J Ornithol DOI 10.1007/s10336-016-1417-4

ORIGINAL ARTICLE

Comparative life history of the south temperate Cape Penduline ( minutus) and north temperate Remizidae

1,2 1 1 Penn Lloyd • Bernhard D. Frauenknecht • Morne´ A. du Plessis • Thomas E. Martin3

Received: 19 June 2016 / Revised: 22 October 2016 / Accepted: 14 November 2016 Ó Dt. Ornithologen-Gesellschaft e.V. 2016

Abstract We studied the breeding biology of the south parental nestling care. Consequently, in comparison to the temperate Cape (Anthoscopus minutus)in other two species, the exhibits greater order to compare its life history traits with those of related nest attentiveness during incubation, a similar per-nestling north temperate members of the family Remizidae, namely feeding rate and greater post-fledging survival. Its rela- the ( pendulinus) and the tively large clutch size, high parental investment and (Auriparus flaviceps). We used this comparison to associated high adult mortality in a less seasonal environ- test key predictions of three hypotheses thought to explain ment are consistent with key predictions of the adult latitudinal variation in life histories among species— mortality hypothesis but not with key predictions of the the seasonality and food limitation hypothesis, nest pre- seasonality and food limitation hypothesis in explaining dation hypothesis and adult mortality hypothesis. Contrary life history variation among Remizidae species. These to the general pattern of smaller clutch size and lower adult results add to a growing body of evidence of the impor- mortality among south-temperate living in less sea- tance of age-specific mortality in shaping life history sonal environments, the Cape Penduline Tit has a clutch evolution. size larger than that of the Verdin and similar to that of the Eurasian Penduline Tit, and higher adult mortality than Keywords Cooperative breeding Á Nest predation Á both of the other two species. The most notable difference Reproductive success Á Life history traits between the Cape Penduline Tit and the two other species is in parental behavioural strategy, with the former Zusammenfassung exhibiting bi-parental care at all stages of nesting together with facultative cooperative breeding, whereas the Eur- Vergleichende Lebensgeschichte der in der su¨dlichen asian Penduline Tit has uni-parental care and the Verdin gema¨ßigten Zone vorkommenden Kapbeutelmeise has a combination of female-only incubation but bi- (Anthoscopus minutus) und den in der no¨rdlichen gema¨ßigten Zone vorkommenden Beutelmeisen (Remizidae) Communicated by F. Bairlein.

& Penn Lloyd Wir untersuchten die Brutbiologie der in der su¨dlichen [email protected] gema¨ßigten Zone vorkommenden Kapbeutelmeise

1 (Anthoscopus minutus), um ihre Lebensgeschichte (life DST/NRF Centre of Excellence, Percy FitzPatrick Institute, history) mit denen verwandter, in der no¨rdlichen University of Cape Town, Private Bag X3, Rondebosch 7701, gema¨ßigten Zone vorkommenden Mitgliedern der Familie Remizidae, na¨mlich Beutelmeise (Remiz pendulinus) und 2 Present Address: Biodiversity Assessment and Management Pty Ltd, P.O. Box 1376, Cleveland 4163, Australia Goldko¨pfchen (Auriparus flaviceps), vergleichen zu ko¨nnen. Wir haben diesen Vergleich gemacht, um die 3 U. S. Geological Survey Montana Cooperative Wildlife Research Unit, University of Montana, Missoula, MT 59812, Hauptvorhersagen dreier Hypothesen zu testen, welche die USA mit dem Breitengrad zusammenha¨ngende Variation in der 123 J Ornithol

