Human-mediated and natural dispersal of an invasive fish in the eastern Great Lakes.

The globally invasive Round Goby (Neogobius melanostomus) was introduced to the Great Lakes around 1990, spreading widely and becoming the dominant benthic fish in many areas. The speed and scope of this invasion is remarkable and calls into question conventional secondary spread models and scenarios. We utilized nine microsatellites to identify large-scale genetic structure in Round Goby populations in the eastern Great Lakes, and assessed the role of colonization vs. secondary transport and dispersal in developing this structure. We identified three clusters, corresponding with Lake Huron, eastern Lake Erie, and western Lake Erie plus eastern Lake Ontario, along with three highly divergent populations. Bottleneck analysis identified founder effects in two divergent populations. Regression analyses of isolation by distance and allelic richness vs. distance from the initial invasion site were consistent with limited migration. However, some populations in eastern Lake Erie and Lake Ontario showed anomalously low genetic distance from the original site of colonization, consistent with secondary transport of large numbers of individuals via ballast water. We conclude that genetic structure of Round Goby in the Great Lakes principally resulted from long-distance secondary transport via ballast water with additional movement of individual via bait buckets and natural dispersal. The success of Round Gobies represents an interesting model for colonization characterization; however, those same attributes present significant challenges for conservation and fisheries management. Current management likely prevents many new species from arriving in the Great Lakes, but fails to address the transport of species within the lakes after they arrive; this is an issue of clear and pressing importance.

Aquatic to terrestrial transfer of sediment associated persistent organic pollutants is enhanced by bioamplification processes.

Ephemeral emergent insects, such as mayflies (Hexagenia spp.), are commonly used as biomonitors of persistent organic pollutants (POPs) and provide a vector for aquatic-terrestrial contaminant transfer. Mayflies bioaccumulate sediment-associated contaminants by bioconcentration and biomagnification during the aquatic stage and concentrate POP residues postemergence due to bioamplification, which occurs as a result of weight and lipid loss without contaminant loss. The present study quantified polychlorinated biphenyl (PCB) bioamplification in male and female emergent mayflies at three sites. Male mayflies used 36 to 68% of their lipids during emergence, with the exception of caged males that were prevented from flight. Females did not lose lipid content between pre-emergent nymph and emerged life stages. Mass balance indicated no PCB elimination between life stages. The mean PCB bioamplification factor, expressed as the ratio of lipid-equivalent PCB concentrations across life stages, was 2.05 ± 0.38 for male imagos/nymphs and 1.91 ± 0.18 for male imago/subimago life stages. For females, bioamplification factors were close to unity. Wildlife consumers of imago stages of emergent mayflies can potentially increase their total daily intake of PCBs by 36% depending on the sex-ratio composition of their diet relative to animals that feed predominantly on nymph or subimago stages during mass emergence events.

The seminal vesicle synthesizes steroids in the round goby Neogobius melanostomus.

In this study, we examine the possible contribution of the seminal vesicles of the male round goby to the production of putative steroidal pheromones. A previous study showed that the testes of the round goby are rich in steroid-producing Leydig-like cells; and when incubated in vitro, convert tritiated androstenedione to at least six other steroids, including one not previously identified in fish--namely 3alpha-hydroxy-5beta-androstane-11,17-dione (11-oxo-etiocholanolone, 11-oxo-ETIO). The seminal vesicles of reproductively mature males were examined by conventional histology, transmission electron microscopy and immunocytochemistry (utilizing an antibody against 3beta-hydroxysteroid dehydrogenase--a key enzyme in vertebrate steroid synthesis). All three procedures identified Leydig cells in the proximal and medial regions of the seminal vesicles. In vitro incubation of seminal vesicles with tritiated androstenedione demonstrated biosynthesis of 11-oxo-androstenedione, 11-oxo-testosterone (more commonly known as 11-ketotestosterone) and 11 oxo-ETIO. These data indicate that the seminal vesicles, as well as the testes are involved in the synthesis of steroidal compounds that may function as pheromones.

Use of chemical communication in the management of freshwater aquatic species that are vectors of human diseases or are invasive.

