Life History Traits of Caribbean Octocorals of the Genus Antillogorgia and Their Implications for Larval Dispersa

In an era of growing concern about the fate of coral reefs worldwide, knowledge about the processes contributing to ecosystem resilience is crucial. In the context of marine benthic organisms like corals, larval supply is a key process modulating species resilience to ever- increasing disturbances (e.g., pollution, overfishing, global warming), as population replenishment, and thus recovery, largely depends on new larvae recruiting to adult populations. Consequently, a substantial body of research has focused on determining whether populations are connected by larval exchange or instead maintained by local supply of larvae. In the process of these endeavors, the generalized belief that marine populations are well connected via larval dispersal gave way to the notion that local retention of larvae is common among many demersal and benthic species, as a result of the multitude of processes involved in larval transport. Among coral species, conclusions about the scales of larval dispersal are often species-specific and almost always location-specific. However, some generalities can be recognized. Extreme cases of larval philopatry are more common in brooders. Conversely, large-scale dispersal is seemingly more common in broadcast spawners where a pre-competency period and a potentially long-lived larval phase provide a template for more distant dispersal. In between these extremes, the divide is less clear and complex patterns of population connectivity are widespread between the two developmental modes. Resolving connectivity at demographically relevant scales remains challenging because it is impossible to directly estimate dispersal of millions of minute larvae over large spatial scales, and considerable methodological improvements are needed. Nevertheless, both genetic analyses and biophysical models of dispersal are rapidly maturing and provide increasingly sophisticated analyses of connectivity. In addition to these methodological challenges, the paucity of empirical data on the biological traits that influence dispersal has also limited our ability to quantify dispersal and connectivity in marine systems. The reproductive and larval biology of two congener species of Caribbean octocorals with contrasting modes of reproduction were characterized in detail. One species, the internal brooder Antillogorgia hystrix, was studied in the shallow-water reefs of Great Abaco (The Bahamas) from 2009 to 2010, whereas the other, the broadcast spawner Antillogorgia americana, was studied in the Florida Keys (USA) in 2014. Both species are gonochoric and reproduce annually. The population of A. hystrix was found to have a skewed sex ratio toward females (~3:1). Oogenesis preceded spermatogenesis by several months, and lasted at least 9 months, with oocytes >100 mum in diameter first becoming visible in dissections of samples from February. Mature oocytes (400-- 900 mum), which were larger than the spermaries (< 400 mum), were present in samples from late October--November. Brooded planulae were observed in polyps from early November to mid- December, and planula release was observed in aquaria in December 2009, which suggests that planulation occurs continuously over this period. Histological sections showed that planulae contained dinoflagellate symbionts, presumably acquired during embryogenesis and/or by mature planulae while inside the gastrovascular cavity of the polyp. Similar to other coral species, spawning of A. americana in the Florida Keys, USA, was associated with the lunar cycle and occurred over 2 separate events following the full moon of November. Despite the rapid larval development (2?3 d) and onset of competency to settle at ~4 d, most larvae delayed settlement for an extended period of time, with 50% of the cohort transitioning to the benthos by 36 d, and 95% by 58 d. Larval mortality in the laboratory was surprisingly low (10% over 58 d). Egg buoyancy and larval swimming behavior were highly variable both within cohorts and over time. In particular, there was a significant decrease in propagule buoyancy during embryogenesis, which was gradually offset by the increase in larval swimming activity (~3?4 d). Most larvae had negative geotactic behavior for up to 20 d. In contrast to A. hystrix, which releases negatively buoyant competent larvae and is uncommon in most of The Bahamas and Caribbean, the observed capacity of A. americana to delay settlement suggests the dispersal potential is high, which undoubtedly contributes to its broad distribution in the Caribbean. Importantly, our results underline the inherent variation observed in A. americana larval traits, particularly swimming behavior, which has potentially important implications for dispersal, but are rarely considered in models of larval dispersal because of the presumably weak swimming capabilities of coral larvae. Building on this premise, the Connectivity Modeling System, a spatially-explicit biophysical model of dispersal, was used to evaluate the effect of A. americana ontogenetic changes in propagule buoyancy (OCB) on modeled connectivity in NE Caribbean and tropical NW Atlantic. It was found that the inclusion of propagule OCB in the model resulted in increased connectivity between reefs and regions, decreasing subpopulation fragmentation of the reef network. In general, the advection of propagules as passive particles fails to describe processes like egg buoyancy, onset of upward larval swimming and subsequent increase of larval density as lipid reserves are depleted of A. americana, all of which increase the initial dispersal away from source reefs, as well as the likelihood of larvae being advected (vertically) to settlement substrata later on. Importantly, we found that variation in connectivity introduced by considering OCB was of similar orders of magnitude to that resulting from inter-annual variation in hydrodynamic transport. When integrated over millions of larvae, the combined effect of propagules OCB and a stochastic physical environment creates a diversity of paths larvae can take that fundamentally differs from those taken by passive propagules. These findings highlight the shortcomings of oversimplifying the role of coral larval behavior in dispersal models aiming to predict patterns of larval supply.