- Email: [email protected]
Maintenance of male reaction to the congeneric song in the Hippolais warbler hybrid zone
Behavioural Processes 46 (1999) 151 – 158
Maintenance of male reaction to the congeneric song in the Hippolais warbler hybrid zone J. Secondi a,*, B. Faivre a, M. Kreutzer b b
a Laboratoire Ecologie-E6olution, Uni6ersite´ de Bourgogne, 6, Bl6d. Gabriel, 21000 Dijon, France Laboratoire de Psychophysiologie et d’e´thologie, Uni6ersite´ Paris X. 200, A6enue de la Re´publique, 92001 Nanterre Cedex, France
Received 30 September 1998; received in revised form 25 February 1999; accepted 1 March 1999
Abstract Both hybridization and competition may induce character shift on communication systems in hybrid zones, leading either to convergence or divergence. Melodious warblers Hippolais polyglotta and Icterine warblers H. icterina are interspecifically territorial and hybridize along a narrow contact zone. This spatial distribution is favoured by a reaction to the congeneric song. A character displacement, e.g. a decrease of the reaction, was expected within the hybrid zone because of reproduction costs lower than in allopatry. We investigated the pattern of variation of the interspecific reaction by comparing allopatric and sympatric populations. However, our data did not support the hypothesis character displacement and we propose several alternatives to account for the maintenance of interspecific reaction in sympatry. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Competition; Hybridization; Song learning; Territoriality; Moving front
1. Introduction Reaction to heterospecific signals can be favoured under various ecological conditions, ranging from cooperation (Moynihan 1968; Hurd, 1996) to competition (Cody 1973; Catchpole 1978; Catchpole and Leisler, 1986; Martin et al., 1996). In the latter case, the reaction to a heterospecific signal will often depend on local ecological condi* Corresponding author.
tions. For instance, Great Tits Parus major and Chaffinches Fringilla coelebs have been reported to actively respond to songs of the other species in an insular environment, whereas no such response was reported for their mainland counterparts exploiting a more heterogeneous environment (Reed, 1982). In the case of closely-related species that are active at the same season and in the same environment, reaction to heterospecific signals may correspond to competition (Orians and Willson, 1964; Rohwer, 1972; Catchpole, 1978; Rice,
0376-6357/99/$ - see front matter © 1999 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 6 - 6 3 5 7 ( 9 9 ) 0 0 0 2 9 - 7
152
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
1978; Leisler, 1986; Martin et al., 1996) or simply result from a lack of divergence in the communication system of both species (Murray, 1971, 1976, 1981). The second situation may happen when two species come into secondary contact after separation (Ferry and Deschaintre, 1974; Murray, 1976; Robbins et al., 1986). Hybrid zones are thus particularly interesting for the study of interspecific territoriality between closely related species because the existence of allopatric populations may provide a baseline from which to evaluate separately the relative influence of interspecific competition and relatedness. Most studies concern hybrid zones which are stable in place and time (Moore and Buchanan, 1985; Hewitt, 1988; Rising, 1996), whereas gradual shifts of hybrid zones remain rare and poorly documented (Barton and Hewitt, 1985; Gill, 1997). We studied reactions to congeneric vocal signals in two closely related passerine species, the Melodious warbler Hippolais polyglotta and the Icterine warbler H. icterina, for which species interspecific territoriality has been previously reported (Ferry and Deschaintre, 1974). Their parapatric breeding distributions overlap over 350 km width in Belgium, northern and eastern France and Switzerland (Cramp, 1992). During the last decades, H. polyglotta has expanded its range, while H. icterina has regressed over all the contact zone. This resulted in a shift northwards and eastwards in the position of the contact zone as the Melodious warbler progressively replaced its sibling species (Glutz Von Blotzheim and Bauer, 1991; Faivre, 1993). Evidence of introgression for morphological characters suggest that hybrids can backcross with at least one parental species (Faivre et al., 1999). In addition, mixed pairings have also been observed in sympatry (Faivre et al., 1999). These pairs tend to have a reduced breeding success compared with homospecific pairs (Faivre, unpublished results). In this context, a decrease in the male reaction to the congeneric song in sympatric populations of Hippolais warblers could be expected in both species. In the present study, we test the hypothesis of a character displacement. We compare males’ reactions to congeneric songs between allopatric and sympatric populations of Hippolais warblers.
We discuss the observed pattern in relation to competition and hybridization and propose that the demographic context and behavioural mechanisms, related to song learning and mate choice, are key factors of the evolution and maintenance of interspecific reaction
2. Methods
2.1. Populations sampled One allopatric population of Melodious warblers was studied near Tours (Central France) about 400 km away from the nearest Icterine warbler population (Yeatman-Berthelot and Jarry, 1994). One allopatric population of Icterine warblers was sampled near Lie`ge (Belgium), 50 km north of the contact zone. Sympatric sites were located in Burgundy and Franche-Comte´ (Eastern France) at the western border of the contact zone (Fig. 1). They are part of the oldest areas of sympatry and Icterine warblers are geographically relatively isolated from allopatric populations.
2.2. Playback experiment A tape recorder and a loudspeaker in a basket were hung onto one song post of the focal bird or inside the territory less than 5 m of a song post when hanging was not possible. Three min of silence preceded playback. The observer took place at 10–20 m of the loudspeaker during the first min. Each experiment was divided in three 4-min periods, each one containing 2 phases of 2 min length: a playback (ON) and a silent phase (OFF) (Fig. 2). During the first playback period, hereafter referred to as the control period, the recording of a phylogenetically unrelated species, the nightingale Luscinia megarhynchos was played and provided a baseline for each test. This species is widely sympatric with both Hippolais warblers but no evidence of systematic aggression has been reported (Cramp 1992, personal observation). During the second playback period, hereafter referred to as the test period, a sympatric or an
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
153
presentation of the periods because we intended to measure the reaction to congeneric song. Therefore, we needed a baseline, e.g. the playback of another species, to assess any change of activity. Playing specific song can alter the behaviour of birds over a long period. Broadcasting a stimulus from the same location a few minutes apart could still alter the reaction to that stimulus (Falls, 1992). Tests were carried out on 16 sympatric and 15 allopatric Melodious warblers. Six allopatric and ten sympatric Icterine warblers were tested. Each bird was tested only once. Experiments were performed between 4 and 11 A.M. (G.M.T.) during the breeding season, from 1 May to 13 June in 1996 and 1997.
