Download - Population density and the intensity of paternity assurance behaviour in a monogamous wader: the Curlew Numenius arquata

his (2000) 142, 372-381

Population density and the intensity of paternity assurance behaviour in a monogamous wader: the Curlew

Numenius arquata

DAVE CURRIE & JAR1 VALKAMA' Section of Ecologx Department of Biologx University of Turku, NN-20014 Turku, Finland

We compared paternity assurance behaviour and related displays in high (1.6 pairs per km*) and low (6.7 pairs per km2) density populations of the Curlew Numenius arquata breeding on arable farmland in western Finland. There was little evidence of individuals pursuing extra-pair copulations or males exhibiting paternity assurance behaviour. Furthermore, there was no variation in the frequency of intrusions or in the intensity of paternity assurance behaviour relative to lay date. However, intrusions and approaches to the pair female by extra-pair males were more frequent at high breeding density, and pair males remained closer to their female, followed her more and exhibited a higher frequency of copulatory behaviours in the high-density population. Therefore, high breeding density appeared to increase opportunities for individuals to copulate outside the pair-bond and resulted in more intense male paternity guards. Male song flight displays were also more frequent in the high-density population. Territorial absences by males were infrequent in both areas. The increased frequency of intrusions and interactions between non-pair individuals (male-male and male-female) at high density were probably the major factors in explaining area differences in the intensity of paternity assurance and territorial behaviour.

Although the majority of bird species are monogamous (Lack 1968, Merller 1986), both males and females have been observed copulating outside the pair-bond (59% of 70 studies; Birkhead & Merller 1992). The opportunities for individuals to pursue extra-pair copulations (EPCs) can be influenced by several ecological, demographic and behavioural factors (see reviews in Westneat et al. 1990, Birkhead & Merller 1992). Breeding density is a potentially important ecological factor in determining opportunities for EPCs, as rates of encounters between non-pair individuals are likely to be more frequent a t higher breeding densities (Hatchwell 1988, Merller 199 1 a, Birkhead et al. 1992, Birkhead & Merller 1992). Westneat & Sherman (1 997) found a positive correlation between breeding density and the frequency of extra-pair paternity (EPP) within species, although this was not the case in a cross-species comparison.

Two main paternity guards have been identified in birds: mate-guarding (Beecher & Beecher 1979,

'Corresponding author. Ernail: [email protected]

Birkhead 1979) and high copulation rates (Birkhead et al. 1987, Birkhead & Lessels 1988, Hunter etal. 1992), although the two are not necessarily mutually exclu- sive (Sheldon 1994, Korpimalu et al. 1996). Since male paternity guards can be considered to be the evolutionary corollary of the pursuit of EPCs, they are likely to be more intense when opportunities for EPCs are also high (Merller 1987, Birkhead & Merller 1992).

Although Merller (1 99 1 b) concluded that many shorebirds exhibit mate-guarding behaviour, there are actually few quantitative data detailing this phenome- non in monogamous species (but see Heg et al. 1993, Pierce & Lifjeld 1998, Byrkjedal & Thompson 1998). The Curlew Numenius arquata is a large, long-lived, territorial shorebird, typically found on farm- and moorland in northern Europe (Cramp & Simmons 1983). There is considerable paternal investment in each breeding attempt: males set up and defend a territory, and although both parents incubate, offspring desertion by females has been observed from halfway through the fledging period (approximately 35 days) while males usually remain with chicks through to near independence (Cramp & Simmons 1983,

0 2000 British Ornithologists' Union

Paternity guards in the Curlew 373

Valkama 1999). Species which exhibit a high level of paternal investment should exhibit paternity assurance behaviour (Birkhead & M~iller 1992). We investigate behavioural evidence for paternity assurance behaviours in the Curlew. We also examine the effect of

were not used when plotting territory boundaries. The number of neighbouring territories was measured by observing boundary interactions between focal and neighbouring males.

