Folia Zoologia 2003-03_str 275

Folia Zool. – 52(3): 275–286 (2003)
Song repertoire and microgeographic variation in song types
distribution in the corn bunting Miliaria calandra from Poland
Tomasz S. OSIEJUK1 and Katarzyna RATY¡SKA2
Department of Animal Morphology, Institute of Environmental Biology, Adam Mickiewicz
University, 28 Czerwca 1956/198, 61-485 Poznaƒ, Poland; 1e-mail: [email protected], 2e-mail:
[email protected]
Received 20 June 2002; Accepted 28 May 2003
A b s t r a c t . Corn buntings in the Wielkopolska region (W Poland) show a clear local dialect
pattern of microgeographic song variation only in relatively dense and stable populations, which
inhabited typical farmland landscape. In less preferred habitats, where males were much more
dispersed, or in sites that where colonized recently, we found no such a pattern of song type
sharing. The between-individual song type variation was higher in such sites and males from
such locations did not sing any common dialect. The pattern of full and shortened song variant
usage was rather inconsistent. Shortened song variants were used more frequently during
counter-singing than solo-singing, but some song types were shortened more often than others
regardless of the context.
Key words: song variation, dialect, song variants, passerines
Introduction
Passerine songs undoubtedly play an important role in mate attraction and stimulation as well
as male-male competition (C a t c h p o l e & S l a t e r 1995). As a sexually selected trait,
songs vary substantially between species with respect to acoustic structure and temporal
pattern. Many hypotheses involving intra- and inter-sexual selection and several putative
constraints have been presented in an attempt to explain this variation (K r o o d s m a &
B y e r s 1991, P o d o s 1997, G i l & G a h r 2002). Comparisons within and between
species reveal that our knowledge is limited. In particular, influence of various factors on
evolutionary trajectories in song complexity require investigation (K r o o d s m a &
B y e r s 1991, K r o o d s m a 1996, V e h r e n c a m p 2000).
Members of the family Emberizidae have been subjects of numerous bioacoustic
investigations, which have employed a wide range of methods, from simple observations
(A n d r e w 1987, M ø l l e r 1983) to comparative studies (C a t c h p o l e &
M c G r e g o r 1985) and advanced playback experiments (S t o d d a r d et al. 1991,
B e e c h e r et al. 2000). The corn bunting M. calandra (L., 1758), the only representative
of the genus Miliaria possesses many similarities to its closest relatives (i.e. Emberiza spp.)
but diverges from them in some traits, such as sexual dimorphism, mating system and song
complexity (C a t c h p o l e & M c G r e g o r 1985, G r a p u t t o et al. 2001). The corn
bunting thus offer a unique opportunity to compare relationships between song and other
traits within the bunting family. The most characteristic features of the corn bunting are: the
polygynous mating system and sexual dimorphism expressed only in size (males are ca. 8%
larger than females). The majority of well-studied Emberiza spp., including yellowhammer
E. citrinella, cirl bunting E. cirlus, ortolan bunting E. hortulana and reed bunting
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E. schoeniclus, are monogamous (at least socially) and have more or less distinct plumage
sexual dimorphism (C a t c h p o l e & M c G r e g o r 1985, C r a m p & P e r r i n s
1994). The corn bunting seems to be clearly different from its relatives also in terms of
song. Admittedly, the corn bunting is also a typical discontinuous singer with a small song
repertoire (typically 2–3 song types), like many other buntings, but it is characterized by a
mosaic pattern of geographical variation, reflected in the formation of so-called “local
dialects”. In such a pattern each male within a local dialect population sings only several
song types characteristic of the population. Very few males sing song types of two dialects.
Except for those unusual individuals, all song types within a local population of the corn
bunting are shared (M c G r e g o r 1980, 1986, H o l l a n d et al. 1996). By contrast, other
Emberiza buntings typically share only some song types within a local population
(C a t c h p o l e & M c G r e g o r 1985, O s i e j u k et al. 2003). Unfortunately, no study
has provided an unambiguous answer to the question of whether local dialects are functional
(C a t c h p o l e & S l a t e r 1995). Local dialects sometimes persist over a decade, but the
mechanism of their maintenance is also unknown (T r a i n e r 1983, C a t c h p o l e &
S l a t e r 1995, H o l l a n d et al. 1996). In the case of the corn bunting, C z i k e l i (1982)
suggested that usage of different song types is density-dependent and related to habitats
occupied by the birds. However, there are no direct proofs of such a mechanism working
and there are some disagreements between C z i k e l i (1982) and other authors in
understanding the concept of song type and song dialect in the corn bunting (C r a m p &
P e r r i n s 1994).
The main aims of this study were (1) to describe song variation of the corn bunting from
Poland (no other data on this subject are available from this part of Europe), (2) compare the
pattern of microgeographical song types distribution between local populations of different
density, and (3) compare these data with other populations studied earlier in Europe.
Material and Methods
Study area and population
The study was carried out in three open areas located south of the city of Poznaƒ – in the
Wielkopolska National Park (Plot A) and its vicinity (Plots B and C) - (W Poland, 52°17’N,
16°56E’, Fig. 1). The study area is typical for this region of Poland, dominated by farmland
with a mosaic of fields, meadows, rough ground and wasteland. Some parts of Plot A are
overgrown with young oak (Quercus sp.), beech (Fagus silvatica) and birch (Betula sp.) trees
(< 10 years, 1-3 m high). The area between plots is generally unsuitable for corn buntings
(woodlands, wetlands) or for recordings (fields along a major road). Territories of corn
buntings are often placed linearly and at the geographical scale chosen for the study birds
generally tend to occur in clusters. Therefore, the density estimations for study plots (A - 3
males ⋅ 10 km-2, B - 6 males ⋅ 10 km-2, C - 11 males ⋅ 10 km-2) are low and did not reflect real
differences in distribution. These values much more depend on the size of the study area and
how many aggregations were found within it. So we assigned males to one of two simple
categories: (1) those with ≤ 1 neighbour, or (2) those with ≥ 2 neighbours within hearing
range. Base on this assumption, we can indicate one high density population on Plot A, two
on Plot B and one on Plot C (Fig. 1). There was also one crucial difference between study
plots. Plot A was know to be relatively unsuitable for corn bunting, which generally avoid
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Fig. 1. Map of the study area, showing Plots A, B, C and location of male corn bunting , Wielkopolska Region,
Poland. Black arrows indicate area of high corn bunting density. A two examples of low and high density area are
enlarged for detailed comparison of song types distribution.
forest vicinity (K u ê n i a k 2000). Detailed census in the entire Wielkopolska NP in 1992
revealed occurrence of only five males, but subsequently the number increased to 16 in 1995
(B e d n o r z 1997). Birds from the only high density group on Plot A inhabited an area,
which was overgrown by small trees and became suitable for them a few years ago (area
accessible since 1991). More than five males was observed here firstly in 2000. On the other
hand, local populations on Plot B and C were connected with stable agricultural or wasteland
habitat, which remained unchanged for at least 20 years. These population were known to be
rich and stable at least since 1996, when we started recording of other buntings in this area
(O s i e j u k unpublished).
Basic methods
The study was conducted between March and June 2001. Birds were recorded in the morning
(between 0500 and 1100) using a HHB PDR 1000 Professional DAT recorder with a Telinga
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V Pro Science parabola, and a SONY TCD-D8 recorder with a Sennheiser ME 67 shotgun
microphone. All recorded males were positioned on a map with the use of Garmin 12CX GPS
with at least ± 10 m accuracy. We estimate that we recorded over 90% of males present in the
field. For identification we also used recordings from playback experiments, which were
conducted simultaneously and will be a subject of another paper. In sites of higher density of
males, neighbours were recorded simultaneously by two observers, which also ensured that
identification of different males was unequivocal. Although the birds were not marked
individually, it was usually easy to identify males because each had a few permanent song
posts within the territory.
Sonogram analysis and bioacoustic terminology used
All recordings were digitally transferred from the above-mentioned HHB DAT recorder via
a SPDIF cable to a PC workstation with SoundBlaster Live! 5.1 (full version) using 48 kHz
/ 16 bit sampling and analysed using Avisoft SASLab Pro 3.9 software (S p e c h t 2002). All
sonogram measurements were calculated using the following settings of SASLab: 1024 FFTlength, Frame [%] = 25, Window = Hamming and Temporal Overlap = 87.5%. This gave
244 Hz bandwidth with 42 Hz frequency and 2.9 ms time resolution.
We used the same terminology as in previous studies of corn bunting vocalisation and
tried to identify each strophe according to a level of its completeness (henceforth called
variant), song type and finally a dialect (e.g. M c G r e g o r 1980, H o l l a n d et al. 1996
or L a t r u f f e et al. 2000). First, regardless of belonging to a particular song type and
dialect, each song represented a full or incomplete strophe. Detailed comparison of
sonograms revealed that predominantly males shorten strophes in fixed positions, which
enabled categorization into different song lengths variants: (a) full song phrase, (b) song
phrase lacking a portion of the final part, (c) song phrase lacking the final part and a portion
of the middle part, and (d) only the initial part of song phrase (Fig. 2). Second, each male
had a finite repertoire of strophes similar in structure, which were called song types (Fig. 3).
Third, we hypothesized that neighbouring males (within so called local dialect) would share
the same song repertoire types and that in their song types the back part of a strophe-end
would be similar (M c G r e g o r 1980, M c G r e g o r & T h o m p s o n 1988,
H o l l a n d et al. 1996). Song types that shared the same strophe end were assigned to the
same dialect (Fig. 3). However, many song types identified, even within a repertoire of
particular male, did not share any part of a strophe. Therefore, we were unable to assign
such a song types to any dialect. Different song type strophes (regardless of their
completeness) were named with a capital letter (e.g. A, B, etc.) or letters (AA, AB, AC, etc.).
If two or more song types shared strophe ends, their were designated as belonging to the
same dialect named by Arabic numerals (1, 2 and so on).
The sonograms were categorized through a three-step process. First, the second author
assigned song strophes to different types and variants within each type by visual inspection.
At this stage, each new type and variant for each male was printed and described. In the
second step, the first author checked the coherence of categorization at random examples of
each song category for each male. In cases of any doubt, more examples where compared
visually and with respect to the measured parameters: frequency range, frequency of
maximal amplitude and cross-correlation coefficients. In the third step, song types sharing
strophe-ends were grouped into dialects.
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Fig. 2. Sonograms of examples of the four song variants (a, b, c, d) of song type A, in corn bunting of the
Wielkopolska Region, Poland. The following sonograms illustrate the method of distinguishing complete and
incomplete song versions.
We also tested geographical pattern of song type sharing. Within the studied group of 86
males we randomly generated 43 pairs and repeated such drawing 10 000 times (M a n l y
1991). Then we tested the relation between male to male distance and the probability that
randomly paired males had at least one common song type in their repertoires.
Results
A total of 145 recordings of 86 male corn buntings (Plot A – 15 males, Plot B – 49 males,
Plot C – 22 males) were made, containing 4,149 song phrases and last over 10 h. Most males
were recorded only once, but some males were recorded twice or more times, also in different
contexts (e.g. solo- or counter-singing).
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Repertoire composition
The visual inspection of sonograms enabled us to distinguish 32 song types. The most
common song types were: A (25 males; 29.1%), M (20 males; 23.3%), B (19 males; 22.1%),
I (19 males; 22.1%), H (18 males; 21.0%) and AC (13 males; 15.1%). The next 10 popular
song types were sung by 2 to 6 males (i.e. 2.3–7.0%) and the other 16 types were sung only
by single males from the studied population. Altogether we found 36 combinations of one or
more song types building individual repertoires. Only 4 of them were common: H + I (13
males), A + B (12 males), M (8 males) and M + AC (7 males), and another 4 occurred in
2-4 males: A (4 males), H (3 males), F + G and G (2 males). The remaining 28 repertoire
combinations were specific to a single male.
We were able to distinguish only four clear dialects: dialect 1 with five song types (A, B,
C, D, Q); dialect 2 with two song types (S, T), dialect 3 with two song types (M, AC) and
dialect 4 with two song types (H, I) (Fig. 3). In all cases, song types within dialect shared a
large portion of the-end strophe. All of the other 21 song types were much more different
from each other and did not share either of the initial or final parts of a strophe.
We also found three examples of evident mixing of song types within a repertoire. Male
23, which sang types B and C from dialect 1, occasionally (3 times per 92 strophes
Fig. 3. Sonograms of song types from dialects in corn bunting of the Wielkopolska Region, Poland: 1 (A, B), 2
(S, T), 3 (M, AC) and 4 (H, I). Joined rectangles indicate parts of song strophes, which are common for a particular
dialects. Sonograms of strophes F, N, O and Z are examples of song types, which were not find to share final part
with any other type. Sonograms marked as pla1 – pla4 are examples of plastic strophes sung successively by one
male early in the season.
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recorded) uttered phrases with mixed B–C initial part of song. Such mixed versions were
always preceded by song type B and followed by song type C. The second example, male
153, was similar. Only once in the 64 strophes recorded for this individual was a mixed D-A
song version recognized; thus still matched dialect 1 characteristics. In the third example,
male 137 mixed song phrases that did not belong to one dialect, i.e. AC and AI, and this
behaviour was sporadic (2 times per 130 strophes recorded).
Two males sang a number of variable strophes, which differed slightly in consecutive
performance (Fig. 3), in addition to songs that could be assigned to particular types.
However, in both cases the recordings were made rather early in the season and the reason
for this variation was probably an unfinished process of repertoire crystallization, rather
than exceptional repertoire size. Therefore, we did not analyse these recordings in the
context of repertoire size.
Repertoire size
Reliable data on individual repertoire size depends upon a sufficiently large sample of
recorded phrases with which to estimate full repertoire size. The situation of the corn bunting
is ambiguous, as we found that some males switched song types very rarely. In an extreme
example, a male switched to the second song type after 120 phrases in a bout. If we consider
only bouts of at least 50 song phrases, then the second song type appeared on average (± SE)
after 24 ± 3.7 phrases (min-max: 2–121, n = 37). The third type appeared after 25 ± 5.5
phrases (min-max: 4–45, n = 8) and the fourth type after 55 ± 13.0 phrases (min-max: 39–81,
n = 3). As we had recordings varying from 1 to 200 phrases in a bout, the possibility of
underestimating repertoire size for some males was high. Therefore, we present data on
repertoire size just as they are (Table 1), and note that the proportion of males having more
than one song type in their repertoire is probably higher. On the other hand, there is no doubt
that repertoires composed of two song types predominated in the studied population.
Table 1. Song type repertoire size of corn bunting males from Wielkopolska. (*Including one male with two
typical song types and one mixed song type and one male with two typical song types and several plastic song
phrases; **Including two males singing three typical song types and one mixed song type; ***Including one
individual singing 4 typical song types and several plastic song phrases).
Repertoire size
1
2
3
4
Total
n
%
24
48*
10**
4***
27.9
55.8
11.6
14.7
86
100.0
Microgeographical distribution of song types and dialects
The distribution of males in the study area was not even (Fig. 1). In some locations, several
males had territories close to each other, but in other locations territories were separated by
hundreds of meters. We also found some males that were acoustically isolated from other
individuals. The large gaps between aggregations of males are natural to a large extent,
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because the gaps are dominated by forest stands, wetlands or urban areas, which are
unsuitable for the corn bunting. On the other hand, even in some seemingly suitable habitats
we found no singing males. In places of highest male density, we found a high withinpopulation homogeneity of repertoires.
In Plot C, all males sang one or both song types from dialect 3 (i.e. M and AC) We found
only one male singing song type M outside this area (ca. 10 km away). Song type AC was
exclusive to this population (Fig. 1). In Plot B, we found two high-density populations
separated by a distance of a few kilometers. In the northern plot, we found only males
singing song types from dialect 4 (H, I), whereas the southern plot was dominated by males
singing song types A and B from dialect 1. Along the road linking the two plots, we found
males inhabiting roadside fields and rough lands but in a much lower density; this
distribution resembled the shape of hourglass, with a few linearly distributed males linking
the two plots. In the southern plot, we found a few males singing the northern dialect as well
as males singing songs from both the northern and the southern dialect.
