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Colony Development and Density-Dependent Processes in Breeding Grey Herons

Colony Development and Density-Dependent Processes in Breeding Grey Herons Hindawi Publishing Corporation International Journal of Zoology Volume 2013, Article ID 404065, 10 pages http://dx.doi.org/10.1155/2013/404065 Research Article Colony Development and Density-Dependent Processes in Breeding Grey Herons Takeshi Shirai Department of Biology, Tokyo Metropolitan University, Minamiosawa 1-1, Hachioji, Tokyo 192-0397, Japan Correspondence should be addressed to Takeshi Shirai; ardea@k00.itscom.net Received 14 December 2012; Accepted 8 January 2013 Academic Editor: Eugene S. Morton Copyright © 2013 Takeshi Shirai. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The density-dependent processes that limit the colony size of colonially breeding birds such as herons and egrets remain unclear, because it is difficult to monitor colonies from the first year of their establishment, and the most previous studies have considered mixed-species colonies. In the present study, single-species colonies of the Grey Heron (Ardea cinerea) were observed from the first year of their establishment for 16 years in suburban Tokyo. Colony size increased aeft r establishment, illustrating a saturation curve. The breeding duration (days from nest building to fledging by a pair) increased, but the number of fledglings per nest decreased, with colony size. eTh reproductive season in each year began earlier, and there was greater variation in the timing of individual breeding when the colony size was larger. The prolonged duration until nestling feeding by early breeders of the colony suggests that herons at the beginning of the new breeding season exist in an unsteady state with one another, likely owing to interactions with immigrant individuals. Such density-dependent interference may aec ff t reproductive success and limit the colony size of Grey Herons. 1. Introduction colony sites appears to be unimportant in determining the reproductive success or survival in most species [5, 6]. Instead Wading birds such as herons and egrets nest in colonies in of tracking yearly changes in a single colony, intercolonial relatively limited areas and at high density, oeft n reaching comparisons in the same year are useful to detect density- hundreds or thousands of pairs [1]. Herons and egrets are dependent processes, and such comparisons have been con- usuallyquitelargebirds,andthedynamicsoftheirpopulation ducted in herons and egrets. Results have shown that final attract much attention, as estimating the number of breeding breeding success is negatively correlated with colony size pairs is easier in colony-breeding birds than in noncolony in Grey Herons (Ardea cinerea)inBelgium [7]and Great breeders. Population u fl ctuations may be caused by density- Blue Herons (Ardea herodias)inCanada[8]. However, in dependent and density-independent processes, although the Grey Herons in northern Poland, breeding success increases two are not mutually exclusive. with colony size [9]. Different conditions within each colony Density dependence is a negative feedback between habitat, such as the distance to feeding sites and predation population growth rate and population density [2]. In a risks, may cause opposing results for the relationship between White Heron (Egretta alba)colony, themeannumberof colony size and breeding success. fledglings per nest decreased as the number of nests in the Density-independent factors have also been suggested colony increased, suggesting a density-dependent response to affect the population u fl ctuations of herons and egrets. [3]. The first egg-laying date was delayed when colony size Unpredictable factors such as cold weather, high winds, was large in a Purple Heron (Ardea purpurea)colony[4]. disease, food shortage, and human impacts can explain However, little unequivocal evidence shows that density- reducedbreedingsuccess andincreased mortalityinsome dependent factors regulate population u fl ctuations of wading regions without invoking density-dependent mechanisms birds, because intraspecific competition for breeding and 2 International Journal of Zoology [5, 10, 11]. In particular, winter temperature is known to aeff ct 2.2. Observations. After colony establishment was first noted populations of herons and egrets via increased mortality [12– at Renkoji in mid-1996 [28], the herons were observed 15]. Winter temperature also aeff cts the onset of the breeding systematically beginning from the next year (1997) using season in Grey Herons [16–19]. binoculars (×10) and a spotting scope (×20–60; TSN-1, Kowa, Short-term studies are suboptimal for detecting the Nagoya). Herons that stayed in their nests were identified effects of density on the dynamics of wading bird populations, to species. I monitored the typical behavior of breeding because birds are long-lived and breed annually [1]. Even individuals (nest building, incubation, or guarding) and the in the several long-term studies conducted to date, census number and body size of chicks (small, medium, or large), if data were not recorded beginning with colony establishment present, at intervals of 3–7 days in 1997 and every 7–10 days but with mature colonies (e.g., [10–12, 20–23]). eTh tendency in 1998–2000. In 2000, the 49 breeding pairs of this colony of wading birds to form mixed-species groups has posed haddisappeared by late April, andnoheronswereobserved another difficulty for detecting density-dependent processes aer ft wards. However, 14 pairs were observed making nests in colony size regulation; in these cases, both intra- and inter- since late March in 2000. er Th efore, I continued to census specific interactions aeff ct individual behavior and survival this consecutive colony at intervals of 7–10 days in 2001, [24, 25]. butatintervals of 3-4daysin2002–2008 and7days in In the present study, to simplify the factors affecting 2009–2011. From the census data, the breeding and nestling density-dependent processes of colony breeders, a single- feeding durations of each nest were calculated as the period species colony of Grey Herons was selected and monitored from the day that nest-building behavior was rfi st recorded for 16 years beginning at its establishment. I investigated until fledging was completed (all fledglings disappeared in the long-term population fluctuation patterns in this colony the nest) and the period from ending incubation (judged and examined density-dependent phenomena based on indi- from continuous standing of parents) to complete fledging, vidual breeding behavior and reproductive successes in respectively. If predation occurred in the efi ld, the predators the colony. With respect to density-independent factors, I were identiefi d and recorded. examined how winter