breeding density on the rate of intrusions, the pursuit of EPCs and the intensity of guarding behaviours. Behavioural observations

METHODS

Study areas

The study was carried out in two arable farmland areas separated by 200 km in western Finland between April and May (1996-97): Vammala (ca. 61"N 22"E) and Kauhava (ca. 63"N 22"E). Vammala comprises a patchwork of small agricultural areas (usually less than 5 km*) separated by woodland, farms and small vil- lages, while Kauhava is part of a larger uniform flat farmland area (100 k m 2 ; for more details see Korpimaki & Norrdahl 1991). However, Curlew breeding habitat is very similar as both areas are inten- sively cultivated and the predominant habitat type is tillage (69%; Valkama et al. 1998).

Trapping adults

Adults were trapped at the nest during the last two weeks of incubation using a drop-trap or walk-in trap (90%: 74/82 during the last week of incubation), sexed on the basis of morphometric characteristics (Cramp & Simmons 1983, Berg 1992, Ylimaunu et al. 1996) and individually colour-ringed. In addition, we calculated two measures of body condition: [weight (9) x ]Oh]/

tarsus (mm)3 after Petrie (1983), and [weight (g) x lO5]/ wing(mm)3.

Both members of the pair were simultaneously observed from soon after pairing through to the onset of incubation. In the Curlew, eggs are laid every 24-48 hours (Cramp & Simmons 1983) and incubation typically commences on the laying of the third egg (Ylimaunu & Ylimaunu 1984). Individuals were observed from 100-1 50 m using binoculars between 05:OO-2O:OO h. In 1996, focal pairs were observed for between 30-60 minutes every 3-4 days (as part of another study), while in 1997 individuals were observed for one hour every second day. Watches that had less than 30 minutes of data were excluded from the analyses. The mean number of hours of observation per territory (f se) was 1.90 f 0.14 h in 1996 (on average 3.5 observations per territory) and 4.76 f 0.26 h in 1997. Observations ceased when only one adult was observed on territory (which indicated that the other member of the pair was incubating).

During behavioural observations we noted: (i) intra-pair distance (m) every minute; (ii) the proportion of female flights which were followed by the pair male; (iii) the frequency of copulatory related behaviours, specifically male approaches (which involved the pair male either flying directly to, or walking after their mate), solicitations and copulations; (iv) the frequency of song flights; and (v) the number of intrusions, defined as individuals other than members of the pair observed within territory boundaries. In 1997, we also noted responses by members of the pair to intruders and timed the duration of song flight displays to the nearest second.

Measuring population density and territory size Two types of intrusion were observed: (i) terrestrial, Both areas were surveyed every 2-3 days from mid- April until the end of May. We noted the number and location of displaying males (including unpaired territorial males) and pairs. We then compared this with the number and location of nests found and number of pairs known to have failed, from which we calculated a number of territories per k m 2 (mean over two years). Territory size was obtained by plotting the position of boundary disputes and the outermost observations for focal pairs during behavioural observations (see below) on a scale map (1 : 10 000) and connecting these points to form a minimum convex polygon. As aerial &splays occurred over territories other than the owner's they

where the intruder landed on the focal territory and (ii) aerial, during which non-pair individuals were observed flying above the focal territory. The majority of terrestrial intruders were identified from colour- rings (as some individuals had been trapped in previous years) or observing individuals either leaving or returning to their own territory. In addition, although the sexes are identical in plumage, females are consider- ably larger than males (Cramp & Simmons 1983, Berg 1992, Ylimaunu et al. 1996). We were able to sex some intruders by comparing their overall body size and bill length to that of members of the focal pair. During aerial intrusions, it was not possible to sex or

@ 2000 British Ornithologists' Union, Ibis, 142, 372-381

374 D. Currie & J. Valkama

identi@ the majority of individuals reliably, although it was possible to identify some indiiTiduals by observing them either leaving or returning to territory and on the basis of behaviour, e.g. only males \\.ere observed to perform song flight displays during the behavioural observations.