A completely different situation was observed in areas where territories were distributed
in small groups of one or a few males (northern part of Plot A and the southern part of Plot
B). In such cases, the repertoire of the population was much more variable, but still
neighbouring males shared some song types (Fig. 1). Males did not exhibit local dialect
pattern on relatively recently inhabited area in SW part of the Plot A, where birds were local
density was at similar level to that of Plots B and C.
This distribution of song types reflects to some extent the mosaic pattern of local
dialects. The randomization procedure showed that the probability of sharing song types
decreases with growing distance between males (Fig. 4). However, boundaries between
males singing different dialects were not always sharp.
Fig. 4. Probability (mean ± SE) of sharing at least one song type (P) for randomly chosen pairs of male corn
bunting in the Wielkopolska Region, Poland. The procedure of choosing 43 pairs was repeated 10 000 times.
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Song versions
Most males sang a few versions of each song type from their own repertoires, but full and
slightly shortened versions predominated (Table 2). Males sang shorter versions more
frequently when counter-singing (31.9% of strophes) than when singing solo (25.6%). To
avoid pseudo-replication, we randomly chosen one recording per male. The differences in
proportion of shortened strophes sung during solo and counter-singing context were not
significant (Mann-Whitney U-test, Z = -0.043, n = 86, P = 0.966). We also tested differences
in proportion of singing incomplete strophes sung by the same male recorded during solo
(median = 0.17, 95% CI = 0.02 – 0.53) and counter-singing (median = 0.33, 95% CI = 0.09
– 0.75) context (Wilcoxon matched pairs test Z = -1.572, n = 8, P = 0.156). The last test
indicate that males may shorten song strophes in aggressive context but we had to small
sample size of “paired” recordings to reach significance level. The last method of testing
seems to be the most valuable as it eliminates an influence of between males differences in
song type repertoires. On the other hand, our results indicate also that shortening of strophes
may be connected with a character of a particular song type. Among most popular song types
(i.e. A, B, H, I, M and AC) for which we have a representative number of recordings (i.e. both
recordings of different males and in different context), all types except AC where shortened
in ca. 30% of cases. Song type AC was shortened in about 75% of all recorded performances
and simultaneously had one of the longest complete variant, lasting over 3 seconds. We also
found that there was a general positive relationship between strophe duration (complete song)
and the frequency of shortening in particular song types (r = 0.49, n = 15, P = 0.066; for the
most common 15 song types).
Table 2. Length (sec) and frequency singing complete (a) and incomplete (b-d) variants of song strophes in corn
bunting from Wielkopolska Region, Poland.
Variant
Mean
SE
n
%
a
b
c
d
2.02
1.73
1.47
0.61
0.004
0.006
0.012
0.055
2884
953
301
11
69.5
23.0
7.2
0.3
Total
1.91
0.004
4149
100
Discussion
Song type repertoire and local dialects
If we consider only areas with high density of corn buntings, then the pattern of song type
variation and the system of local dialects found in Wielkopolska corresponds in general with
results obtained in Britain (M c G r e g o r 1980,1986, H o l l a n d et al. 1996,
M c G r e g o r et al. 1997). However, when all studied sites in Wielkopolska are considered,
song variation is higher in Poland than in the UK (M c G r e g o r 1980, 1986, M c G r e g o r
et al. 1988). First, the UK populations studied by those authors were dominated by males
singing exactly the same number and combination of song types, with the rare exception of
mixed dialect singers. Although our study area was also dominated by males with 2 song
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types in their repertoire, over 16% of individuals had 3 or 4 song types. Furthermore, many
males inhabiting less preferred sites sang strophes typical for more than one dialect, or song
types, which did not share final parts (i.e. could not be assigned to the same dialect).The term
local song dialects is typically used to refer to clear microgeographic song variation with
a mosaic of different dialects occurring within the species’ dispersal capacities
(M c G r e g o r 1980). Our findings and those of some earlier studies indicate that local
dialects may have slightly different character if viewed from a larger geographical
perspective. For example in Portugal, song types were found to be restricted to sub-groups of
males within local dialect rather than all males singing all song types as in Britain
(L a t r u f f e et al. 2000). Whereas no local dialects have been reported for Azerbaydzhan
(S u l t a n o v & G u m b a t o v a 1989). The local dialect pattern also seems to be
a density-dependent phenomenon, in which formation and maintenance depend on habitat
changes, duration and stability of local population. In Poland, clear local dialects were typical
only for three high-density populations inhabiting Plots B and C (Fig. 1). Outside these highdensity areas, the pattern of song type distribution was much more random, and neighbouring
males often did not share any song type. We also found that borders between dialects were
not sharp under some conditions. For example, males were observed singing songs typical for
one dialect in an area dominated by another dialect. Moreover, some males had song types of
different dialects in their repertoires or they even mixed song types from two dialects in one
song phrase. M c G r e g o r & T h o m p s o n (1988) reported similar results. Similar to
H o l l a n d et al. (1996), we found males singing a song characteristic of a dialect
population several km away from the centre of that population, which indicates that birds can
disperse to recolonise.
Furthermore, in this study we found an evident example of a disturbance of a local
dialect pattern and this disturbance was found on less preferred or relatively new sites
(B e d n o r z 1997, own unpubl. data). Thus, it might be an effect of, for example, offspring
overproduction, increased winter survival, or other reasons that caused some males to fail to
settle within the local dialect area. Such males try to recolonise or colonise less suitable
areas, which is manifested in a higher song variation in such areas (multiple founder effect,
see H o l l a n d et al. 1996). Formation of a new local dialect in such less suitable areas is
rather unlikely. First, corn bunting males in less suitable areas have larger territories, often
separated by unoccupied areas (C r a m p & P e r r i n s 1994, this paper), which due to
reduced social interaction lower the chance of creating a common dialect. Second, in corn
buntings, females tend to be mated to males singing the same local dialect as their father
(M c G r e g o r et al. 1997), which should acts as a stabilizing factor for the existing local
dialect population and at the same time negatively affects mating success on recolonised
areas outside (see M c G r e g o r & T h o m p s o n 1988, H o l l a n d et al. 1996).
Song variants
The usage of full and shortened song versions gives ambiguous results. Generally, males sang
shorter versions during counter-singing, but some song types were shortened more frequently
regardless of the context. C o n s t a b l e (1989) and S h e p h e r d (1992) (both after
C r a m p & P e r r i n s 1994) showed similar results, namely some song types in populations
studied by them were more likely to be sung as incomplete versions. S h e p h e r d (1992)
found that mated males sang more incomplete phrases of one song type from their two-type
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repertoire. The pattern found in Wielkopolska indicates that longer complete versions of a
song type are more likely to be abbreviated during song performance. It is difficult to
determine now whether shortening songs should be considered as an independent level of
within-song type variation, which may serve as, for example, an aggressive signal. A few
other explanations are still possible, e.g. variant switching might be a signal of
submissiveness, tendency to shortening may be culturally transmitted or even represent only
a production error, and should be tested experimentally (S e a r c y & N o w i c k i 1999,
S e a r c y et al. 2000).
Acknowledgements
We would like to thank J. P. C y g a n , A. S t a s z y ƒ s k a and J. M. R u t k o w s k a for their assistance in the
field and two anonymous referees for their valuable comments. The financial support was provided by the Polish
Committee for Scientific Research (KBN grant no. 6/P04C/038/17).
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Folia Zool. – 52(3): 287–298 (2003)
Spring migration of birds in relation to North Atlantic Oscillation
Zdenûk HUBÁLEK
Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Kvûtná 8, CZ-60365 Brno,
Czech Republic; e-mail: [email protected]
Received 21 August 2002; Accepted 22 May 2003
A b s t r a c t. Long-term spring phenological instants of 57 migratory bird species, i.e. arrival
in summer visitors and departure in winter visitors, were recorded in South Moravia (Czech
Republic) from 1952 through 2001 and evaluated for annual correspondence with the North
Atlantic Oscillation (NAO) weather system. The migration instants occurred significantly earlier
following positive winter/spring NAO index values (causing periods warmer than normal in
Europe) in a number of short-distance migrants with a European winter range (e.g., Alauda
arvensis, Columba palumbus, Corvus frugilegus, Motacilla alba, Phoenicurus ochruros,
Phylloscopus collybita, Serinus serinus, Sturnus vulgaris, Vanellus vanellus), whereas they did
not correlate with NAO in most long-distance migrants having a sub-Saharan winter range (e.g.,
Acrocephalus spp., Anthus trivialis, Apus apus, Cuculus canorus, Delichon urbica, Ficedula
albicollis, Hippolais icterina, Hirundo rustica, Jynx torquilla, Lanius collurio, Locustella spp.,
Muscicapa striata, Oriolus oriolus, Phylloscopus sibilatrix, Riparia riparia, Streptopelia turtur,
Sylvia spp.). The winter/spring (especially February and March) NAO conditions thus affect the
migration timing of short-distance migrants that winter in western or southern Europe, and could
explain their earlier than normal arrival that had been observed in Europe since the 1980s.
Key words: phenology, migration, weather, climate, temperature, NAO
Introduction
Recent climate warming is often regarded as the cause of the advanced spring arrival and
egg-laying dates of migratory birds that has been recorded in Europe and North America
since the 1980’s (e.g., F o r c h h a m m e r et al. 1998, W i n k l e r et al. 1999, B o t h &
V i s s e r 2001, S o k o l o v 2001, Z a l a k e v i c i u s & Z a l a k e v i c i u t e 2001). An
approach to test this hypothesis could be to evaluate whether the bird arrival data correlate
with some global measure of the weather/climate change. It has been demonstrated that El
Niƒo/Southern Oscillation (ENSO) system of ocean and atmosphere circulation in the
tropical Pacific affects the biota in the Americas, Australia, southern Asia and eastern Africa
either directly, through extreme precipitation or temperature, or indirectly, through ecosystem
changes (J a c o b s et al. 1994, K a r l et al. 1995, S i l l e t t et al. 2000, N o t t et al. 2002,
S t e n s e t h et al. 2002). Another major mode of the world climate variability is the North
Atlantic Oscillation (NAO) that profoundly affects the weather in continental Europe and
eastern North America (W a l l a c e & G u t z l e r 1981, B a r n s t o n & L i v e z e y 1987,
H u r r e l l 1995, Y o o & D ’ O d o r i c o 2002). The NAO system can be expressed
quantitatively using simple monthly, seasonal or annual indices that make a correlation
analysis possible and relatively easy. A number of papers have reported a correspondence
between the NAO fluctuation and plant phenology (P o s t & S t e n s e t h 1999,
C h m i e l e w s k i & R o t z e r 2001, P o s t et al. 2001), cephalopod migration (S i m s
et al. 2001), marine fish migration (A l h e i t & H a g e n 1997, R e i d et al. 2001),
287
mammalian population dynamics (P o s t & S t e n s e t h 1999, T k a d l e c 2000, P o s t
& F o r c h h a m m e r 2002, S t e n s e t h et al. 2002) or the avian breeding phenology and
productivity (F o r c h h a m m e r et al. 1998, P r z y b y l o et al. 2000, S a e t h e r et al.
2000, B o t h & V i s s e r 2001, S o k o l o v 2001, M ø l l e r 2002, N o t t et al. 2002,
S a n z 2002). However, the effect of NAO on the variability of bird migration instants in
Europe has not been studied until very recently (F o r c h h a m m e r et al. 2002, J o n z é n
et al. 2002, T r y j a n o w s k i et al. 2002, H ü p p o p & H ü p p o p 2003).
Material and Methods
Study area
Observations of birds were carried out in the Bfieclav area (48°40’–48°50’N,
16°30’–17°00’E) of South Moravia, Czech Republic. The relief is a mostly flat to slightly
undulating lowland (150 to 200 m a.s.l.), formed largely by accumulations of Pleistocene
loess and riverine sand deposits on Pliocene sedimentaries. The climate is relatively dry and
warm (annual precipitation 550 mm; annual mean air temperature 9.5 °C ( January -1.8 °C,
July 19.1 °C). There are agroecosystems (mostly arable fields), forest ecosystems (floodplain
forests, subxerophilic mixed deciduous oak stands), fishponds and big water reservoirs (Nové
Ml˘ny) in the wider area. Local community is composed of about 150 species of breeding
terrestrial and water birds (H á j e k 1992, · È a s t n ˘ et al. 1996, H u b á l e k 1997,
Z u n a - K r a t k y et al. 2000), and many migrants use the area for stopovers.
Bird phenology data
Longitudinal records of migratory birds were documented from 1969 through 2001. Spring
phenological instants recorded for each species involved the first occurrence (spring arrival)
in summer visitors, and the last occurrence (spring departure) in winter visitors. In addition
to the author’s observations, data of H á j e k (1992) were used for the years 1952 to 1969.
Total length of the period thus covered 50 years (1952–2001), and 57 common bird species
with a distinct pattern of spring phenology and a sufficient number of annual records were
selected for the correlation and regression analysis.
North Atlantic Oscillation data
Monthly (January; February; March; April) and seasonal (December to March, DJFM;
January to March, JFM; February to April, FMA) NAO indices for particular years 1952
through 2001 were extracted from the Internet at http://www.cgd.ucar.edu/~jhurrell/nao.html
(H u r r e l l 1995: NAOH) and http://www.cpc.ncep.noaa.gov/data/teledoc/nao.html
(B a r n s t o n & L i v e z e y 1987: NAOBL; W a l l a c e & G u t z l e r 1981: NAOEA, the
East Atlantic Pattern). The indices are based on normalized sea-level pressure differences
between two points or areas: (1) Ponta Delgada (Azores) and Stykkisholmur/Reykjavik
(Iceland) in the eastern sector of North Atlantic (NAOH); (2) the central latitudes
(35°N–40°N) and Greenland (NAOBL, reflecting thus spatially a more broad-scale
atmospheric pressure pattern in the western North Atlantic sector); and (3) NAOEA covers the
eastern North Atlantic sector. The positive NAO index generally shows that the atmospheric
pressure over the subtropical part of the North Atlantic is higher than normal while that over
288
the northern sector of the North Atlantic is lower than normal; this increased pressure
difference between the two sectors results in more and stronger storms crossing the Atlantic
Ocean and, in turn, causing warm and wet weather (especially in winter) in northern and
central Europe. The negative NAO index reflects an opposite pattern of height and pressure
anomalies over these sectors; this reduced pressure gradient results in fewer and weaker
storms crossing the Ocean, bringing cold air to northern (and central) Europe and moist, often
cold air into the Mediterranean (H u r r e l l 1995).
Statistical analysis
Calendar data of phenological instants were transformed into sequential numbers (e.g., 1 for
1st January, 32 for 1st February, 60 for 1st March, 91 for 1st April, 121 for 1st May 1; in leapyears, the sequential numbers were corrected by adding 1, starting from 1st March). Linear
correlation and regression models were then used to examine relationships between avian
spring phenological instants of particular bird species and the three NAO indices (NAOH,
NAOBL, NAOEA); Pearson’s correlation coefficient values were calculated and statistical test
done for all comparisons using SOLO 4.0 (BMDP Statistical Software, Los Angeles, CA).
Results
The late-winter and early-spring NAO weather system conditions affected significantly the
spring arrival (in summer visitors) or departure (in winter visitors) instants of some bird
species (Tables 1 and 2, Fig. 1). The species significantly inversely correlated with both the
‘JFM’ and ‘FMA’ seasonal NAO indices (i.e., the phenological instants occurred earlier
following the January-February-March and February-March-April seasonal air pressure
difference in the North Atlantic higher than normal) were Alauda arvensis, Anas crecca,
Aythya ferina, Bucephala clangula, Columba palumbus, Corvus frugilegus, Gallinago
gallinago, Mergus merganser, Motacilla alba, Phoenicurus ochruros, Phylloscopus collybita,
P. trochilus, Pyrrhula pyrrhula, Regulus regulus, Remiz pendulinus, Saxicola torquata,
Serinus serinus, Sterna hirundo, Sturnus vulgaris, Sylvia atricapilla, Tringa glareola, Turdus
philomelos and Vanellus vanellus. In some species, there was a single statistically significant
seasonal (either ‘JFM’ or ‘FMA’) NAO index (Acrocephalus scirpaceus, Anas querquedula,
Charadrius dubius, Hirundo rustica, Luscinia megarhynchos, Phylloscopus sibilatrix,
Streptopelia turtur, Sylvia communis, Tringa nebularia, T. totanus), whereas the remaining
species did not correlate with NAO at p<0.05: Acrocephalus arundinaceus, A. palustris,
A. schoenobaenus, Actitis hypoleucos, Anthus trivialis, Apus apus, Cuculus canorus,
Delichon urbica, Ficedula albicollis, Hippolais icterina, Jynx torquilla, Lanius collurio,
Locustella fluviatilis, L. luscinioides, L. naevia, Motacilla flava, Muscicapa striata,
Nycticorax nycticorax, Oriolus oriolus, Riparia riparia, Sylvia borin, S. curruca, S. nisoria
and Upupa epops.
