Behavioral Ecology Advance Access originally published online on November 17, 2007
Behavioral Ecology 2008 19(1):79-86; doi:10.1093/beheco/arm108
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Shared parental care is costly for nestlings of common cuckoos and their great reed warbler hosts
a School of Biological Sciences, University of Auckland, Private Bag 1143, Auckland, New Zealand b Animal Ecology Research Group of the Hungarian Academy of Sciences, c/o Hungarian Natural History Museum, Ludovika ter 2., Budapest H-1083, Hungary
Address correspondence to M.E. Hauber. E-mail: m.hauber{at}auckland.ac.nz.
Received 23 April 2007; revised 19 September 2007; accepted 28 September 2007.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Obligate avian brood parasitism typically involves one of 2 strategies: parasite chicks are either 1) virulent and evict all other eggs and nest mates to be raised alone or 2) more tolerant and share foster parental care with host chicks for some or the entirety of the nestling period. We studied the consequences of experimentally forced mixed broods of age-matched one common cuckoo (Cuculus canorus) and 2 great reed warbler (Acrocephalus arundinaceus) chicks. In these broods, both cuckoo and host chicks grew slower than did either individual cuckoos or great reed warblers in broods of 1 parasite or 3 host chicks, respectively. Video records showed that in mixed broods, cuckoo chicks received feedings less frequently than the 33% predicted by chance at 4 days of age but parental food allocations increased to chance levels at 8 days of age. The consistent patterns of lower growth rates arose even though chicks in broods of 1 parasite and 2 hosts received the largest prey items per feeding. In addition, several other measures of parental provisioning also did not predict species and brood-specific differences in nestling growth rates across the different treatments. However, variation in begging displays and its specific costs on host and parasite chicks in the different nest treatments were not quantified in this study. We conclude that young of nest mate–evictor common cuckoos benefit from the sole occupancy of host nests in part owing to an initial competitive disadvantage for parental care in broods with age-matched great reed warbler chicks.
Key words: brood parasitism, chick discrimination, eviction behavior, nestling competition, parental provisioning, virulence.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Young of obligate brood parasitic species require parental care from genetically unrelated fosterers, and the survival of some of the hosts' own young does not contribute to the parasite young's indirect genetic benefits (Zink 2000
). Therefore, it might be evolutionarily advantageous for brood parasitic adults (through egg pecking and removal) and young (through eviction or pecking) to reduce or eliminate eggs and nest mates from parasitized broods (Davies 2000). This is because sole parasite chicks might benefit from forgoing costly begging displays (Kilner 2001). Avoidable costs of cohabitation with host chicks also include the per capita loss of the amount or the quality of food delivered to broods with multiple chicks, possibly including other parasite nest mates (Grim and Honza 1997; Kilner 2005; Martín-Gálvez et al. 2005).
Yet nestling brood parasitic birds in some avian lineages do not routinely evict or otherwise destroy all eggs and nest mates shortly after hatching (Davies 2000; Servedio and Hauber 2006; Broom et al. 2007; Forbes 2007). Comparative (Kilner 2003) and experimental work (Kilner et al. 2004) demonstrated that nestling parasites of the brown-headed cowbird (Molothrus ater) benefit through increased survival and growth in the presence of 1–2 host nest mates because foster parents increase the rate of feeding trips to larger broods, of which the cowbird chick receives a greater than fair share of feedings (also see Dearborn 1998; Lichtenstein and Sealy 1998). As a result, a cowbird chick in a mixed brood receives more food and grows faster than in a brood of 1 parasite only (Kilner et al. 2004). However, in nests with several brood parasite chicks, individual cowbirds fair less well than in nests with fewer host or parasite nest mates (Trine 2000; Hoover 2003).
Alternatively, chicks may be physically constrained from evicting or otherwise destroying host nest mates in other brood parasitic lineages, either because of the structural barriers imposed by deep or cavernous host nest structures or owing to hatching asynchrony and size limitations when parasitizing earlier hatching or larger host species (Rutila et al. 2002; Soler 2002; Grim 2006a, 2006b). These constraints could represent an evolutionary lag in some lineages of brood parasites that have only recently come into association with their current host species (Hosoi and Rothstein 2000). Yet, in other parasitic taxa special adaptations (e.g., lethal beak hooks of chicks of honeyguides [Indicatoridae]: Spottiswoode and Colebrook-Robjent 2007 and ground cuckoos [Dromococcyx spp.]: Davies 2000) or increased begging vigor (Lichtenstein and Sealy 1998; Hauber 2003a) have evolved to specifically eliminate or outcompete host nest mates, even in cavity nests from which eggs and chicks cannot be tossed out (Hoover 2003). The physical or physiological constraint hypothesis may therefore be more likely to apply to cohabitation between parasite and host chicks for those parasite species whose young routinely do evict host egg and young, but occasionally fail to do so.
