Latitudinal differences in the breeding phenology of Grey Warblers

CSIRO PUBLISHING

Emu, 2013, 113, 187–191

Short Communication

http://dx.doi.org/10.1071/MU12086

Latitudinal differences in the breeding phenology of Grey Warblers covary with the prevalence of parasitism by Shining Bronze-Cuckoos Michael G. Anderson A,E, Brian J. Gill B, James V. Briskie C, Dianne H. Brunton A and Mark E. Hauber D A

Ecology, Behaviour and Conservation Group, Institute of Natural and Mathematical Sciences, Massey University, Albany Campus, Private Bag 102-904, North Shore Mail Centre, Auckland, New Zealand. B Auckland War Memorial Museum, Private Bag 92018, Auckland, New Zealand. C School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand. D Department of Psychology, Hunter College and the Graduate Center of the City University of New York, New York, NY 10065, USA. E Corresponding author. Email: [email protected]

Abstract. Variation in the temporal patterns of nest availability through the breeding season or across the geographical range of a host is expected to be an important selection pressure shaping the breeding biology of avian brood parasites. The archipelago-wide distribution of the endemic Grey Warbler (Gerygone igata) in New Zealand, and its parasitism by the specialist Shining Bronze-Cuckoo (Chalcites lucidus), makes this a valuable system in which to study small-scale latitudinal gradients in host breeding phenology and the effects of these on the prevalence of brood parasitism. Nest records from throughout New Zealand and our study sites on both the North and South Islands indicated that, as expected, clutch-sizes were larger at higher, more southern, latitudes. Contrary to predictions, breeding began later and finished earlier, and usually involved only one brood on the North Island, compared with a longer breeding season with two broods on the South Island. Prevalence of brood parasitism covaried positively with latitude, suggesting that geographical patterns in breeding phenology of hosts may influence the prevalence of parasitism. Additional Keywords: breeding biology, brood parasitism, Chalcites lucidus, clutch-size, Gerygone igata, latitude. Received 24 January 2012, accepted 29 January 2013, published online 7 May 2013

Introduction In most birds, the timing and duration of breeding are affected by a variety of ecological factors, such as the availability of food and temperature. Birds adapt to these factors by altering their breeding phenology to optimise the quality and number of offspring they produce over their lifetime (Lack 1947; Jetz et al. 2008). However, avian obligate brood parasites are completely dependent on the availability of host nests, and the timing of their breeding is dictated and constrained by the breeding activity of their hosts (Møller et al. 2011). Many birds show latitudinal or altitudinal clines in breeding traits, including variation among populations of the same species (Jetz et al. 2008). This can be the result of either phenotypic flexibility or genotypic differences in reproductive traits, leading to individuals optimising the onset, duration and extent of their reproductive efforts (Ricklefs and Wikelski 2002; Sheldon et al. 2007). Many other factors can play a role in influencing fine-scale variation in breeding traits, including the availability of foraging and breeding resources, rates of predation (Zanette et al. 2006) and even the perceived risk of predation (Zanette et al. 2011). The Journal compilation
BirdLife Australia 2013

resulting variation in the timing and investment of host breeding can lead to changes in the timing of availability of nests, clutch-size and the frequency of breeding, placing geographically variable selection pressures on brood parasites across different regions (Soler et al. 1995; Strausberger 1998). For hosts of obligate brood parasites, theoretical and empirical work have also uncovered complex patterns of host maternal investment in clutch-size and number of breeding attempts in response to greater prevalence of brood parasitism (Hauber 2003; Cunningham and Lewis 2005). This can lead to apparent mismatches between the timing of breeding of hosts and parasites as each party evolves adaptations and counter-adaptations to increase their reproductive success. More recently, anthropogenic effects, such as climate change, have been implicated in altering the onset of breeding in many long-distance migratory brood parasites relative to their hosts (Saino et al. 2009). Here we examine intraspecific variation in breeding phenology with latitude in a temperate-zone southern hemisphere non-migratory passerine host, the Grey Warbler (Gerygone igata), and its specialist migratory brood parasite, the Shining www.publish.csiro.au/journals/emu

