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

The evolution of marine larval dispersal kernels in spatially structured habitats: Analytical models, individual-based simulations, and comparisons with empirical estimates.

Author Posting. © University of Chicago Press, 2019. This article is posted here by permission of University of Chicago Press for personal use, not for redistribution. The definitive version was published in Shaw, A. K., D'Aloia, C. C., & Buston, P. M. The evolution of marine larval dispersal kernels in spatially structured habitats: Analytical models, individual-based simulations, and comparisons with empirical estimates. American Naturalist, 193(3), (2019):424-435, doi:10.1086/701667.Understanding the causes of larval dispersal is a major goal of marine ecology, yet most research focuses on proximate causes. Here we ask how ultimate, evolutionary causes affect dispersal. Building on Hamilton and May’s classic 1977 article “Dispersal in Stable Habitats,” we develop analytic and simulation models for the evolution of dispersal kernels in spatially structured habitats. First, we investigate dispersal in a world without edges and find that most offspring disperse as far as possible, opposite the pattern of empirical data. Adding edges to our model world leads to nearly all offspring dispersing short distances, again a mismatch with empirical data. Adding resource heterogeneity improves our results: most offspring disperse short distances with some dispersing longer distances. Finally, we simulate dispersal evolution in a real seascape in Belize and find that the simulated dispersal kernel and an empirical dispersal kernel from that seascape both have the same shape, with a high level of short-distance dispersal and a low level of long-distance dispersal. The novel contributions of this work are to provide a spatially explicit analytic extension of Hamilton and May’s 1977 work, to demonstrate that our spatially explicit simulations and analytic models provide equivalent results, and to use simulation approaches to investigate the evolution of dispersal kernel shape in spatially complex habitats. Our model could be modified in various ways to investigate dispersal evolution in other species and seascapes, providing new insights into patterns of marine larval dispersal.We thank S. Levin, M. Neubert, S. Proulx, L. Sullivan, R. Warner, and several anonymous reviewers for helpful comments. This work was carried out in part using computing resources at the University of Minnesota Supercomputing Institute. The project was supported by a start-up award from the University of Minnesota to A.K.S. and a National Science Foundation award (OCE-1260424) to P.M.B. and colleagues; C.C.D. was supported by the Weston Howland Junior Postdoctoral Scholarship from the Woods Hole Oceanographic Institution.2020-01-1

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

Description of surface transport in the region of the Belizean Barrier Reef based on observations and alternative high-resolution models

Author Posting. © The Author(s), 2015. This is the author's version of the work. It is posted here for personal use, not for redistribution. The definitive version was published in Ocean Modelling 106 (2016): 74–89, doi:10.1016/j.ocemod.2016.09.010.The gains from implementing high-resolution versus less costly low-resolution models to describe coastal circulation are not always clear, often lacking statistical evaluation. Here we construct a hierarchy of ocean-atmosphere models operating at multiple scales within a 1×1° domain of the Belizean Barrier Reef (BBR). The various components of the atmosphere-ocean models are evaluated with in situ observations of surface drifters, wind and sea surface temperature. First, we compare the dispersion and velocity of 55 surface drifters released in the field in summer 2013 to the dispersion and velocity of simulated drifters under alternative model configurations. Increasing the resolution of the ocean model (from 1/12° to 1/100°, from 1 day to 1 h) and atmosphere model forcing (from 1/2° to 1/100°, from 6 h to 1 h), and incorporating tidal forcing incrementally reduces discrepancy between simulated and observed velocities and dispersion. Next, in trying to understand why the high-resolution models improve prediction, we find that resolving both the diurnal sea-breeze and semi-diurnal tides is key to improving the Lagrangian statistics and transport predictions along the BBR. Notably, the model with the highest ocean-atmosphere resolution and with tidal forcing generates a higher number of looping trajectories and sub-mesoscale coherent structures that are otherwise unresolved. Finally, simulations conducted with this model from June to August of 2013 show an intensification of the velocity fields throughout the summer and reveal a mesoscale anticyclonic circulation around Glovers Reef, and sub-mesoscale cyclonic eddies formed in the vicinity of Columbus Island. This study provides a general framework to assess the best surface transport prediction from alternative ocean-atmosphere models using metrics derived from high frequency drifters’ data and meteorological stations.This research is supported by the National Science Foundation award NSF-OCE 1260424

Strategic growth in social vertebrates

Individual differences in growth and size of vertebrates often represent adaptive, plastic responses to contrasts in ecological conditions. Recent studies show that vertebrates can also modify their growth and size in an adaptive fashion in response to fine-grain changes in social conditions (which we refer to as strategic growth). Here, we review experimental evidence for strategic growth in social vertebrates. We describe a set of conditions under which strategic growth commonly occurs, and highlight potential examples of convergent evolution of strategic growth across the tree of life. This synthesis has implications for the way we think about organismal growth and size, because it underscores that the size of individuals can often be fine-tuned to their social environment.Accepted manuscrip

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

Heritability of dispersal-related larval traits in the clown anemonefish Amphiprion percula

A major goal of marine ecology is to identify the drivers of variation in larval dispersal. Larval traits are emerging as an important potential source of variation in dispersal outcomes, but little is known about how the evolution of these traits might shape dispersal patterns. Here, we consider the potential for adaptive evolution in two possibly dispersal-related traits by quantifying the heritability of larval size and swimming speed in the clown anemonefish (Amphiprion percula). Using a laboratory population of wild-caught A. percula, we measured the size and swimming speed of larvae from 24 half-sibling families. Phenotypic variance was partitioned into genetic and environmental components using a linear mixed-effects model. Importantly, by including half-siblings in the breeding design, we ensured that our estimates of genetic variance do not include nonheritable effects shared by clutches of full-siblings, which could lead to significant overestimates of heritability. We find unequivocal evidence for the heritability of larval body size (estimated between 0.21 and 0.34) and equivocal evidence for the heritability of swimming speed (between 0.05 and 0.19 depending on the choice of prior). From a methodological perspective, this work demonstrates the importance of evaluating sensitivity to prior distribution in Bayesian analysis. From a biological perspective, it advances our understanding of potential dispersal-related larval traits by quantifying the extent to which they can be inherited and thus have the potential for adaptive evolution.https://onlinelibrary.wiley.com/doi/full/10.1002/ece3.954

Vertebrate growth plasticity in response to variation in a mutualistic interaction

Vertebrate growth can be phenotypically plastic in response to predator-prey and competitive interactions. It is unknown however, if it can be plastic in response to mutualistic interactions. Here we investigate plasticity of vertebrate growth in response to variation in mutualistic interactions, using clown anemonefish and their anemone hosts. In the wild, there is a positive correlation between the size of the fish and the size of the anemone, but the cause of this correlation is unknown. Plausible hypotheses are that fish exhibit growth plasticity in response to variation in food or space provided by the host. In the lab, we pair individuals with real anemones of various sizes and show that fish on larger anemones grow faster than fish on smaller anemones. By feeding the fish a constant food ration, we exclude variation in food availability as a cause. By pairing juveniles with artificial anemones of various sizes, we exclude variation in space availability as a single cause. We argue that variation in space availability in conjunction with host cues cause the variability in fish growth. By adjusting their growth, anemonefish likely maximize their reproductive value given their anemone context. More generally, we demonstrate vertebrate growth plasticity in response to variation in mutualistic interactions.https://link.springer.com/content/pdf/10.1038/s41598-022-14662-4.pdfPublished versio

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