Reproduction, early development, and larval rearing strategies for two sponge-dwelling neon gobies, Elacatinus lori and E.colini

A major goal of the aquaculture industry is to reduce collection pressure on wild populations by developing captive breeding techniques for marine ornamental species, particularly coral reef fishes. The objective of this study was to develop a rearing protocol for two recently described species of neon gobies that are endemic to the Mesoamerican Barrier Reef: 1) Elacatinus lori; and 2) Elacatinus colini. First, the current study describes the reproductive behavior and larval development of both species. Second, it evaluates the effects of different rotifer and Artemia densities on the survival and growth of E. lori and E. colini larvae. Third, it compares the survival and growth of E. colini larvae fed wild plankton to those fed a combination of rotifers and Artemia. Once acclimated, pairs of E. lori began spawning in 53.2 ± 12.4 d (mean ± sd), while pairs of E. colini took only 12.2 ± 10.3 d. E. lori produced more embryos per clutch (1009 ± 477) than E. colini (168 ± 83). E. lori larvae hatched 8.18 ± 0.4 days after initial observation with a notochord length of 3.67 ± 0.2 mm. In comparison, E. colini larvae hatched 6.8 ± 0.4 days after initial observation with a notochord length of 3.51 ± 2.3 mm. Both species settled as early as 28 days post hatch at 9–9.5 mm standard length, following the fusion of the pelvic fins to form a pelvic disc. During rotifer density trials, from 0 to 6 days post hatch, there was no significant difference in survival or standard length between treatments fed 10, 15 or 20 rotifers ml^− 1 for either species. During Artemia density trials, from 6 to 14 days post hatch, control treatments fed solely on 15 rotifers ml^− 1 had significantly higher survival than treatments that were fed rotifers in combination with 3, 6 or 9 Artemia ml^− 1. Finally, E. colini larvae that were fed wild plankton had significantly higher survival and growth than those fed with a combination of 15 rotifers ml^− 1 and 3 Artemia ml^− 1. The results of this study suggest that Artemia nauplii are not a suitable prey for E. lori or E. colini larvae. Our results demonstrate the feasibility of rearing E. lori and E. colini to settlement, and suggest that 10–20 rotifers ml^− 1 and wild plankton provide a viable starting point for optimizing the survival and growth of Elacatinus spp. larvae.We would like to thank the Belizean government and Fisheries Department for permission to conduct this research. Thank you to the staff at the International Zoological Expeditions for their support in the field. Special thanks to Katrina Catalano, Kevin David, Robin Francis, Jeremiah Seymour, James Ferrito, Derek Scolaro and Alex Ascher for their assistance in the lab and rearing larvae. Dr. John Crawford, Dr. Karen Warkentin and Dr. Jacqueline Webb provided helpful comments on this manuscript. This research comprises a portion of JEM's doctoral thesis requirements (Boston University). Funding was provided by a start-up award to PMB from the Trustees of Boston University, the IDC account of JA and a Warren McLeod Summer Research Scholarship awarded by the Boston University Marine Department to JEM. Additional funding was provided by two NSF grants (OCE-1260424 and OCE-1459546), and an NSF Doctoral Dissertation Improvement Grant (IOS-1501651). The authors would also like to thank the Marine Aquarium Societies of North America's Dr. Junda Lin Memorial Fund for Publishing Open Access Marine Aquarium Research for offsetting the open access publishing costs of this article. More info at tiny.cc/MASNAPubFund. All work was approved by the Belize Fisheries Department and the Boston University IACUC (protocol # 10-036). (Trustees of Boston University; Warren McLeod Summer Research Scholarship - Boston University Marine Department; OCE-1260424 - NSF; OCE-1459546 - NSF; IOS-1501651 - NSF Doctoral Dissertation Improvement Grant; IDC account; Marine Aquarium Societies of North America's Dr. Junda Lin Memorial Fund for Publishing Open Access Marine Aquarium Research)Published versio

Patterns, causes, and consequences of marine larval dispersal

Quantifying the probability of larval exchange among marine populations is key to predicting local population dynamics and optimizing networks of marine protected areas. The pattern of connectivity among populations can be described by the measurement of a dispersal kernel. However, a statistically robust, empirical dispersal kernel has been lacking for any marine species. Here, we use genetic parentage analysis to quantify a dispersal kernel for the reef fish Elacatinus lori, demonstrating that dispersal declines exponentially with distance. The spatial scale of dispersal is an order of magnitude less than previous estimates—the median dispersal distance is just 1.7 km and no dispersal events exceed 16.4 km despite intensive sampling out to 30 km from source. Overlaid on this strong pattern is subtle spatial variation, but neither pelagic larval duration nor direction is associated with the probability of successful dispersal. Given the strong relationship between distance and dispersal, we show that distance-driven logistic models have strong power to predict dispersal probabilities. Moreover, connectivity matrices generated from these models are congruent with empirical estimates of spatial genetic structure, suggesting that the pattern of dispersal we uncovered reflects long-term patterns of gene flow. These results challenge assumptions regarding the spatial scale and presumed predictors of marine population connectivity. We conclude that if marine reserve networks aim to connect whole communities of fishes and conserve biodiversity broadly, then reserves that are close in space (<10 km) will accommodate those members of the community that are short-distance dispersers.We thank Diana Acosta, Alben David, Kevin David, Alissa Rickborn, and Derek Scolaro for assistance with field work; Eliana Bondra for assistance with molecular work; and Peter Carlson for assistance with otolith work. We are grateful to Noel Anderson, David Lindo, Claire Paris, Robert Warner, Colleen Webb, and two anonymous reviewers for comments on this manuscript. This work was supported by National Science Foundation (NSF) Grant OCE-1260424, and C.C.D. was supported by NSF Graduate Research Fellowship DGE-1247312. All work was approved by Belize Fisheries and Boston University Institutional Animal Care and Use Committee. (OCE-1260424 - National Science Foundation (NSF); DGE-1247312 - NSF Graduate Research Fellowship)Published versio