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Bronze-Cuckoo (Chalcites lucidus). In New Zealand (excluding the Chatham Islands), Shining Bronze-Cuckoos parasitise only the endemic Grey Warbler (Gill 1983a). There has been no previous study of latitudinal variation of breeding traits in any native New Zealand passerine, even though the archipelago’s main islands stretch over 1400 km from north to south. We also examined whether and how prevalence of brood parasitism covaried with latitude and with breeding phenology of the Warbler. We predicted that the initiation of breeding should be earlier at lower, more northern, latitudes, clutch-size should increase with increasing latitude, and that fewer opportunities for parasitism caused by variation in host breeding phenology should result in a reduction in the prevalence of brood parasitism. Materials and methods Data on the breeding phenology of Grey Warblers were compiled from four sources. We used data collated from three of our field studies, which were conducted at two sites. One of the sites was Tawharanui Regional Park, near Auckland, North Island (36
220 S, 174
500 E; herein referred to as the Northern Site), where Grey Warblers were monitored from 2005 to 2008 (Anderson et al. 2010). The second site was at Kowhai Bush, near Kaikoura, South Island (42
220 S, 173
350 E; herein referred to as the Southern Site). Grey Warblers were studied there from 1976 to 1979 (Southern Site 1; Gill 1982a) and from 2001 to 2007 (Southern Site 2; Massaro et al. 2008). At the Northern Site, searches for nests began on 1 August each year, and at Southern Site 1 searches began in late July. Nest searching ceased shortly after nest-building stopped, which was early December at both sites. Monitoring at Southern Site 2 was part of a more general study, and searches for nests were conducted only from August to mid-December. The two studies at the Southern Site were treated separately in our analysis given the difference in the years of coverage and the shorter seasonal sampling period in the second study. The fourth source of information was the Nest Record Scheme of the Ornithological Society of New Zealand (OSNZ) for the period 1934–98. These data have been collected by volunteers, independently of the hypotheses tested here, over a period of several decades across multiple locations throughout New Zealand (median latitude, 40
590 S; range, 35
030 –45
020 S). We included only those records for which clutch-size was known to be complete as confirmed by visits separated by 2 or more days (i.e. the inter-egg laying interval of Grey Warblers; Gill 1982a); of 104 records, clutch-size could be accurately determined for only 66 nests (45 nests on the North Island; 21 on the South Island). From each set of nest records, we extracted information on clutch-size, laying date of each egg in the clutch, and whether or not the nest was parasitised. To establish the timing of breeding, the laying dates of all eggs were grouped into weekly intervals. For breeding season date, we used the date of the first recorded egg being laid at the study site as Day 0. Dates were obtained from multiple visits to nests during the laying period or by determining key events, such as hatching dates or fledging dates, and backdating to estimate the laying dates of each egg by using the laying interval (2 days), average duration of the incubation period (20 days) and nestling period (17 days) (Gill 1982a). These data are from Southern Site 1 and may differ between sites, but this is not known from the published literature. The length of the

M. G. Anderson et al.

breeding season at Southern Site 2 could not be calculated as observations began after the start of breeding and ended before it was completed. We tested the covariation of laying date and latitude on host clutch-size (OSNZ data), compared clutch-sizes between the two studies at the Southern Site and the Northern Site, and analysed seasonal and latitudinal patterns of brood parasitism prevalence using non-parametric or logistic analyses. Statistical tests were carried out using SPSS v.15.0 (SPSS Inc., Chicago, IL, USA). Results Geographical variation in clutch-size The clutch-size of Grey Warblers varied from two to five eggs. Clutch-size varied significantly between the Northern Site and the two study periods at the Southern Site (Kruskal–Wallis: c2 = 83.3, d.f. = 2, P < 0.001; pairwise comparisons: Northern Site v. Southern Site 1, c2 = 42.8, P < 0.001; Northern Site v. Southern Site 2, c2 = 66.7, P < 0.001; Southern Site 1 v. Southern Site 2, c2 = 23.9, P = 0.01). Clutch-size was smallest at the Northern Site (n = 57 clutches, median 3 eggs, range 2–4; proportion of clutches: C/2, 10.5%; C/3, 84.2%; C/4, 5.3%), relative to either of the studies at the Southern Site. Clutch-size also decreased between Southern Site 1 (n = 59, 4, 3–5; C/3, 8.5%, C/4, 89.8%, C/5, 1.7%) and Southern Site 2 (n = 38, 4, 2–5, C/2, 5.3%, C/3, 34.2%, C/4, 57.9%, C/5, 2.6%) (Mann–Whitney U-test: Z97 = –3.15, P = 0.001), although this result may reflect differences in search effort for nests between the two studies. When only known first clutches were considered (those before 23 October at the Southern Site and 5 November at the Northern Site), these differences in clutch-size remained significant (Kruskal–Wallis: c2 = 76.93, d.f. = 2, P < 0.001; pairwise comparisons, Northern Site v. Southern Site 1, c2 = 34.11, P < 0.001; Northern Site v. Southern Site 2, c2 = 49.92, P < 0.001; Southern Site 1 v. Southern Site 2, c2 = 15.81, P = 0.05). The OSNZ nest-record data also showed the same latitudinal pattern, with median clutch-size in the South Island (n = 22, median 4 eggs, range 3–4; clutch-size: C/3, 27.3%, C/4, 72.7%) greater than the North Island (n = 50, 3, 2–4; C/2, 6%, C/3, 50%, C/4, 44%; Mann–Whitney U-test: Z71 = 2.3, P = 0.02). The OSNZ nest-record data confirmed a significant positive relationship between latitude and clutch-size in the Grey Warbler using the individual nests as data points (Spearman’s rank correlation: n = 72, r = 0.24, P = 0.04). There was no significant relationship between laying date and clutch-size in either the Southern Site 2 (data available only for the second study, not available for Southern Site 1; n = 32, Spearman’s rank correlation: r = –0.3, P = 0.09) or the Northern Site (n = 57, r = 0.08, P = 0.57). However, there was a significant negative correlation between laying date and clutch-size using the OSNZ nest records (n = 59, r = –0.26, P = 0.049) and with the data from all studies combined (n = 147, r = –0.245, P = 0.003). Geographical variation in duration of the breeding season At the Northern Site, Grey Warblers laid a single clutch, starting in the second week of September (Fig. 1). Clutches laid later were known to be replacement clutches for those lost to predation (M. G. Anderson, unpubl. data, five nests). This was confirmed by taking into account the inter-clutch interval of successful nests