The winter NAOH index (DJFM data, not given in Table 1) correlated significantly
(p<0.01) with phenological instants of Columba palumbus (-0.45), Mergus merganser
(-0.68), Phylloscopus collybita (-0.49), Sturnus vulgaris (-0.44), Tringa nebularia (-0.51)
and Vanellus vanellus (-0.40). According to monthly NAO indices (data not given in Table 1),
the number of avian species significantly (p<0.05) correlated in their phenology with
NAOH/NAOEA during January, February, March and April were 8/8, 12/12, 9/13 and 3/3,
respectively. Therefore, the NAO conditions especially in February and March have
289
Table 1. Spring phenology instants of 57 migratory bird species in South Moravia, 1952–2001, with the number
of years (n), the mean date of arrival or departure (mm/dd), principal wintering area (W), and Pearson’s correlation
coefficient value (r) between the avian phenology data and the mean seasonal indices (JFM, January to March;
FMA, February to April) of NAOH (H), NAOBL (BL) and NAOEA (EA); r values in bold are significant (p<0.05).
The bird species are arranged according to the mean arrival/departure date.
JFM
Bird species
n
Mean
date
Alauda arvensis A
Sturnus vulgaris A
Mergus merganser D
Turdus philomelos A
Corvus frugilegus D1/2
Motacilla alba A
Vanellus vanellus A
Aythya ferina A
Anas crecca A
Pyrrhula pyrrhula D
Bucephala clangula D
Columba palumbus A
Phylloscopus collybita A
Phoenicurus ochruros A
Saxicola torquata A
Regulus regulus D
Anas querquedula A
Gallinago gallinago A
Serinus serinus A
Remiz pendulinus A
Tringa totanus A
Sylvia atricapilla A
Phylloscopus trochilus A
Hirundo rustica A
Charadrius dubius A
Anthus trivialis A
Motacilla flava A
Jynx torquilla A
Nycticorax nycticorax A
Upupa epops A
Sylvia curruca A
Ficedula albicollis A
Acrocephalus schoenobaenus A
Actitis hypoleucos A
Delichon urbica A
Phylloscopus sibilatrix A
Cuculus canorus A
Luscinia megarhynchos A
Tringa nebularia A
Locustella luscinioides A
Streptopelia turtur A
Sylvia communis A
Riparia riparia A
Tringa glareola A
Sterna hirundo A
49
50
18
39
35
47
47
24
23
27
30
38
36
38
35
23
29
26
38
37
27
33
37
46
33
45
35
42
18
38
44
45
32
41
40
30
50
39
29
28
34
44
23
31
29
02/28
03/01
03/05
03/08
03/09
03/10
03/11
03/12
03/15
03/19
03/20
03/23
03/23
03/24
03/24
03/26
03/26
03/26
03/30
03/30
04/01
04/03
04/06
04/09
04/10
04/12
04/12
04/13
04/13
04/14
04/15
04/16
04/19
04/20
04/21
04/21
04/22
04/23
04/23
04/24
04/24
04/24
04/25
04/26
04/27
290
W
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
E
A
E
E
E
E
E
A
A
E
A
A
A
A
A
A
A
A
A
A
A
A
A
E
A
A
A
A
E
E
H
FMA
BL EA
H
-.47
-.43
-.47
-.33
-.62
-.42
-.39
-.50
-.52
-.39
-.52
-.38
-.40
-.54
-.02
-.26
-.36
-.29
-.23
-.58
-.33
-.53
-.44
-.03
-.07
+.13
-.12
-.12
-.22
-.31
-.14
-.03
-.07
-.13
+.06
-.36
-.14
+.02
-.56
-.06
-.39
-.12
-.28
-.21
-.01
-.35
-.53
-.59
-.06
-.55
-.31
-.42
-.42
-.42
-.18
-.26
-.58
-.54
-.34
-.47
-.49
-.19
-.43
-.34
-.49
-.24
-.10
-.20
-.20
-.15
+.11
-.19
-.15
-.21
-.13
-.05
+.15
-.17
-.08
+.29
+.14
-.09
-.26
-.27
-.30
-.08
-.26
+.08
-.45
-.53
-.16 -.09
-.51 -.44
-.61 -.60
+.06 +.25
-.52 -.41
-.11 -.08
-.34 -.28
-.46 -.45
-.42 -.51
-.14 -.15
-.10 -.20
-.55 -.55
-.60 -.52
-.38 -.33
-.46 -.40
-.44 -.55
-.28 -.30
-.56 -.48
-.44 -.36
-.38 -.26
-.46 -.39
-.12 -.15
-.18 -.19
-.17 -.26
-.48 -.38
+.18 +.08
-.30 -.15
-.08 -.16
-.34 -.23
-.21 -.12
-.12 -.03
+.10 +.17
-.26 -.13
-.00 -.02
+.24 +.23
+.00 -.06
-.13 -.21
-.36 -.31
-.45 -.42
-.16 -.23
-.22 -.25
-.33 -.33
-.13 +.13
-.39 -.33
-.43 -.52
BL EA
-.19
-.45
-.54
+.15
-.38
-.22
-.27
-.40
-.51
-.27
-.21
-.56
-.44
-.32
-.46
-.62
-.22
-.30
-.29
-.39
-.27
-.24
-.25
-.34
-.25
+.07
-.24
-.07
-.21
-.14
+.09
+.13
-.25
-.17
+.13
+.01
-.23
-.23
-.30
-.37
-.18
-.21
+.12
-.33
-.36
-.31
-.28
-.33
-.44
-.54
-.45
-.29
-.42
-.34
-.52
-.57
-.19
-.20
-.42
+.14
-.21
-.23
+.04
-.06
-.41
-.13
-.56
-.42
-.01
+.11
-.11
+.13
-.29
-.15
-.27
-.03
-.08
+.03
-.26
+.17
-.41
-.10
+.24
-.23
-.14
-.23
-.04
-.35
+.03
+.01
Table 1 – continued.
Sylvia borin A
Apus apus A
Acrocephalus arundinaceus A
Acrocephalus scirpaceus A
Locustella naevia A
Oriolus oriolus A
Hippolais icterina A
Locustella fluviatilis A
Muscicapa striata A
Sylvia nisoria A
Lanius collurio A
Acrocephalus palustris A
37
37
31
22
26
42
44
29
33
41
31
24
04/29
04/29
04/30
05/02
05/04
05/05
05/07
05/07
05/07
05/07
05/09
05/10
A
A
A
A
A
A
A
A
A
A
A
A
-.26
-.17
+.24
-.34
-.12
+.12
-.04
+.23
+.08
-.05
+.01
+.05
-.29
-.20
+.20
-.44
-.21
+.15
-.07
+.26
-.07
+.05
-.16
-.10
-.11
-.25
-.02
-.20
-.03
-.08
+.15
-.03
-.03
-.12
-.06
-.03
-.19
-.12
+.10
-.45
+.03
+.13
+.07
+.16
+.06
-.04
-.15
-.38
-.20
-.01
+.03
-.45
-.04
+.17
+.08
+.25
-.02
-.02
-.22
-.38
-.04
-.27
-.12
-.06
+.01
-.15
+.14
-.13
-.12
-.10
-.10
-.24
A
arrival of the first bird; D departure (the last observed bird in the spring); D1/2 departure of about half of the
wintering population. Principal wintering area (W): E, southern, western or central Europe, Mediterranean;
A, sub-Saharan Africa (or southwestern Asia).
Table 2. Regression (y = a + b.x) of 18 selected bird species on seasonal NAO index (see Fig. 1).
NAO index
Bird species
W
Type
Alauda arvensis
Sturnus vulgaris
Corvus frugilegus
Columba palumbus
Phoenicurus ochruros
Remiz pendulinus
Phylloscopus collybita
Phylloscopus sibilatrix
Sylvia atricapilla
Sylvia curruca
Charadrius dubius
Actitis hypoleucos
Hirundo rustica
Delichon urbica
Ficedula albicollis
Muscicapa striata
Hippolais icterina
Cuculus canorus
E
E
E
E
E
E
E
A
E
A
E
A
A
A
A
A
A
A
EA
H
H
H
EA
EA
H
H
EA
EA
H
H
EA
EA
H
H
H
H
Season
Regression
slope (b)
Intercept
(a)
R2
JFM
JFM
JFM
JFM
JFM
JFM
JFM
JFM
JFM
JFM
JFM
JFM
JFM
JFM
JFM
JFM
FMA
FMA
-8.5757***
-2.4273***
-1.4594**
-2.8513***
-5.7958***
-8.5900***
-2.2751***
+0.0008
-4.9794**
-1.1621
-2.4511**
-0.0652
-0.7587
+0.2758
+0.2707
+0.1748
+0.2002
-0.2552
58.71
60.26
69.87
83.05
83.44
89.97
84.23
111.31
93.40
105.36
100.26
110.08
99.47
111.03
105.87
127.38
127.19
112.19
0.216
0.261
0.275
0.308
0.306
0.338
0.356
0.000
0.282
0.018
0.231
0.000
0.006
0.001
0.011
0.006
0.004
0.009
W, principal wintering area. NAO index type: EA, NAOEA; H, NAOH ). Other abbrevations as for Table 1.
**, significant at p<0.01; ***, significant at p<0.001.
a profound effect on many early-spring migrants that usually winter in western or southern
Europe (Mediterranean). On the other hand, NAO does not seem to affect significantly the
timing of long-distance migrants arriving in Central Europe later, having wintering grounds
largely in sub-Saharan Africa. The seasonal (JFM) NAOH index explained on the average
18% (range 1–37%) variability in the phenological instants of the 25 short-distance
migrants, whereas only 4% (range, 0–13%) variability in the 32 long-distance migrants; the
difference between the two categories of migratory birds is highly significant (p<0.001) as
found with either t-test or nonparametric Mann-Whitney two-sample test.
291
ALA.ARV.
STU.VUL.
COR.FRU.
COL.PAL.
PHO.OCH.
REM.PEN.
Fig. 1. Scatter plot diagrams of relations between seasonal (JFM or FMA) NAO indices (NAOH or NAOEA) and spring
migration instants in 18 selected bird species (acronymes) in South Moravia, 1952–2001. Y-axis shows calendar data
of the phenological instants transformed into sequential numbers. For the regression analysis, see Table 2.
292
Fig. 1 – continued.
293
ACT.HYP.
CHA.DUB.
SYL.CUR.
SYL.ATR.
PHY.SIB.
PHY.COL.
Fig. 1 – continued.
294
HIR.RUS.
DEL.URB.
FIC.ALB.
MUS.STR.
HIP.ICT.
CUC.CAN.
Discussion
T r y j a n o w s k i & S p a r k s (2001) suggested that the relationship between arrival date
and population size should be considered in particular bird species: an increasing population
of Lanius collurio showed an advanced arrival in western Poland during 1983–2000. In the
present study, usually common and abundant avian species were taken into account whose
population sizes did not change considerably with time. The exceptions with the population
steadily low (l), on decline (d) or increasing (i) were Acrocephalus spp. (d), Anas spp. (d),
Ficedula albicollis (i), Gallinago gallinago (d), Lanius collurio (i), Motacilla flava (d),
Nycticorax nycticorax (l), Sylvia nisoria (l), Tringa nebularia (l), T. totanus (d), Upupa epops
(d) and Vanellus vanellus (d) (H á j e k 1992, · È a s t n ˘ et al. 1996, H u b á l e k 1997,
etc.). However, the results yielded in these species do not seem to contradict the general
conclusion that long-distance migrants are not affected significantly with the NAO activity,
in contrast to short-distance migratory species.
The positive NAO index values mean generally a stronger than usual subtropical high
pressure center and a deeper than usual subarctic atmospheric low. The increased pressure
difference causes intense atmospheric mass circulation resulting in more winter storms
crossing the Atlantic Ocean on a more northerly track, a milder winter and the whole year in
Europe, and specifically a warmer (but drier) than normal weather over central Europe
(H u r r e l l 1995). For the Czech Republic, a significant correlation was found between the
winter (DJFM) NAOH index and local winter air temperature (r = 0.78), but that between
this index and winter precipitation (r = -0.30) was insignificant (T k a d l e c 2000). The
milder temperatures associated with the positive NAO phase lead to higher invertebrate
loads in spring which might benefit short-distance migrants more than long-distance
migratory species (N o t t et al. 2002).
Three indices that characterize NAO were used in this study. Although NAOH and
NAOBL correlated well (r value for JFM season was 0.87), NAO BL seemed to be less
sensitive in the phenology of European migratory birds (in terms of the number of
significant correlations with avian species) than NAO H, probably because it describes
weather conditions in the western sector of the North Atlantic and may thus be more
relevant for the North American continent than for Europe. The eastern Atlantic measures
NAOH and NAOEA were comparable in their phenological sensitivity although they did not
correlate well (r value for JFM season was very low, 0.17): in contrast to NAOH, NAOEA
revealed a marked correspondence between NAO activity and phenological instants in
Alauda arvensis, Bucephala clangula, Motacilla alba, Pyrrhula pyrrhula, Sylvia atricapilla
and Turdus philomelos, whereas NAOH, contrary to NAOEA, yielded significant correlations
with phenological data of Charadrius dubius, Gallinago gallinago, Larus ridibundus,
Regulus regulus, Saxicola torquata, Serinus serinus, Sterna hirundo, Tringa totanus and T.
glareola. At present, it is difficult to evaluate which of the two indices is better for the use in
the European phenology; they might be used as complementary measures.
In an earlier study, a cluster analysis of temporal spring migration patterns of birds in
Moravia between 1881 and 1960 revealed several groups (called ‘migrons’) of co-related
avian species: the first (‘Mediterranean’) migron consisted almost exclusively of shortdistance migrants wintering in southern or western Europe (Alauda arvensis, Sturnus
vulgaris, Fringilla coelebs, Columba palumbus, Motacilla alba, Vanellus vanellus, Turdus
philomelos, Erithacus rubecula, Scolopax rusticola), whereas the remaining migrons had
been called ‘African’ in that they involved long-distance migrants Hirundo rustica, Jynx
295
torquilla, Delichon urbica, Cuculus canorus, Luscinia megarhynchos, Streptopelia turtur,
Apus apus, Oriolus oriolus and Coturnix coturnix, i.e. species having their winter quarters in
sub-Saharan Africa (H u b á l e k 1985). In the present study, the seasonal winter/spring
NAO index did not correlate significantly with the arrival of a vast majority of long-distance
migratory bird species wintering in tropical and southern Africa (only 2 of 32 those species
tested revealed significant both ‘JFM’ and ‘FMA’ seasonal measures). Timing of their
departure from the winter grounds must therefore be based on principles other than the
weather system fluctuation at northern latitudes. However, significant inverse relationship
was found between the arrival of nearly all (22) short-distance migrants wintering in
western and southern Europe (25 species tested) and the seasonal winter/spring NAO index,
indicating that a higher than normal air pressure difference over the North Atlantic during
the winter/spring (especially in February and March) determines an earlier than normal
arrival of these birds in Central Europe. This result is not in accord with a very recently
published study of F o r c h h a m m e r et al. (2002), who found no significant difference in
the effect of NAO on spring arrival between long-distance and short-distance migrants (but
only three species of each group were tested) breeding in Norway, although it corresponds
well with the results of N o t t et al. (2002).
Positive values of the winter NAO index prevailed in 11 out of 15 years between 1987
and 2001 (H u r r e l l 1995), as did the bird phenological data in South Moravia during the
same period: earlier than normal early-spring bird instants occurred in 12 out of 15 years,
whereas those markedly later than normal in one year only (H u b á l e k 1997, H u d e c et
al. 1999, unpublished data for 1998–2001). The present study revealed that the NAO
weather system affects spring phenological instants in a number of bird species and that this
effect could explain the earlier than normal arrival of common migratory species (e.g.,
Alauda arvensis, Sturnus vulgaris, Vanellus vanellus, Columba palumbus, Motacilla alba,
Phoenicurus ochruros, Phylloscopus collybita and Serinus serinus) that has been observed
in Central Europe since the 1980s. When we accept that the NAO system is an indicator (or
even the proximate causative mechanism) of the climate change, then the earlier than
normal spring arrival of migratory birds should be considered as both a result of, and
evidence for, the climate warming in the last two decades.
