata were prepared with films developing in laboratory aquaria and under field conditions for 7 days. These substrata were then exposed in the field, and analysis of 19 sessile taxa, distributed over seven phyla, showed that no species recruited at significantly different densities onto surfaces of these two origins. Field films were prepared by covering substrata with plankton meshes, to exclude larvae, and additional laboratory treatments showed that such handling does not produce different recruitment from that onto substrata that were unnetted. One further experimental treatment was plates that had been placed in sterile seawater, and recruitment onto these surfaces confirmed that both field and laboratory films did have positive (and negative) effects on recruitment. In a second experiment, we prepared laboratory microbial films of four ages: 0, 1, 3, and 6 days. These substrata were immersed in the field for 3 and 6 days in a balanced experiment. Recruitment rates varied significantly with age of film for five of 13 taxa. Two polychaete species and two arborescent bryozoans ( Bugula stolonifera and Bugula neritina ) showed a positive relationship, and the barnacle Balanus variegatus recruited in greater numbers onto less filmed surfaces. Seven other taxa, including one protozoan, a sponge, and five ascidian taxa, showed no relationship with age of microbial film, despite high recruitment rates of these taxa. Summed across all taxa, total recruitment increased with age of film, almost doubling from unfilmed surfaces to those that began the field period with 6-day-old films. Comparison of 3- and 6-day field immersion periods showed that mean daily recruitment of some species, including a number of those responding to the presence of films, was higher on substrata left in the field for 6-days. Some of these patterns were consistent with the hypothesis that laboratory-derived films become supplemented by further microbial organisms in the field, making them even more attractive to settling larvae. An alternative hypothesis, that higher recruitment onto plates immersed for 6 days reflects temporally patchy recruitment, with pulses of recruitment in the latter half of the experimental period, could not be rejected. The experiments show that under field conditions, invertebrate larvae settle at very different rates onto surfaces differing only in the composition of the microbial community. Such settlement choices may be important in determining recolonization sequences following small-scale disturbances.

Phenotype–environment mismatches reduce connectivity in the sea

The connectivity of marine populations is often surprisingly lower than predicted by the dispersal capabilities of propagules alone. Estimates of connectivity, moreover, do not always scale with distance and are sometimes counterintuitive. Population connectivity requires more than just the simple exchange of settlers among populations: it also requires the successful establishment and reproduction of exogenous colonizers. Marine organisms often disperse over large spatial scales, encountering very different environments and suffering extremely high levels of post-colonization mortality. Given the growing evidence that such selection pressures often vary over spatial scales that are much smaller than those of dispersal, we argue that selection will bias survival against exogenous colonizers. We call this selection against exogenous colonizers a phenotype-environment mismatch and argue that phenotype-environment mismatches represent an important barrier to connectivity in the sea. Crucially, these mismatches may operate independently of distance and thereby have the potential to explain the counterintuitive patterns of connectivity often seen in marine environments. We discuss how such mismatches might alter our understanding and management of marine populations.

