Fledgling Survival Increases with Development Time and Adult Survival Across North and South Temperate Zones

Ibis (2016), 158, 135–143

Fledgling survival increases with development time and adult survival across north and south temperate zones

PENN LLOYD1,2* & THOMAS E. MARTIN3 1Percy FitzPatrick Institute, DST/NRF Centre of Excellence, University of Cape Town, Private Bag X3, Rondebosch 7701, South Africa 2Biodiversity Assessment and Management Pty Ltd, PO Box 1376, Cleveland, Qld 4163, Australia 3U.S. Geological Survey Montana Cooperative Wildlife Research Unit, University of Montana, Missoula, MT 59812, USA

Slow life histories are characterized by high adult survival and few offspring, which are thought to allow increased investment per offspring to increase juvenile survival. Consis- tent with this pattern, south temperate zone birds are commonly longer-lived and have fewer young than north temperate zone species. However, comparative analyses of juvenile survival, including during the first few weeks of the post-fledging period when most juvenile mortality occurs, are largely lacking. We combined our measurements of fledgling survival for eight passerines in South Africa with estimates from published studies of 57 north and south temperate zone songbird species to test three predictions: (1) fledgling survival increases with length of development time in the nest; (2) fledgling survival increases with adult survival and reduced brood size controlled for development time; and (3) south temperate zone species, with their higher adult survival and smaller brood sizes, exhibit higher fledgling survival than north temperate zone species controlled for development time. We found that fledgling survival was higher among south temperate zone species and generally increased with development time and adult survival within and between latitudinal regions. Clutch size did not explain additional variation, but was confounded with adult survival. Given the importance of age-specific mortality to life history evolution, understanding the causes of these geographical patterns of mortality is important. Keywords: adult survival, evolution, fledgling survival, life history.

Globally, avian life-history strategies vary with lati- north temperate zone (Martin 1996). Theory sug- tude; in comparison with north temperate zone gests that low adult mortality in the southern tem- species, tropical birds have life histories typified by perate zone should favour increased parental smaller clutch sizes, longer developmental periods, investment per offspring to increase juvenile sur- higher nest predation, extended post-fledging par- vival (Skutch 1949, MacArthur & Wilson 1967, ental care and higher adult survival (Skutch 1985, Pianka 1970, Martin 2015). Increased investment Martin 1996, 2002, Ghalambor & Martin 2001, per offspring may be expressed in larger eggs Russell et al. 2004, Lloyd et al. 2014). These slow (Martin 2008), higher feeding rates per offspring life-history strategies appear to extend to the south (Martin et al. 2011, Gill & Haggerty 2012, Martin temperate zone, where adult mortality and life- 2015) or longer parental care after fledging (Rus- history expression seem to be more similar to sell et al. 2004). Increased investment and parental those of tropical species than to species of the care after fledging is expected to increase fledgling survival (Russell et al. 2004, Styrsky et al. 2005, Tarwater & Brawn 2010, Martin 2015), and varia- *Corresponding author. tion in fledgling survival can exert strong selection Email: [email protected]

