NESTING BIOLOGY OF THE BLACK-THROATED TODY-TYRANT ...

The Wilson Journal of Ornithology 129(4):820–826, 2017

NESTING BIOLOGY OF THE BLACK-THROATED TODY-TYRANT (HEMITRICCUS GRANADENSIS) WITH NOTES ON MATING DISPLAYS ˜ 2 JENNA M. McCULLOUGH1,3 AND GUSTAVO A. LONDONO ABSTRACT.—There is limited information on the breeding biology of members of the speciose genus Hemitriccus (Aves: Tyrannidae), published nest descriptions exist for only six of the 22 species. The Black-throated Tody-Tyrant (Hemitriccus granadensis) is one of these species that lacks information regarding its nesting biology. We provide the first nest, egg, nestling, and incubation behavior descriptions for the species with notes on its courtship behavior. We found three nests and observed one courtship display at three field sites, two in Colombia and one in Peru. The nest of H. granadensis is an enclosed ‘‘purse-like’’ pendant pouch inside of a moss ball suspended from a small branch with a side entrance and obscured by vegetation. Two nests had a single egg, which averaged 18.1 312.9 mm and 1.55 g. Egg appearance varied between nests, the egg at the Colombian site was tan and unmarked, whereas the egg at the Peruvian site was bright white with a few scattered, red specks. We cannot describe the full incubation period or nestling period because of egg infertility and nestling death. However, one nest was discovered with an egg that was incubated for 19 days. Nest attentiveness was 77.5% and average inner nest temperature differed between the Colombian (6SD) (23.79 6 1.58C) and Peruvian (17.27 6 1.548C) nests. We provide observations and video footage of the courtship display that match previous observations of this species. Overall, the nest shape resembles those of other Hemitriccus species, but clutch size differs from information published for the genus. Received 28 July 2016. Accepted 19 April 2017. Key words: Andes, breeding biology, courtship, incubation behavior, nest, tropics.

Tody-Tyrants (Tyrannidae) are a group of small flycatchers with proportionally long, flattened bills that comprise 53 species within eight genera (Fitzpatrick 2004, Gill and Donsker 2017). All of its members forage by striking upward and build purse-like pendant nests (Fitzpatrick 2004). Hemitriccus, one of the most speciose genera in the Tyrannidae, is composed of 22 species that inhabit the northern two-thirds of South America, extending from Colombia and Venezuela to northern Paraguay and Argentina (Clock 2004, Ridgely and Tudor 1994). The systematics of tody-tyrants remains unclear, and recent phylogenetic analyses of Hemitriccus have shown the genus to be polyphyletic (Tello and Bates 2007, Rheindt et al. 2008). Breeding biology and nesting behavior of Hemitriccus is poorly known and only scattered information is available (Clock 2004). Most described nests for Hemitriccus species are enclosed pendant nests with a side entrance suspended from the tip of a branch or vine (Ridgely and Tudor 1994, Fitzpatrick 2004). Published nesting information is limited for this genus: nests have been formally described for six of the 22 species. These include the pendant nests 1 University of New Mexico, Albuquerque, NM 87131, USA. 2 Departamento de Ciencias Biolo´ gicas, Universidad ICESI, Cali, Colombia. 3 Corresponding author; e-mail: [email protected]