Calculating egg volume and first egg dates

Curlews arrived in mid- to late April in both areas and first eggs were usually laid in the first two weeks of May. Nests were usually found after clutch comple- tion, typically during the first two weeks of incubation. Egg lengths and breadths were measured to the nearest millimetre, and egg weight was measured to the nearest gram. Egg volume was estimated after Currie and Valkama (1998)’ and a mean egg volume was calculatcd for each nest. For nests that survived through to hatching we back-calculated first-egg dates (FEDs) from hatching dates after Berg (1992). In 1997, egg dimensions and iceights were measured on each nest visit (maximum of three nest visits between finding the nest and hatching) and egg density (g/mm3) was calculated after Hoyt (1976, 1979). From the regression of mean egg-density index (per clutch) versus hatching date we were able to predict hatching dates for clutches that did not survive through to hatching (number of days to hatching = 273203.63 x [mean density of clutch] - 115.03; see also Robson et ill. 1995, Grant 1996). Predicted hatching dates were used fbr one nest in the high-density population and sevc‘n nests in the low-density area in 1997 respectively. Furthermore, since the Curlew is a long-lived species and exhibits a high degree of mate and territory fidelity between years (Berg 1994, pers. obs.), analyses of breeding success data were considered separately by year to avoid pseudoreplication. Measures of breeding success only include data on first broods and esclude relays and second broods.

Data analyses

Data tor intensity of behaviours are presented for 17 territorics in thc low-density population (nine in 1996 anti eight in 1997) and 20 territories in the high- density population (eight in 1996 and 12 in 1997) Data to1 territories from which we did not obtain FED5 arc exJuded from the analyses Two instances of thc sanw p m on the 5ame territories were obserced in 1 ‘VJ6 and 1 W 7

To tr5t for ditferences in the intensity of behaviours hetween areas and relative to FED (day 0), we com-

pared mean values for each behaviour for focal pairs in three arbitrarily assigned periods using repeated- measure ANOVA (hereafter referred to as ANOVAR). These time periods were: (i) ‘after pairing’ (days prior to day -5; 26% of observations); (ii) ‘before laying’ (day -5 to -1; 40% of observations); and (iii) ‘after laying’, but prior to the onset of incubation (34% of observations). In ANOVAR (model: behaviours versus density [high or low]), intrusion rates, song flights and intra-pair distance were log-transformed. Due to non- normality of data even after transformation, other behaviours were analysed on an area basis using Friedman two-way ANOVAS. For behaviours analysed with non-parametric ANOVAS in which there was no pattern relative to FED, we compared means for the respective behaviours for all focal pairs for the complete duration of behavioural observation (soon after pairing until the onset of incubation) between areas using univariate non-parametric statistics (Mann-Whitney U-tests) .

There were numerous missing cells in the ANOVAR

and complete data sets were only available for 35% of territories (1 3/37; seven a t high-density and six at low density). Since so many data were excluded from these analyses, we re-analysed the data with factorial ANOVAS; two-way ANOVAS (behaviour versus density and reproductive stage) for normally distributed data and Kruskal-Wallis one-way ANOVAS (behaviour versus reproductive stage) for non-normally distributed data. The data were not independent in these analyses (data from same pair are considered more than once); however, we only used these ANOVAS, which utilized all our data, to compare the results obtained using ANOVAR which were based on a small subset of our data. The conclusions from ANOVAR and factorial ANOVAS were the same for all analyses, and results are only presented for ANOVAK. Statistical tests are two- tailed and follow Siege1 and Castellan (1988) and Sokal and Rohlf (1981). Data were analysed using Statview 5 12“’ (Abacus Concepts 1988). Inter- actions in ANOVAR are non-significant unless other- wise stated.