A third scenario, according to parental investment theory, predicts that hosts of evictor parasites are species whose reproductive strategies are incompatible with the presence of an asynchronously hatching, different sized chick in a mixed brood of hosts and parasites (Soler 2002). According to this model, host taxa that follow a brood reducer strategy would provide disproportionately less food to smaller chicks (whether conspecific or heterospecific) in the nest (Lichtenstein 2001). In contrast, brood adjuster host species may provision disproportionately less to the larger, more intensively begging (again, either conspecific or heterospecific) chick in the brood (Soler 2002; Grim 2006b).
A further possibility is that cohabitation between parasite and host increases the chance of discrimination of parasite chick from own chicks (Lotem 1993; Lawes and Marthews 2003; Grim 2007a). Finally, some host species may be more likely to abandon broods that contain too few chicks, including single chick broods of one parasite or one host nestling, than other host taxa (Langmore et al. 2003; Grim et al. 2003; Grim 2007b). Under all these scenarios, the foreign chicks in nests of some host types may either benefit from cohabitation with one or more nest mates of varying sizes or benefit from evicting all types of host nest mates.
When parasitizing most of its host species that build open nests, the common cuckoo (Cuculus canorus, hereafter cuckoo) chick almost always evicts all nest content, that is eggs or nestlings (Wyllie 1981; Honza et al. 2007). However, observations across several typical host species showed that common cuckoo chicks occasionally did not clear the nest cups of eggs and nest mates shortly after hatching (Malchevsky 1960; Rutila et al. 2002). It was suggested that physical constraints or barriers associated with hosts' nest structure (e.g., deep nests and cavities) interfered with nest mate displacement, such that the cuckoo hatchling attempted but was eventually unable to remove host eggs and nestlings (Rutila et al. 2002). However, common cuckoo chicks in these naturally mixed broods with redstart (Phoenicurus phoenicurus) nestlings did not survive at either higher (in contrast to nest mate–tolerant cowbirds, Kilner 2003) or lower rates (as predicted for a nest mate–evictor taxon) compared with lone cuckoo chicks in naturally parasitized broods from which hosts were successfully eliminated (Rutila et al. 2002; Aviles et al. 2005).
In contrast, and as predicted, when the cuckoo chick was naturally raised together with one fieldfare (Turdus pilaris) nestling, the parasite grew more slowly than usual (Petrescu and Béres 1997). Similarly, observations on great reed warbler (Acrocephalus arundinaceus) nests showed that unsuccessful eviction attempts could lead to the survival of the hosts, but with the cuckoo hatchling appearing to have become exhausted during eviction attempts and dying a few days later (e.g., 8 such cases reported by Molnár 1939). In another case, when the cuckoo egg was experimentally introduced into an already incubated host nest, and consequently the great reed warbler nestlings were older than the cuckoo by 1 day, unsuccessful eviction attempts caused the death of the cuckoo chick at the age of 5 days (Molnár 1939).
Because cuckoo hatchlings continue to attempt to displace foreign objects from the nest cup up to approximately 4 days of age after hatching (Wyllie 1981; Varga 1994), observations and correlations alone cannot identify the relative causes of reduced growth and survival for cuckoo chicks in mixed broods. For instance, death or reduced growth may be owing to the costs of continuous physical labor during attempted eviction owing to a trade-off between lower begging effort and increased eviction attempts (Kleven et al. 1999; Soler 2002). Alternatively, or in addition, lower growth and survival may be owing to the cuckoo chick's reduced ability to monopolize parental feedings delivered to the nest (Martín-Gálvez et al. 2005). There might also be increased costs of begging displays for parental care in larger broods (Kilner 2001) and a loss in the selectivity and the quality of food items delivered by foster parents to broods with greater demands (Grim and Honza 1997, 2001; Martín-Gálvez et al. 2005).
Previous experimental work with common cuckoos examined parental food delivery rates and food size allocations in mixed broods of parasite and host chicks and naturally parasitized and nonparasitized broods of rufous bush robins (Cercotrichas galactotes) (Martín-Gálvez et al. 2005). This research documented that cuckoo chicks in mixed broods did not receive different diets, prey sizes, or food delivery rates compared with single host nest mates. The results from the experimentally mixed broods of Martín-Gálvez et al. (2005), thus imply, that cuckoo chicks in mixed broods do not represent a supernormal stimulus on a per capita basis, which ordinarily might be necessary to procure the adequate parental care required by the faster growing cuckoo chick (Kilner et al. 1999; Butchart et al. 2003; Grim 2006a). This finding was in contrast to experimental work on reed warblers (Acrocephalus scirpaceus) in which broods of single cuckoo chicks received more feedings per capita than did individual chicks in broods of host chicks only (Kilner et al. 1999) and were provisioned with a different diet and larger prey sizes than were broods of single, weight-matched host chicks (Grim and Honza 2001).
