Avian brood parasitism by Common hawk cuckoo (Hierococcyx varius) and Jacobin cuckoo (Clamator jacobinus) in Bangladesh
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1 The 2017; 4(3): ISSN JOZS 2017; 4(3): JOZS 2017 Received: Accepted: Avian brood parasitism by Common hawk cuckoo (Hierococcyx varius) and Jacobin cuckoo (Clamator jacobinus) in Bangladesh Sajeda Begum Department of Zoology, Jahangirnagar University, Savar 1342, Dhaka, Bangladesh Corresponding Author: Begum S Corresponding bsajeda@yahoo.com Abstract The avian brood parasitic cuckoo species namely Common hawk cuckoo (Hierococcyx varius) and Jacobin cuckoo (Clamator jacobinus) parasitized the same host species Jungle babbler (Turdoides striata). Breeding season of Jungle babbler started in mid- February and ended in late June which coincides with the breeding season of the parasitic cuckoos, Common hawk cuckoo (March-May) and Jacobin cuckoo (June-July) respectively. Competition for same host has been found to reduce because these two cuckoo species have different breeding seasons. The common hawk cuckoo and Jacobin cuckoo eggs are not easily identifiable from those of their host Jungle babbler because of a very similar color and size. Maximum number of nests of Jungle babbler was found in Acacia (Acacia auriculiformis). Flock size of Jungle babbler was an important predictor of parasitism in both the cuckoo species with increased parasitism risk in nests at small group size of 4 to 8 members. The host species suffered the costs of cuckoo parasitism, predation and desertion. Keyword: Avian brood parasitic cuckoo, host, flock size, parasitism, Hierococcyx varius, Clamator jacobinus, Bangladesh Introduction Obligate brood parasites depend on other host species to raise their offspring and as a consequence, generally reduce the reproductive success of the hosts 29, 38. They possess an orderly arrangement of adaptation which help them to succeed at their alternative breeding strategy and as a result these may reduce hosts fitness in different ways. Brood parasites may remove or puncture host eggs, hence reduces the hosts clutch size, eventually sometimes causes the hosts to abandon the nests 15, 32, 42. In some cases, because of relatively short incubation period among brood parasites hatches sooner than the host eggs which may cause the hosts to stop incubation their eggs 20. On the other hand, parasite nestlings may impose additional costs on hosts, if host eggs hatch, the nestlings may be outcompeted by parasitic chicks 33, 36. Some parasitic chicks eliminate this competition by evicting host nestlings or eggs and also in extreme cases, host chick killing in the nest by specialized mandibular hooks developed in honeyguides (Indicator spp.) and Striped cuckoo (Tapera naevia) has been recorded 14. Adaptiveness of host egg destruction and egg removal has been described in some researches 41, 42, 14, 31. The adaptation of host eggs and nestling eviction by parasitic cuckoo nestlings is to ensure that the cuckoo chick may obtain the full parental care of the host parents 40. The Jungle babbler (Turdoides striata) has been mentioned as host of the Common hawk cuckoo (Hierococcyx varius), one of the most widely distributed cuckoos also known as brain fever bird in the Indian sub-continent 2. Brood parasitism in Common hawk cuckoo has been previously reported by Himmatsinjhi (1980) 21 and their preferred host was recorded as Jungle babbler in Kerala 1, 19, 34. Many species of laughing thrushes and as well as babbler species such as, Turdoides affinis, Turdoides striata, Turdoides rufescens, Turdoides caudata have been reported as hosts of the Common hawk cuckoo 6, 43. The Common babbler (Turdoides caudata) was parasitized by Jacobin cuckoo and recorded as potential host of this parasitic cuckoo 44. Jungle babbler also reported as host of Jacobin Cuckoo 17, 19. Few facts have been published about the breeding biology of the Common hawk cuckoo and Jacobin cuckoo. There is very little information exists on the timing, extent or effects of these two species of cuckoo parasitism. Details regarding coevolutionary interactions of sympatric parasitic cuckoos and their hosts are still unravelled in many parts of the world, such as in Bangladesh at the southeastern part of the Indian subcontinent. A preliminary study has been conducted on several sympatric cuckoo species, viz. the Asian koel (Eudynamys scolopacea), Common hawk cuckoo (Hierococcyx varius), Jacobin cuckoo (Clamator jacobinus) and Indian cuckoo (Cuculus micropterus) live in sympatry in heterogenous habitats in Bangladesh. Page 6
