Keeping it regular: Development of thermoregulation in four tropical seabird species

Author’s Accepted Manuscript Keeping it regular: development of thermoregulation in four tropical seabird species Lorinda A. Hart, Colleen T. Downs, Mark Brown

www.elsevier.com/locate/jtherbio

PII: DOI: Reference:

S0306-4565(16)30343-6 http://dx.doi.org/10.1016/j.jtherbio.2016.12.003 TB1857

To appear in: Journal of Thermal Biology Received date: 18 October 2016 Revised date: 6 December 2016 Accepted date: 6 December 2016 Cite this article as: Lorinda A. Hart, Colleen T. Downs and Mark Brown, Keeping it regular: development of thermoregulation in four tropical seabird s p e c i e s , Journal of Thermal Biology, http://dx.doi.org/10.1016/j.jtherbio.2016.12.003 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting galley proof before it is published in its final citable form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

1

Keeping it regular: development of thermoregulation in four tropical seabird species Lorinda A. Hart, Colleen T. Downs*, Mark Brown

School of Life Sciences, University of KwaZulu-Natal, P/Bag X01, Scottsville, Pietermaritzburg, 3209, South Africa.

*Corresponding author E-mail: [email protected]

2

Abstract Thermoregulatory capacity of a species can determine which climatic niche it occupies. Its development in avian chicks is influenced by numerous factors. Furthermore, it is suggested that altricial chicks develop their thermoregulatory capacity post-hatching, while precocial chicks develop aspects of this in the egg. We investigated the development of thermoregulation of four co-occurring seabird species in the Seychelles; namely white, ground-nesting white-tailed tropicbirds (Phaethon lepturus) and tree-nesting fairy terns (Gygis alba); and dark plumaged, tree-nesting lesser noddies (Anous tenuirostris) and groundand tree-nesting brown noddies (A. stolidus). White-tailed tropicbirds have semi-altricial, while the remaining species have semi-precocial chicks. Cloacal temperatures (Tb) were measured at five day intervals from newly hatched chicks and compared over time, and with adult Tbs. Initial Tbs of all chicks, except fairy terns, were lower than those taken when chicks were older. Brooding cessation generally coincided with feather development, as did an increase in Tb. Mean chick Tb was significantly lower than mean adult Tb for all species, but only white-tailed tropicbird and brown noddy chicks in tree nests differed significantly from mean adult Tb when chick Tb at five day intervals were considered. There was a significant interactive effect of nest site and age on brown noddy chick Tb, but chick colour did not have a significant effect on Tb. However, brown noddy chicks on dune crests maintained a constant Tb sooner than chicks in tree nests. Our results demonstrate that tropical seabird species have a more delayed onset of thermoregulatory capabilities when compared with those in temperate environments, perhaps as nest sites are less thermally challenging. Nest microhabitats and behavioural thermoregulation, are likely more important during early chick development for these species.

Keywords: Body temperature, Chick development, Chick colour, Feather development, Nest

microhabitat, Seabird, Thermoregulation.

1.

Introduction The effect of climate change on species distributional ranges has important implications

for conservation strategies (Araújo et al., 2011; Chen et al., 2011) as species can be affected both directly and/or indirectly (Lennon et al., 2000). Thermoregulatory ability determines the climatic niches of various endotherm species (Porter and Kearney, 2009). It is therefore essential that we begin to quantify the current and potential future effects of rising global temperatures, caused by climate change. Birds are useful vertebrate models to use to study the

3

impacts of climate change as they generally have high metabolisms, short generation times, and are highly mobile. So far researchers have assessed the influence of climate change on birds in terms of phenology, in particular migration (Huppop and Huppop, 2003; Altwegg et al., 2011; Bussière et al., 2015) and time of breeding (Crick et al., 1997; Visser et al., 2004), protandry (Moller, 2004; Rainio et al., 2007), adult survival (Sandvik et al., 2005; Robinson et al., 2007), morphology e.g. body mass and wing length changes (Yom-Tov, 2001; Yom-Tov et al., 2006; Van Buskirk et al., 2010), distribution (Hitch and Leberg, 2007; Maclean et al., 2008; Sekercioglu et al., 2008), and demography and population sizes (Crick, 2004; Wormworth and Mallon, 2007). Relatively little data is available to assess the influence of changes in temperature on other aspects of birds, including moult patterns (Dawson, 2005; Hedenström et al., 2007) and metabolism (Lindsay et al., 2009b; Lindsay et al., 2009a), although Thompson et al. (2015) demonstrate metabolic flexibility in a generalist bird will negate increased ambient temperature to some extent. It could be possible to assess a species’ rate of adaptation to climate change by analysing various components of its life history and ecology (Visser, 2008). The thermal niche of endotherms is defined by the interaction of environmental conditions and the individuals size and shape, which in turn influences core body temperature and insulation (Porter and Kearney, 2009). While large scale studies measure the effect of climate change on species distributions on a global scale (Pearson and Dawson, 2003; Wiens et al., 2009; Logan et al., 2013), the physiological mechanisms behind what limits species distributions remains largely unknown (Parmesan et al., 2005), and the capacity to adapt to a changing environment through metabolic flexibility is largely ignored (Thompson et al., 2015). This may be due to indirect and direct limitations that act simultaneously and are often difficult to identify separately. The development of homeothermy in avian chicks may be influenced by numerous factors including growth rate, behavioural thermoregulation, predation risk, environmental factors, and development of a chick’s thermoregulatory capacity (Brown and Downs, 2002). Whittow and Tazawa (1991) suggest that unlike altricial chicks which develop thermoregulatory abilities post-hatching, precocial chicks start developing components of this during the embryonic phase. This is aided by the feathers of precocial chicks which provide efficient insulation once the hatched chick is dry (Booth and Jones, 2002). The rate of oxygen diffusion through the egg shell, metabolic capacity and development of embryonic tissues, as well as the thermal conductance of the egg limit the degree of this early thermoregulatory development (Whittow and Tazawa, 1991). Western gull (Larus occidentalis wymani)