Acknowledgements
I am grateful to Emil T k a d l e c for advice about the NAO index, and to M. Philip N o t t for valuable suggestions
on the manuscript.
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Folia Zool. – 52(3): 299–308 (2003)
Postmating sexual selection in house sparrows: can females estimate
“good fathers” according to their early paternal effort?
Herbert HOI1*, Radovan VÁCLAV2 and Du‰ana SLOBODOVÁ3
1
Konrad Lorenz Institut für vergleichende Verhaltensforschung, Österreichische Akademie der
Wissenschaften, Savoyenstraße 1a, A-1160 Vienna, Austria; e-mail: [email protected]
2
Institute of Zoology, Slovak Academy of Sciences, Dúbravská cesta 9, SK-842 06 Bratislava, Slovakia;
e-mail: [email protected]
3
Department of Animal Physiology and Ethology, Comenius University, Mlynská dolina, SK-842 15
Bratislava, Slovakia
Received 30 September 2002; Accepted 6 March 2003
A b s t r a c t . Recently, several studies suggested that in species with biparental care, male
parental effort (for instance in terms of nest building) serves as a sexual signal to females. In this
study on free-living house sparrows Passer domesticus, we investigated how male contribution to
parental care varies between breeding stages and whether early parental care of a male reflects his
paternal effort in later stages. We found that nest building was performed predominantly by males.
However, hatching success was not related to male participation in nest building or early nest
guarding. The contribution of males to incubation and chick brooding was lower than in females.
Investment in chick feeding did not differ between partners, but varied considerably between
males. Only the male effort in chick feeding was related to the number of young at fledging age,
suggesting that male assistance is essential to maximise reproductive success in house sparrows.
Except for the positive correlation between male nest building and male incubation during egg
laying, we found no relationship between early (nest building and nest guarding) and later
paternal effort (late incubation, brooding and provisioning rates). Consequently, intensity of male
nest building and early nest guarding do not seem to be honest indicators of later paternal effort
in the house sparrow. Instead, we speculate that high early paternal effort might be a strategy of
some males to manipulate the reproductive effort of their partners.
Key words: paternal care, nest building, sexual selection, house sparrows, breeding success
Introduction
One important mechanism of sexual selection, female mate choice, operates through females
preferring males that display certain morphological and behavioural traits (Z a h a v i 1975,
W e s t - E b e r h a r d 1979, C a t c h p o l e 1980, H a m i l t o n & Z u k 1982, N u r &
H a s s o n 1984, R y a n et al. 1990). Females are supposed to benefit from their choice
indirectly by acquiring “good genes” for their offspring (Z a h a v i 1975, W e a t h e r h e a d
& R o b e r t s o n 1979, P o m i a n k o w s k i 1987, I w a s a et al. 1991), or directly by a
greater assistance of their mates in chick rearing or territory defence (T r i v e r s 1972,
B o r g i a 1979, B u r l e y 1981, K i r k p a t r i c k 1985, H o e z l e r 1989, P r i c e et al.
1993). However, sexual selection can operate also after mate choice (see S o l e r et al.
1998a,b). Hereby, some males can produce more or higher quality offspring as their mates
invest in reproduction differentially depending on male physical (e.g. B u r l e y 1988,
M ø l l e r 1994) or parental quality (G i b b o n s 1987, d e L o p e & M ø l l e r 1993).
The latter case should especially account for the species with biparental care, for which male
* Corresponding author
299
parental quality is often crucial to maximise female reproductive success (e.g. M o r e n o et
al. 1999, see M ø l l e r 2000). In order to stimulate their mates to a higher reproductive
effort, males should therefore try to advertise their ability and/or willingness to parental care.
Females should in turn pay attention to the reliability of such advertisements. In fact, some
studies showed that male song display can be an indicator about his parental quality (e.g.
H o i - L e i t n e r et al. 1995, W e l l i n g et al. 1997). Other studies recently demonstrated
that the number of advertised nests, nest size or male nest building activity in wrens
Troglodytes troglodytes, black wheatears Oenanthe leucura, barn swallows Hirundo rustica
and magpies Pica pica might represent a sexual signal involved in postmating sexual
selection (E v a n s & B u r n 1996, S o l e r et al. 1996, S o l e r et al. 1998a, S o l e r et
al. 2001). However, studies examining the reliability of early paternal advertisement and its
potential to manipulate female reproductive decisions are lacking.
The house sparrow Passer domesticus is a suitable species to study postmating sexual
selection with regard to paternal quality because: (i) there is no clear female preference for
males with larger sexual ornament, a melanin based throat patch (K i m b a l l 1996), (ii)
early reproductive decisions of females (date of egg laying, clutch size) were showed to be
related to early male parental effort (V á c l a v & H o i 2002), whereas (iii) chick feeding
as well as fledging success were reported to increase with size of male ornament (M ø l l e r
1988, V á c l a v & H o i 2002). In this study, we examined different male and female
parental activities, including nest building, nest guarding, chick brooding and chick feeding
during (i) pre-laying and laying period, (ii) incubation, (iii) chick brooding and (iv) chick
feeding periods. We wanted to answer the following questions:
(i) How does the contribution of male parental care vary between breeding stages?
(ii) How important is male parental care for hatching and fledging success?
(iii) Is early paternal effort a reliable predictor of male parental effort later on during the
breeding cycle?
Material and Methods
Study area and population
House sparrows were studied in a nest-box colony in the Schönbrunn Zoological Garden,
Vienna in 2001. During the breeding season, 72 of 84 nest boxes were occupied. Nest-boxes
were installed on the opposite walls of 7 barns. Egg laying started at the beginning of April.
From then the contents of all nest-boxes were inspected at least every third day throughout
the breeding season. We recorded the progress in clutch size, number of hatched and fledged
young. In the analyses, we use data collected from 31 different pairs. Only the data from first
breeding attempts for these pairs were used in our analyses, since the largest part of the nests
are constructed prior to the first breeding attempt and afterwards the nest volume changes
only slightly (see C r a m p 1994, R. V á c l a v , unpublished data). Furthermore, female
investment in parental care may later be affected by male performance in the whole first
breeding attempt as well as achieved breeding success. We did not succeed in collecting
sufficient data of nest building behaviour for six pairs; hence the sample size for the
corresponding analyses is only 25 pairs. Hatching success refers to the proportion of hatched
eggs relative to clutch size. Fledgling numbers were estimated according to the number of
chicks found in nest-boxes at the age of 13–15 days. Fledging success corresponds to the
proportion of fledglings relative to the number of hatched chicks.
300
Behaviour of house sparrows was monitored from around three weeks before the first
egg was laid until fledging of the last chick. The behavioural observations were carried out
from 7:00 to 12:00 noon. Throughout the breeding cycle, each pair was observed on average
for 4.5 hrs. The behaviour at each nesting site was recorded daily during 15 min protocols.
In order to avoid an influence of daytime on behaviour, nesting sites were visited following
a rotating scheme. We recorded: (i) nest guarding (time spent at or around the nest-box < 5
m), (ii) nest building (the number of arrivals with a nest material to the nest-box), (iii) time
at incubation (time spent in the nest-box > 1 min), (iv) chick brooding (time spent in the
nest-box after hatching > 1 min), and (v) the number of chick feeding visits. Since
behavioural protocols of the studied pairs covered variable periods of the breeding cycle, we
restricted our analyses to comparable time intervals of nest building, egg laying, incubation
and chick feeding phases (see below). Parental care was classified as early or late,
depending on whether it took place before or after clutch completion. The early parental
care corresponds to the pre-laying and laying period from 5 days prior to the first egg until
the last egg was laid (i.e., late nest building, and nest guarding and incubation during egg
laying). This is not only the period when the presumed fertile period of females occurs in
house sparrows (see M ø l l e r 1987, B i r k h e a d et al. 1994), but also the time when nest
building culminates (S u m m e r s - S m i t h 1963, see C r a m p 1994). Chick feeding was
restricted to the period of the first 10 days after hatching, i.e., approximately 70% of the
chick feeding period (see S u m m e r - S m i t h 1963).
Statistical analyses
Some parametric tests were used after normalising data by a log transformation. The
frequency of male chick feeding visits was related positively, though not significantly, to
brood size (R2 = 0.07, β = 0.27, n = 31, p = 0.14). Because the result would become
significant after removing an outlier, to control for brood size, when examining the effect of
male provisioning rates, we used residual values of male chick feeding. Relative to the
opposite sex or absolute values of parental care activities were used in analyses. To avoid
type-I errors in cases when the same variables would have to be examined more times, we
used multiple regression tests. For examination of the intensity of nest guarding of identical
birds during three breeding stages, we used repeated measures ANOVA. In order to minimise
confounding effects of multiple parental behaviours on the parameters of reproductive
success, we examined the effect of early paternal effort on hatching success and the effect of
later paternal effort on the number of fledglings and fledging success.
Results
Male contribution to parental care throughout the
breeding cycle
Examining male parental effort over the course of the breeding cycle, we found that male
share in parental care was highest during nest building (Fig. 1). In addition, this form of
paternal care varied most dramatically (range: 0–100%, SD = 30.36). Even so, male
contribution to nest building was significantly higher than that of their mates (Wilcoxon
matched pairs, Z = 2.93, n = 25, p = 0.003; Fig. 1). In contrast to nest building, males
contributed the least to incubation and chick brooding (Fig. 1). Again, between-male
301
variation of the parental contribution to these activities was considerable (incubation – range:
0–62.6%, SD = 18.7, n = 31; chick brooding – range: 0–72.5%, SD = 18.0, n = 31). The
average contribution to incubation and chick brooding was significantly lower in males than
females (contribution to incubation: paired t-test, t = -5.09, n = 31, p < 0.001; contribution to
chick brooding: t = -4.67, n = 31, p < 0.001; Fig. 1). In terms of chick feeding, however, male
contribution was in average as high as in females (chick feeding: paired t-test, t = -1.64, n =
31, p = 0.11). Male feeding contribution ranged from 14.7–93.3% (SD = 15.6, n = 31).
Fig. 1. Male (open bars) and female (filled bars) contributions to different categories of parental care (error bars
are SD). Two asterisks (**) indicate p < 0.01, three asterisks (***) p < 0.001.
Relationship between paternal care, female parental
effort and reproductive success
More intensive nest building and constructing bigger nests may decrease incubation or brooding
bouts and increase hatching success. However, incubation and brooding time of neither parent
seemed to be influenced by male nest building activity (male nest building vs. incubation
time of females: R2 = 0.04, β = -0.21, n = 25, p = 0.32, and males: R2 = 0.02, β = 0.13, n = 25,
p = 0.53;male nest building vs. brooding time of females: R2 = 0.08, β = 0.28, n = 25, p = 0.18
and males: R2 = 0.001, β = 0.04, n = 25, p = 0.87). Moreover, hatching success was also not
significantly related to male nest building activity (R2 = 0.05, β = 0.22, n = 25, p = 0.29). To
evaluate the effect of later paternal effort on reproductive success, stepwise multiple regression
analyses were performed with male and female brooding time and feeding frequencies as
independent variables and the number of fledglings as a dependent variable. Only residual male
feeding rates (see method) entered a stepwise regression model at the significance level α < 0.05
(R2 = 0.32, β = 0.57, n = 31, p < 0.001; Fig. 2). Likewise, variation in fledging success was also
explained only by residual male feeding of chicks (R2 = 0.30, β = 0.55, n = 31, p < 0.01).
302
Fig. 2. The relationship between residual male feeding of chicks and number of fledglings. Residual values
represent feeding rates after controlling for the confounding effect of brood size. Number of fledglings are
estimates based on the number of chicks in the nest-box at the age of 13-15 days.
Nest guarding, especially during pre-laying and laying period, made up a considerable
part of the daily time budgets of males and females (Fig. 3). A 2-way ANOVA revealed a
significant effect of the sex and the stage of breeding cycle on the time parents invested in
nest guarding (2-way repeated measures ANOVA: sex effect – F1,60 = 32.9, p < 0.001, period
effect – F2,120 = 77.3, p < 0.001, interaction – F2,120 = 3.0, p = 0.06; Fig. 3). Both sexes
invested in nest guarding most heavily in the onset of the breeding cycle, whereas the
activity decreased towards the end of breeding cycle. A high initial nest guarding may assure
a better protection of the clutch from intra- or inter-specific brood destruction. However, we
found that clutch size was not correlated with the time parents guarded their nests during the
period of egg laying (only female nest guarding entered a stepwise multiple regression: R2 =
0.04, β = 0.19, n = 31, p > 0.3). Similarly, nest guarding during incubation period was not
able to explain the number of hatchlings (only female nest guarding entered the regression
model: R2 = 0.10, β = 0.32, n = 31, p = 0.08), or hatching success (no sex entered the model).
Finally, nest guarding during the period of chick feeding could not explain the number of
young at fledging age or fledging success (no sex entered the models).
Does early male parental contribution reflect his
investment in later breeding stages?
We were unable to detect that the contribution to early male parental activities would have
explained the contribution of male parental care in later stages of the breeding cycle
(regressions between male contribution to nest building vs. (i) incubation: R2 = 0.02, β = 0.15,
303
Fig. 3. Time males (solid line) and females (broken line) spent at nest guarding throughout the three periods of
the breeding cycle (error bars are SD).
n = 25, p = 0.46, (ii) chick feeding: R2 = 0.03, β = 0.17, n = 25, p = 0.40, and (iii) chick
brooding: R2 = 0.001, β = -0.03, n = 25, p = 0.88). The early nest guarding likewise proved
to be a weak predictor of later paternal effort (early nest guarding vs. (i) incubation: R2 =
0.002, β = -0.04, n = 31, p = 0.83, (ii) chick feeding: R2 = 0.04, β = -0.21, n = 31, p = 0.26,
and (iii) chick brooding: R2 = 0.02, β = 0.12, n = 31, p = 0.50). However, after dividing
incubation into early (incubation of incomplete clutches) and late (incubation after clutch
Fig. 4. The relationship between male contribution to nest building and early incubation. Male contribution to nest
building and incubation refers to the relative activity of males to that of their partners. The early incubation
represents the period of time from onset to termination of egg-laying.
304
completions), we found that the male contribution to nest building, but not to early nest
guarding, significantly explained the variation of his contribution to early incubation (nest
building and early incubation: R2 = 0.21, β = 0.46, n = 25, p = 0.022; Fig. 4; early nest
guarding vs. early incubation: R2 = 0.001, n = 25, p = 0.87).
Discussion
Our results revealed variation in paternal care between individuals as well as between
breeding periods. We show that male parental share was highest during nest building,
decreased during incubation and increased again during chick feeding period. Only chick
provisioning turned out to be comparable between partners, whereas nest building was more
intense for males, and incubation and brooding for females. Provided that male parental care
in house sparrows is essential to maximise reproductive success, females may benefit from
correctly assessing male parental ability. Because we found variation of parental effort among
male house sparrows, females should invest in reproduction according to some male cues that
honestly indicate his condition and perhaps also his future parental effort. Although house
sparrows are distinctly sexually dimorphic in their plumage, female assessment of male
condition based on epidermal sexual characters such as plumage may not be accurate. This is
because plumage does not inform about the current male condition, but about the condition
during his previous moult (O w e n s & S h o r t 1995). That is why the size of sexual
ornaments of collared flycatchers Ficedula albicollis or house sparrows was suggested as
informing females mate’s about a male previous rather than future reproductive effort
(G u s t a f s s o n et al. 1995, G r i f f i t h 2000). Hence, in order to estimate male condition
and his paternal ability, females may pay attention to specific male activities happening prior
to pairing and/or copulations. In our study, the fact that male contribution to nest building was
highest of all parental activities suggests that this behaviour could be in the house sparrow a
candidate for sexual signal. Male nest building was indeed demonstrated to be involved in
sexual signalling in several bird species (G a r s o n 1980, M ø l l e r 1982, B o r g i a 1985,
E v a n s & B u r n 1996, S o l e r et al. 1998b), but also in invertebrates (e.g. B a c k w e l l
et al. 1995). For instance, the number of advertised nest cups, nest volume or intensity of nest
building were shown experimentally to affect mating success in wrens (E v a n s & B u r n
1996), laying date and clutch size in barn swallows (S o l e r et al. 1998a) and magpies
(S o l e r et al. 2001). Similarly, V á c l a v & H o i (2002), who studied the same house
sparrow population, found that females started to breed earlier and laid larger clutches when
mated with those males investing in early paternal care more heavily than other males. Larger
nests in penduline tits Remiz pendulinus provide a better insulation and increase hatching
success (G r u b b a u e r & H o i 1996). In collared flycatchers, the time of incubation bouts
shortens with increasing nest size, whereas hatching success is not compromised (M o r e n o
et al. 1991). However, we were unable to find any significant relationships between the
intensity of male nest building and hatching success or time at incubation. Because we did
not measure any physical parameters of the nest, we cannot rule out the possibility that
intensity of nest building during the observed period did not reflect, for example, a nest size.
