The quality of a breeding site may have major ﬁtness consequences. A fundamental step to under- standing the process of nest-site selection is the identiﬁcation of the information individuals use to choose high-quality nest sites. For secondary cavity-nesting bird species that do not add nest lining ma- terial, organic remains (faeces, pellets) accumulated inside nest cavities during previous breeding events may be a cue for high-quality nest-sites, as they contain information about past successful breeding and may improve thermal insulation of eggs during incubation. However, cavities in which breeding was successful might also contain more nest-dwelling ectoparasites than unoccupied cavities, offering an incentive for prospective parents to avoid them. We exposed breeding cavity-nesting lesser kestrels (Falco naumanni) to nestbox dyads consisting of a dirty (with a thick layer of organic substrate) and a clean nestbox (without organic material). Dirty nestboxes were strongly preferred, being occu- pied earlier and more frequently than clean ones. Hatching success in dirty nestboxes was signiﬁcantly higher than in clean ones, suggesting a positive effect of organic nest material on incubation efﬁciency, while nestbox dirtiness did not signiﬁcantly affect clutch and brood size. Nestlings from dirty nestboxes had signiﬁcantly higher ectoparasite load than those from clean nestboxes soon after egg hatching, but this difference was not evident a few days later. Nest substrate did not signiﬁcantly affect nestling growth. We concluded that nest substrate is a key driver of nest-site choice in lesser kestrels, although the adaptive value of such a strong preference appears elusive and may be context-dependent. Key words: Carnus hemapterus, ectoparasites, nestbox, nest substrate, nest-site selection Breeding and oviposition site quality affects individual fitness, animals can evaluate to decide where to settle and breed may be di- implying that parents should be highly selective when making deci- verse, including nest substrate quality (e.g. in species where it pro- sions about where to lay their eggs and rear their offspring vides direct fitness benefits, such as Lepidoptera; review in Renwick (Refsnider and Janzen 2010). As a consequence, animals continu- and Chew 1994), conspecific behavior, reproductive success (the so- ously sample the environment to gather useful information for called “public information”; Valone and Templeton 2002), per- choosing the optimal breeding site. The type of information that ceived predation risk (Eggers et al. 2006), presence of parasites V C The Author(s) (2018). Published by Oxford University Press. 693 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact firstname.lastname@example.org Downloaded from https://academic.oup.com/cz/article-abstract/64/6/693/4835146 by Ed 'DeepDyve' Gillespie user on 11 January 2019 694 Current Zoology, 2018, Vol. 64, No. 6 (Rosenheim 1988), or a combination of those factors. Nest-site On the whole, although some studies suggest the preference or choice may also be context-dependent, with individuals choosing avoidance of previously used nest cavities (see above), nest-site low-quality nest-sites if no better options are available in the sur- choice in secondary cavity-nesters appears rather insensitive to the roundings (Stanback and Rockwell 2003). presence of old nest material, with several studies not reporting any Cues used by prospecting individuals for choosing their breeding clear preference pattern (e.g., Olsson and Allander 1995; Toma ´s site may be based on direct observations of conspecific presence, et al. 2007; review in Mazgajski 2007). Furthermore, the adaptive which may generate territorial aggregations (“conspecific attraction”; value of breeding in previously used versus non-used nest cavities Stamps 1988), or conspecific behavior, such as offspring feeding effort has yet to be elucidated. In the majority of studies conducted so far, by parents, which is expected to provide reliable information about no significant impact of the presence of old nest material was found breeding patch quality (Doligez et al. 2002; Pa ¨rt and Doligez 2003; on clutch size, fledging success or nestling condition (review in Ward 2005). Moreover, prospecting individuals may directly assess Mazgajski 2007). Statistically significant fitness effects (mostly conspecifics’ breeding success (quantity/condition of offspring) in a negative) of breeding in cavities with old nest material have been re- given season and use this information to decide where to settle and ported only occasionally (e.g., Toma ´ s et al. 2007; Gonza ´ lez-Braojos breed subsequently (Boulinier and Danchin 1997). et al. 2012; review in Mazgajski 2007). Prospecting individuals may also exploit indirect cues of conspe- Lesser kestrels Falco naumanni appear to make wide use of pub- cific reproduction, such as tracks or signs of reproductive activity lic, social, and environmental information for dispersal, colony-site occurring in the past. In birds, these may include the density of old settlement decisions, and nest-site selection, with breeding success of nests (e.g., Erckmann et al. 1990; Gergely et al. 2009; Ringhofer conspecifics being an important cue (Negro and Hiraldo 1993; and Hasegawa 2014), or, in cavity-nesting species, the presence of Serrano et al. 2001, 2003; Aparicio et al. 2007). In lesser kestrel col- old nest material within suitable nest cavities (review in Mazgajski onies, most successful breeding attempts take place in previously 2007; see also Brown and Shine 2005 for a study of reptiles). The occupied cavities, which are also occupied earlier compared to sel- presence of old nest material in nest cavities (nest lining material, dom used cavities (Negro and Hiraldo 1993). However, to our