4

embryos tolerate overnight cooling, but risk mortality if exposure to warming is prolonged (Bennett et al., 1981). Warming is generally slow, due to the large egg size (Bennett et al., 1981). Of particular importance to a bird’s breeding success is the selection of a suitable nest site. Nest site selection is an adaptive process, as preferred nest sites yield greater success (Martin, 1998). Once eggs are laid, birds are bound to their nest site until chicks leave. Predation risk has been identified as one of the primary drivers of this process (Burger and Gochfeld, 1988; Martin and Roper, 1988; Negro and Hiraldo, 1993), as has competition (Burger and Shisler, 1978; Ingold, 1994), and various environmental conditions. Nest microhabitat can influence the degree of exposure which ultimately influences the thermal environment experienced by the egg, chick and incubating parent bird. Denser vegetation is preferred in tropical climates by laughing gulls (Larus atricilla), compared to their counterparts in more temperate climates (Burger and Gochfeld, 1986). Similarly, sooty terns (Sterna fuscata) nest in denser vegetation where higher rainfall and ambient temperatures are experienced (Burger and Gochfeld, 1986). To our knowledge no studies have considered the development of thermoregulation simultaneously in co-occurring species of both ground- and tree-nesters, of dark and light colouration. In this study the presence of a stable internal body temperature (Tb) was considered a reflection of a chick’s ability to thermoregulate. We investigated development of thermoregulation in four seabird species found in the Seychelles, namely white, groundnesting white-tailed tropicbirds (Phaethon lepturus) and tree-nesting fairy terns (Gygis alba); and dark plumaged, tree-nesting lesser noddies (Anous tenuirostris) and ground- and treenesting brown noddies (A. stolidus). White-tailed tropicbirds produce a single semi-altricial chick, while all other species in this study produced one semi-precocial chick per pair. Additionally, brown noddy chicks have both light and dark morphs prior to feather development. We hypothesised that development of thermoregulation differs between semiprecocial and semi-altricial seabird chicks in this tropical environment. We predicted that semi-precocial chicks would show some degree of thermoregulatory development post hatching, while semi-altricial chicks would show greater development post-hatching. Additionally, chicks’ initial Tbs would be lower than adult Tbs, and become more similar to adult Tbs as they reached maturity. Finally, we predicted that brown noddy nest site and chick colour would influence the development of thermoregulation. Chicks in hotter, more exposed nest sites would maintain Tbs sooner than chicks in more sheltered nest sites, and dark chicks would absorb more radiant heat and regulate Tbs sooner than light chicks.

5

2.

Materials and methods Data were collected from June to August 2014 on Cousine Island, Seychelles 4°21'41"S

and 55°38'51"E. Cousine is a 25.7 ha privately owned, conservation-centred island that is free of alien mammals (Samways et al., 2010). Cousine Island supports breeding populations of white-tailed tropicbird (± 740 pairs), fairy terns (± 1800 pairs), lesser noddies (± 38 000 pairs), and brown noddies (± 3000 pairs; 2014 population count, Cousine Island Conservation Management, unpublished data). All chicks hatch covered in down feathers but differ in colour. Initially white-tailed tropicbird chicks are grey; fairy tern chicks are multi-coloured grey, white, brown and black; lesser noddy chicks are black; brown noddy chicks are predominantly dark brown, but rarer white chicks also occur (Samways et al., 2010). Lesser noddy and fairy tern chicks were monitored until they could fly off the nest platform, after which trapping individuals was not possible. This occurred at ~40 and ~50 days old respectively, when chicks could fly but stayed near the nest platform and received food from parent birds. Lesser noddies are considered fully fledged from 55-70 days while fairy terns from 90-100 days (Burger and Lawrence, 2000). White-tailed tropicbirds were monitored up 70 days old, and brown noddies monitored up to 45 days old when the duration of our island sampling ended. They fledge between 67-89 days old and 40-55 days respectively (Phillips, 1987; Burger and Lawrence, 2000), but no individuals from our study had fully fledged. Chick internal body temperature was measured as cloacal temperature (Tb) and together with body mass (BM) was recorded from hatching in white-tailed tropicbirds (n = 13), fairy terns (n = 7), lesser noddies (n = 15), and brown noddies in tree nests (n = 15), and those on dune crests (n = 18), at five day intervals between 07:00 – 12:00 am. A thermocouple probe (Cole-Palmer Digi-Sens®) was greased with a thin layer of Vaseline® Blue Seal Petroleum Jelly and inserted ~5-10mm into the cloaca to determine Tb. Concurrent ambient temperature (Ta) was also recorded and presence of a parent bird incubating the chick noted. Chick feather development was observed based on three developmental stages namely C1 chicks (newly hatched with no pins or feathers), C2 chicks (have a combination of pins and emerged feathers), and C3 chicks (have only feathers present) (Burger and Lawrence, 2000). Finally, the cloacal Tbs and concurrent Tas of adult lesser noddies (n = 38), fairy terns (n = 18), brown noddies (n = 18), and white-tailed tropicbirds (n = 21) were randomly recorded throughout the duration of this study. White-tailed tropicbird nests were predominantly next to granite rocks or logs. Only two nests in this study were inside a rock or log crevice. Nests were well-shaded, and were mostly

6

within the forest. Fairy tern nests were also generally well-shaded and within the woodlands behind the dunes. Brown noddy tree nests were all in palm trees along the beachfront. Birds nested in the cups formed at the base of the leaves. Nests experienced varying amounts of sunlight based on the angle of the sun and density of the palm canopy above the nest. Dune crest nests were in full sun on grassy dunes. Vines and grasses provided a dense carpet that chicks would burrow into once they hatched. In a concurrent study, nest site temperatures measured at ten minute intervals by temperature logging devices yielded a Ta range of 23.6 32.6°C (min – max) for white-tailed tropicbird nests, 24.7 - 32.2°C for brown noddy nests in trees, 25.2 - 40.7°C for brown noddy nests on dunes, 24.6 - 31.6°C for lesser noddy nests and 22.7 - 35.7°C for fairy tern nest sites (Hart et al., 2016a). To determine if chick Tb was influenced by body mass, age or ambient temperature a simple linear correlation (Pearson r) was run. As body mass (BM) was highly correlated with chick age for all species in this study (lesser noddy r = 0.85, brown noddy r = 0.95 and r = 0.93, white-tailed tropicbird r = 0.91, and fairy tern r = 0.91), chick age was used for comparative Tb analysis as BM can vary based on food provisioning and growth rate of individuals. For each species, chick Tbs measured at 5 day intervals were compared using Repeated Measures Analysis of Variance (RMANOVA), and where significant differences were detected post-hoc Tukey tests were run. For brown noddies an additional RMANOVA was run to compare Tbs at five day intervals measured at dune crest and tree nests, and from dark and light chicks, as well as the interaction of these factors. Chick Tb at each age stage was compared with randomly selected adult Tbs and compared using RMANOVA. Adult Tbs were compared between species by one-way analysis of variance (ANOVA). Nest Ta was compared between species using RMANOVA and further analysis with a post-hoc Tukey test.