However, the prior experiments with mixed broods of cuckoos and hosts included different brood sizes in nonparasitized hosts (mode: 3 chicks) and mixed broods (mode: 4 chicks) and a hatching asynchrony of 0–4 days between nest mates in mixed broods (Martín-Gálvez et al. 2005). Similarly, although the experiments with brown-headed cowbirds and eastern phoebes (Sayornis phoebe) established mixed broods of age-matched chicks, nonparasitized broods consisted of 4 host chicks, whereas mixed broods had a total size of 3 (1 cowbird and 2 phoebe) chicks (Kilner et al. 2004). Finally, a prior test of the supernormal stimulus hypothesis with cuckoos and reed warblers used broods of single size-matched host versus parasite chicks (Grim and Honza 2001).
We therefore, set out to examine the consequences of experimentally mixed broods of age-matched single common cuckoo and 2 host great reed warbler chicks on species- and context-specific nestling growth rates. We also determined the effects of these brood treatments on parental food delivery rates, food sizes, and relative allocation decisions between nestling species. These data were then compared with the same measures from naturally parasitized broods of single common cuckoos and nonparasitized broods of 3 great reed warbler host chicks. Chick growth and parental responses to broods of 1 parasite, 3 host chicks, or 1 parasite and 2 host chicks were studied between ages 4–8 days after hatching at which point cuckoo chicks typically cease eviction attempts. This was to avoid the confound of the costs of the nest mate eviction behavior (Kleven et al. 1999; Martín-Gálvez et al. 2005; Honza et al. 2007) by cuckoo chicks during the early days immediately after hatching (approximately up to 4 days of age: Wyllie 1981). This time frame also allowed for the estimation of growth rates of cuckoo and host young during the linear phases of growth (Kilner et al. 1999; Butchart et al. 2003; Grim 2006a) across the 3 different brood treatments.
We predicted that, if cuckoo chicks paid a cost of cohabitation with host nest mates either owing to increased begging competition or an inability to solicit sufficient parental provisioning from foster parents, the parasite nestlings would grow more slowly in broods of 1 parasite and 2 host chicks compared with broods of 1 parasite chick.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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The study was conducted in the Hungarian Great Plain, within a 20-km radius of Apaj (47°07'N, 19°05'E), approximately 40 km south of Budapest. Great reed warblers nest at this site in 2- to 4-m-wide strips of reeds (Phragmites australis) along narrow flood relief and irrigation channels. In our study area, modal clutch size of great reed warblers is 5 eggs and modal brood size is 4 chicks (Moskát C, unpublished data). This host population is heavily parasitized by common cuckoos (ca. 64% of nesting attempts) (Moskát and Honza 2002
). Consequently, great reed warbler nests are frequently parasitized by multiple cuckoo eggs (23% of all host nests: Moskát et al. 2006), allowing for suitable sample sizes of experimental cross-fostering of cuckoo chicks into nonparasitized host nests. Fieldwork was conducted from 2003 to 2006, between mid-May and late June. Once great reed warbler nests were located in the reeds, they were checked daily to establish clutch size and completion date, parasitism status, and rejection of naturally laid parasite eggs (Moskát and Honza 2002). We compared nestling growth rates, host provisioning behaviors, and feeding decisions across broods from 3 treatment groups.
Experimental broods
The cuckoo chick typically evicts all eggs and/or nestlings from the nest of the host under natural circumstances and grows up alone (Wyllie 1981; Honza et al. 2007). In this treatment, we forced cuckoo nestlings to grow up together with great reed warbler nestlings by mixing 4- or 5-day-old cuckoo chicks (day of hatching: 0 day) in the nests of great reed warblers with 2 host nestlings of the same age. The size of these broods were arranged to comprise "1 parasite and 2 host chicks" (n = 15). In 5 of the nests, 2 host nestlings were left and the rest were transported to nonstudy nests. In 10 additional parasitized nests, 2 host chicks were added to a brood of a single cuckoo chick. Two of these 10 nests had originally not been parasitized but were given a cuckoo egg by the experimenters. Nests were assigned to this treatment when age-matched chicks were available for translocation between broods in our study site.