2.3. Recording samples
Fig. 1. Breeding ranges and overlap zone of Melodious and Icterine warblers in western Europe. Dots indicate the location of study and recording sites.
Fig. 2. Playback design used in the experiment. The vocal activity is recorded during three 4-min periods ( ). Songs are played during the first 2 min of each period. Inst., installation 3-min period after placing the loudspeaker. ‘ON’ indicates that the loudspeaker is playing a recording. ‘OFF’ indicates that no song is broadcast. See Section 2 for the description of each period.
allopatric recording of the congeneric species was played. The recording type was alternated between birds. A specific recording of the sampled population was broadcast during the third period referred to as the specific period. Each experiment lasted 15 min. We did not balance the order of
One recording of Nightingale provided the control signal. Its potency was indirectly assessed as in many trials Nightingales approached and sang after its broadcasting. For each species, ten congeneric recordings of 2 min length were chosen. Five sympatric recordings came from our study sites and five allopatric recordings came from distant locations of the distribution areas (Fig. 1). Two birds recorded in the population provided the specific controls. All the signals were digitized using SoundEdit 16 software on a Macintosh computer. The sampling frequency was 22050 Hz and the amplitude resolution was 8 bits. All the recordings were broadcast without any cutting or rearrangement but every gap between the songs of the recordings was replaced by a low frequency noise (below 500 Hz) that mimicked the natural noise and suppressed the songs of other species on the tapes. The synthetic noise was also emitted during the silent phases. The whole sequence of 15 min was recorded with a numeric tape recorder Sony TCD D7 and was broadcast with an amplified speaker Sony SRS-68.
2.4. Measure of the beha6ioural response Behavioural responses were assessed by monitoring the vocal activity. Preliminary tests showed that specific songs induced an increase in song rate (J. Secondi, unpublished data). Approach can
154
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
be elicited (Ferry and Deschaintre, 1974) but it appears unreliable for a standardized protocol. In most cases, the distance to the speaker cannot be measured accurately because birds are often hidden in the vegetation (personal observation). Thus, we measured the vocal activity that we defined as the amount of time spent singing during each period. Occasionally, the tape masked the songster so that the vocal activity was not accurately recorded. We discarded these trials from our sample for Melodious warblers. Thus, the vocal activity is given period by period. Because of the small sample in allopatry, we could not discard trials for Icterine warblers and measured the responses using the silent phases only.
2.4.1. Reaction to congeneric song The reaction to congeneric song was assessed by comparing the vocal activity during control and test periods. We also compared control and specific control periods so that we could check that the territorial reaction was released. Finally, we compared the relative potency of congeneric signals and specific signals. However, the measure of the reaction to the specific recording is not completely accurate since the congeneric recording could have altered the reaction to the specific recordings. In each case, sympatric and allopatric populations were analyzed separately using Wilcoxon signed-ranked test (Siegel and Castellan, 1988). Because variables were used in more than one test, significance thresholds were corrected using Bonferroni method (Sokal and Rohlf, 1995). 2.4.2. Character displacement We tested the hypothesis of character displacement in a two-step analysis. For each species, we compared the vocal activity of the allopatric and the sympatric populations to ensure that the vocal activity was similar during the control period in both populations. We then computed the difference of vocal activity between test and control periods and compared the populations for this difference. Finally, we tested the effect of the congeneric recording origin, e.g. sympatry vs. allopatry, on the inten-
sity of the reaction. Mann–Whitney U-tests were used in these analyses. Sample sizes were not held constant between analyses because we discarded the individuals for which the variables could not be measured during one playback or silent phase.
3. Results
3.1. Reaction to congeneric song When comparing the control and the test period, we observed a significant increase of the vocal activity during the latter period in sympatry and allopatry for the Melodious warbler. The same trend was observed for Icterine warblers (Table 1). Actually, 6 out of 8 sympatric birds and five out of six allopatric birds increased their song rate during the congeneric period. Thus, each population exhibited a tendency to respond to the sibling species song. However, sample sizes were small for this species and the power of the tests was consequently reduced. It is likely that larger sample sizes would have yielded significant differences. Both Melodious warblers populations showed an increase of their vocal activity during the specific period relatively to the control period (Table 1). The vocal response was strong and the difference between the periods was highly significant. The same pattern was observed in sympatric Icterine warblers as all birds increased their song rate during the specific period whereas in allopatry, only three out of six birds showed a higher vocal activity. An increase of the vocal activity was also observed in both populations of Melodious warblers during the specific period relatively to the test period, whereas Icterine warblers showed no variation in vocal activity between these two periods (Table 1). The highest vocal activity was recorded during the specific period in Melodious warblers. So the response was graded in this species. In contrast, in Icterine warblers, the maximal activity has been reached since the test period, when broadcasting the congeneric recording.
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
155
Table 1 Means and standard deviations for the vocal activity during playback experiments in allopatric and sympatric populations of Hippolais warblersa Control period (1) (s)
Congeneric period (2) (s)
Specific period (3) (s)
Congeneric reaction (2)-(1) P
Specific reaction (3)-(1) P
Specificcongeneric (3)-(2) P
H. polyglotta Allopatry Sympatry
53.7 950.6 67.2 9 59.2
100.7942.4 107.89 56.6
131.79 40.2 133.49 56.5
0.012* (15) 0.001* (16)
B0.001* (15) B0.001* (16)
0.006* (15) 0.023* (16)
H. icterina Sympatry Allopatry
45.6 923.2 55.8 9 35.4
64.3925.0 68.2930.9
76.29 7.1 63.19 15.4
0.028 (10) (ns) 0.245 (6) (ns)
0.005* (10) 0.462 (6) (ns)
0.155 (9) (ns) 0.528 (6) (ns)
a The total vocal activity is measured for the whole 4-min periods in H. polyglotta and for the silent 2-min phases in H. icterina. Sample sizes are noted in parentheses. P-values are the results of Wilcoxon signed-rank tests for test vs. control period, specific control vs. specific periods and test vs. specific periods. Significance thresholds were corrected using Bonferroni method for the baseline.