The Evolutionary Ecology of Offspring Size in Marine Invertebrates

Intraspecific variation in offspring size is of fundamental ecological and evolutionary importance. The level of provisioning an organism receives from its mother can have far reaching consequences for subsequent survival and performance. In marine systems, the traditional focus was on the remarkable variation in offspring size among species but there is increasing focus on variation in offspring size within species. Here we review the incidence and consequences of intraspecific offspring-size variation for marine invertebrates. Offspring size is remarkably variable within and among marine invertebrate populations. We examined patterns of variation in offspring size within populations using a meta-analysis of the available data for 102 species across 7 phyla. The average coefficient of variation in offspring size within populations is 9%, while some groups (e.g., direct developers) showed much more variation (15%), reflecting a fourfold difference between the largest and smallest offspring in any population. Offspring-size variation can have for reaching consequences. Offspring size affects every stage of a marine invertebrates life history, even in species in which maternal provisioning accounts for only a small proportion of larval nutrition (i.e., planktotrophs). In species with external fertilization, larger eggs are larger targets for sperm and as such, the sperm environment may select for different egg sizes although debate continues over the evolutionary importance of such effects. Offspring size affects the planktonic period in many species with planktotrophic and lecithotrophic development, but we found that this effect is not universal. Indeed, much of the evidence for the effects of offspring size on the planktonic period is limited to the echinoids and in this group and other taxa there is variable evidence, suggesting further work is necessary. Post-metamorphic effects of offspring size were strong in species with non-feeding larvae and direct development: bigger offspring generally have higher post-metamorphic survival, higher growth rates and sometimes greater fecundity. Although there is limited evidence for the mechanisms underlying these effects, the size of post-metamorphic feeding structures and resistance to low-food availability appear to be good candidates. There was limited evidence to assess the effects of offspring size on post-metamorphic performance in planktotrophs but surprisingly, initial indications suggest that such effects do exist and in the same direction as for species with other developmental modes. Overall, we suggest that for direct developers and species with non-feeding larvae, the post-metamorphic effects of offspring size will be greatest source of selection. Offspring-size variation can arise through a variety of sources, both within and among populations. Stress, maternal size and nutrition, and habitat quality all appear to be major factors affecting the size of offspring, but more work on sources of variation is necessary. While theoretical considerations of offspring size can now account for variation in offspring size among mothers, they struggle to account for within-brood variation. We suggest alternative approaches such as game theoretic models that may be useful for reconciling within-clutch variation. While some of the first theoretical considerations of offspring size were based on marine invertebrates, many of the assumptions of these models have not been tested, and we highlight some of the important gaps in understanding offspring-size effects. We also discuss the advantages of using offspring size as a proxy for maternal investment and review the evidence used to justify this step. Overall, offspring size is likely to be an important source of variation in the recruitment of marine invertebrates. The quality of offspring entering a population could be as important as the quantity and further work on the ecological role of offspring size is necessary. From an evolutionary standpoint, theoretical models that consider every life-history stage, together with the collection of more data on the relationship between offspring size and performance at each stage, should bring us closer to understanding the evolution of such a wide array of offspring sizes and developmental modes among species.

Occupation of patches in the epifaunal communities on pier pilings and the bivalve Pinna bicolor at Edithburgh, South Australia

SummaryThe reoccupation of artificially cleared patches in a subtidal epifaunal community was investigated in two field experiments on the pilings of Edithburgh pier, South Austrlia. In most cases, the greatest proportion of the patch was reoccupied by the vegetative extension of established sponge and tunicate colonies adjacent to it. Larval recruitment by sponges, bryozoans, tunicates and serpulids contributed to the reoccupation but resulted in only a small proportion of the mean percentage cover. The relative abundances of individual species established in any patch were shown to be a function of the (1) position in space, (2) age, (3) time of creation, (4) initial size of the patch.There was a large amount of between-patch variation in all cases. Overgrowth interactions occurred frequently within patches, and for many pairs of species, neither species consistently overgrew the other. Overgrowth interactions were tested statistically, and a large number of pairs of species were found to be competitively equivalent. This represents a possible situation additional to the alternatives recognized in the literature, namely competitive hierarchies or networks. Interactions between species should be regarded as stochastic, with a wide range of possible outcomes. The situation at Edithburgh is likely to produce greater between-patch variability than either a network or a hierarchy.Despite this large variation, super-specific taxa differ fairly consistently in capacity for overgrowth. Tunicates overgrow sponges, which overgrow bryozoans, which overgrow serpulids. The occupation of most patches was directional in the sense that bryozoans and serpulids invaded first, but tunicates and sponges excluded them and came to dominate the patch. These realtionships are used to predict patterns of abundance for substrata which are small and isolated, and these predictions are compared with the epifauna of the bivalve Pinna bicolor, which provides such substrata adjacent to the pier.

