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Genetic Monogamy in Von Der Decken's and Northern Red-Billed

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Genetic Monogamy in Von Der Decken's and Northern Red-Billed IUCN HSG Genetic monogamy in Von der Decken’s and Northern Red-billed hornbills Margaret F. Kinnaird1* and Timothy G. O’Brien2 1World Wide Fund for Nature International, Nairobi, Kenya 2Wildlife Conservation Society, Nairobi, Kenya *Corresponding author - [email protected] Abstract Avian monogamy is usually characterized by pair bond between a male and female, often social monogamy, a cooperative pair bond characterized by cooperation in resource ac- rather than genetic monogamy, a pair bond ac- companied by fidelity. Hornbills (Bucerotidae, quisition and parental care (Bennett and Ow- Bucorvidae) have a range of monogamous so- ens 2002). Genetic monogamy is defined as an cial systems, but only one species, Monteiro’s exclusive pair bond accompanied by exclusive hornbill (Tockus monteiri) has been confirmed parentage or fidelity (Gowaty 1996, Reichard to be genetically monogamous. We exam- ined paternity patterns for two Tockus species, 2003). Social and genetic monogamy are not Northern Red-billed hornbill (T. erythrorynchus) always equivalent; on average, 12.5% of off- and Von der Decken’s hornbill ( ). spring of socially monogamous species result We collected blood from females and chicks from extra-pair copulations (Bennett and Owen in nestboxes, and the putative father deliver- ing food to the nestbox, or accompanying ju- 2002). venile birds. Paternity was determined using a double-digest restriction site-associated DNA sequencing (ddRAD-seq). All males delivering Asian hornbill species exhibit four monoga- food for both species (n = 35 males). For males mous social systems including nomadic pairs, accompanying juveniles, 14 of 15 putative fa- part-time territorial pairs, year-round territorial thers were identified as the genetic father. Our results extend the occurrence of genetic mo- pairs, and territorial family groups (Kinnaird and nogamy to three species of Tockus hornbills. O’Brien 2007). Among African hornbills, savan- na species including ground-hornbills (Bucor- vus spp.) and Tockus hornbills (Tockus spp.) are Keywords: genetic monogamy, Tockus hornbills, pair bonds, fidelity the best studied (Kemp 1995). Ground-hornbills are cooperative breeders on large territories and savanna Tockus hornbills are monogamous Introduction pairs on part-time or year-round territories. Avian monogamy has been a topic of inter- est for many decades (Lack 1968). However, Only one study has been published on genet- only recently has social monogamy been dis- ic monogamy in a hornbill species, Monteiro’s tinguished from genetic monogamy. Social Hornbill (Tockus monteiri) in Namibia (Stanback monogamy (85% of bird species) is defined et al. 2002), where blood was obtained from 38 as an exclusive living arrangement involving a hornbill families including 138 chicks. No evi- 12 Vol. 1(1):12–16, 2020 PB IUCN HSG Hornbill Nat. Hist. & Conserv. dence of extra-pair copulations was found and door for examining the female and chicks (Fig. all chicks were assigned to their putative father. 1). Boxes were placed in trees or on 4 m poles In this paper, we report on the results of a pa- along service roads. Boxes were examined ev- ternity analysis of chicks of two African savanna ery 4 days. Blood samples were obtained from hornbill species, Von der Decken’s hornbill (T. females in nestboxes after chicks were hatched, deckeni) and Northern Red-billed hornbill (T. and from chicks 2 weeks after hatching. Finally, erythrorhynchus) in northern Kenya. males delivering food to nest boxes were cap- tured using mist nests placed in front of nest boxes and using recorded male hornbill calls Methods as an audio lure. All hornbills were tagged with This project was conducted at the Mpala Ranch a National Museums of Kenya metal identifica- and Research Center, Laikipia County, Ken- tion leg band and colored plastic leg bands. ya (0.284 – 0.5248 N and 36.828 – 36.8838 E). Mpala Ranch is a 200 km2 cattle ranch and wildlife conservancy. Topographically, Mpala Genetic analysis was conducted at the Cornell Ranch consists of rolling hills, an uplifted pla- Laboratory of Ornithology to identify the genet- teau, granitic inselbergs, and is bordered by ic parentage of chicks. They used a double-di- rivers along more than half of its boundary. An- gest restriction site-associated DNA sequenc- nual rainfall averages 594 mm in the south and ing (ddRAD-seq: Puritz et al. 2014) analysis. 