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Diet of the Bobolink (Dolichonyx oryzivorus) in rice fields on its wintering grounds in Argentina

Diet of the Bobolink (Dolichonyx oryzivorus) in rice fields on its wintering grounds in Argentina Revista Brasileira de Ornitologia 27(1): 10 0 0–16 6 6. ARTICLE March 2019 Diet of the Bobolink ( ( (Dolichonyx oryzivorus s s) in rice fi elds on its wintering grounds in A A Argentina 1,5 1 2 3 1 R R Rodrigo E. Lorenzón , Carolina E. A A Antoniazzi , Franco N. Fabre , Virginia M. Quiroga a a , Silvia A. R R Regner , 4 1 1 1 A A Ana L. R R Ronchi-Virgolini , Pamela F. Olguin , E E Evelina J. Leon & A A Adolfo H. Beltzer Instituto Nacional de Limnología (CONICET-UNL), Ciudad Universitaria, Santa Fe, Argentina. Facultad de Humanidades y Ciencias (FHUC-UNL), Ciudad Universitaria, Santa Fe, Argentina. Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción (CICyTTP-CONICET), Matteri y España, Diamant e, Argentina. Universidad Autónoma de Entre Ríos (UADER), Corrientes y Andrés Pasos, Paraná, Argentina. Corresponding author: roylorenzon@gmail.com Received on 29 September 2018. Accepted on 12 March 2019. ABSTRACT T T: Winter diet of Bobolinks (Dolichonyx oryzivorus s s), a bird considered a pest of rice fi elds, is known to consist primarily of seeds. However, it is not yet possible to establish the extent to which non-rice plants and animal components contribute to its diet. To contribute to these issues, we studied the diet of the Bobolink found in rice fields on its wintering grounds in Santa Fe, Argentina, to provide information on (i) the composition of the diet and (ii) the relative importance of plant and animal components in the diet and of the diff erent prey categories. We captured Bobolinks with mist nets and obtained samples of stomach contents by warm water and emetic-based regurgitation to determine the composition of the diet (n = 46 samples) and the importance of the different pre y (n = 25 samples), mainly during March, just prior to northbound migration. We confi rmed that the Bobolink's diet in this region during this period is predominantly herbivorous (97%) and rice-based (55%), although it also consumes a large number of seeds of non-cultivated plants that represented 42% of the diet. Invertebrates, although of less importance than plant components (3%), had been consumed by 97% of captured individuals. Our results document the importance of non-cultivated plants and animal prey in the diet of Bobolinks in addition to rice. K K KE E EY-WORDS: agroecosystems, birds, emetic, foraging, pests. INTR R RODUCTION relies on rice during austral summer remains largely unknown (Renfrew et al. 2017). Although the diet of Bobolink (Dolichonyx oryzivorus s s), an obligate-grassland Bobolink on its wintering grounds is known to consist species, has one of the longest annual migrations of any primarily of plant material (Renfrew & Saavedra 2007), New World passerine (≈ 20,000 km round trip), with no empirical studies have established the importance of breeding and wintering grounds located in North America rice and animal parts (invertebrates) in relation to other and South America, respectively (Renfrew et al. 2015). items in the diet. Recently, Renfrew et al. (2017) used Reports of population declines on the breeding grounds stable isotopes to demonstrate that Bobolinks rely on (Sauer et al. 2004) highlighted the need for studies on rice for approximately one-third of their diet and that the natural history and ecology of the species, in order importance of rice in the diet is higher in rice fields than to identify threats to the development of conservation in natural grasslands within their wintering grounds. strategies, mainly on the wintering grounds where studies Beyond these contributions, however, yet there is have been more limited (Renfrew et al. 2015). no quantitative information on the diet of the Bobolink Knowledge of Bobolink ecology on its wintering on diff erent parts of its wintering grounds, information grounds has increased significantly in the last decade necessary for a more precise quantification of damages (López-Lanús et al. 2007, Renfrew & Saavedra 2007). and benefits that the s pecies contributed to rice-field Additional research needed to guide conservation of agroecosystems, based on the relative importance of rice, Bobolinks includes investigating its trophic ecology on non-cultivated plants and invertebrates in the Bobolink wintering grounds (Renfrew & Saavedra 2007, Blanco & diet. Here, we studied the diet of Bobolinks found on López-Lanús 2008), because the Bobolink is considered rice fi elds in Santa Fe, Argentina, an area where a large a pest of rice fields (Ló pez-Lanús et al. 2007, Renfrew & concentration > 100,000 individuals has been documented Saavedra 2007), although the extent to which the species during several seasons (López-Lanús et al. 2007, López- Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. placed one to three mist nets in foraging sites and near Lanús & Marino 2010). Our objectives were to provide day roosts. We opened the mist nets only after we had information on (i) the diet of the species and (ii) the observed foraging behavior of flocks for at least 2 h to relative importance of plant and animal components of the diet and of the different prey cate gories. obtain captures after individuals have foraged to increase the regurgitation rate (Durães & Marini 2003). We assessed the diet with a combination of techniques. METHODS First, we used warm water to force regurgitation because this technique is considered less harmful to the bird than Study area emetic-based regurgitation, although also less effective (Major 1990, Poulin et al. 1994). Warm water was Th e study area included the rice zone located in the administered orally into the beak and down the esophagus eastern part of Santa Fe province, Argentina (Fig. 1). This by means of a 1 cm syringe connected to a 1.5 mm zone covers a north-south band, approximately 10–20 km diameter silicone tube that had been moistened in saline wide, west of the San Javier River, part of the Paraná River solution or vaseline. We inverted the bird over a plastic o o system, from approximately Romang (29 29'S; 59 45'W) cup so that, as fluid was forced into its stomach, the excess o o in the north to Cayasta (31 11'S; 60 9'W) in the south. fluid plus the stomach contents flowed into the cu p (Hess This area is characterized by xero philous forests of the 1997). We obtained 13 samples using this technique. Espinal