on life-history strategies (Martin 2014, 2015). temperate zones, (2) that fledgling survival Thus, low adult mortality may favour increased increases with adult survival and reduced brood parental investment in fewer young, resulting in size controlled for development time within and lower fledgling mortality (Martin 2015). As a between temperate zones, and (3) that south tem- result, we expect positive covariation of adult and perate zone species with their higher adult survival fledgling mortality rates among species, and latitu- and smaller brood sizes exhibit higher or similar dinal differences in fledgling mortality that parallel fledgling survival to north temperate zone species those observed for adults. So far, these possibilities when controlling for development time. We test have not been tested. these predictions by combining measurements of Survival of offspring after leaving the nest (i.e. fledgling survival for eight south temperate zone fledglings) can be influenced by the length of time passerines with data from published studies of spent developing in the nest, at least in the north fledgling survival from around the world. We temperate zone (Cox et al. 2014, Martin 2014). In define fledgling survival as the survival of young particular, species with higher nest predation risk through the first few weeks after leaving the nest. spend less time developing in the nest, causing their young to fledge with smaller relative body METHODS mass and reduced wing development (Cheng & Martin 2012, Martin 2014, 2015). Of critical rele- South Africa study vance, increased parental investment in species with slower life histories (i.e. species with higher We studied fledgling survival as part of an inten- adult survival and smaller clutch size) results in sive study of life-history variation (Martin et al. fledglings with better-developed wings but similar 2006, 2007, 2011) in a community of birds inhab- relative body mass compared with species with fas- iting the 2900-ha Koeberg Nature Reserve ter life histories for the same development time (33°410S, 18°260E, elevation 10 m), on the south- (Martin 2015). Body mass can be important to west coast of South Africa. The vegetation is fledgling survival in both north temperate coastal shrubland, with an average shrub height of (Krementz et al. 1989, Linden et al. 1992, Both 1–2 m (Nalwanga et al. 2004). The region has a et al. 1999) and tropical/south temperate zones Mediterranean climate with hot, dry summers and (Green & Cockburn 2001, Lloyd et al. 2009, cool, wet winters: 80% of mean annual rainfall falls Tarwater et al. 2011). However, most studies find during April to September. The breeding season of predation is the primary source of fledgling mortal- birds in the community lasts from late July to ity (Martin 2014). Consequently, traits such as early November. From 2000 to 2007 we under- wing development that can affect the ability to took intensive monitoring of nests (Martin et al. escape predators (Dial et al. 2006) may then be 2007, 2011) combined with ringing of breeding particularly important to fledgling survival. The adults with a unique combination of three colour similar body mass but greater wing development rings and a numbered metal ring. Approximately in species with slower life histories yields contrast- 1400 adults attending nests had been colour-ringed ing predictions for fledgling survival. In particular, by the end of 2007 (Lloyd et al. 2014). Nests if relative body mass is critical to fledgling survival, were located using parental behaviour, usually dur- then fledgling survival should not differ between ing the building stage, and checked at 1- to 4-day regions with differences in life histories when con- (mostly 1- to 2-day) intervals to determine clutch trolling for development time. In contrast, if size, stage transition dates and fate (Martin et al. mobility from wing development is critical, then 2006). To prevent premature fledging from the fledging survival should be greater among species nest, nestlings were measured and ringed within with slower life histories. Ultimately, the impor- 1–2 days of their primary feathers breaking pin, tance of offspring development time, and possible which occurs approximately 4–5 days before fledg- differences between slow vs. fast life histories (i.e. ing. For identification of fledglings out of the nest, adult survival, offspring number) for fledgling sur- nestlings were ringed with a numbered metal ring vival across latitudinal regions needs testing. and either: (1) a single coloured plastic ring, with We test three predictions: (1) that fledgling sur- each brood member receiving a different colour, vival increases with length of development time in or (2) a unique combination of three colour rings the nest within and between north and south (one species only).