Potential roles of smell and taste in the orientation behaviour of coral‐reef fish larvae: insights from morphology

An ontogenetic analysis of the olfactory organ and the number and distribution of internal taste buds was carried out in two neon gobies (Elacatinus lori and Elacatinus colini) with the goal of revealing morphological trends that might inform an understanding of the roles of olfaction and taste in larval orientation behaviour. The pattern of development of the olfactory organ is unremarkable and enclosure of the olfactory epithelium occurs concurrently with metamorphosis and settlement in both species. Like other gobies, juvenile and adult E. lori and E. colini lack complex olfactory lamellae, and lack the accessory nasal sacs present in some adult gobies that could facilitate active olfactory ventilation (i.e., sniffing). A small number of internal taste buds are present at hatch with most found in the caudal region of the buccal cavity (on gill arches, roof of buccal cavity). As taste bud number increases, they demonstrate an anterior spread to the lips, buccal valves and tongue (i.e., tissue covering the basihyal). In the absence of an active ventilatory mechanism for the olfactory organs, the water that moves through the buccal cavity with cyclic gill ventilation may provide chemical cues allowing the internal taste buds to play a role in chemical‐mediated orientation and reef‐seeking behavior in pelagic larval fishes

An integrative investigation of sensory organ development and orientation behavior throughout the larval phase of a coral reef fish

The dispersal of marine larvae determines the level of connectivity among populations, influences population dynamics, and affects evolutionary processes. Patterns of dispersal are influenced by both ocean currents and larval behavior, yet the role of behavior remains poorly understood. Here we report the first integrated study of the ontogeny of multiple sensory systems and orientation behavior throughout the larval phase of a coral reef fish—the neon goby, Elacatinus lori. We document the developmental morphology of all major sensory organs (lateral line, visual, auditory, olfactory, gustatory) together with the development of larval swimming and orientation behaviors observed in a circular arena set adrift at sea. We show that all sensory organs are present at hatch and increase in size (or number) and complexity throughout the larval phase. Further, we demonstrate that most larvae can orient as early as 2 days post-hatch, and they swim faster and straighter as they develop. We conclude that sensory organs and swimming abilities are sufficiently developed to allow E. lori larvae to orient soon after hatch, suggesting that early orientation behavior may be common among coral reef fishes. Finally, we provide a framework for testing alternative hypotheses for the orientation strategies used by fish larvae, laying a foundation for a deeper understanding of the role of behavior in shaping dispersal patterns in the sea

Hydrodynamic and biological constraints on group cohesion in plankton

•Fish larvae and plankton have the abilities to actively counteract the dispersive effects of micro-scale turbulence and could maintain group cohesion.•Some fish larvae could form groups early on in development.•Specific swimming strategies would help maintain group cohesion.•Migration to low turbulence regions should enhance group cohesion.•Behavioral experiments should be done in natural turbulent environment. The dynamics of plankton in the ocean are determined by biophysical interactions. Although physics and biotic behaviors are known to influence the observed patchiness of planktonic populations, it is still unclear how much, and if, group behavior contributes to this biophysical interaction. Here, we demonstrate how simple rules of behavior can enhance or inhibit active group cohesion in plankton in a turbulent environment. In this study, we used coral-reef fish larvae as a model to investigate the interaction between microscale turbulence and planktonic organisms. We synthesized available information on the swimming speeds and sizes of reef fish larvae, and developed a set of equations to investigate the effects of viscosity and turbulence on larvae dispersion. We then calculated the critical dispersion rates for three different swimming strategies – cruise, random-walk, and pause-travel – to determine which strategies could facilitate group cohesion during dispersal. Our results indicate that swimming strategies and migration to low-turbulence regions are the key to maintaining group cohesion, suggesting that many reef fish species have the potential to remain together, from hatching to settlement. In addition, larvae might change their swimming strategies to maintain group cohesion, depending on environmental conditions and/or their ontogenic stage. This study provides a better understanding of the hydrodynamic and biological constraints on group formation and cohesion in planktonic organisms, and reveals a wide range of conditions under which group formation may occur

Data from: Differential persistence favors habitat preferences that determine the distribution of a reef fish