ecoregion at higher elevations, and by marshes Individuals that did not regurgitate on the fi rst attempt and fl ooded grasslands in lower elevations (López-Lanús were released to minimize stress. Preliminary inspection & Marino 2010). in the laboratory revealed few food items, represented by highly disaggregated seeds and arthropods. Given the Bird captures and samples of stomach contents low eff ectiveness of this method because very little food was regurgitated, we chose to use an emetic (potassium We captured Bobolinks (n = 70 individuals) with mist antimony tartrate) to obtain additional samples of nets to obtain samples of stomach contents in three rice stomach contents. Following Poulin et al. (1994), we gave fi elds from 14 January to 12 March 2016 (Fig. 1). We birds 0.8 cm of a 1.5% solution of antimony potassium Figure 1. Location of the thr fh h ee rice fields ( fi ld ( ( ( (A A, B B and d C C)) wh here Bbl Bobolinkks ((D Dl olichonyx or h yzivorus s) w ) ere captured in mist nets and d sampled for gut contents. Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. tartrate per 100 g of body mass. After the solution was the abundance (N%), frequency of occurrence (F%), given orally through a 1.5-mm diameter flexible plastic volume (V%) and index of relative importance (IRI%) tube attached to a l cm syringe, we placed the bird in a of each category of prey to determine the contribution small box lined with absorbent paper for 15 to 20 min of each category to the diet of the species. We calculated to allow them to regurgitate and also to recover after the biovolume of ingested categories by approximation to regurgitation (Poulin et al. 1994, Johnson et al. 2002, regular geometric shapes. The volume of fractionated and Carlisle & Holberton 2006). We obtained 23 samples disarticulated prey was estimated by comparison with using this technique after which we discontinued its use reference prey. However, this was implemented mostly because mortality rate was high (33%, n = 10 individuals). for animal prey since seeds were found intact in most Two additional samples were from the stomach contents cases. Index of relative importance of prey (Pinkas et al. analysis of two individuals that did not regurgitate and 1970) was used to determine the importance of each prey died. Dead individuals were collected and deposited in category in the diet. the collection of the National Institute of Limnology (INALI: CONICET-UNL). Subsequently, we resumed RESULTS using the saline solution regurgitation method obtaining eight more samples, and all of these birds were released successfully after samples were obtained. All gut contents General composition of the diet were preserved in 70% ethanol. We recorded 1597 items from all samples (n = 46 samples), A A Analysis of digestive tract contents corresponding to 17 food item categories (Table 1). Of the total items, 1521 (95%) were from plants, represented by We examined contents of digestive tracts under a 6 families and 10 plant species (in the case of rice, Oryza Nikon® stereoscope binocular. We counted, measured sativa, two varieties were recorded and treated separately: and classified prey cate gories to the lowest possible Rice and Red Rice, cultivated and weed, respectively) and taxonomic level. We considered all samples, regardless of 76 items (5%) were from invertebrates, represented by the collection technique to inventory the total number 6 orders (Table 1). Plant items were mainly Cyperaceae of prey items found in the diet of Bobolink (n = 46 (48%) and Poaceae (43%). Th e high degree of digestion samples). Th ese samples were obtained from 14 January did not allow finer taxonomic resolution of invertebrate to 12 March 2016. However, to assess relative importance samples, with the exception of nymphs of Hemiptera of prey categories, we did not use samples obtained by assigned to the family Pyrrhocoridae and a Hemipteran water-based forced regurgitation because this technique assigned to the family Lygaeidae. likely under sampled vegetal fraction of stomach contents (26.4 vs. 2.6 plants by sample in emetic- and water- R R Relative importance of prey categories based forced regurgitation samples, respectively) aff ecting the comparison with the animal fraction, which was Among the 25 individuals represented by complete (or affected, but to a lesser extent, by the techni que (1.4 vs. mostly complete) stomach contents, plants represented 0.5 animal prey by sample in emetic- and water-based almost the entire diet (IRI% = 97%), while animals forced regurgitation samples, respectively). Thus, we were a minor component (IRI% = 3%), refl ecting the calculated the number and frequency of prey types only greater number and volume of seeds in the diet (Table from 25 samples to assess relative importance of prey 1). However, although only 4% of the total number of categories, 15 represented only by emetic samples, two prey items was invertebrates, 92% of the samples had at only by digestive tract dissection, and eight represented least one item from this category, indicating that most by both emetic and digestive tract samples. In this way, Bobolink individuals consumed at least some animal the samples considered in this analysis were obtained prey. Th e highest number and frequency of invertebrate only at the beginning of March (between 08–11 March in the diet corresponded to the orders Hemiptera and 2016). Given that we could only identify mature seeds in Coleoptera (Table 1). the digestive tract, the importance of rice in the diet was Rice was the most important component of the diet underestimated because we could not quantify immature because it was the most frequent prey category (F% = liquid or “milky” stages of rice. However, because 73%) and represented the largest volume (V% = 59%) of estimation of relative importance of rice was based on items in the diet (Table 1). Th e most abundant component samples obtained in the fi nal stage of rice production of the diet was a species of the family Cyperaceae (N% = during March, it is unlikely that the immature liquid or 48% vs. N% = 15% for rice) that, although it also had “milk” stage of rice represented a high proportion of the a high frequency among samples (F% = 58%), had a rice consumed at this stage of the crop. We quantified minor relative importance in the diet than rice due to the Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. T T Table 1. Total number (n = 46 samples) and importance (n = 25 samples) of the prey categories found in diet samples of Bobolinks (Dolichonyx oryzivorus s s) on its wintering grounds in Argentina. Prey categories within the plant and animal fractions are arranged in decreasing order according to the number of categories of prey recorded. Values in bold indicate the totals for the plant and animal fractions. The script indicates that the item was not found in this group of samples. Total number of prey categories is based on all samples. Abbreviations: percentages of number (N%), frequency (F%), volume (V%) and index of relative importance (IRI%); NI: not identified . Importance Total number Prey category (n) N% F% V% IRI% Plant fraction1521 96 96 95 97 Echinochloa sp. 235 15 15 6 3 Oryza sativa a (Rice) 232 15 73 59 55 Paspalum sp. 96 6 35 3 3 Oryza sativa a (Red Rice) 94 5 15 20 4 Cyperaceae NI 733 48 58 4 30 Polygonaceae 63 4 42 1 2 Solanum sp. 30 2 8 0 0 Conyza bonariensis 20 1 31 0 0 Amaranthus s sp. 8 0 8 0 0 Sp. NI (Asteraceae?) 