We determined whether young had fledged for 60 species (Supporting Information Table S1). from a nest by monitoring nests close to fledging Among the 37 north temperate zone species, at 1- to 2-day intervals and confirming that par- fledgling survival estimates included the use of ents were carrying food to young out of the nest radio-telemetry in 21 species and re-sighting of when the nest was first found empty. Thereafter, colour-ringed birds in the remainder. Among the the survival of young was monitored at weekly latter 16 species, nine species were year-round res- intervals until 21 days post-fledging, the most com- idents, six species were confidently monitored dur- mon interval among studies of fledgling survival ing the period prior to any dispersal from the natal (Martin 2014). All species monitored for fledgling territory taking place and one species (Purple Mar- survival were year-round territorial residents. As tin Progne subis) was monitored at predictable family groups did not disperse from the natal terri- roosting colonies. The survival estimates for all 28 tory post-fledging, reliance on radiotelemetry to south temperate zone species were derived from monitor survival was not required. Instead, knowl- re-sighting. edge of the territory boundaries of each pair meant that surviving fledglings were located relatively Analyses easily once the provisioning adults had been located. Resighting was further facilitated by the We corrected for possible phylogenetic effects low, open vegetation of the study area. The provi- (Felsenstein 1985) using the Caper (Orme 2013) sioning by parents was monitored until the ring package in R v3.0.3 for Windows (R Development combinations of all surviving fledglings had been Core Team, Vienna, Austria). Phylogenetic trees confirmed. For all species except Karoo Scrub were obtained from www.birdtree.org (Jetz et al. Robin Cercotrichas coryphaeus, we estimated fledg- 2012) using the Hackett et al. (2008) backbone ling survival as percentage of total fledglings surviv- and imported into the program MESQUITE (Mad- ing in each of the 3 weeks after fledging because dison & Maddison 2011) where a majority rules the resighting probability at each interval was close consensus tree was constructed based on 1000 to 100%. The fledglings of Karoo Scrub Robin trees (Supporting Information Fig. S1). This con- proved to be too difficult to locate in the dense sensus tree was then used in phylogenetically con- cover they used during the first 2 weeks post- trolled analyses that incorporate Pagel’s lambda fledging. Therefore their survival was determined (Pagel 1992) to transform branch-lengths. only at the end of the 3rd week post-fledging, We analysed data in two sets: (1) all studies when they were more active and following the par- that reported fledgling survival to between 18 and ents into the open. 24 days after fledging, and (2) all studies that reported fledgling survival regardless of the length of time monitored. In the latter case, we included Literature review length of the monitoring period as a covariate in To test our three predictions, we combined data analyses. As survival may vary with body mass from our eight species with published estimates of (Cox et al. 2014), we also included adult body fledgling survival of passerine birds from around mass as a covariate. Fledgling and adult survival the world, as well as estimates of annual adult sur- were arcsine-transformed and adult body mass was vival probability, clutch size and nestling period ln-transformed prior to analysis. length. If more than one source provided an esti- mate of survival for the same species, we used the RESULTS average of the estimates. We compared birds studied in two latitude regions: north and south tem- Weekly survival rates of fledglings ranged between perate zones defined as latitudes equal to or 0.86 and 1.00 among the eight south temperate greater than 23.5°N and S, respectively. We found zone species studied in South Africa (Table 1). published fledgling survival estimates for 57 Survival from fledging to 21 days post-fledging passerine bird species and we added estimates for ranged from 0.77 to 0.97 among species (Table 1) eight more south temperate zone species, yielding and averaged 0.89 ( 0.06 se). Most mortality of fledgling survival data on 28 south temperate zone fledglings occurred within the first week post-fled- species and 37 north temperate zone species. Of ging, with generally negligible mortality thereafter these, adult survival estimates were also available (Table 1).

Table 1. Fledgling survival of eight South African passerine species through each week, with overall survival to 21 days post-ﬂed- ging. Sample sizes of the number of individual ﬂedglings monitored from the start of each week are indicated in parentheses. As not all family groups were monitored through all 3 weeks, survival to 21 days is calculated as the product of weekly survival, except for Cercotrichas coryphaeus, for which survival was determined at 21 days. NA, not applicable.

Survival (n)

Family Species Week 1 Week 2 Week 3 To 21 days

Cisticolidae Apalis thoracica 0.926 (27) 1.000 (25) 1.000 (25) 0.926 Cisticolidae Cisticola subruﬁcapilla 0.870 (23) 1.000 (16) 1.000 (10) 0.870 Cisticolidae Prinia maculosa 0.926 (326) 0.993 (269) 0.962 (209) 0.884 Muscicapidae Cossypha caffra 0.976 (41) 0.972 (36) 1.000 (26) 0.949 Muscicapidae Cercotrichas coryphaeus NA NA NA 0.772 (167) Remizidae Anthoscopus minutus 0.969 (32) 1.000 (27) 1.000 (22) 0.969 Macrosphenidae Sphenoeacus afer 0.900 (10) 1.000 (8) 1.000 (5) 0.900 Sylviidae Sylvia subcaerulea 0.857 (21) 1.000 (10) 1.000 (9) 0.857

18 12 (a) (d) 16 10 14 12 8 10 6 8 6 4 4

Number of species 2 2 0 0

21 12.5 15.0 17.5 20.0 22.5 25.0 30.0 8–1114–1718–20 22–2425–3031–37 >37 8–9.9 >30.0 Interval (days of study) Nestling period (days) 10 12 (b) (e)

