Anim Cogn (2015) 18:355–360 DOI 10.1007/s10071-014-0806-4
ORIGINAL PAPER
Nest sanitation behavior in hirundines as a pre-adaptation to egg rejection to counter brood parasitism Canchao Yang • Longwu Wang • Wei Liang Anders Pape Møller
•
Received: 6 March 2014 / Revised: 28 August 2014 / Accepted: 9 September 2014 / Published online: 18 September 2014 Ó Springer-Verlag Berlin Heidelberg 2014
Abstract Previous studies suggested that nest sanitation behavior may have been a pre-adaptation from which egg rejection of brood parasite eggs evolved. We tested this hypothesis in two swallow species, the red-rumped swallow (Cecropis daurica) and the barn swallow (Hirundo rustica). Our results indicated that the red-rumped swallow, which is an accepter of foreign eggs, rejected a low percentage of non-egg-shaped objects and did so less often than the barn swallow, which is an intermediate rejecter of foreign eggs. Furthermore, the egg rejection rates of the barn swallow increased with the increase in rejection rates of non-egg-shaped objects among different populations. These results showed that nest cleaning behavior could have evolved into a means of reducing the costs of brood parasitism, suggesting that egg recognition ability has evolved from recognition of non-egg-shaped objects. This finding advances our understanding of the evolution of egg recognition behavior in birds. Keywords Cecropis daurica Egg recognition Egg rejection Hirundo rustica Nest cleaning
C. Yang L. Wang W. Liang (&) Ministry of Education Key Laboratory for Tropical Plant and Animal Ecology, College of Life Sciences, Hainan Normal University, Haikou 571158, China e-mail: [email protected] L. Wang College of Life Sciences, Wuhan University, Wuhan 430072, China A. P. Møller Laboratoire d’Ecologie, Syste´matique et Evolution, CNRS UMR 8079, Universite´ Paris-Sud, Baˆtiment 362, 91405 Orsay Cedex, France
Introduction Eggs constitute future offspring, and hence, there should be a strong incentive for parents to retrieve any egg-shaped structure that is found in the neighborhood of a nest. Indeed, Tinbergen (1953) showed for the herring gull (Larus argentatus) that nest owners would retrieve eggs or egg-shaped structures from a considerable distance by rolling these into their nests, when an experimenter placed eggs even at a significant distance from the nest. Studies and casual observations have shown that gulls and other ground nesting species are known to sit on egg-shaped stones and other structures as if such objects were real eggs (Tinbergen 1953). The downside of such egg retrieval is the incorporation of foreign objects into nests thereby interfering with or eliminating reproductive success. Removal of such objects through nest cleaning behavior is ubiquitous in altricial birds (Moska´t et al. 2003; Guigueno and Sealy 2012), while egg discrimination is regarded as a specific derived behavior that has evolved to protect against avian brood parasitism (Rothstein 1975; Davies 2000). Rothstein (1975) first proposed that nest cleaning may have been a pre-adaptation from which egg rejection evolved, and Moska´t et al. (2003) proposed a hierarchical concept to understand nest cleaning behavior versus egg discrimination as an explanation for rejection of foreign eggs. They both suggested that nest cleaning behavior has evolved into a means of reducing the costs of brood parasitism. If this mechanism was at work, we would expect that nest cleaning behavior would be particularly prominent in species with nests into which foreign objects may fall at a regular basis. Thus, we would expect that species such as swallows and martins that use holes in the ground or nests built out of mud would have an elevated risk of
123
356
finding pellets of mud or small stones in their nests. Indeed, one of us has often found small pellets of mud from the nest in the nest cup of barn swallows as a consequence of wear of the mud nest during reproduction, and that such pellets are invariably removed from the nest (A. P. Møller unpublished observations). Such objects may interfere with efficient incubation, and also pose a risk of damaging eggs, hence creating a selection pressure for their removal. Zolei et al. (2012) showed in experiments with a rejecter species, the great reed warbler (Acrocephalus arundinaceus), that artificial eggs with two blunt poles were rejected more often than eggs with a single blunt pole or two sharp poles, showing that there is selection on egg shape by hosts. In contrast, Stokke et al. (2010) found no difference in rate of