The term “site” is used here, as in Orchard (2011), to mean a discrete body of standing water–generally a lake, pond, or pool–where some or all life stages of bullfrogs are present. All bullfrogs examined came from 60 lakes and ponds spread across the coastal lowlands of southeastern Vancouver Island, 44 (73%) of which are clustered in peninsular regional Victoria (Figure 1, Table S1). All of these lakes and ponds are situated between the latitudes 49.8047 and 48.3867 (Figure 1) and range in surface area from lakes as large as 61 ha² (Langford Lake: 48.4484, -123.5296) with perimeter distances of almost 5 km down to very small ponds of less than 1 ha². Most of the sites were florally complex with thick patches of floating aquatic and emergent vegetation, often with surrounding riparian thickets of willow (Salix spp.) and hardhack (Spiraea douglasii). Conversely, many of the smaller ponds were highly disturbed and modified habitats such as at farm ponds or golf course ponds with relatively little vegetation either in the water or around the shoreline.

All fieldwork was carried out by one 2-person team working full-time, approximately 125 nights per season (April-September). Adult and juvenile bullfrogs were captured live using a patented manual “electro-frogger” technique that stuns them momentarily in the water so that they can be netted. They were later euthanized in a two-stage process that cooled them to torpor below 2⁰ C before being quick frozen (Orchard 2011). After at least 48 hours in a deep freeze, the bullfrogs were thawed and body lengths measured with Vernier calipers (BL; snout to anus) recorded to the nearest 0.1 mm. The alimentary canal of each bullfrog was incised at the anterior and posterior sphincters of the stomach. All contents were removed and examined. Vegetation and other non-animal material were not included in this analysis. Size-classes were grouped according to body length and categorized as “juvenile” (< 80 mm; includes metamorphs but excludes tadpoles), “young adult” (80–120 mm), and “mature adult” (> 120 mm) (Table 2). “Metamorph” is a transitional stage whose morphology is primarily that of a juvenile but exhibiting some residual larval (tadpole) characteristics. We classed metamorphs as juveniles. Tadpoles did not figure in this study. The terms juvenile, young adult, and mature adult generally correspond to age-class cohorts, e.g. bullfrogs at this latitude spend their first year post-metamorphosis as a juvenile, their second year as a young adult, and their third year as a mature adult. Gender was determined by dissection for all specimens greater than or equal to 80 mm.

Six calendar months were available for fieldwork (April to September, inclusive) but only one site was sampled in all six calendar months (Florence Lake, 48.4589, -123.5127). This site provided 33% (n = 1, 681) of the total sample. Conversely, 58% (n = 35) of the total sites sampled were each visited in only one calendar month of each of the 6 months available but these collectively produced only 10% (n = 516) of the total sample. Most of the total bullfrog sample (68%, n = 3, 455) came from 8 sites that were visited in at least 4 of the 6 months (Table S1, Table S2).

Insects were found in 93% of the 4, 602 bullfrog stomachs with contents, which is consistent with Korschgen and Moyle’s (1955) 83.5% from a much smaller sample (n = 455). Of total identifiable remains 84% were insects, whereas Cohen and Howard (1958) found only about 67% insects in a sample of 300 from California’s San Joaquin Valley. The differences in these figures likely reflect lower latitude, seasonality, sample size, and size-class mix; however, the conclusions are all fundamentally the same, e.g. insects are consistently the most numerous organisms in the bullfrog diet. Certain insect groups, such as odonates and beetles, have frequently been identified as predominate (Bruggers 1973, Werner et al. 1995, Hothem et al. 2009).

This study found that early in the bullfrog active season, Odonata (dragonflies and damselflies; May: 45% adults; June: 81% adults) were a consistently important prey for all size-classes of bullfrogs, and this has also been reported by Werner et al. (1995). Water striders (Gerridae) were most frequently consumed by juvenile bullfrogs and were of particular importance during the first few weeks after spring emergence. On the other hand, Hothem et al. (2009) found a greater frequency of water striders in adult bullfrogs (21.5%) than in juveniles (6.5%), but from a much smaller series of only 107 bullfrogs (11 had no stomach contents), 31 of which were juveniles.

Bullfrogs are seemingly immune to many natural predator defenses. Previous studies have alluded to the toxic or potentially repellent effects of natural prey defense mechanisms on predatory bullfrogs. For example, Brodie (1968) found that northern rough-skinned newts from Oregon were lethally toxic to bullfrogs. Later, it was determined that newts from Vancouver Island were at least 1, 000 times less toxic than those from Oregon (Brodie and Brodie 1991). Of the 50 northern rough-skinned newts removed from bullfrogs, we recovered as many as three partially to well-digested newts from a single bullfrog stomach. It appears, therefore, that bullfrogs routinely ingest and safely digest rough-skinned newts on southern Vancouver Island with no apparent lethal effects. This situation likely makes northern rough-skinned newts on Vancouver Island exceptionally vulnerable to bullfrog predation.