8 10

8 6 6 4 4 2

Number of species 2

0 0 0.3 0.4 0.5 0.6 0.7 0.8 0.9 <0.40 0.45 0.50 0.55 0.60 0.65 0.70 0.75 0.80 0.90 1.00 Fledgling survival probability (18–24 days) Adult survival probability

12 14 (c) (f) 10 12 10 8 8 6 6 4 4

Number of species 2 2

0 0 0.2 0.3 0.4 0.5 0.6 0.7 0.8 0.9 <1020304050607080>80 Fledgling survival probability (11–49 days) Adult mass (g)

Figure 1. Frequencies of raw data among species and between north (solid bars) and south temperate (grey bars) zones for: (a) the interval (in days) that fledgling survival was measured, (b) fledgling survival probability for studies that measured it for 21 3 days, (c) fledgling survival probability for all monitoring intervals, (d) nestling periods, (e) adult survival probability and (f) adult mass.

1.4 (a) (a) 0.4 Anthoscopus minutus 1.2

0.2 1.0

0.8 0.0

0.6 –0.2 Arcsin fledgling survival 0.4 Arcsin fledgling survival North temperate North temperate South temperate –0.4 South temperate 0.2 0.9 1.0 1.1 1.2 1.3 1.4 1.5 –0.4 –0.2 0.0 0.2 0.4

0.8 (b) (b) 0.6 0.6

Anthoscopus minutus 0.4 0.4

0.2 0.2 0.0 0.0 –0.2

Arcsin fledgling survival –0.4 –0.2 Arcsin fledgling survival –0.6 –0.4 –0.3 –0.2 –0.1 0.0 0.1 0.2 0.3 0.4

Log10 nestling period (days) –0.4 –0.2 0.0 0.2 0.4 Adult survival probability Figure 2. Fledgling survival probability at (a) 18–24 days and (b) variable monitoring intervals controlled for monitoring inter- Figure 3. Fledgling survival probability at (a) 18–24 days and val relative to length of the period of development in the nest (b) variable monitoring intervals controlled for monitoring inter- (nestling period) in north (closed circles) and south (open cir- val relative to adult survival probability controlled for nestling cles) temperate zones. period, and clutch size in north (closed circles) and south (open circles) temperate zones. The Cape Penduline Tit Anthoscopus minutus is an outlier. The interval over which post-fledging survival was monitored varied among studies, ranging from 8 to 49 days post-fledging. However, 63% of stud- P < 0.001). Finally, body mass did not differ ies reported post-fledging survival for 21 3 days between zones (Fig. 1f; t63 = 0.59, P = 0.56). post-fledging, and 82% reported survival for Fledgling survival increased with length of the 21 7 days post-fledging (Fig. 1a, Table S1). nestling development period but remained higher in Intervals over which fledgling survival was moni- south than north temperate zone species with esti- tored did not differ among studies in north vs. mates of 21 3 days while correcting for nestling south temperate zones (t63 = 1.31, P = 0.19). period (nestling period: t38 = 3.02, P = 0.004; Fledgling survival estimated over the total region: t38 = 5.40, P < 0.001; Fig. 2a). A similar rela- interval monitored was higher in south temperate tionship was also true for fledgling survival estimates zone species whether based on monitoring at across all monitoring period lengths, controlled for 21 3 days post-fledging (Fig. 1b; t63 = 6.22, monitoring period (nestling period: t61 = 4.26, P < 0.001) or on all monitoring intervals (Fig. 1c; P < 0.001; region: t61 = 4.51, P < 0.001; monitoring t63 = 3.55, P < 0.001). Log-transformed nestling interval: t61 = 2.57, P = 0.013; Fig. 2b). period did not differ between zones (Fig. 1d; Fledgling survival obtained at 21 3 days post- t63 = 0.20, P = 0.84). Annual adult survival proba- fledging (Fig. 3a) and over all monitoring intervals bility was higher among south temperate than (Fig. 3b) was related to adult survival but not north temperate species (Fig. 1e; t58 = 6.78, clutch size, while controlling for nestling period

