Bioecology and breeding performance of cattle egret (Bubulcus ibis) in selected sites at Sharkia Governorate, Egypt

Abstract Cattle egret Bubulcus ibis, feeds on insect pests in many agro-ecosystems. Thus, there is an urgent need to study the breeding chronology of cattle egret, in order to develop suitable protection programs for this beneficial bird to perform its role as abiological control agent in Egyptian agro-ecosystems. The study was conducted at Sharkia Governorate, Egypt, from December 2018 to December 2020; in different habitats (irrigation canals, drainage canals, garbage collection areas and Abbasa ponds). The mean clutch size ranged from 2-5 eggs/nest with an incubation period ranging between 21-25 days. The mean percentage of hatching success was 90.21%, while the total number of mortality eggs was 47 and the total egg hatching was 433. Also the total number of nests located nearby tree trunks were 73, while nests located in the core of the tree were 47 nests, and nests located at the peripherals were 15 nests.


Introduction
The cattle egret, Bubulcus ibis, belongs to order: Pelecaniformes (Issa, 2019).It is a cosmopolitan species of heron (Family: Ardeidae) found in tropical, subtropical, and warm temperature zones.It has undergone the most rapid, and wide reaching natural expansion (Dalio, 2018).The worldwide success of cattle egret resulted in its ability to survive, and adapt to different environments, also its ability to feed on a variety of prey items such as fishes, frogs, insects and mollusks (Gochfeld and Burger, 1982;Subramanya, 1996;Kopij, 2008;Choi et al., 2016).It's a common breeding resident bird in Egypt across the Nile were sufficiently close in order to communicate vocally and visually with neighboring individuals (Gochfeld, 1980).Each egg, within a tagged nest, was marked by drawing a dot on it for the first laid egg and two dots for the second and so on.Any damage to the egg surface was recorded as crush mark, also non-hatched eggs were recorded.

Clutch size, incubation and fledging period
According to the method of (Drent, 1970) clutch size is the number of eggs laid per nest.The incubation period is the number of days elapsed between the last egg laid and the hatching of that egg (Enemar, 1997).The percentage of hatching success was calculated according to Kour and Sahi (2013), as follow: Hatching success % = (Number of egg hatched/Total egg laid) × 100 While the fledged period is the period when the young could fly and leave the nest (Mostafa et al., 2008).A nest that contains at least one hatchling is considered a successful nest (Klett and Johnson, 1982).The young were considered successfully fledged when they were old enough to fly across open space to trees away from the nests (Pratt and Winkler, 1985).The fledging rate measured according to Soliman et al. (2021) as follow: Fledging rat% = (Number of chick fledged/Total chicks hatched) × 100

Nest placement
Nests were classified according to their positions on the tree: Peripheral nests: where nests located at peripheral branches.
Core nests: where nests located in the core.
Trunk nests: where nests located nearby the trunk.

Statistical analysis
Statistical analysis was executed using one-way analysis of variance (ANOVA) to assess the significant difference between the colony sites (e.g.among IC, DC, GC and AP) treatment groups.While differences between means of the two years (e.g. between 2019 and 2020) were compared using Student t test.The mean is expressed as mean ± standard error (SE).The p-value was considered statistically significant at p < 0.05.Analysis of data was carried out in SPSS software version 16 as well as Microsoft Excel (Microsoft office, 2007).

Results
The photo in (Figure 1) showing some biological aspects associated with breeding of cattle egret Bubulcus ibis at Sharkia Governorate.

Nests, nest site, hatching rate and fledging rate
Most of the nesting sites of cattle egrets were found near human settlements in rural areas, villages and urban areas where the feeding places were in range.Table 1 showed the number of nests monitored during the two studied years as 135 nests, and the total numbers of eggs laid were 480 eggs.The highest number of eggs laid, was 160 eggs in colonies rough, superficial, bowel shaped, not well lined and simple stage (Abdullah et al., 2017).
The aim of this study is to assess some breeding aspects (i.e.Hatching success, fledging rate, clutch size, incubation period, fate of eggs and nest placement) of cattle egret, Bubulcus ibis, in different sites at Sharkia Governorate, Egypt.