3.2. Character displacement For both Hippolais warblers, the vocal activity during the baseline was similar in sympatry and in allopatry (Table 2). We could then compare the reactions to the congeneric song in allopatry and in sympatry. We found no significant difference between the populations (Table 2). Thus, there was no evidence for a weaker reaction to the congeneric song inside the overlap zone. Finally, we assessed the difference of reaction to sympatric and allopatric congeneric recordings. This analysis was carried out in Melodious warblers only because sample sizes were too small in icterine warblers. No significant difference was observed (Mann–Whitney: sympatry: n =16, U = 40.5, P = 0.254; allopatry: n =15, U = 32, P =0.643). Whatever the recording origin relatively to the contact zone, allopatric and sympatric individuals did not exhibit differential reaction.
4. Discussion Our study suggests the existence of a vocal reaction to the sibling species song in sympatric and allopatric populations of Hippolais warblers. The reaction was characterized by a significant increase of the vocal activity during the congeneric playback in Melodious warblers. The
same trend was also observed in Icterine warblers. Our results were congruent with an earlier study by Ferry and Deschaintre (1974) that reported a motor reaction. However, in this preliminary study the duration of playbacks was not standardized, thus hampering the comparison of the populations. In the present study, we could compare the reactions of allopatric and sympatric populations to assess the hypothesis of character displacement. Data showed no significant difference between populations in both Hippolais species. Thus, our data do not provide evidence of character displacement in the male reactions to the sibling species song. The intensity of the congeneric reaction could also vary because of character shift on signal. Thus, we tested if sympatric and allopatric songs elicited quantitatively different reactions. The comparison was available for Melodious warblers only but, here again, no significant difference was found. Melodious warblers did not react differently to allopatric and sympatric signals. Thus, even if variations existed between Icterine warbler recordings according to their origin, these differences were apparently not used by birds to adjust their behaviour. The Hippolais warblers hybrid zone provides conditions to study character displacement on communication systems. Song is an essential feature of territorial defence and very likely of mate attraction (Secondi, unpublished data). A shift in
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
156
Table 2 Comparison of the vocal activity during the control period (baseline) and comparison of the reaction to the congeneric song between sympatric and allopatric populations of Hippolais warblersa Allopatry (s)
Sympatry (s)
nallopatry
nsympatry
U
P
Baseline H. polyglotta H. icterina
53.7 55.8
67.2 45.6
15 6
16 10
133.5 40
0.509 ns 0.277 ns
Congeneric reaction H. polyglotta H. icterina
47.0 18.7
40.6 12.4
15 6
16 10
128 32.5
0.752 ns 0.786 ns
a The reaction to the congeneric song is measured as the difference of scores between the test and the control periods. Significance thresholds were corrected using Bonferroni method when comparing the baselines. Ns, non significant difference.
signal or in behavioural response to signal should be highly expected then but our data did not support this hypothesis. Instead, they suggested the maintenance of the reaction in Melodious and Icterine warblers in sympatry. However, one should be cautious in interpreting these results. Indeed, sample sizes in Icterine warblers are small, particularly for the allopatric population. It results that the power of the tests could be low. In this species, we are aware that the external validity of the experiment should have been improved by increasing sample sizes. However, this was not possible because of time and logistic constraints. Anyway, we feel relatively confident with our results because they are congruent with the strong motor response already described in sympatry by Ferry and Deschaintre (1974). Several hypotheses could account for the maintenance of the male reaction in sympatry. However, each species should be considered in a different demographic context. Colonization and migration rates could be higher in the expanding Melodious warbler than in the regressing Icterine warbler (but see Kirkpatrick and Barton, 1997). In the former species, sympatric populations could be diluted by constant immigration that would disrupt adaptations evolved in older resident populations. In addition, the slipping of the overlap zone could be too quick to observe character displacement. Icterine warbler populations could go extinct before adaptation occurs. Adding to this demographic background, other non-exclusive hypotheses can be proposed. Firstly, in sympatry, competition with other spe-
cies could increase the overlap in resource use for Hippolais warblers. This could promote interspecific territoriality (Cody, 1973) and the maintenance of the reaction to the congeneric song. Secondly, song learning and cultural transmission could hamper the divergence of populations, e.g. the loss of the reaction to the congeneric song in sympatry. Hippolais warblers are very similar morphologically (Cramp, 1992). This characteristics could favour heterospecific tutoring in syntopy, particularly in the less abundant species (Thielcke, 1972; Clausen and Toft, 1988). Moreover, learning to discriminate songs could also be a difficult task. Species recognition can use both acoustic and visual cues (Baker and Baker, 1990). However, Hippolais are virtually indistinguishable on the basis of plumage coloration (Jouard, 1935; Wallace, 1964). Thus, the association between song and species identity probably cannot rely on visual cues. Thirdly, an active female choice could also select for the maintenance of signal design. Given the close ancestry of both species, some choice criteria could be similar. Signal differentiation could be constrained and a certain level of heterospecific pairing could be maintained in sympatry if females would exhibit conservative preferences for song. In addition, in Hippolais warblers, hybrids seem viable and fertile as introgression of some morphological characters of Melodious warblers in Icterine warblers has been observed in sympatry (Faivre et al., 1999). However, one can reasonably think that hybridization costs may be too low to drive a reinforcement process on song (Liou and Price, 1994; Hostert, 1997).
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
Demographic, ecological, behavioural or explanations can explain the absence of character displacement in the contact zone. Knowledge of population dynamics is needed to fully understand the observed patterns. However, it appears that detailed data on song learning are important as well since epigenetic mechanisms seem to be able to maintain a high level of interspecific interaction. Finally, testing other sympatric populations would be most informative. Character displacement could have occurred in other zones of sympatry where different conditions could prevail. Age of the secondary contact, relative density of each species, gene flows from allopatric populations, ecological constraints related to the bird community are such sources of geographical variation in interspecific interactions. Their relative weight should vary between different hybrid zones. They can also explain the variations in the internal structure of a given hybrid zone.