Lebensgeschichte von Vogelarten zu erkla¨ren versuchen, incidence of cooperative breeding (Jetz and Rubenstein die Saisonabha¨ngigkeits- und Nahrungslimitations- 2011). Yet, the reasons for these latitudinal differences Hypothese, die Nestpra¨dations-Hypothese und die remain unclear, and further comparisons can benefit Altvogelmortalita¨ts-Hypothese. U¨ blicherweise haben clarification. Arten der su¨dlichen gema¨ßigten Zone, die in weniger Differences in the life history of north temperate and saisonalen Umwelten leben, kleinere Gelege und niedrigere south temperate birds have been explained on the basis of Altvogelmortalita¨t. Entgegengesetzt zu diesem Muster hat three main hypotheses, namely the seasonality and food die Kapbeutelmeise jedoch gro¨ßere Gelege als das limitation hypothesis, adult mortality hypothesis and the Goldko¨pfchen, eine a¨hnliche Gelegegro¨ße wie die nest predation hypothesis. The seasonality and food limi- Beutelmeise und ho¨here Altvogelmortalita¨t als beide tation hypothesis proposes that populations are regulated Arten. Die Kapbeutelmeise unterscheidet sich am during the non-breeding (typically winter) season when sta¨rksten hinsichtlich ihrer Brutpflegestrategie—sie weist food resources are scarcer. In less seasonal environments, in allen Stadien der Brut biparentale Brutpflege nebst such as those of the south temperate zone (Chown et al. fakultativem kooperativem Bru¨ten auf, wohingegen bei der 2004; Lloyd et al. 2014), a lower differential in food Beutelmeise uniparentale Brutpflege und beim availability between non-breeding and breeding seasons Goldko¨pfchen eine Kombination aus alleiniger Bebru¨tung results in greater density-dependent competition and durch das Weibchen und biparentaler Nestlingsfu¨rsorge reduced food availability during the breeding season vorkommen. Folglich verbringt die Kapbeutelmeise (Ashmole 1963; Ricklefs 1980). Reduced food availability wa¨hrend der Bebru¨tung mehr Zeit auf dem Nest und hat is predicted to result in smaller clutch size, reduced incu- eine a¨hnliche Fu¨tterungsrate pro Nestling und besseres bation attentiveness, reduced per-nestling feeding rates, U¨ berleben nach dem Ausfliegen. Die relativ großen greater brood reduction due to starvation, longer develop- Gelege, das hohe Elterninvestment und die damit ment periods and longer re-nesting intervals (Gill and verbundene ho¨here Altvogelmortalita¨t bei der Haggerty 2012). The adult mortality hypothesis proposes Kapbeutelmeise in einer weniger saisonalen Umwelt that the lower annual adult mortality typical of south stimmen mit den Hauptvorhersagen der temperate birds selects for reduced total parental effort in Altvogelmortalita¨ts-Hypothese u¨berein, jedoch nicht mit reproduction but increased parental investment per off- denen der Saisonabha¨ngigkeits- und Nahrungslimitations- spring to enhance offspring survival (Martin Hypothese, wenn es darum geht, Variation in der 1996, 2002, 2014, 2015). The adult mortality hypothesis Lebensgeschichte zwischen verschiedenen Arten der predicts smaller clutch size, reduced incubation attentive- Familie Remizidae zu erkla¨ren. Diese Ergebnisse liefern ness, greater per-nestling feeding rates, lower brood weitere Belege fu¨r die Bedeutung altersspezifischer reduction due to less starvation, longer development peri- Mortalita¨t bei der Evolution der Lebensgeschichte von ods and longer re-nesting intervals among species with Arten. lower annual adult mortality (Gill and Haggerty 2012; Martin 2002, 2014, 2015). The lower annual adult mor- tality of south temperate species may be a consequence of lower seasonality and milder minimum winter tempera- Introduction tures resulting from the moderating influence on climate of a greater ratio of ocean to land in the south temperate zone Comparison of the ecologies of closely related species by comparison with the north temperate zone (Chown et al. occupying different geographical regions and environments 2004; Lloyd et al. 2014). Finally, at the same time, nest can provide valuable insights into the evolution of life predation can interact with adult mortality as part of age- history and behaviour (Martin 1996; Bennett and Owens specific mortality hypotheses (Law 1979; Michod 1979; 2002). Such studies have established that birds of the south Martin 2002, 2014, 2015; Martin et al. 2015). The temperate zone tend to lay smaller clutches (Martin et al. increased nest predation risk typical of south temperate 2000, 2006; Llambı´as et al. 2015) and have longer devel- birds can favor reduced clutch size, lower nestling feeding opment periods (Martin et al. 2007; Llambı´as et al. 2015) rates and faster development (Skutch 1949; Martin et al. and lower adult (Lloyd 2008; Lloyd et al. 2014) and 2000; Martin 2002, 2014, 2015). We examine these three fledgling mortality (Lloyd and Martin 2016) than related hypotheses based on comparisons of three species species in the north temperate zone. Behaviour of south in the family Remizidae. temperate species also tends to differ, with south temperate In this study, we describe the breeding biology of the species showing reduced incubation attentiveness (Chal- little-studied south temperate Cape Penduline Tit (Antho- foun and Martin 2007; Martin et al. 2007), longer post- scopus minutus) to enable a comparison of its life history fledging care (Russell et al. 2004) and exhibiting a higher traits with those of the related and well-studied north 123 J Ornithol temperate Eurasian Penduline Tit (Remiz pendulinus) and (Sony Corp., Tokyo, Japan) mounted on tripods. Nests the Verdin (Auriparus flaviceps), all small insectivores. were