temperatures aeff ct colony size and To examine the eeff cts of winter temperature on popula- individual breeding behavior. tion u fl ctuations and the timing of breeding, air temperatures were used from public data recorded by the automated meteorological data acquisition system of the Japan Meteo- ∘ 󸀠 ∘ 󸀠 rological Agency at Fuchu, Tokyo (35 41 N, 139 29 E), located 2. Methods 8.4 km northeast from Tama Zoological Park. eTh minimum 2.1. Study Animal and Study Sites. eTh breeding range of value among the mean 10-day temperatures recorded from Grey Herons covers most of the Old World south of the December 1 to January 31 was used as the coldness value Arctic Circle, including Europe, Africa, Asia, and the East starting thebreedingseasonineachyear. Indies islands to Wallace’s Line [1]. Aeft r the breeding season, Some unintended effects of observations on breeding generally when the young can fly, they disperse in all direc- heron behavior have been identiefi d [ 29, 30], particularly tions [1]. Therefore, the nonbreeding range expands outside researcher visits to colonies during nest building and early incubation, leading to abandonment of nests [31]. Artificial of the breeding range. eTh se birds are sedentary and widely distributed in Japan [26]. eTh y feed on a variety of aquatic effects on heron behavior may be negligible in this study, animals such as sh, fi amphibians, crustaceans, insects, and because census observations were made carefully and far from the nests to avoid disturbing the herons, and because worms [1]. Feeding sites include ponds, lakes, rivers, marshes, andseashores(shallowtidalbays),andtheyoeft nusearticfi ial the nests were so high in the trees that any eggs in the nests water environments such as rice elds, fi sh fi farms, parks, and were not examined. dams [27]. In 1996, a breeding colony of Grey Herons became estab- ∘ 󸀠 lished at a hillside at Renkoji in suburban Tokyo (35 39 N, 3. Results ∘ 󸀠 139 28 E); this was selected as a long-term monitoring site. This site is located near the Oguri-gawa River where it just In 2001 and 2002, eight and two pairs of Black-Crowned joins the Tama-gawa River. eTh colony (250 m along the Night Herons (Nycticorax nycticorax) were found, respec- major axis, 80 m along the minor axis) was located in a tively, in the Tama Zoological Park Grey Heron colony. The small area of woods surrounded by houses in a newly built park staff also reported that this colony included at least town. eTh woods mainly consisted of Quercus serrata and Q. 13 nests of Black-Crowned Night Herons in 2000 [32]. In acutissima and some Pinus densiflora . In 2000, however, the all other years, only Grey Herons nested within the colony. colony abandoned this site and relocated to a new breeding The number of nests used by the pairs increased annually ∘ 󸀠 ∘ 󸀠 site on a hilltop in Tama Zoological Park (35 38 N, 139 24 E), aer ft colony establishment at Renkoji but tended to become located about 5 km west of Renkoji along the Tama-gawa saturated aeft r about 10 years ( Figure 1). The mean duration River. In the zoo, woods are patchily distributed, and the of breedingbyeachpairrangedfrom99.1to129.0 days,and Grey Herons useanarea(290m alongthe majoraxis, the mean duration of nestling feeding ranged from 53.6 to 67.8 220 m along the minor axis) consisting of Quercus serrata, days (Table 1). eTh proportion of successful nests that fledged Q. acutissima, Carpinus tschonoskii, Prunus jamasakura,and was 62.6%–85.3%, excluding all that were unsuccessful by the Pinus densiflora . abandonment of the site in 2000 (Table 1). The maximum International Journal of Zoology 3 snake Elaphe climacophora (𝑁=1 )and thejunglecrow Tama zoological park Corvus macrorhynchos (𝑁=14 ). 80 Renkoji 4. Discussion 4.1. Density Dependence. The Renkoji site was abandoned 4 years aer ft establishment and the colony relocated to a Year new site in Tama Zoological Park close to Renkoji along the Tama-gawa River. Higher rates of nest mortality lead Figure 1: Yearly changes in the number of nests in the Renkoji to significant decreases in colony size, and breeding colony and Tama Zoological Park colonies. In 2000, the Renkoji site distributions oeft n shift in association with these reductions was abandoned, and a new colony was established at the Tama in colony size [33, 34]. For example, a colony of Great Blue Zoological Park close to Renkoji. Herons at Pender Harbour, British Columbia, abandoned their site after 2 years of high predation by Ravens ( Corvus corax), Bald Eagles (Haliaeetus leucocephalus), and probably raccoons (Procyon lotor)[8, 35]. Heavypredation maythus number of fledglings was four, and the mean number of force colony abandonment by herons. In the study popu- fledglings per successful nests ranged from 1.8 to 3.1 ( Table 1). lation, however, predation was rarely observed. eTh snake eTh date that the rfi st pair(s) began to breed in the colony Elaphe climacophora and the crow Corvus macrorhynchos differed from year to year, ranging from January 4 to March were theonlypredators of eggs andchicksrecordedinthe 3(Table 1). eTh mean start date of breeding by pairs also present study. Colony nesting of birds sometimes damages differed yearly, and the coefficient of variation (CV) in the vegetation, mainly by altering soil nutrient concentration [36, start date of colony members ranged from 20.8% to 55.6% 37]. Vegetation degradation may cause shifting the colony (Table 1). site [38]. In this study, however, obvious change in vegetation For the effect of colony size on breeding parameters occurred for 16 years even at the central part of colonies. us, Th (Figure 2), breeding duration increased with colony size, but the cause of the relocation of the colony remains unknown. nestling feeding duration was not correlated with colony In the present study, the colony size increased yearly size. Colony size did not aeff ct the proportion of successful aer ft establishment and later became saturated ( Figure 1), nests, but the mean number of fledglings per successful nest similartothe patterns reported forGreyHeronsintwo decreased with colony size. As the colony size increased, the Spanish colonies [39, 40]. Density-dependent processes may date of the rfi st breeding became earlier, and variation in the be important factors causing such a demographic pattern. timing of the onset of breeding by individual pairs was higher. The mean clutch size and fledglings per successful nest have In the relationships between the date that each pair been reported to be 3.3–4.2 and 2.1–3.9, respectively, for Grey began breeding and the duration of breeding or nestling Herons [41]. In the present study, fledglings per successful feeding (Figure 3, Table 2), the breeding duration was usually nest ranged from 1.8 to 3.1 with a mean of 2.2 (SD = 0.3, longer in early breeders than in late breeders. However, 