5 0 12 0 0 Sp. NI 5 0 4 0 0 A A Animal fraction 76 4 92 5 3 Coleoptera 25 1 42 3 1 Hemiptera 18 1 23 1 1 Diptera 4 0 12 0 0 Hymenoptera 3 0 4 0 0 Psocoptera 2 0 8 0 0 Araneae 1 - - - - Undetermined 23 1 50 0 0 smaller size and volume of the seeds (Table 1). Overall, seeds and fruits of non-rice species were more abundant and frequent than rice among the individuals analyzed, but rice accounted for a greater volume of the diet due to the larger size of the grains (Table 1, Fig. 2). DISCUSSION Bobolinks are persecuted by rice producers in their wintering grounds because they are considered pests of rice crops (López-Lanús et al. 2007, Renfrew & Saavedra 2007). However, knowledge of its trophic ecology on the wintering grounds is limited because, although Renfrew et al. (2017) estimated the importance of rice, no previous study has assessed quantitatively the importance Figure 2. Relative importance index (IRI%) of rice (Oryza of non-cultivated plants and animal prey in their diet. sativa) vs. other plant species in the Bobolink (Dolichonyx In this study, in agreement with previous studies of the oryzivorus s) diet in Santa Fe, Argentina. Abbreviations: species (e.g., Martin & Gavin 1995, Renfrew & Saavedra percentages of number (N%), volume (V%) and frequency 2007), we confirmed that Bobolinks have a diet that is (F%). Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. predominantly herbivorous and rice-based during March, mentioned as part of the Bobolink diet (e.g., Echinochloa just prior to northbound migration (i.e., emetic-based crus-galli, Echinochloa polystachya, Sorghum halepense, samples, on which the calculations of relative importance Hymenachne amplexicaulis s s) were not found in samples of the prey were based, were obtained at the beginning of during our study. this month) in areas of intensive rice production. However, Remaining plant items corresponded to native or our results also indicate that Bobolinks consume more naturalized non-cultivated herbs and mostly coincided seeds of non-cultivated plants. Invertebrates, although with those documented in previous studies. However, fruits of minor importance in relation to plants, were present of Polygonaceae and seeds of Solanum sp. (Solanaceae) in the diet of most individuals, possibly as a result of and Amaranthus s sp. (Amaranthaceae), although of little occasional intake of invertebrates found while birds were importance, had not previously been mentioned as part searching for seeds (e.g., arthropods associated with seeds of the Bobolink diet in the area. Presence of Polygonaceae of plants). species has been reported in the Bobolink diet from breeding and stopover sites in the United States (Beal General composition of the diet 1900, Meanley & Neff 1953). Presence o f Solanum sp. seeds suggests that unless Bobolinks extract the Grains of mature Rice (O. sativa) represented an seeds without ingesting the fruit, Bobolinks could also important fraction of the diet in this study, which is in consume fleshy fruits such as those of these plant species. agreement with previous studies that have examined Solanaceae species have not been mentioned as part of the diet composition of Bobolinks in rice fields within their Bobolink diet in any previous study and, thus, this could wintering area (e.g., López-Lanús et al. 2007, Renfrew simply correspond to an occasional intake, although it & Saavedra 2007, Blanco & López-Lanús 2008). Rice was found in samples from two individuals in rice field B. was more important in the diet because it was abundant, Results of the current study also have expanded our frequent, and comprised the greatest volume of the plant knowledge of invertebrates consumed by Bobolinks. For component in the diet. The observed relative im portance example, although Hemiptera have been mentioned as of rice in the Bobolink diet (55%) was lower than that present in the diet of the Bobolinks in the wintering area reported by Renfrew et al. (2017), who found that the (López-Lanús & Marino 2010), the present study provides relative proportion of rice was approximately 69% in a the fi rst documentation of Hemiptera in diet samples; rice-producing region in Bolivia. Our results about the eight Hemiptera nymphs were found in the sample from relative importance of the rice correspond only to the a single individual Bobolink. Similarly, although some of days before harvest, i.e. we only used samples obtained the recorded invertebrate prey have been documented in by emetics and stomach analysis obtained between 08– samples from breeding and stopover sites (e.g., Coleoptera, 11 March 2016 to determine the relative importance of Hemiptera, Hymenoptera and Araneae; Beal 1900, the different prey, when the rice is already in a mature Meanley & Neff 1953), documentation of invertebrate and hard stage. Under these conditions, Bobolinks could prey in the diet of Bobolinks on their wintering grounds include a greater proportion of other plants in their diet was previously limited to caterpillars (Lepidoptera; Renfrew because rice is no longer found in the milky and soft & Saavedra 2007, López-Lanús et al. 2008). stages preferred by the species in the studied rice fi elds. Echinochloa a sp. and a Cyperaceae species were Considerations on the techniques used to study among the most abundant food items. However, because Bobolink diet these seeds and fruits are small, these were lower in volume of diet and relative importance than rice. Seeds Our study showed that water-based forced regurgitation of Echinochloa a sp. probably corresponded to E. colona, is a technique much less