RESULTS

The southern study area (Vammala) had a much lower breeding density than the northern area (Kauhava; 1.6 pairs per k m l versus 6.7 pairs kmz), and therefore territory size and inter-nest distance were both smaller in the high-density population (Table 1). However, breeding chronology was similar in the two areas, and there was no significant difference in distribution

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Table 1. Breeding parameters of high and low-density population (means f se). Data on territory size and inter-nest distance are from 1996-97, and data on number of neighbouring territories are from 1997. Sample sizes are given in parentheses.

Territory size (ha) Inter-nest distance (m) No. of neighbouring territories Clutch size

1995 1996 1997

1995 1996 1997

Egg volume (cm3)

*Mann-Whitney U-tests. **P < 0.01,

High density Low density t

12.10 f 1.10 (25) 321 5 5 * 28.6 (60)

3.67 f 0.19 (14)

3.67 f 0.16 (18) 3.79 f 0.08 (28) 3.94 f 0.04 (32)

67.68 k 1.75 (17) 66.87 k 1.1 1 (23) 71.63 rt 0.87 (32)

28.80 f 2.6 (37) 706.55 f 43.70 (58)

2.22 f 0.32 (1 1)

3.72 f 0.08 (32) 3.67 f 0.1 1 (39) 3.68 f 0.13 (25)

69.77 f 1.26 (20) 68.33 f 1.18 (29) 72.07 f 1.20 (25)

5.23** 7.6W 3.17*'

-0.21 -0.32 -1.95

-0.95 -0.31 -0.39

of lay dates of first broods between populations (Kolrnogorov-Smirnov two sample test; 1996: high density [n = 221 versus low density [n = 171, D,, = 0.278, ns; 1997: high density [n = 311 versus low density [n = 241, D,, = 0.271, ns; 1996-1997: high density [n = 531 versus low density [n = 411, D,,, = 0.23, ns). Furthermore, there was no significant difference in clutch size and mean egg volume (Table 1) or in adult size and body condition (Table 2), between the two populations.

Intrusions

Territory intrusions were typically of short duration, usually less than one minute. Ninety-one percent (41/45) of intruders were identified as males (73% on the basis of colour-rings and observing intruders returning to their own territory, and 27% using a combination of behaviour and morphometric characteristics). The remainder could not be sexed reliably.

There was no significant difference in the frequency of terrestrial intrusions relative to FED (ANOVAR,

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Figure 1. Territorial intrusions (mean f se) versus reproductive stage. An overall mean for the three time periods is also shown. D, High density; 0, low density. There was no temporal difference in the rate of intrusions, but intrusions were more frequent in the high-density population. Statistics are given in text. Sample sizes denote number of territories.

within-subject effect, F2,22 = 0.79, ns; Fig. 1). Rates of intrusions prior to the onset of incubation were signif-

Table 2. Adult characteristics (mean f se) in high and low-density populations (1 995-97). Sample sizes are given in parentheses. Two- way ANOVAS (adult characteristic versus sex and density) were used to compare adult characteristics between areas. F-values for density are shown.

Male characteristics Female characteristics

High density Low density High density Low density F-value P

Tarsus* (mm) 79.09 rt. 0.59 (30) 80.87 f 0.71 (13) 84.89 f 0.69 (10) 82.96 k 1.08 (5) 0.06 0.80 Wing (mm) 297.65 f 0.65 (37) 296.22 f 1.57 (22) 307.70 f 2.23 (10) 310.40 f 1.70 (13) 0.24 0.62 Weight (9) 662.52 f 7.22 (37) 645.67 f 14.93 (21) 799.20 f 18.96 (10) 765.20 f 25.97 (12) 0.25 0.62 BC1 13.64 f 0.33 (30) 12.10 f 0.47 (12) 13.09 f 0.38 (10) 13.43 f 0.62 (5) 1.24 0.27 BC2 2.52 f 0.04 (37) 2.50 f 0.07 (21) 2.74 k 0.04 (10) 2.68 f 0.05 (12) 0.49 0.49

*Data on tarsus only available 1996-97. BC1 = [weight x 104]/tarsus3, BC2 = [weight x 105]/wing3.