430 mm in the north, with rains typically occur- This approach simultaneously locates single nu- ring during April-May and October-November. cleotide polymorphisms (SNP) and genotyping Droughts are sporadic, but increasing in fre- steps and is optimized to return a statistically quency (Franz 2007). The landscape is covered powerful set of SNP markers (typically 150-600 by bushland dominated by Acacia mellifera, A. after stringent filtering) from large numbers of etbaica, A. brevispica, and Grewia tenax, and individuals (up to 240 per run). For full details of by A. drepanolobium open woodland. Hornbill the analysis, see Thrasher et al. (2017). species observed on the ranch include Eastern yellow-billed (T. flavirostris), Crowned (T. albo- Results terminatus), Northern red-billed (T. erythroryn- chus), Von der Decken’s (T. deckeni), African We monitored 10 Northern red-billed horn- grey (T. nasutus) and Silvery-cheeked hornbills bill (NRBH) successful nesting events in 2012 (Bycanistes brevis). Only Von der Decken’s and (n = 2), 2013 (n = 3), and 2015 (n = 5) involv- Northern red-billed hornbills have been ob- ing nine females and 19 chicks, and captured served to breed on Mpala. four young juvenile birds with putative fathers in walk-in traps. For Von der Decken’s hornbills (VDDH), we monitored 27 successful nesting We used three strategies to capture hornbills. events in 2012 (n = 2), 2013 (n = 9), 2014 (n = 6) First, we used walk-in traps, baited with pea- and 2015 (n = 10) involving 26 females and 40 nuts and set around the Mpala Research Cen- chicks, and 11 capture events involving young ter from 2011 to 2015. Second, we deployed juveniles traveling with an adult. For chicks 90 nest boxes during the breeding seasons of banded and bled at the nest site, we had 100% March – July 2012 through 2015. Boxes were assignment of social father to genetic father for 25 x 20 x 50 cm with a 6 cm diameter entrance, both species. For four cases of juvenile NRBH a perch below the hole, and a lockable side captured with an associated adult male, in all 13 PB IUCN HSG Fig. 1. Male Von der Decken’s hornbill delivering a beetle to female in nestbox. cases, the adult male was the genetic father. believed that the threat of withholding food For 11 cases of juvenile VDDH captured with from females was sufficient to constrain her, an associated adult male, in 10 of 11 cases, the since female Tockus hornbills generally molt tail male was identified as the genetic father. and wing feathers during incubation and are unable to fly, and male desertion would doom the female and her chicks. Such conflict-medi- Discussion ated reproductive strategies assume that costs Our results extend the finding of genetic mo- incurred are tolerable for (at least) one sex and nogamy in Montiero’s hornbill (Stanbeck et al. that one sex gains at a cost to the other (Mock 2002) to two additional Tockus species, North- and Forbes 1992). ern red-billed and Von der Decken’s hornbills. Tockus hornbills exhibit several characteristics Stanback et al. (2002) note that mate guarding of long-term monogamy including year-long is not particularly strong in Montiero’s hornbills associations, territoriality, courtship feeding and Finnie (2012) found the same in Southern and sperm storage. Mulder et al. (1994) argued yellow-billed hornbills (T. leucomelas). This that any tendency toward extra pair copula- loose guarding, combined with sperm storage, tions in birds would be a compromise between allows for the possibility of extra-pair copula- females seeking genetically superior males and tions prior to entering the nest. Purple Sand- her dependence on male provisioning during pipers (Calidris maritima) are long-lived, social- nesting. Gowaty (1996) also believed that the ly monogamous sandpipers also characterized female should always seek a genetically superi- by strong mate and territory fidelity, high male or male and that socially bonded males should parental investment and loose mate guarding, attempt to restrict access to females through that rarely seek extra-pair copulations (Pierce mate guarding or other constraints. Gowaty 14 PB IUCN HSG Hornbill Nat. Hist. & Conserv. and Lifjeld 1998). Both Stanback et al (2002) evolved as an anti-predator behavior which in and Pierce and Lifjeld (1998) argue that, when turn led to long-term sperm storage, high male male paternal investment is high, the females investment, and cooperation over conflict. We have little to gain from extra-pair copulations argue that if nest sealing was an effective an- and should resist extra-pair copulations, mak- ti-predator behavior, it should have evolved ing male attempts energetically expensive. more often among cavity nesters (Kinnaird and Stanback et al. (2002) also argue that the com- O’Brien, 2008). Although hornbills have higher plete dependence of female and chicks on nesting success than other cavity nesting spe- male provisioning results in a strong overlap in cies, the result is not significantly different. We reproductive interests of males and females, re- believe that female nest sealing evolved as a sulting in cooperation rather than conflict. female strategy to ensure the cooperation of the male. For seven females (NRBH = 1 and VDDH = 6) that nested at least twice during our study, we Our study strengthens the argument that Tock- found that the same male was the father af- us hornbills are genetically monogamous as ter two to four years, indicating extended pair well as socially monogamous. It also leads us bonds in both Tockus species.
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