video-taped at two stages during incubation, namely One of Africa’s smallest birds, the Cape Penduline Tit early incubation (between 2 and 5 days after the last egg of inhabits semi-arid to arid shrublands and savannas in the clutch was laid) and late incubation (between 9 and southern Africa (Dean 2005). It is best known for building 13 days after clutch completion). Video-taping during the a surprisingly large, strong, oval-shaped nest of fine plant nestling period occurred between 2 and 20 days after the fibres that are worked into a thick and waterproof, felted hatching of the last chick. Nest attentiveness during incu- nest wall through repeated teasing and jabbing with its bation was measured as the percentage time a bird was finely-pointed beak (Skead 1959). A further unusual fea- inside the nest chamber over the recording period. Nestling ture of the nest is a blind-ending pocket (also termed a false provisioning rates were measured as the average number of entrance) on the side of the nest. Birds entering and exiting feeding visits per nestling per hour. the nest perch on the rim of the pocket, opening and closing The banding of adults with a unique combination of the true nest entrance, a flexible spout that the birds open three colour bands and a numbered metal band commenced with a foot before entering and close with a push of the in 2002 and continued annually to 2007. Adults and any beak or butting of the head after exiting. Breeding pairs and fledged young roost in the nest throughout the nesting their fledged young roost in their nests throughout the period and also post-breeding. Therefore, birds were caught breeding season and roost communally with other family by covering the entrance spout with a cloth bag at first light groups after the breeding season, with up to 18 birds until all birds had exited the nest. To prevent premature roosting in a single nest (Skead 1959). The Cape Penduline fledging from the nest, nestlings were weighed and banded Tit is reported to be a facultative cooperative breeder based with a numbered metal band and a single coloured plastic on observations of more than two birds attending a nest band at an age of 10–15 days post-hatching. Birds were (Harrap and Quinn 1996), but the breeding biology of the sexed based on behaviour: only the breeding male sings the species is poorly described. Here, we report the first species’ advertising song (van Dijk et al. 2010). A total of detailed study of the breeding biology of the species to 55 adults, 66 juveniles and 139 pre-fledging nestlings were allow comparisons with north temperate Remizids and a banded during the study, with some juveniles and nestlings consideration of the three hypotheses described above. later re-trapped as adults. The length of the laying season was estimated from the number of nests initiated each month using the MacArthur Methods index (Ricklefs 1966). Nesting success was calculated as the product of the daily stage-specific survival rate in the We studied a population of Cape Penduline Tit as part of a average laying, incubation and nestling periods, respec- broader study of the breeding bird community (see Martin tively, according to the method of Mayfield (1961). To test et al. 2006, 2007, 2011; Lloyd et al. 2014) within a 260-ha whether nest attentiveness varied with group size (pair vs. area of the 2900-ha Koeberg Nature Reserve (33°410S, cooperative group), controlling for incubation stage (days 18°260E), which is situated on the west coast of South of incubation), we used a linear mixed-effect model that Africa. The site has a Mediterranean climate with warm, included nest attentiveness as the response variable, group dry summers, cool, wet winters and a mean annual rainfall size and incubation stage as fixed effects and female iden- of 375 ± 77 mm [±1 standard deviation (SD); Lloyd et al. tity as a random effect to account for repeated observations 2009]. The mean minimum temperature of the coldest on some females. To test whether the per-nestling feeding month is 7.3 °C and the mean maximum temperature of the rate varied with group size (pair vs. cooperative group), hottest month is 26.4 °C. The vegetation is coastal shrub- controlling for nestling age, we used a linear mixed-effect land with a typical height of 1–2 (maximum 2.2) m. model that included per-nestling feeding rate as the During the years 2000–2008 we undertook intensive response variable, group size and nestling age as fixed monitoring of nests combined with the banding of breeding effects and group identity as a random effect to account for adults with a unique combination of three colour bands and repeated observations on some groups. Models were fitted a numbered metal band. Nests were located based on using ‘lmer’ in the ‘lme4’ package in R Ò Core Team parental behaviour, usually during the building stage, and 2016). The results of these analyses are reported in the text checked at 1- to 4-day intervals to determine clutch size, as the mean ±1 SD, unless otherwise stated. We obtained stage transition dates and fate (Martin et al. 2006). To comparative information on the life history traits of the monitor parental care behaviours at the nest, we video- Eurasian Penduline Tit and Verdin from published sources. taped nests continuously for the first 3–7 h of the day Differences in mean clutch size between species were tested (average 5.5 ± 1.6 h, n = 69 recordings), beginning using a one-way analysis of variance and the Holm within 0.5 h of sunrise, using Sony Hi8 video cameras adjustment for post hoc pairwise comparisons (Holm 1979). 123 J Ornithol

