FRONTISPIECE. Three-striped Warblers (Basileuterus tristriatus) were studied in the northern Andes of Venezuela. Temperate and tropical parulids differ strongly in life histories. Three-striped Warblers have smaller clutches, longer incubation periods, lower nest attentiveness, longer off-bouts, and slower nestling growth rates than most temperate species. Water color by Don Radovich. Published by the Wilson Ornithological Society
VOL. 121, NO. 4 December 2009 PAGES 667–914
The Wilson Journal of Ornithology 121(4):667–678, 2009
BREEDING BIOLOGY OF THE THREE-STRIPED WARBLER IN VENEZUELA: A CONTRAST BETWEEN TROPICAL AND TEMPERATE PARULIDS
W. ANDREW COX1,3 AND THOMAS E. MARTIN2
ABSTRACT.—We document reproductive life history traits of the Three-striped Warbler (Basileuterus tristriatus) from 146 nests in Venezuela and compare our results to data from the literature for other tropical and temperate parulid species. Mean (6 SE) clutch size was 1.96 6 0.03 eggs (n 5 96) and fresh egg mass was 2.09 6 0.02 g. The incubation period was 15.8 6 0.2 days (n 5 23) and the nestling period was 10.5 6 0.3 days (n 5 12). Males did not incubate and rarely provided food for females during incubation. Females had 57 6 2% (n 5 49) nest attentiveness (% of time on the nest incubating), which caused egg temperature to commonly become cold relative to development. Both adults fed nestlings and feeding rates increased with nestling age. The growth rate constant for nestlings based on mass was K 5 0.490, which is slower than for north temperate warblers. Predation was the primary source of nest failure and only 22% of nests were successful based on a Mayfield daily predation rate of 0.048 6 0.006. Our literature review indicates parulids differ strongly in life histories between temperate and tropical/subtropical sites with species in the tropics having, on average, smaller clutches, longer incubation periods, lower nest attentiveness, longer off-bouts, and longer nestling periods. Received 11 October 2008. Accepted 6 June 2009.
Life history strategies often show strong appear to show strong latitudinal patterns in life differences between north temperate versus sub- history traits (Martin et al. 2000, Martin 2002, tropical and tropical sites (Moreau 1944; Lack Auer et al. 2007). The wood-warbler genus 1947; Ricklefs 1976; Martin et al. 2000, 2006, Basileuterus, comprised of 20 species, is a 2007; Martin 2004), although the extent of particularly widespread group distributed from differences varies among phylogenetic groups Argentina to Mexico with records reaching as far (Fierro-Caldero´n and Martin 2007, Martin and north as southern Texas and Arizona (Dunn and Schwabl 2008). Wood-warblers (Parulidae) in- Garrett 1997). One species is endangered (B. clude a diversity of species across latitudes and griseiceps), but most others are common through- out their range and are of low conservation 1 Division of Biological Sciences, University of Missouri, concern (IUCN 2006). Little is known about the 105 Tucker Hall, Columbia, MO 65211, USA. life histories of most species despite their broad 2 USGS, Montana Cooperative Wildlife Research Unit, Avian Studies Program, 205 Natural Science, University of distribution and relative abundance. Basic infor- Montana, Missoula, MT 59812, USA. mation including nest descriptions and clutch size 3 Corresponding author; e-mail: [email protected] is lacking for many species (Curson et al. 1994). 667 668 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 121, No. 4, December 2009