Krupa (2002) examined bullfrog stomach contents from New Mexico and noted that wasps were commonly consumed. He posed the question: Are bullfrogs immune to the effects of wasp stings or do individuals consume wasps until they develop a conditioned avoidance? For example, in our results 35 bullfrogs had each eaten at least 10 social wasps and as many as 19 without any apparent conditioned avoidance to the wasp sting. Wasps and bees were eaten throughout the active season. Govindarajulu et al. (2006), in examining a small sample of stomach contents from Vancouver Island, also reported wasps as being important in sub-adult bullfrogs. Similarly, Diaz De Pascual and Guerrero (2008) discovered hymenopterans to be the most important dietary item for juvenile bullfrogs in Venezuela; however, it is not stated what type of hymenopterans. Interestingly, the bullfrog’s close relative, the green frog (Rana clamitans), showed the same seasonal pattern in terms of wasp and bee consumption in Michigan (Werner et al. 1995).

Sticklebacks were the most numerous vertebrate prey and were also one of the most defensively armed. Bullfrogs, however, were seemingly immune to the discomfort of stickleback spines, and we recovered as many as five of these fish from a single stomach. Bullfrogs are reported to have eaten both scorpions and rattlesnakes along the lower Colorado River (Clarkson and de Vos 1986), so their powers of overcoming or withstanding highly evolved, mechanical and chemical, prey defenses are known to be impressive.

Dragonfly nymphs are known to prey on bullfrog tadpoles (Hunter et al. 1992), but, conversely, adult and juvenile bullfrogs are major predators of adult and nymphal dragonflies (Table 4). It is fair to speculate that increasing densities of invasive predatory bullfrogs could create a corresponding decline in the densities of dragonfly nymphs. In some previous studies, dragonflies and damselflies are spoken of collectively as odonates (Korschgen and Moyle 1955, Werner et al. 1995, Diaz De Pascual and Guerrero 2008), whereas in this study the two groups are reliably separated. Of damselflies, 83% consumed were adult; and of dragonflies, 73% were adult (Table 4). Other studies have found adult odonates to be important in the bullfrog diet (Werner et al. 1995), but Hothem et al. (2009) in California and Korschgen and Moyle (1955) in Missouri found that the nymphal stage was more frequently consumed.

In 2011, we observed an adult common garter snake (Thamnophis sirtalis) eating a juvenile bullfrog, and this aquatic-foraging snake when at full adult size should be easily able to eat at least half-grown bullfrogs. Smith (1977) considered larger Thamnophis sirtalis as a likely bullfrog predator but also reported smaller Thamnophis sirtalis in bullfrog stomachs. All three native garter snake species found on Vancouver Island (Thamnophis elegans, Thamnophis ordinoides, Thamnophis sirtalis) were recorded in the bullfrog diet (Table S4). Taken together, the 11 garter snakes of three species reported here would rank just above red-legged frogs in total number of instances. It seems unlikely that the two aquatic foragers, Thamnophis sirtalis and Thamnophis elegans, would be able to avoid falling prey to adult bullfrogs. Seigel (1994) found that Thamnophis atratus, not native to British Columbia, is an ineffective predator of bullfrog tadpoles, and only the largest snakes can eat them.

A giant water bug (Belostomatidae) was observed killing a bullfrog tadpole in captivity (K. Jancowski, personal observation), and they are known predators of other anurans including ranids (Toledo 2005). At one site, Filberg Marsh (49.8047, -125.0594; May 27, 2010), 43% of the 44 adult bullfrogs captured had consumed one or more giant water bugs. Consequently, predation of giant water bugs by adult bullfrogs may be just one more example of adult bullfrog predation facilitating the survival of bullfrog tadpoles.

Another organism found in the adult bullfrog diet, and also a predator of bullfrogs (Hunter et al. 1992) is the predacious diving beetle, which was found in almost 7% of bullfrog stomachs and had been consumed at 67% of sites (Table 4).

Bullfrogs routinely leave the water and migrate overland as adults and juveniles, presumably feeding as they travel. This may account for species turning up in the bullfrog diet that are strictly terrestrial, e.g. Townsend’s voles, terrestrial shrews, northern alligator lizards, western red-backed salamanders (Plethodon vehiculum), and Oregon ensatina salamanders (Ensatina eschscholtzii).