A central focus of population ecology is understanding what factors explain the distribution and abundance of organisms within their range. This is a key issue in marine systems, where many organisms produce dispersive larvae that develop offshore before returning to settle on benthic habitat. We investigated the distribution of the neon goby, Elacatinus lori, on sponge habitat and evaluated whether variation in the persistence of recently settled individuals (i.e., settlers) among different sponge types can result in habitat preferences and establish their observed distribution. We found that E. lori settlers were more likely to occur on large yellow tube sponges (Aplysina fistularis) than on small yellow sponges or brown tube sponges (Agelas conifera). An experiment seeding settlers onto multiple species and sizes of sponge habitat revealed that settlers persist longer on large yellow sponges than on small yellow sponges or brown sponges. Habitat preference experiments also indicated that settlers prefer large yellow sponges over small yellow sponges or brown sponges. Settlers achieved these preference behaviors using visual, but not chemical, cues. Finally, new settlers arriving from the water column were more likely to occur on large yellow sponges than on small yellow sponges or brown sponges, indicating that the observed habitat preferences existed independent of prior experience. These results support the hypothesis that E. lori have evolved behavioral preferences for sponge habitats that will maximize their post-settlement persistence, and that decisions at settlement will shape the population level pattern of settler distribution on coral reefs

Organization and Ontogeny of a Complex Lateral Line System in a Goby (Elacatinus lori), with a Consideration of Function and Ecology

Gobies (family Gobiidae) have a complex mechanosensory lateral line system characterized by reduced lateral line canals and a dramatic proliferation of small superficial neuromasts (on sensory papillae ), which are arranged in lines on the head, trunk, and tail. A suite of morphological methods was used to describe the distribution and morphology of canal and superficial neuromasts in the neon goby, Elacatinus lori, and to describe the ontogeny of the lateral line system for the first time for any gobiiform fish. Portions of only three cranial lateral line canals are retained and they contain a total of eight canal neuromasts. In addition, 128-155 superficial neuromasts are found in six head series (comprising 33 neuromast lines or rows). Superficial neuromasts are found in one body series (65-80 neuromasts arranged in three groups of vertical lines or stitches ) and one caudal fin series (3 lines, each located between fin rays and comprised of many small neuromasts; total of 27-53 neuromasts) extending to the tip of the caudal fin. The general distribution of neuromasts is established early during the larval stage, and neuromast numbers increase within and among lines resulting in an increase in overall complexity of the system. On day-of-hatch, a total of 22 neuromasts are present. At ∼15 days post-hatch, all eight cranial canal neuromasts are present, and, in post-settlement juveniles ( settlers ), they are enclosed in canals and a total of ∼185 neuromasts are found on the head, trunk, and tail. All neuromasts are small (∼40 lm long) and diamond-shaped, but three subpopulations (canal neuromasts, canal neuromast homologs, superficial neuromasts) are defined based on their location and their arrangement within lines ( tip-to-tip or side-by-side ). The ontogeny of the lateral line system and distinctions among neuromast subpopulations help to reveal the structural and functional organization of the complex lateral line system in Elacatinus and will contribute to the interpretation of neuromast patterns in other gobiiforms. A comparison of superficial neuromast number in 12 species of Elacatinus and Tigrigobius (sister genera) revealed variation among species that live in different reef microhabitats, which suggests that adaptive evolution in the lateral line system is evident among closely related taxa

Export sites shape file

This .shp file shows the centroids of the six additionally sampled export reef patches for the export parentage analysis. Suggested projection: Datum (WGS 84); Projection (UTM zone 16N)

Data from: Self-recruitment in a Caribbean reef fish: a method for approximating dispersal kernels accounting for seascape

Characterizing patterns of larval dispersal is essential to understanding the ecological and evolutionary dynamics of marine metapopulations. Recent research has measured local dispersal within populations, but the development of marine dispersal kernels from empirical data remains a challenge. We propose a framework to move beyond point estimates of dispersal towards the approximation of a simple dispersal kernel, based on the hypothesis that the structure of the seascape is a primary predictor of realized dispersal patterns. Using the coral reef fish Elacatinus lori as a study organism, we use genetic parentage analysis to estimate self-recruitment at a small spatial scale (<1 km). Next, we determine which simple kernel explains the observed self-recruitment, given the influx of larvae from reef habitat patches in the seascape at a large spatial scale (up to 35 km). Finally, we complete parentage analyses at six additional sites to test for export from the focal site and compare these observed dispersal data within the metapopulation to the predicted dispersal kernel. We find 4.6% self-recruitment (CI95%: ±3.0%) in the focal population, which is explained by the exponential kernel y = 0.915x (CI95%: y = 0.865x, y = 0.965x), given the seascape. Additional parentage analyses showed low levels of export to nearby sites, and the best-fit line through the observed dispersal proportions also revealed a declining function y = 0.77x. This study lends direct support to the hypothesis that the probability of larval dispersal declines rapidly with distance in Atlantic gobies in continuously distributed habitat, just as it does in the Indo-Pacific damselfishes in patchily distributed habitat