An opportunist predator hidden in the vegetation: on the predation of birds by Philodryas olfersii (Serpentes: Dipsadidae)

ABSTRACT

Snakes are common predators of birds. However, reported cases of snake predation on Troglodytes musculus are scarce. Here, we report a predation attempt of a Troglodytes musculus nestling by the dipsadid snake Philodryas olfersii. We also present a list with bird species recorded as prey of this snake species. We found 25 predation events of P. olfersii on adult, juvenile, and nestling birds. A total of 19 bird species from 14 families have been reported as prey of P. olfersii. Most predation events occurred on the vegetation, while some others were observed on the ground, cage, and artificial nest.

Serpentes são predadores comuns de aves. No entanto, casos relatados de predação de Troglodytes musculus por serpentes são escassos. Aqui, relatamos uma tentativa de predação de um filhote de Troglodytes musculus pela serpente Philodryas olfersii. Também apresentamos uma lista de espécies de aves registradas como presas dessa espécie de serpente. Encontramos 25 eventos de predação de P. olfersii sobre aves adultas, juvenis e filhotes. Um total de 19 espécies de aves pertencentes a 14 famílias foram relatadas como presas de P. olfersii. A maioria dos eventos de predação ocorreu na vegetação, enquanto alguns outros foram observados no solo, gaiola e ninho artificial.

KEYWORDS:

• Dipsadidae
• green snake
• nestling predation
• Troglodytidae

The Neotropical dipsadid Philodryas olfersii (Lichtenstein 1823) is a medium-sized venomous, semi-arboreal and diurnal snake widely distributed throughout South America, where it occurs in Argentina, Bolivia, Brazil, Colombia, French Guiana, Guyana, Paraguay, Peru, Uruguay, and Venezuela [1,2]. It inhabits mainly forest and forest edge habitats [3], but can also be found in swampy and agricultural areas as well as in the vicinity of human habitations [4–7]. As a generalist predator, P. olfersii preys on a wide variety of small vertebrates such as frogs, lizards, snakes, birds, rodents and bats [8–11].

Snakes employ two foraging strategies to hunt prey – active searching and ambush [12,13]. They are common predators of birds, with their predation on nestlings being one of the main causes of nest failure for most birds [14,15]. However, reported cases of snake predation on adults and nestlings of passeriform Troglodytes musculus Naumann, 1823, are scarce [16,17].

Troglodytes musculus is recognized as a species distinct from Troglodytes aedon Vieillot, 1809, by the Brazilian Ornithological Records Committee [18], although BirdLife International [19] does not acknowledge this distinction and treats T. aedon as a single species living throughout the Americas. Troglodytes musculus often builds nests in natural cavities or among human construction, such as on walls and under tiles [20]. It uses grass and/or roots to install nests, depending on the place they have chosen, and incubates 3 to 7 eggs, which hatch after 15 days [20,21]. Here we reported a predation attempt of a Troglodytes musculus nestling by the dipsadid snake Philodryas olfersii, and provide a list of bird species recorded as prey of this snake.

Field observation was performed in the rural zone of the municipality of Assaí, northern Paraná State, southern Brazil (−23.4709°S, −50.8926°W, Datum WGS 84). A bibliographic search was conducted using Google Scholar to summarize the records of P. olfersii predating individuals of other bird species. The search terms used were: “Philodryas olfersii”, “diet”, “feeding behavior” and “birds”. Natural history notes published in Atualidades Ornitológicas, Herpetological Bulletin, Herpetology Notes, and Herpetological Review were also searched for predation records. Photos and videos of predation records were also obtained from WikiAves (https://www.wikiaves.com.br/) and YouTube (www.youtube.com).

At 14:30 h on 28 December 2018 an adult P. olfersii was observed trying to reach a nest of T. musculus containing three nestlings in the backyard of a house in the rural zone of the municipality of Assaí (Figure 1). The nest was located inside a cylindrical cardboard container on top of a short wall. While unsuccessfully trying to climb the wall, the snake was mobbed by an adult T. musculus (https://www.youtube.com/watch?v=AyRA_wsYh9Q&feature=youtu.be). The adult bird uttered alarm calls, displayed approaches and attacked three times by pecking the snake in the head (Figure 2). Disturbed by the mobbing behavior, the snake took shelter on a roll of barbed wire below a table near the wall. The snake remained motionless with its head directed towards to the cardboard container (Figure 3). After some minutes, the snake then climbed the table, reached the wall and entered into the cardboard container with the nest. While was holding one of the three nestlings, it was mobbed by the adult bird, at which point the property owner removed the snake from the cardboard container and killed it.

Figure 1. Nestlings of Troglodytes musculus.

Figure 2. Sequence of images showing Philodryas olfersii being mobbed by Troglodytes musculus. The position of the bird is indicated by the letter B, while the position of the snake is indicated by the letter S. (a) Adult of T. musculus preparing to attack an individual P. olfersii. (b) Bird flying toward the snake. (c) Bird strikes the snake. (d) and (e) Snake retreats after the attack. (f) and (g) Second attack by bird. (h) and (i) Bird flies and lands on top of the wall and then utters an alarm call. (j) and (k) Third attack by bird

Figure 3. Philodryas olfersii taking shelter after predation attempts

Our review of the literature and photos and videos of predation records uncovered 25 events of P. olfersii preying upon adult, juvenile and nestling birds (Table 1). These 25 records reveal that 19 bird species belong to 14 families have been reported as prey of P. olfersii. Thraupidae was the family with the greatest number of reported predation events with seven records. Most of the predation events occurred on vegetation, although some cases occurred on the ground, in a cage or in an artificial nest (Table 1).