EFFECTS OF PERIODIC DISTURBANCES FROM TRAMPLING ONROCKY INTERTIDAL ALGAL BEDS

We investigated the ability of an assemblage of animals and plants on rocky shores in southeastern Australia to resist and/or recover from repeated pulse disturbances in the form of trampling. Disturbances of four different intensities were applied experi- mentally over six summers, with no human access at other times of the year. The dominant intertidal plant, the brown alga Hormosira banksii, was affected by trampling, but the effects were heterogeneous between sites. At two sites, a series of pulse disturbances produced a series of pulse responses, although the effect of a given pulse varied among years, possibly related to the severity of summer desiccating conditions each year. At the third site, pulse disturbances produced a press response; at high levels of trampling, Hor- mosira was almost eliminated within 2 yr, and at two intermediate levels of trampling, cover was reduced from >90 to 60-70%, where it remained for 4 yr. Effects of trampling showed little small-scale spatial variation. Untrampled areas did fluctuate through time, often as a result of summer burnoff of algae. Natural disturbances occurred irregularly through the study, and their effects varied on very small spatial scales (among plots <30 m apart). Trampling enhanced the densities of a range of herbivorous mollusks, especially limpets, and reduced the abundance of articulated coralline algae, which were abundant in the understory of Hormosira mats. These effects varied among sites but showed much less variation on smaller spatial scales. The reductions in coralline algae may be a direct effect of trampling, but increases in mollusk abundance occurred some time after changes to Hormosira cover, and those changes may be an indirect effect of trampling. We compared the effects of trampling on areas of the shore that had been trampled for two and four summers, to test whether a past history of disturbance influenced the effect of a new disturbance. No significant effects were found on algae or mobile animals, although a mild summer may have made our test of history relatively weak. Hormosira banksii fits the definition of a keystone species or engineer and, as such, is an appropriate focus for management and as an indicator. Spatially heterogeneous effects of a constant physical perturbation, however, mean that management of these rocky shores requires more complex models and indicate that caution should be used in adopting this species as a uniform indicator of environmental change.

OFFSPRING SIZE AFFECTS THE POST-METAMORPHIC PERFORMANCE OF A COLONIAL MARINE INVERTEBRATE

The positive relationship between offspring size and offspring fitness is a fundamental assumption of life-history theory, but it has received relatively little attention in the marine environment. This is surprising given that substantial intraspecific variation in offspring size is common in marine organisms and there are clear links between larval experience and adult performance. The metamorphosis of most marine invertebrates does not represent a newbeginning, and larval experiences can have effects that carry over to juvenile survival and growth. We show that larval size can have equally important carryover effects in a colonial marine invertebrate. In the bryozoan Bugula neritina, the size of the non-feeding larvae has a prolonged effect on colony performance after metamorphosis. Colonies that came from larger larvae survived better, grew faster, and reproduced sooner or produced more embryos than colonies that came from smaller larvae. These effects crossed generations, with colonies from larger larvae themselves producing larger larvae. These effects were found in two populations (in Australia and in the United States) in contrasting habitats.

Dynamics of the Epifauna of the Bivalve Pinna Bicolor: Interactions Among Recruitment, Predation, and Competition

The epifauna on the shells of a subtidal population of the bivalve Pinna bicolor is composed mainly of encrusting bryozoans and serpulid polychaetes, with tunicates and sponges relatively uncommon. Only a small subset of the observed interactions between sessile organisms were capable of changing the patterns of abundance on individual Pinna shells. Didemnid tunicates were capable of excluding most other species, but the most common competitive interactions, those between encrusting bryozoans, had variable outcomes and frequently did not result in the exclusion of the loser from a patch (shell). Sponges were also capable of excluding bryozoans and serpulids, although at slower rates than tunicates. Serpulids were overgrown by all other species, although overgrowth usually did not result in their exclusion from patches. Predators were, in general, not capable of influencing the abundance of any species greatly. The exception involved two species of monacanthid fish, juveniles of which ate newly metamorphosed didemnid ascidians. These fish thus could prevent monopolization of some patches by tunicates. The effects of predation by juvenile fish and overgrowth by tunicates were variable in space and time. The interaction between variable tunicate recruitment and predation was important. Didemnids recruited in low numbers and, even in a year of high recruitment, did not colonize a large number of patches; in addition, most recruits were eaten by fish. Predation by fish played no role in another year, because few tunicates recruited. It is likely that the abundance of fish was also variable, since their recruitment is also likely to be variable in time. The combination of these factors has resulted in few patches being colonized by tunicates. In the 2 yr of the study, none of the fifty patches under observation was colonized successfully by didemnids, and observations on other Pinna shells suggest that no substantial establishment occurred in the 2—3 yr preceding this study. Thus, in most patches, predation and competition did not strongly influence the abundance of sessile organisms. The patterns of occupation of individual patches, and the overall abundance of sessile species in the community, could be explained adequately by the observed patterns of recruitment. This situation contrasts with the occupation of patches on the pilings of a nearby pier, where competitive interactions between occupants of a patch are the most important factor. The results of these experiments provide a mechanism to explain the previously noted difference in the abundance of sessile invertebrates on the shells of Pinna bicolor and on the pilings of the pier.