2 These cuckoos parasitize different host species, such as House crow (Corvus splendens), Long-tailed shrike (Lanius schach), Common myna (Acridotheres tristis), Black drongo (Dicrurus macrocercus), Jungle babbler (Turdoides striata) and others 7. All of the sympatric cuckoo species throughout the Indian subcontinent are obligate brood parasites. In the present study the aim was to investigate interactions between the two parasitic cuckoos viz. Common hawk cuckoo and Jacobin cuckoo and their particular host species Jungle babbler living in sympatry in the natural habitat of Jahangirnagar University campus, Bangladesh. Very little is known about the different species of cuckoos competing to parasitize the same host species in areas where they occur in sympatry. The main prediction is that if two or more parasitic cuckoos parasitize the same host they should be expected to differ in other fundamental ways, e.g. either different breeding periods or different arrival dates in the breeding habitat, or parasitizing the same host in diverse habitats, or different breeding strategies by the host species. Furthermore, risk of parasitism on the host Jungle babbler by these two parasitic cuckoos was studied. During field work, investigations were carried out to test these predictions in Jahangirnagar University campus. 2. Materials and Methods 2.1 Study Area The study was conducted in Jahangirnagar University Campus, central part of Bangladesh (23 52 N, E), 32 km north of Dhaka city (Fig.1). The size of the entire campus area is approximately 200 hectares consisting of diverse vegetation in and around human settlement 8, 9. The Jahangirnagar University Campus has isolated patches of sal (Shorea robusta) forest, which originated from an earlier tropical deciduous sal forest community 28. The campus has various vegetation types, forming a mixture of diverse habitats. In addition, the area consists of agricultural lands, orchards and botanical gardens in and around human settlements. A total of 195 bird species, including 81 passerines and 114 non-passerines, have been recorded in the area. In total, 78 passerine species have been found to be breeding residents 8. Fig 1: Map of the Jahangirnagar University campus 7 The basic data on parasitic cuckoos are described in more detail by 9, 10 and 28. The host Jungle babbler is one of the most common passerine birds throughout the whole peninsula of India 49. This species serves as host for several cuckoo species 24. It is a common bird found in gardens near human habitations as well as deciduous forests and cultivated areas 2. They are gregarious, occurring in parties of about 6 to 12 individuals and are commonly known as seven sisters due to their social habits 49, 2. Jungle babblers mainly feed on insects, but fruits like figs and berries are also a part of their diet. Their nests are normally built in small trees, and the breeding season lasts from March to September 2. Page 7
3 2.2 Methods This study on natural parasitism was carried out in three successive breeding seasons from 2010 to 2013 (January to August, each year). During these years, nests of the host species were systematically searched in different habitats within the study area. Data were collected on different factors, including the host nest tree, nest height, egg measurements, and egg mimicry. Mimicry of the parasitic egg with the host eggs was scored according to a scale from 1 (perfect) to 5 (poor mimicry) 26. On the other hand, flock size of the host was also recorded to find out the parasitism risks. Parasitism was determined after laying of cuckoo egg, hatching and identification of a cuckoo nestling. All nest locations were recorded by using GPS. When first found, the number of host eggs or nestlings and number of cuckoo eggs or nestlings were recorded. Most nests were found during the egg laying/incubation stage. 