At 4–5 days of age, cuckoo chicks routinely cease attempting to displace host nest mates; therefore, our experiment was not confounded by the potential costs of nest mate–eviction behavior (Kleven et al. 1999). As nestlings grew larger, at about 7 days of age, we elevated the natural nest by placing a small fence ridge constructed from nearby plants or by circling the rim with plastic tape (sticky sides glued together) to prevent accidental falling of growing and competing nestlings (Hauber 2003b; Bize and Roulin 2006).
There was no statistical difference in the initial clutch size (cuckoo and host eggs combined to account for removal of a host egg by the female cuckoo, Davies 2000) of originally parasitized (mean ± standard deviation [SD]: 5.3 ± 0.79 eggs) and nonparasitized clutches (4.72 ± 0.49 eggs; unpaired t-tests: t = 1.68, P = 0.12). This implies no clear a priori quality differences between host parents of either nest type within this brood treatment. There was also no statistical difference in any of the chick growth or parental feeding parameters measured (see below) between broods that initially had cuckoo or great reed warbler chicks only (unpaired t-tests: all t > 2.0, P > 0.135).
Single-species broods
We used 2 types of control nests. In broods of "1 parasite" (n = 12), we followed unmanipulated, naturally parasitized nests with a single cuckoo chick. In broods of "3 host chicks" (n = 14), we followed naturally nonparasitized nests with 3 great reed warbler nestlings. If these latter nests had more than 3 warbler nestlings, the supernumerary chicks were transported to a nonexperimental nest. Sample sizes gradually diminished throughout the experiment (to n = 9, 10, and 11 at 8 days of age for nests with 1 parasite and 2 hosts, 1 parasite, and 3 hosts, respectively), due to nest loss owing to predation and inclement weather. There was no statistical difference in the initial total clutch size (host and parasite eggs combined, to account for host eggs removed by cuckoos; Wyllie 1981) of hosts between the 3 brood types in our study (mode: 5, one-way analysis of variance: F2,38 = 1.852, P = 0.171). This implies no clear a priori quality differences between parents caring for the different brood types.
To test the hypothesis that cuckoo chicks grow more slowly in experimental broods, nest contents were checked daily and the weight of each chick was measured to the nearest 0.1 g using pesola scales. We then calculated daily growth rates of cuckoo and warbler chicks as the slope of the linear regression fitted against weight changes between 4 and 8 days of ages posthatch for each nest that escaped predation during this period. As mentioned, these ages represent the linear phase of growth of common cuckoos in other host species' nests (Kilner et al. 1999; Grim 2006a) and of both host and parasite chicks in great reed warbler nests (Butchart et al. 2003).
To determine the relationship between chick growth rates and parental provisioning decisions, for nests in each of the treatment groups, we also video recorded parental feeding activity on days 4 or 5 (mode: 4) and 8 or 9 (mode: 8) posthatch to calculate food delivery rates, to record parental feeding decisions, and to quantify the size category of food items delivered to the nest and chicks. We estimated prey size by comparing the volume of each food item relative to the bill size of the host parent within bins of 25% (e.g., 25%, 50%, 75%, ..., 300%, etc., of bill volume). We used Canon MV500i and 550i fully compatible digital video cameras with Fuji 60 min. DX cassettes for recording. The cameras were left for 15–20 min before recording started for habituating the birds, with the equipment placed 4–5 m from the nest. Recording sessions typically lasted 60 min (range: 27–62, mean ± SD: 58.8 ± 7.6), unless interrupted by inclement weather (rain). There were no significant differences in the time of day at which nests from different treatments were recorded (median: 13:30, unpaired t-tests, all P > 0.18) or effects of time of day on feeding rates (F1,49 = 0.262, P = 0.611) independent of treatment.
Videotapes were viewed after the field seasons on a television screen to be able to more accurately estimate prey sizes and feeding decisions. In the absence of systematic color banding in this population of hosts, we could not discriminate female and male parents. Because of the depth of the great reed warbler nest, the angle of view of the recording equipment, and wind, we could not reliably quantify begging behaviors of nestling hosts and parasites prior to feeding events at each videotaped nest (Kilner et al. 1999, 2004). However, for those broods with 1 parasite and 2 host chicks where nestling gape colors were visible during subsequent feeding events, we recorded which chick species (cuckoo: red gape or greet reed warbler: yellow gape) received the food item. This accounts for the differences between sample sizes of growth rate and feeding rate data. Individual host chicks were not marked and so we averaged food delivery and prey size data between the 2 and 3 host chicks in the different brood treatments to obtain per capita measures of parental provisioning for host chicks.
The statistical analyses focused on 3 different estimates of parental provisioning for host and parasite chicks. First, we calculated the "per capita feeding rate" per unit time for chicks in broods with 1 parasite, 1 parasite and 2 hosts, and 3 hosts. In broods with 1 parasite and 2 hosts, this included data on whether the cuckoo or the warbler chicks received food during feedings. Per capita feeding rates were calculated for warblers in 1 parasite and 2 host as well as 3 host chicks by dividing warbler-feeding rates by 2 or 3, respectively.