faeces, pellets, prey remains, feathers, etc.) does in fact contain in- knowledge, no study has experimentally addressed whether the formation about previous breeding activity: cavities containing such presence of old nest material is used as a cue for choosing specific material may be preferred as they may be perceived as being more nest-sites within a breeding colony. We performed a nestbox choice suitable than similar cavities where no sign of previous reproduction experiment whereby breeding pairs had the opportunity to select ei- is evident (Brown and Shine 2005; Sumasgutner et al. 2014). At the ther a nestbox without organic nest material (clean nestbox) or a same time, in species that do not add any material to line their nest, paired nestbox with a thick organic layer from previous nesting at- the presence of organic material from previous breeding events may tempts (dirty nestbox). Based on previous studies carried out in this be a further cue to nest-site quality because it may contribute to in- species (Negro and Hiraldo 1993) and in the closely related crease thermal insulation and reduce egg heat loss (Hilton et al. Eurasian kestrel (Sumasgutner et al. 2014), we expected a preference 2004; Mazgajski 2007; Mainwaring et al. 2014), potentially im- for settling in dirty nestboxes. In addition, by exploiting a larger proving incubation efficiency. sample of unpaired dirty and clean nestboxes and adopting a cor- In line with the above, experimental removal of old nest material relative approach, we assessed whether breeding in dirty versus decreased nestbox occupancy in the subsequent breeding season in clean nestboxes was associated with variation in breeding perform- burrowing owls Athene cunicularia, with birds returning from migra- ance and nestlings’ mortality, ectoparasite load, and early growth tion avoiding cleaned nestboxes (Riding and Belthoff 2015). Similarly, patterns. female Eurasian kestrels Falco tinnunculus laid eggs later in experi- mentally cleaned nestboxes compared to uncleaned ones, indicating a Materials and Methods preference for old nest material (Sumasgutner et al. 2014). A prefer- ence for nestboxes with old nest material was observed also in some Study species, study area and general methods passerine species, such as the pied flycatcher Ficedula hypoleuca The lesser kestrel is a small (120 g), colonial breeding, Afro- (Orell et al. 1993; Mappes et al. 1994; Olsson and Allander 1995), Palearctic migrant raptor. European individuals reach breeding the house wren Troglodytes aedon (Thompson and Neill 1991), and areas in February/March, and start laying eggs between late April the eastern bluebird Sialia sialis (Davies et al. 1994). and early May. Females lay 3–5 eggs (single brooded), which are In spite of the potential benefits of choosing cavities with old incubated for 30 days. Nestlings fledge when 40 days old. Being nest material, some species/populations avoid breeding in previously a secondary cavity-nester, the lesser kestrel does not build its own used cavities (e.g. Merino and Potti 1995; Mazgajski 2003; review cavity: it breeds in holes and cavities in rocks, ruins, roof tiles of in Mazgajski 2007). Breeding in previously used cavities may indeed buildings in urban areas or isolated abandoned farmhouses in the entail non-trivial costs. Nests containing old nest material may be countryside, and it does not add any nest lining material (Cramp subjected to increased predation risk due to predators memorizing 1998). However, it readily settles in nest cavities containing an or- nest positions (e.g. Sonerud 1985; Nilsson et al. 1991). Importantly, ganic substrate resulting from previous breeding attempts, similarly organic nest material is a highly favourable ground for the develop- to other secondary cavity-nesters (Cramp 1998; Negro and Hiraldo ment of nest-dwelling ectoparasites and pathogens (Rendell and 1993). Verbeek 1996). Nest-dwelling parasites infest adults and especially The study was carried out during April–July 2016 in the city of nestlings, eventually impairing individual growth, condition and fit- Matera (Southern Italy; 40 67’ N, 16 60’ E), hosting a large colony ness (Møller et al. 1990; Martı ´nez et al. 2011). Nest parasites can of 1,000 lesser kestrel pairs (La Gioia et al. 2017). Several hun- impair fitness either directly (e.g. in the case of blood sucking by dreds of nestboxes were deployed in 2008–2010 within the frame- haematophagous species; e.g. Heylen and Matthysen 2008; Toma ´s work of the LIFE Project “Rapaci Lucani” (LIFE05NAT/IT/00009), et al. 2008) or indirectly, transmitting bacterial or viral pathogens so that presently an unknown (but likely large) fraction of pairs and spreading disease (Møller et al. 1990). breeds in nestboxes. We relied on 175 nestboxes that were placed on Downloaded from https://academic.oup.com/cz/article-abstract/64/6/693/4835146 by Ed 'DeepDyve' Gillespie user on 11 January 2019 Podofillini et al. Nest-site choice in the lesser kestrel 695 the roof terraces of two large buildings located 500 m apart in the hatching, mixed model with nestbox identity as a random intercept city center. Nestboxes were made by a hollow refractory brick effect, effect of sex: F ¼ 0.01, P ¼ 0.98), sex did not confound 1, 167 (300 300 370 mm external size) closed by two wooden panels nestling rank assignment. (300 300 20 mm), the frontal one with an entrance hole of As proxies of breeding performance, we used clutch size (number 65 mm diameter. Ventilation of the nest chamber was provided by 9 of eggs laid), hatching success (proportion of eggs hatched in a small holes (10 mm) on the wood panels. The front panel could be clutch), and brood size (number of nestlings in the nest), the latter easily opened for nest inspection. being recorded at each monitoring session. Upon