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Geology topics

Tyler J. Buchinger

Publications and source records attributed to Tyler J. Buchinger.

15 recordsLinked to original sources

Male lake char release taurocholic acid as part of a mating pheromone

The evolutionary origins of sexual preferences for chemical signals remain poorly understood, due, in part, to scant information on the molecules involved. In the current study, we identified a male pheromone in lake char ( Salvelinus namaycush ) to evaluate the hypothesis that it exploits a non-sexual preference for juvenile odour. In anadromous char species, the odour of stream-resident juveniles guides migratory adults into spawning streams. Lake char are also attracted to juvenile odour but have lost the anadromous phenotype and spawn on nearshore reefs, where juvenile odour does not persist long enough to act as a cue for spawning site selection by adults. Previous behavioural data raised the possibility that males release a pheromone that includes components of juvenile odour. Using metabolomics, we found that the most abundant molecule released by males was also released by juveniles but not females. Tandem mass spectrometry and nuclear magnetic resonance were used to identify the molecule as taurocholic acid (TCA), which was previously implicated as a component of juvenile odour. Additional chemical analyses revealed that males release TCA at high rates via their urine during the spawning season. Finally, picomolar concentrations of TCA attracted pre-spawning and spawning females but not males. Taken together, our results indicate that male lake char release TCA as a mating pheromone and support the hypothesis that the pheromone is a partial match of juvenile odour.

Journal of Experimental Biology

Spatiotemporal segregation by migratory phenotype indicates potential for assortative mating in lake sturgeon

Migratory diversity can promote population differentiation if sympatric phenotypes become temporally, spatially, or behaviorally segregated during breeding. In this study, the potential for spatiotemporal segregation was tested among three migratory phenotypes of lake sturgeon ( Acipenser fulvescens ) that spawn in the St. Clair River of North America’s Laurentian Great Lakes but differ in how often they migrate into the river and in which direction they move after spawning. Acoustic telemetry over 9 years monitored use of two major spawning sites by lake sturgeon that moved north to overwinter in Lake Huron or south to overwinter in Lake St. Clair. Lake St. Clair migrants were further distinguished by whether they migrated into the St. Clair River each year (annual migrants) or intermittently (intermittent migrants). Social network analyses indicated lake sturgeon generally co-occurred with individuals of the same migratory phenotype more often than with different migratory phenotypes. A direct test for differences in space use revealed one site was almost exclusively visited by Lake St. Clair migrants whereas the other site was visited by Lake Huron migrants, intermittent Lake St. Clair migrants, and, to a lesser extent, annual Lake St. Clair migrants. Analysis of arrival and departure dates indicated opportunity for co-occurrence at the site visited by all phenotypes but showed Lake Huron migrants arrived approximately 2 weeks before Lake St. Clair migrants. Taken together, our results indicated partial spatiotemporal segregation of migratory phenotypes that may generate assortative mating and promote population differentiation.

Michigan, Ontario

Intra-specific variation in responses to habitat restoration: Could artificial reefs increase spatiotemporal segregation between migratory phenotypes of lake sturgeon?

Habitat restoration is an important tool used to conserve biodiversity and restore species, but its effects are notoriously difficult to predict. Although outcomes of restoration projects are usually assessed using indices of species abundance and diversity, phenotypic differences among individuals within species are likely associated with differing responses to restored habitats. Here, we use lake sturgeon ( Acipenser fulvescens ) as a case study to illustrate how responses to habitat restoration can differ between phenotypes and potentially lead to unanticipated effects on populations. North America’s St. Clair River supports one of the largest remaining populations of lake sturgeon but has lost much spawning habitat due to its role as a major industrial corridor between the Laurentian Great Lakes Erie and Huron. Two artificial reefs were recently built in the lower and middle segments of the river to increase the available sturgeon spawning habitat. Interestingly, lake sturgeon in the St. Clair River express different migratory phenotypes that may be associated with different likelihoods of colonizing artificial reefs. Acoustic telemetry revealed that artificial reefs were more likely to be used by sturgeon that migrated downstream to overwinter in Lake St. Clair than those that migrated upstream to overwinter in Lake Huron. Furthermore, increasing time spent at the artificial reefs by Lake St. Clair migrants was associated with later arrival to and shorter occupancy of the river’s only natural spawning site, the primary location where the two phenotypes have opportunity to interbreed. Additional research is necessary to determine the ultimate impacts of the artificial reefs on lake sturgeon populations; nevertheless, our study showed phenotype-specific opportunity to colonize restored habitat and a mechanism through which this could lead to changes in gene flow. Our results illustrate the importance of considering intra-specific diversity when planning restoration projects and assessing the effects on populations.