Acknowledgements We are very grateful to Emile Clotuche and Jean-Paul Jacob for their kindness and help in Belgium. We are indebted to Karl-Heinz Frommolt, Jean-Claude Roche´ and Patrick Sellar for providing recordings of allopatric Icterine warblers. We thank very much Yann Doisneau, Franck Grossiord and Francis Raoul for their assistance in the field and Frank Cezilly for his comments and valuable improvements of the manuscript.
References Barton, N.H., Hewitt, G.M., 1985. Analysis of hybrid zones. Ann. Rev. Ecol. Syst. 16, 113–148. Barton, N.H., Hewitt, G.M., 1985. Analysis of hybrid zones. Ann. Rev. Ecol. Syst. 16, 113–148. Catchpole, C.K., 1978. Interspecific territorialism and competition Acrocephalus warblers as revealed by playback experiments in area of sympatry and allopatry. Anim. Behav. 26, 1072 – 1082. Catchpole, C.K., Leisler, B., 1986. Interspecific territorialism in Reed warblers: a local effect revealed by playback experiments. Anim. Behav. 34, 299–300.
157
Clausen, P., Toft, S., 1988. Mixed singers and imitation singers among short-toed treecreepers. Br. Birds 81, 496 – 503. Cody, M.L., 1973. Character convergence. Annu. Rev. Syst. Ecol. 4, 189 – 211. Cramp, S., 1992. Handbook of birds of Europe, the Middle East and North Africa, vol. 6. Oxford University Press, Oxford. Faivre, B., 1993. La pre´dation joue-t-elle un roˆle dans la re´gression de l’Hypolaı¨s icte´rine Hippolais icterina. Rev. Ecol. (Terre Vie) 48, 399 – 420. Faivre B., Secondi J., Ferry C., Chastragnat L. and Ce´zilly F., 1999. Morphological variation and the recent evolution of wing length in the Icterine warbler: a case of unidirectional introgression? J. Av. Biol., in press. Falls, J.B., 1992. Playback: a historical perspective. In Playback and studies of animal communication. Plenum Press, New York, pp. 11 – 34. Ferry, C., Deschaintre, A., 1974. Le chant, signal interspe´cifique chez Hippolais icterina et H. polyglotta. Alauda 17, 289 – 312. Gill, F.B., 1997. Local cytonuclear extinction in the Goldenwinged warbler. Evolution 51, 519 – 523. Glutz Von Blotzheim, U.S., Bauer, K.M., 1991. Handbuch der Vo¨gel Mitteleuropas. Aula-Verlag, Wiesbaden, pp. 565 – 625. Hewitt, G.M., 1988. Hybrid zones-natural laboratories for evolutionary studies. Tree 3, 1988. Hostert, E.E., 1997. Reinforcement: a new perspective on an old perspective. Evolution 51, 697 – 702. Hurd, C.R., 1996. Interspecific attraction to mobbing calls of Black-capped chickadees (Parus atricapillus). Behav. Ecol. Sociobiol. 38, 287 – 292. Jouard, H., 1935. Sur la distribution en France des deux espe`ces d’Hypolaı¨s, et sur quelques-uns des caracte`res propres a` les faire distinguer surement. Alauda 7, 85 – 99. Kirkpatrick, M., Barton, N.H., 1997. Evolution of a species’ range. Am. Nat. 150, 1 – 23. Leisler, B., 1986. Interspecific interactions among European marsh-nesting passerines. In: Ouellet, H. (Ed.), XIX Congressus internationalis ornithologici. Ottawa University Press, Ottawa, pp. 2635 – 2644. Liou, L.W., Price, T.D., 1994. Speciation by reinforcement of premating isolation. Evolution 48, 1451 – 1459. Martin, P.R., Fotheringham, J.R., Ratcliffe, L., Robertson, R.J., 1996. Response of American redstarts (Suborder Passeri ) and Least flycatcher (suborder Tyrannii ) to heterospecific playback: the role of song in aggressive interactions and interference competition. Behav. Ecol. Sociobiol. 39, 227 – 235. Moore, W.S., Buchanan, D.B., 1985. Stability of the Northern flicker hybrid zone in historical times: implications for adaptive speciation theory. Evolution 39, 135 – 151. Moynihan, M., 1968. Social mimicry; character convergence versus character displacement. Evolution 22, 315 – 331. Murray, B.G., 1976. A critique of interspecific territoriality and character convergence. Condor 78, 518 – 525.
158
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
Murray, B.G., 1981. The origins of adaptive interspecific territorialism. Biol. Rev. 56, 1–22. Murray, B.G.J., 1971. The ecological consequences of interspecific territorial behavior in birds. Ecology 52, 414–423. Orians, G.H., Willson, M.F., 1964. Interspecific territories of birds. Ecology 45, 736–745. Reed, T.M., 1982. Interspecific territoriality in the Chaffinch and Great Tit on islands and the mainland of Scotland: playback and removal experiments. Anim. Behav. 30, 171– 181. Rice, J.C., 1978. Behavioural interactions of interspecifically territorial vireos. I-Song discrimination and natural interactions. Anim. Behav. 26, 527–549. Rising, J.D., 1996. The stability of the Oriole hybrid zone in western Kansas. Condor 96, 658–663. Robbins, M.B., Braun, M.J., Tobey, E.A., 1986. Morphological and vocal variation across a contact zone between the
chickadees Parus atricapillus and P. carolinensis. Auk 103, 655 – 666. Rohwer, S.A., 1972. Significance of sympatry to behaviour and evolution of Great plains meadowlarks. Evolution 27, 44 – 57. Siegel, S., Castellan, N.J., 1988. Non parametric statistics for the behavioral sciences. MacGraw-Hill, New York, p. 399. Sokal, R.R., Rohlf, F.J., 1995. Biometry. Freeman and Co, New York, p. 887. Thielcke, G., 1972. Waldbaumla¨ufer (Certhia familiaris) ahmen artfremdes signal nach und reagieren darauf. J. Orn. 113, 287 – 296. Wallace, D.I.M., 1964. Field identification of Hippolais warblers. Br. Birds 57, 282 – 301. Yeatman-Berthelot, D., Jarry, G., 1994. Nouvel atlas des oiseaux nicheurs de France 1985-1989. Socie´te´ Ornithologique de France, Paris, p. 775.
.