Reproductive traits including incubation period, calculated following Mayfield (1961, 1975) and nest attentiveness, and nestling growth are Hensler and Nichols (1981). Nesting season described for even fewer members of Basileuterus length was estimated as the middle 90% of nest or other parulid genera (but see Skutch 1954, initiations (exclusion of earliest 5% and latest Ghalambor and Martin 2001, Martin 2002, Auer 5%) following Martin (2007). We used video et al. 2007). The dearth of information from the cameras to measure parental behavior for 6–8 hrs Tropics and the suggestion that Wood-warblers starting at dawn during incubation and nestling may show strong latitudinal patterns make them phases. Nest attentiveness (% of time on the nest an important group to study for improving our incubating) was calculated for each nest as the understanding of latitudinal patterns in life history number of minutes on the nest/total minutes traits. video-monitored. We calculated the incubation We describe the reproductive biology of the period as the number of days that lapsed between Three-striped Warbler (B. tristriatus) in northern the day the last egg was laid and when the first Venezuela. This warbler inhabits the understory egg hatched (Briskie and Sealy 1990). We of mature and second growth forests from 800 to calculated the nestling period as the number of 2,700 m elevation in Costa Rica, Panama, and in days that lapsed from when the first egg hatched the Andes from Venezuela to Bolivia (Hilty until the first nestling fledged. 2003). Nest and clutch sizes have been described Egg temperatures (uC) were measured for B. in both Ecuador and Costa Rica (Greeney et al. tristriatus by inserting thermisters on the first or 2005, Jablonski et al. 2006), but no other second day of incubation into the center of one reproductive traits have been documented. We egg in each nest through a small hole sealed with provide detailed data based on 146 nests in a glue (Weathers and Sullivan 1989). The wire was montane cloud forest in Venezuela during 2002– threaded through the nest and connected to a 2006. We also present a review of the current HOBO Stowaway XTI datalogger (Onset Corpo- literature for all parulids and compare our results ration, Bourne, MA, USA) that recorded temper- to other species throughout North, Central, and atures every 12–24 sec for 5–7 days per nest South America. (Martin et al. 2007, Martin and Schwabl 2008). Ambient temperatures were measured over the METHODS same periods using a shaded probe near the nest. We searched for nests from March to July, We also measured egg temperatures for Red-faced 2002–2006, in Yacambu´ National Park in Lara, Warblers (Cardellina rubrifrons) in northern Venezuela (09u 429 N, 69u 429 W). This moun- Arizona using the same methodology (Martin et tainous park on the northernmost edge of the al. 2007). Andes is characterized by second growth and We searched the literature for life-history data mature tropical forest. The park ranges from 500 for all species in the Parulidae with which to to 2,200 m and our field sites occurred from 1,350 compare our results. We first consulted The Birds to 2,000 m elevation. We located nests via of North America data base (Poole 2005) and systematic and behavioral searches, and moni- supplemented these data with those from other tored them every 2–4 days, except at stage- literature. We calculated weighted means for changing events (laying, hatching, fledging) when clutch sizes, incubation periods (days), and we monitored nests daily or twice daily (Martin nestling periods (days) when multiple mean and Geupel 1993). Nest, egg, and nestling values and sample sizes were provided, or when measurements, and behavioral data were collected only raw data were available. We recorded a following Martin et al. (2000, 2006, 2007) and range of values when means could not be reliably Fierro-Caldero´n and Martin (2007). We measured calculated; these were excluded from analyses egg mass (g) and nestling growth using ACCU- when we compared temperate and tropical/ LAB (Elk Grove, IL, USA) portable electronic subtropical species. scales with an accuracy of 60.001 g during early Statistical Analysis.—Means are reported with incubation (days 0–2) for egg mass and every 61 standard error (SE) for all data and sample other day (starting on day 0 or 1) for nestling sizes reflect numbers of nests sampled. We used growth. Growth rates for non-experimental nests SPSS Version 15.0 (2006) for all statistical tests. were calculated following Remesˇ and Martin We used analysis of variance (ANOVA) to test for (2002), and nest predation and survival rates were temporal changes in nest attentiveness (% time on Cox and Martin N BREEDING BIOLOGY OF A TROPICAL WARBLER 669