Michigan, Ontario

Local diversity in phenological responses of migratory lake sturgeon to warm winters

Rich intraspecific diversity in traits that shape responses to environmental conditions implies that effects of climate change will differ within species or even populations. Nevertheless, few studies investigate how different groups within species respond to climatic fluctuations, and most risk assessments rely upon species-wide generalizations. We studied effects of among-year variation in air temperature on the spring migratory phenology of a metapopulation of lake sturgeon Acipenser fulvescens within waters connecting Lake Huron and Lake Erie of the Laurentian Great Lakes. Sturgeon here express multiple migratory phenotypes that all spawn in either the St. Clair River or Detroit River but differ in their use after spawning of more than 86 000 km 2 of accessible lake and river habitat. Acoustic tracking over nine years (2012–2020) revealed mixed phenological responses to late-winter air temperatures, with three migratory groups arriving at rivers earlier during warm years and one whose arrival was consistent across years regardless of temperature. Notably, two groups that spawn in the same river but overwinter in different lakes entered the river with greater synchrony during warm years because one advanced its phenology while the other did not. The results indicated warm weather could alter the dynamics of the metapopulation and broader community, and exemplify the complexity hidden beneath broadscale generalizations of species' response to climate change.

Michigan, Ontario

Phylogenetic distribution of a male pheromone that may exploit a nonsexual preference in lampreys

Pheromones are among the most important sexual signals used by organisms throughout the animal kingdom. However, few are identified in vertebrates, leaving the evolutionary mechanisms underlying vertebrate pheromones poorly understood. Pre-existing biases in receivers’ perceptual systems shape visual and auditory signaling systems, but studies on how receiver biases influence the evolution of pheromone communication remain sparse. The lamprey Petromyzon marinus uses a relatively well-understood suite of pheromones and offers a unique opportunity to study the evolution of vertebrate pheromone communication. Previous studies indicate that male signaling with the mating pheromone 3-keto petromyzonol sulfate (3kPZS) may exploit a nonsexual attraction to juvenile-released 3kPZS that guides migration into productive rearing habitat. Here, we infer the distribution of male signaling with 3kPZS using a phylogenetic comparison comprising six of ten genera and two of three families. Our results indicate that only P. marinus and Ichthyomyzon castaneus release 3kPZS at high rates. Olfactory and behavioral assays with P. marinus, I. castaneus and a subset of three other species that do not use 3kPZS as a sexual signal indicate that male signaling might drive the evolution of female adaptations to detect 3kPZS with specific olfactory mechanisms and respond to 3kPZS with targeted attraction relevant during mate search. We postulate that 3kPZS communication evolved independently in I. castaneus and P. marinus , but cannot eliminate the alternative that other species lost 3kPZS communication. Regardless, our results represent a rare macroevolutionary investigation of a vertebrate pheromone and insight into the evolutionary mechanisms underlying pheromone communication.

Journal of Evolutionary Biology

Temporal constraints on the potential role of fry odors as cues of past reproductive success for spawning lake trout

Deciding where to reproduce is a major challenge for most animals. Many select habitats based upon cues of successful reproduction by conspecifics, such as the presence of offspring from past reproductive events. For example, some fishes select spawning habitat following odors released by juveniles whose rearing habitat overlaps with spawning habitat. However, juveniles may emigrate before adults begin to search for spawning habitat; hence, the efficacy of juvenile cues could be constrained by degradation or dissipation rates. In lake trout ( Salvelinus namaycush ), odors deposited by the previous year's offspring have been hypothesized to guide adults to spawning reefs. However, in most extant populations, lake trout fry emigrate from spawning reefs during the spring and adults spawn during the fall. Therefore, we postulated that the role of fry odors in guiding habitat selection might be constrained by the time between fry emigration and adult spawning. Time course chemical, physiological, and behavioral assays indicated that the odors deposited by fry likely degrade or dissipate before adults select spawning habitats. Furthermore, fry feces did not attract wild lake trout to constructed spawning reefs in Lake Huron. Taken together, our results indicate fry odors are unlikely to act as cues for lake trout searching for spawning reefs in populations whose juveniles emigrate before the spawning season, and underscore the importance of environmental constraints on social cues.