Results 35 30 Cape Penduline Tits occurred at a relatively low density 25 within the study area, with between four and nine occupied 20 territories within the core 260-ha study area in any 1 year (Fig. 1). Most territories were occupied by a pair nesting 15 10 alone, but occasionally the breeding pair was assisted by Nests iniated one (n = 3) or two (n = 1) helpers (Fig. 1). 5 Nests were typically constructed at a height of 1–2 m 0 above ground, mostly in thorny shrubs; Putterlickia pyra- Jul Aug Sep Oct Nov Month cantha was the most commonly used shrub, but nests were also constructed in Lycium ferocissimum, Rhus laevigata Fig. 2 Number of new nests of the Cape Penduline Tit initiated each var. villosa, R. glauca, and Solanum sp. Construction of the month during the 9 years of the study first nests of the season took an average 26.1 ± 6.1 days (range 19–35 days, n = 9) between the initiation of (n = 14 eggs from 4 clutches). Incubation duties were building and the laying of the first egg, and the pair con- shared equally by the breeding pair, and the few data on tinued to add material to the nest throughout the incubation pairs breeding with one helper suggest that helpers incu- period. Following the loss of a clutch or brood, breeding bate to a lesser extent than the breeding pair (Fig. 3). Total pairs re-nested rapidly, commonly re-using the original incubation attentiveness did not vary with length of incu- nest if it was not damaged during predation. The re-nesting bation (t = 1.09, P = 0.29) and did not differ between interval after failure was shorter (t = 3.89, P = 0.003) if pairs incubating with or without helper assistance the original nest was re-used (6.5 ± 1.6 days, range (t =-1.57, P = 0.13; 33 observations from 19 females). 4–9.5 days, n = 8) than if a new nest was built Overall incubation attentiveness was 79.0 ± 10.6%. (10.6 ± 2.4 days, range 8–14.5 days, n = 7). Similarly, Both members of the pair fed and brooded the nestlings. the re-nesting interval following successful fledging Helpers also assisted with nestling feeding, but there was appeared to be shorter if the original nest was re-used no evidence that the presence of helpers increased the per- (10.6 ± 5.7 days, range 4.5–26 days, n = 17) than if a nestling feeding rate (Fig. 4). Nestling feeding rates new nest was built (20.8 ± 0.4 days, range 20.5–21 days, increased with nestling age (t = 4.87, P \ 0.001), but did n = 2). not differ between pairs and cooperative groups (t = 1.14, The earliest and latest clutch initiation dates were 7 July P = 0.26; 37 observations from 18 pairs/groups); however, and 17 November, respectively, but most clutches (91%) data on cooperative groups were limited (Fig. 4). The were initiated in the months of August to October (Fig. 2). average incubation period was 14.8 ± 0.9 days (n = 31), MacArthur’s index of the length of the laying season was and the average nestling period was 21.7 ± 1.0 days 3.83 months. Eggs were laid daily, and mean clutch size (n = 22). Hatching was partially asynchronous, with the was 4.9 ± 0.9 eggs (range 3–7 eggs, n = 78 clutches). The last chick hatching 1 day (5 nests) to 2 days (1 nest) after average mass of a freshly laid egg was 0.775 ± 0.030 g 100 27 6 90 10 Cooperave groups Pairs 80 9 70 8 60 7 18 18 50 3 6 3 40 5 30 4 Territories 20 3