ejection between large- and normal-sized model eggs by reed warblers (Acrocephalus scirpaceus). Guigueno and Sealy (2012) showed that shape and size of model eggs were the significant factors eliciting rejection for all host species that received experimental non-egg-shaped objects added to their nests before hatching. Furthermore, Underwood and Sealy (2006) provided evidence to suggest that egg rejecters have more refined abilities to discriminate against non-egg-shaped objects than egg accepters. They concluded that nest sanitation may be a pre-adaptation for anti-parasite defenses by playing a role in their evolution. Indeed, Ortega and Cruz (1988) showed for two species of blackbirds that they accepted all egg-shaped objects, but rejected all other objects from their nests. This finding is as expected if egg discrimination has evolved in response to removal of random objects from nests during nest sanitation. A recent study on tree sparrows (Passer montanus) by Pola´cˇek et al. (2013) also speculated that nest sanitation plays a key role in the evolution of the removal of parasitic eggs. Here, we performed a foreign object experiment (including non-egg-shaped and egg-shaped models) to test the relationship between egg recognition and rejection and nest sanitation by comparing two swallow species, the redrumped swallow (Cecropis daurica, formerly Hirundo daurica) and the barn swallow (Hirundo rustica), and by comparing different populations of barn swallows. A recent study showed that the former species is a total accepter, while the latter is an intermediate rejecter of non-mimetic eggs (Liang et al. 2013). Therefore, we predicted that (1) both swallow species would reject a certain percentage of non-egg-shaped objects and that barn swallows would reject more than red-rumped swallows if nest cleaning has been a pre-adaptation from which egg rejection evolved. Furthermore, we predicted that (2) different populations of barn swallows would have different egg rejection rates related to rejection rates of non-egg-shaped objects if nest sanitation abilities differed between populations. In other
123
Anim Cogn (2015) 18:355–360
words, populations with higher egg rejection rates would reject more non-egg-shaped objects.
Materials and methods Study area and species This study was performed at Zhalong National Nature Reserve (46°480 –47°310 N, 123°510 –124°370 E), Heilongjiang, north China, during June 2013, at Nanbao village (19°420 N, 109°350 E), Hainan, south China, from April to May, 2014 and at Kraghede (578120 N, 108000 E), Denmark, during June 2013. Both the red-rumped swallow and the barn swallow are common passerines belonging to the swallow family. The red-rumped swallow breeds in open hilly country of temperate southern Europe and Asia, while the barn swallow can be found in Europe, Asia, Africa and America. Barn swallows have open cup-shaped nests made out of mud, straw and feathers, while the red-rumped swallow has retort-shaped nests built out of mud, straw and feathers, with the long entrance efficiently protecting the nest from brood parasitism. A recent study has shown that red-rumped swallows have no egg recognition ability of non-mimetic model cuckoo eggs, while the barn swallow rejects 15–42 % of non-mimetic eggs (Liang et al. 2013). Red-rumped swallows do not breed in Hainan, southern China, and Denmark, and thus, they were only used for experiments in north China. Testing for foreign objects recognition We used polymer clay to manufacture both egg-shaped, stick-shaped and coin-shaped models with the same texture, color (blue) and mass (Fig. 1; the size of models is presented in Table 1). Egg models or stick models (randomly chosen for each nest) were inserted into the nests of the two swallow species, and the nests were monitored for 6 days. For comparison of barn swallows between China and Denmark, coin-shaped models were also used. The experimental procedure was the same as the artificial parasitism widely used in studies of host responses to brood parasitism (e.g., Liang et al. 2013), in which the results were mainly classified as either acceptance if foreign objects were incubated or kept warm in the nests or rejection if foreign objects were ejected or left cold (deserted). However, no desertion was found in our experiment, and thus, ejection was the only means of rejection recorded here. Additionally, we conducted artificial parasitism and nest checks using a small spoon with a long handle and flashlight for the red-rumped swallow, which builds retort-shaped nests.
