Are invasive fire ants kept in check by native aerial insectivores?

Abstract

Aerial predator–prey interactions may impact populations of many terrestrial species. Here, we use altitude loggers to study aerial foraging in a native insectivore, the purple martin (Progne subis), in the southern USA. Purple martins fed primarily on mating queens and males of the invasive red imported fire ant (Solenopsis invicta), and doubled their foraging efficiency by doing so. Across the USA, purple martins likely eat billions of fire ant queens each year, potentially impacting the spread of this species. Alternatively, predation on fire ants may help sustain populations of purple martins and other aerial insectivores.

1. Introduction

Most terrestrial animal species fly to forage, mate, evade predators, disperse or migrate [1]. Because most land animals fly, and all flying animals land, terrestrial and aerial food webs are linked by the movement of individuals between them. Dispersing insects, for example, occur at high densities hundreds of metres above the ground and may form the bases of aerial food webs [2].

Ants, as some of the most abundant animals in terrestrial environments [3], are also probably prominent players in the air. Although worker ants are wingless, most ant species rely on flight for reproduction [3]. Mature colonies produce winged queens and males that fly to mate and disperse, often aggregating in swarms. Ant sexuals are relatively defenceless and more nutritious than many other insects. Queens, in particular, which found new colonies after mating, contain abdominal reserves of fats, proteins and glycogen that constitute up to 70% of their body weight [4–5]. As dense aggregations of nutritious prey, ant mating flights thus present attractive targets for predators [6].

Within the USA, the invasive red imported fire ant (Solenopsis invicta) is a conspicuous potential prey. Native to South America, S. invicta was accidentally introduced to the USA in the 1930s and to other countries since, including Australia, China and several areas in Central America and Southeast Asia [7]. In its non-native ranges, S. invicta lives at high densities in anthropogenic or disturbed habitats. One hectare of pasture can produce approximately 40 000 queens per mating flight and 250 000 per year, and the resulting swarms of millions of individuals can cover thousands of square kilometres [7–8]. Fire ants have an extended breeding season in which flights occur repeatedly throughout the spring and summer, and in warm environments can happen year-round [9]. Fire ants are, perhaps, one of the most abundant, nutritious and reliable food sources available to an aerial predator. Yet, no native predators are known to feed heavily on them, and release from predation probably contributes to their invasion success [7].

We examined the value of fire ants as prey for aerial predators by tracking the foraging altitudes and prey capture of nesting purple martins (Progne subis). Purple martins are the highest-foraging songbirds in North America. They routinely forage over 150 m above the ground [10] and show up on radar up to 4000 m [11]. They are abundant and widespread, and capture a variety of insect prey during flight [12,13]. They sometimes eat ants [12] and have been seen flying near S. invicta mating swarms [6], but predation on fire ants has not been demonstrated.

2. Material and methods

We studied purple martins breeding in nest-boxes at the University of Oklahoma Biological Station on Lake Texoma, Marshall County, OK, US (33°52′50″ N, 96°48′02″ W, elevation 196 m), from 27 May to 15 June 2014. This was within the mating seasons of many regional ant species [14], including fire ants [7].

To measure foraging altitudes, we attached altitude loggers to 25 nesting purple martins (13 females and 12 males). Each logger consisted of a battery, air temperature and barometric pressure sensors, a clock, memory and a harness made of 0.7 mm ©Stretch Magic elastic cord. The entire apparatus weighed approximately 0.5–1.0 g, approximately 1–2% of average breeding purple martin body weight [13]. The loggers recorded temperature and pressure every 20 or 30 s, and we compared these readings with those made simultaneously at a weather station 22 km away at North Texas Regional Airport, Grayson County, TX, USA (33°42′50.4″ N, 96°40′22.8″ W, elevation 228 m). Using the weather station data as a reference, we calculated flight altitudes using the barometric formula

where h = bird altitude (m), h_b = airport altitude (m), R* = the universal gas constant (8.31432 N m K⁻¹ mol⁻¹), P = logger pressure (Pa), P_b = airport pressure (Pa), g = standard gravitational acceleration (9.80665 m s⁻²) and M = the molar mass of air (0.0289644 kg mol⁻¹).

When examining profiles of altitude over time, peaks represent aerial foraging trips and troughs show when parents returned to the nest level, often to deliver prey to nestlings (figure 1). Altitude readings at the nest level fluctuated slowly about ±15 m throughout the day, probably owing to slightly different weather conditions between our study site and the weather station. To correct for fluctuations, we subtracted adjacent trough altitudes from foraging altitudes, giving accurate measurements of foraging height relative to the nest level. Trough altitudes were set at 5 m (the height of the nest-boxes) and foraging heights were adjusted accordingly.