3 Incubation attentiveness (%) 10 2 0 1 Total Female Male Total Female Male Helper Pair Group 0 2002 2003 2004 2005 2006 2007 Year Fig. 3 Mean incubation attentiveness [percentage of recording time spent in the nest ±1 standard deviation (SD; whiskers)] at nests of Fig. 1 Number of territories occupied by pairs and cooperative Cape Penduline Tit pairs and cooperative groups. Numbers above groups of the Cape Penduline Tit (Anthoscopus minutus) in years bars Sample size. Sex was unknown at some nests, and these nests when the entire core study area was surveyed contributed to increased sample size to totals 123 J Ornithol

14 A least five were attributed to small-mammal predation on the 3 12 6 basis of video evidence, including predation by the Cape 6 Grey Mongoose (Galerella pulverulenta). Three nest videos 10 13 also captured Boomslang (Dispholidus typus) snakes and 8 3 a Black Harrier hawk (Circus maurus) investigating nests 6 containing nestlings without predation success. 4 The daily nest predation rate was 2.86% during the 4 2 (feeds/nestling/hr)

Nestling feeding rate laying period, 1.55% during the incubation period and 2 0.46% during the nestling period. The overall daily nest 0 mortality rate was 1.28%, and nest success during the PG PG P PG average 4-day laying period, 15-day incubation period and 2-3 8-10 12-15 18-20 Nestling age (days) 22-day nestling period was 59.7% (n = 2582 observation days at 104 nests). Pairs commonly re-nested after suc- cessful fledging, but no pair fledged more than two broods 3.5 3 B in a season. The number of fledged young produced per 3 pair in a season averaged 4.85 ± 2.49 (range 0–9, n = 33 3 3 2.5 pair-seasons over 7 years). There were insufficient coop- 3 erative groups to test the prediction that pairs with helpers 2 3 fledged more young than pairs without helpers. 1.5 Among the 260 birds banded as pre-fledging nestlings, 3 juveniles and adults and monitored over a period of 1 (feeds/nestling/hr)