Anim Cogn (2015) 18:355–360
357
Fig. 1 Photos of experimental models used in the present study. a Blue egg model, b coin model, c stick model and d the three models for comparison
Table 1 Size and weight of different experimental models and eggs of two swallow species in this study
Model
Length (mm, mean ± SD)
Width (mm, mean ± SD)
Weight (g, mean ± SD)
Sample size (n)
Blue model egg
17.66 ± 0.28
12.28 ± 0.20
1.71 ± 0.17
20
Blue model stick
27.64 ± 0.14
10.69 ± 0.08
3.60 ± 0.05
14
Blue model coin
22.38 ± 0.12 (diameter)
3.58 ± 0.07
15
Half peanut shell
26.10 ± 1.75
12.78 ± 0.77
1.13 ± 0.28
20
Barn swallow egg
18.41 ± 0.91
13.27 ± 0.44
1.51 ± 0.22
80
Red-rumped swallow egg
20.56 ± 0.45
14.44 ± 0.24
2.71 ± 0.10
20
In 2014, we used half peanut shells in nests of barn swallows and red-rumped swallows to test for the fundamental recognition ability of foreign objects by these two swallow species. We conducted 242 replicates, with 74 in Denmark and 168 in China. The distribution of rejecters and accepters in the two species is shown in Table 2.
5.44 ± 0.06 (thickness)
Statistical analyses We used likelihood ratio tests and Fisher exact probability tests to test for heterogeneity in rejection rates of different types of models introduced into nests. We used logistic regression to test for the statistical independence of model
123
358
Anim Cogn (2015) 18:355–360
Table 2 Data on model experiments in two swallow species in China and Denmark Species
Egg models Accept
Stick models Reject
Accept
Coin models Reject
Accept
Half peanut shells Reject
Accept
Reject
Barn swallow northeast China
13
4
4
13
4
8
2
13
Barn swallow southeast China
9
9
4
14
5
11
0
13
Red-rumped swallow northeast China
14
0
12
3
11
2
Barn swallow Denmark
10
17
4
21
4
18
Numbers represent the number of responses to experimental parasitism
Fig. 2 Comparison of discrimination of foreign objects between red-rumped swallows and barn swallows. Percentages on bars refer to the percentage of rejection
types between the two countries by entering the interaction between model type and country in a statistical model that also included the two main effects. We carried out all tests using the software JMP (SAS 2012).
Results Barn swallows rejected a larger fraction of peanut shells than red-rumped swallows (barn swallow: 26 out of 28 clutches; red-rumped swallow: 2 out of 13 clutches: v2 = 25.65, df = 1, P \ 0.0001, likelihood ratio test), suggesting that the former species showed a fundamental ability to recognize foreign objects. There was no significant difference in rejection rate between sites for the barn
123
swallow (Hainan: 13 out of 13 nests, Heilongjiang: 13 out of 15: v2 = 2.63, df = 1, P = 0.10, likelihood ratio test). We found a significant difference in rejection behavior between the three model types (39 % for egg models, 74 % for coin models and 68 % for stick models, P = 0.0008, Fisher’s exact test). There was a significantly higher frequency of rejection in Denmark than in China (49 % in China versus 76 % in Denmark, v2 = 23.70, df = 1, P \ 0.0001, likelihood ratio test). The effect of egg model by country interaction was not statistically significant for barn swallows, implying that the egg model effect was similar in the two countries (v2 = 0.69, df = 2, P = 0.70, logistic regression). Likewise, the species by egg model interaction was not statistically significant (v2 = 1.48, df = 2, P = 0.22, logistic regression). Finally, the
Anim Cogn (2015) 18:355–360
rejection rate was higher in barn swallows than in redrumped swallows (v2 = 34.73, df = 1, P \ 0.0001, barn swallow 67 % versus red-rumped swallow 10 %, likelihood ratio test). Among different populations of barn swallow, rejection rates of egg models tend to increase with the increase in rejection rates in non-egg-shaped models (i.e., stick models) (Fig. 2). All red-rumped swallows accepted the non-mimetic egg models, while barn swallows rejected 48 %, this difference being statistically significant (Fig. 2; v2 = 16.08, df = 1, P = 0.0006, likelihood ratio test). For stick models, red-rumped swallows rejected 20 %, which was much less than the 80 % in barn swallows (v2 = 18.97, df = 1, P = 0.0001, likelihood ratio test).