effective than emetic-based a naturalized grass introduced from Europe (Pensiero & technique to study the Bobolink's diet. However, use Gutiérrez 2005) that previously was reported by López- of emetic implied a relatively high mortality rate that Lanús et al. (2008) as part of the diet of Bobolinks in the limited the number of samples obtained. This contrasts same area. Cyperus s sp. is among the probable Cyperaceae with studies that have shown that mortality caused by genera corresponding to the species found in the rice emetics is relatively low in icterids (Poulin et al. 1994, fi eld A, because this also has been reported as part of the Poulin & Lefebvre 1995). However, responsiveness to diet of Bobolink in the area (López-Lanús et al. 2008). emetics is highly species-specifi c (Durães & Marini 2003). The same stud y also mentioned that Bobolinks feed on Although the manipulation of birds mainly during the oral Conyza bonariensis, a grass species that was also found administration into the beak and down the esophagus by during the present study, mainly in samples from field A, means of a syringe connected to a silicone tube can cause where grasslands composed of this plant were observed. damage to the birds if not implemented correctly, all the Other plant species present in the area that have been birds that received the same treatment, but with warm Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. water were not damaged and were successfully released. Alianza del Pastizal and BirdLife International. We This indicates that the mortality was directly related to the are grateful to A. Muchiutti and G. Marino for their emetic and not to the manipulation. Emetic solution was assistance throughout the development of this project, prepared in laboratory by a professional chemist to assure to A. Galimberti for assistance in the field work, to rice a correct preparation. Characteristics that differentiate the workers Cooperativa de Arroceros de Villa Elisa, Questa a and Bobolink from other icterids like the high energetic cost San Roque e for allowing us to work in the rice fields, to of migration and the use of agrochemicals in rice fields B. Schneider (INALI-CONICET-UNL) for help in the where they feed could be related to this sensitivity to the identification of collected plants, to J.G. Blake for English emetic. Th ese aspects could be evaluated by studying the editing and constructive comments on the drafts of this health conditions of these populations. Beyond this, we paper and to an anonymous reviewer that contributed to do not recommend the use of emetics for the study of improve the manuscript. The study was authorized by the the diet of Bobolink. Alternatively, the use of water-based Dirección General de Recursos Naturales y Ecología of the forced regurgitation can be used to establish qualitative Ministerio de Medio Ambiente de la Provincia de Santa Fe, lists of ingested prey, and not of their relative importance, Argentina (Administrative Resolution 060-16). because of the little food regurgitated by this technique in relation to the use of emetic. Other techniques such as the use of stable isotopes and the genetic analysis of feces REFERENCES could improve our knowledge of the Bobolink diet on its Beal F.E.L. 1900. Food of the Bobolink, Blackbirds and Grackles, v. 13. wintering grounds. Washington: Department of Agriculture, Division of Biological Survey. Conservation implications Blanco D.E. & López-Lanús B. 2008. Ecología no reproductiva y conservación del Charlatán ( ( (Dolichonyx oryzivorus s) en el noreste de Argentina. Buenos Aires: Wetlands International. Our results show that Bobolinks consume a great quantity Carlisle J.D. & Holberton R.L. 2006. Relative efficiency of fecal versus of seeds and grains of non-cultivated plant species. These regurgitated samples for assessing diet and the deleterious eff ects results are remarkable because we captured Bobolinks of a tartar emetic on migratory birds. Journal of Field Ornithology within rice fields where the rice cro p is the predominant 77: 126–135. land-cover. Th us, these results agreed with the idea that Durães R. & Marini M.Â. 2003. An evaluation of the use of tartar emetic in the study of bird diets in the Atlantic Forest of damage to rice crops could be lower in fi elds that maintain southeastern Brazil. Journal of Field Ornithology y 74: 270–280. the presence of non-cultivated patches and roadsides with Hess C.A. 1997. Stomach fl ushing: sampling the diet of Red-cockaded the presence of naturally occurring grass, which provide Woodpeckers. Wilson Bulletin 109: 535–539. an alternative food source to the Bobolink. Johnson M.D., Ruthrauff D.R., Jones J.G., Tietz J.R. & Robinson J.K. 2002. Short-term eff ects of tartar emetic on re-sighting rates Our results also showed that Bobolinks could of migratory songbirds in the non-breeding season. Journal of contribute to the control of pest insects in rice fields. Field Ornithology 73: 191–196. Although the insect component of the diet was of Kruger R.D. & Burdyn L. 2015. Guía para la identificación de plaga s relatively minor importance, the documentation and del cultivo del Arroz ( ( (Oryza sativa L.) para la provincia de Corrientes. confirmation of the presence of invertebrates in the Corrientes: Instituto Nacional de Tecnología Agropecuaria (INTA). Bobolink diet suggest that Bobolinks can potentially López-Lanús B., Blanco D.E., Serra M., Ducommun M.P., Di have a beneficial role in a groecosystems based on their Giacomo A.S. & Di Giacomo A.G. 2008. Distribución, contribution to the regulation of populations of these evaluación poblacional y usos de las arroceras por el Charlatán insects. This function can be important considerin g (Dolichonyx oryzivorus s s) en Santa Fe, p. 13–22. In: Blanco D.E. & López-Lanús B. (eds.). Ecología no reproductiva y conservación that the number of Bobolinks counted in the region has del Charlatán ( ( (Dolichonyx oryzivorus s) en el noreste de Argentina. exceeded 100,000 individuals (López-Lanús et al. 2007, Buenos Aires: Wetlands International. López-Lanús & Marino 2010). Insects consumed by López-Lanús B. & Marino G.D. 2010. Aportes al conocimiento de la Bobolinks included members of the orders Hemiptera ecología del Charlatán y su estado actual en la provincia de Santa Fe, and Coleoptera, both of which include species that Argentina. Buenos Aires: Aves Argentinas/Asociación Ornitológica del Plata. can damage rice crops (Kruger & Burdyn 2015). The López-Lanús B., Roesler I., Blanco D.E., Petracci P.F., Serra M. & opportunistic behavior shown by the Bobolink to capture Zaccagnini M.E. 2007. Bobolink (Dolichonyx oryzivorus s s) numbers their animal prey can be important when these groups of and non breeding ecology in the rice fields of San Javier, Santa Fe insects become abundant. province, Argentina. Ornitología Neotropicall 18: 493–502. Major R.E. 1990. Stomach flushing of an insectivorous bird: an assessment of differential digestibility of prey and the risk to birds. Wildlife Research 17: 647–657. ACKNOW W WLEDGEMENTS Martin S.G. & Gavin T.A. 1995. Bobolink (Dolichonyx oryzivorus s s). In: Poole A. & Gill F. (eds.). The birds of North Americ a. Washington: Th is study was supported by funds from Aves Argentinas, Academy of Natural Sciences. Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. Meanley B. & Neff J.A. 1953. Food habits of the Bobolink in Arkansas inferred from feather isotopes. Condor 119: 439–448. rice fiel ds. Auk 70: 211–212. Renfrew R.B. & Saavedra A.M. 2007. Ecology and conservation of Pensiero J.F. & Gutiérrez H.F. 2005. Flora vascular de la provincia Bobolinks (Dolichonyx oryzivorus s s) in rice production regions of de Santa Fe: claves para el reconocimiento de las familias y géneros: Bolivia. Ornitología Neotropical 18: 61–73. catálogo sistemático de las especies. Santa Fe: Universidad Nacional Renfrew R.B., Strong A.M., Perlut N.G., Martin S.G. & Gavin T.A. del Litoral. 2015. Bobolink (Dolichonyx oryzivorus s s). In: Rodewald P.G. (ed.). Pinkas L., Oliphant M.S. & Iverson I.L.K. 1970. 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Diet of the Bobolink (Dolichonyx oryzivorus) in rice fields on its wintering grounds in Argentina

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Abstract

Revista Brasileira de Ornitologia 27(1): 10 0 0–16 6 6. ARTICLE March 2019 Diet of the Bobolink ( ( (Dolichonyx oryzivorus s s) in rice fi elds on its wintering grounds in A A Argentina 1,5 1 2 3 1 R R Rodrigo E. Lorenzón , Carolina E. A A Antoniazzi , Franco N. Fabre , Virginia M. Quiroga a a , Silvia A. R R Regner , 4 1 1 1 A A Ana L. R R Ronchi-Virgolini , Pamela F. Olguin , E E Evelina J. Leon & A A Adolfo H. Beltzer Instituto Nacional de Limnología (CONICET-UNL), Ciudad Universitaria, Santa Fe, Argentina. Facultad de Humanidades y Ciencias (FHUC-UNL), Ciudad Universitaria, Santa Fe, Argentina. Centro de Investigaciones Científicas y Transferencia de Tecnología a la Producción (CICyTTP-CONICET), Matteri y España, Diamant e, Argentina. Universidad Autónoma de Entre Ríos (UADER), Corrientes y Andrés Pasos, Paraná, Argentina. Corresponding author: roylorenzon@gmail.com Received on 29 September 2018. Accepted on 12 March 2019. ABSTRACT T T: Winter diet of Bobolinks (Dolichonyx oryzivorus s s), a bird considered a pest of rice fi elds, is known to consist primarily of seeds. However, it is not yet possible to establish the extent to which non-rice plants and animal components contribute to its diet. To contribute to these issues, we studied the diet of the Bobolink found in rice fields on its wintering grounds in Santa Fe, Argentina, to provide information on (i) the composition of the diet and (ii) the relative importance of plant and animal components in the diet and of the diff erent prey categories. We captured Bobolinks with mist nets and obtained samples of stomach contents by warm water and emetic-based regurgitation to determine the composition of the diet (n = 46 samples) and the importance of the different pre y (n = 25 samples), mainly during March, just prior to northbound migration. We confi rmed that the Bobolink's diet in this region during this period is predominantly herbivorous (97%) and rice-based (55%), although it also consumes a large number of seeds of non-cultivated plants that represented 42% of the diet. Invertebrates, although of less importance than plant components (3%), had been consumed by 97% of captured individuals. Our results document the importance of non-cultivated plants and animal prey in the diet of Bobolinks in addition to rice. K K KE E EY-WORDS: agroecosystems, birds, emetic, foraging, pests. INTR R RODUCTION relies on rice during austral summer remains largely unknown (Renfrew et al. 2017). Although the diet of Bobolink (Dolichonyx oryzivorus s s), an obligate-grassland Bobolink on its wintering grounds is known to consist species, has one of the longest annual migrations of any primarily of plant material (Renfrew & Saavedra 2007), New World passerine (≈ 20,000 km round trip), with no empirical studies have established the importance of breeding and wintering grounds located in North America rice and animal parts (invertebrates) in relation to other and South America, respectively (Renfrew et al. 2015). items in the diet. Recently, Renfrew et al. (2017) used Reports of population declines on the breeding grounds stable isotopes to demonstrate that Bobolinks rely on (Sauer et al. 2004) highlighted the need for studies on rice for approximately one-third of their diet and that the natural history and ecology of the species, in order importance of rice in the diet is higher in rice fields than to identify threats to the development of conservation in natural grasslands within their wintering grounds. strategies, mainly on the wintering grounds where studies Beyond these contributions, however, yet there is have been more limited (Renfrew et al. 2015). no quantitative information on the diet of the Bobolink Knowledge of Bobolink ecology on its wintering on diff erent parts of its wintering grounds, information grounds has increased significantly in the last decade necessary for a more precise quantification of damages (López-Lanús et al. 2007, Renfrew & Saavedra 2007). and benefits that the s pecies contributed to rice-field Additional research needed to guide conservation of agroecosystems, based on the relative importance of rice, Bobolinks includes investigating its trophic ecology on non-cultivated plants and invertebrates in the Bobolink wintering grounds (Renfrew & Saavedra 2007, Blanco & diet. Here, we studied the diet of Bobolinks found on López-Lanús 2008), because the Bobolink is considered rice fi elds in Santa Fe, Argentina, an area where a large a pest of rice fields (Ló pez-Lanús et al. 2007, Renfrew & concentration > 100,000 individuals has been documented Saavedra 2007), although the extent to which the species during several seasons (López-Lanús et al. 2007, López- Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. placed one to three mist nets in foraging