Second, we also estimated the "food size per actual feedings" by averaging prey size (percentage bill) across all events when food was transferred to either cuckoo or warbler chicks. Finally, combining food delivery rates and food sizes allowed us to estimate "per capita food amount delivery rates," measured as cumulative percentage bill size of prey items fed to each chick per unit time.
For each of these 3 measures, we evaluated the statistical difference between chicks of the parasite and host species across the 3 brood treatment types and accounted for covariation with the different ages of chicks using generalized linear mixed models in JMP 5.1, based on restricted maximum-likelihood estimates (Grim 2007b). Nest identity and year of experiment were included as nominal random factors in these models but not month because all videotaping took place during June across the different years of the study. We tested for significant interaction between treatment and age when both of these factors were significant but included and reported the interaction term in the final model only if it was also significant. One-sample t-tests were used for univariate comparisons in Statview 5.0.1, with data from younger and older (4–5 vs. 8–9 days old) nestlings combined into binary nominal data. In all tests, the alpha level was set at 0.05 and the analyses were 2 tailed. We used raw data for illustrations by plotting mean + standard error (SE) of each of our measures for the different brood treatments and age groups.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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Initial weights of approximately 4-day-old cuckoo chicks were similar between chicks in broods of 1 parasite (mean ± SE: 17.7 ± 0.97 g) and broods of 1 parasite and 2 host chicks (19.8 ± 0.99 g) (unpaired t19 = –1.49, P = 0.153). There was also no statistical difference in the initial average weights of individual warbler chicks in broods of 3 host chicks (13.9 ± 1.08 g) and broods of 1 parasite and 2 hosts (14.5 ± 0.45 g) (unpaired t19 = –0.495, P = 0.626). Furthermore, the combined growth rates of chicks for entire broods were similar from 4 to 8 days of age (brood growth rate: 7.30 ± 0.99, 6.32 ± 0.36, and 7.28 ± 0.55 g/day for broods of 1 parasite and 2 hosts, 1 parasite, and 3 hosts, respectively) between treatment groups (F2,25 = 0.896, P = 0.432). However, growth rates of individual nestlings varied significantly across treatment groups: cuckoo chicks in broods of 1 parasite grew faster than did cuckoo chicks in broods of 1 parasite and 2 hosts (F1,16 = 4.68, P = 0.046) (Figure 1). Also, warbler chicks in broods of 3 hosts grew faster than did warbler chicks in broods of 1 parasite and 2 hosts (F1,10 = 7.01, P = 0.024) (Figure 1).
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Cuckoo chicks in broods of 1 parasite and 2 hosts received disproportionately fewer feedings per capita than predicted by chance for a brood of 3 chicks (33%) at 4 days of age (one-sample t10 = –2.87, P = 0.017) (Figure 2). The proportion of feedings per cuckoo chick increased by 8 days of age (F1,4 = 7.97, P = 0.048) to the level predicted by chance (one-sample t5 = 1.12, P = 0.298) (Figure 2).
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Feeding rates per brood were significantly different between each treatment group (F2,21 = 9.07, P = 0.002). Specifically, larger broods of 1 parasite and 2 host chicks or 3 host chicks received more feeds per unit time than did broods with a lone parasite (Figure 3), after accounting for the pattern that older broods received higher feeding rates compared with younger broods (F1,21 = 8.74, P = 0.008).
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Cuckoo chicks received higher per capita feeding rates in broods of 1 parasite compared with broods of 1 parasite and 2 host chicks (F1,35 = 7.65, P = 0.009), when controlling for higher feeding rates with increasing age (F1,35 = 11.9, P = 0.003) (Figure 4). In contrast, warbler chicks received similar per capita feeding rates in broods of 1 parasite and 2 hosts and broods of 3 hosts (F1,12 = 0.620, P = 0.447), and there was no statistically significant variation of feeding rates with age (F1,12 = 4.54, P = 0.055). Cuckoo chicks in broods of 1 parasite were fed at higher rates compared with per capita feeding rates of warbler chicks in broods of 3 hosts (F1,40 = 15.1, P < 0.0001), when accounting for increased feeding rates with greater age (F1,40 = 11.3, P = 0.0005) (Figure 4).