deployment, the floor of all nestboxes was coated with a As a part of a parallel study, unrelated to the present one, in a layer of sand and fine gravel to increase insulation towards the ce- sample of 44 nestboxes (20 belonging to dyads and 24 unpaired) out ment brick and reduce the probability of egg breakage during nest of the 98 where the clutch size was completed and incubation inspection or egg turning by the female. started, we performed a food supplementation by which we pro- In February 2016, before arrival of lesser kestrels at the colony vided laying pairs with laboratory mice after the laying of the first site, nestboxes were organized in “dyads” of clean and dirty nest- egg and during the early nestling period. Pairs breeding in non- boxes (N ¼ 40 dyads, see below) and “unpaired” nestboxes [24 old supplemented nestboxes served as controls. This concomitant ex- (dirty) nestboxes (all of which had been used for breeding and roost- periment, whose results will be reported elsewhere (S. Podofillini ing in previous years) and 71 new (clean) nestboxes (deployed in et al., manuscript in preparation), could not alter nestbox occupa- February 2016 and never previously used by lesser kestrels)]. Both tion patterns because supplementation started after a given nestbox dyads and unpaired (dirty and clean) nestboxes were randomly pos- had been chosen by the kestrels (i.e., after the first egg had been itioned along the entire perimeter of each terrace, at a minimum dis- laid). tance of 2 m from each other. Old nestboxes had never been cleaned after their original deployment (2008–2010). Hence, most Assessment of nest-site preference old nestboxes had a thick (5 cm), hard coating of organic material Nest-site preference was experimentally investigated based on 40 deriving from previous breeding events spread over the floor of the nestbox dyads. A dyad consisted of two paired nestboxes placed nestbox (see also section “Assessment of nest-site preference”). The side-by-side (the sides were touching each other), one of which was position of all old nestboxes was randomly shuffled in February “dirty” while the other was “clean”, with the two front panels with 2016 to accomodate deployment of new clean nestboxes and to the entrance holes pointing towards the same direction (Figure 1). In form dyads, as well as to avoid nest recognition bias (see section this way, we aimed at forcing the choice between the dirty and the “Assessment of nest-site preference”). clean nestbox while eliminating any confounding effect due to nest All nestboxes were regularly checked throughout the breeding orientation, position (e.g., shaded versus unshaded, disturbance season to record breeding bird performance. Nestboxes were level), nestbox wear (see below), predation risk, and surrounding checked until the oldest nestling in the brood was 16 days old (we habitat quality. refrained from checking nestboxes after that age because nestlings When assembling dyads, one old nestbox, in which clear signs of started wandering outside the nest and freely moved on the terraces, previous breeding attempts were obvious, was paired with an identi- making monitoring difficult and increasing the risk of inducing pre- cal, brand-new nestbox. Old nestboxes, besides containing com- mature fledging); over this period, each nestbox was checked five pressed organic material (mostly consisting of prey remains, times (i.e., five monitoring sessions), with monitoring sessions regurgitated pellets, faeces, feathers, etc.), had a rather worn exter- occurring at an average of 0.8 (range 0–3), 3.0 (2–5), 5.3 (4–9), 7.9 nal appearance (i.e., faded colouration), including front panels. To (7–11), and 16.0 (14–18) days from hatching of the first egg in a remove any confounding effect of external nestbox wear on nest-site nestbox, respectively. preference, we shuffled front panels and nest material between old Upon hatching, nestlings were individually marked with differ- and new nestboxes according to all eight possible combinations ent combinations of small black dots on the down of the nape using (Figure 1), each of which was applied five times (there were five a non-toxic black permanent marker, then ringed with metal rings dyads for each combination). The old nest material was carefully when 10 days old. Nestling body mass (accuracy of 0.1 g using an removed from any old nestbox included in a dyad, vigorously electronic scale) and ectoparasite load (see below) were recorded minced, shaken, and placed back either into the old or the new nest- from the first to the fourth monitoring session, while tarsus (accur- box according to the predetermined combinations. To avoid any acy 0.1 mm with dial calliper) and forearm length we report in this side bias, the old nestbox was placed alternately on the left or the study (accuracy 1 mm with a ruler) were recorded at the fourth right side. Hence, dirty nestboxes within a dyad were characterized monitoring session only. At the fourth monitoring session, a small by the presence of old, organic nest material (a cue of previous (200 ml) blood sample was collected in capillary tubes by punctur- breeding attempts) while clean nestboxes did not have any organic ing the brachial vein with sterile needles in order to determine nest- nest material but only a thin layer of gravel and sand on the bottom ling sex. This was achieved by means of polymerase chain reaction of the nestbox (no cue of previous breeding attempts). Dyads were amplification of the sex-specific avian CHD-1 gene, following stand- randomly interspersed among unpaired nestboxes along the perim- ard protocols (Griffiths et al. 1998). eter of terraces, and were positioned at a minimum distance of 2 m Each nestling in a given nestbox was ranked according to hatch from nearby dyads or unpaired