𝑁=14 ), but the fledgling number decreased with colony the nestling feeding duration did not differ greatly between size (Figure 2(d)), suggesting a density-dependent response. earlier and later breeding pairs, suggesting that the duration In a study on White Herons in New Zealand, the mean until nestling feeding was elongated in earlier breeders. In number of fledglings per nest also decreased as the number most years, the number of fledglings decreased as the date of of nests in the colony increased [3]. In the present study, the the onset of breeding was delayed (Figure 4, Table 2). timing of breeding may have also been density dependent, Air temperatures were warmer (4.0–5.4 Cinmeantem- because the breeding duration became longer (Figure 2(a)), perature for a period of 10 days of the coldest period) at thereproductiveseasonoccurredearlier (Figure 2(e)), and the beginning of breeding in 2000, 2002, 2004, 2007, and variation among individuals increased (Figure 2(f))asthe 2009, but were colder (1.9–2.9 C) in 1998, 2001, 2003, 2006, colony size increased. The tendency to delay the initial egg- and 2011, compared to temperatures in 1997, 1999, 2005, laying date when colony size is large has also been reported 2008, and 2010 (3.6–3.9 C).However,wintertemperaturewas for Purple Herons in southern France [4]. unlikely to explain yearly changes in colony size (Figure 1). The mechanisms of density dependence in demography Moreover, the two groups of warmer and colder years did not involve both extrinsic (food) and intrinsic (social behavior) significantly differ in the date of the onset of breeding of the factors [42]. Increased feeding visits by parents (i.e., higher colony (Student’s t-test; t =0.70, df =8,𝑃 = 0.70 ), the CV food availability to chicks) decrease the chick mortality of in individual breeding date (t =1.14, df =7,𝑃 = 0.29 ), or Grey Herons [9]. The nestling feeding duration of Grey other reproductive traits (breeding duration: t =0.04, df =7, Herons, particularly when feeding small chicks, becomes 𝑃=0.97 ; nestling feeding duration: t =0.22, df =7,𝑃=0.83 ; longer when the frequency of returns to the nest decreases, number of successful nests: t =0.51, df =7,𝑃=0.63 ;number likely because of less food availability at hunting sites [43]. of fledglings per successful nest: t = 0.43, df = 7,𝑃=0.68 ). In a eld fi experiment using food supplements, Great Blue Predation rarely occurred during the censuses. eTh Herons showed increased clutch size and fledging success but observed predators of eggs and chicks were the Japanese rat no difference in the seasonal timing of nesting [ 44]. u Th s, Colony size (number of nests) 2011 4 International Journal of Zoology Th Table 1: Mean values of the breeding duration, nestling feeding duration, number of fledglings per successful nest, and date starting breeding in each nest. e proportion of successful nests to fledge and the date of the first breeding in the colony are also shown. Breeding duration Nestling feeding Successful Number of fledglings/ Date of the Date of the beginning Number of Colony Year (days) duration (days) nests successful nest first breeding of each nest breeding nests used Mean SD N Mean SD N Percentage N Mean SD N in the colony Mean SD CV (%) N Renkoji 1996 10 Renkoji 1997 37 102.5 6.9 19 67.3 17.1 15 85.3 34 3.1 0.7 29 48 78.1 26.4 33.8 34 Renkoji 1998 43 106.7 14.7 24 58.6 16.3 24 92.1 38 2.5 0.9 35 62 74.9 18.1 24.1 33 Renkoji 1999 60 106.6 16.0 20 64.6 17.0 20 64.4 45 2.2 0.7 29 62 79.6 16.5 20.8 58 Renkoji 2000 49 0 0 0.0 49 0 47 0 Tama Zoo 2000 14 Tama Zoo 2001 26 114.6 15.0 15 65.9 16.8 7 85.0 20 1.9 0.7 17 45 83.8 18.0 21.5 25 Tama Zoo 2002 122 99.1 16.2 56 57.3 12.1 43 70.7 92 2.1 0.9 65 49 75.5 22.1 29.3 78 Tama Zoo 2003 111 113.4 15.5 82 64.6 11.0 76 82.5 103 2.5 0.8 85 42 75.9 26.0 34.3 106 Tama Zoo 2004 136 111.1 19.2 79 60.6 17.6 77 79.5 122 2.4 0.9 97 26 72.1 29.2 40.6 135 Tama Zoo 2005 175 120.9 22.1 112 60.4 13.4 95 81.5 157 2.1 0.8 128 4 64.3 35.8 55.6 156 Tama Zoo 2006 201 123.8 21.1 102 61.7 14.5 89 62.6 182 2.0 0.8 114 12 68.6 27.4 39.9 195 Tama Zoo 2007 218 126.6 21.3 125 63.4 17.4 106 79.9 174 2.1 0.8 139 35 69.4 29.2 42.0 208 Tama Zoo 2008 178 114.3 16.9 102 59.3 11.6 96 75.8 149 2.0 0.8 113 27 67.4 21.2 31.4 166 Tama Zoo 2009 180 129.0 21.1 105 67.8 16.7 85 79.1 153 1.8 0.6 121 23 57.0 24.4 42.8 183 Tama Zoo 2010 171 125.9 21.3 117 53.6 17.4 113 77.7 157 1.9 0.6 122 31 67.9 20.9 30.8 155 Tama Zoo 2011 167 125.2 24.7 93 63.3 18.5 99 79.3 150 2.0 0.8 119 38 73.6 31.2 42.4 130 a b All nests were abandoned in this year; date is presented by days since the 1st of January in each year. International Journal of Zoology 5 𝑟=−0.268,𝑁=14, NS 𝑟=0.736,𝑁=14,𝑃<0.01 0 100 200 300 0 100 200 300 Colony size (number of nests) Colony size (number of nests) (a) (b) 𝑟= −0.564,𝑁=14,𝑃<0.05 𝑟=−0.369,𝑁=14, NS 0 0 0 100 200 300 0 100 200 300 Colony size (number of nests) Colony size (number of nests) (c) (d) 𝑟= −0.759,𝑁=15,𝑃<0.01 𝑟=0.705,𝑁=14,𝑃<0.01 0 100 200 300 0 100 200 300 Colony size (number of nests) Colony size (number of nests) (e) (f) Figure 2: Relationships between colony size and (a) breeding duration, (b) nestling feeding duration, (c) proportion of successfully fledged nests, (d) number of fledglings per successful nest, (e) date of the first breeding in the colony, and (f) coefficient of variation in the date of the onset of breeding by individuals. Bars indicate± SD. Breeding duration (days) Date of the first breeding Successive nests (%) Variation in breeding date No. of fledglings Nestling feeding duration (days) 6 International Journal of Zoology 200 1997 200 2007 2002 200 180 180 160 160 140 140 120 120 100 100 80 80 60 60 40 40 20 20 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 200 2003 200 2008 180 180 160 160 140 140 120 120 100 100 80 80 60 60 20 20 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 200 1999 200 2004 200 2009 180 180 160 160 160 140 140 120 120 120 100 100 100 80 80 80 60 60 60 40 40 20 20 0 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 200 200 2005 2010 180 180 160 160 140 140 120 120 100 100 Not examined 80 80 60 60 40 40 20 20 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 200 200 200 180 180 160 160 160 140 140 120 120 120 100 100 100 80 80 80 60 60 60 40 40 20 20 0 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 Date Date Date (days from January 1st) (days from January 1st) (days from January 1st) Figure 3: Breeding ( ∙) or nestling feeding (×) durations of each pair of Grey Herons in relation to the date of the beginning of breeding in each year. Regression lines are shown when the correlation coefficients are statistically significant (see Table 2). competition for limited food is a possible source of density depend on the presence of freshwater and saltwater habitats dependence. However, the effect of food availability