3. Results During the study period a total of 80 nests of the host species Jungle babbler were recorded during breeding seasons (February to July, each year) and among them 25 nests were parasitized by the two cuckoo species Common hawk cuckoo (N=23) and Jacobin cuckoo (N=2) respectively. A total of 38 nests where host nestlings were successfully fledged among the unparasitized nests (N=55) whereas, 12 nests were predated and 5 nests were deserted. Among the parasitized nests (N=25) only the parasitic cuckoo fledged successfully in 14 nests (N=12 by Common hawk cuckoo; N=2 by Jacobin cuckoo) and the rest of the 11 nests were found unsuccessful because of predation (N=8) and desertion (N=3) (Table1). Predation pressure was very high where 20 nests (25%) were predated in both parasitized and unparasitized nests. The peak month for nesting of Jungle babbler was considered April when the highest number (n=31) of nests was found (Table 1). Table 1: Number of nests in different months Month Total nests Parasitic cuckoo No of Parasitized Nest (%) No of Unparasitized Nest (%) Successful nest (%) Predated nest (%) Deserted nest (%) February 14 *CHC March 20 CHC Unpara=12 Para=4 Unpara=2 Para=0 Unpara=2 Para=0 April 31 CHC Unpara=13 Para=5 Unpara=3 Para=5 Unpara=2 Para=3 May 13 CHC Unpara=6 Para=3 Unpara=1 Para=3 Unpara=0 Para=0 June 2 *JC Total 80 CHC/JC 25 (31.2) 55 (68.8) 52 (65) 20 (25) 08 (10) *CHC=Common Hawk Cuckoo; JC=Jacobin Cuckoo Different plant species were used by the Jungle babblers for nest building at different nesting height. The highest number of nests (n=19) were found in Acacia (Acacia auriculiformis) and lowest (n=2) in Coconut (Cocos nucifera) tree (Table 2). The mean nest height from the ground was 4.24 meter for parasitized nest where it was 5.61 for unparasitized nest (Table 2). Breeding Jungle babbler groups consisting of 4 to 15 individuals were followed for periods varying from 1 to 5 hours. The flock size varied during breeding and non-breeding season. During non-breeding season 11 to 15 individuals were observed foraging in a large flock which may remain throughout the breeding season. However, in some cases during breeding season it splits into a group of 5 to 8 birds in a flock which consists of 5 to 6 individuals commonly known as helpers with the breeding pair. Difference was found in the flock or group size for parasitized and unparasitized nests of Jungle babbler. Flock size varied from 4 to 8 in parasitized nests whereas it ranged from for unparasitized nests (Table 2). Predation pressure (N= 12) was also high in case of small flock size ranged from 6 to 9 for unparasitized nests. Page 8
4 Table 2: Unparasitized and parasitized nests with flock size and nest height Unparasitized nest Parasitized nest Acacia auriculiformis Albizia lebbeck Nesting tree Shorea robusta Tectona grandis Lagerstroemia speciosa Mangifera indica Polyalthia longifolia Artocarpus heterophyllus Swietenia mahagoni Mimusops elengi Acacia auriculiformis Albizia lebbeck Shorea robusta Syzygium cumini Lagerstroemia speciosa Mangifera indica Polyalthia longifolia Swietenia mahagoni Gmelina arborea Azadirachta indica Cocos nucifera Mean flock size (range) 10.6 (10-14) 7.04 (4-8) Mean nest height in meter (range) 5.61 (1-13) 4.24 (3-7) Successful nest Predated nest Deserted nest The clutch size was measured only from unparasitized nest because for parasitized nest it was unknown of exactly how many eggs were removed by the cuckoos. In parasitized nests of Jungle babbler, single cuckoo egg found when it was parasitized by Common hawk cuckoo whereas two cuckoo eggs found when it was parasitized by Jacobin cuckoo. Common hawk cuckoo and Jacobin cuckoo eggs were highly mimetic to the eggs of the Jungle babbler in both color pattern and size. The mimicry score was 1.1; n=3 and 1.0; n=1 respectively (Fig.2). The Jungle babbler eggs were deep turquoise blue and glossy in texture whereas, the Common hawk cuckoo eggs were similar in color but less glossy and slightly more elongated. The Jacobin cuckoo eggs were similar in color and glossy but slightly smaller and roundish than host eggs (Fig. 2). The number of host young fledged between parasitized and unparasitized varied significantly in Jungle babbler as Common hawk cuckoo chicks are evictor. Common hawk cuckoo nestlings evicted all host eggs or nestlings (Fig.3). There was only two parasitized nest of Jungle babbler which was parasitized by Jacobin cuckoo where two cuckoo chicks in each nest fledged as Jacobin cuckoo is a non-evictor cuckoo (Fig.3). Fig 2: Eggs of Jacobin cuckoo (2) and Jungle babbler (2) from left to right (Upper); Eggs of Common hawk cuckoo (1) and Jungle babbler (2) from left to right (Lower) Page 9