3.

Results

3.1. Intraspecific chick Tb comparisons Chick Tbs for all species in this study were weakly correlated with Ta, except for fairy tern chicks’ Tb which had a moderately positive correlation to Ta (Supplementary table S1). Tas varied between species (RMANOVA, F4,23 = 54.37, P < 0.001). Tas of white-tailed tropicbird nests were significantly lower and less variable than those at nests of other species (post-hoc Tukey, P < 0.001; Fig. 1). Brown noddy nests in trees also had significantly lower Tas than brown noddy nests on dune crests and lesser noddies (P < 0.001 and P = 0.04 respectively). Chick Tbs of all the species in this study, except fairy terns, differed

7

significantly at five day intervals (Table1). Fairy tern chicks maintained a fairly constant Tb from when they hatched (Table 2). Fairy tern chicks’ pins started emerging at 11 days old and by 30 days old were predominantly fully feathered (n = 7; Fig. 1; Table 2). Brooding ceased between 8-17 days, although in older chicks only the head would fit under the parent bird’s chest (Table 2). All white-tailed tropicbird Tbs from 6-65 days old differed significantly from those recorded from 0-5 days (post-hoc Tukey, P < 0.001). Tbs recorded from 56-65 days old were significantly higher than 6-10 days, as were Tbs from 51-65 days compared with 16-20 days old (post-hoc Tukey, P < 0.001). From c. 21-25 days old, Tb remained relatively constant (Table 2). White-tailed tropicbird chicks started producing feather pins at 16 days old and were fully feathered (>95%) at 47 days old (n = 13; Fig. 1; Table 2). Brooding stopped between 7-19 days. One chick of 2 days old was found alone and was observed shivering. Lesser noddy chicks Tbs from 0-10 days were significantly lower than Tbs from 16-40 days (post-hoc Tukey, P < 0.001). Tbs from 11-15 days were also significantly lower than Tbs from 21-30 days (post-hoc Tukey, P < 0.001). Chick development was rapid in lesser noddy chicks, with pins starting to emerge at 7 days old and chicks well feathered by 22 days old (n = 15; Fig. 1; Table 2). Chicks were initially brooded, but as they became too big, parent birds sat next to chicks with bodies touching until chicks were 16-24 days old, after which chicks were left alone at the nest site (Table 2). This coincided with the age at which chicks were able to maintain a constant Tb (Table 2). Brown noddy chicks on dune crests Tbs at 6-10 and 21-25 days old were significantly lower than Tbs at 31-35 days old (post-hoc Tukey, P < 0.001). Pins emerged at ~9 days old (n = 19, Fig. 1) and parent birds remained next to chicks (predominantly providing shade) until they chicks were 10 days old. Chicks were fully feathered at 33 days old and feathered chicks that did not seek out shade in nearby vegetation were observed displaying gular fluttering (pers. obs.). Tbs of brown noddy chicks in tree nests from 21-40 days were significantly higher than Tbs from 6-15 days old. Additionally, 26-30 and 36-40 day old chick Tbs were significantly higher than Tbs from 0-20 days old. At eight days old back feather pins started emerging on chicks and parent birds were observed initially brooding and later sitting next to chicks until they were ten days old (n = 15; Fig. 1; Table 2). At 34 days old, chicks were mostly fully feathered (Fig. 1; Table 2). Brown noddy chicks on dune crests were able to maintain a constant Tb from 11-15 days old, while this ability was delayed in their tree nesting counterparts (21-25 days; Table2). Final Tb for all brown noddy chicks was similar.

8

The colour of brown noddy chicks did not have a significant effect on Tb, nor did it have an interactive effect with nest site and / or chick age. However, the mean (±SE) Tb of dark chicks on dune crests was 40.03 ± 0.11°C (n = 15) compared with light chicks 39.69 ± 0.21°C (n = 3). Their light chicks initially had higher Tbs than dark chicks on dune crests, but from 11-15 days old they had lower Tbs than dark chicks (Fig. 2). In tree nests their dark chicks were slightly warmer than light chicks (Fig. 2). Mean Tb of light chicks in tree nests was 39.93 ± 0.26°C (n = 2); similar to Tb of dark chicks in tree nests 39.63 ± 0.11°C (n = 13). When dark and light chicks were combined, at 6-10 days old, light chicks had higher Tbs by 0.8°C. However, from 11-40 days old, dark chicks had higher Tbs by 0.2°C and thereafter were 0.4-0.6°C warmer at each age stage. Combined dune crest and tree nest brown noddy Tbs differed significantly with age (RMANOVA, F6,90 = 4.54, P < 0.001), but were similar between nest sites (RMANOVA, F1,15 = 0.26, P = 0.62). However, there was a significant interactive effect of nest site and age on chick Tb (RMANOVA, F6,90 = 2.65, P = 0.02).

3.2. Intraspecific chick and adult Tb comparison Tbs of adult birds varied significantly between the four species (ANOVA, F3,91 = 22.69, P < 0.001). White-tailed tropicbirds had a significantly lower Tb than all other species in this study (post-hoc Tukey, P < 0.001; Table 1). Mean adult Tb compared with chick Tbs were significantly different for all species in this study (Table 1). When comparing chick Tb at various age stages to randomly selected mean adults Tbs, only white-tailed tropicbirds and brown noddy chicks in tree nests differed significantly from adult Tbs (Table 1). White-tailed tropicbird chicks aged 0-5 days had significantly lower Tbs than adults, as did brown noddy chicks aged 0-25 days.

4.

Discussion This study reflects the natural Tb changes experienced by wild tropical seabird chicks.