of H. nidipenulus (Euler 1900), H. margaritaceiventer (Hilty and Brown 1986, de la Peña 1987, Narosky and Salvador 1998), H. striaticollis (Kirwan and Whittaker 2009), and H. rufigularis (Clock 2004), as well as the atypical, ball-shaped nest attached to vertical stalks of bamboo for H. obsoletus (Bencke et al. 2001) and the globular pensile nest of H. diops (Kirwan and Whittaker 2009). A clutch of two eggs has been reported for six species: H. obsoletus (Bencke et al 2001), H. diops (Kirwanand Whittaker 2009), H. striaticollis (Kirwan and Whittaker 2009), H. nidipendulus (Hilty and Brown 1986, de la Peña 1987, Narosky and Salvador 1998), H. rufigularis (Clock 2004), and H. orbiatus (M. Cohn-Haft unpubl. data in Bencke et al 2001). H. margaritaceiventer has a 1– 3 egg clutch, but one egg has only been reported on a single occasion, and a nestling period of 13– 14 days (Hilty and Brown 1986, de la Peña 1987, Narosky and Salvador 1998). There is no information regarding incubation behavior or nestling period for any species in this genus. The Black-throated Tody-Tyrant (Hemitriccus granadensis) is a small, inconspicuous understory species that varies from uncommon to fairly common across its geographic range (Clock 2004). The species is split into seven subspecies that inhabit humid, mossy montane cloud forest 1,800–3,300 m in the Perija´ Mountains of Venezuela, the Santa Marta Mountains of Colombia, and the west and central Andes of Colombia,

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McCullough and Londoño NESTING OF THE BLACK-THROATED TODY-TYRANT

continuing down the Andean range into Ecuador, Peru, and Bolivia (Hilty and Brown 1986, Clock 2004). Information on breeding biology is limited to records of individuals with enlarged gonads in March through July in Colombia and December in Peru. The species is reported to have a clutch of two eggs, but no further details are provided (Clock 2004). The mating display of this species has been documented in January through August in Ecuador and Colombia (Botero-Delgadillo and Krabbe 2011). But to our knowledge, the nest, incubation behavior, and other aspects of nesting have not been described in the literature. Here, we provide the first description of the nest, eggs, and incubation behavior of H. granadensis, with notes on its mating display. METHODS Study Area.—This study was conducted at three broadly separated field stations located at different elevations in the Farallones de Cali National Park and the Tatama´ National Natural Park in Colombia, and at the Wayqecha station near Manu National Park, Peru. The Farallones research station, Zygia, belongs to the Universidad ICESI, and is located in the Farallones de Cali National Park (38 26 0 32.0 00 N, 768 39 0 48.8 00 W; 2,300 m). The station is located in a humid montane cloud forest interrupted by surrounding smallholder agriculture at the buffer zone and illegal logging at the park edge. During 2015, the mean annual temperature at the study site was 15.138C (min-max ¼ 10.4–33.3) and the total annual precipitation was 1,664 mm. The nest encounter in Colombia occurred during a single nest-searching season, from April to July 2015. The nests monitored in Peru came from seven breeding seasons (2007–2013), from early August until mid-December at the Wayqecha Biological Station (138 10 0 30.1 00 S, 718 35 0 14.0 00 W; 2,900 m), in the Kosñipata Valley, Cusco, Peru, located in the buffer area of Manu National Park. The vegetation is a typical high elevation cloud forest with a canopy height of 10 m. The second Colombian field station in Tatama National Natural Park did not have a nest, but video of courtship behavior was made (T. Forester, pers. comm.). The station is located at the Cerro Montezuma (058 13 0 59.5 00 N, 768 05 0 25.7 00 W), in the Parque Nacional Natural Tatama´, Risaralda, Colombia, on the western slope of the Western