Discussion We made extensive experiments on rejection of model eggs differing in shape, showing that two species of swallows had lower rejection rates of egg-shaped models compared with models of other shapes. Rejection behavior differed between species and countries. The main findings of these experiments were that (1) the egg recognition ability of barn swallows increased with the increase in rejection of non-egg-shaped objects among populations; (2) red-rumped swallows had no egg recognition ability and rejected few non-egg-shaped objects compared with barn swallows. These results suggested that nest sanitation behavior has been a pre-adaptation from which egg rejection behavior evolved. The evolution of egg rejection behavior constitutes a major adaptation to fight brood parasitism by parasitic cuckoos and other parasites. Nest sanitation has been hypothesized to constitute the ancestral state of egg rejection behavior because nest sanitation is ubiquitous, while egg rejection is not. In other words, we should be able to document that nest sanitation constitutes a pre-adaptation to rejection of eggs of brood parasites. Indeed, a recent review provided evidence consistent with the claim of ubiquitous nest sanitation (Guigueno and Sealy 2012). Furthermore, there was evidence of studies having shown that size and shape of model eggs were important determinants of eliciting rejection behavior (Moska´t et al. 2003; Guigueno and Sealy 2012). Our experiments showed that both swallow species rejected non-egg-shaped objects, namely stick and coin models. In addition, barn swallows rejected more stick models than red-rumped swallows. This difference between species is as expected because barn swallows are intermediate egg rejecters, while red-rumped swallows show no egg recognition ability (Liang et al. 2013). Although nest sanitation may be a pre-curser of egg rejection, this intuitively appealing hypothesis may not be able to account for all such
359
differences in behavior among species. The finding that barn swallows rejected a larger fraction of non-egg-shaped models and peanut shells than red-rumped swallows is inconsistent with the nest sanitation hypothesis. If this hypothesis was valid, we should expect rejection of nonegg-shaped objects to be more common in species in which there is a higher probability of mud pellets falling into the nest cup. If that was the case, we should expect a higher rejection rate in the red-rumped swallow with its retortshaped nest than in the barn swallow with its cup-shaped nest. The high rate of rejection of stick models by barn swallows suggests that brood parasitism even plays an important role in augmenting the rate of rejection of nonegg-shaped objects. Alternatively, red-rumped swallows have lost the egg rejection behavior secondarily from their ancestors because hirundine molecular phylogeny suggests that retort-type nesting represents a more advanced stage of evolution than mud cup nesting (Winkler and Sheldon 1993; Sheldon et al. 2005). In summary, our study contributes to advance the understanding of the evolution of egg recognition behavior in birds. Acknowledgments This work was supported by the National Natural Science Foundation of China (Nos. 31260514, 31272328 and 31472013), Program for New Century Excellent Talents in University (NCET-13-0761), Key Project of Chinese Ministry of Education (No. 212136) and Program of International S & T Cooperation (KJHZ2013-12).