Ecology and Evolution

Increased pheromone signaling by small male sea lamprey has distinct effects on female mate search and courtship

Male body size affects access to mates in many animals. Attributes of sexual signals often correlate with body size due to physiological constraints on signal production. Larger males generally produce larger signals, but costs of being large or compensation by small males can result in smaller males producing signals of equal or greater magnitude. Female choice following multiple male traits with different relationships to size might further complicate the effect of male body size on access to mates. We report the relationship between male body size and pheromone signaling, and the effects on female mate search and courtship in the sea lamprey ( Petromyzon marinus ). We predicted that pheromone production in the liver and the liver mass to body mass ratio would remain constant across sizes, resulting in similar mass-adjusted pheromone release rates across sizes but a positive relationship between absolute pheromone release and body mass. Our results confirmed positive relationships between body mass and liver mass, and liver mass and the magnitude of the pheromone signal. Surprisingly, decreasing body mass was correlated with higher pheromone concentrations in the liver, liver mass to body mass ratios, and mass-adjusted pheromone release rates. In a natural stream, females more often entered nests treated with small versus large male odors. However, close-proximity courtship behaviors were similar in nests treated with small or large male odors. We conclude that small males exhibit increased release of the main pheromone component, but female discrimination of male pheromones follows several axes of variation with different relationships to size.

Behavioral Ecology and Sociobiology

Evidence for partial overlap of male olfactory cues in lampreys

Animals rely on a mosaic of complex information to find and evaluate mates. Pheromones, often comprised of multiple components, are considered to be particularly important for species-recognition in many species. While the evolution of species-specific pheromone blends is well-described in many insects, very few vertebrate pheromones have been studied in a macro-evolutionary context. Here, we report a phylogenetic comparison of multi-component male odours that guide reproduction in lampreys. Chemical profiling of sexually mature males from eleven species of lamprey, representing six of ten genera and two of three families, indicated the chemical profiles of sexually mature male odours are partially shared among species. Behavioural assays conducted with four species sympatric in the Laurentian Great Lakes indicated asymmetric female responses to heterospecific odours, where Petromyzon marinus were attracted to male odour collected from all species tested but other species generally preferred only the odour of conspecifics. Electro-olfactogram recordings from P. marinus indicated that although P. marinus exhibited behavioural responses to odours from males of all species, at least some of the compounds that elicited olfactory responses were different in conspecific male odours compared to heterospecific male odours. We conclude that some of the compounds released by sexually mature males are shared among species and elicit olfactory and behavioural responses in P. marinus , and suggest that our results provide evidence for partial overlap of male olfactory cues among lampreys. Further characterization of the chemical identities of odour components is needed to confirm shared pheromones among species.

Journal of Experimental Biology

Five-year evaluation of habitat remediation in Thunder Bay, Lake Huron: Comparison of constructed reef characteristics that attract spawning lake trout

Degradation of aquatic habitats has motivated construction and research on the use of artificial reefs to enhance production of fish populations. However, reefs are often poorly planned, reef design characteristics are not evaluated, and reef assessments are short-term. We constructed 29 reefs in Thunder Bay, Lake Huron, in 2010 and 2011 to mitigate for degradation of a putative lake trout spawning reef. Reefs were designed to evaluate lake trout preferences for height, orientation, and size, and were compared with two degraded natural reefs and a high-quality natural reef (East Reef). Eggs and fry were sampled on each reef for five years post-construction, and movements of 40 tagged lake trout were tracked during three spawning seasons using acoustic telemetry. Numbers of adults and spawning on the constructed reefs were initially low, but increased significantly over the five years, while remaining consistent on East Reef. Adult density, egg deposition, and fry catch were not related to reef height or orientation of the constructed reefs, but were related to reef size and adjacency to East Reef. Adult lake trout visited and spawned on all except the smallest constructed reefs. Of the metrics used to evaluate the reefs, acoustic telemetry produced the most valuable and consistent data, including fine-scale examination of lake trout movements relative to individual reefs. Telemetry data, supplemented with diver observations, identified several previously unknown natural spawning sites, including the high-use portions of East Reef. Reef construction has increased the capacity for fry production in Thunder Bay without apparently decreasing the use of the natural reef. Results of this project emphasize the importance of multi-year reef assessment, use of multiple assessment methods, and comparison of reef characteristics when developing artificial reef projects. Specific guidelines for construction of reefs focused on enhancing lake trout spawning are suggested.