Maintenance of male reaction to the congeneric song in the Hippolais warbler hybrid zone J. Secondi a,*, B. Faivre a, M. Kreutzer b b
a Laboratoire Ecologie-E6olution, Uni6ersite´ de Bourgogne, 6, Bl6d. Gabriel, 21000 Dijon, France Laboratoire de Psychophysiologie et d’e´thologie, Uni6ersite´ Paris X. 200, A6enue de la Re´publique, 92001 Nanterre Cedex, France
Received 30 September 1998; received in revised form 25 February 1999; accepted 1 March 1999
Abstract Both hybridization and competition may induce character shift on communication systems in hybrid zones, leading either to convergence or divergence. Melodious warblers Hippolais polyglotta and Icterine warblers H. icterina are interspecifically territorial and hybridize along a narrow contact zone. This spatial distribution is favoured by a reaction to the congeneric song. A character displacement, e.g. a decrease of the reaction, was expected within the hybrid zone because of reproduction costs lower than in allopatry. We investigated the pattern of variation of the interspecific reaction by comparing allopatric and sympatric populations. However, our data did not support the hypothesis character displacement and we propose several alternatives to account for the maintenance of interspecific reaction in sympatry. © 1999 Elsevier Science B.V. All rights reserved. Keywords: Competition; Hybridization; Song learning; Territoriality; Moving front
1. Introduction Reaction to heterospecific signals can be favoured under various ecological conditions, ranging from cooperation (Moynihan 1968; Hurd, 1996) to competition (Cody 1973; Catchpole 1978; Catchpole and Leisler, 1986; Martin et al., 1996). In the latter case, the reaction to a heterospecific signal will often depend on local ecological condi* Corresponding author.
tions. For instance, Great Tits Parus major and Chaffinches Fringilla coelebs have been reported to actively respond to songs of the other species in an insular environment, whereas no such response was reported for their mainland counterparts exploiting a more heterogeneous environment (Reed, 1982). In the case of closely-related species that are active at the same season and in the same environment, reaction to heterospecific signals may correspond to competition (Orians and Willson, 1964; Rohwer, 1972; Catchpole, 1978; Rice,
0376-6357/99/$ - see front matter © 1999 Elsevier Science B.V. All rights reserved. PII: S 0 3 7 6 - 6 3 5 7 ( 9 9 ) 0 0 0 2 9 - 7
152
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
1978; Leisler, 1986; Martin et al., 1996) or simply result from a lack of divergence in the communication system of both species (Murray, 1971, 1976, 1981). The second situation may happen when two species come into secondary contact after separation (Ferry and Deschaintre, 1974; Murray, 1976; Robbins et al., 1986). Hybrid zones are thus particularly interesting for the study of interspecific territoriality between closely related species because the existence of allopatric populations may provide a baseline from which to evaluate separately the relative influence of interspecific competition and relatedness. Most studies concern hybrid zones which are stable in place and time (Moore and Buchanan, 1985; Hewitt, 1988; Rising, 1996), whereas gradual shifts of hybrid zones remain rare and poorly documented (Barton and Hewitt, 1985; Gill, 1997). We studied reactions to congeneric vocal signals in two closely related passerine species, the Melodious warbler Hippolais polyglotta and the Icterine warbler H. icterina, for which species interspecific territoriality has been previously reported (Ferry and Deschaintre, 1974). Their parapatric breeding distributions overlap over 350 km width in Belgium, northern and eastern France and Switzerland (Cramp, 1992). During the last decades, H. polyglotta has expanded its range, while H. icterina has regressed over all the contact zone. This resulted in a shift northwards and eastwards in the position of the contact zone as the Melodious warbler progressively replaced its sibling species (Glutz Von Blotzheim and Bauer, 1991; Faivre, 1993). Evidence of introgression for morphological characters suggest that hybrids can backcross with at least one parental species (Faivre et al., 1999). In addition, mixed pairings have also been observed in sympatry (Faivre et al., 1999). These pairs tend to have a reduced breeding success compared with homospecific pairs (Faivre, unpublished results). In this context, a decrease in the male reaction to the congeneric song in sympatric populations of Hippolais warblers could be expected in both species. In the present study, we test the hypothesis of a character displacement. We compare males’ reactions to congeneric songs between allopatric and sympatric populations of Hippolais warblers.
We discuss the observed pattern in relation to competition and hybridization and propose that the demographic context and behavioural mechanisms, related to song learning and mate choice, are key factors of the evolution and maintenance of interspecific reaction
2. Methods
2.1. Populations sampled One allopatric population of Melodious warblers was studied near Tours (Central France) about 400 km away from the nearest Icterine warbler population (Yeatman-Berthelot and Jarry, 1994). One allopatric population of Icterine warblers was sampled near Lie`ge (Belgium), 50 km north of the contact zone. Sympatric sites were located in Burgundy and Franche-Comte´ (Eastern France) at the western border of the contact zone (Fig. 1). They are part of the oldest areas of sympatry and Icterine warblers are geographically relatively isolated from allopatric populations.
2.2. Playback experiment A tape recorder and a loudspeaker in a basket were hung onto one song post of the focal bird or inside the territory less than 5 m of a song post when hanging was not possible. Three min of silence preceded playback. The observer took place at 10–20 m of the loudspeaker during the first min. Each experiment was divided in three 4-min periods, each one containing 2 phases of 2 min length: a playback (ON) and a silent phase (OFF) (Fig. 2). During the first playback period, hereafter referred to as the control period, the recording of a phylogenetically unrelated species, the nightingale Luscinia megarhynchos was played and provided a baseline for each test. This species is widely sympatric with both Hippolais warblers but no evidence of systematic aggression has been reported (Cramp 1992, personal observation). During the second playback period, hereafter referred to as the test period, a sympatric or an
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
153
presentation of the periods because we intended to measure the reaction to congeneric song. Therefore, we needed a baseline, e.g. the playback of another species, to assess any change of activity. Playing specific song can alter the behaviour of birds over a long period. Broadcasting a stimulus from the same location a few minutes apart could still alter the reaction to that stimulus (Falls, 1992). Tests were carried out on 16 sympatric and 15 allopatric Melodious warblers. Six allopatric and ten sympatric Icterine warblers were tested. Each bird was tested only once. Experiments were performed between 4 and 11 A.M. (G.M.T.) during the breeding season, from 1 May to 13 June in 1996 and 1997.