Chemical communication occurs when both originator (signaller) and one or more receiver(s) possess specializations for chemical exchange of information. Chemical information can be used by a wide variety of species to locate food and mates, avoid predators and engage in social interactions. In this review, we focus on chemical signalling between mates or cues from nest sites or hosts by selected aquatic pest species and indicate how chemical information can be used to manage pests. The pests are vectors of disease (blood-sucking insects) or invasive species (crayfishes and fishes) that have exhibited detrimental effects on indigenous species. Pheromones released by females attract and stimulate males in some taxa (insects, crayfish, goldfish, and crucian carp), whereas pheromones released by males attract females in others (round goby, sea lamprey). Other chemicals (e.g., habitat odours or odours given off by developmental stages of conspecifics) can affect oviposition decisions of pest species. In areas of aquatic environments where other cues may be limited (e.g., visual), freshwater organisms may rely solely on chemical signals or in concert with environmental cues for reproduction. Once the chemical structure of odour attractants are identified and shown to lure conspecifics to traps, odorants or their blends can be used to control the aquatic pests. There is promise for the application of pheromone traps to control the malarian vector (Anopheles gambiae) or invasive species such as signal crayfish (Pacifastacus leniusculus), sea lamprey (Petromyzon marinus) and the round goby (Neogobius melanostomus) by disrupting the reproductive behaviours of these species.

Differential behavioral responses by reproductive and non-reproductive male round gobies (Neogobius melanostomus) to the putative pheromone estrone.

Previous studies have shown that the frequency of gill ventilation during exposure to estrone and gonadal extracts in the round goby (Neogobius melanostomus) is linked to olfactory sensory input. Control over gill ventilation may be a regulatory mechanism used for odorant sampling during reproductive periods. In this study, we examined changes in gill ventilation in osmic and anosmic (nasal occluded), reproductive and non-reproductive male round gobies to a putative steroidal pheromone estrone (1,3,5(10)-estratrien-3-ol-17-one). We tested 5 different concentrations of estrone (10(-12) to 10(-8) M) and showed that the response threshold for estrone varied with the male's reproductive status; it was 10(-11) M in reproductive males, and rose to 10(-9) M in non-reproductive males. However, anosmic reproductive and non-reproductive males did not respond to estrone. These findings suggest that olfactory responses to putative pheromones may change depending on the reproductive status of the fish.

Olfactory sensory input increases gill ventilation in male round gobies (Neogobius melanostomus) during exposure to steroids.

In teleostean fish, ventilation increases have been observed in response to low dissolved oxygen levels, visual stimuli, and gustatory cues. However, olfactory sensory input may also stimulate gill ventilation rate. We investigated whether olfactory sensory input mediates gill ventilation responses, as suggested by the observation that steroidal compounds detected by the olfactory system elicited increases in opercular activity in the perciform teleost, the round goby (Neogobius melanostomus). Close parallels between gill ventilation and olfactory responses, led us to conduct an empirical study that used two different olfactory sensory deprivation techniques to seek a causal relationship between olfactory epithelial activity and hyperventilation. Chemical lesion of olfactory sensory neurons or mechanical occlusion of the nasal cavities inhibited gill ventilation responses of reproductive male round gobies to estrone (1,3,5(10)-estratrien-3-ol-17-one) and to ovarian extracts. This direct evidence demonstrates the role of olfactory sensory input for the gill ventilation response to putative reproductive pheromones and may represent an important regulatory mechanism for odorant sampling during pheromone communication.

In vitro biosynthesis of novel 5beta-reduced steroids by the testis of the round goby, Neogobius melanostomus.