Study area
The study sites were monitored from December 2018 to December 2020 in some districts of Sharkia Governorate (30°34'N, 31°30'E and 16 meter above sea level).The study was conducted at the following sites.

Irrigation Canal Areas (ICA)
Sites were founded around the sides of the Ismailia Canal Branch, in Belbies district.Several Eucalyptus (E.tereticornis) trees were scattered around the Canal sides, varied from eight to fifteen meters high, with several crowns according to tree age.

Drainage Canals (DC)
The drainage canals serving agricultural lands and were chosen at Belbies nearby villages.Many tall trees, mainly Acacia (A. spp.), Willows (Salix spp.), Mulberry (Morus spp.) and Eucalyptus (from four to thirteen meters high) were located at both sides of these canals.

Garbage Collection Areas (GCA)
These were located near villages and rural areas.Eucalyptus and Ficus (F.benjamina) trees, ranged from two to thirteen meters in height, were located.

Abbassa Ponds (AP)
Belonging to the Central Laboratory of Aquaculture Research, which measures 1,480 feddans (6,216,000 square meters), with open canals and drainages, runing through the ponds.Eucalyptus trees were found nearby and Reeds were grown on some drainage sides.
The birds were observed with naked eye and through a binocular (Bushnell 7x50) (Issa, 2019).

Data collection
Before the breeding season, old nests were present in old colonies and the new nests were marked by tying plastic tape with a number around the nearest branch to the nest.The most breeding aspects; like nesting, egg laying and incubation were observed at marked nests from March to August during the breeding seasons of 2019 and 2020.Colonies were inspected twice weekly from starting of nesting.Cattle egrets have no agnostic behavior but leave the nests during nest examination.

Nesting
Nesting colony was defined as a site with an aggregation of more than 5 nests.In the nesting colony, individual birds Brazilian Journal of Biology, 2023, vol.83, e271632 3/10 Breeding of cattle egret (Bubulcus ibis) nearby the garbage collection area, in 41 nests, while the lowest number of eggs found in colonies nearby irrigation canals (99 eggs), in 29 nests.The total eggs hatched were 433 eggs, which yield 90.21% hatching success.The highest hatching success was in nests at the trees nearby Abbassa Ponds (91.45% hatchability) followed by nests in trees nearby GC (91.25%), then nests located on trees nearby Drainage Canals (89.42%) and finally in nests on trees nearby Irrigation Canals (87.88%).The number of fledged birds was 216 birds (49.88%).The fledging rate at nests in the trees nearby Irrigation Canals was 55.17%, followed by nests located in trees nearby Drainage Canals (51.61%). 2 revealed that the highest number of nests were 60 with 3eggs/nest, followed by 51 nests with 4 eggs/nest, and the number of eggs per cultch varied from 2-5 eggs/nest.The nests located on trees nearby Garbage Collection Areas received 160 eggs in 41 nests with an average of 3.9eggs/nest, with the highest mean compared with other sites.The average clutch size differed according to the colony site in descending order i.e. 3.59, 3.41 and 3.25 egg/nest at trees nearby Drainage Canals, Irrigation Canals and Abbassa Ponds, respectively.

Incubation period
Data in Table 3 showed that the incubation period varied from 21-25 days.The highest number of nests (35) recorded 22 days of incubation period during the two years of the study.But the lowest number of nests (9 nests) recorded 25 days of incubation period from a total of 135 monitored nests.The longest days of incubation period was 538 days (equal sum of the multiplication of the number of days in the number of nests, (e.g., 8x21 + 6x22 + 5x23 + 2x24 + 3x25) obtained from 24 nests in year 2019 in the location nearby Abbassa Ponds, with an average of 22.42 days.The grand mean of incubation period of cattle egret was 22.55 days resulting from 135 nests.

Fate of eggs
Data in Table 4 showed that, the addled (infertile) eggs were 21 eggs, while the eggs with dead embryos were 17 eggs.The numbers with broken eggs (cracked shells) were 9 eggs.Thus the total failures were 47 eggs during the two study years at different locations.