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(a)

20

15

Eggs laid (percentage of total)

10

5

0

14

(b)

12

10

8

6

4

2

0 0

7

14

21 28 35 42 49 56 63 70 77

84 91 98 105 112 119 126 133 140 147 154 161 168 175 182 189 196 203

Breeding season (day) Fig. 1. Seasonal pattern of laying in Grey Warblers in: (a) our study sites (white bars, the Northern Site (n = 169 eggs); black bars, Southern Site 1 (n = 240)); and (b) OSNZ nest-record data (black bars, North Island data (n = 147 eggs); white bars, South Island data (n = 70)). The numbers of eggs laid are grouped into 7-day intervals starting on 25 June (Day 0) and converted to percentage of total eggs per site.

(67 days, i.e. laying, incubation and nestling periods combined plus the delay before initiation of the second clutch) (Gill 1982a), which was too long for these to be second clutches. In contrast, at the southern study site Grey Warblers were typically doublebrooded. Colour-banded pairs of Grey Warblers from Southern Site 1 were observed to have laid two clutches, with the first eggs laid in the last week of August and the last laid in mid-December (Fig. 1). The timing of laying events could not be closely examined for Southern Site 2, because searching for nests did not begin at the start of the breeding season, but the pattern of double brooding at Southern Site 1 was evident, with many nests in September found with nestlings already present and with new clutches being laid in November.

The OSNZ nest-record data also showed an early peak in timing of laying, primarily during September, with a second peak during late October to late November (Fig. 1). When we examined the relationship between latitude and date of laying for the OSNZ nest-record data, the peaks in laying were consistent with Grey Warblers having laid only one clutch in the North Island and two clutches in the South Island (Fig. 2). Geographical variation in patterns of brood parasitism The prevalence of brood parasitism by the Shining BronzeCuckoo was higher in the South Island (25.7%) than the North Island (11.6%, OSNZ data, whole season). In the OSNZ dataset,

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Non-parasitised nests

Parasitised nests 34

Latitude (degrees)

36

38

40

42

44

First clutch

46 0

50

Second clutch 100

150

200

250

Breeding season (day)

Fig. 2. Date of laying of first egg of each clutch for 66 nests throughout the country in the OSNZ Nest Record Scheme. The boundary between the North and South Islands is indicated by the horizontal dotted line (at ~41
). Laying started on 25 June (Day 0) and finished on 12 January (Day 201). The earliest start of a known second clutch is 23 October (Day 120) for the South Island and 5 November (Day 133) for the North Island. The division between first and second clutches on each island is indicated by the vertical dotted line; the parasitism status of each Grey Warbler nest by Shining Bronze-Cuckoos is also shown.

the mean latitude for parasitised nests (latitude converted to decimals (mean  s.e): 41.61
S  0.47
, n = 17) was significantly higher than for non-parasitised nests (40.01
S  0.3
, n = 87) (Mann–Whitney U-test: Z104 = 2.11, P = 0.04). Prevalence of parasitism across the entire breeding season was also significantly higher at Southern Site 1 (27%) and Southern Site 2 (26%) than the Northern Site (0%; c2 = 164.2, d.f. = 1, P < 0.001). Discussion Our analyses reveal that the availability of host nests for migratory Shining Bronze-Cuckoos varies considerably across their range in New Zealand. The sole host species on the main islands of New Zealand, the Grey Warbler, conforms to the general avian pattern of covariation between breeding phenology and latitude. As predicted, clutch-size increased with latitude, with Grey Warblers in the South Island laying between 0.5 and 1 egg more per clutch than their counterparts on the North Island. However, both the timing of breeding and the number of clutches per season showed the opposite pattern to that predicted, with birds at higher latitudes breeding earlier, for longer, and producing more clutches. Grey Warblers at higher latitudes typically have two clutches of four eggs during a breeding season that spans almost 4 months, whereas those at lower latitudes have a