However, R. V á c l a v (unpublished results) found for a Viennese population of house
sparrows a positive correlation between the intensity of early parental care and nest weight.
Overall, our results suggest that instead of constructing a well insulated nest to protect the
clutch and chicks from cold, exaggerated male nest building in the house sparrow may
305
represent a sexual display. Nest guarding may also increase reproductive success, because it
lowers the likelihood of egg or brood destruction (S u m m e r s - S m i t h 1963, V e i g a
1990, for house sparrows). Nevertheless, nest guarding that was maintained in our house
sparrows high until clutch completion did not explain the variation in clutch size.
Male assistance in parental care was lowest in terms of incubation and brooding. This
has likely to do with the fact that, as in many other passerines, male house sparrows have
lower capacity to incubate than females (S e l a n d e r & Y a n g 1966). Yet, we detected
that the intensity of male incubation of incomplete and complete clutches was not
consistently correlated with the intensity of nest building. The loss of the relationship
between male nest building and the incubation of complete clutches might be explained by a
reduction of the circulating testosterone of aggressive males as the fertile period of their
partners finished. This is a typical image for males in many species with biparental care
(W i n g f i e l d & M o o r e 1987, W i n g f i e l d et al. 1990). However, such a result
could also be a consequence of less aggressive males withdrawing to further advertise their
parental ability after clutch completion. The highest egg losses that were found in the nests
of males investing heaviest in the early forms of parental care (V á c l a v & H o i 2002)
could in reality be the consequence of such a reduction of paternal care. Importantly, we
found that the intensity of male nest building was not only unrelated to late incubation, but
also to male feeding visits. This finding is important because we have shown that male
parental assistance is critical during the period of chick feeding. Namely, as in several other
studies (e.g. B a r t & T o r n e s 1989, M a r k m a n et al. 1996, D i c k i n s o n &
W e a t h e r s 1999), we found that solely male provisioning was able to explain the
variation in fledgling numbers and fledging success. Similarly as for nest building, early
nest guarding was related neither to male incubation, nor to chick feeding. Moreover,
intensity of nest guarding itself was not consistent throughout the breeding cycle, declining
with time of the breeding cycle.
No matter how intensively they are displayed, male nest building and early nest guarding
do not always seem to reliably indicate later paternal effort, say during chick feeding. Some
other behaviours, such as courtship feeding in common terns Sterna hirundo, might serve as
more reliable signals of paternal quality (N i s b e t 1973). Nevertheless, as V á c l a v &
H o i (2002) reported, female house sparrows do allocate their reproductive effort in
relation to the intensity of early parental activity of their partners. Hence, males are
potentially able to manipulate (stimulate) females to start breeding earlier and lay bigger
clutches by displaying a high initial paternal effort or, alternatively, just by providing them a
complete nest earlier than other males. The latter option is however less likely, because
females were often found to lay eggs into almost empty nest-boxes (pers. obs.). As a result
of elevated investment in early parental activities, males can benefit through stimulating
females to lay larger clutches and potentially produce more offspring. However, as such males
are occupied with parental care and leave their partners unguarded just when they are fertile,
the likelihood that they will be cuckolded may likewise increase (V á c l a v et al. 2002).
Acknowledgement
We thank the staff of the Vienna Zoo for allowing us to carry out this study on their property. Authors are grateful
to R. M a n n and anonymous referees and to all who contributed to the discussion and improved the manuscript.
R.V. and D. S. were supported by the exchange programme between Austrian and Slovak Academy of Sciences
and by the Konrad Lorenz Institute in Vienna.
306
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308
Folia Zool. – 52(3): 309–316 (2003)
Breeding ecology of Algerian woodchat shrikes Lanius senator: low
breeding success
Zahra BRAHIMIA1, Hamdi DZIRI1, Slim BENYACOUB1, Yassine CHABI1 & Jerzy BA¡BURA2*
1
Department of Biology, Faculty of Science, Badji Mokhtar University, B.P. 12, Annaba, Algeria
2
Department of Experimental Zoology and Evolutionary Biology, University of ¸ódê, Banacha 12/16,
PL-90237 ¸ódê, Poland; e-mail: [email protected]
Received 17 January 2002; Accepted 28 February 2003
A b s t r a c t . Breeding ecology of woodchat shrikes Lanius senator was investigated in the ELKala National Park in North-East Algeria (36°53’N; 8°30’E) in 1998–1999. Quercus suber was
the tree species most frequently used as support for nests, which were constructed at a mean
height of 5 m. First eggs in clutches were laid 7 May, and clutch size was 4.9. Approximately
42% eggs gave fledglings. Clutch size declined during the course of the breeding season but
fledgling success did not. Fledging success was positively correlated with per clutch mean egg
length and the height of the nest location above ground. We suggest that the major selective
pressures that shape the life history of Algerian woodchat shrikes are relatively heavy predation
and poor food availability.
Key words: North Africa, passerine, biology, clutch size, nesting, egg size, nestling growth, fledging success
Introduction
Over most of the Western Palearctic area, populations of the woodchat shrike Lanius senator
are in decline, and the species is now considered threatened in many countries (S n o w &
P e r r i n s 1998) but remains relatively common in the Mediterranean area, including North
Africa (S n o w & P e r r i n s 1998, I s e n m a n n & F r a d e t 1998, B e n y a c o u b &
C h a b i 2000). The breeding biology of this species remains poorly known and many
aspects require further study.
Reproductive strategies of passerine birds show some consistent patterns, which most
probably evolved under selection pressures generated by food and predation (M a r t i n
1995). Food of insectivorous birds is usually abundant and accessible for a rather short
period during the breeding season (M a r t i n 1995). Predation on nests is an especially
important factor of selection, and its rate is to a large extent associated with nesting sites and
sometimes also with time during the breeding season (R i c k l e f s 1969, M a r t i n 1995).
Open nests located in bushes or short trees experience particularly heavy predation
(R i c k l e f s 1969). As such, a common pattern of decline in clutch size and breeding
success has been observed over the course of the breeding season (P e r r i n s 1970,
C r i c k et al. 1993), as has careful nest site selection by breeding pairs (M a r t i n 1995).
We aim in this paper to analyse some characteristics of the breeding ecology of the
woodchat shrike in Algeria, an area for which detailed data have been so far lacking. The
main objectives of this study were to: 1) obtain information on nest location and size, clutch
size, egg sizes, nestling growth and fledging success; 2) characterize timing of egg laying
and its relation with other life history traits; and 3) investigate whether fledging success is
* Corresponding author
309
related to other life history traits and nest location. Our study raised the important question
of whether failure or success of a brood is influenced by bird quality related variables. If so,
then we can predict that fledging success of a particular clutch should be positively
influenced by nest and nesting characteristics or egg size (c.f. G o o d b u r n 1991).
Material and Methods
The study was carried out in the EL-Kala National Park in North-East Algeria (36°53’N;
8°30’E) over a two-year period (1998–1999). Climatic conditions during April and May of
the study were largely similar, with relatively high mean temperature 14–19 °C and rainfall
21–53 mm per month. The study area was extensively cultivated farmland, with nonintensive livestock systems influencing the character of vegetation (B e n y a c o u b &
C h a b i 2000). The study site was located amongst the mosaic of degraded forest habitats
with Quercus suber dominating and concurring with shrubs of Myrtus comunis, Rubus
ulmifolius, Pistacia lentiscus, Calycotome villosa, Daphne gnidum, Erica arborea, Genista
tricuspidata, Lolium multiflorum, Lythrum hypossopifolia and others.
Searching for nests started in February and was conducted at least once a week. Thirtynine initiated clutches of the woodchat shrike were monitored during the course of nesting
(23 nests in 1998 and 16 in 1999) every 1–5 days, more frequently during the expected time
of hatching and the nestling period. As the search for nests within the forest patches studied
was detailed, it is unlikely that any initiated woodchat shrike clutch could remain nonrecorded in the study area. Consequently, we were able to consider a within-clutch
proportion of eggs, which produced fledglings as a simple measure of fledging success.
The nesting tree/shrub species were determined in 1998 (n = 22 records, 1 record lost).
In 1998–1999, tree height and the height of nest location were measured (with n = 37
records of nest location height), with n = 27 of the nests measured to the nearest mm
(external diameter, nest cup diameter and depth). The sample sizes differ for different
variables due to subsampling or incompleteness of records. All of the initiated clutches
were controlled to record the date of the onset of egg laying, clutch size, the number of
fledglings and losses at different stages. Egg dimensions were measured in a subsample of
clutches to the nearest 0.1 mm with calipers: egg length (L) and breadth (B). These
measurements were used to calculate egg volume (V) and egg shape (ES) according to the
formulas: V = 0.000507*L*B2 (H o y t 1979), and ES = B/L*100%. All characteristics
related to egg dimensions are presented as means per clutch to avoid the non-independence
of egg traits within clutches (B a ƒ b u r a & Z i e l i ƒ s k i 1990, 1998, Z i e l i ƒ s k i &
B a ƒ b u r a 1998). For descriptive purposes, we also studied the growth of nestling
woodchat shrikes. In 16 broods, the growth of nestlings was monitored by weighing
a random nestling from a brood, from the day 1 to 13 of the nestling life (3–7 nestlings from
different broods per day).
The data were analysed by standard parametric and non-parametric methods (S o k a l &
R o h l f 1995). In the analysis of the within-clutch proportion of eggs that produced
fledglings (binomial error), the generalized linear model approach was applied (D o b s o n
1990). Original nest characteristics were used to calculate principal components for further
analysis. Split-linear regression was conducted following K o v á ã et al. (1999). All
analyses and calculations were carried out using MS Excel and STATISTICA 5.5
(S t a t S o f t 1997).
310
Results
Sixteen or 69.57% ± 9.59 (SE), of the 22 nests analysed in 1998 were constructed on Quercus
suber, 2 on Fraxinus angustifolia, 2 on Crategus monogyna, 1 on Olea oleaster and 1 on
Pyrus communis. Woodchat shrikes tended to select trees rather than bushes on which to
construct a nest; nest height varied greatly (Table 1).
Table 1. Nest site and nest characteristics of woodchat shrikes in 1998–1999 in Algeria.
Variable
n
Mean ± SD
Median
Min
Max
Nesting tree height (m)
Nest site height (m)
Nest external diameter (mm)
Nest cup diameter (mm)
Nest cup depth (mm)
35
37
27
27
27
6.4 ± 2.7
5.1 ± 1.6
119.6 ± 15.3
77.6 ± 5.7
54.4 ± 8.3
5.9
5.0
119.7
78.0
55.0
2.5
1.7
91.8
50.0
47.0
16.0
9.0
160.0
90.0
90.0
No significant difference in the distribution or mean value of the date of the onset of laying
was recorded between 1998 and 1999 (Kolmogorov-Smirnov test: P > 0.1; Mann-Whitney
test: P = 0.31). No between-year difference in clutch size, fledgling number or egg traits
(length, breadth, volume, shape; 56 eggs in 11 clutches in 1998 and 40 eggs in
7 clutches in 1999; mean clutch size in the subsample: 5.3 ± 0.2 SE) was found (Hotelling
T test: P = 0.60; individual t tests with separate variance estimation: 0.11 < P < 0.56).
Consequently, pooled characteristics are presented hereafter (Tables 2 and 3). Incubation lasted
15–17 days, mean 15.7 ± 0.2 (SE), from the moment of having laid the last egg in the clutch.
Clutch size was negatively correlated with laying date (r = -0.62, n = 35, P < 0.0001)
(Fig. 1). Successful and non-successful broods did not differ in the date of laying (MannTable 2. The date of the onset of laying, clutch size and the number of fledglings in woodchat shrike broods in
1998–1999 (pooled) in Algeria.
Variable
n
Mean ± SD
Median
Min
Max
Laying date
Clutch size
Fledgling number
Fledgling number
(non-0)
39
35
35
17
7 May ± 11.37
4.91 ± 1.01
2.14 ± 2.40
4.41 ± 1.28
4 May
5.00
0
4
13 April
3
0
2
11 June
6
6
6
Table 3. Characteristics of eggs of woodchat shrikes in 1998–1999. Per-clutch mean values for 17 complete
clutches included.
Variable
Mean ± SD
Median
Min
Max
Egg length (mm)
Egg breadth (mm)
Egg volume (cm3)
Egg shape
22.9 ± 0.65
16.7 ± 1.06
3.0 ± 0.40
72.9 ± 4.08
22.9
16.9
3.1
73.2
21.7
13.4
1.8
61.2
24.1
17.6
3.5
78.9
311
Whitney test: P = 0.46). A generalized linear model with laying date as the independent
variable and fledging success (binomial error) as response variable showed no relation
between these two variables (χ2: P = 0.30).
Fig. 1. Relationship between clutch size and the onset of egg laying in the woodchat shrikes studied in 1998–1999.
Seventy-five of 178 eggs gave fledglings (42.13% ± 3.71 SE), and 17 out of 39 clutches
(43.59% ± 7.94 SE) gave at least 2 fledglings (Table 2). So, most breeding attempts failed
(56.41 % ± 7.94 SE): 20.51% ± 6.46 (SE) of the 39 initiated clutches were abandoned at
different stages of egg laying and incubation probably due to predation; 25.64% ± 6.99 (SE)
of the clutches were completely destroyed by human or animal predators; 2.56% ± 2.53 (SE)
were completely destroyed at the nestling stage; and 7.69% ± 4.27 (SE) were completely
destroyed at the stage of nestlings after first having partially destroyed eggs (n = 39). Partial
destruction occurred in 10.26% ± 4.86 (SE) at the stage of eggs and in 7.69% ± 4.27 (SE) at
the stage of nestlings (n = 39). We found no breeding losses caused by bad weather.
Mean egg size positively influenced fledging success (generalized linear model:
χ21 = 39.34, P < 0.0001); mean egg length in successful clutches was 23.25 mm ± 0.21 (SE)
as compared with 22.58 mm ± 0.18 (SE) for clutches that failed to produce any fledglings. A
generalized linear model with nest and nest site characteristics as independent variables and
fledging success as response variable showed that the height of the nest location above
ground positively influenced fledging success (χ21 = 14.77, P = 0.0001), whereas neither
nest characteristics nor the height of the nesting tree were related to fledging success (NS).
Nests that produced no fledglings were generally constructed at a lower height than
successful nests: 4.73 m ± 0.40 (SE) v. 5.68 m ± 0.25 (SE).
Growth of nestlings was fast and roughly linear during the first 9 day period (slope =
2.83 ± 0.11 SE), then markedly slower reaching fledging mass (slope = 0.92 ± 0.38 SE), as
shown by the split-linear regression (Fig. 2). Day 9 ± 0.59 SE is the breakpoint of the splitlinear regression line. The split-linear regression accounted for more variation (R2 = 0.95)
312
than a simple linear regression (R2 = 0.94) or a quadratic regression (R2 = 0.92) which were
analysed for comparison (F tests: P < 0.001).
Fig. 2. Growth of woodchat shrike chick body mass with a split regression curve shown.