Previous studies indicate that, in the round goby Neogobius melanostomus, the reproductively mature male releases a pheromone that attracts ripe females. Furthermore, studies suggest that the pheromone may be a steroid (more specifically a 5beta-reduced androgen) produced by specialized glandular tissue in the testes. In the present study, it is shown that the testis of the male round goby contains such specialized glandular tissue. In vitro, the testes convert [3H]androstenedione into 3alpha-hydroxy-5beta-androstane-11,17-dione (i.e., 11-oxo-etiocholanolone, 11-oxo-ETIO); 11-oxo-ETIO sulfate (11-oxo-ETIO-s); 11-oxo-testosterone (i.e., 11-ketotestosterone), 3alpha-hydroxy-5beta-androstan-17-one (etiocholanolone, ETIO); 11beta-hydroxy-androstenedione; ETIO sulfate and testosterone. Glucuronidated steroids were not identified. Neither 11-oxo-ETIO nor 11-oxo-ETIO-s has previously been identified in teleost gonads. Both these steroids are formed in the round goby testis even when [3H]17-hydroxyprogesterone is used as a precursor. The fact that, for both steroids, the carbon A ring has a 5beta-configuration (already linked with olfactory sensitivity and behavior induction in two other species of gobies) makes them likely candidate pheromones in the round goby. However, their in vivo production and pheromonal activity remain to be proved.

Morphology and histochemistry of the peripheral olfactory organ in the round goby, Neogobius melanostomus (Teleostei: Gobiidae).

This first comprehensive study of the peripheral olfactory organ from a representative of the large and economically important order of teleost fishes, the Perciformes, shows a compact structure with olfactory sensory neurons distributed widely throughout the olfactory chamber. The spatial organization of the nasal cavity in the bottom-dwelling round goby (Gobiidae, Neogobius melanostomus) was examined using impression material injection, immunocytochemistry, and transmission electron microscopy. The olfactory chamber contains a single olfactory lamella; prominent dorsocaudal lachrymal and ethmoidal accessory nasal sacs are situated ventrocaudal to the chamber. The location of the olfactory mucosa within the olfactory chamber is novel for teleost fish, as it extends beyond the ventral surface to the lateral and dorsal regions. Microvillar olfactory sensory neurons and ciliated olfactory sensory neurons were identified by transmission electron microscopy and the spatial distribution of these two cell types was assessed through immunocytochemistry against olfactory receptor coupled G-proteins. Both G(alphaolf)-immunoreactive ciliated olfactory sensory neurons and the G(alphao)-immunoreactive microvillar form were located throughout the olfactory epithelium. Ciliated crypt cells were G(alphao) immunoreactive and were found throughout the olfactory epithelium of some specimens. The widespread occurrence of olfactory sensory neurons in the olfactory chamber supports the idea that olfactory signaling is important to the survival of the round goby. The prominence of the lachrymal and ethmoidal accessory nasal sacs indicates the capacity to regulate the flow of odorant molecules over the sensory surface of the olfactory sensory neurons, possibly through a pump-like mechanism driven by opercular activity associated with gill ventilation.

Effects of emergence date and maternal size on egg development and sizes of eggs and first-instar nymphs of a semelparous aquatic insect.

We examined whether or not sizes of eggs and offspring were related to emergence date or maternal size in a semelparous aquatic insect (the burrowing mayfly, Hexagenia) in which parental care is lacking and oviposited eggs are passively dispersed. We quantified the size of males and female imagos over the emergence span at a site on the Detroit River, Canada, and investigated relationships between emergence date and female size and (1) egg size and (2) size of first-instar nymphs. Although size of female imagos (H. limbata and H. rigida combined) declined significantly (P<0.025) over the emergence season, there was no significant relationship between body length and emergence date for males of either species. Males were significantly (P<0.001) smaller than females. H. limbata eggs, subsampled from three individuals from each of three size classes of female imagos collected on seven sampling dates, were measured using video image analysis. Eggs (n=100) oviposited by each of 63 H. limbata imagos were inspected daily for hatching. Newly hatched nymphs were removed, counted and measured. Egg size (P<0.001) and size of first-instar nymphs (P<0.001) varied significantly with emergence date, but not maternal size. The largest eggs and newly hatched nymphs occurred at peak emergence of adults. The synchronous release of larger (faster-sinking) eggs may result in reduced predation. Plasticity in egg development time and egg and nymph size may account for the ability of this taxon to recover from episodes of massive population reduction.