single clutch of three eggs during a breeding season of less than 2.5 months. Brood parasitism also showed latitudinal variation, with prevalence of parasitism higher with increasing latitudes and greater on the South Island than on the North Island. The latitudinal variation in availability of host nests for Shining Bronze-Cuckoos in New Zealand has several implications for reciprocal host–parasite selection pressures. The shorter breeding season of the hosts at the northern end of their range is likely to place intense constraints on the breeding behaviour of the resident Shining Bronze-Cuckoos and may even liberate some hosts from parasitism altogether, which is perhaps reflected by the low prevalence of brood parasitism in the North Island. Single brooding by Grey Warblers in the North Island may be an adaptation to limit brood parasitism, although environmental constraints cannot be ruled out. Typically, it is only the second broods that face the risk of parasitism in the South Island (Gill 1983a). The timing of migration is critical for a brood parasite (Saino et al. 2009). The New Zealand population of Shining BronzeCuckoos migrates from New Zealand to the Solomon Islands, likely via eastern Australia, a return distance of ~12 000 km (Gill 1983b). Despite the large latitudinal range of the Shining BronzeCuckoo in New Zealand, their arrival across the country is fairly uniform, with the first birds arriving in the southern part of the country at the same time or only a little later than first arrivals in the North Island (Cunningham 1955). As the timing of breeding by Grey Warblers changes in a non-uniform pattern across their range, this may make it difficult for Shining BronzeCuckoos to adapt to the timing of breeding of their hosts in some areas. Geographical variation in clutch-size is not well understood, especially in southern hemisphere birds (Martin et al. 2000). The observed covariation of clutch-size and breeding attempts with latitude we found in Grey Warblers may have multiple potential causes, although the pattern of increasing clutch-size and the simultaneous increase in number of breeding attempts at higher latitude in our study does not appear to fit any of the traditional explanations. Nonetheless, the increase in clutch-size, and hence brood-size, suggests that host parents are better able to provide for a Shining Bronze-Cuckoo in the higher latitudes of their range. Gill (1982b) showed that the total brood weight and provisioning rate for a Shining Bronze-Cuckoo chick by Grey Warblers was approximately equivalent to (or less than) three host chicks. This may be at the upper limit of host parents’ abilities at the lower latitudes of their range. Further research, including experimentation, is required to fully elucidate the causative factors that have led to this unusual mixture of life-history traits within the Grey Warbler. We were unable to document historical predation pressure at our two sites, or across a latitudinal gradient. It is possible that predation risk may affect breeding traits by reducing clutch-size and increasing the number of clutches and that the risk differs in different parts of the Grey Warbler’s range (Zanette et al. 2006, 2011). For example, it is also possible that several factors in combination may have selected for the unusual pattern of breeding phenology and life-history traits in Grey Warblers. Even if Lack’s (1947) rule may be the explanation for an increase in clutch-size with latitude, other selection pressures (e.g. greater predation or more brood parasitism) may have resulted in a second clutch being

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laid without the expected concomitant decrease in clutch-size. Additional work is also required to compare these patterns with other New Zealand and southern hemisphere terrestrial species, both parasite–host and non-host taxa, to determine if this geographical variation is unique to a specialist parasite’s host or more widespread among endemic forest birds (Anderson et al. 2009). Regardless of the cause of the variation in breeding phenology, we have shown that there is considerable latitudinal variation in the timing of availability of host nests for the Shining BronzeCuckoo. The effect of this variation on the Shining BronzeCuckoo’s migratory and nest-selection behaviours remains to be tested fully, including its potential effect on genetic isolation and the formation of gentes, or host races, between lineages parasitising hosts with different life-history traits (Møller et al. 2011). Given the differences we observed between northern and southern populations of the Grey Warbler in the timing and number of broods, it is possible that Shining Bronze-Cuckoos parasitising each host population may show differences in their behaviour and life history similar to that of gentes seen in other brood parasitic systems. Acknowledgements We are grateful to many colleagues and volunteers for assistance in field work and to Luis Ortiz Catedral, Jim Dale, Kevin Parker, Joanne Peace and Liana Zanette for many useful discussions. We thank the OSNZ for access to Grey Warbler records in their Nest Record Scheme. We received funding from the Bright Futures Top Achiever Scholarship and Massey University Scholarship (to M. G. Anderson), the National Geographic Society (to M. E. Hauber and B. J. Gill), the Professional Staff Congress of the City University of New York Research Award and the Human Frontier Science Program (to M. E. Hauber), and the Royal Society of New Zealand Marsden Fund (to M. E. Hauber and to D. H. Brunton).

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