Table 2. Coefficients and standard errors (B (se)), t-values, broad relationships demonstrate that relative and significance from phylogenetic generalized least squares development of offspring at fledging differs with using the CAPER package (Orme 2013) to explain variation in nestling period. Thus, the increase in fledgling fledgling survival among species of north and south temperate zones. Analyses are first presented for all species with (a) 18– survival with nestling period in north and south 24 days and (b) all intervals of monitoring. The Cape Pendu- temperate zones (Fig. 2) suggests an important line Tit Anthoscopus minutus is an outlier (Fig. 2) and analy- role of developmental stage at fledging on ses are conducted with this outlier removed for (c) 18–24 days survival. and (d) all intervals of monitoring. On the other hand, the higher fledgling survival of south compared with north temperate species Variable B (se) tP-value for the same nestling period suggests that relative (a) 18–24 days’ monitoring of fledgling survival (df = 33) development of offspring at fledging differs Adult survival probability 0.432 (0.197) 2.20 0.035 between zones. The actual mechanistic differences Clutch size 0.038 (0.024) 1.58 0.12 in development that are key to fledgling survival Nestling period (days) 0.962 (0.223) 4.31 < 0.001 (b) All monitoring intervals of fledgling survival (df = 55) remain largely unstudied, but a couple of infer- Adult survival probability 0.331 (0.186) 1.78 0.081 ences are possible. First, relative body mass influ- Clutch size 0.037 (0.022) 1.73 0.090 ences fledgling survival in many species across Nestling period (days) 0.896 (0.187) 4.80 < 0.001 latitudes (e.g. Krementz et al. 1989, Linden et al. Monitoring interval 0.010 (0.004) 2.54 0.014 1992, Both et al. 1999, Green & Cockburn 2001, Anthoscopus minutus excluded (c) 18–24 days’ monitoring of fledgling survival (df = 32) Lloyd et al. 2009, Tarwater et al. 2011), suggesting Adult survival probability 0.655 (0.182) 3.61 0.001 greater body mass at fledging may reduce starva- Clutch size 0.027 (0.021) 1.27 0.21 tion risk or indicate better muscle development. Nestling period (days) 0.776 (0.200) 3.88 < 0.001 Yet, relative body mass at fledging does not differ fl = (d) All monitoring intervals of edgling survival (df 54) between fast (north temperate) and slow (tropical) Adult survival probability 0.504 (0.186) 2.71 0.009 Clutch size 0.030 (0.021) 1.45 0.15 life histories (Martin 2015). The lack of difference Nestling period (days) 0.773 (0.182) 4.26 < 0.001 in relative body mass despite differences in fledg- Monitoring interval 0.010 (0.004) 2.67 0.010 ling survival between zones may indicate that body mass is not a critical determinant of fledgling survival in a broader evolutionary context. This conclusion gains support from studies that have and monitoring interval (Table 2a,b). However, found body mass at fledging did not predict fledg- one species (Cape Penduline Tit Anthoscopus min- ling survival (e.g. Sullivan 1989, Anders et al. utus) was an influential outlier (Fig. 3). If that out- 1997, Sankamethawee et al. 2009, Jackson et al. lier is excluded, then fledgling survival was 2011). strongly related to adult survival, but still not to Secondly, and in contrast, relative wing devel- clutch size, while controlling for nestling period opment differs between north temperate and trop- and monitoring interval (Table 2c,d; Fig. 3). Nest- ical zones for the same nestling period and these ling period was a strong determinant of fledgling differences are associated with differences in life survival in all cases (Table 2). histories (Martin 2015). In particular, smaller clutch sizes and higher adult survival (i.e. slower life histories) are associated with relatively greater DISCUSSION wing development (Martin 2015). The increase in Nest predation is widely thought to be a strong fledgling survival in species with higher adult selection pressure that constrains nestling develop- survival controlled for development time (Fig. 3) ment time (Reme^s & Martin 2002, Martin et al. may indicate similar effects of slow life histories 2011) and this constraint may then impact fledg- for offspring quality as reflected by wing develop- ling survival (Cox et al. 2014, Martin 2014, ment and the consequences for fledgling survival. 2015). Nestling development time was a strong This possibility makes sense given that most stud- influence on fledgling survival within and between ies find that predation is the primary source of the two temperate zones (Fig. 2). Both relative fledgling mortality, and most mortality occurs dur- body mass and wing lengths increase with nestling ing the first few days after fledging, when mobility period among north temperate and tropical spe- is most restricted (Martin 2014). However, relative cies (Cheng & Martin 2012, Martin 2015). These wing development at fledging was not tested across