Nests placement
The cattle egret nests in colonies, which are often but not always, found around bodies of water.Data in Table 5 cleared that cattle egret nests were located on the tree crown in three strata i.e. nests nearby the trunk, nests in the core of the tree and nest at the peripheral of the tree crown, represented 54.07%, 34.81% and 11.11%, respectively.The primary branches of the tree crown received 83 nests (61.48% of total nests), but the secondary branches received 52 nests (38.52%).

Discussions
Total of 135 nests, of cattle egret, were found in this study.Cattle egret colony nearby the garbage collection areas gives the highest number of nests (41 nests, including 160 eggs).The suitability of these sites for cattle egret breeding attribute to the presence of trees for building nests and the specific needs of valuable foraging habitats especially during chick rearing.
The hatching success of cattle egret during the study period was 90.21%, while the fledging rate was 49.88%, these results agree with previous studies.For example, the hatching success of cattle egret in northeast Texas ranged from 71-96% (Telfair II and Bister, 2004).In Algeria Metallaoui et al. (2020) stated that the hatching success of cattle egret was 80, 90 and 100%, while the fledging success was 93.1 and 100%.On the other hand, hatching success was higher than that described in India (58.85%) (Kour and Sahi, 2013).The difference in hatchability percentage and fledging rates could originate from the genetic variation of phenotypic response to environmental condition.
The fledging rate in our study is probably to the death of siblings due to competition, starvation and predators, as we saw chick's downfall nests and hooded crow (Corvuse corone) attack adults.As mentioned by Blaker (1969), that death of chicks resulting from competition and starvation.
In Australia, McKilligan (1987) revealed that causes of The average clutch size of cattle egret in our study was 3.56 eggs per nest which is quite similar to that reported by Omar and Hassan (2019) in Sohage governorate, Egypt; they found that the average clutch size of cattle egret varied from 2.90 to 3.80 eggs, whereas El-Danasoury (2002) indicated an average of 3.5 eggs per nest in El-Minoufia governorate, Egypt.It's also in range of recorded by Abdullah et al. (2017) in Faisalabad, Pakistan, where the clutch size of cattle egret was 3 to 4 eggs, 3 eggs being the prevailing and uncommonly 5 eggs.In northern Algeria Metallaoui et al. (2020) find that clutch size was an average 3.43 ± 0.91 eggs.But our results were slightly higher than that of Samraoui et al. (2007), they reported that clutch size of cattle egret was 3.10 ± 0.13 eggs/nest.Clutch size variations in the different habitat are a response of the bird to the surrounding environment and often related to the parents age with too older parents or too younger laying smaller number of eggs (Klomp, 1970).Burger (1978) assigns that larger clutch size of cattle egret in New Jersey, USA, than other places according to the sufficient of food resources.The clutch size variations at different locations are a response to feeding area, type of food supply and food abundance per unit area (Van Noordwijk et al., 1980).Kazantzidis et al. (1996) revealed that feeding condition are reflected to clutch size of little egret in Camargue, Greece and Macedonia, France.
Variation in the incubation period, seem to be depend on the environmental conditions with parental traits (Higgott et al., 2020).Our results revealed that incubation period of cattle egret ranged from 21 to 25, with grand mean of 22.55 days resulted from 135 nests.This reporting was not significantly different from that of Abdullah et al. (2017) in Pakistan they revealed that the incubation period varied from 22-25 days.In India, Kour and Sahi (2012) reported that Incubation period was from 21-24 day.
The same trend was found in the United States and southern Canada, from 23 to 25 days (Weber, 1975).But in central Japan FUJIOKA (1984) found that the average of incubation period ranged from 22 to 27 days.On the other hand, our result was slightly higher than that found by Kour and Sahi (2013).They reported that incubation periods were from 21-23 day, in the same trend Omar and Hassan (2019) in Upper Egypt, noticed that incubation period varied from 19 to 22 days, that's differences in Upper Egypt may be due to temperature degrees as described by El-Danasoury (2002) who revealed that, incubation period of Cattle egrets decreased when temperature increased, as our study sites at Sharkia Governorate which located in North Egypt, where's the weather is colder than Upper Egypt.
The total unhatched eggs were 47 eggs, which make up about 9.8% of the total eggs laid, theses failure eggs were distributed as follows: addled (infertile) eggs 44.7%, dead embryo eggs 36.2% and 19.1% with cracked shells.These results were in accordance with Sharah and Ali (2008) in Nigeria, they found that about 7.5% of eggs unhatched were broken shells, rotten, smelly embryos and 1% to undefined factors.In Florida about 25% of egg and nestling losses was due to infertile or addled eggs while 75% is due to predation (Maxwell II and Kale II, 1977).In southeast Queensland, Australia, McKilligan (1987) revealed that about 34% of cattle egret eggs were broken or failed to hatch.
Nest site selection is important for rearing offspring, therefore the cattle egret locate their nests position to get more secure features (Ye et al., 2021).Cattle egret choose the tree with specific characteristics (the solidity of branches, trunk) which are suitable conditions for nesting site gave birds protection against predators, abundant materials to backup and construct the nest (Metallaoui et al., 2020).Our results cleared that the primary branches of the tree crown received 61.48% of cattle egret nests, while the secondary branches received 38.52%.These results agreed with Sbiki et al. (2015), they stated that cattle egret builds their nests mainly on the strong elementary branches of trees (30%) or minor branches at the periphery of the tree's crown (29%).In addition, cattle egret nests' were located nearby the trunk (54.07%), in the core of the tree (34.81%) and at the peripheral of the tree crown (11.11%).The cattle egret nested closer to the main trunk than the peripheral branches, but the peripheral nests wide distributed at varying distances from the trunk (Arendt and Arendt, 1988).The main explication of the peripheral nests widely distributed, is that central nests position were taken by old and experienced birds, thus young and inexperienced pairs are forced to take peripheral positions (Klomp, 1970).The higher fledging success of cattle egrets was close to the trunks of the trees (Si Bachir et al., 2008), because the central nests of cattle egret were safer than peripheral nests (Metallaoui et al., 2020).In contrast Patankar et al. (2007) revealed that, the majority of cattle egret nests (96%) were located on peripheral and only 4% were on core.