Chicks from all the species in this study, except fairy terns, did not maintain a constant body temperature throughout the nestling period. Lesser noddies maintained a relatively constant Tb from 16-20 days old, while white-tailed tropicbird and brown noddy chicks were older, 21-25 days old. Interestingly, brown noddy chicks on dune crests were able to regulate Tb sooner, at 11-15 days old. In contrast to altricial chicks which lack the ability to generate heat as hatchlings (Kuroda et al., 1990), precocial chicks, despite Tb being lower than in adults, are able to increase their heat production up to threefold (Booth, 1984). Similar rates of increase have been measured in semi-precocial gull chicks (Dawson and Bennett, 1981). However,

9

body size of chicks can affect this ability as smaller bodies have greater mass-specific heat loss per surface area and would require greater energetic efforts to increase and maintain T b (Whittow and Tazawa, 1991). Per unit mass, the fairy tern egg has the longest incubation period of all tern species, of which only two exhibit prolonged incubation (Whittow, 1980). White-tailed tropicbirds also have longer than expected incubation periods, while lesser and brown noddies do not (Whittow, 1980; Pettit et al., 1984; Hart et al., 2016a). Extended incubation in seabirds is associated mostly with tropical species and the long pipping period is considered to be of great physiological importance in terms of developing their ability to thermoregulate (Whittow, 1980). The eggs of such species have various traits which may include slow embryo growth, relatively large egg size when compared with the parent bird, higher energy content and subsequently greater oxygen consumption, reduced water vapour conductance from the shell and water loss from unpipped eggs (Whittow, 1980; Whittow and Grant, 1985). However, it must be noted that while some tropical seabirds may have long incubation periods, they do not necessarily have prolonged chick growth rates (Pettit et al., 1984). Sooty terns (Sterna fuscata) have very short incubation periods, but long (60 day) nestling periods; black noddies (Anous minutus) and fairy terns have similarly long incubation periods, but the semi-precocial fairy tern chicks take longer to reach maturity (Pettit et al., 1981; Pettit et al., 1984). Thus, extended incubation does not always translate to reduced metabolic demands of chicks (Pettit et al., 1984). However, our results show that the semi-precocial fairy tern chick that hatches after prolonged incubation maintains a relatively constant Tb, similar to adult Tbs. This is likely due to the chicks’ physiological ability to thermoregulate, however brooding, nest microhabitat, and parental care can all play a role. In contrast white-tailed tropicbird chicks are semi-altricial and only develop thermoregulatory capabilities after 21-25 days. From an ecological perspective, extended incubation is linked with food supply, largely because of pelagic feeding habits and tropical environments where food availability is often unpredictable and patchy (Whittow, 1980). Hatchling growth rate is also generally slower in such environments and may be linked to parents foraging further offshore, which results in large meal sizes, but infrequent feeding (Schaffner, 1990; Ramos et al., 2004). Additionally, in pelagic species, such as the white-tailed tropicbird, chicks accumulate large fat deposits with fledglings weighing more than adult birds (Schaffner, 1990). However, it is unlikely that these fat deposits serve an insulatory role (Thomas et al., 1993). White-tailed tropicbirds forage up to 200 km offshore (Schaffner, 1990; Ramos and Pacheco, 2003; Malan et al., 2009), while fairy terns feed nearer inshore (Diamond, 1978), yet food is also provided

10

infrequently in large meals (Dorward, 1963). This could be due to parental food provisioning experience, food availability, or anti-predator and anti-pirate strategies (Dorward, 1963). As a result chick BM, development, size, and fledgling period varies between individuals; particularly as chicks reach maturity (Dorward, 1963; Thomas et al., 1993). Such variation was observed in chicks from this study. Although BM and age were highly correlated, age increased independently from environmental factors and should therefore be used to compare Tb changes in chicks. Mean chick Tb differed significantly from mean adult Tb for all species in this study but when chick Tbs at five day intervals were compared with mean adult Tbs, only white-tailed tropicbird and brown noddy chicks in tree nests differed significantly. Tb in wild chicks reflects the net product of a chicks thermoregulatory capacity, but may be influenced by brooding parents, huddling with siblings and nest material insulating the chick (Whittow and Tazawa, 1991). Huddling and brooding reduces chicks’ energy expenditure to generate heat as they receive direct heat and insulation (Spellerberg, 1969; Sherry, 1981; Thomas et al., 1993). In this study brooding ceased approximately when chicks started developing feathers. Unlike other species in this study, white-tailed tropicbirds lack a brood-patch and use their feet to incubate eggs (Hart et al., 2016b). Young chicks are brooded under the wing. Brooding frequency and duration varies with changes in ambient temperature, chick age, and broodpatch temperature (Sherry, 1981). In tropical environments where ambient temperatures are less variable and where nest site selection can favour more stable micro-habitats (Hart et al., 2016a), the length of brooding in tropical species could be reduced. Results from this study suggest that nest micro-habitat can also influence the Tb of chicks in tropical habitats, as brown noddy chicks on dune crests were able to maintain a constant Tb ten days sooner than chicks in tree nests. During incubation, brown noddy parents undergo a period of thermal stress as they shade their immobile eggs which are exposed to ambient temperatures that exceed incubated egg temperatures on dune crests (Hart et al., 2016a). Selecting such exposed and hot nest sites may be initially costly, but can be beneficial during the chick phase. In moderate temperatures (19-28ᵒC) gull chicks’ Tbs remain similar to adult Tbs, however in colder temperatures their regulative capacities diminish (Dawson and Bennett, 1981). Indeed, reducing incubation temperatures by as little as 1ᵒC can influence chick phenotype and translate into a 27 - 40% increased metabolic costs in hatchlings (DuRant et al., 2012). Brooding is often initiated by precocial chicks, as they are capable of behavioural thermoregulation (Sherry, 1981). The insulative capacities of chicks’ down is less than that of adult birds and chicks may still rely on behavioural thermoregulation by parent birds in the