FIG. 1. Temporal distribution of nest initiation dates (date the first egg is laid in a nest) for the Three-striped Warbler among weekly (7 day) intervals. the nest) and mean on- and off bouts during from 8 March to 25 June across years (Fig. 1). incubation by separating the stage into three Nests were usually initiated after 10 April (n 5 categories (early, 2–3 days; middle, 5–7 days; 103), although three nests were initiated in March; late, 12–14 days). We used least-significant two of these were from the same individual in difference tests (LSD) to conduct post hoc tests consecutive years based on color-banding. The when ANOVA results were significant (a # 0.05). median date of nest initiations was 16 May (Fig. 1). We used linear regression to test for relationships The nesting season lasted 68 days (Fig. 1). between temporal changes in parental behavior Eggs were white with irregular brown spots. during the nesting stage (e.g., brooding effort, Fresh egg mass (measured between day 0 and day feeding rates). We examined distributions of life- 2 of incubation) was 2.09 6 0.02 g (n 5 90), history trait data for temperate and subtropical/ which represented 17.7% of adult female body tropical warblers using a Shapiro-Wilks test. One mass (11.80 6 0.18 g, n 5 33). Five of 96 or both of the distributions departed from clutches had one egg (5%), one had three eggs normality for most life-history traits, so we used (1%), and the rest had two eggs (94%), yielding non-parametric Mann-Whitney U-tests to test for an average clutch size of 1.96 6 0.03 eggs. differences in life-history traits between temperate Incubation Period.—The incubation period and subtropical/tropical warblers (Zar 2010). averaged 15.8 6 0.2 days (n 5 23) and was longer than for north temperate parulids, which RESULTS averaged 12.2 6 0.1 days (n 5 32 species; Nest and Eggs.—We found 146 nests in 5 years Table 1). Males did not incubate and rarely of field work. Three-striped Warblers build a provided food for incubating females, averaging small, domed nest with a side entrance. The inside 0.03 6 0.02 trips to the nest/hr (n 5 29) during of the cup measured 5.08 6 0.08 cm in diameter early incubation (days 2–4) and 0.06 6 0.04 trips/ and 3.38 6 0.10 cm in height, while the outside hr (n 5 14) during late incubation (days 11–16). diameter and height averaged 11.46 6 0.38 cm Nest attentiveness averaged 57 6 2% (n 5 49) and 7.29 6 0.35 cm, respectively. Nests were on and was slightly lower than for other tropical the ground (n 5 146) on a steep slope or bank, parulids, which averaged 64 6 1% for 15 species. built into leaf litter or under the base of saplings Nest attentiveness was much lower than for north and small trees. Nests were frequently placed in temperate parulids, which averaged 77 6 1% (n the forest interior but some were built into 5 31 species, Table 1). Attentiveness changed exposed roadside banks, culverts, and drainages. over the incubation period for the Three-striped Dates of nest initiation (i.e., first egg laid) ranged Warbler (ANOVA, F2,46 5 6.4, P 5 0.004); nest 670 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 121, No. 4, December 2009
TABLE 1. Reproductive traits of temperate and tropical parulids. Only species with data available for multiple life-history traits are included.