sites and near Lanús & Marino 2010). Our objectives were to provide day roosts. We opened the mist nets only after we had information on (i) the diet of the species and (ii) the observed foraging behavior of flocks for at least 2 h to relative importance of plant and animal components of the diet and of the different prey cate gories. obtain captures after individuals have foraged to increase the regurgitation rate (Durães & Marini 2003). We assessed the diet with a combination of techniques. METHODS First, we used warm water to force regurgitation because this technique is considered less harmful to the bird than Study area emetic-based regurgitation, although also less effective (Major 1990, Poulin et al. 1994). Warm water was Th e study area included the rice zone located in the administered orally into the beak and down the esophagus eastern part of Santa Fe province, Argentina (Fig. 1). This by means of a 1 cm syringe connected to a 1.5 mm zone covers a north-south band, approximately 10–20 km diameter silicone tube that had been moistened in saline wide, west of the San Javier River, part of the Paraná River solution or vaseline. We inverted the bird over a plastic o o system, from approximately Romang (29 29'S; 59 45'W) cup so that, as fluid was forced into its stomach, the excess o o in the north to Cayasta (31 11'S; 60 9'W) in the south. fluid plus the stomach contents flowed into the cu p (Hess This area is characterized by xero philous forests of the 1997). We obtained 13 samples using this technique. Espinal ecoregion at higher elevations, and by marshes Individuals that did not regurgitate on the fi rst attempt and fl ooded grasslands in lower elevations (López-Lanús were released to minimize stress. Preliminary inspection & Marino 2010). in the laboratory revealed few food items, represented by highly disaggregated seeds and arthropods. Given the Bird captures and samples of stomach contents low eff ectiveness of this method because very little food was regurgitated, we chose to use an emetic (potassium We captured Bobolinks (n = 70 individuals) with mist antimony tartrate) to obtain additional samples of nets to obtain samples of stomach contents in three rice stomach contents. Following Poulin et al. (1994), we gave fi elds from 14 January to 12 March 2016 (Fig. 1). We birds 0.8 cm of a 1.5% solution of antimony potassium Figure 1. Location of the thr fh h ee rice fields ( fi ld ( ( ( (A A, B B and d C C)) wh here Bbl Bobolinkks ((D Dl olichonyx or h yzivorus s) w ) ere captured in mist nets and d sampled for gut contents. Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. tartrate per 100 g of body mass. After the solution was the abundance (N%), frequency of occurrence (F%), given orally through a 1.5-mm diameter flexible plastic volume (V%) and index of relative importance (IRI%) tube attached to a l cm syringe, we placed the bird in a of each category of prey to determine the contribution small box lined with absorbent paper for 15 to 20 min of each category to the diet of the species. We calculated to allow them to regurgitate and also to recover after the biovolume of ingested categories by approximation to regurgitation (Poulin et al. 1994, Johnson et al. 2002, regular geometric shapes. The volume of fractionated and Carlisle & Holberton 2006). We obtained 23 samples disarticulated prey was estimated by comparison with using this technique after which we discontinued its use reference prey. However, this was implemented mostly because mortality rate was high (33%, n = 10 individuals). for animal prey since seeds were found intact in most Two additional samples were from the stomach contents cases. Index of relative importance of prey (Pinkas et al. analysis of two individuals that did not regurgitate and 1970) was used to determine the importance of each prey died. Dead individuals were collected and deposited in category in the diet. the collection of the National Institute of Limnology (INALI: CONICET-UNL). Subsequently, we resumed RESULTS using the saline solution regurgitation method obtaining eight more samples, and all of these birds were released successfully after samples were obtained. All gut contents General composition of the diet were preserved in 70% ethanol. We recorded 1597 items from all samples (n = 46 samples), A A Analysis of digestive tract contents corresponding to 17 food item categories (Table 1). Of the total items, 1521 (95%) were from plants, represented by We examined contents of digestive tracts under a 6 families and 10 plant species (in the case of rice, Oryza Nikon® stereoscope binocular. We counted, measured sativa, two varieties were recorded and treated separately: and classified prey cate gories to the lowest possible Rice and Red Rice, cultivated and weed, respectively) and taxonomic level. We considered all samples, regardless of 76 items (5%) were from invertebrates, represented by the collection technique to inventory the total number 6 orders (Table 1). Plant items were mainly Cyperaceae of prey items found in the diet of Bobolink (n = 46 (48%) and Poaceae (43%). Th e high degree of digestion samples). Th ese samples were obtained from 14 January did not allow finer taxonomic resolution of invertebrate to 12 March 2016. However, to assess relative importance samples, with the exception of nymphs of Hemiptera of prey categories, we did not use samples obtained by assigned to the family Pyrrhocoridae and a Hemipteran water-based forced regurgitation because this technique assigned to the family Lygaeidae. likely under sampled vegetal fraction of stomach contents (26.4 vs. 2.6 plants by sample in emetic- and water- R R Relative importance of prey categories based forced regurgitation samples, respectively) aff ecting the comparison with the animal fraction, which was Among the 25 individuals represented by complete (or affected, but to a lesser extent, by the techni que (1.4 vs. mostly complete) stomach contents, plants represented 0.5 animal prey by sample in emetic- and water-based almost the entire diet (IRI% = 97%), while animals forced regurgitation samples, respectively). Thus, we were a minor component (IRI% = 3%), refl ecting the calculated the number and frequency of prey types only greater number and volume of seeds in the diet (Table from 25 samples to assess relative importance of prey 1). However, although only 4% of the total number of categories, 15 represented only by emetic samples, two prey items was invertebrates, 92% of the samples had at only by digestive