11

early stages (Dawson and Bennett, 1981). Brown noddy chicks are semi-precocial and on dune crests in particular they leave the nest area and burrow into thick grass or shade under dune vines (LH, pers. obs.). Such behavioural thermoregulation would protect them from strong winds experienced during the breeding season, as well as from direct radiant heat from the sun. In this study huddling would not occur as all species have single clutches (Burger and Lawrence, 2000). Nests consist of no nesting material and where materials are used, nests have a platform design and offer no insulation (Burger and Lawrence, 2000). It is more likely that nest micro-habitat would have an influence on Tb as more sheltered nests experience more constant Ta, than exposed nest sites (Hart et al., 2016a). All chicks did receive some initial brooding, but despite this, initial chick Tbs were still significantly lower than final Tb for most species in this study. Coastal Antarctic McCormick skua (Catharacta maccormicki) chicks are precocial and maintain Tb from ~10 days old, although marked increases in Tb and thermoregulation are observed within the first few days post-hatching (Spellerberg, 1969). By the time chicks are too large to brood, they are capable of thermoregulation (Spellerberg, 1969). Similarly Antarctic petrel chicks, Thalassoica antarctica maintain a Tb >36°C from 11 days old (Bech et al., 1991). Precocial red junglefowl (Gallus gallus) are able to thermoregulate from approximately 10 days old, maintaining a Tb of approximately 40.5°C (Sherry, 1981). White Pelican (Pelecanus erythrorhynchos) chicks display some thermoregulatory capacity by seven days old, but are fully competent at 16 days, which coincides with brooding cessation (Abraham and Evans, 1999). However, for some gull species, chicks develop a thermoregulatory capacity within the first day and near adult Tbs are obtained after three days (Bartholomew and Dawson, 1952; Bartholomew and Dawson, 1954). Chicks from our study developed thermoregulatory abilities later than those reported elsewhere, except in fairy terns which maintained a fairly constant Tb within the first five days post-hatching. This could be due to the tropical environment and nest site micro-habitat of these birds being less thermally stressful and the demand for early development of thermoregulation being reduced. Indeed, brown noddies were able to thermoregulate sooner in warmer nest sites, suggesting environmental and behavioural aspects may be more important for tropical species. Although Tbs were not significantly different between light and dark brown noddy chicks, some variations were evident. Brown noddy chicks are very mobile shortly after hatching and seek out shade during the heat of the day (LH pers. obs.). It has been suggested that dark plumage would be favoured over light plumage, particularly in cold climates, as they absorb more radiant heat (Lustick, 1971; Beasley and Ankney, 1988), however the dark

12

morph is more common in tropical brown noddy chicks, irrespective of habitat. Unfortunately, trends from this study are weak due to a small sample size. In a study on lesser snow gosling (Chen caerulescens caerulescens) polymorphism, dark and light morphs had similar daily energy expenditures; but darker morphs did expend comparatively more energy on windy, sunny days compared with calm, cloudy days (Beasley and Ankney, 1988). Literature on colour polymorphism in chicks is scarce, and the reason for this occurrence in brown noddies is unclear. There may be thermal advantages to chick polymorphism, but behavioural thermoregulation is likely more important (Beasley and Ankney, 1988). In a Hawaiian study, where brown noddy colonies are predated on by great frigatebirds (Fregata minor), dark and light chicks were as likely to fledge regardless of plumage colouration and nest site (Megyesi and Griffin, 1996). Additional suggestions for adult polymorphism is detectability and foraging success within light and dark habitats, or activity during the day and night (Galeotti et al., 2003; Tate et al., 2016), variations in UV reflectance (Burkhardt and Finger, 1991), adaptations to environmental condition (Amar et al., 2013), and anti-predator strategies (Gotmark, 1992). Melanin has also been associated with immune responses (Gasparini et al., 2009) and parasite loads (Lei et al., 2013) in birds. Brown noddies nest in both trees and on dune crests and adults are active at nest sites during the day and night (Hart et al., 2016a). Such variation within a species may stand it in good stead under predicted climate change scenarios. Understanding, and representing variations in thermoregulatory behaviour and ability are becoming increasingly important in the inclusion of climate change models, particularly for endotherms which have received less attention when compared with ectotherms (Boyles et al., 2011). Metabolic demands fluctuate in response to environmental temperature changes (Lowell and Spiegelman, 2000) and understanding how these may influence the early life stages of endotherms and the resulting phenotypes of offspring (DuRant et al., 2012) has implication for the survival and genetic structure of future populations. Our results highlight the importance that nest microhabitat, life history strategies, and variations within a species can have in the development of an individual’s ability to thermoregulate. We propose that as future ambient temperatures increase, tropical seabird chicks could maintain near adult Tbs sooner and that behavioural thermoregulation in mobile chicks will become increasingly important – particularly at more thermally stressful nest sites.

Acknowledgments

13

The Department of Environment and the Seychelles Bureau of Standards granted permission for this project and the University of KwaZulu-Natal and National Research Foundation provided funding to MB and LH. We sincerely thank the Cousine Island owners and staff, particularly J. Gane and I. Olivier for their hospitality and assistance with the project. We are also grateful to J. Hart for his help with fieldwork.