2.3. Recording samples
Fig. 1. Breeding ranges and overlap zone of Melodious and Icterine warblers in western Europe. Dots indicate the location of study and recording sites.
Fig. 2. Playback design used in the experiment. The vocal activity is recorded during three 4-min periods ( ). Songs are played during the first 2 min of each period. Inst., installation 3-min period after placing the loudspeaker. ‘ON’ indicates that the loudspeaker is playing a recording. ‘OFF’ indicates that no song is broadcast. See Section 2 for the description of each period.
allopatric recording of the congeneric species was played. The recording type was alternated between birds. A specific recording of the sampled population was broadcast during the third period referred to as the specific period. Each experiment lasted 15 min. We did not balance the order of
One recording of Nightingale provided the control signal. Its potency was indirectly assessed as in many trials Nightingales approached and sang after its broadcasting. For each species, ten congeneric recordings of 2 min length were chosen. Five sympatric recordings came from our study sites and five allopatric recordings came from distant locations of the distribution areas (Fig. 1). Two birds recorded in the population provided the specific controls. All the signals were digitized using SoundEdit 16 software on a Macintosh computer. The sampling frequency was 22050 Hz and the amplitude resolution was 8 bits. All the recordings were broadcast without any cutting or rearrangement but every gap between the songs of the recordings was replaced by a low frequency noise (below 500 Hz) that mimicked the natural noise and suppressed the songs of other species on the tapes. The synthetic noise was also emitted during the silent phases. The whole sequence of 15 min was recorded with a numeric tape recorder Sony TCD D7 and was broadcast with an amplified speaker Sony SRS-68.
2.4. Measure of the beha6ioural response Behavioural responses were assessed by monitoring the vocal activity. Preliminary tests showed that specific songs induced an increase in song rate (J. Secondi, unpublished data). Approach can
154
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
be elicited (Ferry and Deschaintre, 1974) but it appears unreliable for a standardized protocol. In most cases, the distance to the speaker cannot be measured accurately because birds are often hidden in the vegetation (personal observation). Thus, we measured the vocal activity that we defined as the amount of time spent singing during each period. Occasionally, the tape masked the songster so that the vocal activity was not accurately recorded. We discarded these trials from our sample for Melodious warblers. Thus, the vocal activity is given period by period. Because of the small sample in allopatry, we could not discard trials for Icterine warblers and measured the responses using the silent phases only.
2.4.1. Reaction to congeneric song The reaction to congeneric song was assessed by comparing the vocal activity during control and test periods. We also compared control and specific control periods so that we could check that the territorial reaction was released. Finally, we compared the relative potency of congeneric signals and specific signals. However, the measure of the reaction to the specific recording is not completely accurate since the congeneric recording could have altered the reaction to the specific recordings. In each case, sympatric and allopatric populations were analyzed separately using Wilcoxon signed-ranked test (Siegel and Castellan, 1988). Because variables were used in more than one test, significance thresholds were corrected using Bonferroni method (Sokal and Rohlf, 1995). 2.4.2. Character displacement We tested the hypothesis of character displacement in a two-step analysis. For each species, we compared the vocal activity of the allopatric and the sympatric populations to ensure that the vocal activity was similar during the control period in both populations. We then computed the difference of vocal activity between test and control periods and compared the populations for this difference. Finally, we tested the effect of the congeneric recording origin, e.g. sympatry vs. allopatry, on the inten-
sity of the reaction. Mann–Whitney U-tests were used in these analyses. Sample sizes were not held constant between analyses because we discarded the individuals for which the variables could not be measured during one playback or silent phase.
3. Results
3.1. Reaction to congeneric song When comparing the control and the test period, we observed a significant increase of the vocal activity during the latter period in sympatry and allopatry for the Melodious warbler. The same trend was observed for Icterine warblers (Table 1). Actually, 6 out of 8 sympatric birds and five out of six allopatric birds increased their song rate during the congeneric period. Thus, each population exhibited a tendency to respond to the sibling species song. However, sample sizes were small for this species and the power of the tests was consequently reduced. It is likely that larger sample sizes would have yielded significant differences. Both Melodious warblers populations showed an increase of their vocal activity during the specific period relatively to the control period (Table 1). The vocal response was strong and the difference between the periods was highly significant. The same pattern was observed in sympatric Icterine warblers as all birds increased their song rate during the specific period whereas in allopatry, only three out of six birds showed a higher vocal activity. An increase of the vocal activity was also observed in both populations of Melodious warblers during the specific period relatively to the test period, whereas Icterine warblers showed no variation in vocal activity between these two periods (Table 1). The highest vocal activity was recorded during the specific period in Melodious warblers. So the response was graded in this species. In contrast, in Icterine warblers, the maximal activity has been reached since the test period, when broadcasting the congeneric recording.
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
155
Table 1 Means and standard deviations for the vocal activity during playback experiments in allopatric and sympatric populations of Hippolais warblersa Control period (1) (s)
Congeneric period (2) (s)
Specific period (3) (s)
Congeneric reaction (2)-(1) P
Specific reaction (3)-(1) P
Specificcongeneric (3)-(2) P
H. polyglotta Allopatry Sympatry
53.7 950.6 67.2 9 59.2
100.7942.4 107.89 56.6
131.79 40.2 133.49 56.5
0.012* (15) 0.001* (16)
B0.001* (15) B0.001* (16)
0.006* (15) 0.023* (16)
H. icterina Sympatry Allopatry
45.6 923.2 55.8 9 35.4
64.3925.0 68.2930.9
76.29 7.1 63.19 15.4
0.028 (10) (ns) 0.245 (6) (ns)
0.005* (10) 0.462 (6) (ns)
0.155 (9) (ns) 0.528 (6) (ns)
a The total vocal activity is measured for the whole 4-min periods in H. polyglotta and for the silent 2-min phases in H. icterina. Sample sizes are noted in parentheses. P-values are the results of Wilcoxon signed-rank tests for test vs. control period, specific control vs. specific periods and test vs. specific periods. Significance thresholds were corrected using Bonferroni method for the baseline.