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Food item sizes per feeding were consistently different between broods of 1 parasite and broods of 3 host chicks, as sole cuckoo chicks received significantly larger prey items than did warblers (F1,16 = 24.9, P = 0.0001), with no significant change with age (F1,16 = 0.362, P = 0.556) (Figure 5). Surprisingly, cuckoo chicks in broods of 1 cuckoo and 2 hosts received even larger food item sizes than did cuckoo chicks in broods of 1 parasite (F1,10 = 5.70, P = 0.038), independently of age (F1,10 = 1.24, P = 0.292). Similarly, warbler chicks in broods of 1 parasite and 2 hosts received larger food item sizes than did warblers in broods of 3 hosts (F1,13 = 11.1, P = 0.005), independently of age (F1,13 = 1.04, P = 0.328). In addition, cuckoo chicks received larger food items per feed than warbler chicks within broods of 1 parasite and 2 hosts (paired t7 = 2.76, P = 0.028), irrespective of age (F1,13 = 0.040, P = 0.861) (Figure 5).
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Per capita food amount delivery rates showed that cuckoo chicks received similar amounts of food per time in broods of 1 parasite and in broods of 1 parasite and 2 hosts (F1,10 = 2.50, P = 0.145), when controlling for increasing food amounts delivered with increasing age (F1,10 = 5.71, P = 0.038) (Figure 6). In contrast, per capita food amount delivery rates were higher for warblers in broods of 1 parasite and 2 hosts compared with broods of 3 hosts (F1,11 = 11.3, P = 0.006), with no significant change across ages (F1,11 = 2.62, P = 0.134). Older sole cuckoo chicks in broods of 1 parasite received increasingly more food per capita per time than did older warbler chicks in broods of 3 hosts (brood: F1,15 = 72.5, P < 0.0001; age: F1,15 = 38.2, P = 0.0009; interaction: F1,15 = 9.55, P = 0.008). Similarly, cuckoo chicks received more food per capita per time than did warbler chicks within broods of 1 parasite and 2 hosts (paired t7 = 2.46, P = 0.043), but there was no relative change with increasing age (F1,9 = 0.012, P = 0.917) (Figure 6).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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We studied the consequences of cohabitation by chicks of host great reed warblers and virulent, evictor brood parasitic common cuckoos. Our experimental approach matched brood sizes and ages of chicks in broods containing either 1 parasite and 2 hosts or 3 hosts, with age-matched comparisons with broods of 1 parasite chick. We then collected data on chick growth rates, parental feeding decisions, feeding rates, food sizes, and food amount delivery rates. Our growth rate estimates for individual cuckoos (6.3 g/day) and great reed warblers (2.4 g/day) in broods of 1 parasite and broods of 3 hosts, respectively (Figure 1), were very similar in magnitude to the values previously published for observations on great reed warbler nests with either single common cuckoo chicks (6.2 g/day between ages 3 and 14 days: Kleven et al. 1999
, 5.7 g/day between ages 4 and 9 days: Butchart et al. 2003) or several host chicks (2.4 g/day between ages 4 and 9 days: Butchart et al. 2003, assuming a brood of 4 nestlings). Our results are generally consistent with the hypothesis that common cuckoo chicks benefit from their virulent strategy of typically evicting host eggs and nest mates (Kilner 2005). Lone parasite chicks are able to avoid the costs of lower growth rates, documented here in broods containing a mix of hosts and parasites, and the presumed reduction in fledgling survival and breeding recruitment owing to lower fledging weights (Weatherhead and Dufour 2000).
The lower growth rates of parasites in experimentally mixed broods of evictor parasites and hosts are in contrast to findings from mixed broods of hosts and parasites with less virulent, nonevictor brood parasitic brown-headed cowbirds which benefit from the presence of host nest mates through higher growth rates and survival (Kilner 2003; Kilner et al. 2004; Forbes 2007). Broods of 1 cuckoo and 2 great reed warblers in our study received higher feeding rates (Figure 3) and larger food sizes than broods of 1 parasite or 3 hosts (Figure 5). But, in contrast to cowbird chicks (Kilner et al. 2004), the cuckoo chicks in our study were unable to monopolize parental provisioning at the ages studied, as they received random proportions of feedings delivered at approximately 8 days of age and fewer feedings than expected at approximately 4 days of age (Figure 2). It still remains to be determined experimentally how cowbird and cuckoo chicks would fare in broods with several other parasite nest mates (Briskie et al. 1994). This would be particularly relevant in host–parasite systems with high rates of multiple parasitism (Trine 1998, 2000; Hoover 2003), including our common cuckoo-great read warbler system in central Hungary (Moskát and Honza 2002; Moskát et al. 2006). Experimental work on multiple parasite chicks per nest is of particular relevance because the avoidance of such superparasitism has been suggested to be one possible evolutionary origin of nest mate eviction behavior (Brooker and Brooker 1990; Trine 2000; Hauber and Montenegro 2002).