References Davies NB (2000) Cuckoos, cowbirds and other cheats. Poyser, London Guigueno MF, Sealy SG (2012) Nest sanitation in passerine birds: implications for egg rejection in hosts of brood parasites. J Ornithol 153:35–52 Liang W, Yang C, Wang L, Møller AP (2013) Avoiding parasitism by breeding indoors: cuckoo parasitism of hirundines and rejection of eggs. Behav Ecol Sociobiol 67:913–918 Moska´t C, Sze´kely T, Kisbenedek T, Karcza Z, Ba´rtol I (2003) The importance of nest cleaning in egg rejection behaviour of great reed warblers Acrocephalus arundinaceus. J Avian Biol 34:16–19 Ortega CP, Cruz A (1988) Mechanisms of egg acceptance by marshdwelling blackbirds. Condor 90:349–358 Pola´cˇek M, Griggio M, Bartı´kova´ M, Hoi H (2013) Nest sanitation as the evolutionary background for egg ejection behaviour and the role of motivation for object removal. PLoS One 8(11):e78771 Rothstein SI (1975) An experimental and teleonomic investigation of avian brood parasitism. Condor 77:250–271 SAS (2012) JMP version 10.0. SAS Inc., Cary, NC, USA Sheldon FH, Whittingham LA, Moyle RG, Slikas B, Winkler DW (2005) Phylogeny of swallows (Aves: Hirundinidae) estimated from nuclear and mitochondrial DNA sequences. Mol Phylogenet Evol 35:254–270 Stokke BG, Polacikova L, Dyrcz A, Hafstand I, Moksnes A, Røskaft E (2010) Responses of Reed Warblers Acrocephalus
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360 scirpaceusto non-mimetic eggs of different sizes in a nest parasitism experiment. Acta Ornithol 45:98–104 Tinbergen N (1953) The herring gull’s world. Praeger, Oxford Underwood TJ, Sealy SG (2006) Influence of shape on egg discrimination in American robins and gray catbirds. Ethology 112:164–173
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Anim Cogn (2015) 18:355–360 Winkler DW, Sheldon FH (1993) Evolution of nest construction in swallows (Hirundinidae): a molecular phylogenetic perspective. Proc Natl Acad Sci USA 90:5705–5707 Zolei A, Hauber ME, Geltsch N, Moska´t C (2012) Asymmetrical signal content of egg shape as predictor of egg rejection by great reed warblers, hosts of the common cuckoo. Behaviour 149:391–406
ORIGINAL PAPER
Nest sanitation behavior in hirundines as a pre-adaptation to egg rejection to counter brood parasitism Canchao Yang • Longwu Wang • Wei Liang Anders Pape Møller
•
Received: 6 March 2014 / Revised: 28 August 2014 / Accepted: 9 September 2014 / Published online: 18 September 2014 Ó Springer-Verlag Berlin Heidelberg 2014
Abstract Previous studies suggested that nest sanitation behavior may have been a pre-adaptation from which egg rejection of brood parasite eggs evolved. We tested this hypothesis in two swallow species, the red-rumped swallow (Cecropis daurica) and the barn swallow (Hirundo rustica). Our results indicated that the red-rumped swallow, which is an accepter of foreign eggs, rejected a low percentage of non-egg-shaped objects and did so less often than the barn swallow, which is an intermediate rejecter of foreign eggs. Furthermore, the egg rejection rates of the barn swallow increased with the increase in rejection rates of non-egg-shaped objects among different populations. These results showed that nest cleaning behavior could have evolved into a means of reducing the costs of brood parasitism, suggesting that egg recognition ability has evolved from recognition of non-egg-shaped objects. This finding advances our understanding of the evolution of egg recognition behavior in birds. Keywords Cecropis daurica Egg recognition Egg rejection Hirundo rustica Nest cleaning
C. Yang L. Wang W. Liang (&) Ministry of Education Key Laboratory for Tropical Plant and Animal Ecology, College of Life Sciences, Hainan Normal University, Haikou 571158, China e-mail: [email protected] L. Wang College of Life Sciences, Wuhan University, Wuhan 430072, China A. P. Møller Laboratoire d’Ecologie, Syste´matique et Evolution, CNRS UMR 8079, Universite´ Paris-Sud, Baˆtiment 362, 91405 Orsay Cedex, France
Introduction Eggs constitute future offspring, and hence, there should be a strong incentive for parents to retrieve any egg-shaped structure that is found in the neighborhood of a nest. Indeed, Tinbergen (1953) showed for the herring gull (Larus argentatus) that nest owners would retrieve eggs or egg-shaped structures from a considerable distance by rolling these into their nests, when an experimenter placed eggs even at a significant distance from the nest. Studies and casual observations have shown that gulls and other ground nesting species are known to sit on egg-shaped stones and other structures as if such objects were real eggs (Tinbergen 1953). The downside of such egg retrieval is the incorporation of foreign objects into nests thereby interfering with or eliminating reproductive success. Removal of such objects through nest cleaning behavior is ubiquitous in altricial birds (Moska´t et al. 2003; Guigueno and Sealy 2012), while egg discrimination is regarded as a specific derived behavior that has evolved to protect against avian brood parasitism (Rothstein 1975; Davies 2000). Rothstein (1975) first proposed that nest cleaning may have been a pre-adaptation from which egg rejection evolved, and Moska´t et al. (2003) proposed a hierarchical concept to understand nest cleaning behavior versus egg discrimination as an explanation for rejection of foreign eggs. They both suggested that nest cleaning behavior has evolved into a means of reducing the costs of brood parasitism. If this mechanism was at work, we would expect that nest cleaning behavior would be particularly prominent in species with nests into which foreign objects may fall at a regular basis. Thus, we would expect that species such as swallows and martins that use holes in the ground or nests built out of mud would have an elevated risk of