3.2. Character displacement For both Hippolais warblers, the vocal activity during the baseline was similar in sympatry and in allopatry (Table 2). We could then compare the reactions to the congeneric song in allopatry and in sympatry. We found no significant difference between the populations (Table 2). Thus, there was no evidence for a weaker reaction to the congeneric song inside the overlap zone. Finally, we assessed the difference of reaction to sympatric and allopatric congeneric recordings. This analysis was carried out in Melodious warblers only because sample sizes were too small in icterine warblers. No significant difference was observed (Mann–Whitney: sympatry: n =16, U = 40.5, P = 0.254; allopatry: n =15, U = 32, P =0.643). Whatever the recording origin relatively to the contact zone, allopatric and sympatric individuals did not exhibit differential reaction.
4. Discussion Our study suggests the existence of a vocal reaction to the sibling species song in sympatric and allopatric populations of Hippolais warblers. The reaction was characterized by a significant increase of the vocal activity during the congeneric playback in Melodious warblers. The
same trend was also observed in Icterine warblers. Our results were congruent with an earlier study by Ferry and Deschaintre (1974) that reported a motor reaction. However, in this preliminary study the duration of playbacks was not standardized, thus hampering the comparison of the populations. In the present study, we could compare the reactions of allopatric and sympatric populations to assess the hypothesis of character displacement. Data showed no significant difference between populations in both Hippolais species. Thus, our data do not provide evidence of character displacement in the male reactions to the sibling species song. The intensity of the congeneric reaction could also vary because of character shift on signal. Thus, we tested if sympatric and allopatric songs elicited quantitatively different reactions. The comparison was available for Melodious warblers only but, here again, no significant difference was found. Melodious warblers did not react differently to allopatric and sympatric signals. Thus, even if variations existed between Icterine warbler recordings according to their origin, these differences were apparently not used by birds to adjust their behaviour. The Hippolais warblers hybrid zone provides conditions to study character displacement on communication systems. Song is an essential feature of territorial defence and very likely of mate attraction (Secondi, unpublished data). A shift in
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
156
Table 2 Comparison of the vocal activity during the control period (baseline) and comparison of the reaction to the congeneric song between sympatric and allopatric populations of Hippolais warblersa Allopatry (s)
Sympatry (s)
nallopatry
nsympatry
U
P
Baseline H. polyglotta H. icterina
53.7 55.8
67.2 45.6
15 6
16 10
133.5 40
0.509 ns 0.277 ns
Congeneric reaction H. polyglotta H. icterina
47.0 18.7
40.6 12.4
15 6
16 10
128 32.5
0.752 ns 0.786 ns
a The reaction to the congeneric song is measured as the difference of scores between the test and the control periods. Significance thresholds were corrected using Bonferroni method when comparing the baselines. Ns, non significant difference.
signal or in behavioural response to signal should be highly expected then but our data did not support this hypothesis. Instead, they suggested the maintenance of the reaction in Melodious and Icterine warblers in sympatry. However, one should be cautious in interpreting these results. Indeed, sample sizes in Icterine warblers are small, particularly for the allopatric population. It results that the power of the tests could be low. In this species, we are aware that the external validity of the experiment should have been improved by increasing sample sizes. However, this was not possible because of time and logistic constraints. Anyway, we feel relatively confident with our results because they are congruent with the strong motor response already described in sympatry by Ferry and Deschaintre (1974). Several hypotheses could account for the maintenance of the male reaction in sympatry. However, each species should be considered in a different demographic context. Colonization and migration rates could be higher in the expanding Melodious warbler than in the regressing Icterine warbler (but see Kirkpatrick and Barton, 1997). In the former species, sympatric populations could be diluted by constant immigration that would disrupt adaptations evolved in older resident populations. In addition, the slipping of the overlap zone could be too quick to observe character displacement. Icterine warbler populations could go extinct before adaptation occurs. Adding to this demographic background, other non-exclusive hypotheses can be proposed. Firstly, in sympatry, competition with other spe-
cies could increase the overlap in resource use for Hippolais warblers. This could promote interspecific territoriality (Cody, 1973) and the maintenance of the reaction to the congeneric song. Secondly, song learning and cultural transmission could hamper the divergence of populations, e.g. the loss of the reaction to the congeneric song in sympatry. Hippolais warblers are very similar morphologically (Cramp, 1992). This characteristics could favour heterospecific tutoring in syntopy, particularly in the less abundant species (Thielcke, 1972; Clausen and Toft, 1988). Moreover, learning to discriminate songs could also be a difficult task. Species recognition can use both acoustic and visual cues (Baker and Baker, 1990). However, Hippolais are virtually indistinguishable on the basis of plumage coloration (Jouard, 1935; Wallace, 1964). Thus, the association between song and species identity probably cannot rely on visual cues. Thirdly, an active female choice could also select for the maintenance of signal design. Given the close ancestry of both species, some choice criteria could be similar. Signal differentiation could be constrained and a certain level of heterospecific pairing could be maintained in sympatry if females would exhibit conservative preferences for song. In addition, in Hippolais warblers, hybrids seem viable and fertile as introgression of some morphological characters of Melodious warblers in Icterine warblers has been observed in sympatry (Faivre et al., 1999). However, one can reasonably think that hybridization costs may be too low to drive a reinforcement process on song (Liou and Price, 1994; Hostert, 1997).
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
Demographic, ecological, behavioural or explanations can explain the absence of character displacement in the contact zone. Knowledge of population dynamics is needed to fully understand the observed patterns. However, it appears that detailed data on song learning are important as well since epigenetic mechanisms seem to be able to maintain a high level of interspecific interaction. Finally, testing other sympatric populations would be most informative. Character displacement could have occurred in other zones of sympatry where different conditions could prevail. Age of the secondary contact, relative density of each species, gene flows from allopatric populations, ecological constraints related to the bird community are such sources of geographical variation in interspecific interactions. Their relative weight should vary between different hybrid zones. They can also explain the variations in the internal structure of a given hybrid zone.