on colony within a 5 km area [45]. Estimating the amount of available size is usually difficult to detect, because food searching food over such a wide range of habitat would be difficult. areas used by colony members cannot be tracked completely. Social factors involved in density dependence may be In Portugal,CattleEgret (Bubulcus ibis) colonies reportedly direct behavioral interference among colony members. In depend on the areas of dry pasture and crops within a 5 km herons and egrets, intraspecific interactions may be critical radius of the colony center, and Little Egrets (Egretta garzetta) in courtship and nesting [1, 46]. In the present study, Duration (days) Duration (days) Duration (days) Duration (days) Duration (days) International Journal of Zoology 7 5 5 5 1997 2002 2007 4 4 4 3 3 3 2 2 2 1 1 0 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 2003 2008 4 4 3 3 2 2 1 1 1 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 5 5 1999 2004 2009 4 4 3 3 2 2 1 1 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 2005 2010 4 4 3 3 Not examined 2 2 1 1 0 30 60 90 120 150 180 0 30 60 90 120 150 180 5 5 4 4 3 3 2 2 1 1 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 Date (days from January 1st) Date (days from January 1st) Date (days from January 1st) Figure 4: Number of fledglings per nest in relation to the date of the beginning of breeding in each nest. Regression lines are shown when the correlation coefficients are statistically significant (see Table 2). earlier breeders took a longer period of time until nestling earlier breeders than for later breeders (Figure 4). A similar feeding (i.e., the period from nest building to completed decline in the number of fledglings with a later date of the egg incubation) than later breeders (Figure 3). The prolonged onset of breeding was observed for Grey Herons in Poland, prenestling feeding duration may have been caused by unsta- although it was not observed every year [19]. Brood size is ble states of colony members at the beginning of the breeding oen ft larger in earlier breeders within a reproductive season season. During this period, interference is expected to be in birds [47], as observed in Grey Herons [7, 48, 49]and other frequent and intense, because the colony includes many birds heron and egret species [50–52]. On the other hand, mean that have arrived and joined the colony that year. To conrm fi brood size increases with the age of parents [53, 54]. Older this interference hypothesis, quantitative data examining the individuals may be more successful in acquiring nest sites relationship between interference frequency and colony size of good quality and have more experience in parental care are needed. [54, 55]. In the present study, these age eect ff s could not be Despite these possible intense interactions in the early assessed. In the future, to discriminate the effects of the age of breeding season, the number of fledged chicks was greater for parents and the timing of breeding on reproductive success, Number of fledglings/nest Number of fledglings/nest Number of fledglings/nest Number of fledglings/nest Number of fledglings/nest 8 International Journal of Zoology Table 2: Correlation coefficients between the date of starting breeding and the breeding duration, the nestling feeding duration, or the number of fledglings in each nest. Breeding duration Nestling feeding duration Number of fledglings Colony Year 𝑟𝑁 𝑃 𝑟 𝑁 𝑃 𝑟 𝑁 𝑃 Renkoji 1996 Renkoji 1997 −0.376 19 NS 0.285 16 NS −0.495 30 ∗∗ Renkoji 1998 −0.751 24 ∗∗∗ −0.135 24 NS −0.048 30 NS Renkoji 1999 −0.647 20 ∗∗ −0.350 19 NS −0.013 37 NS Renkoji 2000 Tama Zoo 2000 Tama Zoo 2001 −0.422 15 NS −0.233 14 NS −0.591 19 ∗∗ Tama Zoo 2002 −0.329 54 ∗ −0.323 40 ∗ −0.327 78 ∗∗ Tama Zoo 2003 −0.475 79 ∗∗∗ −0.121 74 NS −0.233 100 ∗ Tama Zoo 2004 −0.589 78 ∗∗∗ −0.213 76 NS −0.218 117 ∗ Tama Zoo 2005 −0.614 111 ∗∗∗ −0.203 94 NS −0.178 150 ∗ Tama Zoo 2006 −0.548 102 ∗∗∗ −0.342 89 ∗∗ −0.287 180 ∗∗ Tama Zoo 2007 −0.500 125 ∗∗∗ −0.118 106 NS −0.311 170 ∗∗∗ Tama Zoo 2008 −0.743 101 ∗∗∗ −0.136 95 NS −0.252 143 ∗∗ Tama Zoo 2009 −0.751 105 ∗∗∗ −0.311 84 ∗∗ −0.267 137 ∗∗ Tama Zoo 2010 −0.709 117 ∗∗∗ 0.032 110 NS −0.110 150 NS Tama Zoo 2011 −0.702 93 ∗∗∗ −0.255 87 ∗ −0.307 120 ∗ ∗ ∗∗ ∗∗∗ NS,𝑃>0.05 ; 𝑃<0.05 ; 𝑃<0.01 ; 𝑃<0.001 . the age of the Grey Herons must be determined by marking sites for a longer duration in inland locations [19]. u Th s, the individuals. accessibility of feeding sites (lack of ice cover) in spring is an important factor affecting the onset of breeding. However, in suburban Tokyo, winter temperatures are relatively mild 4.2. Density Independence. Unpredictable factors can explain and rarely fall below 0 C. eTh refore, annual dieff rences in the reduced breeding success and increased mortality in some onset of breeding are not likely related to temperature, as in regions without invoking density-dependent mechanisms [5, thecaseofLittleEgretsinFrance[56]. 10, 11]. For example, in a study conducted in the Yucatan Peninsula, most herons and egrets failed to reproduce Acknowledgments becauseoffoodshortagescausedbyexceptionallyheavyrains and flooding of their lowland habitats [ 10]. The author thanks Fumio Hayashi, Tamotsu Kusano, and Another well-known density-independent process that Tadashi Suzuki for their help with many aspects of this canreducepopulationsizeinheronsand egrets is unpre- study and particularly F. Hayashi for the improvement of dicted severely low temperatures in winter. eTh Grey Heron an earlier version of this paper. He also thanks Kazuyoshi population in England and Wales usually numbers 4500– Ito, Etsuo Narushima, Tomoko Yabe, Yasumasa Tomita, and 4800, but aer ft severe winters, it decreases to around 3000 HeizoSugitafor allowing himtostudy at Tama Zoological [12]. In particular, winter (January to March) temperature Park and Fumio Nakamura for his help in initiating a study strongly affects the survival rate of rfi st-year Grey Herons there. in England, as estimated by the annual recovery of banded nestlings from 1955 to 1974 [13]. In those studies, in a References year when temperatures reached about 1 C, few young birds survived, whereas during years with winter temperatures [1] J. A. Kushlan and J. A. Hancock, The Herons , Oxford University above 6 C, more than half survived. A large number of Grey Press, New York, NY, USA, 2005. Herons also died during a cold spell in January and February [2] I. Newton, Population Limitation in Birds, Academic Press, 1976 in The Netherlands [ 14]. 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Colony Development and Density-Dependent Processes in Breeding Grey Herons

International Journal of Zoology , Volume 2013 – Feb 13, 2013

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Copyright © 2013 Takeshi Shirai. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.