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icantly higher in the high-density population (ANOVAR, between-subject effect, F , ,, = 7.72, P < 0.01; Fig. 1).

Eighty-two percent (24/34) of territory intruders in the high-density area and 85Yo (6/7) in the low- density area were identified, the majority of which were nearest neighbours: 95010 (23/24) and 100% ( 6 4 in the high and low-density populations respectively. Since nearest neighbours of focal territories were usually colour-ringed, unidentified intruders probably came from more distant territories or were non- territorial individuals. Although it was not possible to sex or identify the majority of individuals reliably during aerial intrusions, on the basis of behaviour and vocalizations most appeared to be males (39%: 7/18 were identified as neighbouring males by observing individuals leaving or returning to their own territory).

Intrudcrs were not observed feeding during terrestrial intrusions and were normally chased off by the pair male. On average, 51% of all intruders (aerial and terrestrial combined) in 1997 were chased, however more terrestrial than aerial intruders were chased by the pair male (73% versus 33%; chi-squared test, x’ = 6.85, P < 0.01; data on both populations combined).

In the high-density population, intruding males were more frequently observed approaching the pair female than in the low-density area although the difference was not significant (Fisher exact test, P = 0.17); 2 1 Yo

(8/37) of intrusions in the high-density population involved the extra-pair male approaching the female while none were observed in the low-density area. No extra-pair copulations were observed during these approaches, but in three instances the intruding extra- pair male was observed to perform the wing-lift display, which we interpret as a male solicitation display, and which is frequently observed prior to copulation (Cramp & Simmons 1983). Furthermore, one of these approaches involved the intruding male interrupting a within-pair copulation. Eighty-eight percent 17/83 of approaches in the high-density area were by neighbouring males (the majority of which were paired; 677) and occurred between days -5 and 3, usually near the territory boundary of the respective extra-pair males, but within the territory of the focal pair. ‘I’hc pair female either flew away from, or responded aggressively to, approaches and solicitations by extra-pair males.

Territory absences

On several occmons focal males were observed to fly off-tcmtory Females were not observed to leave

territory prior to the onset of incubation. Some of these absences involved males intruding onto neighbouring territories, but males were also observed to fly out of sight (more than one territory away). Male absences from territory were observed between days -4 to 4 (day 0 = FED). There was no difference in the frequency or duration of territorial absences between areas (eight observed at low density, five at high- density). The mean duration of absences (+ se) was 13.8 k 3.7 minutes (n = 10; the durations of three absences were not noted).

Male displays

Paired focal males usually displayed within their territory boundaries/airspace, although unpaired non- focal individuals were occasionally observed displaying off-territory. Rates of display differed relative to FED, and were highest immediately after pairing in both areas, but declined before and during laying (ANOVAR, within-subject effect, F,,,, = 8.38, P < 0.01; Fig. 2a). Song flights were more frequently observed in the high-density population (ANOVAR, between-subject effect, F,, , , = 5.47, P < 0.05; Fig. 2a3, although their duration was longer in the low-density population (mean duration of song flights in seconds k se; high density = 31 k 3 [data from eight males]; low density = 63 k 13 [data from six males]; Mann-Whitney U-test, z = 1.98, P < 0.05).

On average, 40% of song flights were responses to intruders (both terrestrial and aerial); 43% a t high density versus 25O/o at low density (chi-square test, x 2 = 0.92, ns). There was also a weak correlation between the mean rate of intrusions (terrestrial and aerial combined) and mean display rates in the high-density population (r3 = 0.43, n = 20, P < 0.07). However, song flights were still more frequent in the high-density area even when we controlled for the number of male displays initiated in response to intrusions (ANOVAR, between-subject effect, Fl,9 = 7.63, P < 0.05; Fig. 2b). Furthermore, rates of these ‘spontaneous’ displays also declined soon after pairing (ANOVAR, within-subject effect, F,,,, = 4.13, P < 0.05; Fig. 2b).