tract dissection, and eight represented least one item from this category, indicating that most by both emetic and digestive tract samples. In this way, Bobolink individuals consumed at least some animal the samples considered in this analysis were obtained prey. Th e highest number and frequency of invertebrate only at the beginning of March (between 08–11 March in the diet corresponded to the orders Hemiptera and 2016). Given that we could only identify mature seeds in Coleoptera (Table 1). the digestive tract, the importance of rice in the diet was Rice was the most important component of the diet underestimated because we could not quantify immature because it was the most frequent prey category (F% = liquid or “milky” stages of rice. However, because 73%) and represented the largest volume (V% = 59%) of estimation of relative importance of rice was based on items in the diet (Table 1). Th e most abundant component samples obtained in the fi nal stage of rice production of the diet was a species of the family Cyperaceae (N% = during March, it is unlikely that the immature liquid or 48% vs. N% = 15% for rice) that, although it also had “milk” stage of rice represented a high proportion of the a high frequency among samples (F% = 58%), had a rice consumed at this stage of the crop. We quantified minor relative importance in the diet than rice due to the Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. T T Table 1. Total number (n = 46 samples) and importance (n = 25 samples) of the prey categories found in diet samples of Bobolinks (Dolichonyx oryzivorus s s) on its wintering grounds in Argentina. Prey categories within the plant and animal fractions are arranged in decreasing order according to the number of categories of prey recorded. Values in bold indicate the totals for the plant and animal fractions. The script indicates that the item was not found in this group of samples. Total number of prey categories is based on all samples. Abbreviations: percentages of number (N%), frequency (F%), volume (V%) and index of relative importance (IRI%); NI: not identified . Importance Total number Prey category (n) N% F% V% IRI% Plant fraction1521 96 96 95 97 Echinochloa sp. 235 15 15 6 3 Oryza sativa a (Rice) 232 15 73 59 55 Paspalum sp. 96 6 35 3 3 Oryza sativa a (Red Rice) 94 5 15 20 4 Cyperaceae NI 733 48 58 4 30 Polygonaceae 63 4 42 1 2 Solanum sp. 30 2 8 0 0 Conyza bonariensis 20 1 31 0 0 Amaranthus s sp. 8 0 8 0 0 Sp. NI (Asteraceae?) 5 0 12 0 0 Sp. NI 5 0 4 0 0 A A Animal fraction 76 4 92 5 3 Coleoptera 25 1 42 3 1 Hemiptera 18 1 23 1 1 Diptera 4 0 12 0 0 Hymenoptera 3 0 4 0 0 Psocoptera 2 0 8 0 0 Araneae 1 - - - - Undetermined 23 1 50 0 0 smaller size and volume of the seeds (Table 1). Overall, seeds and fruits of non-rice species were more abundant and frequent than rice among the individuals analyzed, but rice accounted for a greater volume of the diet due to the larger size of the grains (Table 1, Fig. 2). DISCUSSION Bobolinks are persecuted by rice producers in their wintering grounds because they are considered pests of rice crops (López-Lanús et al. 2007, Renfrew & Saavedra 2007). However, knowledge of its trophic ecology on the wintering grounds is limited because, although Renfrew et al. (2017) estimated the importance of rice, no previous study has assessed quantitatively the importance Figure 2. Relative importance index (IRI%) of rice (Oryza of non-cultivated plants and animal prey in their diet. sativa) vs. other plant species in the Bobolink (Dolichonyx In this study, in agreement with previous studies of the oryzivorus s) diet in Santa Fe, Argentina. Abbreviations: species (e.g., Martin & Gavin 1995, Renfrew & Saavedra percentages of number (N%), volume (V%) and frequency 2007), we confirmed that Bobolinks have a diet that is (F%). Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. predominantly herbivorous and rice-based during March, mentioned as part of the Bobolink diet (e.g., Echinochloa just prior to northbound migration (i.e., emetic-based crus-galli, Echinochloa polystachya, Sorghum halepense, samples, on which the calculations of relative importance Hymenachne amplexicaulis s s) were not found in samples of the prey were based, were obtained at the beginning of during our study. this month) in areas of intensive rice production. However, Remaining plant items corresponded to native or our results also indicate that Bobolinks consume more naturalized non-cultivated herbs and mostly coincided seeds of non-cultivated plants. Invertebrates, although with those documented in previous studies. However, fruits of minor importance in relation to plants, were present of Polygonaceae and seeds of Solanum sp. (Solanaceae) in the diet of most individuals, possibly as a result of and Amaranthus s sp. (Amaranthaceae), although of little occasional intake of invertebrates found while birds were importance, had not previously been mentioned as part searching for seeds (e.g., arthropods associated with seeds of the Bobolink diet in the area. Presence of Polygonaceae of plants). species has been reported in the Bobolink diet from breeding and stopover sites in the United States (Beal General composition of the diet 1900, Meanley & Neff 1953). Presence o f Solanum sp. seeds suggests that unless Bobolinks extract the Grains of mature Rice (O. sativa) represented an seeds without ingesting the fruit, Bobolinks could also important fraction of the diet in this study, which is in consume fleshy fruits such as those of these plant species. agreement with previous studies that have examined Solanaceae species have not been mentioned as part of the diet composition of Bobolinks in rice fields within their Bobolink diet in any previous study and, thus, this could wintering area (e.g., López-Lanús et al. 2007, Renfrew simply correspond to an occasional intake, although it & Saavedra 2007, Blanco & López-Lanús 2008). Rice was found in samples from two individuals in rice field B. was more important in the diet because it was abundant, Results of the current study also have expanded our frequent, and comprised the greatest volume of the plant knowledge of invertebrates consumed by Bobolinks. For component in the diet. The observed relative im portance example, although Hemiptera have been mentioned as of rice in the Bobolink diet (55%) was lower than that present in the diet of the Bobolinks in the wintering area reported by Renfrew et al. (2017), who found that the (López-Lanús & Marino 2010), the present study provides relative proportion