References Abraham, C. L., Evans, R. M., 1999. The development of endothermy in American white pelicans. Condor 101, 832-841. Altwegg, R., Broms, K., Erni, B., Barnard, P., Midgley, G. F., Underhill, L. G., 2011. Novel methods reveal shifts in migration phenology of barn swallows in South Africa. Proc R Soc B 279, 1485-1490. Amar, A., Koeslag, A., Curtis, O., 2013. Plumage polymorphism in a newly colonized black sparrowhawk population: classification, temporal stability and inheritance patterns. J Zool 289, 60-67. Araújo, M. B., Alagador, D., Cabeza, M., Nogués-Bravo, D., Thuiller, W., 2011. Climate change threatens European conservation areas. Ecol Lett 14, 484–492. Bartholomew, G. A., Dawson, R. D., 1952. Body temperatures in nestling western gulls. Condor 54, 58-60. Bartholomew, G. A., Dawson, W. R., 1954. Temperature regulation in young pelicans, herons, and gulls. Ecology 35, 466-472. Beasley, B. A., Ankney, C. D., 1988. The effect of plumage color on the thermoregulatory abilities of lesser snow goose goslings. Can J Zool 66, 1352-1358. Bech, C., Mehlum, F., Haftorn, S., 1991. Thermoregulatory abilities in chicks of the Antarctic petrel (Thalassoica antarctica). Polar Biol 11, 233-238. Bennett, A. F., Dawson, W. R., Putnam, R. W., 1981. Thermal environment and tolerance of embryonic western gulls. Physiol Zool 54, 146-154. Booth, D. T., 1984. Thermoregulation in neonate mallee fowl Leipoa ocellata. Physiol Zool 57, 251-260. Booth, D. T., Jones, D. N., 2002: Underground Nesting in the Megapods. In: Avian Incubation: Behaviour, Environment, and Evolution. (Deeming, D. C., ed). Oxford University Press, New York. pp. 192-206. Boyles, J. G., Seebacher, F., Smit, B., McKechnie, A. E., 2011. Adaptive thermoregulation in endotherms may alter responses to climate change. Integr Comp Biol 51, 676-690. Brown, M., Downs, C. T., 2002. Development of homeothermy in hatchling crowned plovers Vanellus coronatus. J Therm Biol 27, 95-101. Burger, A. E., Lawrence, A. D., 2000: Seabird Monitoring Handbook for the Seychelles. BirdLife Seychelles, Mahe, Seychelles. Burger, J., Gochfeld, M., 1986. Nest site selection in sooty terns (Sterna fuscata) in Puerto Rico and Hawaii. Colonial Waterbirds 9, 31-45. Burger, J., Gochfeld, M., 1988. Nest-site selection by roseate terns in two tropical colonies on Culebra, Puerto Rico. The Condor 90, 843-851. Burger, J., Shisler, J., 1978. Nest site selection and competitive interactions of herring and laughing gulls in New Jersey. The Auk 95, 252-266. Burkhardt, D., Finger, E., 1991. Black, white and uv: How birds see birds. Naturwissenschaften 78, 279-280. Bussière, E. M. S., Underhill, L. G., Altwegg, R., 2015. Patterns of bird migration phenology in South Africa suggest northern hemisphere climate as the most consistent driver of change. Global Change Biol 21, 2179–2190. Chen, I.-C., Hill, J. K., Ohlemüller, R., Roy, D. B., Thomas, C. D., 2011. Rapid range shifts of species associated with high levels of climate warming. Science 333, 1024-1026. Crick, H. Q. P., 2004. The impact of climate change on birds. Ibis 146, 48-56. Crick, H. Q. P., Dudley, C., Glue, D. E., Thomson, D. L., 1997. UK birds are laying eggs earlier. Nature 388, 526. Dawson, A., 2005. The effect of temperature on photoperiodically regulated gonadal maturation, regression and moult in starlings – potential consequences of climate change. Funct Ecol 19, 995-1000. Dawson, W. R., Bennett, A. F., 1981. Field and laboratory studies of the thermal relations of hatchling western gulls. Physiol Zool 54, 155-164. Diamond, A. W., 1978. Feeding strategies and population size in tropical seabirds. Am Nat 112, 215-223. Dorward, D. F., 1963. The fairy tern Gygis alba on Ascension Island. Ibis 103b, 365-378.

14

DuRant, S. E., Hopkins, W. A., Wilson, A. F., Hepp, G. R., 2012. Incubation temperature affects the metabolic cost of thermoregulation in a young precocial bird. Funct Ecol 26, 416-422. Galeotti, P., Rubolini, D., Dunn, P. O., Fasola, M., 2003. Colour polymorphism in birds: causes and functions. J Evol Biol 16, 635–646. Gasparini, J., Bize, P., Piault, R., Wakamatsu, K., Blount, J. D., Ducrest, A.-L., Roulin, A., 2009. Strength and cost of an induced immune response are associated with a heritable melanin-based colour trait in female tawny owls. J Anim Ecol 78, 608–616. Gotmark, F., 1992. Anti-predator effect of conspicuous plumage in a male bird. Anim Behav 44, 51-55. Hart, L. A., Downs, C. T., Brown, B., 2016a. Sitting in the sun: Nest microhabitat affects incubation temperatures in seabirds. J Therm Biol 60, 149-154. Hart, L. A., Downs, C. T., Brown, M., 2016b. Hot footing eggs: thermal imaging reveals foot mediated incubation in white-tailed tropicbirds, Phaethon lepturus. J Ornithol 157, 635-640. Hedenström, A., Barta, Z., Helm, B., Houston, A. I., McNamara, J. M., Jonzén, N., 2007. Migration speed and scheduling of annual events by migrating birds in relation to climate change. Clim Res 35, 79-91. Hitch, A. T., Leberg, P. L., 2007. Breeding distributions of North American bird species moving north as a result of climate change. Conserv Biol 21, 534-539. Huppop, O., Huppop, K., 2003. North Atlantic oscillation and timing of spring migration in birds. Proc R Soc B 270, 233–240. Ingold, D. J., 1994. Influence of nest-site competition between European starlings and woodpeckers. Wilson Bulletin 106, 227-241. Kuroda, O., Matsunaga, C., Whittow, G. C., Tazawa, H., 1990. Comparative metabolic responses to prolonged cooling in precocial duck (Anas domestica) and altricial pigeon (Columba domestica) embryos. Comp Biochem Phys A 95, 407-410. Lei, B., Amar, A., Koeslag, A., Gous, T. A., Tate, G. J., 2013. Differential haemoparasite intensity between black sparrowhawk (Accipiter melanoleucus) morphs suggests an adaptive function for polymorphism. PLoS ONE 8, e81607. Lennon, J. J., Greenwood, J. J. D., Turner, J. R. G., 2000. Bird diversity and environmental gradients in Britain: a test of the species–energy hypothesis. J Anim Ecol 69, 581–598. Lindsay, C. V., Downs, C. T., Brown, M., 2009a. Physiological variation in amethyst sunbirds (Chalcomitra amethystina) over an altitudinal gradient in summer. J Therm Biol 34, 190-199. Lindsay, C. V., Downs, C. T., Brown, M., 2009b. Physiological variation in amethyst sunbirds (Chalcomitra amethystina) over an altitudinal gradient in winter. J Exp Biol 212, 483-493. Logan, M. L., Huynh, R. K., Precious, R. A., Calsbeek, R. G., 2013. The impact of climate change measured at relevant spatial scales: new hope for tropical lizards. Global Change Biol 19, 3093–3102. Lowell, B. B., Spiegelman, B. M., 2000. Towards a molecular understanding of adaptive thermogenesis. Nature 404, 652-660. Lustick, S., 1971. Plumage colour and energetics. Condor 73, 121-122. Maclean, I., Austin, G. E., Rehfisch, M. M., Blew, J. A. N., Crowe, O., Delany, S., Devos, K., Deceuninck, B., Gunther, K., Laursen, K., Van Roomen, M., Wahl, J., 2008. Climate change causes rapid changes in the distribution and site abundance of birds in winter. Global Change Biol 14, 2489-2500. Malan, G., Hagens, D. A., Hagens, Q. A., 2009. Nesting success of white terns and white-tailed tropicbirds on Cousine Island, Seychelles. Ostrich 80, 81-84. Martin, T. E., 1998. Are microhabitat preferences of coexisting species under selection and adaptive? Ecology, 656–670 Martin, T. E., Roper, J. J., 1988. Nest predation and nest-site selection of a western population of the hermit thrush. Condor 90, 51-57. Megyesi, J. L., Griffin, C. R., 1996. Brown noddy chick predation by great frigatebirds in the northwestern Hawaiian Islands. Condor 98, 322-327. Moller, A. P., 2004. Protandry, sexual selection and climate change. Global Change Biol 10, 2028–2035. Negro, J. J., Hiraldo, F., 1993. Nest-site selection and breeding success in the lesser kestrel Falco naumanni. Bird Study 40, 115-119. Parmesan, C., Gaines, S., Gonzalez, L., Kaufman, D. M., Kingsolver, J., Peterson, A. T., Sagarin, R., 2005. Empirical perspectives on species borders: from traditional biogeography to global change. Oikos 108, 58-75. Pearson, R. G., Dawson, T. P., 2003. Predicting the impacts of climate change on the distribution of species: are bioclimate envelope models useful? Global Ecol Biogeogr 12, 361–371. Pettit, T. N., Grant, G. S., Whittow, G. C., 1984. Nestling metabolism and growth in the black noddy and white tern. Condor 86, 83-85. Pettit, T. N., Grant, G. S., Whittow, G. C., Rahn, H., V.Paganelli, C., 1981. Respiratory gas exchange and growth of white tern embryos. Condor 83, 355-361.