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Hindawi Publishing Corporation International Journal of Zoology Volume 2013, Article ID 404065, 10 pages http://dx.doi.org/10.1155/2013/404065 Research Article Colony Development and Density-Dependent Processes in Breeding Grey Herons Takeshi Shirai Department of Biology, Tokyo Metropolitan University, Minamiosawa 1-1, Hachioji, Tokyo 192-0397, Japan Correspondence should be addressed to Takeshi Shirai; ardea@k00.itscom.net Received 14 December 2012; Accepted 8 January 2013 Academic Editor: Eugene S. Morton Copyright © 2013 Takeshi Shirai. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. The density-dependent processes that limit the colony size of colonially breeding birds such as herons and egrets remain unclear, because it is difficult to monitor colonies from the first year of their establishment, and the most previous studies have considered mixed-species colonies. In the present study, single-species colonies of the Grey Heron (Ardea cinerea) were observed from the first year of their establishment for 16 years in suburban Tokyo. Colony size increased aeft r establishment, illustrating a saturation curve. The breeding duration (days from nest building to fledging by a pair) increased, but the number of fledglings per nest decreased, with colony size. eTh reproductive season in each year began earlier, and there was greater variation in the timing of individual breeding when the colony size was larger. The prolonged duration until nestling feeding by early breeders of the colony suggests that herons at the beginning of the new breeding season exist in an unsteady state with one another, likely owing to interactions with immigrant individuals. Such density-dependent interference may aec ff t reproductive success and limit the colony size of Grey Herons. 1. Introduction colony sites appears to be unimportant in determining the reproductive success or survival in most species [5, 6]. Instead Wading birds such as herons and egrets nest in colonies in of tracking yearly changes in a single colony, intercolonial relatively limited areas and at high density, oeft n reaching comparisons in the same year are useful to detect density- hundreds or thousands of pairs [1]. Herons and egrets are dependent processes, and such comparisons have been con- usuallyquitelargebirds,andthedynamicsoftheirpopulation ducted in herons and egrets. Results have shown that final attract much attention, as estimating the number of breeding breeding success is negatively correlated with colony size pairs is easier in colony-breeding birds than in noncolony in Grey Herons (Ardea cinerea)inBelgium [7]and Great breeders. Population u fl ctuations may be caused by density- Blue Herons (Ardea herodias)inCanada[8]. However, in dependent and density-independent processes, although the Grey Herons in northern Poland, breeding success increases two are not mutually exclusive. with colony size [9]. Different conditions within each colony Density dependence is a negative feedback between habitat, such as the distance to feeding sites and predation population growth rate and population density [2]. In a risks, may cause opposing results for the relationship between White Heron (Egretta alba)colony, themeannumberof colony size and breeding success. fledglings per nest decreased as the number of nests in the Density-independent factors have also been suggested colony increased, suggesting a density-dependent response to affect the population u fl ctuations of herons and egrets. [3]. The first egg-laying date was delayed when colony size Unpredictable factors such as cold weather, high winds, was large in a Purple Heron (Ardea purpurea)colony[4]. disease, food shortage, and human impacts can explain However, little unequivocal evidence shows that density- reducedbreedingsuccess andincreased mortalityinsome dependent factors regulate population u fl ctuations of wading regions without invoking density-dependent mechanisms birds, because intraspecific competition for breeding and 2 International Journal of Zoology [5, 10, 11]. In particular, winter temperature is known to aeff ct 2.2. Observations. After colony establishment was first noted populations of herons and egrets via increased mortality [12– at Renkoji in mid-1996 [28], the herons were observed 15]. Winter temperature also aeff cts the onset of the breeding systematically beginning from the next year (1997) using season in Grey Herons [16–19]. binoculars (×10) and a spotting scope (×20–60; TSN-1, Kowa, Short-term studies are suboptimal for detecting the Nagoya). Herons that stayed in their nests were identified effects of density on the dynamics of wading bird populations, to species. I monitored the typical behavior of breeding because birds are long-lived and breed annually [1]. Even individuals (nest building, incubation, or guarding) and the in the several long-term studies conducted to date, census number and body size of chicks (small, medium, or large), if data were not recorded beginning with colony establishment present, at intervals of 3–7 days in 1997 and every 7–10 days but with mature colonies (e.g., [10–12, 20–23]). eTh tendency in 1998–2000. In 2000, the 49 breeding pairs of this colony of wading birds to form mixed-species groups has posed haddisappeared by late April, andnoheronswereobserved another difficulty for detecting density-dependent processes aer ft wards. However, 14 pairs were observed making nests in colony size regulation; in these cases, both intra- and inter- since late March in 2000. er Th efore, I continued to census specific interactions aeff ct individual behavior and survival this consecutive colony at intervals of 7–10 days in 2001, [24, 25]. butatintervals of 3-4daysin2002–2008 and7days in In the present study, to simplify the factors affecting 2009–2011. From the census data, the breeding and nestling density-dependent processes of colony breeders, a single- feeding durations of each nest were calculated as the period species colony of Grey Herons was selected and monitored from the day that nest-building behavior was rfi st recorded for 16 years beginning at its establishment. I investigated until fledging was completed (all fledglings disappeared in the long-term population fluctuation patterns in this colony the nest) and the period from ending incubation (judged and examined density-dependent phenomena based on indi- from continuous standing of parents) to complete fledging, vidual breeding behavior and reproductive successes in respectively. If predation occurred in the efi ld, the predators the colony. With respect to density-independent factors, I were identiefi d and recorded. examined how winter temperatures aeff ct colony size and To examine