Aphids, because they are tiny, would seem to be an unlikely temptation to bullfrogs. However, aphids ranked second only to social wasps in number of instances of insect predation (Table 4). One probable explanation for this is that in late-summer aphids aggregate in large numbers to feed on the floating leaves of the yellow pond-lily (Nuphar polysepalum). The aphids, in turn, attract the attention of predatory wasps, dragonflies, damselflies, brachyceran flies, lacewings, and ladybird beetles, which also attract the interest of predatory bullfrogs. In the process of catching or attempting to catch these larger insects, bullfrogs are inadvertently picking up aphids on their sticky tongues. Approximately 55% of bullfrogs containing aphids had also eaten one or more of these associated species. Consequently, pond-lily leaves can be important feeding stations for bullfrogs as aphids gather on them in late summer.

Cannibalism, though well known to occur in bullfrogs, has not been very comprehensively studied (Bury and Whelan 1984). Cannibalism in this study was of minor significance overall (0.43% of total prey remains) on south Vancouver Island, with 80% consumed in August and September (Table 6). Similarly, in Brazil, Silva et al. (2009) sampled 79 “adult bullfrogs” but found only one case of cannibalism in 49 cases of anuran predation. By contrast, Govindarajulu et al. (2006) reported bullfrogs in the stomachs of almost half (44%) of a sample of 68 “large” (> 130 mm) bullfrogs from southern Vancouver Island. One study from New Mexico (Stuart and Painter 1993) found evidence of cannibalism in 56 (40.6%) of 138 stomachs examined. In Venezuela, another study looked at 338 bullfrogs and reported cannibalism in 5% of sub-adults and 32% in adults (Diaz De Pascual and Guerrero 2008).

We sampled 448 bullfrogs that were greater than or equal to 130 mm in body length, or comparable in body size to the “large” category in Govindarajulu et al. (2006). Of our 448, only 35 (7.8%) had conspecifics in their stomachs. We sampled throughout the bullfrog active season (April to September) rather than just in the latter half of summer and we sampled 56 more sites than Govindarajulu et al. (2006). The smallest cannibalistic bullfrog that we found was 85 mm in body length, one of 25 cases involving bullfrogs less than 130 mm body length. Overall, we recorded 240 instances of bullfrog predation on amphibians with cannibalism accounting for only 34%.

In the absence of alternative prey, cannibalism remains an option for this species that would be of variable importance from site to site, season to season, and year to year. In the long-term, unmanaged bullfrog populations might conceivably drive down native species numbers to the point where cannibalism becomes increasingly important to bullfrog population sustainability.

Of native amphibians, the Pacific treefrog was the most frequently eaten by bullfrogs (Table 6). Treefrogs peaked in the bullfrog diet in May (39%) as male treefrogs migrate into the water to set up a mating chorus closely followed by females. At least 30% of treefrogs eaten in April and May were females, and 53% of these were gravid. Although bullfrogs are eating more adult males than adult females during this spawning period, the numerical loss of eggs to persistent (April to July) bullfrog predation could be substantial. Male treefrogs are likely in the water for a much longer interval than the females and they are making themselves more conspicuous by vocalizing (Smith 1977), which may account for their higher rate of mortality. Mid-summer predation of treefrogs is primarily attributable to the mass transformation of treefrog tadpoles and their subsequent migration to land (Table 6).

Second to treefrogs are rough-skinned newts. Predation on newts peaked in May (36%) and then rose again in August (26%) (Table 6). These peaks coincide with the May migration of gravid adult female newts to the water to reproduce and the late-summer transformation of larval newts into terrestrial juveniles migrating away from the water (Oliver and McCurdy 1974).

Krupa (2002) has also noted a mid-summer increase in the consumption of social wasps, rising steeply in August then dropping slightly in September (Table 4). Social wasps (Vespidae) become more accessible to bullfrogs in August as the wasps prey upon aphids that aggregate on pond-lily leaves. This wasp-aphid association is an annually recurring phenomenon that may account for the extraordinary abundance of aphids in the bullfrog diet.

Included in this study were the four sites sampled over 5 years by Govindarajulu et al. (2006). We documented more species overall, which included additional vertebrate species. Our early-spring sampling of Beaver Lake Pond (48.5102, -123.3991) on April 24 and May 5, 2010 undoubtedly accounts for our records of recently hatched red-listed western painted turtles. This species would have certainly been missed entirely if fieldwork had been carried out at any other time. Similarly, timing may have been a factor in our discovery of coho salmon at Prior Lake (48.4764, -123.4672) on July 3, 2010.