Patterns of recruitment of sessile invertebrates in two subtidal habitats

Abstract Recruitment of sessile marine invertebrates onto small panels at two subtidal sites in southern Australia varied considerably on all spatial and temporal scales. Recruitment at West Lakes was consistently higher than at Edithburgh, usually by an order of magnitude or more. There were strong seasonal trends in the number of recruits and the number of colonizing species per panel at West Lakes, but these trends were unclear at Edithburgh. Small panels received fewer recruits than did larger panels, although the number of recruits per cm 2 did not change. Individual species showed similar patterns of recruitment. The temporal pattern varied from year-round settlement, with seasonal peaks (most serpulids), to regular recruitment at the same time each year ( Didemnum sp., Botrylloides leachii Savigny), to irregular, intense peaks of recruitment ( Electroma georgiana Quoy and Gaimard, Ciona intestinalis (Linnaeus)). Even those species that showed regular peaks in recruitment showed great variation between years in the magnitude of the peaks. The spatial pattern of recruitment of individual species varied from random ( Spirorbis spp.) to strongly aggregated ( Elminius modestus Darwin, Mania ione Gray). Aggregated patterns of recruitment were probably due to settlement near adult conspecifics ( Elminius modestus , Balanus amphitrite Darwin), or to “swarms” of larvae settling together ( Hydroides norvegica (Gunnerus)). There was little synchrony between the two sites. Major peaks in recruitment at one site were not accompanied by peaks at the other site, and even a good year for a particular species at one site was not necessarily matched for the species at the other site, providing little support for the concept of generally “good” or “bad” years for a coastal region as a whole. Replicated panels that were immersed at the same time varied greatly in their recruitment. This was partly explained by the distance between panels: the similarity between a pair of panels sometimes decreased as the distance between them increased. This relation rarely explained >20% of the variation in similarities, however. Small panels were generally less similar to each other than were large panels. The increase in similarity as panels became closer together could not always be explained by gregarious behaviour of larvae, and was probably due to small-scale patchiness in the distribution of larvae in the plankton. There remained a large amount of variation in recruitment that could not be explained by the behaviour of individual species or by patchiness in the plankton.

Responses of settling invertebrate larvae to bioorganic films : effects of large-scale variation in films