nestboxes (see also section “Study order. When two or more nestlings were first found hatched on the species, study area and general methods”). same monitoring session, rank was assigned based on body mass Since lesser kestrels show a high natal and breeding philopatry (larger nestlings had higher rank). The first hatched nestling was as- (57% of first-time breeders recruit to the natal colony, and 72% signed the highest rank (i.e. rank 1), while subsequent nestlings were of adults return to the colony where they bred in the previous year; assigned lower ranks (i.e. 2–5; no more than 5 nestlings were found Negro et al. 1997; Serrano et al. 2001), nest-site preference could be in each nestbox). As there were no statistically significant sex differ- affected by previous experience and recognition of previous year’s ences in body mass at hatching (body mass recorded within 1 day of nest-sites. To avoid this bias, in February 2016, all old nestboxes Downloaded from https://academic.oup.com/cz/article-abstract/64/6/693/4835146 by Ed 'DeepDyve' Gillespie user on 11 January 2019 696 Current Zoology, 2018, Vol. 64, No. 6 to overwinter inside nest organic material, waiting for potential hosts to settle (Roulin 1998; Valera et al. 2006). Nestlings were inspected to estimate the number of adult flies on the furcula (interclavicular depression) and on the right and left axillae (underwings) from the first to the fourth monitoring session. We could not accurately count all flies as they were fast-moving and hid rapidly within the nestling down upon handling. Hence, nestling ectoparasite load was rapidly scored upon handling each nestling by estimating vis- ible flies for each body district on a 0–3 scale (0: no ectoparasites, 1: 1–3 flies, 2: 4–6 flies and 3:> 6 flies) and then computing the mean value between all body districts before statistical analyses. Statistical analyses Nest-site preferences were assessed based on the sample of 40 dyads. The number of dyads with occupied dirty versus clean nestboxes was compared by means of a binomial test for deviation from equality. The effects of nestbox dirtiness on laying date, breeding perform- ance, nestling mortality, ectoparasite load, and growth patterns were assessed based on pooling data collected both from dyads and unpaired nestboxes. This was necessary because of the very low sample size of occupied clean nestboxes belonging to dyads (see “Results” section). The effect of nestbox dirtiness on proxies of breeding performance [clutch size, hatching success, brood size at 8 Figure 1. Schematic illustration of the different combinations adopted to ran- and 16 days from hatching of the first egg] was evaluated by general- domize nest material, front panel, and cement block in dyads of adjacent clean ized linear models (GLMs) with nestbox dirtiness (clean versus and dirty nestboxes. The combinations were illustrated using white panels and dirty) and laying date (day of laying of the first egg) as predictors (to white cubes for front panels and cement blocks installed for ﬁrst time in 2016; control for seasonal variation in breeding performance). Hatching brown panels and gray cubes for old front panels and cement blocks white success was expressed as the proportion of eggs hatched on clutch holes: clean nestboxes; white and gray holes: dirty nestboxes. The dirty nest- box was alternately placed on the left or right side, to avoid any side bias. A size, and tested in a binomial GLM using the events/trials syntax. In dyad was interspersed in random order between unpaired nestboxes or other models of clutch and brood size (count variables), we assumed a dyads along the perimeters of the terraces of two buildings, and was at a min- Poisson error distribution. To reduce noise in estimates of egg hatch- imum distance of 2 m from any nearby dyad/unpaired nestbox. ing success and nestling survival, we excluded from the analysis all 16 nests where clutch size was completed but no eggs hatched (likely (either included in dyads or not) were randomly shuffled along the deserted by parents; 16% of the 98 nestboxes where clutch size was perimeter of terraces. completed; see “Results” section). This did not affect our conclu- Nest-site preference was determined by assessing the settlement sions concerning the effect of nestbox dirtiness on other breeding of a breeding pair in each nestbox of the dyad (laying of eggs). parameters because the proportion of nests abandoned before hatch- Laying date of the first egg was used to establish which of the two ing did not significantly differ between clean (0.22) and dirty (0.12) nestboxes of a dyad was occupied first (in case both nestboxes of a nestboxes [binomial GLM: effect of dirtiness, estimate (SE): 0.39 dyad were occupied). Lesser kestrel females may occasionally start (0.59), Z¼0.66, P ¼ 0.51; effect of laying date, estimate (SE): laying one egg in a nest and then lay the other eggs in nearby nests, 0.07 (0.04), Z ¼ 1.68, P ¼ 0.09], though there was a trend for clean especially when several identical nestboxes are placed nearby (au- nestboxes to be abandoned more frequently than dirty ones. thors’ personal observation). This was not the case in our dyads, The effect of nestbox dirtiness on nestling mortality was investi- where occupancy mostly occurred in only one of the two nestboxes, gated using a binomial mixed model whereby mortality of each nest- and when both nestboxes of a dyad were occupied, we found differ- ling (0¼ alive, 1¼ found dead or disappeared) at the fifth monitoring ent females in the nests. In one dyad, however, a single egg was laid session was the dependent variable, while nestbox dirtiness, nestling in a clean nestbox and then abandoned. This dyad was considered in rank, brood size (maximum brood size across all monitoring sessions), the