the eeff cts of winter temperature on popula- individual breeding behavior. tion u fl ctuations and the timing of breeding, air temperatures were used from public data recorded by the automated meteorological data acquisition system of the Japan Meteo- ∘ 󸀠 ∘ 󸀠 rological Agency at Fuchu, Tokyo (35 41 N, 139 29 E), located 2. Methods 8.4 km northeast from Tama Zoological Park. eTh minimum 2.1. Study Animal and Study Sites. eTh breeding range of value among the mean 10-day temperatures recorded from Grey Herons covers most of the Old World south of the December 1 to January 31 was used as the coldness value Arctic Circle, including Europe, Africa, Asia, and the East starting thebreedingseasonineachyear. Indies islands to Wallace’s Line [1]. Aeft r the breeding season, Some unintended effects of observations on breeding generally when the young can fly, they disperse in all direc- heron behavior have been identiefi d [ 29, 30], particularly tions [1]. Therefore, the nonbreeding range expands outside researcher visits to colonies during nest building and early incubation, leading to abandonment of nests [31]. Artificial of the breeding range. eTh se birds are sedentary and widely distributed in Japan [26]. eTh y feed on a variety of aquatic effects on heron behavior may be negligible in this study, animals such as sh, fi amphibians, crustaceans, insects, and because census observations were made carefully and far from the nests to avoid disturbing the herons, and because worms [1]. Feeding sites include ponds, lakes, rivers, marshes, andseashores(shallowtidalbays),andtheyoeft nusearticfi ial the nests were so high in the trees that any eggs in the nests water environments such as rice elds, fi sh fi farms, parks, and were not examined. dams [27]. In 1996, a breeding colony of Grey Herons became estab- ∘ 󸀠 lished at a hillside at Renkoji in suburban Tokyo (35 39 N, 3. Results ∘ 󸀠 139 28 E); this was selected as a long-term monitoring site. This site is located near the Oguri-gawa River where it just In 2001 and 2002, eight and two pairs of Black-Crowned joins the Tama-gawa River. eTh colony (250 m along the Night Herons (Nycticorax nycticorax) were found, respec- major axis, 80 m along the minor axis) was located in a tively, in the Tama Zoological Park Grey Heron colony. The small area of woods surrounded by houses in a newly built park staff also reported that this colony included at least town. eTh woods mainly consisted of Quercus serrata and Q. 13 nests of Black-Crowned Night Herons in 2000 [32]. In acutissima and some Pinus densiflora . In 2000, however, the all other years, only Grey Herons nested within the colony. colony abandoned this site and relocated to a new breeding The number of nests used by the pairs increased annually ∘ 󸀠 ∘ 󸀠 site on a hilltop in Tama Zoological Park (35 38 N, 139 24 E), aer ft colony establishment at Renkoji but tended to become located about 5 km west of Renkoji along the Tama-gawa saturated aeft r about 10 years ( Figure 1). The mean duration River. In the zoo, woods are patchily distributed, and the of breedingbyeachpairrangedfrom99.1to129.0 days,and Grey Herons useanarea(290m alongthe majoraxis, the mean duration of nestling feeding ranged from 53.6 to 67.8 220 m along the minor axis) consisting of Quercus serrata, days (Table 1). eTh proportion of successful nests that fledged Q. acutissima, Carpinus tschonoskii, Prunus jamasakura,and was 62.6%–85.3%, excluding all that were unsuccessful by the Pinus densiflora . abandonment of the site in 2000 (Table 1). The maximum International Journal of Zoology 3 snake Elaphe climacophora (𝑁=1 )and thejunglecrow Tama zoological park Corvus macrorhynchos (𝑁=14 ). 80 Renkoji 4. Discussion 4.1. Density Dependence. The Renkoji site was abandoned 4 years aer ft establishment and the colony relocated to a Year new site in Tama Zoological Park close to Renkoji along the Tama-gawa River. Higher rates of nest mortality lead Figure 1: Yearly changes in the number of nests in the Renkoji to significant decreases in colony size, and breeding colony and Tama Zoological Park colonies. In 2000, the Renkoji site distributions oeft n shift in association with these reductions was abandoned, and a new colony was established at the Tama in colony size [33, 34]. For example, a colony of Great Blue Zoological Park close to Renkoji. Herons at Pender Harbour, British Columbia, abandoned their site after 2 years of high predation by Ravens ( Corvus corax), Bald Eagles (Haliaeetus leucocephalus), and probably raccoons (Procyon lotor)[8, 35]. Heavypredation maythus number of fledglings was four, and the mean number of force colony abandonment by herons. In the study popu- fledglings per successful nests ranged from 1.8 to 3.1 ( Table 1). lation, however, predation was rarely observed. eTh snake eTh date that the rfi st pair(s) began to breed in the colony Elaphe climacophora and the crow Corvus macrorhynchos differed from year to year, ranging from January 4 to March were theonlypredators of eggs andchicksrecordedinthe 3(Table 1). eTh mean start date of breeding by pairs also present study. Colony nesting of birds sometimes damages differed yearly, and the coefficient of variation (CV) in the vegetation, mainly by altering soil nutrient concentration [36, start date of colony members ranged from 20.8% to 55.6% 37]. Vegetation degradation may cause shifting the colony (Table 1). site [38]. In this study, however, obvious change in vegetation For the effect of colony size on breeding parameters occurred for 16 years even at the central part of colonies. us, Th (Figure 2), breeding duration increased with colony size, but the cause of the relocation of the colony remains unknown. nestling feeding duration was not correlated with colony In the present study, the colony size increased yearly size. Colony size did not aeff ct the proportion of successful aer ft establishment and later became saturated ( Figure 1), nests, but the mean number of fledglings per successful nest similartothe patterns reported forGreyHeronsintwo decreased with colony size. As the colony size increased, the Spanish colonies [39, 40]. Density-dependent processes may date of the rfi st breeding became earlier, and variation in the be important factors causing such a demographic pattern. timing of the onset of breeding by individual pairs was higher. The mean clutch size and fledglings per successful nest have In the relationships between the date that each pair been reported to be 3.3–4.2 and 2.1–3.9, respectively, for Grey began breeding and the duration of breeding or nestling Herons [41]. In the present study, fledglings per successful feeding (Figure 3, Table 2), the breeding duration was usually nest ranged from 1.8 to 3.1 with a mean of 2.2 (SD = 0.3, longer in early breeders than in late breeders. However, 𝑁=14 ), but the fledgling number decreased with colony the nestling feeding duration did not differ greatly between size (Figure 2(d)), suggesting a density-dependent response. earlier and later breeding pairs, suggesting that the duration In a study on White Herons in New Zealand, the mean until nestling feeding was elongated in earlier breeders. In number of fledglings per nest also decreased as the number most years, the number of fledglings decreased as the date of of nests in the colony increased [3]. In the present study, the the onset of breeding was delayed (Figure 4, Table 2). timing of breeding may have also been density dependent, Air temperatures were warmer (4.0–5.4 Cinmeantem- because the breeding duration became longer (Figure 2(a)), perature for a period of 10 days of the coldest period) at thereproductiveseasonoccurredearlier (Figure 2(e)), and the beginning of breeding in 2000, 2002, 2004, 2007, and variation among individuals increased (Figure 2(f))asthe 2009, but were colder (1.9–2.9 C) in 1998, 2001, 2003, 2006, colony size increased. The tendency to delay the initial egg- and 2011, compared to temperatures in 1997, 1999, 2005, laying date when colony size is large has also been reported 2008, and 2010 (3.6–3.9 C).However,wintertemperaturewas for Purple Herons in southern France [4]. unlikely to explain yearly changes in colony size (Figure 1). The mechanisms of density dependence in demography Moreover, the two groups of warmer and colder years did not involve both extrinsic (food) and intrinsic (social behavior) significantly differ in the date of the onset of breeding of the factors [42]. Increased feeding visits by parents (i.e., higher colony (Student’s t-test; t =0.70, df =8,𝑃 = 0.70 ), the CV food availability to chicks) decrease the chick mortality of in individual breeding date (t =1.14, df =7,𝑃 = 0.29 ), or Grey Herons [9]. The nestling feeding duration of Grey other reproductive traits (breeding duration: t =0.04, df =7, Herons, particularly when feeding small chicks, becomes 𝑃=0.97 ; nestling feeding duration: t =0.22, df =7,𝑃=0.83 ; longer when the frequency of returns to the nest decreases, number of successful nests: t =0.51, df =7,𝑃=0.63 ;number likely because of less food availability at hunting sites [43]. of fledglings per successful nest: t = 0.43, df = 7,𝑃=0.68 ). In a eld fi experiment using food supplements, Great Blue Predation rarely occurred during the censuses. eTh Herons showed increased clutch size and fledging success but observed predators of eggs and chicks were the Japanese rat no difference in the seasonal timing of nesting [ 44]. u Th s, Colony size (number of nests) 2011 4 International Journal of Zoology Th Table 1: Mean values of the breeding duration, nestling feeding duration, number of fledglings per successful nest, and date starting breeding in each nest. e proportion of successful nests to fledge and the date of the first breeding in the colony are also shown. Breeding duration Nestling feeding Successful Number of fledglings/ Date of the Date of the beginning Number of Colony Year (days) duration (days) nests successful nest first breeding of each nest breeding nests used Mean SD N Mean SD N Percentage N Mean SD N in the colony Mean SD CV (%) N Renkoji 1996 10 Renkoji 1997 37 102.5 6.9 19 67.3 17.1 15 85.3 34 3.1 0.7 29 48 78.1 26.4 33.8 34 Renkoji 1998 43 106.7 14.7 24 58.6 16.3 24 92.1 38 2.5 0.9 35 62 74.9 18.1 24.1 33 Renkoji 1999 60 106.6 16.0 20 64.6 17.0 20 64.4 45 2.2 0.7 29 62 79.6 16.5 20.8 58 Renkoji 2000 49 0 0 0.0 49 0 47 0 Tama Zoo 2000 14 Tama Zoo 2001 26 114.6 15.0 15 65.9 16.8 7 85.0 20 1.9 0.7 17 45 83.8 18.0 21.5 25 Tama Zoo 2002 122 99.1 16.2 56 57.3 12.1 43 70.7 92 2.1 0.9 65 49 75.5 22.1 29.3 78 Tama Zoo 2003 111 113.4 15.5 82 64.6 11.0 76 82.5 103 2.5 0.8 85 42 75.9 26.0 34.3 106 Tama Zoo 2004 136 111.1 19.2 79 60.6 17.6 77 79.5 122 2.4 0.9 97 26 72.1 29.2 40.6 135 Tama Zoo 2005 175 120.9 22.1 112 60.4 13.4 95 81.5 157 2.1 0.8 128 4 64.3 35.8 55.6 156 Tama Zoo 2006 201 123.8 21.1 102 61.7 14.5 89 62.6 182 2.0 0.8 114 12 68.6 27.4 39.9 195 Tama Zoo 2007 218 126.6 21.3 125 63.4 17.4 106 79.9 174 2.1 0.8 139 35 69.4 29.2 42.0 208 Tama Zoo 2008 178 114.3 16.9 102 59.3 11.6 96 75.8 149 2.0 0.8 113 27 67.4 21.2 31.4 166 Tama Zoo 2009 180 129.0 21.1 105 67.8 16.7 85 79.1 153 1.8 0.6 121 23 57.0 24.4 42.8 183 Tama Zoo 2010 171 125.9 21.3 117 53.6 17.4 113 77.7 157 1.9 0.6 122 31 67.9 20.9 30.8 155 Tama Zoo 2011 167 125.2 24.7 93 63.3 18.5 99 79.3 150 2.0 0.8 119 38 73.6 31.2 42.4 130 a b All nests were abandoned in this year; date is presented by days since the 1st of January in each year. International Journal of Zoology 5 𝑟=−0.268,𝑁=14, NS 𝑟=0.736,𝑁=14,𝑃<0.01 0 100 200 300 0 100 200 300 Colony size (number of nests) Colony size (number of nests) (a) (b) 𝑟= −0.564,𝑁=14,𝑃<0.05 𝑟=−0.369,𝑁=14, NS 0 0 0 100 200 300 0 100 200 300 Colony size (number of nests) Colony size (number of nests) (c) (d) 𝑟= −0.759,𝑁=15,𝑃<0.01 𝑟=0.705,𝑁=14,𝑃<0.01 0 100 200 300 0 100 200 300 Colony size (number of nests) Colony size (number of nests) (e) (f) Figure 2: Relationships between colony size and (a) breeding duration, (b) nestling feeding duration, (c) proportion of successfully fledged nests, (d) number of fledglings per successful nest, (e) date of the first breeding in the colony, and (f) coefficient of variation in the date of the onset of breeding by individuals. Bars indicate± SD. Breeding duration (days) Date of the first breeding Successive nests (%) Variation in breeding date No. of fledglings Nestling feeding duration (days) 6 International Journal of Zoology 200 1997 200 2007 2002 200 180 180 160 160 140 140 120 120 100 100 80 80 60 60 40 40 20 20 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 200 2003 200 2008 180 180 160 160 140 140 120 120 100 100 80 80 60 60 20 20 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 200 1999 200 2004 200 2009 180 180 160 160 160 140 140 120 120 120 100 100 100 80 80 80 60 60 60 40 40 20 20 0 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 200 200 2005 2010 180 180 160 160 140 140 120 120 100 100 Not examined 80 80 60 60 40 40 20 20 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 200 200 200 180 180 160 160 160 140 140 120 120 120 100 100 100 80 80 80 60 60 60 40 40 20 20 0 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 Date Date Date (days from January 1st) (days from January 1st) (days from January 1st) Figure 3: Breeding ( ∙) or nestling feeding (×) durations of each pair of Grey Herons in relation to the date of the beginning of breeding in each year. Regression lines are shown when the correlation coefficients are statistically significant (see Table 2). competition