Nestling feeding rate 7 years, the longest living bird, a male, survived for 4 years 1 0.5 1 after having been banded as a nestling (Table 1). Of the 185 birds banded as nestlings or juveniles at the natal nest, 0 F M H1 H2 F M H1 H2 17 (9 females, 8 males) were recaptured as breeders in the Age 3 days Age 18 days study area the year after banding. The average natal dis- persal distance between the natal nest site and breeding Fig. 4 Mean per-nestling feeding rates (whiskers ±1 SD) of pairs without a helper (P) and pairs with one or more helpers (G)at nest site was 731 ± 485 (range 130–1770) m and did not different stages of the nestling period (a) and of the breeding female differ between females (727 ± 445 m) and males (F), male (M) and helpers at 3 and 18 days after hatching in three (737 ± 569 m; t = 0.04, P = 0.97). cooperative groups, two with a single helper (H1) and one with two The data in Table 1 show that the Cape Penduline Tit helpers (H1 and H2). Numbers above bars Sample size exhibits many similarities in life history traits with its north the first-hatching chick. Of the 262 eggs that survived to temperate relatives, including low adult survival, large hatching, 20 (7.6%) failed to hatch. Brood reduction not clutch size, low nest mortality, high annual productivity attributable to predation occurred within 18 (42%) of 43 and similar development periods, but differs in having broods during the nestling period, with an average of 1.6 greater biparental care, greater investment in incubation (range 1–3) chicks lost from broods experiencing brood attentiveness and longer re-nesting intervals. Clutch size reduction. The average brood size at fledging was differed between species (F3,378 = 7.72, P \ 0.001); while 3.7 ± 1.1 fledglings (range 1–6 fledglings, n = 46 broods). the clutch size of the Cape Penduline Tit did not differ Among the 104 nests monitored during the study, 56 from that of the Eurasian Penduline Tit at either 56°N survived to fledge young, 33 failed due to natural causes, two (Holm post hoc P = 0.8) or 46°N (Holm post hoc failed due to research activities (not included in calculations P = 0.2), the Cape Penduline Tit had a larger mean clutch of demographic parameters) and 13 were still active when size than the Verdin (Holm post hoc P = 0.005). The Cape monitoring was discontinued. Nest failures included 29 lost Penduline Tit had higher incubation attentiveness than the to predation, two nests at which all nestlings died following Eurasian Penduline Tit (t = 7.34, P \ 0.001) but a similar the mortality of a member of the breeding pair, one nest per-nestling feeding rate (t = 1.49, P = 0.16; Table 1). dislodged during a storm and one that failed due to unknown causes. Of 22 predation events at nests with eggs, 15 (68%) involved the loss of eggs with no observable damage to the Discussion nest and were attributed to predation by snakes, particularly the Rhombic Egg-eater (Dasypeltis scabra). The remaining The Cape Penduline Tit at our study site inhabits a less seven predation events were attributed to small-mammal seasonal environment, with milder mean minimum winter predation. Of six predation events at nests with nestlings, at temperatures and less extreme seasonal temperature 123 J Ornithol

Table 1 Comparison of environmental characteristics and life history traits of the Eurasian Penduline Tit, Verdin and Cape Penduline Tit Species EPTa EPTb VERc VERd CPTe