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Cordillera. The area covers an elevation range between 1,200 and 2,600 m. The vegetation is a typical Andean cloud forest with dense epiphytic cover, and during 2015 the mean monthly temperature was 17.0 8C and the annual rainfall was 2,199 mm. Nest Searching.—We conducted daily nest searches, nest searches, 10 hrs a day, 6 days a week at Farallones between May–July and at Wayqecha between August–December. We documented behavior at nests with video and motion sensor cameras (PC85 Rapid-fire professional; Reconyx Inc., Holmen, WI, USA). We used calipers with an accuracy of 0.1 mm to measure the nest, egg, and nestling dimensions. We measured the mass with a 0.05-g digital scale (Flip-Scale F2, Phoenix, AZ, USA). At two of the three nests, we placed motion sensor cameras within 1 m of the nest and camouflaged them with foliage to allow us to monitor nest activity with limited anthropogenic disturbance. Cameras were programmed to take one photo every minute, and 10 photos in rapid succession when motion was detected. Incubation Behavior.—We monitored incubation behavior for two nests with thermocouples attached to U-12 HOBO data loggers (Onset Computer Corporation, Pocasset, MA, USA) that recorded temperatures every minute until the eggs hatched or the nest was inactive. We installed two sensors in each nest, one thermocouple inside the nest and under the egg to measure the internal nest temperature. This allowed us to infer the activity of the incubating female through thermal fluctuation when leaving or returning to the nest. The ambient temperature sensor was attached to the exterior side of the nest (ca. 10 cm). This allowed us to monitor nest microclimate and have a baseline for the thermal fluctuation inside the nest. Temperature fluctuations were used to determine the nest attentiveness (percentage of time in nest during daylight hours of incubation period) and incubation behavior (number and duration of nest absences) of both monomorphic parents (Cooper and Mills 2005, Londoño 2009). To test for normality, we conducted a Wilcoxon signed-rank test and we found that the data were not normally distributed with a bimodal distribution for incubation temperatures (P ¼ ,0.05). Therefore, we used the Mann-Whitney U-test to compare nests. All the statistical analyses were conducted with R (R

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Development Core Team 2013). Mean values are presented as means 6 SD. RESULTS We found and monitored three nests of H. granadensis. Two were found at the Peruvian Wayqecha station (2,900 m) in 2009 and one at the Colombian Farallones station (2,300 m) in 2015. The Colombian nest was discovered during nest construction on 31 May 2015. One infertile egg was laid on 20 June and was incubated until 16 July, 26 days after it had been laid. One of the two Peruvian nests was found with a single developed egg on 1 October 2009. The egg hatched 18 days later on 19 October, however the hatchling was found dead in the nest on 22 October. Photos from the camera trap stationed at the nest did not help us identify the cause of its death. The second Peruvian nest was found with a fully-grown nestling that fledged upon discovery; hence, we could not collect any measurements from this nestling. Nest All three nests were an enclosed ‘‘purse-like’’ pendant pouch inside of a moss ball that hung from a small branch (Fig. 1). The nests’ external measurements were on average (6SD) 102.2 6 13.8 3 64.5 3 194.4 6 46.9 mm (n ¼ 3), length, width and height, respectively. The internal measurements were 64.3 6 35.0 3 35.15 6 14.9 mm (n ¼ 2). The nests were 96 6 55 cm above ground (min-max ¼ 40–150 cm). All three nests were similar in construction but differed in components. The materials of two Peruvian nests were examined in detail but the materials in the Colombian nest were not examined. On average, the masses of the Peruvian nests were 30.72 6 5.77 g. The external layer was made of green and brown moss, bamboo leaves and fibers, and small roots (10.93 6 4.58 g). The internal layer of the two nests were composed of bamboo leaves and fibers, brown moss, and woolly seed coats (18.79 6 11.77 g; n ¼ 2). The Colombian nest differed from the Peruvian nests; the external layer was mostly composed of green moss and the internal cup consisted of small roots and hyphae. The Colombian nest had a thin side entrance placed near the top of the nest at an approximate 458 angle and long pieces of green moss (ca. 104.5 cm)

FIG. 1. Nest of the Black-throated Tody-Tyrant (Hemitriccus granadensis). (A) Nest located in Farallones de Cali National Park, Colombia. (B) Nest located near Manu National Park, Peru.