for limited food is a possible source of density depend on the presence of freshwater and saltwater habitats dependence. However, the effect of food availability on colony within a 5 km area [45]. Estimating the amount of available size is usually difficult to detect, because food searching food over such a wide range of habitat would be difficult. areas used by colony members cannot be tracked completely. Social factors involved in density dependence may be In Portugal,CattleEgret (Bubulcus ibis) colonies reportedly direct behavioral interference among colony members. In depend on the areas of dry pasture and crops within a 5 km herons and egrets, intraspecific interactions may be critical radius of the colony center, and Little Egrets (Egretta garzetta) in courtship and nesting [1, 46]. In the present study, Duration (days) Duration (days) Duration (days) Duration (days) Duration (days) International Journal of Zoology 7 5 5 5 1997 2002 2007 4 4 4 3 3 3 2 2 2 1 1 0 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 2003 2008 4 4 3 3 2 2 1 1 1 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 5 5 1999 2004 2009 4 4 3 3 2 2 1 1 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 2005 2010 4 4 3 3 Not examined 2 2 1 1 0 30 60 90 120 150 180 0 30 60 90 120 150 180 5 5 4 4 3 3 2 2 1 1 0 0 0 30 60 90 120 150 180 0 30 60 90 120 150 180 0 30 60 90 120 150 180 Date (days from January 1st) Date (days from January 1st) Date (days from January 1st) Figure 4: Number of fledglings per nest in relation to the date of the beginning of breeding in each nest. Regression lines are shown when the correlation coefficients are statistically significant (see Table 2). earlier breeders took a longer period of time until nestling earlier breeders than for later breeders (Figure 4). A similar feeding (i.e., the period from nest building to completed decline in the number of fledglings with a later date of the egg incubation) than later breeders (Figure 3). The prolonged onset of breeding was observed for Grey Herons in Poland, prenestling feeding duration may have been caused by unsta- although it was not observed every year [19]. Brood size is ble states of colony members at the beginning of the breeding oen ft larger in earlier breeders within a reproductive season season. During this period, interference is expected to be in birds [47], as observed in Grey Herons [7, 48, 49]and other frequent and intense, because the colony includes many birds heron and egret species [50–52]. On the other hand, mean that have arrived and joined the colony that year. To conrm fi brood size increases with the age of parents [53, 54]. Older this interference hypothesis, quantitative data examining the individuals may be more successful in acquiring nest sites relationship between interference frequency and colony size of good quality and have more experience in parental care are needed. [54, 55]. In the present study, these age eect ff s could not be Despite these possible intense interactions in the early assessed. In the future, to discriminate the effects of the age of breeding season, the number of fledged chicks was greater for parents and the timing of breeding on reproductive success, Number of fledglings/nest Number of fledglings/nest Number of fledglings/nest Number of fledglings/nest Number of fledglings/nest 8 International Journal of Zoology Table 2: Correlation coefficients between the date of starting breeding and the breeding duration, the nestling feeding duration, or the number of fledglings in each nest. Breeding duration Nestling feeding duration Number of fledglings Colony Year 𝑟𝑁 𝑃 𝑟 𝑁 𝑃 𝑟 𝑁 𝑃 Renkoji 1996 Renkoji 1997 −0.376 19 NS 0.285 16 NS −0.495 30 ∗∗ Renkoji 1998 −0.751 24 ∗∗∗ −0.135 24 NS −0.048 30 NS Renkoji 1999 −0.647 20 ∗∗ −0.350 19 NS −0.013 37 NS Renkoji 2000 Tama Zoo 2000 Tama Zoo 2001 −0.422 15 NS −0.233 14 NS −0.591 19 ∗∗ Tama Zoo 2002 −0.329 54 ∗ −0.323 40 ∗ −0.327 78 ∗∗ Tama Zoo 2003 −0.475 79 ∗∗∗ −0.121 74 NS −0.233 100 ∗ Tama Zoo 2004 −0.589 78 ∗∗∗ −0.213 76 NS −0.218 117 ∗ Tama Zoo 2005 −0.614 111 ∗∗∗ −0.203 94 NS −0.178 150 ∗ Tama Zoo 2006 −0.548 102 ∗∗∗ −0.342 89 ∗∗ −0.287 180 ∗∗ Tama Zoo 2007 −0.500 125 ∗∗∗ −0.118 106 NS −0.311 170 ∗∗∗ Tama Zoo 2008 −0.743 101 ∗∗∗ −0.136 95 NS −0.252 143 ∗∗ Tama Zoo 2009 −0.751 105 ∗∗∗ −0.311 84 ∗∗ −0.267 137 ∗∗ Tama Zoo 2010 −0.709 117 ∗∗∗ 0.032 110 NS −0.110 150 NS Tama Zoo 2011 −0.702 93 ∗∗∗ −0.255 87 ∗ −0.307 120 ∗ ∗ ∗∗ ∗∗∗ NS,𝑃>0.05 ; 𝑃<0.05 ; 𝑃<0.01 ; 𝑃<0.001 . the age of the Grey Herons must be determined by marking sites for a longer duration in inland locations [19]. u Th s, the individuals. accessibility of feeding sites (lack of ice cover) in spring is an important factor affecting the onset of breeding. However, in suburban Tokyo, winter temperatures are relatively mild 4.2. Density Independence. Unpredictable factors can explain and rarely fall below 0 C. eTh refore, annual dieff rences in the reduced breeding success and increased mortality in some onset of breeding are not likely related to temperature, as in regions without invoking density-dependent mechanisms [5, thecaseofLittleEgretsinFrance[56]. 10, 11]. For example, in a study conducted in the Yucatan Peninsula, most herons and egrets failed to reproduce Acknowledgments becauseoffoodshortagescausedbyexceptionallyheavyrains and flooding of their lowland habitats [ 10]. The author thanks Fumio Hayashi, Tamotsu Kusano, and Another well-known density-independent process that Tadashi Suzuki for their help with many aspects of this canreducepopulationsizeinheronsand egrets is unpre- study and particularly F. Hayashi for the improvement of dicted severely low temperatures in winter. eTh Grey Heron an earlier version of this paper. He also thanks Kazuyoshi population in England and Wales usually numbers 4500– Ito, Etsuo Narushima, Tomoko Yabe, Yasumasa Tomita, and 4800, but aer ft severe winters, it decreases to around 3000 HeizoSugitafor allowing himtostudy at Tama Zoological [12]. In particular, winter (January to March) temperature Park and Fumio Nakamura for his help in initiating a study strongly affects the survival rate of rfi st-year Grey Herons there. in England, as estimated by the annual recovery of banded nestlings from 1955 to 1974 [13]. In those studies, in a References year when temperatures reached about 1 C, few young birds survived, whereas during years with winter temperatures [1] J. A. Kushlan and J. A. Hancock, The Herons , Oxford University above 6 C, more than half survived. A large number of Grey Press, New York, NY, USA, 2005. Herons also died during a cold spell in January and February [2] I. Newton, Population Limitation in Birds, Academic Press, 1976 in The Netherlands [ 14]. 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