INTRODUCTION
Aerial insectivores like birds and bats are decreasing at alarming rates
across North America (Spiller & Dettmers, 2019), in part due to
simultaneous declines of aerial insects (Sánchez-Bayo & Wyckhuys,
2019). Niche theory predicts that in resource-limited environments,
species that occupy the same guild will partition dietary resources to
avoid competitive exclusion (MacArthur & Levins, 1964). Such
partitioning is often underpinned by variations in morphology or
behavior that allow species to exploit different resources (Schoener,
1974). Dietary niche partitioning related to prey size (Vesterinen et
al., 2018), predator morphology, and echolocation behavior (Emrich et
al., 2014) is evident among many sympatric bat species. If and how
dietary partitioning occurs among co-occurring nocturnal insectivorous
birds and bats is less clear, but by identifying the processes that
promote the coexistence of aerial insectivores, we can better predict
future community dynamics.
Interactions between bats and moths provide a model system for studying
the evolution of predator-prey relationships (Waters 2003; Hofstede and
Ratcliffe 2016). Prey capture by bats is often dependent on echolocation
behavior and how insects respond (Fenton and Fullard 1979). Moths with
ultrasound-sensitive ears can hear echolocation calls at distances up to
100 meters (e.g., noctuids; Miller and Surlykke 2001) and avoid
predation through evasive maneuvers or sounds (Dunning and Kruger,
1996). This adaptation arose independently in moths at least six times
(Hofstede & Ratcliffe, 2016). In turn, some bats echolocate at low
intensities or high enough frequencies to go undetected by moths (Faure,
Fullard, and Barclay 1990; Hofstede and Ratcliffe 2016). Yet, how
evolutionary interactions between moths and bats may extend to dietary
resource partitioning between bats and nocturnal insectivorous birds is
unknown (Yack et al., 2020). Nocturnal birds often use visual cues and
possess adaptions for silent flight that enable them to evade detection
by insects (Clark et al., 2020). These adaptations may allow them to
exploit resources that bats cannot. For example, eared moths can only
detect the cyclic wingbeats of approaching birds within 2.5 meters
(Hofstede and Ratcliffe 2016; Waters 2003), perhaps making moths more
vulnerable to predation by visually-oriented insectivores. The
distributions of bats and nocturnal insectivorous birds suggests that
they interact. However, little research exists on if, or to what extent
they may partition prey resources, or the underlying mechanisms (Fenton
and Fleming 1976).
We used fecal DNA barcoding to analyze the diets of seven co-occurring
nocturnal aerial insectivores (hereafter NAIs). We compared the diet
composition and richness of three nocturnal birds: Chordeiles
minor (Common Nighthawks), Phalaenoptilus nuttallii (Common
Poorwills), Psiloscops flammeolus (Flammulated Owls), and four
bat species: Eptesicus fuscus (Big Brown Bats),Lasionycteris noctivagans (Silver-haired Bats), Myotis
Volans (Long-legged Myotis), and Myotis evotis (Western
Long-eared Myotis). Despite differences in prey detection methods used
by these insectivores (Table 1), previous studies using microscopy of
fecal samples have reported broad similarities in the insects they
consume, primarily moths and beetles (Agosta, 2002; Csada et al., 1992;
Ober & Hayes, 2008; Reynolds & Linkhart, 1987; Todd et al., 1998;
Whitaker, 1995). However, NAI diets vary across regions and over time,
hampering cross-study comparisons. Additionally, traditional methods of
prey analysis in feces primarily result in prey identification to only
the order or family level, which masks resource partitioning at finer
taxonomic resolutions.
As with differences in prey detection methods, NAIs in this study also
display different foraging behaviors. For example, Flammulated Owls
(Goggans 1985) and Common Poorwills (Brigham and Barclay 1992) are
sit-and-wait predators (Table 1). Both use their legs to launch after
prey from the ground or perches, a foraging behavior not found in
insectivorous bats. Modifications of the pelvis that allow bats to hang
from perches and fly prevent bats from jumping into flight (Schutt et
al., 1997). Instead, the bats in this study hunt by foraging insects
while in flight, termed “aerial hawking” (Saunders & Barclay, 1992),
or, as in Long-eared Myotis, sometimes by gleaning insects from the
ground and foliage (Faure and Barclay 1994). Like bats, Common
Nighthawks are also aerial hawkers and prey on insects at a wide range
of heights above ground and over great distances in a single foraging
bout (Clark et al., 2020).
It is not always clear if or to what extent differences in prey
detection and foraging behavior translate to differences in diet.
Insectivores with different foraging behaviors may still target the same
prey (e.g., Brigham and Fenton 1991; Kent and Sherry 2020). Prey
movement may also overlap with the foraging range of more than one type
of predator. Still, foraging behaviors and prey detection methods that
do correspond to dietary differences may decrease interspecific
competition among NAIs.
To our knowledge, this is the first study to use fecal DNA barcoding to
investigate the diets of multiple, distantly related, co-occurring NAIs.
Our objectives were two-fold. First, we developed a reference barcode
database from 56,191 locally collected arthropod specimens to provide
more accurate taxonomic assignments of potential prey items than
possible in previous studies. We then used DNA barcoding of fecal
samples to match prey DNA to our insect barcodes and determine the
degree to which NAI diets differ. We expected that differences in diet
would depend on NAI species identity and correspond with 1. prey
detection methods (i.e., echolocation or visual hunting) and 2.
differences in foraging behavior (i.e., aerial hawking or sit-and-wait
predators). We found evidence of dietary partitioning among all species.
Additionally, eared moths were consumed significantly more often by
birds than by echolocating bats, suggesting that evolutionary
interactions between bats and moths may enhance resource partitioning
between bats and birds.