Cheryl Ann Zimmer

Patterns and Processes of Larval Emergence in an Estuarine Parasite System

Trematode parasites in intertidal estuaries experience constantly varying conditions, with the presence or absence of water potentially limiting larval transport between hosts. Given the short life spans (≤24 h) of cercariae, emergence timing should be optimized to enhance the probability of successful transmission. In the present study, field measurements and laboratory experiments identified processes that regulate the emergence of cercariae from their first intermediate snail hosts in an intertidal marsh. Larvae emerged over species-specific temperature ranges, exclusively during daylight hours, and only when snails were submerged. The three factors operate over different temporal scales: temperature monthly, light diurnally (24-h period), and water depth tidally (12-h period). Each stimulus creates a necessary condition for the next, forming a hierarchy of environmental cues. Emergence as the tide floods would favor transport within the estuary, and light may trigger direct (downward or upward) swimming toward host habitats. Abbreviated dispersal would retain asexually reproduced cercariae within the marsh, and local mixing would diversify the gene pool of larvae encysting on subsequent hosts. In contrast to the timing of cercarial release, emergence duration was under endogenous control. Duration of emergence decreased from sunrise to sunset, perhaps in response to the diminishing lighted interval as the day progresses. Circadian rhythms that control cercarial emergence of freshwater species (including schistosomes) are often set by the activity patterns of subsequent hosts. In this estuary, however, the synchronizing agent is the tides. Together, exogenous and endogenous factors control emergence of trematode cercariae, mitigating the vagaries of an intertidal environment.

LARVAL SWIMMING OVERPOWERS TURBULENT MIXING AND FACILITATES TRANSMISSION OF A MARINE PARASITE

Planktonic cercariae (parasite larvae) of digenetic flatworms (Himasthla rhigedana) encyst up to 100% of intermediate host populations. Toward explaining such high prevalence, larval behavior and passive-transport processes were evaluated experimentally for their roles in waterborne parasite transmission. Using a new application of laser and digital video imaging technologies, we quantified cercarial movements in still water and in simulated field flows. In still water, downward swimming in response to light, irrespective of intensity or source, and gravity brought larvae to the bottom three-times faster than gravitational sinking alone. A 33% elevation in temperature (18–24°C) caused a 71% increase in swim speed. In flume flows characteristic of southern California salt marshes (u* = 0.2 cm/s, occurring >80% of the time), vertical larval distributions were highly bottom skewed. The mean downward swim speed (0.59 cm/s at 24°C) was three times faster than turbulent fluctuations (w′ = 0.23 cm/s), indicating...

MECHANISMS RECONCILING GREGARIOUS LARVAL SETTLEMENT WITH ADULT CANNIBALISM

Marine benthic invertebrates living in dense, intraspecific aggregations are important community members because they provide structural habitat for other species. Here, we determined the mechanisms that facilitate gregarious larval settlement and promote group living. Using suspension-feeding oysters (Crassostrea gigas) residing in large assemblages (“reefs”), experiments were conducted under laboratory conditions that simulated critical aspects of natural estuarine habitats. Oyster larvae were attracted to the scent of their conspecific elders. In still-water trials, they moved downward and settled after contacting a waterborne, adult chemical cue. Yet, mortality of larvae placed in the adult pallial cavity was very high (mean of 91.3%). This seeming paradox of larval attraction to adult cannibals was resolved via laboratory flume (2 cm/s and 6 cm/s flows) experiments. Suspension-feeding activity did not significantly affect flow speeds or directions. Moreover, weak (mean of 1.65 mm/s) adult ciliary currents effectively entrained phytoplankton but rarely captured larvae. In fact, only a small percentage (≤4.6%) of settlers was cannibalized in flume trials, even when they passed within 1 mm of the inhalant opening, or “gape” (a narrow slit between two valves). Larvae cued by conspecifics potentially attach to any portion of the shell surface, but there is a low probability that they will land in or near the inhalant opening. On juvenile and adult oysters, for example, the mean ratio of gape to shell surface area was only 0.025. Furthermore, in surveys of juvenile/adult oysters at nine field sites (Hood Canal and eastern Olympic Peninsula, Washington, USA), the gape was ≤5.2% of the total plane surface area of the reef. Thus, an oyster larva settling onto a reef of suspension-feeding adults is unlikely to be cannibalized. Given this low mortality risk at settlement, future fitness payoffs (e.g., improved fertilization success) may drive the evolution of a gregarious settlement cue that promotes group living.