Table 1. Bird species reported as prey of Philodryas olfersii.

Bird species	Prey age	Predation microhabitat	Locality (all in Brazil)	Source
Cardinalidae
Cyanoloxia brissonii (Ultramarine Grosbeak)	?	Cage	Montenegro, RS	[30]
Columbidae
Columbina picui (Picui Ground-Dove)	?	?	Carlos Chagas, MG	[31]
Columbina talpacoti (Ruddy Ground-Dove)	?	?	Pentecoste, CE	[6]
	?	?	São Jerônimo and Barão do Triunfo, RS	[32]
Dendrocolaptidae
Lepidocolaptes angustirostris (Narrow-billed Woodcreeper)	Adult	Vegetation	Três Rios, RJ	[33]
Fringillidae
Spinus magellanicus (Hooded Siskin)	?	Vegetation	Baependi, MG	[34]
Icteridae
Gnorimopsar chopi (Chopi Blackbird)	?	?	Distrito Federal, DF	[35]
Passerellidae
Zonotrichia capensis (Rufous-collared Sparrow)	Adult	Vegetation	Piraju, SP	[36]
	?	Vegetation	Pelotas, RS	[37]
	Nestling	Vegetation	Paraibuna, SP	[38]
Passeridae
Passer domesticus (House Sparrow)	Adult	Vegetation	Campinas, SP	[4]
	Adult	Vegetation	Nazaré da Mata, PE	[39]
Pipridae
Chiroxiphia caudata (Swallow-tailed Manakin)	Nestling	Vegetation	Nova Lima, MG	[40]
Psittacidae
Melopsittacus undulates (Budgerigar)	?	Cage	Lavras, MG	[41]
Rhynchocyclidae
Tolmomyias sulphurescens (Yellow-olive Flycatcher)	Nestling	Vegetation	Cuiabá, MT	[42]
Thraupidae
Coereba flaveola (Bananaquit)	Juvenile	Vegetation	Campinas, SP	[4]
	?	Vegetation	Campinas, SP	[24]
	Juvenile	Vegetation	Gurupi, TO	[43]
Sicalis flaveola (Saffron Finch)	Adult	Vegetation	Carlos Chagas, MG	[44]
Sporophila caerulescens (Double-collared Seedeater)	?	Cage	Bossoroca, RS	[30]
Tangara sayaca (Sayaca Tanager)	Adult	Vegetation	Campinas, SP	[4]
	Adult	Vegetation	Sabinópolis, MG	[45]
Thamnophilidae
Thamnophilus palliatus (Chestnut-backed Antshrike)	?	?	Carlos Chagas, MG	[31]
Troglodytidae
Troglodytes musculus (Southern House Wren)	Nestling	Artificial nest	Assaí, PR	This study
Turdidae
Turdus leucomelas (Pale-breasted Thrush)	Nestling	Vegetation	Carlos Chagas, MG	[46]
Turdus rufiventris (Rufous-bellied Thrush)	Nestling	Ground	Santa Margarida do Sul, RS	[47]

Brazilian states: CE, Ceará; DF, Distrito Federal; MG, Minas Gerais; MT, Mato Grosso; PE, Pernambuco; PR, Paraná; RJ, Rio de Janeiro; RS, Rio Grande do Sul; SP, São Paulo; TO, Tocantins

? – data not available.

Among snakes of the genus Philodryas, only Philodryas chamissonis, P. nattereri and P. patagoniensis have been reported as predating nestlings of Troglodytes aedon and T. musculus [17,22,23]. There were no reports of T. musculus as prey of P. olfersii among the 25 predation events obtained from the literature and photos and videos of predation records. Therefore, this reported case adds P. olfersii to the list of predators of T. musculus.

Philodryas olfersii is a green snake that actively forages both on the ground and among vegetation [2]. In southern Brazil, P. olfersii has been reported to prey mainly on nestlings [2]. The present study, however, found adults and nestlings to account for most records of predation by P. olfersii (see Table 1), which seems to reflect its generalist feeding strategy and the availability of these prey items in the habitats where this snake species is found [2,4,24]. Furthermore, the higher number of bird predation events that occurred in vegetation is associated with foraging strategies and camouflage of P. olfersii in this type of microhabitat, which favors hunting for prey and avoiding visually oriented predators [2].

Potential prey employ mobbing behavior in an attempt to confound, distract or physically attack the predator [25,26]. In southeastern Brazil, attempts by P. olfersii to prey on birds were hindered by a group of mockingbirds (Mimus saturninus) that displayed mobbing behavior towards the snake [24]. Although mobbing by a group increases the chances of hindering predation [24], the mobbing behavior displayed by the single adult T. musculus did not prevent P. olfersii from trying to prey one of the nestlings.

Philodryas olfersii occasionally preys on adult and nestling birds living in cages and artificial nests in human habitations near native vegetation [27,28, this study]. As observed in the present study, individuals of P. olfersii can be killed by humans while actively searching for prey in human habitations, while in other cases humans can be envenomed by the snake [27–29].

Disclosure statement

No potential conflict of interest was reported by the authors.

Additional information

Funding

DLS received finacial support from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - CAPES [88887.342372/2019-00] and FHO received finacial support from CAPES/Fundação Cearense de Apoio ao Desenvolvimento Científico e Tecnológico [88887.162751/2018-00].