Mean Mean Nest Mean Mean Mean Nestling clutch incubation attentiveness on-bout off-bout Mate nestling growth Species size period (days) (%) duration (min) duration (min) feed? period (days) rate (K) Referencesa Temperate species Blue-winged Warbler (Vermivora pinus) 4.37 10–11 Y 9.3 0.559 1, 2 Golden-winged Warbler (V. chrysoptera) 5.00 10–12 9–10 1, 2, 4 Tennessee Warbler (V. peregrina) 5.59 7–8 Y 0.654 1, 3, 5 Orange-crowned Warbler (V. celata) 4.54 12.6 80 49 12 11.3 1, 6, 7, 8 Nashville Warbler (V. ruficapilla) 4.71 11–12 73 39 14 Y 9–11 1, 6, 9 Virginia’s Warbler (V. virginiae) 3.57 12.3 73 31 11 Y 11.4 1, 7, 8 Northern Parula (Parula americana) 3.94 12.5 79 21 6 Y 10–11 1, 6, 10 Yellow Warbler (Dendroica petechia) 4.08 11.3 78 36 10 Y 8.4 0.579 1, 3, 6 Chestnut-sided Warbler (D. pensylvanica) 3.88 11.0 75 23 7 Y 10–11 1, 6, 11, 12 Magnolia Warbler (D. magnolia) 3.96 12.0 70 17 7 8–10 1, 13 Black-throated Blue Warbler (D. caerulescens) 3.80 13.0 72 31 12 Y 8.6 0.647 1, 2, 6, 14 Yellow-rumped Warbler (D. coronata) 3.86 12.8 77 25 7.4 Y 12.6 15 Golden-cheeked Warbler (D. chrysoparia) 3.90 12.1 74 37 13 Y 10.5 1, 16 Black-throated Green Warbler (D. virens) 3–5 12.0 78 50 15 10.0 0.736 1, 3, 6 Townsend’s Warbler (D. townsendi) 5.70 12.5 9.9 17 Blackburnian Warbler (D. fusca) 3–5 72 21 8 Y 1, 6 Yellow-throated Warbler (D. dominica) 3–5 12.0 1 Grace’s Warbler (D. graciae) 3.20 10–12 Y 1 Kirtland’s Warbler (D. kirtlandii) 4.63 14.2 82 51 11 Y 9.4 0.547 1, 3, 6 Prairie Warbler (D. discolor) 3.92 12.0 77 55 15 Y 9.6 0.507 1, 3, 6 Palm Warbler (D. palmarum) 4.59 12.0 Y 12.0 1 Bay-breasted Warbler 1, 6, 18, (D. castanea) 5.43 12–13 80 18 5 Y 10.5 19, 20 Blackpoll Warbler (D. striata) 4.32 11.5–12 77 19 6 Y 9.5 0.538 1, 6 Cerulean Warbler (D. cerulea) 3.60 11.4 83 50 10 Y 10.4 1, 21 Black-and-white Warbler (Mniotilta varia) 4–6 10–12 Y 8–12 1 Cox and Martin N BREEDING BIOLOGY OF A TROPICAL WARBLER 671
TABLE 1. Continued.
Mean Mean Nest Mean Mean Mean Nestling clutch incubation attentiveness on-bout off-bout Mate nestling growth Species size period (days) (%) duration (min) duration (min) feed? period (days) rate (K) Referencesa American Redstart (Setophaga ruticilla) 3.89 10–13 82 23 5 Y 7–9 0.613 1, 3, 6 Prothonotary Warbler (Protonotaria citrea) 4.55 12.5 56 18 14 Y 10.0 0.654 1, 3 Worm-eating Warbler (Helmitheros vermivorum) 4.82 13.0 Y 9.0 1 Swainson’s Warbler (Limnothlypis swainsonii) 3.22 13.9 78 59 16 Y 9.9 1, 6, 22 Ovenbird (Seiurus aurocapilla) 4.31 12.2 85 110 19 Y 7.9 0.473 1, 3, 6 Northern Waterthrush (S. noveboracensis) 4.11 12.0 75 30 10 Y 9.0 1, 3, 6, 23 Louisiana Waterthrush 1, 3, 6, 24, (S. motacilla) 5.00 12.7 79 35 9 Y 10.8 0.590 25 Kentucky Warbler (Oporornis formosus) 4.12 11.0 Y 8.4–9.5 0.680 1, 6, 26 Mourning Warbler (O. philadelphia) 3.71 12.0 75 39 13 Y 8.0 1, 6, 27 MacGillivray’s Warbler (O. tolmiei) 4.12 12.5 77 22 8.5 Y 10.4 1, 8, 15 Common Yellowthroat (Geothlypis trichas) 3.99 12.0 80 49 16 Y 9.8 0.537 1, 3, 6 Hooded Warbler (Wilsonia citrina) 3.61 11.0 60 8–9 1 Wilson’s Warbler (W. pusilla) 4.11 11.9 81 22 5 Y 10.2 1, 6 Canada Warbler (W. canadensis) 4.37 12.0 85 32 7 Y 1 Red-faced Warbler (Cardellina rubrifrons) 4.16 12.8 75 37.4 10.5 Y 11.1 1, 7, 8, 28 Painted Redstart (Myioborus pictus) 3.15 13.2 75 Y 13.0 0.557 1, 3, 29 Yellow-breasted Chat (Icteria virens) 3.68 11.6 74 45 15 Y 8.9 1 Subtropical and tropical species Colima Warbler (Vermivora crissalis) 3–4 12.0 11.0 1 Flame-throated Warbler (Parula gutturalis) 2.00 16.0 61 27 17 13.0 30, 31 Crescent-chested Warbler (P. superciliosa) 2–3 13+ 68 20 10 30, 32 Tropical Parula (P. pitiayumi) 3.14 13.0 32, 33 Adelaide’s Warbler (Dendroica adelaidae) 2–3 50 26 34, 35 Masked Yellowthroat (Geothlypis aequinoctialis) 3.10 13.3 61 22.5 17.7 9.7 8, 36, 37 Grey-crowned Yellowthroat (G. poliocephala) 2.70 12.8 11.0 38 672 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 121, No. 4, December 2009
TABLE 1. Continued.
