METHODS

Dark-billed Cuckoo nesting observations were made in a mangrove forest at Playa Tortuga Negra (0°14’S, 91°23’W), on the northwest coast of Isabela Island. This mangrove forest is 20 ha, consisting of three mangrove species: White Mangrove (Laguncu-laria racemosa), Red Mangrove (Rhizophora mangle), and Black Mangrove (Avicennia germinans) (^{Dvorak et al. 2000}). Nesting observations were made opportu-nistically while monitoring the reproductive success of the Mangrove Finch (Camarhynchus heliobates) from February 18 to April 22, 2022.

We made direct observations of three Dark-billed Cuckoo nests using binoculars (Nikon 10x42) from a distance of no less than 7 m. We obtained 13.5 h of observations: Nest 1: 7 h 4 min, once during the in-cubation period and four times during the nestling period; Nest 2: 5 h 5 min, four times during the in-cubation period; and Nest 3: 1 h 21 min, twice during the incubation period. Observations were carried out at different times of the day between 6:25 and 17:52 h, and ranged from 17 min to 2 h 21 min in duration. We documented incubation bouts, some adult incubation behavior, and some adult chick feeding behavior.

Additionally, we monitored Nest 1 through indi-rect observations with a trail camera (Reolink with an internal recharging solar panel battery) from March 18 to March 29, 2022. The camera, covered in camou-flague tape to reduce its visibility, was located 1.5 m from the nest on a branch in an adjacent mangrove tree. The camera was active day and night (24 hours), set on motion-detect video mode, recording for 30 s when triggered. It was deployed one day before the eggs hatched, so it documented adult behavior during the nestling period until fledging. The camera recor-ded at least one video per day, totaling 139 videos recorded between 6:43 and 15:48 h. These videos showed the nestlings’ plumage development, and adult and nestling behavior.

We estimated the height above ground of the three nests when the tide was low, using the height of a per-son as a reference. Nests were collected after confir-ming that they had been abandoned by fledglings and adults, with 40 min monitoring for two consecutive days. Nest 1 was collected two days after the fledglings left the nest, and Nest 2 was collected eight days after the adults abandoned the nest. We took the following measurements from Nests 1 and 2 with a metal ruler: external diameter, internal diameter, cup depth, and nest height. We also described the materials of Nests 1 and 2 and looked for the presence of Avian Vampire Fly pupae. This fly is introduced to the Galapagos Ar-chipelago and its larvae parasitize nestlings, resulting in many negative impacts on terrestrial birds (Fessl et al. 2001, 2018, Fessl and Tebbich 2002, McNew and Clayton 2018). We took length and width measu-rements of the infertile eggs with electronic calipers accurate to 0.02 mm: 1 egg in Nest 1 and 2 eggs in Nest 2. Data collection followed the protocols of Cade-na-Ortiz (2018) and Fierro-Calderón et al. (2021). For nest shape, we followed Simon and Pacheco (2005), for egg shape Baicich and Harrison (1997), and for color Smithe (1975).

RESULTS

Copulation

On March 17 and April 5, 2022, we observed two pairs of Dark-billed Cuckoos copulating in the unders-tory layer of the mangrove. One individual swooped towards a branch, and another individual approa-ched. The first one situated itself on top of the second bird, which turned its body in a lateral position. They raised their tails and copulated for approximately 15 s. Subsequently, the individual that was in a lateral position flew away, then the other ruffled its feathers briefly and flew away. These observations were made about 300 m from the nests described in this article, so we don’t know if these pairs are the ones in our study or others.

Figure 1: A) Dark-billed Cuckoo (Coccyzus melacoryphus) in Nest 3. B) Location of Nest 1 in a mangrove swamp. C) Pupae of the Avian Vampire Fly (Philornis downsi) found in Nest 1. D) Unhatched infertile eggs of Nest 2.

We located Nest 1 on March 14, 2022, with three eggs and incubating adults observed. We located Nest 2 on March 21, 2022, when an adult was observed incubating. We located Nest 3 on March 22, 2022, when we observed an adult incubating (Fig. 1A). We could not access Nests 2 and 3 to view their contents so the number of eggs in these nests was not determined at the time, we identified incubation because we saw the adults sitting on the nest for at least 20 continuous minutes. We only documented chicks hatch in Nest 1. The adults abandoned Nest 2 during incubation, and we did not observe the outcome of Nest 3.