In addition, it also remains to be examined experimentally what the rate is at which cuckoo chicks will grow in mixed broods of host and parasite in species other than rufous bush robins (Martín-Gálvez et al. 2005) and great reed warblers (this study). Comparative patterns will need to be evaluated especially with respect to variation in relative host size (Kleven et al. 1999; Grim 2006a; Rivers 2007) and the brood adjuster versus brood reducer breeding parental strategies of various host species of common cuckoos (Soler 2002; Grim 2006a). Finally, it awaits determination as to what the extent and the consequences of costs related to successful and unsuccessful eviction attempts are for common cuckoos in hosts whose nest architecture facilitates or constrains eviction behavior (Kleven et al. 1999; Rutila et al. 2002; Aviles et al. 2005; Grim 2006b).
On different levels of analysis, our results remain silent about the evolutionary causes leading to virulence in common cuckoos: reduced competitive abilities at younger ages may be either a cause or an outcome of cuckoo chicks' evictor strategies (Kilner 2005; Grim 2006b). Furthermore, from an ontogenetic perspective, our results are in agreement with the developmental shift of the needs and abilities of growing cuckoos to solicit and receive food by having to beg increasingly more at older ages to procure enough provisions from foster parents (Kilner et al. 1999). This is opposed to host chicks that would need to beg vigorously from the start because they are raised in the company of nest mates (Briskie et al. 1994) with whom they continuously compete for parental provisioning (Kilner et al. 1999; Butchart et al. 2003).
Regarding the effects of our experimental treatments on parental behaviors, we documented a complex relationship between brood composition and parental feeding, food size, and food amount delivery rates. Despite our custom-designed experimental paradigm, the reported parental feeding patterns were not consistently predictive of chick growth rates across treatments. It is possible that longer or more frequent video-recording sessions of parental visits and feeding decisions, together with additional weight gain data up to the fledging stage, would have resulted in a more consistent set of foster parental feeding patterns with respect to brood age, size, and species composition. Nonetheless, in agreement with published results on reed warblers (Kilner et al. 1999), we found that cuckoo chicks in broods of 1 parasite received higher food delivery rates than did great reed warbler chicks per capita in broods of 3 hosts (Figure 4). In addition, within broods of 1 parasite and 2 host chicks, cuckoos received larger food items (Figure 5) and greater amounts of food per unit time (Figure 6) than did nest mate great reed warbler chicks on a per capita basis.
However, cuckoo chicks did not receive a greater than random share of feeding events from fostering great reed warblers (Figure 2). This matches prior data from mixed broods of common cuckoos and rufous bush robins in which food delivery rates and food sizes were also similar between hosts and parasites on a per capita basis (Martín-Gálvez et al. 2005). It therefore remains uncertain whether common cuckoo chicks represent a supernormal stimulus for foster parents in broods of great reed warblers (Davies et al. 1998; Grim and Honza 2001). Future experiment tests will be required to compare parental responses to broods of single host or parasite chicks (Langmore et al. 2003; Grim 2007b) or within mixed broods of a single host chick and a single parasite chick.
We also found that both cuckoo and host chicks in experimental broods of 1 parasite and 2 hosts received larger food items than did cuckoo and host chicks in broods of a single parasite or 3 hosts (Figure 5). However, contrary to the sibling symbiosis hypothesis (Forbes 2007), we found that both cuckoo and host chicks grew more slowly in mixed broods compared with chicks in broods of single cuckoos or 3 hosts, respectively. Nevertheless, similar to other passerine species (Conrad and Robertson 1992; Forbes 2007), great reed warbler parents provisioned broods at higher feeding rates with both increasing numbers of chicks in the nest (1 vs. 3) and increasing ages of chicks (4 vs. 8 days of age) (Figure 3). Feeding rates of great reed warbler parents for broods of 3 chicks also differed with varying brood composition, showing greater values within broods of a single parasite versus 3 hosts, especially at 4 days of age (Figures 3 and 4). This latter pattern of parental responses parallels increasing parental feeding visitation rates with increasing parasite loads (i.e., number of parasitic chicks per brood size) in other host–parasite systems (Dearborn 1998; Lichtenstein and Sealy 1998; Hauber and Montenegro 2002; Hauber 2006; Hoover and Reetz 2006).