15

Phillips, N. J., 1987. The breeding biology of white-tailed tropicbirds Phaethon lepturus at Cousin Island, Seychelles. Ibis 129, 10-24. Porter, W. P., Kearney, M., 2009. Size, shape, and the thermal niche of endotherms. Proc Nat Acad Sci USA 106, 19666–19672. Rainio, K., Tøttrup, A. P., Lehikoinen, E., Coppack, T., 2007. Effects of climate change on the degree of protandry in migratory songbirds. Clim Res 35, 107–114. Ramos, J. A., Maul, A. M., Bowler, J., Monticelli, D., Pacheco, C., 2004. Laying date, chick provisioning, and breeding success of lesser noddies on Aride Island, Seychelles. Condor 106. Ramos, J. A., Pacheco, C., 2003. Chick growth and provisioning of surviving and nonsurviving white-tailed tropicbirds (Phaethon lepturus). Wilson Bull 115, 414-422. Robinson, R. A., Baillie, S. R., Crick, H. Q. P., 2007. Weather-dependent survival: implications of climate change for passerine population processes. Ibis 149, 357–364. Samways, M., Hitchins, P., Bourquin, O., Henwood, J., 2010: Tropical Island Recovery Cousine Island, Seychelles. Wiley-Blackwell, West Sussex, UK. Sandvik, H., Erikstad, K. E., Barrett, R. T., Yoccoz, N. G., 2005. The effect of climate on adult survival in five species of North Atlantic seabirds. J Anim Ecol 74, 817–831. Schaffner, F. C., 1990. Food provisioning by white-tailed tropicbirds: effects on the developmental pattern of chicks. Ecology 71, 375-390. Sekercioglu, C. H., Schneider, S. H., Fay, J. P., Loarie, S. R., 2008. Climate change, elevational range shifts, and bird extinctions. Conserv Biol 22, 140-150. Sherry, D. F., 1981. Parental care and the development of thermoregulation in red junglefowl. Behaviour 76, 250-279. Spellerberg, I. F., 1969. Incubation temperatures and thermoregulation in the McCormick skua. Condor 71, 5967. Tate, G. J., Bishop, J. M., Amar, A., 2016. Differential foraging success across a light level spectrum explains the maintenance and spatial structure of colour morphs in a polymorphic bird. Ecol Lett 19, 679-686. Thomas, D. W., Bosque, C., Arends, A., 1993. Development of thermoregulation and the energetics of nestling oilbirds (Steatornis caripensis). Physiol Zool 66, 322-348. Thompson, L. J., Brown, M., Downs, C. T., 2015. The potential effects of climate-change-associated temperature increases on the metabolic rate of a small Afrotropical bird. J Exp Biol 218, 1504-1512. Van Buskirk, J., Mulvihill, R. S., Leberman, R. C., 2010. Declining body sizes in North American birds associated with climate change. Oikos 119, 1047–1055. Visser, M. E., 2008. Keeping up with a warming world; assessing the rate of adaptation to climate change. Proc R Soc B 275, 649–659. Visser, M. E., Both, C., Lambrechts, M. M., 2004. Global climate change leads to mistimed avian reproduction. Adv Ecol Res 35, 89-110. Whittow, G. C., 1980. Physiological and ecological correlates of prolonged incubation in sea birds. Am Zool 20, 427-436. Whittow, G. C., Grant, G. S., 1985. Water loss and pipping sequence in the eggs of the red-tailed tropicbird (Phaethon rubricauda). Auk 102, 749-753. Whittow, G. C., Tazawa, H., 1991. The early development of thermoregulation in birds. Physiol Zool 64, 13711390. Wiens, J. A., Stralberg, D., Jongsomjit, D., Howell, C. A., Snyder, M. A., 2009. Niches, models, and climate change: assessing the assumptions and uncertainties. Proc Nat Acad Sci USA 106, 19729-19736. Wormworth, J., Mallon, K. 2007: Bird Species and Climate Change: The Global Status Report version 1.0 Australia. Yom-Tov, Y., 2001. Global warming and body mass decline in Israeli passerine birds. Proc R Soc B 268, 947952. Yom-Tov, Y., Yom-Tov, S., Wright, J., Thorne, C. J. R., Du Feu, R., 2006. Recent changes in body weight and wing length among some British passerine birds. Oikos 112, 91-101.