hanging from the bottom. There were 20 days between finding the Colombian nest in construction on 31 May 2015 and the presence of an egg on 20 June. Eggs We found two nests with eggs, and each had a one-egg clutch. The eggs differed in color and marking patterns (Fig. 2): the Colombian nest contained a tan, unmarked egg (17.8 3 12.3 mm, 1.51 g), and one of the Peruvian nests contained a bright white egg with few red blotches (18.4 3 13.5 mm, 1.60 g) (Fig. 2). The Peruvian egg hatched 19 days after discovery on 19 October. The egg in the Colombian nest was laid on 16 July and did not show any signs of development after 26 days of incubation. Incubation Behavior We monitored incubation behavior during 37.6 days in two nests with thermal sensors, 335.7 hrs


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8C (min-max ¼ 12.6–23.9) in the Colombian nest. Overall, the difference between the inner nest temperature and ambient temperature was higher in the Colombian nest (7.87 6 2.17 8C warmer than ambient temperature) compared to the Peruvian nest (4.79 6 1.47 8C). Nestlings

FIG. 2. Egg and nestling of the Black-throated TodyTyrant (Hemitriccus granadensis): (A) Tan, unmarked egg from nest located in Farallones de Cali National Park, Colombia. (B) White egg with few red blotches from nest located near Manu National Park, Peru. (C) One day old nestling from nest in located near Manu National Park, Peru. (D) The same nestling three days later.

for one Peruvian nest and 567.6 hrs for the Colombian nest. The full incubation period could not be determined because of nest discovery during the incubation phase and an infertile egg, respectively. However, the Peruvian nest was incubated for at least 19 days between discovery and hatching (the 14 days before hatching were monitored using sensors). The percent of time spent on the nest—nest attentiveness—was 77.5% between both nests (75.7% for the Peruvian nest and 78.5% for the Colombian nest) and the daily nest attentiveness varied between nests (Fig. 3A). Foraging trips/off-bouts were only observed during daylight and averaged 23.2 6 5.3 trips per day (min-max ¼ 13–38, n ¼ 37.6 days) (Fig. 3B), which lasted 14.0 6 14.3 mins (min-max ¼ 2–176 mins; n ¼ 886 off-bouts) (Fig. 3C). The length of diurnal on-bouts were slightly longer 15.9 6 7.5 mins (min-max¼ 2–103; n ¼ 827 diurnal onbouts), but differed between the Peruvian (14.0 6 8.8 mins; n ¼ 324 diurnal on-bouts) and Colombian (17.2 6 6.2 mins; n ¼ 503 diurnal on-bouts) nests (P , 0.05). During diurnal incubation, the inner nest temperature in the Peruvian nest averaged 17.27 6 1.54 8C (minmax ¼ 10.64–21.94) and Colombian averaged 23.79 6 1.5 8C (min-max ¼ 14.24–28.77) nests (Fig. 3D). During diurnal foraging trips, inner nest temperature decreased to 14.5 6 1.6 8C (min-max ¼ 9.2–19.2) in the Peruvian nest and to 19.1 6 1.7

We measured the nestling from one nest in Peru in which the nestling died. The single nestling hatched on 19 October 2009, 19 days after the discovery of the nest and egg. The nestling had orange translucent skin with light gray down on its head and back, a white gape, and slightly opened eyes (Fig. 2C, D). Its tarsus and wing measured 5.8 mm and 7.8 mm respectively. On 22 October, the nestling had visible pinfeathers on its head, back, belly, and emerging from the skin on its wings and tail; its tarsus, wing, and tail measured 8.2 mm, 10.7 mm, and 1.2 mm respectively with a mass of 3.91 g. On 25 October, the nestling was found dead inside the nest with no sign of trauma, and no predator was photographed by the camera trap. A second nest of H. granadensis in Peru was discovered with a single, developed nestling on 6 October 2009. Upon discovery and before measurements could be taken, the nestling escaped from the nest and fled by hopping with short bouts of flight while two adults scolded the researcher. He observed that the nestling’s plumage coloration was very similar to the adults except for its shorter tail. The nestling was not measured or photographed. Courtship We observed and video recorded a courtship display of H. granadensis at the Tatama´ field station in Colombia on 14 July 2015 using a Sony CyberShot DSC-HX9V camera (Sony Corp., Tokyo, Japan). The courtship display consisted of the male hovering back and forth in front of a female perched in the middle of canopy near an open area. The male used a perch slightly below the female’s perch during pauses between displays. In the 55-sec video, the duration of hovering displays were consecutively shorter; the first display lasted 8.57 secs and final lasted 1.60 secs (n ¼ 10). Pauses between displays were very short, never more than 0.50 secs (n ¼ 9). During the display, the male made a loud, whirring sound most likely produced by his rapid wing beats. During the tenth display hover,