Lake Huron, Thunder Bay

Female sea lamprey shift orientation toward a conspecific chemical cue to escape a sensory trap

The sensory trap model of signal evolution hypothesizes that signalers adapt to exploit a cue used by the receiver in another context. Although exploitation of receiver biases can result in conflict between the sexes, deceptive signaling systems that are mutually beneficial drive the evolution of stable communication systems. However, female responses in the nonsexual and sexual contexts may become uncoupled if costs are associated with exhibiting a similar response to a trait in both contexts. Male sea lamprey ( Petromyzon marinus ) signal with a mating pheromone, 3-keto petromyzonol sulfate (3kPZS), which may be a match to a juvenile cue used by females during migration. Upstream movement of migratory lampreys is partially guided by 3kPZS, but females only move toward 3kPZS with proximal accuracy during spawning. Here, we use in-stream behavioral assays paired with gonad histology to document the transition of female preference for juvenile- and male-released 3kPZS that coincides with the functional shift of 3kPZS as a migratory cue to a mating pheromone. Females became increasingly biased toward the source of synthesized 3kPZS as their maturation progressed into the reproductive phase, at which point, a preference for juvenile odor (also containing 3kPZS naturally) ceased to exist. Uncoupling of female responses during migration and spawning makes the 3kPZS communication system a reliable means of synchronizing mate search. The present study offers a rare example of a transition in female responses to a chemical cue between nonsexual and sexual contexts, provides insights into the origins of stable communication signaling systems.

Behavioral Ecology

Quantification of 15 bile acids in lake charr feces by ultra-high performance liquid chromatography–tandem mass spectrometry

Many fishes are hypothesized to use bile acids (BAs) as chemical cues, yet quantification of BAs in biological samples and the required methods remain limited. Here, we present an UHPLC–MS/MS method for simultaneous, sensitive, and rapid quantification of 15 BAs, including free, taurine, and glycine conjugated BAs, and application of the method to fecal samples from lake charr ( Salvelinus namaycush ). The analytes were separated on a C 18 column with acetonitrile–water (containing 7.5 mM ammonium acetate and 0.1% formic acid) as mobile phase at a flow rate of 0.25 mL/min for 12 min. BAs were monitored with a negative electrospray triple quadrupole mass spectrometer (Xevo TQ-S™). Calibration curves of 15 BAs were linear over the concentration range of 1.00–5,000 ng/mL. Validation revealed that the method was specific, accurate, and precise. The method was applied to quantitative analysis of feces extract of fry lake charr and the food they were eating. The concentrations of analytes CA, TCDCA, TCA, and CDCA were 242.3, 81.2, 60.7, and 36.2 ng/mg, respectively. However, other taurine conjugated BAs, TUDCA, TDCA, and THDCA, were not detected in feces of lake charr. Interestingly, TCA and TCDCA were detected at high concentrations in food pellets, at 71.9 and 38.2 ng/mg, respectively. Application of the method to feces samples from lake charr supported a role of BAs as chemical cues, and will enhance further investigation of BAs as chemical cues in other fish species.

Journal of Chromatography B: Analytical Technologi

Behavioral evidence for a role of chemoreception during reproduction in lake trout

Chemoreception is hypothesized to influence spawning site selection, mate search, and synchronization of gamete release in chars ( Salvelinus spp.), but behavioral evidence is generally lacking. Here, we provide a survey of the behavioral responses of reproductive male and female lake trout ( Salvelinus namaycush ) to natural conspecific chemosensory stimuli. A flow-through laboratory assay with side-by-side artificial spawning reefs was used to evaluate behavioral preferences of spawning-phase males and females for chemosensory stimuli from juveniles and from spawning-phase males and females. Males and females preferred male and juvenile stimuli over no stimuli, but only had weak preferences for female stimuli. Only females had a preference for male over juvenile stimuli when given a direct choice between the two. The unexpected observation of male attraction to male stimuli, even when offered female stimuli, indicates a fundamental difference from the existing models of chemical communication in fishes. We discuss our results from the perspectives of prespawning aggregation, mate evaluation, and spawning synchronization. Identification of specific components of the stimuli will allow confirmation of the function and may have management implications for native and invasive populations of lake trout that are ecologically and economically important.