Figure 1.

Example of a purple martin altitude profile. We calculated maximum heights and durations of foraging trips matched with prey delivered to nestlings.

While we logged flight altitudes, we also retrieved prey delivered to nestlings by logged parents. To prevent nestlings from swallowing the prey, we fitted them with neck collars [15] made from 0.7 mm ©Stretch Magic elastic cord. We then monitored the nest for 4–11 h per day between 06.30 and 18.30 h. When a parent delivered a bolus of prey, we retrieved it from the chicks' mouths and preserved it in 95% ethanol. We then loosened the collars, fed the chicks mealworms (Tenebrio molitor) and re-fastened their collars. Prey items were counted and identified to species or morphospecies. To estimate biomass, we dried 1–20 specimens of each species for 48 h at 60–65°C and weighed them to 0.001 mg. We multiplied each species' average dry mass by the number of individuals to estimate the total biomass. Species captured only once were excluded from biomass analyses.

To avoid collaring fledglings or injuring young chicks, we targeted nests with chicks approximately one to three weeks old, out of a 28-day nestling period [13]. We began nest monitoring and prey retrieval a day after attaching the loggers. Overall, we monitored 13 nests for 1–4 days each, 12 of which yielded prey samples.

To determine prey altitudes, we associated each prey with a foraging trip by matching the delivery time to a trough in the altitude profile (figure 1). The peak between this point and the most recent prior trough described the foraging trip in which the prey was captured. We then determined the trip's duration and maximum height above ground. We excluded from duration analyses three trips with unclear durations.

Analyses were performed in the program R [16]. We logged approximately 911 h of altitude data (2.2–87.7 per bird, average 43.4 ± 20.4). We collected prey from 311 foraging trips, 86 of which were matched to altitude data. Six birds did not provide nestlings and nine loggers failed during the observation periods, leaving 10 birds with combined altitude and prey data. We compared data collection and flight behaviour of male and female purple martins using t-tests for normal and the Kruskal–Wallis tests for non-normal data. We checked normality with the Shapiro–Wilk tests. The number of altitude-matched foraging trips did not vary with sex (Kruskal–Wallis: p = 0.91, n = 10, four females and six males, female median 3.5 trips, interquartile range 2.5–9.5, male 6.5 trips and interquartile range 1.5–12.0), or maximum flight heights (t-test p = 0.41, n = 10 females and 11 males, female mean 780 ± 198 m, male 912 ± 466) or foraging heights (t-test p = 0.58, n = 4 females and 6 males, female mean 78 ± 56 m, male 105 ± 93). We therefore pooled the data.

We examined the efficiency of fire ants as prey using an optimal foraging approach [17], in which more efficient prey are assumed to yield higher reward per search effort. We predicted that the higher nutrient content and abundance of fire ants compared with other insects should result in shorter purple martin foraging times. We tested this using ANCOVAs of foraging trip duration by prey type, with maximum trip height as a covariate. We limited analyses to foraging trips below the maximum height at which a fire ant of either sex was captured (less than or equal to 163 m, n = 71). We checked for changes in foraging efficiency throughout the day by including prey delivery time as a covariate. We detected no time effect (p = 0.2084) and excluded it from final analyses.

3. Results and discussion

In 311 foraging trips, the purple martins captured 3765 individuals of 79 species, including 8 ants (electronic supplementary material, table S1). Solenopsis invicta was the dominant prey species no matter how they were ranked. Fire ants were captured on 32% of foraging trips, and made up 56% of prey items and 27% of biomass fed to nestlings. The queens alone constituted 29% of foraging trips, 31% of prey items and 22% of biomass. Fire ants were delivered to 9 of 12 nests from which we collected prey, to chicks of all ages. The three nests that did not receive fire ants were monitored during 5 days of dry weather in which no mating flights occurred. Half of all birds with altitude-matched foraging trips captured fire ants, and both sexes did so at similar frequencies (males: 3/6 birds, 12/52 foraging trips (23.1%); females: 2/4 birds, 7/34 trips (20.1%)). No other species approached this prominence in the purple martin diet.