Nest description and placementThe three nests were located in forks of White Mangrove branches in the understory layer, 5, 7, and 9 m above the ground (Fig. 1B). The nests were low/ cup-shaped, and small, so that the cloacal region and tail of the adults protruded from the edges of the nests. The dimensions of Nests 1 and 2 were: an external dia-meter of 16 and 13.2 cm, an internal diameter of 7.3 and 6.9 cm, a cup depth of 2.2 and 1.7 cm, and a nest height of 6.5 and 7 cm (Table 1). The outer layer of Nests 1 and 2 were constructed with White Mangrove branches of different lengths and thicknesses, most ending in small forks, while the inner cups were composed mainly of leaves, stipules, and bark from Red Mangrove stems. They also had smaller quantities of roots, tendrils, and some thinner branches of unidentified plants. In addi-tion, only in Nest 1, when we dissected the nest mate-rials, we found three pupae of the Avian Vampire Fly (Fig. 1C), identified by the presence of a frothy cocoon and their typical endings (Fessl et al. 2006).

Eggs and incubationIn Nests 1 and 2, eggs were short sub-elliptical in shape, and light green in color with no markings (Fig. 1D). The egg from Nest 1 measured: 3.4 x 2.5 cm, and eggs from Nest 2 measured: 3.1 x 2.6 cm, and 3.3 x 2.6 cm (Table 1). The clutch size in Nest 1 was three eggs, while Nest 2 contained two eggs and shells, so we were not able to determine clutch size.

In all three nests, we observed both adults incu-bating the eggs. The incubation bouts varied, with the shortest lasting 4 min and the longest lasting 1 h 6 min (mean= 25.92 min, SD= 21.55, n= 13). The time that adults left the eggs unattended in the nest lasted between 1 and 17 min (mean= 4.35 min, SD= 4.28, n= 17). When an adult left its nest, another individual arrived, or the same individual returned, and conti-nued to incubate. Only on two occasions were two adults found in a nest simultaneously (n= 13 bouts) for a few seconds. At times when the adults were incu-bating, they moved within the nest to one side or the other by at least 2 or 3 cm, keeping the eggs beneath them. Although we did not count how many times they performed these behaviors, they were frequent and occurred in all three nests.

When the adults approached the nest to resume incubation they perched on low branches approxima-tely 1 m below the nest, then began to climb slowly, jumping from branch to branch, turning their head side to side while climbing. On three occasions, we observed an adult arrive with nest materials for the outer layer and the inner cup, and after adding them, it resumed incubation.

Nestlings and nestling attendanceIn Nest 1, through the trail camera video images, we documented the full development of the nestlings after hatching to fledging. The first chick hatched on March 19, 2022. It had gray nessoptiles on its head and back, and the black eye stripe was already evi-dent. The second chick was observed on March 20. On March 22, we observed both chicks with pin feathers on their wings and backs. On March 26, the chicks had their first feathers, which were brown on their wings and beige on their breasts. Their heads kept the gray pin feathers and the black eye stripe. Their tails were short, about a quarter of the size of the tail of an adult. Their wing feathers were also short.

On March 26, one of the chicks left the nest, possi-bly the first to hatch. This chick remained in the nest for seven days from hatching until fledging. On March 27, the other chick was still in the nest. It perched several times on the edge of the nest and flapped its wings constantly. On March 28, the second chick fled-ged, having remained in the nest for eight days since hatching. This chick had more developed plumage and fewer pin feathers than the previous one.

In addition, from reviewing the camera videos we observed both adults directly provisioning the chicks, but only in 2 of 14 observations were both adults found in the nest at the same time. For the first days after hatching, the adults did not deliver whole prey to the nestlings, they crushed the prey and held it in the chicks’ beaks for several seconds. The first time an adult deli-vered whole prey to a chick was when the chick was six days old, one day before it fledged. The chicks begged for food, opening their beaks and flapping their wings, creating sounds similar to bees buzzing. When a chick was seven days old and was alone in the nest, it began to make its first calls, which increased in volume and syllables, until it fledged the following day. The adults were brooding the chicks throughout their time in the nest and an adult was sitting inside the nest next to its chick only hours before the chick fledged the nest. In addition to the video recordings, on four occasions in the field we observed an adult arriving with crickets (Nesoecia cooksoní) for the chicks.

DISCUSSION

Our records and previous records of Dark-billed Cuckoo nesting in the Galapagos Islands (Gifford 1919, Ervin 1989) show a breeding period between January and May. These months coincide with the ra-iny season and the breeding of Galapagos land birds, due to the availability of resources (Grant 1986). In Brazil, nesting of this species is also related to the rainy season; between January and June (Paixao et al. 2021). In Argentina, between October and February (de la Peña 1983, 2013), and in Colombia with one record in October (^{Payne 1997}). It is important to con-sider that all records from Galapagos are occasional, so the breeding period could be longer.

The Dark-billed Cuckoo’s nests described in this paper were low/cup-shaped (Fig. 1B), following the classification of Simon and Pacheco (2005), although other studies have described them as a simple plat-form shape (de la Peña 1983, 2013, Di Giacomo 2005, Paixao et al. 2021).