analyses of nest site preferences, but excluding it did not alter laying date, and ectoparasite load (maximum ectoparasite load across our conclusions (see “Results” section). all monitoring sessions) were included as covariates. Nestbox identity was included as a random intercept effect. Nestling ectoparasite load To assess the effect of nestbox dirtiness on ectoparasite load, we We assessed ectoparasite load of nestlings by estimating infestation by ran a linear mixed model with nestbox dirtiness, nestling rank, a common, small (2 mm) haematophagous ectoparasitic fly (Carnus brood size, and laying date as predictors. We also included monitor- hemapterus, Diptera: Carnidae), whose adults infest nestlings of sev- ing session as a four-level fixed factor to control for variation in eral cavity-nesting bird species (Capelle and Whitworth 1973). ectoparasite infestation throughout the course of the nestling period. Females lay eggs in the organic nest material and the saprophagous Two-way interactions between dirtiness and all other predictors larvae thrive in the nest substrate, where they feed on detritus. The were also included in the initial model. Nestling and nestbox iden- life-cycle of this ectoparasitic fly is synchronized with that of its hosts: tity were included as random intercept effects. the peak of emergence of adult parasites from the nest material coin- We evaluated the effects of nestbox dirtiness on body mass using a cides with the hatching of hosts’ eggs (Roulin 1998). Pupae are able linear mixed model including nestbox dirtiness, nestling age, nestling Downloaded from https://academic.oup.com/cz/article-abstract/64/6/693/4835146 by Ed 'DeepDyve' Gillespie user on 11 January 2019 Podofillini et al. Nest-site choice in the lesser kestrel 697 rank, brood size (number of nestling in the nestbox at each check), the nest-site selection experiment, 38 out of 40 dyads had at least laying date, ectoparasite load, and two-way interactions between one nestbox occupied (i.e., 95% of dyads had at least one nestbox dirtiness and nestling rank, brood size or ectoparasite load, as well as occupied). Among the 38 dyads with at least one nestbox occupied, the two-way interaction between nestling rank and nestling age (to ac- in 31 cases only the dirty nestbox was occupied, in 1 case only count for differential growth of nestlings differing in rank) as fixed the clean nestbox was occupied (binomial test, P< 0.001), and in effects; nestling and nestbox identity were included as random inter- 6 cases both nestboxes were occupied. Among the latter 6 dyads, cept effects. The models of tarsus and forearm length had a fixed ef- the dirty nestbox was occupied earlier in 5 out of 6 cases, the mean fect structure identical to the model of body mass, but as we had a laying date in the dirty nestbox of the dyad being 12.0 (4.1 SE) single measurement per nestling, we included only nest identity as a days earlier than in the clean one (Wilcoxon matched-pairs random intercept effect. Brood size and ectoparasite load referred to test: Z ¼ 2.02, P ¼ 0.043). Considering both unpaired nestboxes the maximum values recorded for that nestbox/nestling during the and dyads, mean laying date in dirty nestboxes was May 13 four monitoring sessions. Age effects on growth were controlled for (1.0 SE, N ¼ 57), while it was May 18 (1.3 SE, N ¼ 41) in clean by including the linear term of age only. Despite generally growth ones (t ¼ 2.89, P ¼ 0.005). curves are sigmoidal-shaped (Starck and Ricklefs 1998), nestling growth of lesser kestrels up to 11 days (out of a nestling period of Nestbox dirtiness, breeding performance, and nestling 30 days) did not significantly deviate from linearity (details not mortality shown for brevity). The effects of nestbox dirtiness (clean versus dirty) on clutch size, In all models, two-way interaction terms were removed in a sin- hatching success and brood size was analysed in the sample of 82 gle step if non-significant (P> 0.05). Full models (including all non- nestboxes where at least one egg hatched. significant interactions) are reported in Supplementary material. Clutch size did not significantly differ between clean and dirty Since the lesser kestrel is sexually size dimorphic, females being nestboxes (Table 1), while hatching success of eggs laid in dirty nest- heavier and larger than males (Cramp 1998), we performed explora- boxes (percentage hatched ¼ 86%) was slightly but significantly tory analyses on the subsample of 209 nestlings (out of 244 hatched) higher than that of eggs laid in clean nestboxes (76%) (Table 1). In that were alive at the fourth monitoring session (when blood sam- spite of a significantly higher hatching success in dirty nestboxes, pling was performed) to investigate possible effects of nestling sex brood size did not significantly differ between clean and dirty nest- (0 ¼ female, 1 ¼ male) on the response variables. Mixed models boxes (Table 1). Breeding performance of lesser kestrels did not sig- (with the same random intercept effects as detailed above) did not nificantly vary across the breeding season, as shown by the lack of reveal any statistically significant difference in response variables ac- significant effects of laying date (Table 1). cording to sex [parasite load: estimate (SE): 0.07 (0.04), F 1, The probability that a nestling had died by the last monitoring ¼ 3.71, P ¼ 0.06; body mass: 1.55 (1.65), F ¼ 0.87, 169 1, 200 session was not significantly affected by nestbox dirtiness (Table 2), P ¼ 0.52; tarsus length: 0.20 (0.48), F ¼ 0.18, P ¼ 0.67; fore- 1, 185 while it was significantly higher among low-ranking nestlings arm length: estimate (SE): 0.38 (0.84), F ¼ 0.20, P ¼ 0.65]. 