Discussion
Woodchat shrikes nested mostly on Quercus suber in our study area. This corroborates
suggestions that open Quercus forests are the species’ preferred habitats, where available, in the
Mediterranean area (S n o w & P e r r i n s 1998). I s e n m a n n & F r a d e t (1998) suggest
that woodchat shrikes generally use the most abundant tree or bush species, so that the selection
of the nest site is rather opportunistic. The tree or shrub species that support shrike nests constrain
the possible range of height at which the nests are constructed. As in most of the species’
breeding area, woodchat shrikes constructed nests at a mean height of about 5 m (G u s e v &
B e d n y i 1961, A d a m i a n 1964, U l l r i c h 1971, H u d e c et al. 1983, C r a m p &
P e r r i n s 1993, B o n a c c o r s i & I s e n m a n n 1994). However, this mean value is much
higher than that of another Algerian population studied near Tizi Ouzou, 2.62 m (M o a l i et al.
1997). Nest external diameter was relatively low in our study area, whereas the diameter and
depth of nest cup were similar to the values reported in other studies (H u d e c et al. 1983,
C r a m p & P e r r i n s 1993). Also, egg dimensions in our woodchat shrike population were
within the range reported for different parts of the species’ area (G u s e v & B e d n y i 1961,
E t c h e c o p a r & H u e 1964, H u d e c et al. 1983, C r a m p & P e r r i n s 1993).
In many areas of woodchat shrike distribution, a mean clutch size is > 5 eggs, but a
mean clutch size of 4.75 has also been reported (I s e n m a n n & F r a d e t 1998,
G u e r r i e r i & C a s t a l d i 2000), so that the value of about 4.9 recorded in our study is
within this range. Typical of single–brooded passerines (P e r r i n s 1970, C r i c k et al.
1993), Algerian woodchat shrikes showed a seasonal decline in clutch size. However, the
timing of breeding did not have any effect on nest or fledging success. In our study area,
laying eggs started at similar time as in the Tizi Ouzou (M o a l i et al. 1997), but earlier
than in southern France (I s e n m a n n & F r a d e t 1998).
313
Nest predation is known to cause relatively low breeding success in different woodchat
shrike populations (C r a m p & P e r r i n s 1993; B e c h e t et al. 1998). Predation by
animals and humans was also a main factor of breeding failure in our study population in
which weather-related causes, important in many shrike populations (e.g. S t a u b e r &
U l l r i c h 1970; T a k a g i 2001), seem to play a non-significant role. In French
populations, B e c h e t et al. (1998) recorded an even lower breeding success (36.5%) than
we observed. Time of the season does not appear to affect nest predation (B e c h e t et al.
1998). A high level of nest loss due to predatory animals is characteristic of the passerines
constructing open nests in shrubs (R i c k l e f s 1969, M a r t i n 1995). A similar
phenomenon may also occur in species that nest in short trees. Our observation that fledging
success is positively correlated with the height at which a nest is located suggests that there
may exist a pressure of natural selection to nest higher up within a tree. On the other hand,
I s e n m a n n & F r a d e t (1998) and B e c h e t et al. (1998) did not record any relation
between breeding success and nest site, including the nest height. This suggests that the
existence and direction of the selection pressure to nest higher may be highly site-specific.
Fledging success was also positively related to egg length, which is not reported very
often (W i l l i a m s 1994). A possible explanation may be that woodchat shrike pairs of
high quality, perhaps old ones, lay bigger eggs, are good at selecting a right location to nest
and are better at nest defense against predators. Such effects were described in some avian
species such as magpies Pica pica (G o o d b u r n 1991).
Comparative data for nestling growth in woodchat shrikes are scarce. G u s e v &
B e d n y i ’ s (1961) graph is similar to ours in general characteristics, but detailed
comparison is not feasible. The shape of the woodchat shrike growth curve may be
considered as a version of the typical curve of altricial passerines (c.f. O ’ C o n n o r 1984).
The curve has one significant break point that divides it into two component lines reflecting
two stages of the nestling development (Fig. 2). At the beginning of the first stage nestlings
develop their thermoregulatory abilities, which reduces energy loss and thus favours mass
gain, which results in the high growth rate. At the second stage, there occurs a decrease in
growth rate at about 9 days old, resulting from energy expenditure to plumage development
(O ’ C o n n o r 1984). The general pattern suggests that nestling shrikes grow as fast as
possible to attain adult body mass (30–40 g, S n o w & P e r r i n s 1998). They do not
show an excess weight before fledging, which combined with slow growth is very
characteristic of many passerines nesting in safe places, such as hole-nesters, especially
aerial insectivores (O ’ C o n n o r 1984, R e m e Ê & M a r t i n 2002).
In summary, the woodchat shrike population studied seems to be exposed to relatively
high predation, resulting in low breeding success (B e n y a c o u b & C h a b i 2000). If
this pressure were consistent over a longer time range, then some changes in breeding
behaviour would be expected (M a r t i n 1995). In general, a tendency to make ontogeny as
short as possible would be expected (R i c k l e f s 1969, M a r t i n 1995, R e m e Ê &
M a r t i n 2002). Nest site choice and nesting behaviour would be predicted to undergo a
strong pressure of natural selection. The actual modifications of the breeding strategy, if the
predation pressure continued to operate, would be constrained by some genetic and
environmental factors. The major environmental constraint in the study area would be a lack
of more suitable trees (accessibility and height). This may also explain some discrepancy
between the results concerning nest site selection reported in this paper and those shown by
I s e n m a n n & F r a d e t (1998) and B e c h e t et al. (1998). We would not predict the
314
occurrence of a selective predation pressure on the timing of breeding as long as the
predation rate is not related to time during the season.
Food is probably also an important factor, influencing both clutch size and breeding
success in Algerian woodchat shrikes. In many European areas, woodchat shrikes prey upon
lizards and frogs (C r a m p & P e r r i n s 1993). These animals are rarely available in our
study site, the diet being composed mostly of insects belonging to Orthoptera and
Coleoptera, whose abundance increases seasonally prior to breeding (unpublished
observation). This may negatively influence the quality of food preferred by woodchat
shrikes. Consequently, we suggest that the major selective pressures that shape the life
history of Algerian woodchat shrikes are relatively heavy predation and poor food
availability and quality (c.f. M a r t i n 1995).
Acknowledgements
We are grateful to the authorities of the El-Kala National Park for their help. We thank Paul I s e n m a n n for
supplying some items of literature. Vladimír K o v á ã kindly helped us in calculating and analysing split-line
regressions. We are grateful to anonymous referees and Gordon H. C o p p for their helpful remarks on the
manuscript.
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316
Folia Zool. – 52(3): 317–322 (2003)
Production-growth model applied in eublepharid lizards
(Eublepharidae, Squamata): accordance between growth and
metabolic rates
LukበKRATOCHVÍL and Daniel FRYNTA
Department of Zoology, Faculty of Sciences, Charles University, Viniãná 7, CZ-128 44 Praha 2, Czech
Republic; e-mail: [email protected]; [email protected]
Received 13 February 2002; Accepted 20 February 2003
A b s t r a c t . We studied growth rates in four eublepharid species in which mass-metabolic
allometry was available from the literature. The lizards were reared in a common garden
environment and the growth data were analysed using the production/growth model (W e s t et
al. 2001: Nature 413: 628–631). The model fits well our data in eublepharid geckos, and thus
the applicability of this model to reptile growth was demonstrated. Estimated values of growthrate parameter (a) fell within the range known in other ectotherm animals. As expected from
theoretical parameter derivation, species sharing the same mass-metabolic allometry
(Eublepharis macularius, Coleonyx mitratus, Coleonyx elegans) show comparable a in spite of
considerable interspecific differences in asymptotic body mass. Moreover, in accordance with
theoretical predictions, the only examined species with the elevated metabolic scaling, i.e.
Coleonyx brevis, showed higher a than the other species.
Key words: growth curve, Eublepharis, mass-metabolic allometry
Introduction
Individual growth of animals has been modeled using a number of growth curves (e.g.
H a i l e y & C o u l s o n 1999, W a n et al. 2001, M o s c a r e l l a et al. 2001). These
empirical functions usually fit to each data set well, on the other hand, their parameters have
been difficult or even impossible to interpret biologically (but see V o n B e r t a l a n f f y
1957, L ó p e z et al. 2000). The need to approach this problem in a new spirit, in particular
to deduce general growth function from basic physiological mechanisms, has been evident.
The production/growth model recently derived by W e s t et al. (2001) is based on the
allocation of metabolic energy between maintenance of existing tissue and the production of
new biomass. Generally, this model ascribes the slowing of growth as body size increases to
limitation on the capacity of networks to supply adequate resources to support further
increase in body mass. W e s t et al. (2001) derived a universal sigmoidal growth curve
⎧ m ⎫1/4
⎡
⎧ m0 ⎫1/4⎤ –at /4M 1/4
⎜ ⎢ = 1 – ⎢1 – ⎜
⎢ ⎢e
⎩M⎭
⎢
⎩M ⎭ ⎢
where m is the body mass at the time t, M is the asymptotic maximum body mass, m0 is the
mass at birth, and a is the curve parameter calculable from fundamental cellular parameters.
Parameter a ≡ B0mc/Ec, where mc is the mass of a cell, Ec is the metabolic energy required to
create a cell and B0 is mass normalized metabolic rate (B0 = B/m3/4, where B is the average
resting metabolic rate of the whole organism at time t), i.e. B0 is constant for a given taxon.
317
The growth-rate parameter (a) is thus expected to be similar for species with similar body
temperature and similar metabolic scaling on body mass (C h a r n o v 2001). The curve
shows good accordance with data on individual growth across a range of animal taxa
(mammals, birds, fish, shrimp), however, the taxonomic spectrum of examined organisms has
been limited, e.g. reptiles has been completely lacking (W e s t et al. 2001).
This work summarizes growth data from a common-garden experiment carried out in
four species of the gecko family Eublepharidae, which are good model organisms for a
study investigating the new model. These lizards exhibit considerable diversity in body size
and standard metabolic rate scaling (D i a l & G r i s m e r 1992, K r a t o c h v í l &
F r y n t a 2002). In fact, few groups have such a broad range of body size within one small
monophyletic assemblage. Large Eublepharis macularius Blyth, 1854, and much smaller
Coleonyx elegans Gray, 1845 and C. mitratus (Peters, 1845) share the same (ancestral)
allometric relationship between standard metabolic rate and body mass. The smallest species
C. brevis Stejneger, 1893 is a member of the desert clade with derived high standard
metabolic rates (D i a l & G r i s m e r 1992). Therefore, when the production/growth
model is fitted on growth data taken at the same temperature, E. macularius, C. elegans and
C. mitratus are expected to show comparable a despite the considerable among-species
differences in asymptotic body mass, and C. brevis, the species with elevated metabolic
scaling, should show relatively higher a.
Material and Methods
Animals born in the laboratory were weighed from hatching up to the age of approximately
two years in intervals of one or two months with a digital balance to the nearest 0.1 g. Lizards
were maintained individually in small cages with shelters and substrate (wet peat-moss or
sand according to preferred humidity) in conditions that allowed no active thermoregulation.
They were placed in a centrally heated room with a 12L:12D photoperiod at 26 ± 1 °C. This
temperature is near the preferred body temperature in eublepharids and the temperature used
in metabolic rate measurements (D i a l & G r i s m e r 1992). Water and food (vitaminised
crickets and mealworms) were provided three times a week, i.e. both were provided ad
libitum. In total, we obtained 624 measurements in 111 individuals of known age (in days)
kept under these standard conditions. Data concerning a single individual (outlier) showing
apparently retarded growth were excluded. Growth curve characteristics of these species in
other measured trait (snout-vent length) were published elsewhere (K r a t o c h v í l &
F r y n t a 2002).
First, we applied a production/growth curve to the overall sample of a given species
using the Levenberg-Marquardt algorithm, which minimized the sum of squares between
predicted and observed values of growth. In this case, the mass at birth (parameter m0) was
estimated as a mean mass of freshly hatched juveniles (weighted within three days after
hatching) from our lab (E. m.: 3.36 g, n = 24; C. m.: 0.83 g, n = 16; C. e.: 1.11 g, n = 30;
C. b.: 0.30 g, n = 8). Because the intersexual differences were much smaller than
interspecific, we pooled data of both sexes in a given species sample. Second, to exclude
pseudoreplicates we selected well-represented individuals, i.e. individuals with more than
seven measurements and measured long enough after the inflection point of growth
trajectory, and fitted the production/growth curve separately to each individual growth
trajectory of these individuals (11 individuals of E. m., 14 ind. of C. m., 7 ind. of C. e., and 3
318
ind. of C. b.). Interspecific differences in growth curve parameters were tested with KruskalWallis nonparametric ANOVA. All calculations were performed using STATISTICA,
version 6.0 (S t a t S o f t Inc. 2001).
Results
The production/growth model fits well our longitudinal growth data as obvious from the plot
of the dimension-less mass ratio versus the dimension-less time variable (Fig. 1). The model
explained 86 %, 85 %, 90 %, 92 % of total variance in E. macularius, C. elegans, C. mitratus,
and C. brevis, respectively. As expected, species differ significantly in asymptotic mass
(Table 1). The parameter a was similar in E. macularius, C. mitratus, and C. elegans.
Confidence intervals (95%) of these values showed extensive overlap, except in the case of
Fig. 1. A plot of dimension-less mass ratio, r = (m/M)1/4, versus the dimension-less time variable, τ = (at/4M1/4)-ln[1(m0/M)1/4], for four species of eublepharids. When plotted in this way, the production/growth model predicts that
growth curves should fall on the same universal parameterless curve 1 – e –τ (shown as solid line). According to the
model, parameter r represents the proportion of total lifetime metabolic power for maintenance and other activities.
Table 1. The number of pseudoreplicates (n), the estimated values (mean ± SE) of the asymptotic mass in g (M)
and the growth rate (a) for the examined species of eublepharid geckos.
Species
E. macularius
C. mitratus
C. elegans
C. brevis
n
279
192
120
33
a
M
0.0289 ± 0.0012
0.0247 ± 0.0010
0.0220 ± 0.0014
0.0421 ± 0.0048
51.53 ± 1.81
10.06 ± 0.29
12.64 ± 0.59
2.35 ± 0.11
319
Fig. 2. Asymptotic body masses (M) estimated from individual growth curves in four species of eublepharid
geckos. Explanations: Em = Eublepharis macularius, Cm = Coleonyx mitratus, Ce = C. elegans, Cb = C. brevis.
Fig. 3. Growth rate parameters (a) estimated from individual growth curves in four species of eublepharid geckos.
Abbreviations as in legend to Fig. 2.
320
E. macularius – C. elegans comparison. However, confidence intervals were systematically
underestimated by inclusion of pseudoreplicates (multiple values obtained from each
individual), and the comparison was not significant when this inflation was avoided (see
below). On the contrary, although the data set concerning C. brevis was small, its parameter
a was significantly higher than in the other species (Table 1).
These observations are supported by non-parametric statistics applied on parameters
estimated from individual growth trajectories of well-represented individuals. KruskalWallis ANOVA confirmed considerable interspecific differences in asymptotic mass
(H = 28.12; P < 0.0001; Fig. 2). More remarkably, Kruskal-Wallis ANOVA found
interspecific differences in growth parameter a (H = 11.70; P < 0.01; Fig. 3). This
significance is clearly the result of the higher a in C. brevis (Kruskal-Wallis ANOVA testing
for differences in a among the other three species: H = 4.35; P = 0.11).
Discussion
The production/growth model shows good accordance with our data in eublepharid geckos,
and thus the applicability of this model to reptilian growth in non-fluctuating thermal
environment was clearly demonstrated (Fig. 1). Lizards fit well universal growth curve
(compare with Fig. 2 in W e s t et al. 2001). Estimated values of growth-rate parameter (a)
for the examined lizards fall within the range (0.017 – 0.1) known in other ectotherm animals
(several fish species, shrimp), but are substantially lower than those approximated for
mammals and birds (0.21 – 1.9). This sharp distinction between ectotherms and endotherms
clearly reflects both the differences in body temperature and in fundamental metabolic
parameters of the cell across taxa (W e s t et al. 2001). A recently published paper
(G i l l o o l y et al. 2001) shows that temperature-compensated resting metabolic rates of
ectoterms are slightly lower than those of birds and mammals.