123
356
finding pellets of mud or small stones in their nests. Indeed, one of us has often found small pellets of mud from the nest in the nest cup of barn swallows as a consequence of wear of the mud nest during reproduction, and that such pellets are invariably removed from the nest (A. P. Møller unpublished observations). Such objects may interfere with efficient incubation, and also pose a risk of damaging eggs, hence creating a selection pressure for their removal. Zolei et al. (2012) showed in experiments with a rejecter species, the great reed warbler (Acrocephalus arundinaceus), that artificial eggs with two blunt poles were rejected more often than eggs with a single blunt pole or two sharp poles, showing that there is selection on egg shape by hosts. In contrast, Stokke et al. (2010) found no difference in rate of ejection between large- and normal-sized model eggs by reed warblers (Acrocephalus scirpaceus). Guigueno and Sealy (2012) showed that shape and size of model eggs were the significant factors eliciting rejection for all host species that received experimental non-egg-shaped objects added to their nests before hatching. Furthermore, Underwood and Sealy (2006) provided evidence to suggest that egg rejecters have more refined abilities to discriminate against non-egg-shaped objects than egg accepters. They concluded that nest sanitation may be a pre-adaptation for anti-parasite defenses by playing a role in their evolution. Indeed, Ortega and Cruz (1988) showed for two species of blackbirds that they accepted all egg-shaped objects, but rejected all other objects from their nests. This finding is as expected if egg discrimination has evolved in response to removal of random objects from nests during nest sanitation. A recent study on tree sparrows (Passer montanus) by Pola´cˇek et al. (2013) also speculated that nest sanitation plays a key role in the evolution of the removal of parasitic eggs. Here, we performed a foreign object experiment (including non-egg-shaped and egg-shaped models) to test the relationship between egg recognition and rejection and nest sanitation by comparing two swallow species, the redrumped swallow (Cecropis daurica, formerly Hirundo daurica) and the barn swallow (Hirundo rustica), and by comparing different populations of barn swallows. A recent study showed that the former species is a total accepter, while the latter is an intermediate rejecter of non-mimetic eggs (Liang et al. 2013). Therefore, we predicted that (1) both swallow species would reject a certain percentage of non-egg-shaped objects and that barn swallows would reject more than red-rumped swallows if nest cleaning has been a pre-adaptation from which egg rejection evolved. Furthermore, we predicted that (2) different populations of barn swallows would have different egg rejection rates related to rejection rates of non-egg-shaped objects if nest sanitation abilities differed between populations. In other
123
Anim Cogn (2015) 18:355–360
words, populations with higher egg rejection rates would reject more non-egg-shaped objects.
Materials and methods Study area and species This study was performed at Zhalong National Nature Reserve (46°480 –47°310 N, 123°510 –124°370 E), Heilongjiang, north China, during June 2013, at Nanbao village (19°420 N, 109°350 E), Hainan, south China, from April to May, 2014 and at Kraghede (578120 N, 108000 E), Denmark, during June 2013. Both the red-rumped swallow and the barn swallow are common passerines belonging to the swallow family. The red-rumped swallow breeds in open hilly country of temperate southern Europe and Asia, while the barn swallow can be found in Europe, Asia, Africa and America. Barn swallows have open cup-shaped nests made out of mud, straw and feathers, while the red-rumped swallow has retort-shaped nests built out of mud, straw and feathers, with the long entrance efficiently protecting the nest from brood parasitism. A recent study has shown that red-rumped swallows have no egg recognition ability of non-mimetic model cuckoo eggs, while the barn swallow rejects 15–42 % of non-mimetic eggs (Liang et al. 2013). Red-rumped swallows do not breed in Hainan, southern China, and Denmark, and thus, they were only used for experiments in north China. Testing for foreign objects recognition We used polymer clay to manufacture both egg-shaped, stick-shaped and coin-shaped models with the same texture, color (blue) and mass (Fig. 1; the size of models is presented in Table 1). Egg models or stick models (randomly chosen for each nest) were inserted into the nests of the two swallow species, and the nests were monitored for 6 days. For comparison of barn swallows between China and Denmark, coin-shaped models were also used. The experimental procedure was the same as the artificial parasitism widely used in studies of host responses to brood parasitism (e.g., Liang et al. 2013), in which the results were mainly classified as either acceptance if foreign objects were incubated or kept warm in the nests or rejection if foreign objects were ejected or left cold (deserted). However, no desertion was found in our experiment, and thus, ejection was the only means of rejection recorded here. Additionally, we conducted artificial parasitism and nest checks using a small spoon with a long handle and flashlight for the red-rumped swallow, which builds retort-shaped nests.