1, 187 (Table 2). Hence, for simplicity and to avoid sacrificing sample size for some of the analyses, we did not consider sex effects any further in the analyses. These results indicate that nestling parasite load is not sig- Nestling ectoparasite load, body mass, and size in nificantly different between sexes and that sexual size dimorphism is relation to nestbox dirtiness not yet evident during the early nestling stage. Nestling ectoparasite load was recorded in 70 nestboxes (28 clean, To check for the possible confounding effects of the food supple- 42 dirty). The model of ectoparasite load revealed a statistically sig- mentation experiment on breeding performance traits, nestling ecto- nificant nestbox dirtiness monitoring session interaction (Table 3, parasite load, body mass and skeletal growth, all relevant models Figure 2): post-hoc tests indicated that mean ectoparasite load was were re-run while including food supplementation (supplemented significantly higher in dirty nestboxes soon after the first eggs had versus control) as a fixed effect. The effect of food supplementation hatched (i.e., in the first monitoring session) (P ¼ 0.003), whereas was never statistically significant (P-values always> 0.14; additional details not shown for brevity). Hence, for simplicity we did not con- Table 1. Effect of nestbox dirtiness on breeding performance sider this variable further. Mixed models were fitted using the lmer or glmer function of the Clean Dirty Estimate (SE) ZP “lme4” library (Bates et al. 2014) for R 3.3.1 (R Core Team 2014). Clutch size (N ¼ 82) Degrees of freedom for linear mixed models were estimated using Dirtiness 4.10 (0.14) 4.34 (0.10) 0.05 (0.11) 0.47 0.64 the Kenward–Rogers approximation (“pbkrtest” library; Halekoh Laying date – – 0.01 (0.01) 0.25 0.80 and Højsgaard 2014). Non-Gaussian GLMs and mixed models were Hatching success (N ¼ 82) not overdispersed (see “Results” section; overdispersion for non- Dirtiness 0.76 (0.04) 0.86 (0.03) 0.65 (0.29) 2.29 0.022 Gaussian mixed models was checked using the “blmeco” library; Laying date – – 0.01 (0.02) 0.04 0.97 Korner-Nievergelt et al. 2015). Brood size, day 7 (N ¼ 82) Dirtiness 2.59 (0.24) 3.16 (0.18) 0.21 (0.14) 1.54 0.12 Laying date – – 0.01 (0.01) 0.55 0.58 Results Brood size, day 15 (N ¼ 82) Dirtiness 2.25 (0.21) 2.70 (0.17) 0.19 (0.15) 1.30 0.19 Nestbox occupancy, nest-site preference, and laying Laying date – – 0.01 (0.01) 0.38 0.70 date Among unpaired nestboxes, old nestboxes were occupied signifi- Mean values (SE) of breeding parameters are reported (binomial SE for hatch- cantly more often than new ones [old nestboxes: 20/24 (83.3%), ing success). Estimates are from Poisson or binomial GLMs (for hatching suc- new nestboxes: 34/71 (47.9%); v ¼ 9.19, df ¼ 1, P ¼ 0.002). In cess). Models were not overdispersed (dispersion parameter always< 1.26). Downloaded from https://academic.oup.com/cz/article-abstract/64/6/693/4835146 by Ed 'DeepDyve' Gillespie user on 11 January 2019 698 Current Zoology, 2018, Vol. 64, No. 6 Table 2. Binomial mixed model of the effect of nestbox dirtiness on other predictors were not significant and were removed from the the probability that a nestling had died by 15 days from start of egg models (tarsus length, all P> 0.30; forearm length, all P> 0.20; see hatching Table S1 in Supplementary material). Predictors Estimate (SE) ZP Dirtiness 0.77 (0.78) 0.99 0.32 Discussion Nestling rank 1.30 (0.26) 4.95 <0.001 Brood size 0.22 (0.36) 0.62 0.53 Studies addressing the preference for dirty vs. clean nestboxes in sec- Laying date 0.08 (0.05) 1.63 0.10 ondary cavity-nesters have provided conflicting evidence, highlighting Ectoparasite load 0.57 (0.48) 1.18 0.24 broad interpopulation and interspecific differences in preference pat- terns (see Introduction and review by Mazgajski 2007). Part of this Nestbox identity was included as a random effect. The model was not over- variability may be due to different experimental designs that were not dispersed (dispersion parameter ¼ 0.81). specifically aimed at testing the effect of cues of previous breeding at- tempts on nest-site choice (Mazgajski 2007). In our carefully designed nestbox choice experiment, lesser kestrels showed a strong preference for nestboxes previously used by conspecifics, breeding pairs settling earlier and more frequently in nestboxes with a dirty substrate. The preference for dirty nestboxes is consistent with two possible explan- ations. First, it is consistent with the idea that the breeders exploit cues about previous breeding attempts by conspecifics to choose their nest cavity or colony site (Negro and Hiraldo 1993; Serrano et al. 2001, 2003; Aparicio et al. 2007). Second, it may reflect preference for a more comfortable nest substrate by females. The organic mater- ial contained in old nests, being 5 cm thick, may improve thermal in- sulation of the nest substrate, reducing heat loss, increasing incubation efficiency, and ultimately lowering the energetic costs of incubation (Mainwaring et al. 2014). Energy demands during incuba- tion largely depend on the rate at which eggs lose heat (Deeming 2002). Incubating birds, especially those (as the lesser kestrel) that lay eggs directly on the substrate without lining their nest cavity, are therefore expected to preferentially lay eggs on those substrates that minimize the energetic costs of incubation (Deeming 2002; Figure 2. Nestling ectoparasite load in each of the four monitoring sessions. Mainwaring et al. 2014). Females may have been roosting in both Filled dots represent the mean ectoparasite load of nestlings reared in dirty nestboxes of a dyad before egg laying, and this might have promoted nestboxes while empty dots refer to nestlings reared in clean nestboxes the choice for the likely more suitable organic nest substrate. Finally, (N ¼ 70 nests, 244 nestlings). Error bars represent SE. earlier egg laying in dirty vs. clean nestboxes