Male-female proximity and copulatory behaviours

There was no pattern in intra-pair distance or male following behaviour relative to FED in either of the populations (intra-pair distance, ANOVAR, within- subject effect, F,,,, = 0.1 1, ns; male following behaviour, Friedman two-way ANOVA, both tests, ns;

0 2000 British Ornithologists’ Union, Ibis, 142, 372-381


a

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A3er Before After Overall pairing laying laying mean

Figure 2. Male song flights (mean f se) versus reproductive stage; (a) total song flights and (b) song flights excluding displays initiated in response to intruders (data from 1997 only). W , High density; 0, low density. An overall mean for the three time periods is also shown for each behaviour. The frequency of song flights (total and excluding displays to intruders) declined soon after pairing in both high- and low-density areas. Song flights were more frequent in the high-density population. Statistics are given in text. Sample sizes denote number of territories.

Fig. 3). However, intra-pair distance was shorter and male following behaviour was more intense in the high-density population (intra-pair distance, ANOVAR, between-subject effect, F,,,, = 4.86, P < 0.05, Fig 3a; male following behaviour, z = 2.92, P < 0.01; Fig. 3b). In general, female flights were rare (84 flights vs 230 male flights, excluding song flights) and occurred within territory boundaries.

There was no significant pattern in the intensity of copulatory-related behaviours relative to FED in either area (Friedman two-way ANOVA, all tests, ns; Figs 4 a - 4 ~ ) . In general, copulatory behaviours were more intense in the high-density population (approaches: z = 2.03, P < 0.05, Fig. 4a; solicitations:

z = 1.82, P < 0.1, Fig. 4b; copulations: z = 2.43, P < 0.01, Fig. 4c). The majority of copulatory related behaviours in both populations occurred between 05:OO-09:OO h; 72% of approaches, 70% of solicitations and 82% of copulations. However, there was no significant difference in intra-pair distance, the intensity of male following behaviour, and rate of song flights or intrusions, between the morning or afternoon or relative to the diurnal peak in copulatory behaviours (Wilcoxon-paired sign rank test, all tests, ns).

DISCUSSION

Considering the substantial paternal investment in the Curlew, there was surprisingly little evidence of male

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Figure 3. Intra-pair distance (m) and proportion of female flights followed by the pair male (mean k se) versus reproductive stage. W , High density; 0, low density. An overall mean for the three time periods is also shown for each behaviour. There was no temporal difference in intra-pair distance or the intensity of male following in either high or low density areas. Intra-pair distance (a) was less and male following behaviour (b) was more intense in the high-density population. Statistics are given in text. Sample sizes denote number of territories and are the same for (a) and (b).



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Figure 4. Copulatory related behaviours (mean i: se) versus reproductive stage: (a) male approaches (data from 1997 only); (b) solicitations; and (c) copulations. D, High density; 0, low density. An overall mean for the three time periods is also shown for each behaviour. There was no temporal difference in the frequency of copulatory behaviours, but they were more frequent in the high-density population than in the low density area. Statistics are given in text. Sample sizes denote number of territories and are the same for (b) and (c).

paternity assurance behaviours (see also Pierce & Lifjcld 1998). This \\'as perhaps expected in light of

the low number of intrusions and extra-pair interactions. However, male displays and behaviours associated with paternity assurance were more frequent a t high density and corresponded with a higher number of intrusions and interactions between non-pair individuals.