The bullfrogs that figured in this study were not collected primarily for the purpose of examining their stomach contents. They were captured and euthanized as part of a research and development program exploring the feasibility and practicality of bullfrog eradication. This was carried out while testing and refining the electro-frogger technique on a regional scale. Most of the 60 sites included in this study (86%) were only visited in three or less of the six months available within the bullfrog’s active season, resulting in only 32% of the overall sample (Table S2). This is because, for the most part, they were smaller ponds where all of the adult and juvenile bullfrogs present could be removed in one or two evenings. In addition, there were a few single-evening reconnaissance missions to sites of interest. The remaining 14% of sites were the larger and more difficult ones where bullfrog densities, immigration rates, and problematical habitats required more effort to bring bullfrog numbers down. The most demanding (Florence Lake, 48.4589, -123.5127) was the only site visited in each of all six months (April to September) and produced 33% of the overall sample (Table S1, Table S2). Consequently, stomach contents from most sites are snapshots of what bullfrogs were eating at that particular site on a specific evening or over a few nights. The database compiled for this analysis is, therefore, a blend of a few sites sampled many times throughout the summer coupled with many sites visited only a few times each in a much more restricted time-frame. The regional database is comprehensive in terms of including samples collected nightly during the entire field season, but is fragmentary in terms of providing seasonally comparative datasets for most of the sites.

American bullfrogs have been identified as, or are suspected to be, a threat to the survival of various vertebrates world-wide, including native fish (Mueller et al. 2006), amphibians (Fisher and Shaffer 1996, Hecnar and M’Closkey 1997, Adams 2000, Kats and Ferrer 2003, Lannoo et al. 1994, Moyle 1973, Hammerson 1982), aquatic turtles (Spetz and Spence 2009), and island endemic birds (Pitt et al. 2005).

In British Columbia, three species of conservation concern relate to this study: the red-listed western painted turtle (Chrysemys picta bellii), the blue-listed northern red-legged frog (Rana (Lithobates) aurora), and, the aquatic-foraging and red-listed, American water shrew (Sorex palustris brooksi). Bullfrogs were found to be consuming hatchling western painted turtles as they entered the water. This was clear from the average carapace length of only 3 cm and the timing of these instances in late April and early May (Table 6). Any loss of hatchling painted turtles is a serious threat to turtle survival because the females produce few eggs and survivorship to recruitment is low (Gregory and Campbell 1996). Hatchling painted turtles are easily swallowed by bullfrogs and will remain vulnerable for at least the first few weeks post-hatching until their shell dimensions exceed a bullfrog’s maximum gape. Red-legged frogs were consumed primarily as fully metamorphosed juveniles and eaten mostly in the month of August (Table 6). American water shrews have not been recorded in the bullfrog diet, but they are flagged because the historical database for this shrew lists localities, such as Hamilton Marsh on Vancouver Island (49.3159, -124.4625), that are now thoroughly invaded by bullfrogs. The presence of shrews (at least some were Sorex vagrans), as well as the larger Townsend’s voles, demonstrate that bullfrogs will take small mammals, and the habits and habitat preferences of the American water shrew should make them especially vulnerable to bullfrog predation. The Pacific water shrew (Sorex bedirii) has also been recorded in the bullfrog diet (Campbell and Ryder 2004).

It is of economic interest that coho salmon (Oncorhynchus kisutch) juveniles were found in 16% of bullfrogs sampled from Prior Lake in early July (Table 6, Table S1). Most of these were about 8 cm long, though bullfrogs have been documented eating trout up to 15 cm in length (Bury and Whelan 1984). It is not known whether coho salmon are being preyed upon locally in lotic habitats. However, many streams on southern Vancouver Island become intermittent in late summer and in shallow isolated pools salmon fry could be more vulnerable to bullfrog predation. Garwood et al. (2010) recently documented an adult bullfrog from a stream in California with an 11.6 cm long coho salmon in its stomach. Lotic habitats were not sampled in our study because bullfrogs aggregate and reproduce locally only in the warmer standing water of lakes and ponds. Salmonids, such as coho salmon, tend to prefer cooler and better oxygenated flowing waterways.

An organism that lies dormant for almost six months of the year must replenish its fat reserves during the relatively brief six-month active season. Mature adults, in particular, should have the life experience to be proficient hunters. They also have energy demanding roles that include vocalizations, territorial defense, egg production, spawning, and may include overland migrations. Then they must end the season with sufficient reserves to overwinter for another six months. The percentage of mature adults of both genders with empty stomachs was, therefore, remarkably high (Table 2B).

Govindarajulu et al. (2006) also found empty stomachs but only in mature males and newly metamorphosed bullfrogs. The so-called “metamorph” is a brief transitional stage at the end of the tadpole stage and at the very beginning of the juvenile stage. During this interval, the frog displays combined morphological characteristics of a larva and a juvenile. Feeding in juveniles is not possible until the mouth and internal organs of the tadpole stage are fully resorbed and reformed into a completely metamorphosed morphology. An indeterminate number of the juveniles with empty stomachs (Table 2B) exhibited tail vestiges and so their empty stomachs may be attributed to this transitional “metamorph” morphology that is not yet fully, or has only just become, operational in the predator mode.