Pheromone pollution from invasive sea lamprey misguides a native confamilial

Animals interact with mates in a sensory environment rife with the footprints of human activities. Frogs chorus over the noise of traffic (Bee and Swanson 2007), glow-worms search for bioluminescent mates against backlight from street lamps (Bird and Parker 2014), and fish attend to conspecific olfactory cues mixed with sewage (Fisher et al. 2006). As invasive species proliferate throughout the world, animals also encounter noise in the form of novel heterospecific signals that can interfere with existing communication channels (Gröning and Hochkirch 2008). Pheromones, for example, are often species-specific in natural contexts involving sympatric heterospecifics but may become detrimental pollution when animals invade regions inhabited by historically allopatric relatives that previously faced less selection for signal divergence (Gozlan et al. 2014). Sea lamprey Petromyzon marinus are a destructive invader of the Laurentian Great Lakes whose pheromones may disrupt communication in native species. The Laurentian Great Lakes host four native species of lamprey who spawn at overlapping times and places as P. marinus, with peak spawning for three native lampreys and P. marinus occurring simultaneously (early June; Johnson et al. 2015). During spawning, male lampreys signal to females using sex pheromones that partially overlap among species (Buchinger et al. 2017b). In P. marinus, the sex pheromone consists of 3-keto petromyzonol sulfate (3kPZS) along with multiple known and unknown minor components (reviewed by Johnson et al. 2015). One native species, the chestnut lamprey Ichthyomyzon castaneus, also communicates with 3kPZS as a major component of its sex pheromone (Buchinger et al. 2017a). Whether shared communication with 3kPZS results in confused mating behaviors in I. castaneus remains unclear as the multiple components of lamprey pheromones likely evolved through distinct mechanisms and minor components may enable species specificity (Buchinger et al. 2017b). In this study, we tested the hypothesis that P. marinus sex pheromones disrupt communication in native I. castaneus. Specifically, we 1) tested attraction of female I. castaneus to male odorants from conspecifics presented alongside male odorants from P. marinus and 2) quantified male release of 3kPZS for each species to evaluate the possible mechanism of any observed preference. Detailed methods are described in the Supplementary Material.

In a natural spawning stream, 100% of responsive female I. castaneus entered nests treated with male odorants from P. marinus over conspecifics (logistic regression χ²₁ = 13.46, P < 0.001; N = 10; Figure 1A). Other fish died (N = 10), remained in the cage (N = 7), moved downstream (N = 1), moved upstream without entering a nest (N = 4), or remained near the cage (N = 5). Notably, lampreys die after a single spawning season that lasts approximately 1.5 weeks (Johnson et al. 2015) and therefore subjects in this experiment often expired or became lethargic while acclimating in the stream for 8 h prior to a trial. Fish were not biased between nests; 6 entered the left nest over the 3 trials in which P. marinus odorant was applied on the left and 4 entered the right nest over the 2 trials in which P. marinus odorant was applied on the right. Females spent more time near odorants from P. marinus than conspecifics, though only 4 ever entered the nest treated with conspecific male odorants (Wilcoxon signed-rank test P = 0.002; Figure 1B). Pheromone quantification indicated male P. marinus (N = 28; 450.6 ± 11.3 mm, 191.1 ± 10.2 g; mean ± SE) released more 3kPZS than male I. castaneus (N = 29; 241.2 ± 1.9 mm, 28.0 ± 0.8 g), whether standardized by individual (Wilcoxon rank-sum test P < 0.001; Figure 1C) or by weight (P. marinus = 263.83 ± 25.99 ng 3kPZS g fish⁻¹ h⁻¹; I. castaneus = 170.05 ± 61.05 ng 3kPZS g/fish/h; Wilcoxon rank-sum test P < 0.001).

Figure 1.

Female chestnut lamprey Ichthyomyzon castaneus orient toward sex pheromones of sea lamprey Petromyzon marinus over conspecifics. (A) All responsive females (N = 10) first entered the nest with odorant from P. marinus over conspecifics (logistic regression P < 0.001). (B) Females spent more time in the nest with odorant from P. marinus over conspecifics (mean ± se; Wilcoxon rank-sum test P = 0.002). Data are presented for all responsive fish (N = 10), but females that eventually entered the conspecific nest (N = 4) also spent more time on the P. marinus nest (357 ± 126.63 s, mean ± se) compared to the conspecific nest (40.5 ± 22.3 s). (C) Male P. marinus release more of the sex pheromone 3-keto petromyzonol sulfate (3kPZS) than male I. castaneus (N = 28, 29; Wilcoxon rank-sum test P < 0.001).

Our results indicate invasive P. marinus introduce “pheromone pollution” (Gozlan et al. 2014) that disorients native I. castaneus. Despite our relatively small sample size, the large observed effect size supports a strong heterospecific response to odorants from P. marinus. Analysis of pheromone release supported previous reports that both species signal with 3kPZS (Buchinger et al. 2017a) but revealed higher release rates by P. marinus. Whether the more concentrated 3kPZS plumes produced by P. marinus elicit heterospecific mating preferences in I. castaneus or prevent female I. castaneus from correctly perceiving conspecifics (i.e., signal jamming; Gröning and Hochkirch 2008) remains unclear. Likewise, our results do not eliminate the possibility that additional pheromone components contribute to the observed cross-reaction. Regardless, our experiment, conducted in a natural spawning stream with the odorants from the two species presented side-by-side, closely approximates the natural context in which these species interact (Johnson et al. 2015) and therefore offers strong support for pheromone interference by invasive P. marinus.

We suggest that pheromone pollution from invasive P. marinus poses an ecologically relevant threat to native lamprey populations. Tactile, electrical, and other nonolfactory cues may guide species-specific mating despite cross attraction to sex pheromones (Johnson et al. 2015); indeed the low proportion of females to move up to a nest, which we attribute primarily to females becoming nonresponsive as they senesce, may be due to the lack of other sensory cues from males. However, anosmic P. marinus fail to find mates (Johnson et al. 2006), indicating olfactory cues are critical to mate search. Therefore, attraction of I. castaneus to P. marinus is likely to at least waste energy and time, which are both limited as lampreys cease feeding months before spawning and die after a short spawning season (Johnson et al. 2015). Waste of gametes may be less consequential because lamprey usually intertwine to align the male’s papilla with the female’s urogenital region and the body size difference between P. marinus and I. castaneus creates a physical mismatch likely to prevent frequent copulation (Johnson et al. 2015). Nevertheless, alternative male tactics and spawning without physical intertwining may allow for cross-fertilization despite differences in body size (Johnson et al. 2015). Interference by P. marinus may also increase mortality by making smaller lamprey species more conspicuous to predators (Johnson et al. 2015). Importantly, current tactics to control invasive P. marinus—namely a piscicide that kills all lampreys (King and Gabel 1985)—almost certainly cause greater harm to native lamprey than cross-reaction to sex pheromones. However, ongoing efforts to refine the current control strategy should consider the potential for detrimental reproductive interference. Indeed, frequent observations of P. marinus on spawning nests with native lampreys indicate cross-reaction to pheromones already results in heterospecific interactions (Johnson et al. 2015). As sex pheromones elicit a suite of behavioral and physiological responses in P. marinus (Johnson et al. 2015), pheromone interference by P. marinus conceivably acts through various mechanisms which could compound to have a significant impact on native lamprey populations.

Supplementary material

Supplementary material can be found at https://academic.oup.com/cz.