is in accordance with the hypothesis that the sequence of cavity occupation in lesser kestrels fol- the effect of dirtiness on ectoparasite load became non-significant in lows a despotic distribution (Negro and Hiraldo 1993; see also all subsequent monitoring sessions (all P> 0.40). Moreover, ecto- Sumasgutner et al. 2014), with early-settling individuals (likely older parasite load strongly decreased with nestling rank, high-ranking and experienced breeders; Catry et al. 2017) preferentially settling in nestlings being more infested than low-ranking (smaller and late dirty nestboxes compared to clean ones. hatched) ones (Table 3). Finally, ectoparasite load markedly With regards to the fitness consequences of settling in a dirty decreased in the course of the breeding season, late clutches being nestbox, we envisage three possible explanations for the 10% significantly less infested than early ones (Table 3). Two-way inter- greater hatching success in dirty versus clean nestboxes. First, the or- actions between nestbox dirtiness and other predictors were not sig- ganic material could allow establishing a favourable nest microcli- nificant and were thus removed from the model (all P> 0.33; see mate through improved thermal insulation and humidity Table S1 in Supplementary material for details). stabilization (Hooge et al. 1999; Ardia et al. 2006), possibly increas- Nestling body mass was not significantly affected by nestbox ing egg viability (Cook et al. 2003). Indeed, previous studies have dirtiness (Table 3), while it significantly decreased in more parasi- shown that nest position and content are important factors in affect- tized nestlings, in low-ranking ones, and among nestlings reared in ing thermal insulation and in buffering the potential negative effects larger broods (Table 3). Moreover, early nestling growth was signifi- of harsh environmental conditions on embryo development (Hilton cantly lower in low-ranking nestlings, as shown by the negative sign et al. 2004; Mainwaring et al. 2014). Second, eggs laid on soft, or- of the significant age nestling rank interaction (Table 3). Other ganic rather than mineral substrate may suffer a lower risk of break- two-way interactions with nestbox dirtiness were not significant and age and/or be more efficiently incubated, resulting in lower egg were removed from the model (all P> 0.60; see Table S1 in failure rates. Alternatively, a higher hatching success in dirty nest- Supplementary material for details). boxes may be due to a better incubation performance/higher pheno- Tarsus and forearm length recorded at the last monitoring ses- typic quality of early settling (older/more experienced; Catry et al. sion were not significantly affected by nestbox dirtiness, while they 2017) pairs occupying these nestboxes. were both lower in low-ranking nestlings (Table 3). Tarsus (but not The higher C. hemapterus load of nestlings hatched in dirty ver- forearm) length was significantly larger in nestlings reared in larger sus clean nestboxes is likely due to the higher parasite load of dirty broods (Table 3). Two-way interactions between dirtiness and versus clean nestboxes. Carnus hemapterus flies undergo a Downloaded from https://academic.oup.com/cz/article-abstract/64/6/693/4835146 by Ed 'DeepDyve' Gillespie user on 11 January 2019 Podofillini et al. Nest-site choice in the lesser kestrel 699 Table 3. Mixed models of the effects of nestbox dirtiness on nestling ectoparasite load, body mass, tarsus, and forearm length, while accounting for the concomitant effects of other predictors Predictors Fdf P Estimate (SE) Ectoparasite load (N ¼ 70 nests and 244 nestlings) Dirtiness 1.95 1, 67 0.17 – Session 0.44 3, 593 0.73 – Nestling rank 11.29 1, 189 <0.001 0.05 (0.01) Brood size 0.11 1, 314 0.75 0.01 (0.02) Laying date 32.90 1, 77 <0.001 0.02 (0.01) Dirtiness session 3.41 3, 581 0.017 – Body mass (N ¼ 70 nests and 244 nestlings; covariates centred on their mean value) Dirtiness 0.01 1, 51 0.82 – Age 4960.8 1, 580 <0.001 6.96 (0.10) Nestling rank 120.2 1, 144 <0.001 4.01 (0.37) Brood size 5.2 1, 294 0.023 1.01 (0.44) Laying date 3.4 1, 68 0.07 0.15 (0.08) Ectoparasite load 4.3 1, 697 0.038 1.55 (0.75) Age nestling rank 123.5 1, 601 <0.001 0.97 (0.08) Tarsus length (N ¼ 63 nests and 202 nestlings) Dirtiness 0.36 1, 53 0.55 Age 212.1 1, 168 <0.001 1.61 (0.11) Nestling rank 63.4 1, 173 <0.001 0.97 (0.12) Brood size 4.73 1, 71 0.033 0.43 (0.20) Laying date 0.03 1, 61 0.86 0.01 (0.03) Ectoparasite load 0.65 1, 194 0.42 0.21 (0.23) Forearm length (N ¼ 63 nests and 203 nestlings) Dirtiness 3.29 1, 145 0.08 – Age 222.0 1, 123 <0.001 2.78 (0.19) Nestling rank 63.6 1, 181 <0.001 1.82 (0.23) Brood size 3.89 1, 67 0.053 0.58 (0.30) Laying date 1.49 1, 57 0.23 0.05 (0.04) Ectoparasite load 0.01 1, 175 0.98 0.01 (0.46) Models for ectoparasite load and body mass included nestbox and nestling identity as random effects, while models for tarsus and forearm length included only nestbox identity as a random effect. prolonged diapause when hosts are absent from the nest cavity, and adaptive, implying that settlement decisions reflect fitness benefits adult emergence is synchronized with nestling hatching (Roulin (in terms of higher breeding success and/or survival; see Orians and 1998). However, ectoparasite load of nestlings raised in clean versus Wittenberger 1991; Martin 1998; Chalfoun and Schmidt 2012), but dirty nestboxes became very similar within a few days after hatching this assumption has only seldom been tested (Brambilla and Ficetola of the first egg, likely because of ectoparasite dispersal between 2012). In secondary-cavity nesters, the effects of nest dirtiness on re- nearby nestboxes to reduce competition for access to hosts (e.g., productive parameters are unclear; the majority of studies have Dawson and