Anim Cogn (2015) 18:355–360
357
Fig. 1 Photos of experimental models used in the present study. a Blue egg model, b coin model, c stick model and d the three models for comparison
Table 1 Size and weight of different experimental models and eggs of two swallow species in this study
Model
Length (mm, mean ± SD)
Width (mm, mean ± SD)
Weight (g, mean ± SD)
Sample size (n)
Blue model egg
17.66 ± 0.28
12.28 ± 0.20
1.71 ± 0.17
20
Blue model stick
27.64 ± 0.14
10.69 ± 0.08
3.60 ± 0.05
14
Blue model coin
22.38 ± 0.12 (diameter)
3.58 ± 0.07
15
Half peanut shell
26.10 ± 1.75
12.78 ± 0.77
1.13 ± 0.28
20
Barn swallow egg
18.41 ± 0.91
13.27 ± 0.44
1.51 ± 0.22
80
Red-rumped swallow egg
20.56 ± 0.45
14.44 ± 0.24
2.71 ± 0.10
20
In 2014, we used half peanut shells in nests of barn swallows and red-rumped swallows to test for the fundamental recognition ability of foreign objects by these two swallow species. We conducted 242 replicates, with 74 in Denmark and 168 in China. The distribution of rejecters and accepters in the two species is shown in Table 2.
5.44 ± 0.06 (thickness)
Statistical analyses We used likelihood ratio tests and Fisher exact probability tests to test for heterogeneity in rejection rates of different types of models introduced into nests. We used logistic regression to test for the statistical independence of model
123
358
Anim Cogn (2015) 18:355–360
Table 2 Data on model experiments in two swallow species in China and Denmark Species
Egg models Accept
Stick models Reject
Accept
Coin models Reject
Accept
Half peanut shells Reject
Accept
Reject
Barn swallow northeast China
13
4
4
13
4
8
2
13
Barn swallow southeast China
9
9
4
14
5
11
0
13
Red-rumped swallow northeast China
14
0
12
3
11
2
Barn swallow Denmark
10
17
4
21
4
18
Numbers represent the number of responses to experimental parasitism
Fig. 2 Comparison of discrimination of foreign objects between red-rumped swallows and barn swallows. Percentages on bars refer to the percentage of rejection
types between the two countries by entering the interaction between model type and country in a statistical model that also included the two main effects. We carried out all tests using the software JMP (SAS 2012).