In contrast to patterns of food delivery rates, the estimated size of food items per feed delivered by great reed warbler foster parents to each chick varied significantly between different treatment broods but did not covary with overall brood size (Figure 5). Cuckoo chicks, when fed, received larger prey items in broods of 1 parasite and 2 host chicks compared with both warbler chicks in such broods and to cuckoo chicks in broods of a single parasite. Great reed warbler chicks in broods of 3 hosts received the smallest prey sizes, and there were no consistent ontogenetic shifts in relative prey sizes delivered by host parents for chicks in different treatment broods of 4 versus 8 days of age, despite the increases in food delivery rates with age. However, these results regarding parental feeding effort and prey size have limited generality because of the restricted nestling age ranges (
4 to 8 days) examined here. For example, previous work showed that prey sizes and taxonomic composition became less selective for older host broods (Grim and Honza 1997, 2001). Specifically, this loss of selectivity occurred when parasitized broods of reed warblers reached the weight of the cuckoo chick and, thus, the presumed feeding requirements of the parasite chick, exceeded those of host brood weights at fledging. Future experiments will be needed to address a similar time frame of brood development for cuckoo, host, and mixed-species chicks in great reed warbler nests.
Larger prey sizes for cuckoo chicks in natural or experimentally mixed broods compared with host chicks were previously reported for other host species of common cuckoos (Martín-Gálvez et al. 2005; but for a nonsignificant difference in prey sizes, see Grim and Honza 1997, 2001). Differences in prey sizes delivered for parasites may be evidence of increased per capita provisioning in response to more intense begging by a single cuckoo chick versus a single host chick (i.e., supernormal stimulus: Grim and Honza 2001). However, neither per capita feeding rates (Figure 4) nor delivered food item sizes (Figure 5) showed a simple predictive covariation with either the food amount delivery rates (Figure 6) or the differences in individual cuckoo and host growth rates between treatments (Figure 1). Total brood growth rates were similar across treatments and, thus, also independent of differences in brood feeding rates between different brood sizes (Figure 3). Finally, differences in per capita feeding rates (Figure 4) did not explain the differences in host chicks' growth rates between broods of 1 parasite and 2 hosts and broods of 3 hosts (Figure 1), and food item sizes were greatest for broods of 1 parasite and 2 hosts (Figure 5), which showed the lowest per capita chick growth rates (Figure 1).
We did not, however, determine the taxonomic diversity of food items delivered to cuckoo and host chicks (Grim and Honza 1997), which would have allowed the testing of the prediction that the reduced growth rates in broods of 1 parasite and 2 hosts were owing to the fosterers' reduced selectivity in providing prey items (Grim 2006c) and, thus, feeding lower quality food items to chicks in these broods (Grim and Honza 2001, Martín-Gálvez et al. 2005). Alternatively, unmeasured costs of increased begging displays and competition for parental provisioning (Kilner 2001) may have resulted in the decreased growth of both cuckoo and great reed warbler chicks in broods of 1 parasite and 2 hosts.
These results suggest that our measures of parental feeding rates, food size and food amount delivery rates, and relative feeding allocation cannot explain the growth rate differences between cuckoos and great reed warbler host chicks in mixed broods. Although, we detected ontogenetic shifts in parental provisioning behaviors and allocation decisions between cuckoo and host chicks in mixed broods depending on age (Figure 2), several costs associated with begging and growing in mixed broods for both common cuckoos and great reed warblers remain unaccounted for in this study. For example, increased competition and greater begging intensity in the presence versus absence of host parents (Roulin et al. 2000; Budden and Wright 2001; Dor et al. 2006), as well as small brood sizes (Gonzalez-Voyer et al. 2007), overcrowding (Dearborn 1996; Hauber 2003b; Bize and Roulin 2006), and reduced competitive ability of common cuckoo chicks in nests even without hatching asynchrony (Molnár 1939; Varga 1994) are all potential factors that were previously implicated as costs of begging behavior and intrabrood competition by a parasite. Therefore, the relative contributions of each of these potential costs to the observed reduced growth rates of both cuckoo and host chicks in broods composed of parasites and hosts remain to be tested experimentally in future work.
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FUNDING |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONFUNDINGREFERENCES |
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The Hungarian Scientific Research Fund (OTKA, T48397 to C.M.); the University of Auckland Research Committee, the National Geographic Society, the New Zealand Marsden Fund, and the Human Frontier Science Program to M.E.H.
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ACKNOWLEDGEMENTS |
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For assistance, we thank M. Bán and T. Kisbenedek during fieldwork and Z. Berényi and B. Igic during data entry. For discussions, we are grateful to M. Anderson, A. Budden, D. Campbell, P. Cassey, D. Dearborn, M. Honza, T. Grim, S. Ismar, A. Lotem, L. Ortiz Catedral, R. Kilner, J. Madden, E. Røskaft, J. Rutila, D. Winkler, and many other colleagues. The research followed Animal Behavior Society guidelines for the ethical use of animals in scientific experimentation and the Duna-Ipoly National Park provided permission for research.
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