Mean Mean Nest Mean Mean Mean Nestling clutch incubation attentiveness on-bout off-bout Mate nestling growth Species size period (days) (%) duration (min) duration (min) feed? period (days) rate (K) Referencesa Red Warbler (Ergaticus ruber) 3.00 16.0 66 10–11 39 Pink-headed Warbler (E. versicolor) 2–4 16.0 71 20.0 8.0 Y 10–11 30, 31 Slate-throated Redstart (Myioborus miniatus) 2.72 14.4 67 37.6 18.2 11.8 0.522 40, 41, 42 Brown-capped Redstart 8, 30, 36, (M. brunniceps) 2.60 16.6 67 33.1 17.4 Y 12.6 37 Collared Redstart (M. torquatus) 2.50 15.0 74 28.5 9.8 13.0 40 Two-banded Warbler (Basileuterus bivittatus) 3.00 14.8 62 46.1 22.6 Y 10.9 8, 36, 37 Pale-legged Warbler (B. signatus) 2.60 16.6 65 30.3 16.5 Y 12.5 8, 36, 37 Golden-crowned Warbler (B. culicivorus) 2–4 62 44.0 26.0 10+ 32 Rufous-capped Warbler (B. rufifrons) 2–4 66 44.0 23.0 12.0 32 Black-cheeked Warbler (B. melanogenys) 2.00 62 29.0 18.0 32 Three-striped Warbler (B. tristriatus) 1.96 15.8 57 45.7 35.0 Y 10.5 0.490 43 Buff-rumped Warbler (Phaeothlypis fulvicauda) 2.00 16–19 68–74 Y 12–15 31 Wrenthrush (Zeledonia coronata) 2.00 17+ 30, 44 Red-breasted Chat (Granatellus venustus) 2–4 14.0 45, 46
a 1. Poole (2005), 2. Remesˇ (2006), 3. Remesˇ and Martin (2002), 4. Canterbury (1990), 5. Holmes and Nixon (2000), 6. Conway and Martin (2000), 7. Palacios and Martin (2006), 8. Martin (2002), 9. Knapton (1984), 10. Graber and Graber (1951), 11. Lawrence (1948), 12. Tate (1970), 13. Nice (1926), 14. Holmes et al. (1992), 15. Martin unpubl. data, 16. Jennifer Reidy (pers. comm.) 17. Matsuoka et al. (1997), 18. Harrison (1984), 19. MacArthur (1958), 20. Mendall (1937), 21. Oliarnyk and Robertson (1996), 22. Thompson (2005), 23. Peck and James (1987), 24. Eaton (1958), 25. Robinson (1987), 26. Vicki McDonald (pers. comm.), 27. Cox (1958), 28. Martin (1995), 29. Marshall and Balda (1974), 30. Curson et al. (1994), 31. Skutch (1954), 32. Skutch (1967), 33. Di Giacomo (2005), 34. Bond (1930), 35. Spaulding (1937), 36. Auer et al. (2007), 37. Martin et al. (2000), 38. Martinez et al. (2004), 39. Elliott (1969), 40. Skutch (1945), 41. Ewert (1975), 42. Collins and Ryan (1994), 43. This study, 44. Hunt (1971), 45. Vega Rivera et al. (2004), 46. Grant (1964). attentiveness during early incubation was similar 12 species) for temperate and tropical species, (LSD, P 5 0.70) to the middle period, and both respectively. These long off-bouts caused egg were less (LSD, P 5 0.026) than during late temperatures of Three-striped Warblers to reach incubation (Fig. 2A). This change was caused by cold levels relative to development (Fig. 3). In a dramatic reduction in length of off-bouts over contrast, the Red-faced Warbler, a north temper- the incubation period (ANOVA, F2,46 5 7.1, P 5 ate relative, kept egg temperatures higher despite 0.002; Fig. 2B). On-bout duration showed a much colder ambient temperatures (Fig. 3). Egg marginal decline in late incubation (ANOVA, temperature of the Three-striped Warbler aver- F2,46 5 2.7, P 5 0.081, Fig. 2B). aged 33.93 6 0.47u C over 24-hr periods from Both on- and off-bouts were relatively long for 27 days of sampling across seven nests (with an the Three-striped Warbler. On-bouts averaged overall mean taken from means of each nest), 45.7 6 2.5 min (n 5 49) (Fig. 2B), but averaged while the mean temperature for the Red-faced 37.2 6 3.4 min (n 5 31 species) and 31.4 6 Warbler was 35.75 6 0.18u C(n 5 3 nests, 2.5 min (n 5 13 species) for temperate and 7 days). tropical species, respectively. Off-bouts averaged Nestling Period.—The nestling period was 10.5 35.0 6 3.1 min (n 5 49) (Fig. 2B), and 10.6 6 6 0.3 days (n 5 12). This period length was 0.7 min (n 5 30 species) and 17.0 6 1.6 min (n 5 similar to north temperate relatives, which Cox and Martin N BREEDING BIOLOGY OF A TROPICAL WARBLER 673