Bortolotti 1997). Moreover, ectoparasite load strongly shown no obvious effects of nest material from previous breeding decreased over the course of the breeding season, late broods being events on fitness traits, though some studies have documented weak significantly less parasitized than early ones. The seasonal decline of statistically significant (mostly negative) effects (Mazgajski 2007). C. hemapterus load is in line with previous studies (e.g., Dawson Our findings are thus in line with such previous evidence. We note and Bortolotti 1997; Sumasgutner et al. 2014), and may be due to however that the detection of significant fitness effects of nest-site natural variation in abundance through the parasite life-cycle preference for previously used nests may be context-dependent. It is (Roulin 1998). known that lesser kestrels use conspecific presence as a major cue The lack of significant effects of nestbox dirtiness on nestlings’ when deciding where to nest and when to breed (Serrano et al. early growth patterns suggests that the higher ectoparasite load of 2003), and our study site may in fact act as a single huge colony of dirty nestboxes is of seemingly minor importance for nestling fitness 1,000 breeding pairs (La Gioia et al. 2017). In this context, selec- (Sumasgutner et al. 2014), in spite of the higher C. hemapterus para- tion of different nest-sites may not be so relevant in terms of fitness sitism of nestlings hatched in dirty nestboxes that we observed soon because the high number of individuals occurring at this colony may after hatching. Together with the observation that breeding success indicate favourable breeding conditions (for instance, larger colonies in dirty nestboxes was not lower than in clean ones, this finding sug- are mostly settled in sites that are less accessible to predators; gests that breeding in dirty nestboxes does not entail fitness costs Serrano et al. 2004). However, in a different context, with small col- (e.g., Sumasgutner et al. 2014). onies that are sparsely distributed through the landscape (thus more On the whole, our results did not provide strong evidence that difficult to be detected by prospecting individual kestrels), the pres- breeding in dirty nestboxes provides fitness payoffs in terms of im- ence of organic material derived from previous breeding attempts in proved reproductive output. Studies of nest-site or breeding habitat a cavity would be an important cue for settlement at a suitable choice commonly assume that observed preference patterns are breeding site and could have significant fitness consequences. Downloaded from https://academic.oup.com/cz/article-abstract/64/6/693/4835146 by Ed 'DeepDyve' Gillespie user on 11 January 2019 700 Current Zoology, 2018, Vol. 64, No. 6 Other findings emerging from this study, unrelated to nestbox Acknowledgments dirtiness, are briefly discussed below. We thank the Provveditorato Interregionale per le Opere Pubbliche (especially First, parasite load negatively affected body mass growth, sug- A. Cecca, M. Cristallo, and P. Cifarelli), the Comune di Matera, Ufﬁcio gesting that intense C. hemapterus parasitism may entail fitness Scuole, the Director of the Istituto Comprensivo “G. Minozzi”, M. R. costs for nestlings (e.g. Hoi et al. 2010). Alternatively, the negative Santeramo, and the employees of the Provincia di Matera (especially N. effect of C. hemapterus parasitism on nestling body mass may be in- Braia, A. Pierro, D. Venezia, and N. Savino) for authorizing (and tolerating) our work on the breeding colonies, as well as for constant support during ﬁeld direct, resulting from higher parasitism in clutches with low-quality activities. We also wish to thank C. Catoni, I. Costa, S. Frau, S. Secomandi, nestlings (i.e. nestlings with a smaller cutaneous immune response; C. Soravia, C. Bonaldi and M. Saba for assistance with ﬁeldwork. Finally, we Bize et al. 2008), or from greater exposure to pathogens that may be thank the Editor, Dr Zhi-Jun Jia, and anonymous reviewers for constructive transmitted through C. hemapterus blood meals. criticisms that helped improving previous versions of the article. Nestboxes Second, the higher C. hemapterus load in high- versus low- were built and purchased under the framework of the LIFE Project “Rapaci ranking nestlings is consistent with the idea that ectoparasites’ host Lucani” (LIFE05NAT/IT/00009) and were designed by G. Ceccolini. Study selection is non-random. Carnus hemapterus seem to aggregate in from the Naumanni76 team (paper#01). larger numbers on older/heavier nestlings, suggesting avoidance of smaller and/or poorer condition nestlings within broods (e.g. Dawson and Bortolotti 1997; Valera et al. 2004; Bize et al. 2008; Author contributions Hoi et al. 2010; but see Roulin et al. 2003). This may occur because: 1) parasites can less easily obtain abundant/high-quality food D.R., J.G.C., M.V., S.Po., and M.G. conceived the study and wrote the paper, resources from such hosts, decreasing their own fitness; 2) lesser with inputs from E.D.C. and N.S.; S.Po., A.C., E.F., S.Pi., L.S., J.G.C., kestrels show a relatively large hatching asynchrony [days between E.D.C., M.G., and D.R. conducted ﬁeldwork and collected the data; S.Po., hatching of the first and the last egg in a clutch: 2 days (range 1–10); D.R., J.G.C., and N.S. analyzed the data. our unpubl. data], whereby early hatched hosts are the only target of parasites before hatching of their younger siblings; 3) smaller References hosts simply provide less resources for parasites (in terms of total blood amount flow/feeding space available on the nestling skin). Aparicio JM, Bonal R, Munoz ~ A, 2007. Experimental test on public informa- tion use in the colonial Lesser Kestrel. Evol Ecol 21:783–800. 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