Latitude (°N) 56 46 32–36 26 -34 Mean maximum temperate of hottest month (°C)f 20.1 26.7 37.2–42.2 32 26.4 Mean minimum temperate of coldest month (°C)f -2.8 -4.4 -2.2 to 1.7 21.5 7.3 Breeding density (pairs/100 ha) 20 46–59 1.2–3.5 Incubation care Uniparental Uniparental Uniparental Biparental Nestling care Uniparental Uniparental Biparental Biparental Breeding season length (months) 1.8 2.8 2.6–3.9 3.8 Clutch sizeg 4.8 ± 1.7 5.2 ± 1.6 3.3–3.8 ± 0.5 2.5–2.9 4.9 ± 0.9 Incubation attentiveness (%) 55 ± 14 55 79 ± 11 Incubation period (days) 14.5 16 14.8 Nestling period (days) 21 18 21.7 Nestling feeding rates (feeds/h)h 18.1 ± 7.1 23.2 ± 11.8 Nestling feeding rates (feeds/nestling/h)h 5.3 ± 1.6 6.6 ± 3.1 Daily nest mortality (%) 1.06 3.0–3.7 1.28 Nest success (%) 64g 62–87 28–36 60 Fledging brood size 3.1 3.7 Brood reduction (% fledgling brood size/clutch size) 40 24 Mean re-nesting interval after failure (days) 4 8.6 Mean re-nesting interval after fledging (days) 2 11.7 Annual productivity (fledged young/female) 5.1 3.6 4.8 Fledgling survival to 21 days (%) 83 97 Annual adult mortality (%) 40 66 Oldest ringed bird (years) 5.8 5.6 4 EPT, Cape Penduline Tit (Anthoscopus minutus); VER, Verdin (Auriparus flaviceps); CPT, Cape Penduline Tit (Remiz pendulinus) a Staav (1998), Cramp et al. (1993) and Persson and O¨ hrstro¨m(1989) b Poga´ny et al. (2012) and Szentirmai et al. (2007) c Taylor (1971), Austin (1977) and Klimkiewicz et al. (1983) d George (1987) e This study, Lloyd et al. (2014) and Lloyd and Martin (2016) f Climate data sourced from http://www.worldweatheronline.com g Excludes nests deserted by both parents prior to incubation h Measured at age 10 days in EPT (n = 29) and at age 8–12 days in CPT (n = 13) variation, than that inhabited by the related north temperate mortality and a larger clutch size than 15 other resident Eurasian Penduline Tit in Europe and the Verdin in the species in the community (annual adult mortality southern USA (Table 1). Consequently, the seasonality and range 0.10–0.38; mean clutch size range 2.1–3.8 eggs; food limitation hypothesis predicts that the Cape Penduline Lloyd et al. 2014). It also has a larger clutch size than the Tit should have lower annual adult mortality and smaller Verdin and a similar clutch size to the Eurasian Penduline clutch size due to greater food constraints during the Tit (Table 1). The higher adult mortality and larger clutch breeding season in a less seasonal environment. However, size of the Cape Penduline Tit does not fit the pattern of based on our observations (Table 1), the Cape Penduline relatively low adult mortality and small clutch sizes typical Tit has quite high annual adult mortality, rivalling the of many southern hemisphere birds (Martin 1996; Martin highest reported among the north temperate et al. 2000, 2006) and of the rest of the breeding bird (Martin 1995; Martin and Clobert 1996). It has higher community in the study area (Lloyd et al. 2014). These trait annual adult mortality than the Verdin and shorter maxi- patterns are inconsistent with the seasonality and food mum longevity than the Eurasian Penduline Tit (Table 1). limitation hypothesis, but are consistent with the adult The Cape Penduline Tit is an anomaly in the breeding bird mortality hypothesis, which predicts that species with community at the study site, with relatively higher annual higher adult mortality should have larger clutches