Intrusions

The majority of territorial intruders were nearest neighbours, and the proximity and higher number of neighbouring territories probably accounted for the increased rate of intrusions in the high-density population (Table 1). The majority of these intrusions only involved extra-pair males temporarily visiting focal territories before being chased away by the pair male. Curlews may occasionally forage off-territory (Cramp & Simmons 1983, pers. obs.), but in this study individuals were never observed to feed during these incursions, although this may mean that intruders were searching for better foraging areas. Furthermore, if this were the case there is no obvious reason why it should only be males that were identified as intruders or observed leaving focal territories prior to the onset of incubation. The majority of intrusions were also not targeted towards the pair female, or timed to coincide with either first-egg dates or the diurnal peak in copulatory behaviours, as might be expected if they were exclusively a means of gaining EPCs. Intrusions by neighbours may also be attempts to extend territory boundaries and/or test the response of surrounding territorial males, while non-local intruders, with presumably less knowledge of territory boundaries, could use responses by conspecifics to their incursions to determine whether an area is already occupied.

The difference between the duration of intrusions and that of territorial absences ( I min versus 13 min) suggests that in some instances males may be visiting either more than one territory and/or more distant territories, and not just nearest neighbours. Although intrusions were more frequent in the high-density area, there was no difference in the frequency or duration of territory absences between areas. I t appears that high intrusion rates were probably a consequence of high breeding density (i.e. a density-dependent effect) and not a result of individual males in the high-density population spending more time off-territory.

The rate of interactions between non-pair individuals is dependent on several ecological factors (Westneat et al. 1990, Birkhead & Mdler 1992, Westneat & Sherman 1997); however, with the excep- tion of density, there were few ecological differences

6 2000 British Ornitnologists Union Ibis, 142, 372-381


between the two study populations. First, individuals bred on similar habitat (arable farmland dominated by tillage) and there were no significant differences in habitat composition of territories or in food avail- ability between areas (Valkama et al. 1998, Currie & Valkama 1998). Secondly, there were no obvious area differences in breeding biology because breeding synchrony (distribution of lay dates), clutch size, and egg volume were all similar at high and low density. In addition, there was no indication that the sex ratio was more male skewed in the high-density population due to the presence of unpaired territorial males. Thirdly, body size and body condition of Curlews did not differ significantly between the two populations (Table 2). Fourth, adult predation was very low in both populations (only two to three adults are known to have been taken in 1995-97) and the densities of two main predators of adult Curlews (Goshawk Accipiter gentilis and Eagle Owls Bubo bubo) were similar in the two areas (Saurola 1985, Vaisanen et al. 1998). Therefore, although intrusions (as well as territorial and certain paternity assurance behaviours) are conspicuous, it seems unlikely that predator avoidance behaviour can account for the marked behavioural differences observed between the two populations.

An important premise in this study is that we were able to measure intrusion rates accurately in both areas. During behavioural observations it was possible to observe most of the focal territory. However, some intrusions may have gone undetected, particularly in the low-density population due to larger territory size, resulting in an underestimate of their frequency. Since males chased the majority of territorial intruders (73%), it is unlikely that enough could have gone undetected to account for a 4.5-fold area difference in intrusion rates, especially due to the open nature of the farmland and the good visibility of territories this allowed. Therefore, although we cannot exclude the possibility that density and behaviour may be functions of an as yet unidentified variable, there were few obvious confounding factors which could explain the significant area difference in male intrusion rates other than the increased proximity of individuals due to higher breeding density.

Paternity assurance behaviours

In the few studies which have examined alternative reproductive strategies in monogamous waders, extra- pair copulations (EPCs) typically occur a t a low frequency ( e g Oystercatcher Haematopus ostralegus, Heg et al. 1993) or not at all (e.g. Purple Sandpiper

Calidris maritima, Pierce & Lifjeld 1998; Golden Plover Pluvialis apricuria, Byrkjedal & Thompson 1998). Similarly, EPCs have not been reported in the Curlew, and none was observed in this study even in the high-density population. However, there was some evidence to suggest that higher breeding density increased the opportunities for both sexes to pursue additional matings; 4.4-times higher intrusion rates, 21 Yo of which resulted in extra-pair males coming into direct contact with, and approaching or soliciting, the pair female. Furthermore, the intensity of behaviours frequently associated with male paternity assurance was higher in the high-density population.