Canadian Journal of Fisheries and Aquatic Sciences

Reproductive ecology of lampreys

Lampreys typically spawn in riffle habitats during the spring. Spawning activity and diel (i.e., during daylight and at night) behavioral patterns are initiated when spring water temperatures increase to levels that coincide with optimal embryologic development. Nests are constructed in gravel substrate using the oral disc to move stones and the tail to fan sediment out of the nest. Spawning habitat used by individual species is generally a function of adult size, where small-bodied species construct nests in shallower water with slower flow and smaller gravel than large-bodied species. The mating system of lampreys is primarily polygynandrous (i.e., where multiple males mate with multiple females). Lamprey species with adult total length less than 30 cm generally spawn communally, where a nest may contain 20 or more individuals of both sexes. Lamprey species with adult sizes greater than 35 cm generally spawn in groups of two to four. Operational sex ratios of lampreys are highly variable across species, populations, and time, but are generally male biased. The act of spawning typically starts with the male attaching with his oral disc to the back of the female’s head; the male and female then entwine and simultaneously release gametes. However, alternative mating behaviors (e.g., release of gametes without paired courtship and sneaker males) have been observed. Future research should determine how multiple modalities of communication among lampreys (including mating pheromones) are integrated to inform species recognition and mate choice. Such research could inform both sea lamprey control strategies and provide insight into possible evolution of reproductive isolation mechanisms between paired lamprey species in sympatry.

Book chapter

Bile salts as semiochemicals in fish

Bile salts are potent olfactory stimuli in fishes; however the biological functions driving such sensitivity remain poorly understood. We provide an integrative review of bile salts as semiochemicals in fish. First, we present characteristics of bile salt structure, metabolism, and function that are particularly relevant to chemical communication. Bile salts display a systematic pattern of structural variation across taxa, are efficiently synthesized, and are stable in the environment. Bile salts are released into the water via the intestine, urinary tract, or gills, and are highly water soluble. Second, we consider the potential role of bile salts as semiochemicals in the contexts of detecting nearby fish, foraging, assessing risk, migrating, and spawning. Lastly, we suggest future studies on bile salts as semiochemicals further characterize release into the environment, behavioral responses by receivers, and directly test the biological contexts underlying olfactory sensitivity.

Chemical Senses

Evidence for a receiver bias underlying female preference for a male mating pheromone in sea lamprey

Receiver bias models suggest that a male sexual signal became exaggerated to match a pre-existing sensory, perceptual or cognitive disposition of the female. Accordingly, these models predict that females of related taxa possessing the ancestral state of signalling evolved preference for the male trait in a non-sexual context. We postulated that female preference for the male-released bile alcohol mating pheromone, 3 keto petromyzonol sulfate (3kPZS), of the sea lamprey (Petromyzon marinus) evolved as a result of a receiver bias. In particular, we propose that migratory silver lamprey (Ichthyomyzon unicuspis), a basal member of the Petromyzontidae, evolved a preference for 3kPZS released by stream-resident larvae as a means of identifying productive habitat for offspring. Larval silver lamprey released 3kPZS at rates sufficient to be detected by migratory lampreys. Females responded to 3kPZS by exhibiting upstream movement behaviours relevant in a migratory context, but did not exhibit proximate behaviours important to mate search and spawning. Male silver lamprey did not release 3kPZS at rates sufficient to be detected by females in natural high-volume stream environments. We infer that female silver lamprey cue onto 3kPZS excreted by stream-resident larvae as a mechanism to locate habitat conducive to offspring survival and that males do not signal with 3kPZS. We suggest that this female preference for a male signal in a non-sexual context represents a bias leading to the sexual signalling observed in sea lamprey.

Michigan