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(Williams 1966; Martin 1996, 2015; Martin et al. 2000; predation is not likely to explain differences in life history Ghalambor and Martin 2001). traits between latitudes (also see Martin et al. 2000). Given the higher adult mortality of the Cape Penduline The length of the breeding season and nesting success of Tit compared with that of the Eurasian Penduline Tit based the Cape Penduline Tit are similar to those of the Verdin, on maximum longevities, a key prediction of the adult but due to a larger clutch size, the former has a greater mortality hypothesis is that the Cape Penduline Tit should breeding productivity despite longer re-nesting intervals, exhibit higher nestling feeding rates, but lower parental fledging an average of 4.8 young per female compared with investment per offspring. By contrast, the food limitation 3.6 fledged young per female in the Verdin (Table 1). hypothesis predicts that the Cape Penduline Tit should Breeding at higher latitudes, the Eurasian Penduline Tit has exhibit lower feeding rates since it occupies a less seasonal a substantially shorter breeding season but still fledges an environment where it is expected to experience greater average of 5.1 young per female (Table 1), possibly due to food constraints during the breeding season. In contrast, the lower nest mortality or some females deserting the first Cape Penduline Tit meets neither prediction, having a clutch to be cared for by a male while they re-nest with similar feeding rate per-nestling (6.6 feeds/nestling/h) as another male (Persson and O¨ hrstro¨m 1989). The lower the Eurasian Penduline Tit (5.4 feeds/nestling/h; Table 1) annual fecundity and annual adult mortality of the Verdin during the mid-nestling period. However, the slightly lower contrasts with the greater annual fecundity and adult feeding rate of the Eurasian Penduline Tit was associated mortality in the Cape and Eurasian penduline tits but is with greater brood reduction (40%) compared to the Cape consistent with the observation that annual fecundity is Penduline Tit (24%) (Table 1), suggesting greater food proportional to annual adult mortality among birds (Martin limitation in this northern species due to its uniparental 1995; Ricklefs 2000). behaviour. The shared parental care exhibited by the Cape The three Remizid species that were the focus of our Penduline Tit enables per-nestling feeding rates similar to study differ most notably in parental behavioural strategy. those in the Eurasian Penduline Tit, while the rates of While both sexes contribute to nest building in all species, nestling feeding by individual Cape Penduline Tit adults gender roles diverge thereafter. The Eurasian Penduline Tit attending the nest are lower. pair members compete to desert the nest first towards the The Cape Penduline Tit experiences substantially lower end of egg-laying, leaving the other member of the pair to nest mortality than other species in the community at the incubate and raise the young alone while the deserting study site, with daily nest predation during the egg stage of individual seeks additional breeding opportunities (Poga´ny 1.8%, as compared with 6.1–12.4% for the 15 other species et al. 2012), a strategy that may allow a greater number of in the community (Martin et al. 2015), and daily nest nesting attempts within the short breeding season (Persson predation during the nestling stage of 0.5%, as compared and O¨ hrstro¨m 1989). Verdin females incubate and tend the with 2.5–7.4% for the other species (Martin et al. 2011). young in their first week alone, whereafter the male con- We attribute the low nest predation experienced by Cape tributes equally to nestling feeding (Taylor 1971). By Penduline Tit to the strength and complexity of its nest, contrast, Cape Penduline Tit pair members share all par- which video evidence confirmed is particularly effective ental duties approximately equally and are occasionally also against predation by snakes, including specialist egg and assisted by one or more helpers. Consequently, the Cape nestling predators. Consequently, the Cape Penduline Tit Penduline Tit has greater nest attentiveness during incuba- did not experience greater rates of egg or nestling mortality tion and high per-nestling feeding rates (Table 1). Embry- or lower nest success than that reported for the related onic temperature can affect embryonic development rate north temperate species (Table 1), despite southern African (Martin et al. 2007, 2015), but greater nest attentiveness in birds generally experiencing substantially greater nest the Cape Penduline Tit (78 versus 55% in both the Eurasian predation than north temperate species (Lloyd 2004; Mar- Penduline Tit and the Verdin) was not unequivocally tin et al. 2011, 2015). Reduced nest predation risk can associated with a shortening of the incubation period. While favor increased clutch size, higher nestling feeding rates the average incubation period in the Cape Penduline Tit was and slower development (Skutch 1949; Martin 1 day shorter than that of the Verdin, it was similar to that of 2002, 2014, 2015). The low nest predation rate experienced the Eurasian Penduline Tit (Table 1). Of course, attentive- by the Cape Penduline Tit may partly explain its larger ness is not a perfect predictor of embryonic temperature clutch size, greater nestling feeding rates and longer (Martin et al. 2007), and the large differences in attentive- incubation and nestling development periods compared to ness and similar incubation periods may indicate a role of other passerine species in the breeding bird community intrinsic determinants of embryonic periods (Ricklefs and (Martin et al. 2007, 2015). However, since nest mortality Starck 1998; Shine and Olsson 2003). and nest success of the Cape Penduline Tit are similar to The south temperate Cape Penduline Tit exhibits an those of the Eurasian Penduline Tit and the Verdin, nest interesting mix of life history traits, including traits such as 123 J Ornithol higher incubation attentiveness and a larger clutch size Dean WRJ (2005) Cape Penduline Tit Anthoscopus minutus. 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Ibis 150:182–187 Acknowledgements We thank the many field assistants who helped Lloyd P, Martin TE (2016) Fledgling survival increases with locate and monitor nests and resight the colour-band combinations of development time and adult survival across north and south breeding adults each year, particularly Sonya Auer, Ron Bassar, temperate zones. Ibis 158:135–143 Joseph Fontaine, Simon Davies, David Nkosi, Pierre-Yves Perroi, Lloyd P, Taylor WA, du Plessis MA, Martin TE (2009) Females Rene´ van Dijk and A´ kos Poga´ny. We thank Gert Greef and Hilton increase reproductive investment in response to helper-mediated Westman for permission to work at ESKOM’s Koeberg Nature improvements in allo-feeding, nest survival, nestling provision- Reserve. This work was supported in part through National Research ing and post-fledging survival in the Karoo scrub-robin Cer- Foundation grants (to PL and RA) and National Science Foundation cotrichas coryphaeus. 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