Dispersal pathways, seed rains, and the dynamics of larval behavior

Dispersing propagules (larvae, seeds, and spores) establish and maintain populations, which serve as templates for subsequent species interactions. Connectivity among demes derives, in large part, from connectivity between consecutive steps, release, transport, and settlement, in dispersal pathways. Concurrent measurements of individuals in each step are a necessary precursor to identifying governing mechanisms. Here we directly and definitively resolved the roles of physics and behavior in mediating dispersal pathways of an estuarine parasite between its intermediate hosts. Planktonic cercariae of Himasthla rhigedana, a parasitic flatworm, are functionally similar to lecithotrophic larvae of many free-living marine invertebrates. The combination of parasite life cycle characteristics and the relatively simple tidal flows in their habitat renders this system an effective model for dispersal studies. Simultaneous field measurements of larval release, transport, settlement, and the flow regime, together with mechanistic experiments, led to empirical understanding of host colonization. All dispersal steps were highly and significantly correlated over time and in space. This tight coupling resulted, unequivocally, from a suite of larval behaviors. Cercariae emerged from first intermediate host snails only during daytime flood tides, enhancing larval retention in the marsh. Daylight triggered downward swimming, and within seconds, cercariae overpowered turbulent mixing, landing in benthic habitat of second intermediate host snails and crabs. Larvae settled (encysted) on external regions of snails/crabs that, presumably, were most vulnerable to ingestion by definitive host shorebirds. In total, cercarial behaviors greatly foreshortened dispersal distances, magnified local parasite prevalence, and increased the likelihood of large-scale transmission by definitive hosts. Cracking open the black box of dispersal thus revealed mechanisms, connectivity, and ecological consequences of the larval stage.

Adult macrofauna effects on Capitella sp. I larval settlement : A laboratory flume study

The opportunistic, deposit-feeding polychaete Capitella sp. I is the overwhelming numerical dominant in disturbed and enriched sediments and rarely co-occurs in appreciable numbers with other abundant mud-dwelling macrofauna. Rapid colonization and population increase in organic-rich sediments is typically followed by subsequent sharp decline. The mechanistic basis for these characteristics was explored in flume-flow experiments that tested whether settling Capitella sp. I larvae avoid sediments inhabited by macrofaunal adults or sediments reworked by them. The first set of experiments consisted of four treatments: conspecific adults or no adults in reworked or non-reworked sediment. Capitella sp. I settlement was significantly altered (depressed) only by pelletized sediment of conspecific adults. The second set of experiments involved similar treatments, but with adults of the deposit-feeding bivalve Tellina agilis. Neither adult presence nor sediment reworking significantly affected settlement of Capitella sp. I larvae. A third set of experiments that compared settlement in sediments with and without the suspension-feeding bivalve Mulinia lateralis demonstrated no significant treatment effect. These results suggest that larval settlement behavior could contribute to population growth in a boom and bust species when a critical limiting resource is overexploited. That is, sediments completely pelletized by Capitella sp. I adults may signal settling larvae that organic matter is depleted. Larvae may therefore settle in smaller numbers and are more likely to be dispersed away from abundant populations of adults. Active avoidance of conspecific adults or adults of other taxa is unimportant for the taxa at the densities tested here.

Sperm Chemotaxis as Revealed With Live and Synthetic Eggs

Fertilization is one of the least understood fundamental biological processes. How sperm search for and find an egg remains enigmatic. Sperm attraction to egg-derived chemical cues may be significant evolutionarily for maintaining species barriers and important ecologically for increasing gamete encounters. New tools are needed, however, to resolve the functional consequences of these dissolved signal molecules. Freshly spawned eggs from red abalone (Haliotis rufescens) naturally release l-tryptophan, which stimulates chemotactic responses by conspecific sperm. Here, microspheres were manufactured to the approximate size and the same shape as female gametes and formulated to emit controlled doses of chemoattractant, imitating natural l-tryptophan release rates. When experimentally tested for effectiveness, male gametes did not distinguish between chemically impregnated mimics and live eggs, demonstrating that l-tryptophan alone is both necessary and sufficient to promote chemotaxis, and confirming the identity of a native sperm attractant. The techniques that we describe can be used to create synthetic eggs for most animal and plant species, including humans. Egg mimics increase the capacity for experimental manipulation and enable realistic studies of sperm behavior even in the absence of female gametes.

Chemical ecology of wave-swept shores: the primacy of contact cues in predation by whelks

Wave-swept shores are valuable for developing and testing key ecological principles. A synthesis of research is nonetheless missing a critical component: the chemosensory basis for behavioral interactions that determine population- and community-wide attributes. Chemical signaling environments on wave-swept shores, given their intense, turbulent mixing and complex topographies, would be difficult or impossible to simulate in a laboratory setting. For this reason, appropriately scaled field studies are needed to advance understanding of chemical stimuli and their biotic effects. Here, we performed a field investigation to establish the relative roles of dissolved and contact cues in predation by whelks (Acanthinucella spirata) on barnacles (Balanus glandula), their preferred prey. Experiments tested responses of whelks to seawater drawn above dense prey patches (10,240–12,180 barnacles m−2) and also over adjacent sand flats (no prey present). There was no evidence of waterborne stimuli associated with prey, even when sea states were nearly tranquil. Field trials also tested faux prey, which were constructed from cleaned barnacle shells and flavored gels. Prospective contact cues were presented to whelks at concentrations typical of epidermal tissue and cuticle in live, intact barnacles. These compounds were highly effective inducers of attack behavior and feeding. Selective enzyme degradations showed that the bioactive material was proteinaceous. Moreover, whelks did not distinguish faux barnacles with a single, purified glycoprotein (named “MULTIFUNCin”) from live counterparts. Combined field results thus demonstrate the importance of contact cues, and indicate little, if any, effect of waterborne cues on predation by whelks under native conditions. Our findings underscore the need for appropriately scaled field experiments, and highlight surface chemistry as a critical factor that drives trophic interactions on rocky, wave-swept shores.

Larval settlement in flocculated particulates

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