Purple martins also doubled their foraging efficiency by targeting fire ant queens. Foraging trips in which fire ant queens were captured lasted 1–8 min shorter than those targeting other prey types at similar altitudes, resulting in approximately 50% decrease in foraging time (figure 2, table 1). Considering trips in which fire ants of either sex were captured yielded similar but more variable results (table 1), suggesting that foraging efficiency increases are driven by nutrient-packed queens rather than males. Efficiency increases are apparent even after excluding exceptionally long trips (more than 2000 s, queens p = 0.002, either sex p = 0.001). Among 27 short trips (less than 500 s), which did not target fire ants, 31 species were captured, none more than six times.

Figure 2.

Foraging durations and flight altitudes. Each point represents a foraging trip which resulted in delivery of a bolus of prey. Filled circles show foraging trips in which fire ant queens were captured and open circles show those in which only other insects were captured.

Table 1.

Purple martin foraging trip durations by prey type and flight altitude. (a) ANCOVA results comparing durations of trips in which fire ants were captured with those targeting only other insects; (b) OLS regressions of duration versus altitude.

	factor	d.f.	F	p-value
(a) ANCOVA
trip duration	max height	1	22.093	<0.001
(queens)	prey type	1	6.880	0.011
	error	68
trip duration	max height	1	22.782	<0.001
(queens and males)	prey type	1	9.214	0.003
	error	68

duration versus max height	n	intercept	slope	r2
(b) OLS regressions
S. invicta queens	15	77.57	3.06	0.55
other prey	56	146.49	5.69	0.25
S. invicta queens and males	19	139.75	2.50	0.30
other prey	52	110.09	6.47	0.40

Purple martins and fire ants overlap in range across approximately 1.5 million km² of the USA (electronic supplementary material, figure S1) [18–19]. We observed purple martins delivering 1152 S. invicta queens to nestlings over 38 logger-days, an average of 30.3 queens per day per parent. If purple martins behave similarly elsewhere, then conservatively assuming one million nesting pairs in the introduced range of S. invicta [20], over a 28-day nestling period their chicks would consume 1.7 billion fire ant queens—each queen a potential new colony. Adding predation by adults, the number likely amounts to at least tens of billions per year.

It is unknown whether this intense predation impacts fire ant population densities or range expansion. It is likewise unclear if consumption of fire ant queens affects predator physiology, as their bodies contain several compounds used in chemical communication and defence [7]. Nevertheless, by doubling foraging efficiency, predation on fire ants may boost purple martin populations. Purple martins in most of the USA rely on man-made nest-boxes for which they compete with other species [13]. Over the past 50 years, purple martin populations have declined across the northern USA and Canada for unknown reasons, but are stable or increasing in southern regions colonized by S. invicta [21]. We suggest that southern populations are likely subsidized by the introduced prey.

Fire ants are also probably a valuable prey for other native insectivores. Populations of barn swallows (Hirundo rustica) and Northern rough-winged swallows (Stelgidopteryx serripennis) are also stable or increasing within the introduced range of S. invicta despite declines elsewhere [21]. Chimney swifts (Chaetura pelagica), tree swallows (Tachycineta bicolor) and Eastern kingbirds (Tyrannus tyrannus) may feed opportunistically on S. invicta queens [6]. We observed four additional species foraging in S. invicta swarms—scissor-tailed flycatchers (Tyrannus forficatus), Western kingbirds (Tyrannus verticalis), great-tailed grackles (Quiscalus mexicanus) and red-headed woodpeckers (Melanerpes erythrocephalus).

Solenopsis invicta is often viewed as an invasive species that negatively impacts animal communities [22], but to some aerial predators it is an abundant, reliable and nutritious food. Species in other regions where S. invicta has been introduced may also take advantage of this new-found prey. Purple martins possess substantial ecological and economic value because of the insects they consume [20]. The potential value of fire ants as prey for these and other avian insectivores should be determined before planning costly control efforts [7].

Ethics

This research followed all applicable laws and was approved by the University of Oklahoma Institutional Animal Care and Use Committee (protocol R12-019C).

Data accessibility

Data used in the analyses are contained in the electronic supplementary material.

Authors' contributions

J.A.H. and E.S.B. conceived the project; all authors designed the study and collected data; J.A.H. performed analyses and drafted the manuscript; all authors revised the manuscript, approved the final version and agreed to be held accountable for the content therein.

Competing interests

We have no competing interests.

Funding

This work was funded by NSF award IDBR-1014891 (E.S.B.), and an NSF Graduate Research Fellowship, OU Alumni Fellowship, UOBS Graduate Summer Research Fellowship and George Miksch Sutton Avian Research Scholarship (J.A.H.).