Figure Legends

16

Figure 1. Mean cloacal temperature (○ ± SE) and mean ambient temperature (●± SE) of chicks of white-tailed tropicbirds (n = 13), fairy terns (n = 7), lesser noddies (n = 15), and brown noddies nesting on dune crests and in trees (n = 18 and n = 15 respectively). Each dot represents a single temperature reading. The horizontal solid line indicates mean adult temperature. Records prior to dotted lines represent C1 chick temperatures, between the dotted and dashed lines are temperatures recorded for C2 chicks, and readings to the right of the dashed line indicate C3 chick temperatures.

Figure 2. Light and dark brown noddy chick Tb measured on dune crest and tree nests (mean ± SE).

Table 1. Outcomes of RMANOVA comparisons of chick Tbs to adult Tbs and at five day age intervals of white-tailed tropicbirds, fairy terns, lesser noddies, brown noddies. (Bold values indicate significant differences at P < 0.05). Species White-tailed tropicbird

Fairy tern

Lesser noddy

Brown noddy *dune crest

Brown noddy *tree

Tb comparison

DF

F

P

mean chick Tb vs mean adult Tb

1, 15

22.84

< 0.001

chick Tb at age stages vs adult Tb

12, 180

4.05

< 0.001

comparison of chick Tb at age stages

12, 36

11.94

< 0.001

mean chick Tb vs mean adult Tb

1, 8

249.30

< 0.001

chick Tb at age stages vs adult Tb

7, 56

1.10

0.376

comparison of chick Tb at age stages

7,14

1.36

0.290

mean chick Tb vs mean adult Tb

1, 16

6.47

0.022

chick Tb at age stages vs adult Tb

7, 112

0.81

0.580

comparison of chick Tb at age stages

7, 14

10.85

< 0.001

mean chick Tb vs mean adult Tb

1, 25

83.61

< 0.001

chick Tb at age stages vs adult Tb

7, 175

1.51

0.167

comparison of chick Tb at age stages

7, 56

3.05

0.010

mean chick Tb vs mean adult Tb

1, 19

294.20

< 0.001

chick Tb at age stages vs adult Tb

7, 133

3.40

0.002

comparison of chick Tb at age stages

7, 35

10.18

< 0.001

Mean chick Tb ± SD (°C) 38.37 ± 1.10

Mean adult Tb ± SD (°C) 39.19 ± 0.97

39.01 ± 1.25

41.89 ± 1.13

40.52 ± 0.99

41.29 ± 1.27

39.97 ± 1.08

41.46 ± 0.86

39.67 ± 0.99

41.46 ± 0.86

Table 2. Chick developmental stages. All values are measured in ‘days’. Incubation and nestling period are cited from Burger and Lawrence (2000).

17

Incubation period

Nestling period

Age feathers start emerging

Age fully feathered

Age chicks left alone at nest

Age of relatively constant Tb

White-tailed tropicbird

40-41

67-89

16

47

7-19

21-25

Fairy tern

30-41

90-100

11

30

8-17

0

Lesser noddy

35

55-70

7

22

16-24

16-20

Brown noddy *dune crest

28-37

40-55

9

33

10

11-15

Brown noddy *tree

28-37

40-55

8

34

10

21-25

Species

42

42

40

40

38

38

Temperature (°C)

Temperature (°C)

18

36 34 32 30

36 34 32 30

28

28

26

26

24

24

White-tailed tropicbird 0

5

10 15 20 25 30 35 40 45 50 55 60 65 70

Fairy tern 0

5

10

15

20

42 40

40

38

38

36 34 32 30

24

Lesser noddy 15

20

25

30

35

40

Age (days)

40

Temperature (°C)

38 36 34 32 30 28 26

Brown noddy *tree 0

5

10

15

20

25

Age (days)

Fig. 1.

55

Brown noddy *dune crest 0

5

10

15

20

25

Age (days)

42

24

50

30

26

10

45

32

28

5

40

34

26

0

35

36

28

24

30

Age (days) 42

Temperature (°C)

Temperature (°C)

Age (days)

25

30

35

40

45

30

35

40

45

19

41.5

41.5

Dark chicks Light chicks

41.0

41.0

40.5

40.5

Temperature ( 0C)

Temperature ( 0C)

Dark chicks Light chicks

40.0

39.5

40.0

39.5

39.0

39.0

38.5

38.5

Dune crest nests 38.0 0-5

6-10

11-15

16-20

21-25

26-30

31-35

36-40

Tree nests

38.0 0-5

6-10

11-15

16-20

21-25

26-30

31-35

36-40

Age (days)

Age (days)

Fig. 2. Highlights 

Development of homeothermy in avian chicks is influenced by numerous factors.



Generally altricial chicks develop this post-hatching.



We investigated the development of thermoregulation of four co-occurring seabird species in the Seychelles.



Initial body temperature (Tbs) of all chicks, except fairy terns were lower than those taken when chicks were older.



Brooding cessation generally coincided with feather development, as did an increase in Tb.



Mean chick Tb was significantly lower than mean adult Tb for all species.



We show that tropical seabird species have a more delayed onset of thermoregulatory capabilities.

Appendix S1 Table of chick and adult Tb correlation results in the current study. Species

White-tailed tropicbird

Age chick chick chick adult chick adult

Correlation age x body mass Tb x age Tb x Ta Tb x Ta Tb x body mass Tb x body mass

Pearson r 0.91 0.61 -0.05 0.25 0.65 -0.09

20

Fairy tern

chick chick chick adult chick adult

age x body mass Tb x age Tb x Ta Tb x Ta Tb x body mass Tb x body mass

0.91 0.16 0.42 0.00 0.15 0.09

Lesser noddy

chick chick chick adult chick adult

age x body mass Tb x age Tb x Ta Tb x Ta Tb x body mass Tb x body mass

0.85 0.74 0.27 0.10 0.69 0.60

Brown noddy *dune crest

chick chick chick adult chick adult

age x body mass Tb x age Tb x Ta Tb x Ta Tb x body mass Tb x body mass

0.95 0.38 0.08 -0.35 0.36 -0.06

Brown noddy *tree

chick chick chick adult chick adult

age x body mass Tb x age Tb x Ta Tb x Ta Tb x body mass Tb x body mass

0.93 0.63 0.04 -0.35 0.66 -0.06