Results Barn swallows rejected a larger fraction of peanut shells than red-rumped swallows (barn swallow: 26 out of 28 clutches; red-rumped swallow: 2 out of 13 clutches: v2 = 25.65, df = 1, P \ 0.0001, likelihood ratio test), suggesting that the former species showed a fundamental ability to recognize foreign objects. There was no significant difference in rejection rate between sites for the barn
123
swallow (Hainan: 13 out of 13 nests, Heilongjiang: 13 out of 15: v2 = 2.63, df = 1, P = 0.10, likelihood ratio test). We found a significant difference in rejection behavior between the three model types (39 % for egg models, 74 % for coin models and 68 % for stick models, P = 0.0008, Fisher’s exact test). There was a significantly higher frequency of rejection in Denmark than in China (49 % in China versus 76 % in Denmark, v2 = 23.70, df = 1, P \ 0.0001, likelihood ratio test). The effect of egg model by country interaction was not statistically significant for barn swallows, implying that the egg model effect was similar in the two countries (v2 = 0.69, df = 2, P = 0.70, logistic regression). Likewise, the species by egg model interaction was not statistically significant (v2 = 1.48, df = 2, P = 0.22, logistic regression). Finally, the
Anim Cogn (2015) 18:355–360
rejection rate was higher in barn swallows than in redrumped swallows (v2 = 34.73, df = 1, P \ 0.0001, barn swallow 67 % versus red-rumped swallow 10 %, likelihood ratio test). Among different populations of barn swallow, rejection rates of egg models tend to increase with the increase in rejection rates in non-egg-shaped models (i.e., stick models) (Fig. 2). All red-rumped swallows accepted the non-mimetic egg models, while barn swallows rejected 48 %, this difference being statistically significant (Fig. 2; v2 = 16.08, df = 1, P = 0.0006, likelihood ratio test). For stick models, red-rumped swallows rejected 20 %, which was much less than the 80 % in barn swallows (v2 = 18.97, df = 1, P = 0.0001, likelihood ratio test).
Discussion We made extensive experiments on rejection of model eggs differing in shape, showing that two species of swallows had lower rejection rates of egg-shaped models compared with models of other shapes. Rejection behavior differed between species and countries. The main findings of these experiments were that (1) the egg recognition ability of barn swallows increased with the increase in rejection of non-egg-shaped objects among populations; (2) red-rumped swallows had no egg recognition ability and rejected few non-egg-shaped objects compared with barn swallows. These results suggested that nest sanitation behavior has been a pre-adaptation from which egg rejection behavior evolved. The evolution of egg rejection behavior constitutes a major adaptation to fight brood parasitism by parasitic cuckoos and other parasites. Nest sanitation has been hypothesized to constitute the ancestral state of egg rejection behavior because nest sanitation is ubiquitous, while egg rejection is not. In other words, we should be able to document that nest sanitation constitutes a pre-adaptation to rejection of eggs of brood parasites. Indeed, a recent review provided evidence consistent with the claim of ubiquitous nest sanitation (Guigueno and Sealy 2012). Furthermore, there was evidence of studies having shown that size and shape of model eggs were important determinants of eliciting rejection behavior (Moska´t et al. 2003; Guigueno and Sealy 2012). Our experiments showed that both swallow species rejected non-egg-shaped objects, namely stick and coin models. In addition, barn swallows rejected more stick models than red-rumped swallows. This difference between species is as expected because barn swallows are intermediate egg rejecters, while red-rumped swallows show no egg recognition ability (Liang et al. 2013). Although nest sanitation may be a pre-curser of egg rejection, this intuitively appealing hypothesis may not be able to account for all such
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differences in behavior among species. The finding that barn swallows rejected a larger fraction of non-egg-shaped models and peanut shells than red-rumped swallows is inconsistent with the nest sanitation hypothesis. If this hypothesis was valid, we should expect rejection of nonegg-shaped objects to be more common in species in which there is a higher probability of mud pellets falling into the nest cup. If that was the case, we should expect a higher rejection rate in the red-rumped swallow with its retortshaped nest than in the barn swallow with its cup-shaped nest. The high rate of rejection of stick models by barn swallows suggests that brood parasitism even plays an important role in augmenting the rate of rejection of nonegg-shaped objects. Alternatively, red-rumped swallows have lost the egg rejection behavior secondarily from their ancestors because hirundine molecular phylogeny suggests that retort-type nesting represents a more advanced stage of evolution than mud cup nesting (Winkler and Sheldon 1993; Sheldon et al. 2005). In summary, our study contributes to advance the understanding of the evolution of egg recognition behavior in birds. Acknowledgments This work was supported by the National Natural Science Foundation of China (Nos. 31260514, 31272328 and 31472013), Program for New Century Excellent Talents in University (NCET-13-0761), Key Project of Chinese Ministry of Education (No. 212136) and Program of International S & T Cooperation (KJHZ2013-12).
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