It is important to note that the values of growth-rate parameter a for eublepharids are in
accordance with the general prediction derived from the production/growth model. Although
the geckos differed considerably in body mass, mass cannot explain the observed
differences in their growth rate. Growth rates apparently follow the size-adjusted metabolic
values. E. macularius, C. elegans and C. mitratus share simultaneously the similar
metabolism allometry and growth parameter values. In contrast, C. brevis demonstrated an
elevated level of metabolic scaling and a correspondingly higher a parameter. Cases such as
this, in which closely related species show different metabolic scaling, may be very
informative when evaluating theoretically derived growth relationships.
Our study is presumably the first to demonstrate that reptilian species also follow the
general production-growth model (at least in non-fluctuating thermal environment). Reptiles
seem to be good model for getting a fundamental understanding of animal growth: unlike
birds and mammals, neonate reptiles show similar metabolic rates to those of adults after
correction for body mass differences (see review by N a g y 2000). Therefore, parameter a
is more likely to be constant during ontogeny.
Moreover, reptiles could be easily reared under different thermal conditions (both
constant and fluctuating), which would be very informative. Such simple manipulation
affects many parameters of the production/growth model, and it is not only the case of the
mass-normalized metabolic rate (parameter B0). But also the mass of a single cell (mc) and
the asymptotic maximum body mass (M) in ectotherms are affected by rearing temperature,
321
both latter generally increase at lower temperatures (A t k i n s o n 1994, V a n
V o o r h i e s 1996). Manipulations of thermal environment in ectothermic animals and
comparison between theoretical predictions and empirical results in future studies can help
us to judge unequivocally the accuracy and universality of this new model.
Acknowledgements
We thank J. P o l e c h o v á , P. M i k u l o v á and two anonymous referees for their useful comments. This
project was supported by Grant Agency of Charles University Project No. B-BIO-121/2001 and the Institutional
Grant given by the Ministry of Education, Youth and Sports of the Czech Republic (No. J13-8113100004).
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322
Folia Zool. – 52(3): 323–328 (2003)
Reproductive biology of Capoeta tinca in Gelingüllü Reservoir, Turkey
Fitnat Güler EKMEKÇİ and Saniye Cevher ÖZEREN
Hacettepe University, Faculty of Science, Biology Department, Beytepe Campus, 06532 Ankara, Turkey;
e-mail: [email protected]
Received 5 November 2001; Accepted 5 June 2003
A b s t r a c t . The breeding and sexual maturation properties of a cyprinid fish Capoeta tinca
were studied in Gelingüllü Reservoir, a recently impounded dam in Central Anatolia. Ripening
of gonads commenced in early spring, whereas spawning occurred between May and June.
Sexual maturity age was 2+ for males and 3+ for females. The results obtained from this study
were compared with those of other populations of C. tinca in Turkey.
Key words: Central Anatolia, spawning, sexual maturity age, gonadosomatic index
Introduction
The Cyprinid fish, Capoeta tinca, has a wide distribution in Anatolia, including the Sakarya,
Kızılırmak and Çoruh river basins as well as some streams in the Marmara region that are
hydrologically connected to the Black Sea. But it is not present in the Mediterranean Basin
and in Thrace, the European part of Turkey (E r k ’ a k a n 1983). Capoeta tinca can adapt
very easily to changes in water regime, it occurs both in lotic and lentic habitats so this
species has economic value as a commercial fish from natural and man-made lakes. In the
meantime, C. tinca has tolerance to salinity and pollution, and lives in streams with salinity
of 10.5 g.l-1 and conductivity of 22000 µS.cm-1 (E k m e k ç i 2002). As an herbivorous fish,
it is not a high value food like Esox lucius, Sander lucioperca and Silurus glanis. However,
owing to its wide distribution and tolerance to different habitats, and its size (max. standard
length=43cm, max weight=1178g; Y ı l m a z & G ü l 1999a), this species is consumed as
food by people.
We examined the breeding and sexual maturation properties up on which minimum
fishing size is to be based for the sustainable management of Gelingüllü Reservoir,
a recently impounded dam in Central Anatolia. There have been a few studies of C. tinca
reproduction (A k g ü l 1986, 1988, Y ı l m a z & G ü l 1996, Y ı l m a z & G ü l 1999b),
though only one in a reservoir (E k m e k ç i 1996). Whereas its growth properties are welldocumented (e.g. S o l a k 1982, E r k ’ a k a n & A k g ü l 1985, A k g ü l 1986,1988,
C e n g i z l e r & E r d e m 1994, Y ı l m a z et al. 1996, E k m e k ç i 1996, 2002,
Y ı l m a z & G ü l 1999a).
Study Area, Material and Methods
The Gelingüllü Reservoir is located to the southeast of the city of Yozgat, in the region of
Central Anatolia (39°36’30’’N, 35°03’20’’E). The reservoir has an area of 2.4 km2 at the
maximum water level. The dam was constructed on the Delice stream, a tributary of
Kızılırmak River (Fig.1). The altitude of the reservoir is 1000 m. above sea level. Typical
continental climate prevails in the study area, maximum and minimum air temperatures were
323
recorded as 37.1 °C (in July) and -23.7 °C (in January) respectively. Surface water
temperature ranges between 22 °C (July) and 2 °C (December), whereas the dissolved
oxygen content varies between 8.9 mg.l-1 (June) and 11.8 mg.l-1 (April). Water pH ranges
between 7.47 and 9.39, and the conductivity ranges between 310 and 430 µS.cm-1. Secchi disc
transparency is 1.11 m in May 1996 and 4.42 m in November 1996.
Fig. 1. Map of the study area.
Beside C. tinca, native fish species such as Capoeta capoeta sieboldi, chub (Leuciscus
cephalus), nase (Chondrostoma regium), bleak (Alburnus orontis), barbel (Barbus tauricus), loach
(Orthrias sp.) and introduced species such as goldfish (Carassius auratus), topmouth gudgeon
(Pseudoraspora parva) and common carp (Cyprinus carpio) live in the Gelingüllü Reservoir.
A total of 220 fish were sampled on a monthly basis between December 1995 to
December 1996, except in January and February 1996, when the lake was frozen. In the
second week of every month samples were collected with the aid of fishermen, using gill
nets of 25 to 110 mm mesh size. During our field studies in Gelingüllü Reservoir, we had
some doubts about the hybrids among C. tinca and C. capoeta. In this study, specimens
suspected of being hybrids were excluded.
324
Fork length (FL) were measured with an accuracy of 1 cm and weighed to nearest 1 g
in the field. Scales were used for age determination. They were firstly cleaned by 4%
NaOH and dry mounts held between microscope slides as given in L a g l e r (1966).
Males differ from females morphologically by the presence of breeding tubercules formed
on the head during the spawning period. The sex of immature fish was confirmed by
observation of gonads with the aid of a binocular. For sex determination of mature
specimens, the gonads of fresh samples were observed macroscopically, and then the
ovaries were removed and weighed. Body weights were determined to the nearest gram,
where as the gonads of females were weighed with an accuracy of 0.1 g. and preserved in
4% formaldehyde for subsequent assignment of gonad development, 29 ovaries could not
be weighed as they were less than 0.1g. Gonadosomatic index (GSI) was calculated as:
GSI = Gonad weight x 100 / total body weight.
a)
b)
Fig. 2 (a). Monthly variation of gonadosomatic index and (b) relative fecundity (eggs.g-1) for female Capoeta tinca.
325
Seasonal changes in GSI, egg diameter and number of eggs per 1 gram of ovary were
used to elucidate the reproductive biology of this species. Egg diameter and number of eggs
could be counted from 50 females whose ovaries contain visible eggs. Age at maturity was
determined from fish collected in April and June based on gonad development.
Fecundity was estimated from counts of yolky eggs in 1 g samples from three different
parts (proximal, middle and distal) of a preserved ovary and multiplying the mean value by
the total weight of both ovaries (B a g e n a l & B r a u m 1971). Mean egg diameter was
calculated from the average of a total of 30 eggs, 10 from the proximal, middle and distal
parts of the ovary, which were measured to the nearest 0.01 mm. The students’ t-test was
used to test for the differences in egg number and diameter between different parts of ovary.
Results and Discussion
Age at maturity in Capoeta tinca of Gelingüllü Reservoir is at age 3. Only 7 % of females
<3 years were immature, whereas the remaining females of ≥ 3 years were all mature. It is
apparent that the females became mature at the age of 3. The males, on the other hand,
become mature at age 2. Although age at maturity of both males and females in C. tinca
populations of other river basins differs from those reported here, the one-year difference
between males and females is characteristic of all populations (A k g ü l 1986, 1988,
E k m e k ç i 1996, Y ı l m a z & G ü l 1996, Y ı l m a z & G ü l 1999b).
The females were dominant in the population to the males by a ratio of 1:4.23 during
the sampling period. In other populations of Capoeta tinca in Turkey, the ratio of males to
females fluctuates between 0.64–1.15:1 (A k g ü l 1986, 1988, E k m e k ç i 1996,
Y ı l m a z & G ü l 1996, Y ı l m a z & G ü l 1999b).
Gonad weight and GSI in females peaked in May (Fig.2a) as did egg diameter (Fig.3),
suggesting that eggs were laid between May and July. In July, all the ovaries were empty and
only a few remaining eggs were observed. However, GSI values from C. tinca populations in
Fig 3. Monthly variation of egg diameter for Capoeta tinca.
326
Fig. 4. Length-fecundity (Fa) relation for Capoeta tinca.
Fig. 5. Relation between age and fecundity (Fa) for Capoeta tinca.
other regions of Turkey indicate that reproduction starts in April and lasts until September,
depending on the water temperature and altitude, with spawning periods in Anatolia such as,
May to June (S o l a k 1982, Y ı l m a z 1994), May–July (E k m e k ç i 1996, Y ı l m a z &
G ü l 1996), July to September (E r k ’ a k a n & A k g ü l 1985), and June–July (A k g ü l
1988). Altitude, climate and the ecological differences of stagnant and running water have
great effects on the spawning period as stated by N i k o l s k i i (1963) and B e n n e t t
(1970). The water temperature in the Gelingüllü Reservoir during the spawning period was
about 19 °C. The recorded water temperatures during the spawning period of C. tinca vary
between 21–22.5 °C (S o l a k 1982; E r k ’ a k a n & A k g ü l 1985, A k g ü l 1988,
Y ı l m a z 1994, E k m e k ç i 1996, Y ı l m a z & G ü l 1996, Y ı l m a z & G ü l 1999b).
Relative fecundity can be used to identify the start of the breeding season, because the
number of eggs in a constant weight decreases when they become ripe. This occurred in
May and June (Fig. 2b). There were no significant differences in means of the number of
327
eggs per g. and egg diameter between the parts of ovary (student’s t-test). The maximum
mean egg diameter (1.88 mm) was measured in June. Y ı l m a z & G ü l (1996, 1999b)
stated the maximum of mean egg diameter as 1.8 mm and 1.62 mm respectively.
The mean number of eggs (absolute fecundity) in ovaries was significantly related to
the mean fork length with (Fig. 4) (F=45.93 df=1,4 p<0.05). A significant relation
(F=27.23, df=1,4 and p<0.05) was also established between age and the mean number of
eggs in ovaries (Fig. 5). The maximum absolute fecundity was found as 58 896 eggs for a
7 year old female with a weight of 720g and 39.9cm total length (36.6cm fork length)
caught in December 1995.
Acknowledgements
The authors extent their sincere thanks to two anonymous referees and G. H. C o p p for both linguistic and
scientific contributions and Ali Celal H o ş for his assistance in field works.
L I T E R AT U R E
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living in Kelkit Stream]. IXth National Biology Congress, Sivas (in Turkish).
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of Fish Production in Fresh Waters. IBP Handbook no:3 Oxford: Blackwell Scientific Publications: 166–198.
BENNET G. W. 1970: Management of lakes and ponds. Van Nostrant Reinhold Company.
CENGİZLER I. & ERDEM Ü. 1994: [Growth of Barbus plebejus, Bonaparte, 1832, Capoeta tinca (Heckel, 1843)
living in Almus Dam Lake]. XIIth National Biology Congress: 36–42 (in Turkish).
EKMEKÇİ (ATALAY) F. G. 1996: Some growth and reproduction properties of Capoeta tinca (Heckel, 1843)
living in Sarıyar Dam Lake (Ankara). Tr. J. of Zool. 20: 117–127 (in Turkish with English summary).
EKMEKÇİ F. G. 2002: The effects of high salinity on the production of Capoeta tinca in a naturally contaminated
river. Tr. J. Zool. 26: 265–270.
ERK’AKAN F. 1983: The fishes of Thrace region. Hacettepe Bull. of Nat. Sci. and Eng. 12: 39–48.
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Technical Research Council of Turkey, Project Report No:VHAG-584, Ankara (in Turkish with English summary).
LAGLER K. F. 1966: Freshwater Fishery Biology, W.M.C. Brown Company, Iowa.
NIKOLSKII G. V. 1963: The ecology of fishes (Translated by L. Birkett). Academic Press, London.
SOKAL R. R. & ROHLF F.J. 1997: Biometry: the principles and practice of statistics in biological research.
W. H. Freeman and Company, New York.
SOLAK K. 1982: Investigations on relations with biology and ecological parameters of Capoeta tinca species
living in Çoruh and Aras Basin. Habiltation Thesis, Erzurum (in Turkish with English summary).
YILMAZ M. 1994: Bio-ecological properties of carp (Cyprinus carpio L., 1758) and In Balığı (Capoeta tinca
(Heckel, 1843) living in Kapulukaya Dam Lake (Kırıkkale). Gazi University, PhD Thesis (in Turkish with
English summary).
YILMAZ M. & GÜL A. 1996: The reproduction properties of In Balığı (Capoeta tinca (Heckel, 1843)) living in
Kirmir Stream of Sakarya River (Ankara, Turkey). G.U. Gazi Eğitim Dergisi 4: 84–97 (in Turkish with
English summary).
YILMAZ M. & GÜL A. 1999a: Growth properties of Capoeta tinca (Heckel, 1843) living in Devres Stream of
Kızılırmak River. G.U. Gazi Eğitim Dergisi 19 (1): 11–26 (in Turkish with English summary).
YILMAZ M. & GÜL A. 1999b: The reproduction properties of In Balığı (Capoeta tinca (Heckel, 1843)) living in
Devres Stream of Kızılırmak River. G.U. Gazi Eğitim Dergisi 19 (2): 57–72 (in Turkish with English summary).
YILMAZ M., GÜL A. & SOLAK K. 1996: Investigation of some biological properties of Capoeta tinca (Heckel,
1843) living in Kirmir stream of Sakarya River. Tr. J. of Zool. 20: 177–187 (in Turkish with English summary).
328
Folia Zool. – 52(3): 329–336 (2003)
The expansion and occurrence of the Amur sleeper (Perccottus glenii)
in eastern Slovakia
Ján KO·âO1, Stanislav LUSK2, Karel HALAâKA2 and Vûra LUSKOVÁ2
1
Department of Ecology, Faculty of Human and Natural Sciences, Univesity of Pre‰ov, 17. novembra 1,
081 16 Pre‰ov, Slovakia; e-mail: [email protected]
2
Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, Kvûtná 8, 603 65 Brno, Czech
Republic; e-mail: [email protected]
Received 14 April 2003; Accepted 21 July 2003
A b s t r a c t . The Amur sleeper, Perccottus glenii Dybowski, 1877, is indigenous in eastern
Asia. During the second half of the 20th century, with the aid of man, it spread over the eastern
part of Europe as well as in central Asia. In the course of 50 years of its dispersal in the western
direction the species already reached the Vistula drainage area (the Baltic Sea basin) and the
Danube drainage area (the Black Sea basin). In the latter basin, its occurrence was ascertained
in the drainage area of the Tisza river in Hungary in 1997. In eastern Slovakia, the Amur sleeper
was first recorded in 1998 in the Latorica drainage area. In the course of subsequent years it has
become a common species in the streams in the basins of the Latorica, Bodrog and Tisza rivers.
In shallow lentic waters densely grown with aquatic plants the species becomes a superdominant
or even exclusive species in the local fish communities. It has no marketable value but presents
a serious threat to the existence of native fish species with similar identical microhabitat
requirements.