studies, and therefore more direct tests of wing Understanding fledgling survival is important development and mobility relative to fledgling sur- because it is a critical component of annual vival are needed across species. demography that can differ from nest predation While adult survival predicted fledgling survival, (Streby & Andersen 2011) and thereby have a crit- clutch size did not. Clutch size and adult survival ical influence on selection on life-history strategies are strongly correlated within and across north and (Martin 2014, 2015). We found strong evidence south temperate zones (t58 = 4.64, P < 0.001; that south temperate zone passerine birds exhibit also Ghalambor & Martin 2001, Lloyd et al. higher fledgling survival within the first few weeks 2014). This covariance makes separation of clutch after fledging than north temperate zone species. size and adult survival effects difficult. Clutch size South temperate species also exhibit extended was examined because of its possible influence on post-fledging care and natal philopatry in compar- parental investment per offspring (Pianka 1970, ison with north temperate species, which is Saino et al. 1997, Martin 2015). However, invest- expected to further favour increased fledgling and ment per offspring is also influenced by total par- juvenile survival (Russell et al. 2004). Age- and ental effort and this may vary somewhat stage-specific mortality can have a strong influence independent of clutch size because of interacting on the evolution of life-history strategies influences of adult and nest mortality on parental (Dobzhansky 1950, Pianka 1970, Reznick et al. effort (Martin 2014, 2015). The higher fledgling 1990, Martin 2002, 2015, Martin et al. 2015). survival of south temperate zone species compared Moreover, age- and stage-specific mortality may with north temperate zone species is consistent interact through habitat saturation and constraints with the hypothesis that low adult mortality in the on independent breeding (Kokko & Lundberg south temperate zone (e.g. Ghalambor & Martin 2001). Thus, the higher fledgling survival of south 2001, Lloyd et al. 2014) favours fewer offspring temperate zone species appears to reflect differen- (Moreau 1944, Martin 1996, 2002, Martin et al. tial life-history evolution in the region. 2006) and increased parental investment per offspring (Skutch 1949, MacArthur & Wilson 1967, We thank the many field assistants and co-workers who Pianka 1970), leading to increased fledgling sur- helped locate and monitor nests and the survival of fl vival (Martin 2015). post- edging young each year, particularly Sonya Auer, Justin Shew, Anna Chalfoun, David Nkosi, Andrew Tay- Fledgling survival may be underestimated if lor, Simon Davies, Riccardo Ton and Ron Bassar. We fl edglings disperse out of the study area during the thank Gert Greef, Hilton Westman and ESKOM for monitoring period, because disappearance of fledg- permission to work at Koeberg Nature Reserve. Com- lings was treated as mortality in all studies ments from Richard Major and two anonymous review- included in our analysis. Therefore, lower fledgling ers considerably improved the manuscript. This work survival in the north than south temperate zone was supported in part through National Science Foun- could simply reflect north temperate zone species dation grants (INT-9906030, DEB-0841764, DEB- fi 1241041 to T.E.M.) and National Research Foundation being more dispersive during the rst 3 weeks grants (to P.L.). Research and banding activities were fl post- edging (e.g. Vega-Rivera et al. 1998, White licensed by the CapeNature and SAFRING, the South & Faaborg 2008, Fisher & Davis 2011, Streby & African bird-ringing scheme that issued the numbered Andersen 2013), leading to lower detectability. metal rings, and approved by the Animal Ethics Com- We believe this possibility is not overly important mittee, University of Cape Town and IACUC #059- due to the use of radiotelemetry to monitor fledg- 10TMMCWRU at the University of Montana. Any use fi ling survival in 57% of the north temperate species of trade, rm or product names is for descriptive pur- fi poses only and does not imply endorsement by the US and high con dence in lack of dispersal during the Government. post-fledging period in the remainder (see Meth- ods). 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