Nest Survival.—Twenty of 146 nests were abandoned before the nest was finished being built or an egg was laid and did not contribute to nest survival analyses. Another 18 nests were excluded because of effects by researcher activ- ities. Twenty-four of the remaining 108 nests fledged young, 18 were still active when moni- toring was discontinued at the end of the season, and 66 failed yielding a total of 1,258.5 days of exposure. Predation was the source of failure for 60 of the 66 failed nests with the remaining six nests failing due to weather, abandonment, or unknown reasons. The overall daily predation rate was 0.048 6 0.006, and the total daily survival rate was 0.948 6 0.006. Daily predation rates were 0.027 6 0.019, 0.042 6 0.007, and 0.070 6 0.015 during egg-laying, incubation, and nestling stages, respectively. The overall nest success based on a total nesting period of 28 days was 22%. Subtropical/Tropical vs. Temperate Species.— Differences between the Three-striped Warbler and temperate species paralleled trends observed from available data for other tropical/subtropical FIG. 2. Average (A) nest attentiveness, and (B) on- and and temperate parulids (Table 1). Clutch size for off-bout durations across three periods of incubation for the tropical parulids averaged 2.53 6 0.12 eggs (n 5 Three-striped Warbler: early (days 2–4), middle (days 5–9), 14), which was lower than the mean clutch size of and late (days 11–16). Sample sizes reflect numbers of nests. 4.20 6 0.10 eggs (n 5 38) for temperate species (U 5 0, P , 0.001). Mean incubation period for tropical warblers was 14.9 6 0.4 days (n 5 13), averaged 10.0 6 0.2 days (n 5 28 species), but which was longer than the mean period of 12.2 6 less than for other tropical species which averaged 0.1 days (n 5 32) for temperate species (U 5 29, 11.9 6 0.3 days (n 5 11 species; Table 1). The P , 0.001). Females of tropical species had lower amount of time that females spent brooding nest attentiveness during incubation (64 6 1%, n nestlings declined (r 520.91, P , 0.001) with 5 15) than temperate species (77 6 1%, n 5 31) age of nestlings (Fig. 4A). Both males and (U 5 21, P , 0.001). This was a result of off- females provisioned nestlings, and rate of visits bouts that averaged 18.4 6 2.0 min (n 5 13), to the nest to feed young increased with nestling which was longer than the mean value of 10.6 6 age (r 5 0.87, P , 0.001; Fig. 4B). Nestlings 0.7 min (n 5 30) for temperate species (U 5 61, weighed 1.70 6 0.07 g (n 5 8) on hatch day and P , 0.001). Mean on-bouts averaged 32.4 6 11.50 6 1.01 g (n 5 9) when the eighth primary 2.5 min (n 5 14) for subtropical/tropical species, feather broke its sheath (i.e., pin break) between similar to the mean value of 37.2 6 3.4 min (n 5 days 6 and 8. Growth rate constant (K) for the 31) for temperate species (U 5 192, P 5 0.54). nestling period based on nestling mass (Fig. 5A) The mean nestling period for subtropical/tropical was greater than when based on tarsus (Fig. 5B), species was 11.8 6 0.3 days (n 5 12), which was and resulted in an estimated asymptote of 13.50 6 longer than the mean value of 10.1 6 0.2 days (n 0.47 g, which was higher than mean mass for 5 28) for temperate species (U 5 53.5, P 5 adult females (11.80 6 0.18 g, n 5 33). The 0.001). The mean growth rate based on mass (K 5 growth rate based on mass (K 5 0.490 6 0.030) 0.506 6 0.016, n 5 2) for tropical species was was slower than for north temperate parulids, marginally different from the mean value (K 5 which averaged K 5 0.591 6 0.018 (n 5 15 0.591 6 0.018, n 5 15) for temperate species (U species; Table 1). 5 3, P 5 0.073). 674 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 121, No. 4, December 2009
FIG. 3. Representative examples of egg temperature fluctuations over days 3 and 4 of incubation in comparisons of the Three-striped Warbler with a north temperate relative, the Red-faced Warbler. The two dashed lines at the top of each cell represent the optimum temperature zone for development (White and Kinney 1974, Webb 1987). The ambient temperature range over the sampling period is shown in each cell.