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FIG. 3. (A) Daily nest attentiveness (the percent of each day an adult is in the nest incubating). (B) Total foraging (offbouts) trips per day. (C) Average length of off-bouts per day. (D) Average inner nest temperature (8C) during diurnal onbouts. The Peruvian nest was monitored for 14 days until its egg hatched; the Colombian egg was infertile and the female incubated it for 24 days.

the male flew out of view, loudly chattering. The video was deposited in the Cornell Laboratory of Ornithology’s Macaulay Library (http:// macaulaylibrary.org, catalog # ML 487218). DISCUSSION We describe for the first time the nest, eggs, incubation behavior, and nestlings of H. granadensis with notes on courtship behavior. We could not describe the full incubation and nestling period because of an infertile egg and nestling mortality. However, we observed 19 days of incubation and six days of the nestling period. The enclosed pendant nest of H. granadensis is similar to most of the known nests in this genus (Clock 2004). While only six species have their nests described in the literature, there are unpublished reports of pendant nests for H. minor (M.

Cohn-Haft in Bencke et al. 2001), H. orbiatus (D. Buzzetti in Bencke et al. 2001), H. zosterops (M. Cohn-Haft in Kirwan and Whittaker 2009), and H. mirande (M. Cohn-Haft in Kirwan and Whittaker 2009). While it is clear that the majority of the members within this genus have the conserved character of purse-like pendant nests, it is intriguing that at least two of the original three Hemitriccus species (H. obsoletus, H. diops, and H. flammulatus; the ‘‘bamboo-tyrants’’ of Ridgely and Tudor [1994]) have atypical nests (Bencke et al. 2001, Clock 2004, Fitzpatrick 2004, Kirwan and Whittaker 2009). These nest architecture discrepancies match with recent phylogenetic analyses that have found the entire genus to be polyphyletic (Tello and Bates 2007, Rheindt et al. 2008). Since nest structure has long been presumed to be a conservative character (von Ihering 1904, Lanyon 1988, Zyskowski and Prum 1999), further published information regarding nest


descriptions is needed in order to provide evidence that could provide new information on the phylogeny of the genus Hemitriccus. Of the three nests we observed, all nests had a clutch/brood size of one egg/nestling. While it is possible that the third Peruvian nest in which the nestling fledged upon discovery could have had an older fledgling that had already left the nest, the other two nests suggest that the species has a clutch of a single egg. This result contrasts with the two egg clutch reported for H. granadensis by J. Fitzpatrick in Clock 2004. Of the tody-tyrants with clutch sizes reported in the literature, only Todirostrum nigriceps produces a single egg per nesting attempt (Walther 2004). However, clutch size has shown to be variable within the tody-tyrants; T. maculatum will lay clutches of 1–2 eggs (Marceliano 1982), and H. margaritaceiventer has a variable clutch of 1–3 eggs (de la Peña 1987, Narosky and Salvador 1998). There were also significant differences in appearance between the two eggs; perhaps because these are different subspecies. There were significant differences in incubation behavior between nests. The Colombian nest experienced fewer, shorter off-bouts, had higher nest attentiveness, and was warmer than the Peruvian nest. Nest attentiveness gradually increased as the incubation period progressed in the Colombian nest, whereas numerous, extended off-bouts caused reduced attentiveness in the Peruvian nest. The combined nest attentiveness (77.5% of the time) is higher than what has been reported for other Neotropical passerines (60%, Auer et al. 2007; and 69% in Martin et al. 2007). The Colombian nest was significantly warmer than the Peruvian nest, possibly because of the difference in latitude, elevation, or ambient temperature. Ambient temperature around the Colombian nest was on average 3.2 8C warmer than the Peruvian nest, which was reflected in the thermal differences between the nest and ambient temperature (7.87 6 2.17 8C for the Colombian nest at 2,300 m compared to 4.79 6 1.47 8C warmed for the Peruvian nest at 2,900 m). While no information has been published within the Hemitriccus genus on incubation period, three tody-tyrant species incubation periods have been described: Southern Bentbill (Oncostoma olivaceum, 19.4 days in Ricklefs and Brawn (2013), Spotted Tody-Flycatcher (Todirostrum maculatum), 16–21 days, (Haverschmidt 1955, Marceliano 1982); and the Common Tody-Flycatcher (Todirostrum cinereum, 17–18 days, (Haversch-