Guarding behaviours are generally characterized by the pair male remaining close to and following the pair female during the fertile period (Beecher & Beecher 1979, Birkhead 1979). We have no data on the duration of the fertile period in the Curlew. However, since behaviourally successful copulations were observed up to 12 days prior to the FED, and female storage of viable sperm for more than one month has been documented in waders (Oring et al. 1992), females may be fertile very soon after settling on territory, especially in light of the short prelaying period of approximately two weeks. A short pre-laying period could also account for the lack of variation in the intensity of paternity assurance behaviours (or intrusions) relative to time of laying.

Shorter intra-pair &stances were not unexpected in the high-density population due to smaller territory size (Table 1) and therefore cannot necessarily be interpreted as a form of paternity assurance. Furthermore, as it would presumably be easier for males to monitor the location and/or behaviour of the pair female in a small, rather than a large, territory then male following behaviour should be more intense in the low-density population. The fact that male following behaviour was more intense in the high- density population, and corresponded with a higher frequency of copulatory-related behaviours and intrusions, is consistent with a perceived increase in sperm competition by the pair male (Birkhead 1979). However, the intensity of paternity assurance behaviours even in the high-density population was much less intense than observed in other monogamous bird species (Birkhead & Maller 1992) and reflects the relative rarity of intrusions and extra-pair males coming into contact with the pair female. Open habitats (farmland in this study), at least in passerines, are also associated with low intensity of paternity assurance behaviours (Sundberg 1992, Shepherd et al. 1996, Currie et al. 1998). The very few opportunities


380 D. Currie & J, Valkama

for males to gain additional matings appeared to be limited to neighbours, and was probably a consequence of smaller territories and higher number of neighbouring males than in the low-density population (Table 1). ln addition, since females avoided contact with extra- pair males, the threat to a male's paternity, even at high breeding density, appeared to be low.

intensity of territorial and paternity assurance behaviours in this study.

We thank Tapio Eeva, Ian Hartley, Erkki Korpimaki, Dave Parish, Roland Redmond, Vesa Ruusila, Brett Sandercock, Des Thompson and Jurgen Wiehn for advice and comments on the manuscript. DC was supported by the Kone Foundation and Turku University's Section of Ecology (Department of Biology). J.V. was supported by the Maj and Tor Nessling Foundation. Male displays

REFERENCES Male display rates were observed to decline soon after Dairing. This combined with anecdotal observations of both unpaired and widowed males exhibiting higher rates of display than paired males, indicates that song flights were involved in mate attraction (Cramp & Simmons 1983). Song flights have also been suggested as a male advertisement for EPCs and/or additional females (Carlson et al. 1985, M d e r 199 1 c), for which the scope is potentially higher a t increased breeding densities. However, there was no evidence of polygamy a t either study site.

A large percentage of displays (40%) were in response to intrusions and there was a weak correlation in the high-density population between the frequency of intrusions and male display rates, which also indicates that song flights had a role in territorial defence. Higher intrusion rates may therefore explain the more frequent displays observed in the high- density population. However, even when displays performed to intruders were excluded, song flights were still more frequent in the high-density population. More frequent male displays may be required at higher breeding densities to maintain the territorial integrity due to the increased competition for space under such conditions. There was limited evidence that song flights were used directly as a paternity guard, since their frequency declined soon after pairing, although territoriality has also been proposed as an additional (supplementary) paternity guard (Mdler 1990). Since Curlews are faithful to site and mate, it is possible that some displays and behaviours observed may be involved in re-establishing and main- taining the pair-bond between years.

In conclusion, the higher frequency of intrusions and intrrac tions hetween non-pair individuals (male-male and male-female) at high density appeared to be a

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Received 16 November 1998; revision accepted 27 June 1999

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