The effects of traffic noise on tadpole behavior and development

We have known for decades that chronic exposure to traffic noise has negative effects on human health and quality of life (Broner 1978), ranging from annoyance (Ouis 2001), to disrupted sleeping patterns (Öhrström et al. 2006), to increased risk for heart disease (Babisch 2000). Roads and their associated traffic are one of the most pervasive and obvious signatures of humans on the landscape; Riitters and Wickham (2003) estimated that less than 3% of the contiguous United States is located more than 5 km from a paved road, and that percentage has almost certainly shrunk since then. In fact, there are plans for a 60% increase in paved miles worldwide by 2050 (Laurance et al. 2014). It is therefore not surprising that ecologists have also been curious about how traffic noise affects wildlife.

As one might expect, traffic noise has been found to produce mainly negative outcomes for wildlife (reviewed in Francis and Barber 2013; Laurance 2015). In a study of woodland birds, traffic noise was the best predictor of the reduced abundance observed near roads (Reijnen et al. 1995), an effect that was reproduced empirically when traffic noise was broadcast in a roadless area (McClure et al. 2013). For individuals and species that do remain in noisy roadside areas, there can be detrimental effects. Traffic noise elevates stress levels in wood frogs (Rana sylvatica; Tennessen et al. 2014) and northern spotted owls (Strix occidentalis caurina; Hayward et al. 2011), and chronically elevated stress levels have been shown across taxa to negatively impact immune function (Martin et al. 2005), growth (Belden et al. 2005), reproduction (Ouyang et al. 2011), and survival (Pride 2005). Chronic environmental noise is associated with decreases in the quality of avian parental care (Leonard and Horn 2012; Schroeder et al. 2012). White-crowned sparrows (Zonotrichia leucophrys) exposed to traffic noise spent less time foraging and more time exhibiting vigilance behaviors, presumably because the noise interferes with their ability to detect predators (Ware et al. 2015). Species that use vocalisations as their primary form of communication (e.g. birds, frogs, many orthopterans) may find their signals masked by traffic noise, necessitating adjustments in amplitude, frequency, and/or timing (birds: Gil and Brumm 2014; frogs: Sun and Narins 2005, Bee and Swanson 2007, Cunnington and Fahrig 2010, Grace and Noss 2018; monkeys: Brumm et al. 2004). Interference with vocal communication can reduce mating success (frogs: Cunnington and Fahrig 2013; Tennessen et al. 2014). Interestingly, some species appear able to adapt physiologically to chronic noise, with individuals from noisy areas showing reduced stress responses relative to individuals from quiet areas (Tennessen et al. 2018). In comparison, it appears to be more difficult to adapt to the disruption in communication caused by traffic noise, with disorientation of signal receivers persisting even in individuals from noisy areas (Senzaki et al. 2018).

While most work has focused on terrestrial animals, aquatic species are not necessarily immune to the negative effects of traffic noise. Roads often pass by or over bodies of water, and the sound can be transmitted to the aquatic environment. Holt and Johnston (2015) found that low-frequency noise from truck traffic on a bridge, which potentially masks the low-frequency signals of the Blacktail Shiner (Cyprinella venusta), propagated throughout a shallow stream further than signals of the fish, essentially creating ‘dead zones’ for fish communication. While Holt and Johnston’s study is the first to show that traffic noise can infiltrate the aquatic environment, other anthropogenic sources of aquatic noise pollution have long been identified, and the effects on aquatic fauna are similar to what has been observed in terrestrial species (Slabbekoorn et al. 2010). Noise from passing ships induces a stress response in various fish species (Wysocki et al. 2006; Purser et al. 2016) and shore crabs (Carcinus maenas, Wale et al. 2013a). It is also known to interfere with schooling behavior in bluefin tuna (Thunnus thynnus, Sarà et al. 2007) and foraging behavior in shore crabs (Wale et al. 2013b). Aquarium noise from filters and pumps increases stress and decreases body condition of lined seahorses (Hippocampus erectus; Anderson et al. 2011).