DISCUSSION The mean incubation period for the Three- The domed ground nests of the Three-striped striped Warbler was typical of tropical parulids Warbler we found in Venezuela were structurally and longer than temperate breeding species, as has similar to those reported in other locations been generally observed (Ricklefs 1969, Martin (Greeney et al. 2005, Jablonski et al. 2006) and 2002, Martin et al. 2007, Martin and Schwabl those built by other members of the genus (Marini 2008). The longer incubation period of the Three- and Cavalcanti 1994, Auer et al. 2007). The dome striped Warbler compared to temperate species can reduce predation risk by making its contents was associated with lower nest attentiveness and less visible (Collias and Collias 1984, Auer et al. longer off-bouts that yielded cooler incubation 2007). Domes may also protect nests from temperatures, as seen for other tropical birds weather in the tropics where heavy rains are (Chalfoun and Martin 2007, Martin et al. 2007, common throughout most of the breeding season Martin and Schwabl 2008). Temperatures de- (Skutch 1967, Snow 1978, Collias and Collias creased to levels sufficiently low to slow devel- 1984). opment (White and Kinney 1974, Webb 1987), Three-striped Warblers had low variation in which explains part of this latitudinal trend clutch size with 94% of all nests containing two (Martin 2002, Martin et al. 2007, Martin and eggs and no nest containing more than three eggs. Schwabl 2008). Nest attentiveness during incuba- The only nest from Costa Rica that has been tion for the Three-striped Warbler was typical of described contained three nestlings (Jablonski et other tropical warblers but on- and off-bouts were al. 2006), which may indicate geographic varia- considerably longer than for other species. This tion in clutch size. Warblers at our site had a might reflect a response to high nest predation smaller clutch size than reported for congeners risk; daily predation rate at our site in Venezuela and other parulids in the Tropics and subtropics, was higher than for related species in Argentina and a much smaller clutch size than north (Martin et al. 2000, Auer et al. 2007) or Arizona temperate relatives (Table 1, also see Martin (Martin 2002). Higher predation risk can favor 1988), reflecting the well-known latitudinal gra- longer bouts to reduce the numbers of trips to the dient (Moreau 1944; Martin et al. 2000, 2006). nest (Weathers and Sullivan 1989, Conway and Cox and Martin N BREEDING BIOLOGY OF A TROPICAL WARBLER 675
FIG. 4. Scatter plots of change with nestling age in (A) female Three-striped Warbler brooding behavior (% time spent brooding) and (B) rates that parents visit the nest to provision nestlings (n 5 14 nests).