Acknowledgements We are very grateful to Emile Clotuche and Jean-Paul Jacob for their kindness and help in Belgium. We are indebted to Karl-Heinz Frommolt, Jean-Claude Roche´ and Patrick Sellar for providing recordings of allopatric Icterine warblers. We thank very much Yann Doisneau, Franck Grossiord and Francis Raoul for their assistance in the field and Frank Cezilly for his comments and valuable improvements of the manuscript.
References Barton, N.H., Hewitt, G.M., 1985. Analysis of hybrid zones. Ann. Rev. Ecol. Syst. 16, 113–148. Barton, N.H., Hewitt, G.M., 1985. Analysis of hybrid zones. Ann. Rev. Ecol. Syst. 16, 113–148. Catchpole, C.K., 1978. Interspecific territorialism and competition Acrocephalus warblers as revealed by playback experiments in area of sympatry and allopatry. Anim. Behav. 26, 1072 – 1082. Catchpole, C.K., Leisler, B., 1986. Interspecific territorialism in Reed warblers: a local effect revealed by playback experiments. Anim. Behav. 34, 299–300.
157
Clausen, P., Toft, S., 1988. Mixed singers and imitation singers among short-toed treecreepers. Br. Birds 81, 496 – 503. Cody, M.L., 1973. Character convergence. Annu. Rev. Syst. Ecol. 4, 189 – 211. Cramp, S., 1992. Handbook of birds of Europe, the Middle East and North Africa, vol. 6. Oxford University Press, Oxford. Faivre, B., 1993. La pre´dation joue-t-elle un roˆle dans la re´gression de l’Hypolaı¨s icte´rine Hippolais icterina. Rev. Ecol. (Terre Vie) 48, 399 – 420. Faivre B., Secondi J., Ferry C., Chastragnat L. and Ce´zilly F., 1999. Morphological variation and the recent evolution of wing length in the Icterine warbler: a case of unidirectional introgression? J. Av. Biol., in press. Falls, J.B., 1992. Playback: a historical perspective. In Playback and studies of animal communication. Plenum Press, New York, pp. 11 – 34. Ferry, C., Deschaintre, A., 1974. Le chant, signal interspe´cifique chez Hippolais icterina et H. polyglotta. Alauda 17, 289 – 312. Gill, F.B., 1997. Local cytonuclear extinction in the Goldenwinged warbler. Evolution 51, 519 – 523. Glutz Von Blotzheim, U.S., Bauer, K.M., 1991. Handbuch der Vo¨gel Mitteleuropas. Aula-Verlag, Wiesbaden, pp. 565 – 625. Hewitt, G.M., 1988. Hybrid zones-natural laboratories for evolutionary studies. Tree 3, 1988. Hostert, E.E., 1997. Reinforcement: a new perspective on an old perspective. Evolution 51, 697 – 702. Hurd, C.R., 1996. Interspecific attraction to mobbing calls of Black-capped chickadees (Parus atricapillus). Behav. Ecol. Sociobiol. 38, 287 – 292. Jouard, H., 1935. Sur la distribution en France des deux espe`ces d’Hypolaı¨s, et sur quelques-uns des caracte`res propres a` les faire distinguer surement. Alauda 7, 85 – 99. Kirkpatrick, M., Barton, N.H., 1997. Evolution of a species’ range. Am. Nat. 150, 1 – 23. Leisler, B., 1986. Interspecific interactions among European marsh-nesting passerines. In: Ouellet, H. (Ed.), XIX Congressus internationalis ornithologici. Ottawa University Press, Ottawa, pp. 2635 – 2644. Liou, L.W., Price, T.D., 1994. Speciation by reinforcement of premating isolation. Evolution 48, 1451 – 1459. Martin, P.R., Fotheringham, J.R., Ratcliffe, L., Robertson, R.J., 1996. Response of American redstarts (Suborder Passeri ) and Least flycatcher (suborder Tyrannii ) to heterospecific playback: the role of song in aggressive interactions and interference competition. Behav. Ecol. Sociobiol. 39, 227 – 235. Moore, W.S., Buchanan, D.B., 1985. Stability of the Northern flicker hybrid zone in historical times: implications for adaptive speciation theory. Evolution 39, 135 – 151. Moynihan, M., 1968. Social mimicry; character convergence versus character displacement. Evolution 22, 315 – 331. Murray, B.G., 1976. A critique of interspecific territoriality and character convergence. Condor 78, 518 – 525.
158
J. Secondi et al. / Beha6ioural Processes 46 (1999) 151–158
Murray, B.G., 1981. The origins of adaptive interspecific territorialism. Biol. Rev. 56, 1–22. Murray, B.G.J., 1971. The ecological consequences of interspecific territorial behavior in birds. Ecology 52, 414–423. Orians, G.H., Willson, M.F., 1964. Interspecific territories of birds. Ecology 45, 736–745. Reed, T.M., 1982. Interspecific territoriality in the Chaffinch and Great Tit on islands and the mainland of Scotland: playback and removal experiments. Anim. Behav. 30, 171– 181. Rice, J.C., 1978. Behavioural interactions of interspecifically territorial vireos. I-Song discrimination and natural interactions. Anim. Behav. 26, 527–549. Rising, J.D., 1996. The stability of the Oriole hybrid zone in western Kansas. Condor 96, 658–663. Robbins, M.B., Braun, M.J., Tobey, E.A., 1986. Morphological and vocal variation across a contact zone between the
chickadees Parus atricapillus and P. carolinensis. Auk 103, 655 – 666. Rohwer, S.A., 1972. Significance of sympatry to behaviour and evolution of Great plains meadowlarks. Evolution 27, 44 – 57. Siegel, S., Castellan, N.J., 1988. Non parametric statistics for the behavioral sciences. MacGraw-Hill, New York, p. 399. Sokal, R.R., Rohlf, F.J., 1995. Biometry. Freeman and Co, New York, p. 887. Thielcke, G., 1972. Waldbaumla¨ufer (Certhia familiaris) ahmen artfremdes signal nach und reagieren darauf. J. Orn. 113, 287 – 296. Wallace, D.I.M., 1964. Field identification of Hippolais warblers. Br. Birds 57, 282 – 301. Yeatman-Berthelot, D., Jarry, G., 1994. Nouvel atlas des oiseaux nicheurs de France 1985-1989. Socie´te´ Ornithologique de France, Paris, p. 775.
.