Here, we focus on the effects of traffic noise on activity level, feeding behavior, and growth of tadpoles. Though previous studies have examined how traffic noise affects adult anurans, i.e. frogs and toads (Sun and Narins 2005; Bee and Swanson 2007; Cunnington and Fahrig 2010, 2013; Tennessen et al. 2014; Grace and Noss 2018), there have been no studies on tadpoles. The effect of traffic noise on tadpoles is relevant because some anuran species lay their eggs in roadside ditches, presumably because these ephemeral water bodies are generally free from fish predators (Mobberly and Pfrimmer 1967; Bridges and Semlitsch 2001). If traffic noise negatively affects tadpole development, however, then roadside ditches could actually be functioning as an ecological trap (Gates and Gysel 1978; Schlaepfer et al. 2002). In addition to noise, anurans have been identified as one of the taxa most vulnerable to direct mortality on roads (reviewed in Andrews et al. 2008; Fahrig and Rytwinski 2009), so gaining a more complete picture of anuran road ecology will help conservation efforts. Given the vulnerability and extinction of many amphibian species worldwide (Houlahan et al. 2000; Stuart et al. 2004), it is critical to understand which factors could contribute to their decline.

We hypothesised that, similar to what was observed in Ware et al.’s (2015) study, traffic noise would cause tadpoles to become more vigilant, altering feeding and behavior and in turn affecting growth. A similar reduction in foraging in response to noise has been observed in Mediterranean damselfish (Chromis chromis; Bracciali et al. 2012). In the presence of a predator, tadpoles from the majority of anuran species tested reduce their activity level (Lawler 1989; Richardson 2001), so we expected to observe a similar reaction to traffic noise. We predicted that if traffic noise has a negative effect on tadpole fitness, then:

Although we observed that exposure to traffic noise increased tadpole activity level and decreased the amount of food consumed during an experimental trial, we did not observe any corresponding effects on timing or size at metamorphosis. This aligns with studies in cultured fish; a study of how rainbow trout (Oncorhynchus mykiss) respond to aquarium noise found no significant effects on growth rate or mortality (Wysocki et al. 2007), and a study of the effects of white noise on goldfish (Carassius auratus) found that the noise produced temporary, but not permanent, spikes in plasma cortisol (Smith et al. 2004). A possible explanation for our findings is that the brief exposure to noise in the activity and feeding experiments produced an acute spike in stress that affects behavior, but that tadpoles are able to acclimate and resume normal patterns of behavior when facing chronic exposure to noise (as their physiological responses adapt, e.g. Tennessen et al. 2018). This could be a positive finding in terms of anuran conservation, but several caveats must be addressed.

Most anuran species decrease their activity level in the presence of a predator or predator cues (Lawler 1989; Richardson 2001), but some species (across the anuran families Bufonidae, Ranidae, and Hylidae) show increased activity, so our finding that both Cuban Treefrogs and Southern Toads increased their time spent active in response to traffic noise is not unprecedented. However, though we hypothesised that traffic noise would induce similar responses in the tadpoles as a predator would, our experiment did not include any actual predators. Previous work has shown that tadpoles with higher activity levels were less likely to survive in the presence of a predator (Lawler 1989), so it is possible that increased activity in response to traffic noise could make tadpoles more vulnerable to predation. Chan et al. (2010) found that Caribbean hermit crabs (Coenobita clypeatus) allowed a simulated predator to approach closer under conditions of anthropogenic noise. However, our experiment did not test for this.

Another caveat that limits extrapolation from our results is that, due to the difficulty in obtaining tadpoles, we only tested one clutch of tadpoles for each species. While a clutch of Cuban Treefrog tadpoles provides more than enough individuals to achieve statistical power in multiple experiments, an experiment where all individuals come from the same clutch is pseudoreplicated. That is, it is possible that the behavioral responses were a quirk of this particular clutch and not a general pattern for the species as a whole. The fact that similar results were found when we tested the activity level of Southern Toad tadpoles helps alleviate this concern, but it is a definite limitation to this set of experiments.

In summary, we did not find that traffic noise had a negative impact on tadpole fitness at metamorphosis, as measured by size at and timing of metamorphosis. Therefore, our findings provide no evidence that traffic noise makes the use of roadside ditches as egg deposition sites by anurans an ecological trap in terms of tadpole growth; however, it is important to note that these results were obtained by testing a very successful invader, the Cuban Treefrog. We did find that tadpoles of both species, the native Southern Toad and the invasive Cuban Treefrog, increased activity levels in response to noise. Going forward, it will be crucial to empirically investigate the potential interaction between traffic noise and predation, mediated by increased activity levels in response to noise, before concluding that traffic noise does not produce negative outcomes for tadpoles.