Martin 2000, Martin et al. 2000). Alternatively, Alternatively, the short nestling period may be a longer bouts might reflect greater food limitation proximate response to greater food availability and females may require long off-bouts for self- relative to brood size. Adults with one of the maintenance (Conway and Martin 2000, Chalfoun smallest average clutch sizes among tropical and Martin 2007). parulids may more easily be able to feed young The nestling period for all tropical parulids at rates adequate for faster growth and earlier spans from as few as 9 days for Masked maturity. Young fledged at a mass that exceeded Yellowthroat (Geothlypis aequinoctialis)toat adults. The generality of this result is difficult to least 17 days for Wrenthrush (Zeledonia coro- assess because growth rates and fledging size for nata) with the Three-striped Warbler’s nestling other tropical parulid species are almost entirely period ,1.4 days shorter than the mean nestling lacking. The growth rate for the Three-striped period for other tropical species. This may be Warbler was slower than that of all temperate related to high nest predation rates; nestling warblers for which data are available except the periods and mortality rates are often negatively Ovenbird (Seiurus aurocapilla). The slower correlated (Lack 1968, Remesˇ and Martin 2002). growth of tropical than temperate birds was noted 676 THE WILSON JOURNAL OF ORNITHOLOGY N Vol. 121, No. 4, December 2009
al. 2007). The lengthy breeding season did not result in substantially more breeding attempts than in other parulids. Some breeding pairs renested four times following nest failure (WAC, pers. obs.), but north temperate parulids may also renest four times or more (Grzybowski and Pease 2005, Murray and Nolan 2007). More detailed observa- tions on individual pairs of tropical parulid species throughout the breeding season are needed to improve our understanding of how high predation rates and breeding season length affect annual fecundity. The Parulidae include 115 species (AOU 1998). Much attention has been placed on the ecology and evolution of species in North America, but strikingly few data are available for species in Central and South America where the majority of parulid species reside (48 tropical and subtropical species are not included in Table 1 due to lack of available information). The Three-striped Warbler had a smaller clutch, longer incubation period, lower nest attentiveness, longer off-bouts, and a slower growth rate than its temperate relatives. Improving data collection efforts outside of North America will lead to a better understanding of FIG. 5. Relationships of (A) mass, and (B) tarsus length tropical strategies and allow for more robust plotted against age for Three-striped Warblers and their comparisons of latitudinal patterns. estimated growth rates (K) and asymptotes (A). The dashed lines represent the (A) mean mass and (B) mean tarsus ACKNOWLEDGMENTS lengths of adults (n 5 135). This study was made possible in part by support under NSF grants DEB-9981527, DEB-0543178, and DEB- by Ricklefs (1976) long ago, although compari- 0841764 to T. E. Martin. Permit numbers are DM/ sons of related species in both areas have 0000237 from FONACIT, PA-INP-005-2004 from INPAR- remained rare. QUES, and 01-03-03-1147 from Ministerio del Ambiente. We thank Carlos Bosque for substantial aid in obtaining Only two other studies we found provided data permits for this work, Karie Decker for statistical help, and on nest predation rates for tropical parulids. The Allison Cox and Robin Hirsch-Jacobson for their comments overall daily predation rate was relatively high for on earlier drafts of this manuscript. Three-striped Warblers at our field site with an estimated nest success rate of only 22%. This was LITERATURE CITED higher than for any parulid at the Argentina site AMERICAN ORNITHOLOGISTS’UNION (AOU). 1998. Check- (Auer et al. 2007) and for the Buff-rumped list of North American birds. Seventh Edition. Warbler (Phaeothlypis fulvicauda) in Costa Rica American Ornithologists’ Union, Washington D.C., (Skutch 1985). A high predation rate may make it USA. difficult for adults to breed successfully in a given AUER, S. K., R. D. BASSAR,J.J.FONTAINE, AND T. E. MARTIN. 2007. Breeding biology of songbirds in a year in addition to its potential to influence clutch subtropical montane forest in northwestern Argentina. size, nest attentiveness, and nestling periods. A Condor 109:321–333. species with low nest success could compensate BOND, J. 1930. The resident West Indian warblers of the by increasing the length of its breeding season. genus Dendroica. Proceedings of the Academy of The breeding season of the Three-striped Warbler Natural Sciences 82:329–337. was about twice the length of seasons for parulids BRISKIE,J.V.AND S. G. SEALY. 1990. Evolution of short incubation periods in the parasitic cowbirds Molothrus in Arizona (Martin 2007), but it only nested about spp. Auk 107:789–793. 10 days longer than related species in Argentina CANTERBURY, R. A. 1990. Breeding ecology of the Golden- that had much lower nest predation rates (Auer et winged Warbler (Vermivora chrysoptera) in Raleigh Cox and Martin N BREEDING BIOLOGY OF A TROPICAL WARBLER 677
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