5 Fig 3: Common hawk cuckoo chick (Upper left) and Jacobin cuckoo chicks with host egg (Upper right); Jungle babbler feeding Common hawk cuckoo chick (Lower) 4. Discussion Jungle babblers form a complex and stable society and are very social in foraging and even during breeding. The habit of foraging and cooperative breeding in small groups which may vary in number from 6 to 10 has made them the names like Seven Sisters or Sath Bhai 3, 16. Jungle babblers also vary in number from 2-20 individuals 18. The group size also ranges from 4 to 16 individuals 3. Such groups usually consist of a breeding female, a dominant male breeder, and non-breeding helpers 12. Predation pressure was very high in both parasitized and unparasitized nests. The host could still avoid brood parasitism by nest desertion, however, higher predation and parasitism risks later in the season makes desertion more costly than accepting the cuckoo egg. It is therefore still a mystery why rejection behaviour has not evolved in Jungle babbler. One probable reason could be that costs of rejection are higher than the benefits, as found in Cape bulbuls Pycnonotus capensis parasitized by Jacobin cuckoos 23. In Jungle babblers, the observations on the breeding males and breeding females as well as in the helper females suggesting that the nest defense, taking care of eggs, incubating them and protecting the young ones is a combined flock activity 12. The individuals of the groups were seen foraging close together in different parts of their home range. Two or one members of the group perch usually higher from where they can look into the surrounding for parasites or predators. The other foraging members of the group get benefitted from the vigilance by guarding individuals. It appears that there is a sort of reciprocal relationship between the individuals of the flock of babblers while foraging and during breeding. The helpers forgo their breeding in order to assist the breeding pair 12. In large flocks, non-breeding member or helper birds were observed driving potential predators and parasites away from the vicinity of the nest on a number of occasions. In many cases the interactions involved the participation of most members of the group, but in some only one or a few birds were involved. The rigorous mobbing of a babbler group was generally sufficient to drive away any potential predator 17. Jungle babblers were parasitized by both the Common hawk cuckoo and the Jacobin cuckoo during the study period. If two or more cuckoos parasitize the same host species it may be predicted that they should show other fundamental differences in their breeding ecology. In support of this prediction, it has been found that the breeding season of the Common hawk cuckoo was much earlier (March) than for the Jacobin cuckoo (June). The Jungle babbler was parasitized at a considerably higher rate by Common hawk cuckoos than by Jacobin cuckoos. The arrival date of these two cuckoo species in the breeding ground suggests that the intensity of Common hawk cuckoo parasitism was highest during March through May, while that of Jacobin cuckoo parasitism Page 10
6 was at the beginning of June during the short term occurrence of this cuckoo in the study area. Gaston (1976) 17 recorded that the overall laying pattern in Jungle babblers is two-peaked, one in March through April and the other peak intensity in July and September with a reduced laying rate in August. A possible reason for the very low parasitism rate of the Jacobin cuckoo in the study area could be that the Jungle babbler nearly seized its breeding in June. It was not possible to estimate the exact number of Jacobin cuckoos, but not more than 2-3 individual birds were observed each year in the beginning of June. After July none were seen in the study area supporting that they were present for a very short period. The first Common hawk cuckoo egg was laid in the middle of March in a Jungle babbler nest, while Jungle babblers started breeding in mid-february. Early