Conclusion
To summarize, our study provided breeding biology aspects for the cattle egret at Sharkia Governorate, Egypt, in four sites.Incubation period for cattle egret was higher than those reported from other districts in Egypt; this may be attributed to geographic variations.The fledging rate was influenced by several factors including competition, starvation and predators.The fate of eggs was due to disturbed parents, whom may break eggs, produce infertile eggs and bad aspect of incubation, which resulted from predators and competition between neighbors.The majority of nests were found to be nearby the trunk and in the core of the trees.These findings can contribute in understanding the mechanism of choosing nesting location.Future studies should be encouraged to gain more knowledge about the importance of geographic variation in breeding biology parameters and to describe the factors responsible for that variation.

Table 1 .
Parameters of breeding biology of cattle egret Bubulcus ibis at Sharkia Governorate during 2019-2020.

Table 2 .
Frequency distribution of clutch size for cattle egret Bubulcus ibis in different locations at Sharkia Governorate during 2019-2020.

Table 3 .
Frequency distribution of incubation period for cattle egret Bubulcus ibis under field condition at Sharkia Governorate during 2019-2020.

Table 4 .
Fate of eggs during incubation period for cattle egret Bubulcus ibis in different locations at Sharkia Governorate.

Table 5 .
Stratifications of cattle egret Bubulcus ibis nest sites on the crown of different trees at Sharkia Governorate during 2019-2020.IC = Irrigation Canal; DC = Drainage Canals; GC = Garbage Collection; AP = Abbassa Ponds; F value = value on the F distribution; P = P-value; Sig = probability significance; S refers to Significant difference at P ≤ 0.05; NS refers to no significant at P > 0.05; M ± SE refers to mean ± standard error.*P ≤ 0.05 Note.Brazilian Journal of Biology, 2023, vol.83, e271632 9/10 Breeding of cattle egret (Bubulcus ibis)