Abstract Results of previous studies have shown that at two sites in southeastern Australia (Williamstown and Mornington), some sessile invertebrate species recruit at higher densities onto surfaces that have a microbial film present, and that some species recruit in proportion to the age (0–6days) of that film. Other sessile species, notably colonial ascidians, do not respond to the presence of these films, and some barnacles may avoid the films. We tested whether larvae can detect or respond to differences in the microbial films that develop in different geographic localities and on longer time scales. To do this, we first confirmed that laboratory-developed microbial films induced higher recruitment of benthic invertebrates at a third site, Queenscliff, in Port Phillip Bay, Victoria, Australia. Approximately two-thirds of the sessile species settling at the time of the experiment were more abundant on the filmed surfaces. We then allowed microbial films to develop at all three sites on experimental substrata that were covered with plankton mesh to exclude larvae. The sites were chosen to represent three different rates of development of microbial films. After 1 week, we removed the plankton meshes and reciprocally transplanted experimental surfaces between all three sites. At the same time, we brought a sample from each site back to the laboratory to estimate the number of recruits passing through plankton meshes. We tested two hypotheses using these data, first that settling larvae at a particular site respond more strongly to locally-developed films than to films originating elsewhere and second, that it is the density of the microbial film, rather than its origin, that determines recruitment. Williamstown appeared to have the fastest-growing, most luxurious microbial films, followed by Mornington and Queenscliff. Locally-developed films were not significantly more attractive than foreign films at Mornington or Queenscliff; none of the 15 taxa tested showed higher recruitment rates to the local treatment, and highest recruitment occurred on substrata filmed at Williamstown. At Williamstown, there were differences in recruitment rates to plates with films of different origin, but in each case, films from Williamstown received the most recruitment. These latter results could not separate our two hypotheses, but those from Mornington and Queenscliff suggest that larvae do not recognize and/or respond to films from their local area, but that more heavily-filmed surfaces may be more attractive to settling larvae. The species showing the strongest responses were polychaetes, encrusting bryozoans, and some solitary ascidians. We also compared the attractiveness of laboratory-developed films varying in age up to 1 month and found that some species (serpulid polychaetes and encrusting bryozoans) recruited onto these surfaces at variable rates, while other species, notably ascidians, did not distinguish between the different substrata.

Larval settlement in hard substratum epifaunal assemblages: a manipulative field study of the effects of substratum filming and the presence of incumbents

Natural larval settlement on black Perspex settlement panels was analysed for two experiments (1 and 2) conducted amongst epifaunal assemblages beneath pier pilings at Williamstown, Victoria and one experiment at Mornington, Victoria, in southeastern Australia. The overall objectives of this manipulative study were to distinguish experimentally the effects of “filming” of the substrata and the presence of previously settled incumbent invertebrates on subsequent larval settlement in the sublittoral. Filming of substrata, whilst largely excluding larval settlement, was permitted by the enclosure of settlement panels within tightly-fitting pouches of plankton gauze of 150 and 236 μm mesh size. Williamstown 1 and Mornington included only fine-mesh treatments and Williamstown 2 included both coarse and fine mesh-sizes and also an additional treatment in which panels were initially filmed intertidally and then deployed sublittorally. Each experiment was conducted over periods of ≈2 wk. For Williamstown 1 filming generally enhanced larval settlement, with the exception of various ascidian species and the erect bryozoan Bugula neritina. Inhibitory effects of incumbents were found for Bugula dentata, the colonial ascidian Trididemnum spp. and Total Settlement: this effect was possibly attributable to Didemnids (excl. Trididemnum spp.). For the repeat of the first experiment (Williamstown 2), Bugula dentata and Serpulins all showed enhanced settlement in response to films developed on panels screened with both mesh sizes. Incumbents inhibited the settlement of Didemnids (excluding Trididemnum spp.) (cf. Williamstown 1) and Encrusting Bryozoans were facilitated. There was no significant difference in sublittoral settlement during the second week of the Williamstown 2 experiment between panels upon which the initial filming was developed either intertidally or sublittorally: settling larvae apparently responded simply to whether or not a substratum was filmed and not to the source of the film, although the possibility remains of rapid modification of the intertidal film to one typical of the sublittoral. At Mornington, Arborescent Bryozoans, Tricellaria occidentaux, Slime Sponges and Spirorbins all showed enhancement of their settlement by filming of the substrata, whereas incumbents significantly inhibited settlement of Didemnids, Microporella sp., Encrusting Bryozoans and Tricellaria occidentalis. The results show clearly the importance of repeating experimental analyses such as these at a given site and of undertaking experiments at different sites. One striking outcome was the marked inhibitory effect on other settlers of Didemnids (excluding Trididemnum spp.) at Williamstown 2. Those ascidians were themselves subject to high levels of post-settlement mortality and, although the cause of their mortality remains unknown, it is possible that the bacteria and ciliates attacking the ascidians were the source of the inhibitory effects on other settlers: these micro-organisms might therefore themselves provide adaptive biological cues indicative of otherwise unfavourable substrata to settling larvae.