breeding could thus be a strategy to avoid parasitism 10. In Bangladesh, the clutch size of Jungle babbler consists of 3 to 5 eggs, but in India, they occasionally lay up to 7 eggs 18. The Jacobin cuckoo (Clamator jacobinus) is an obligate brood parasite with three subspecies 30. Two lay a mimetic blue egg that also matches the host eggs in size, while the subspecies in southern Africa (Clamator jacobinus serratus) parasitizes bulbuls (Pycnonotus spp.) and lays a non-mimetic white egg which is also much larger than the host eggs. The blue eggs of Common hawk cuckoos and Jacobin cuckoos appear highly mimetic to the eggs of Jungle babblers in colour 7, 27. A possible explanation is that the appearance of these two cuckoo species eggs has evolved as a response to rejection by other host species (e.g. other babblers) that also lay blue eggs. If this is the case, egg mimicry in jungle babblers is a fortunate pre-adaptation 11. A pair of Jungle babblers completely destroyed their nest after observing a Common hawk cuckoo near it (S. Begum unpubl. data), indicating that babblers may look upon cuckoos as a threat. The Jacobin cuckoo s late arrival in the study area might theoretically be an adaptation to avoid Common hawk cuckoo nestlings in the nest of the same host thus, promoting survival of their own chicks. Like in other Clamator species 13, 45, 46, the young cuckoo does not evict or kill host young but is raised with them, at least initially 23. Under the evolutionary equilibrium hypothesis, nest parasitism is tolerated because of conflicting selection pressures 35, 50. Costs of ejection errors or abandonment of nests, representing losses of host eggs and energy expended in replacement nesting, may outweigh the costs of raising parasite young; thus, acceptance could be evolutionarily favoured 25. For some hosts, it is simply difficult to puncture the cuckoo egg 4 or they may fail to reject large eggs because rejection costs are too high 39, 47. This may force them to accept cuckoo eggs. The present study of cuckoo-host systems revealed that flock size of Jungle babbler is an important positive predictor of the likelihood of parasitism. The nests of Jungle babbler with flock size from 4 to 8 were significantly more likely to be parasitized than those groups with flock size from 10 to 14. The study also showed remarkably high acceptance of parasitic eggs in host, which might be explained by the existence of lag in the evolution of rejection responses, as suggested for many cowbird hosts 22, 38. The study reveals that host populations are likely not able to recognise parasitic eggs 37 or brood parasitic birds 5, 48 or lack appropriate responses to foreign eggs. 5. Conclusion It has been found that the host species Jungle babbler is used as host by two species of cuckoos Common hawk cuckoo and Jacobin cuckoo, experiencing high parasitism and predation while with small flock size. Although in both cases highly mimetic, the cuckoo egg was accepted by the host, leading to a aparent reduction in host breeding success. Further experimental studies to provide a better understanding of the egg recognition ability in this host are highly recommended. The findings provide a valuable background for further studies designed to understand the interactions between the parasitic cuckoos and their common host species as well the breeding success of both the host and parasitic cuckoos. 6. Acknowledgements I thank Md. Yousuf and Monoronjon for their help in fieldwork. I also thank to Dr. Md. Kamrul Hasan for photograph on Jungle babbler feeding the cuckoo chick. I am indebted to all members and staffs in the Wildlife Research Group, Department of Zoology, Jahangirnagar University for cooperation during data collection in the field. I am furthermore grateful to all the members of the Brood Parasitism Research Group, Department of Biology, Norwegian University of Science and Technology (NTNU) for valuable suggestions during my field work. The study was supported by a Grant through a Quota Scheme at NTNU. 7. References 1. Ali S. The birds of Kerala. Oxford University Press, Bombay, India Ali S, Ripley SD. Compact handbook of the birds of India and Pakistan, (2 nd edition). Bombay. Oxford University Press Page 11
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