Key words: Perccottus glenii, exotic species, invasion, Tisza river basin
Introduction
In an absolute majority of cases, both intentional and unintentional introduction or invasion
of an exotic fish species causes a risky contamination of indigenous ichthyofauna. As a rule,
the presence of one or several exotic taxa exerts a permanent, direct or indirect, negative
influence on the native species, as has been widely demonstrated for fishes (A l l e n d o r f
1991, R o s s 1991, E f f o r d et al. 1997, C r i v e l l i 1995, H o l ã í k 1991). In most
cases, the introduction of an exotic species will not remain limited to the initial hydrological
area into which it had been introduced. Often the species will gradually spread uncontrolled
over a large territory. Any attempt at preventing the exotic element from spreading or even
removing it from the biota it had invaded has failed.
After the non-indigenous form, Carassius auratus, had expanded over the Danube river
basin in the second part of the 20th century (H o l ã í k & Î i t À a n 1978, L u s k et al.
1998), we are now witnessing the expansion of several species of the genus Neogobius
(A h n e l t et al. 1998, Z w e i m ü l l e r et al. 1996, K a u t m a n 2001, S t r á À a i &
A n d r e j i 2001, H o l ã í k 2002, etc.). In recent years, Ictalurus melas (K o ‰ ã o &
K o ‰ u t h 2002) and Perccottus glenii Dybowski, 1877, a species hitherto unknown in central
Europe, have recently occurred and spread in eastern Slovakia (the Tisza drainage area).
Perccottus glenii is indigenous to the Russian Far East, north-eastern China, and the
northern part of the Korean Peninsula (B e r g 1949, N i k o l s k y 1956, K i r p i c h n i k o v
329
1945, E l o v e n k o 1981, B o g u t s k a y a & N a s e k a 2002). In the course of the 20th
century, two introductions into the European part of Russia were recorded. The first
introduction took place in St. Petersburg in 1912. There, after having been temporarily kept
in aquaria, the species was released into small ponds and occurred in free waters in their
environs. Subsequently, the species gradually spread over the drainage area of the Gulf of
Finland (D m i t r i e v 1971, P a n o v et al. 1999). The second introduction took place in
Moscow in 1948 when the species was imported by the participants of the Amur Expedition.
After having been kept in aquaria and having become popular among the aquarium keepers,
the Amur sleeper was released into nature. Then it began spreading over the hydrological
system of the Moscow river and the upper part of the Volga river basin (S p a n o v s k a y a
et al. 1964). Apparently, this second introduction was the onset of a gradual occupation of
the range in the European part of Russia and its dispersal westwards. Its further spread over
both the Asian part of Russia, the Baikal area, Kazakhstan, Uzbekistan, Turkmenistan and
the eastern part of Europe and, in recent years, even the White Sea and the Arctic Ocean
basins is connected with transports of stocking materials of various fish species in which the
Amur sleeper was an undesired admixture (L i t v i n o v & O ’ G o r m a n 1996,
E l o v e n k o 1981, B o g u t s k a y a & N a s e k a 2002). Around 1980 the European
range of the Amur sleeper was limited to the environs of St. Petersburg, the drainage area of
the Oka river (Moscow region) and the middle part of the Volga river basin (E l o v e n k o
1981). At present the species is dispersed over practically the whole European part of the
former Soviet Union, and it is spreading westwards. In Poland the Amur sleeper was first
recorded in the Vistula river (the Baltic Sea basin) in 1993 (A n t y c h o w i c z 1994). Over
of subsequent years it has spread into the middle reaches of the Vistula, including its
floodplains and tributaries (T e r l e c k i & P a l k a 1999). K o z l o v (1993) reports the
species from the Don river, B o g u t s k a y a & N a s e k a (2002) from the Dnieper river.
K o r t e et al. (1999) found the Amur sleeper to be a dominant fish species in the upper
reaches of the Dniester river basin in Carpathian Ukraine. The first finds of the species in
the Danube river system come from the Tisza river basin in Hungary (H a r k a 1998), in
Carpathian Ukraine from the Latorica drainage area (M o s h u & G u z u n 2002), and in
Slovakia from the basins of the Latorica and Bodrog rivers (K o ‰ ã o et al. 1999,
K a u t m a n 1999, our own data).
Material and Methods
In 1999–2002 years the occurrence of the Amur sleeper was studied by means of electrofishing, using a gear producing pulsating electrical current, 170–250 V, 0.5–3.5 A. The fish
caught in the localities under study were determined down to species and released. For later
examinations, samples of fish were preserved in 5 % formaldehyde (food, growth), 80 %
ethyl alcohol (growth, biometrics), frozen (genetic analyses) or kept live (karyology
analysis). The species diversity index (H’) was calculated according S h a n n o n &
W e a v e r (1949) using binary logarithms. The documentary material is deposited in the
collections of the Department of Ecology, Pre‰ov University, Slovakia.
Results and Discussion
In Slovakia the Amur sleeper was first found for in August 1998 in a pool near Kamenná
Moºva in the floodplain of the Latorica river (K o ‰ ã o et al. 1999). K a u t m a n (1999)
330
found the species in April 1999 in the floodplain of the Latorica river, viz., in the Vel’ké
plytãiny and Brestovisko channels near the village of BoÈany, and in the Lelesk˘ channel near
the village of Leles. In July 1999, we caught the Amur sleeper in several places in the
floodplain of the Latorica river. During our subsequent investigations carried out in August
1999, we found the species even in the dead river branches of the Bodrog river.
Fig. 1. Localities of evidenced occurrence (■) of Perccottus glenii in the Latorica, Bodrog and Tisza drainage
areas, eastern Slovakia.
Intense investigations implemented in 2001 and 2002 in the Bodrog, Latorica and Tisza
drainage areas, eastern Slovakia, have shown that the Amur sleeper had become a common
species in the hydrological systems of those rivers (Fig. 1). In shallow lentic waters of various
habitats (gravel pits, channels, backwaters), densely grown with aquatic vegetation (Stratiotes
aloides, Myriophyllum spicatum, Ceratophyllum demersum, Elodea canadensis, Nuphar
luteum, Typha latifolia), the species was dominant in the local fish communities in a number
of places. Such microhabitat types harbour minimum numbers of fish species (Esox lucius,
Perca fluviatilis) reported as important predators of the Amur sleeper (B o g u t s k a y a &
N a s e k a 2002). This is fully confirmed by our own observations: in localities with the
greatest abundance of the Amur sleeper we would usually find only occasional individuals
of E. lucius, less than 150 mm in standard length. The share of the Amur sleeper in samples
of fish taken in the localities under study increases significantly with increasing surface of
the habitat grown with aquatic vegetation. Habitats with high dominance of the Amur
sleeper show rather low species richness and low species diversity (H’) of the fish
community (Table 1). The representation of the Amur sleeper in the fish community in a
locality is significantly dependent upon the degree to which it is grown with aquatic
vegetation (R=0.97, F=177.7, p<0). Likewise, the number of fish species present decreases
significantly with increasing grown-up area (R=0.86, F=34.5, p < 8-5), the same as their
species diversity H’ (R=0.87, F= 36.2, p< 6-5). The number of fish species in the locality
examined decreases with increasing share of the Amur sleeper (R=0.81, F=22.1, p<51-4).
331
Table 1. Occurrence of the Amur sleeper in various localities of eastern Slovakia in 2001–2002.
Locality
(year)
Habitat
type
Grown-up Species
surface
richness
(%)
No. fish
captured
(n)
Share of
P. glenii
(%)
H’
E
Svätá Mária
(2002)
channel backwater
80 %
5
469
95.3
0.35
0.06
Karãa-V. Kamenec
(2001)
river arm
0.5%
17
363
4.1
3.18
0.78
Karãa-V. Kamenec
(2002)
river arm
0.5%
16
484
0.6
2.96
0.74
Hranice-Streda n.B.
(2001)
channel
35%
12
363
19,0
2.63
0.73
Hranice-Streda n.B.
(2002)
channel
40%
11
153
39.2
2.55
0.74
Somotor
(2001)
channel
15 %
10
229
0.9
2.27
0.68
Somotor
(2002)
channel
15 %
17
284
2.5
3.52
0.86
Kamenná Moºva
(2002)
channel
70 %
9
74
71.6
1.60
0.505
Kamenná Moºva
(2002)
3 gravel pits
5%
17
677
0.9
2.36
0.59
Tisa-M.Trakany
(2001)
lakes
10 %
14
197
2.5
2.74
0.68
Tice – Leles
(2002)
old backwater
95%
2
205
82.9
0.66
0.66
KapoÀa
(2001)
backwater
10 %
9
93
2.1
2.35
0.74
KapoÀa
(2001)
gravel pit
45 %
10
147
51,0
2.15
0.65
N.Vieska-Somotor
(2001)
old backwater
40%
9
295
33.9
2.03
0.64
The highly probable source of the Amur sleeper in eastern Slovakia is the upper part of
the Latorica drainage area, lying in the territory of Ukraine. The occurrence of this species
in the Latorica basin near the town of Chop, Carpathian Ukraine, is reported in an editorial
attached to the article by M o s h u & G u z u n (2002) as well as by L i t v i n c h u k &
B o r k i n (2002). Likewise, K a u t m a n (1999) refers to oral information on the
occurrence of the Amur sleeper in the same region. Considering the ecological
characteristics of this species, which is not a good swimmer, it may be expected that it will
spread mainly from localities lying upstream to those lying in lower parts of the river basin.
Usually, the occurrence of a new species will be observed with some time delay from its
first penetration into the drainage area, the species having already reproduced and occurring
in greater numbers. The rather abundant occurrence of this species which, moreover, shows
a widespread occurrence in the Latorica and Bodrog drainage areas, as demonstrated in
1999 and 2000, would suggest that it had invaded the Latorica drainage area prior to 1998.
One may assume that it was the 1998 floods that contributed to the rapid occupation of the
332
wide areas of the Latorica and Bodrog drainage areas. In that way the species got even to the
original floodplain lying behind the levees. Its rapid spread over the Latorica, Bodrog and
Tisza floodplains was also facilitated by the local amelioration channel system. General
observations on a rapid spread of this species over the Vistula drainage area have been
reported by T e r l e c k i & P a l k a (1999), and over the Volga and Don by B o g u t s k a y a
& N a s e k a (2002). The later spread of the species over the Tisza river basin shows an
identical course, the common occurrence of which has also been reported from Serbia,
besides that in Hungary (G e r g e l y 2002, H a r k a & F a r k a s 2001). The occupation
of a river basin is significantly accelerated by high water levels and the connected floods, as
also reported by E l o v e n k o (1981) and as was the case of the Bodrog and Tisza drainage
areas in eastern Slovakia.
According to our observations, the Amur sleeper in the Tisza riverine system, eastern
Slovakia, is currently confined, to the Latorica, Bodrog and Tisza drainage areas, including
their floodplains and the connected amelioration channel systems (Fig. 1). So far, we have
not ascertained the presence of this species in the lower reaches of the Ondava and Laborec
rivers (tributaries to the Bodrog river). This fact also tends to support the hypothesis that the
species will spread chiefly in a downstream direction within a river drainage area. With
regard to the amelioration channel network in the original floodplains along the lower
reaches of the Laborec and Ondava rivers, one may expect that the Amur sleeper may
penetrate even those areas in the next few years.
The causes why the Amur sleeper is spreading beyond its range are unambiguously
connected with man’s activities. At first, there were intentional introductions of this
interesting species (St. Petersburg 1912, Moscow 1948). Some of the introductions were
connected with utilising the Amur sleeper as a predator of mosquito larvae. A considerable
number of introductions were unintentional, the Amur sleeper being introduced together
with stocking materials of other fish species as their undesired admixture. This consideration
even includes the transport and release of this species by amateur fishermen, and one cannot
overlook even the probable releases of this species from aquarium cultures. At any rate, the
fact that the species has overcome the barriers between river basins is connected with man’s
activities (H a r k a & S a l l a i 1999). For a review of literature on the various aspects of
dispersal of the Amur sleeper, see B o g u t s k a y a & N a s e k a (2002).
What will be the further occurrence of this species in Slovakia? It may be supposed that
through natural migration the Amur sleeper will gradually invade the drainage areas of the
lower reaches of the Ondava and Laborec rivers. Its further spread to additional streams in
the Tisza river basin (the Slaná and Hornád rivers) and further on, eventually to the Danube
basin (western Slovakia) through natural migration, is problematical. A much greater
probability is seen in the species spreading through unintentional introduction with the
stocking material of other fish species, as was the case in the past, e.g. with the dispersal of
Carassius auratus or Pseudorasbora parva. Nor can a transfer by intentional activity of
fishermen be ruled out (bait fish). The Amur sleeper is also suitable for aquarium culture
(M a c h l i n 1957, S c h e n k e & G r a m b o w 1965) and therefore one cannot exclude
the possibility of the species being released into nature from aquarium cultures. The rapid
colonization of the Latorica, Bodrog and Tisza river basins in the territory of Slovakia by the
Amur Sleeper in the course of the past 4–5 years was invasive in character. The Amur
Sleeper shows several biological and ecological properties that are typical of the so-called
invasive fish species. Its reproduction capacity is high (portional spawning, the male
333
guarding the spawned eggs), it is resistant to high water eutrophication, including lack of
oxygen. It is even capable of surviving when frozen in ice, or near drying up. It ingests
animal food of all kinds, including smaller fish and amphibian larvae (K i r p i c h n i k o v
1945, S o k o l o v 2001, B o g u t s k a y a & N a s e k a 2002).
Amur sleeper is of no positive economic importance. It attains a maximum of 250 mm in
total length and up to 250 g in weight but the vast majority of populations consists of
individuals less than 120 mm in total length (B e r g 1949, R e s h e t n i k o v 2000). In some
places it is the object of sport angling (D m i t r i e v 1971, V e r i n 1978, S h l y a p k i n &
T i k h o n o v 2001, N a u m e n k o 2002). The initial intention to utilise this species in the
control of mosquitoes did not bring any significant results (K i r p i c h n i k o v 1945). The
Amur sleeper presents a serious threat to the existence of a number of native fish species
that show identical microhabitat requirements (stagnant waters densely grown with aquatic
plants). As regards food, the Amur sleeper is characterised as a potential predator
(S p a n o v s k a y a et al. 1964). The diet of the Amur sleeper consists of aquatic
invertebrates of all sizes, besides larvae and smaller-sized fish and even amphibians. The
predation of the Amur sleeper on other fish species, including individuals of its own species
as well as fish eggs, is described on a general level by a number of authors
(K i r p i c h n i k o v 1945, N i k o l s k y 1956). S h l y a p k i n & T i k h o n o v (2001)
reported on a total disappearance of Leucaspius delineatus by this species in smaller
reservoirs. Likewise, introduced into reservoirs harbouring a single-species fish stock of
Carassius carassius, the Amur sleeper liquidated all individuals smaller than 40 mm in size
(R e s h e t n i k o v 2000). In the diet of Amur sleepers older than one year, living in the
Baikal Lake basin as well as in the Volgograd Dam Lake, fish eggs and small-sized fish
formed a significant share (L i t v i n o v & O ’ G o r m a n 1996, N a u m e n k o 2002).
Likewise, the trophic competition of the Amur sleeper, considering its voraciousness and
capability to produce very numerous populations, is a negative aspect in relation to native
fish species (L i t v i n o v & O ’ G o r m a n 1996). Here it is necessary to point out that a
diet composition similar to that of the Amur sleeper is also found in Umbra krameri
(L i b o s v á r s k ˘ & K u x 1998). For this species showing similar microhabitat
requirements, the Amur sleeper is a deadly threat even as a predator. The devastation action
of the Amur sleeper has been demonstrated even against amphibian larvae and adults
(M a n t e i f e l & B a s t a k o v 1986, R e s h e t n i k o v 2000, 2001, K a u t m a n
1999). We have observed that being captured, individual Amur sleepers regurgitated
swallowed individuals of their own species up to 40 mm in size. In aquarium environment,
individual Amur sleepers 70–90 mm in total length were observed to prey on goldfish up to
45 mm in total length.
For some fish species native to central Europe (Umbra krameri, Leucaspius delineatus,
Carassius carassius, Rhodeus amarus and the larvae of other species), the Amur sleeper
presents a real threat both as regards trophic competition and as a predator. Pains should be
taken to prevent incidental transport of the Amur sleeper with stocking materials of other
fish species to further river basins.
Acknowledgements
The investigations were implemented and financially supported within the research grant No. 1/9209/02 of the
Grant Agency VEGA of the Slovak Academy of Sciences and the Ministry of Education of the Slovak Republic,
and the research project reg. No. S6093007 of the Academy of Sciences of the Czech Republic.
334
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