Nest dimensions described so far, and data from this study, show slight variations in the following me-asurements: internal diameter, cup depth and nest height (1.6, 0.5 and 0.25 cm, respectively), while the external diameter measurement varied up to 6 cm (Gifford 1919, de la Peña 1983, Ervin 1989, Paixao et al. 2021). Meanwhile, the height of the nests from the ground varied quite a bit between 0.17 and 9 m (Gifford 1919, Dabbene 1926, de la Peña 1983, Ervin 1989, Di Giacomo 2005, ^{Salvador 2011}, Paixao et al. 2021). All three nests in this study were located hi-gher than even the nests described on San Cristobal (maximum height= 3.6 m) and Santa Cruz Islands (maximum height= 3.5 m) (Gifford 1919, Ervin 1989). This variation is probably due to the difference in vegetation composition of the sites where nests were found, with notably taller vegetation at our study site. The average height of the forest at Playa Tortuga Negra was evaluated at 12 m (^{Dvorak et al. 2000}) with a maximum canopy height of 25 m (authors pers. obs.).

The materials used to construct the nests were also different, also due to the composition of the su-rrounding vegetation. We found differences between the materials of the outer and inner cups of the nests, as reported from some nests in Argentina (de la Peña 1983, 2013, Di Giacomo 2005). The nests of many bird species differ in the materials used for the outer and inner cups, and there are many hypotheses that describe the possible reasons for this feature (Lovette and Fitzpatrick 2016), perhaps it provides more pro-tection for the eggs and chicks.

We observed three Avian Vampire Fly pupae in a Dark-billed Cuckoo nest, indicating that the larva fed on the nestlings. Despite this, the chicks survived and fledged successfully. This is the second reported case of parasitism in Dark-billed Cuckoo. It has been previously documented in the humid zone of Santa Cruz Island, where 1 of 2 nests reviewed had five Avian Vampire Fly pupae (Fessl et al. 2001, Fessl and Tebbich 2002). With so few records, much remains unknown about the interactions between the Dark-bi-lled Cuckoo and Avian Vampire Flies, which currently threaten 75% of Galapagos land birds species (Fessl et al. 2018). We want to emphasize the small number of pupae found in the two nests reported so far, with only 5 and 3 pupae; on the contrary, the Mangrove Finch, which nests in the same forest, shows very high levels of parasitism (Cunninghame et al. 2015).

The coloration of the eggs has been described as va-rious shades of light blue to light green, while the shape has also been described as elliptical (^{Smyth 1928}, de la Peña 1983, 2013, Ervin 1989, Di Giacomo 2005, Paixao et al. 2021). The clutch size was within the range of pre-vious records ranging from 1 to 6 eggs (Gifford 1919, de la Peña 1983, 2013, Ervin 1989, Di Giacomo 2005, ^{Salvador 2011}, Paixao et al. 2021). Although it is assumed that nests with 1 or 2 eggs were found during laying as incomplete clutches. The most common clutch size ranges from 3 and 5 eggs (Paixao et al. 2021).

We report a nestling period of 7 to 8 days, which is the shortest report published to date for the species, as other authors report a nestling period of up to 15 days (de la Peña 2013), although 10 days is the most common (Di Giacomo 2005, ^{Salvador 2011}, Paixao et al. 2021). The nestlings of their congeners also fledge the nest after a short nestling period, with Yellow-bi-lled Cuckoo (Coccyzus americanus) between 7 and 9 days and Black-billed Cuckoo (C. erythropthalmus) between 6 and 7 days (Hughes 2020a, 2020b), which could suggest that rapid development is an ancestral trait in the family (Riehl 2021). However, it should also be investigated whether the nestling period of Dark-billed Cuckoo is shorter in the Galapagos Islands than on the mainland.

Much remains to be explored about the reproduc-tive biology of the Dark-billed Cuckoo, for example: the factors driving different local and regional nesting adaptations, comparisons between island and main-land nesting, and interactions with other organisms, including invasive species. We therefore encourage the continuation of studies on the species, as they provide a basis for further research.

ACKNOWLEDGEMENT

We thank Charles Darwin Foundation and Galapagos National Park Directorate. Our work was supported by an individual donation, FEIG (Fondo de Especies Invasoras de Galápagos), and Galapagos Conservation Trust. We thank Julia Bolaños for iden-tifying Nesoecia cooksoni and Héctor Cadena for com-ments on an earlier version of the manuscript. This work was carried out under Galapagos National Park Directorate research permits, permit numbers: PC-52-22 and PC-30-22. This publication is contribution number 2506 of the Charles Darwin Foundation for the Galapagos Islands.

Recibido: 8 de mayo 2023

Aceptado: 26 de noviembre 2023