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midt 1978, Lima et al. 2005). This suggests that incubation behavior at the Peruvian nest was monitored during most of its incubation period. Our video-recorded courtship display agrees with Botero-Delgadillo and Krabbe’s (2011) description of short hovering flights with sound produced from the male’s rapid wing beats. However, our observations of the duration of the male’s hovering bouts were much shorter, between 1.5–8.5 secs. The length of each hover significantly declined as the display progressed, which was not included in Botero-Delgadillo and Krabbe’s (2011) summary. There are examples of tyrant flycatchers using wingwhirring during displays, such as the Spectacled Tyrant (Hymenops perspicillatus; Hudson 1920). The closely related Pale-eyed Pygmy-Tyrant (Atalotriccus pilaris) often makes buzzing sounds with rapid wing vibrations that have been presumed to be a part of a display (Clock 2004). Since this courtship behavior has only been documented in H. grandensis and A. pilaris, wing vibration displays could be more common than once thought. We observed the typical elongated pendant pouch nest of Hemitriccus, but documented a different clutch size than what has been reported for the majority of tody-tyrants. There were differences in nest materials, egg appearance, and incubation behavior between the two Peruvian and the single Colombian nest. These differences suggest that further information is required to investigate geographic or phylogenetic differences in H. granadensis (Clock 2004). Additional documentation of breeding biology is needed not just for H. granadensis but for Hemitriccus and tody-tyrants as a whole. ACKNOWLEDGMENTS This study was authorized by the Colombian authorities, Autoridad Nacional de Licencias Ambientales (ANLA, Resolución 509 del 21 de mayo del 2014. 1DB0325) and by permits from the Peruvian government (0239-2013 MINAGRI-DGFFS/DGEFFS 2013). We are especially grateful to C. J. Kingwell and A. O. Quispe for finding and monitoring two of the nests and T. Forrester for recording the courtship display. We want to thank W. Feuerabendt, M. A. L. Muñoz, I. Barragan, S. E. Florez, A. C. Lorenzo, R. P. Garc´ıa for help in the field. We are also grateful to R. P. Garc´ıa for translating data, K. Epperly for assisting with literature review, and M. J. Andersen for providing literature and assisting with manuscript edits. Special thanks to A. Gaffney for substantial assistance with graphs. Finally, we thank parques Naturales Nacionales de Colombia for allowing us to work at Parque Natural Nacional Farallones de Cali and Parque Natural Nacional Tatama´, and

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the SERNAP for giving us permission to work in the buffer zone of Manu National Park. Funding was provided by National Science Foundation Grant DEB-1120682, Louis Agassiz Fuertes Award (Wilson Ornithological Society), Alexander Skutch Award (Association of Field Ornithologists), Alexander Wetmore Award (American Ornithologists’ Union), and the Dexter Fellowships in Tropical Conservation.

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