of rice was approximately 69% in a the fi rst documentation of Hemiptera in diet samples; rice-producing region in Bolivia. Our results about the eight Hemiptera nymphs were found in the sample from relative importance of the rice correspond only to the a single individual Bobolink. Similarly, although some of days before harvest, i.e. we only used samples obtained the recorded invertebrate prey have been documented in by emetics and stomach analysis obtained between 08– samples from breeding and stopover sites (e.g., Coleoptera, 11 March 2016 to determine the relative importance of Hemiptera, Hymenoptera and Araneae; Beal 1900, the different prey, when the rice is already in a mature Meanley & Neff 1953), documentation of invertebrate and hard stage. Under these conditions, Bobolinks could prey in the diet of Bobolinks on their wintering grounds include a greater proportion of other plants in their diet was previously limited to caterpillars (Lepidoptera; Renfrew because rice is no longer found in the milky and soft & Saavedra 2007, López-Lanús et al. 2008). stages preferred by the species in the studied rice fi elds. Echinochloa a sp. and a Cyperaceae species were Considerations on the techniques used to study among the most abundant food items. However, because Bobolink diet these seeds and fruits are small, these were lower in volume of diet and relative importance than rice. Seeds Our study showed that water-based forced regurgitation of Echinochloa a sp. probably corresponded to E. colona, is a technique much less effective than emetic-based a naturalized grass introduced from Europe (Pensiero & technique to study the Bobolink's diet. However, use Gutiérrez 2005) that previously was reported by López- of emetic implied a relatively high mortality rate that Lanús et al. (2008) as part of the diet of Bobolinks in the limited the number of samples obtained. This contrasts same area. Cyperus s sp. is among the probable Cyperaceae with studies that have shown that mortality caused by genera corresponding to the species found in the rice emetics is relatively low in icterids (Poulin et al. 1994, fi eld A, because this also has been reported as part of the Poulin & Lefebvre 1995). However, responsiveness to diet of Bobolink in the area (López-Lanús et al. 2008). emetics is highly species-specifi c (Durães & Marini 2003). The same stud y also mentioned that Bobolinks feed on Although the manipulation of birds mainly during the oral Conyza bonariensis, a grass species that was also found administration into the beak and down the esophagus by during the present study, mainly in samples from field A, means of a syringe connected to a silicone tube can cause where grasslands composed of this plant were observed. damage to the birds if not implemented correctly, all the Other plant species present in the area that have been birds that received the same treatment, but with warm Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. water were not damaged and were successfully released. Alianza del Pastizal and BirdLife International. We This indicates that the mortality was directly related to the are grateful to A. Muchiutti and G. Marino for their emetic and not to the manipulation. Emetic solution was assistance throughout the development of this project, prepared in laboratory by a professional chemist to assure to A. Galimberti for assistance in the field work, to rice a correct preparation. Characteristics that differentiate the workers Cooperativa de Arroceros de Villa Elisa, Questa a and Bobolink from other icterids like the high energetic cost San Roque e for allowing us to work in the rice fields, to of migration and the use of agrochemicals in rice fields B. Schneider (INALI-CONICET-UNL) for help in the where they feed could be related to this sensitivity to the identification of collected plants, to J.G. Blake for English emetic. Th ese aspects could be evaluated by studying the editing and constructive comments on the drafts of this health conditions of these populations. Beyond this, we paper and to an anonymous reviewer that contributed to do not recommend the use of emetics for the study of improve the manuscript. The study was authorized by the the diet of Bobolink. Alternatively, the use of water-based Dirección General de Recursos Naturales y Ecología of the forced regurgitation can be used to establish qualitative Ministerio de Medio Ambiente de la Provincia de Santa Fe, lists of ingested prey, and not of their relative importance, Argentina (Administrative Resolution 060-16). because of the little food regurgitated by this technique in relation to the use of emetic. Other techniques such as the use of stable isotopes and the genetic analysis of feces REFERENCES could improve our knowledge of the Bobolink diet on its Beal F.E.L. 1900. Food of the Bobolink, Blackbirds and Grackles, v. 13. wintering grounds. Washington: Department of Agriculture, Division of Biological Survey. Conservation implications Blanco D.E. & López-Lanús B. 2008. Ecología no reproductiva y conservación del Charlatán ( ( (Dolichonyx oryzivorus s) en el noreste de Argentina. Buenos Aires: Wetlands International. Our results show that Bobolinks consume a great quantity Carlisle J.D. & Holberton R.L. 2006. Relative efficiency of fecal versus of seeds and grains of non-cultivated plant species. These regurgitated samples for assessing diet and the deleterious eff ects results are remarkable because we captured Bobolinks of a tartar emetic on migratory birds. Journal of Field Ornithology within rice fields where the rice cro p is the predominant 77: 126–135. land-cover. Th us, these results agreed with the idea that Durães R. & Marini M.Â. 2003. An evaluation of the use of tartar emetic in the study of bird diets in the Atlantic Forest of damage to rice crops could be lower in fi elds that maintain southeastern Brazil. Journal of Field Ornithology y 74: 270–280. the presence of non-cultivated patches and roadsides with Hess C.A. 1997. Stomach fl ushing: sampling the diet of Red-cockaded the presence of naturally occurring grass, which provide Woodpeckers. Wilson Bulletin 109: 535–539. an alternative food source to the Bobolink. Johnson M.D., Ruthrauff D.R., Jones J.G., Tietz J.R. & Robinson J.K. 2002. Short-term eff ects of tartar emetic on re-sighting rates Our results also showed that Bobolinks could of migratory songbirds in the non-breeding season. Journal of contribute to the control of pest insects in rice fields. Field Ornithology 73: 191–196. Although the insect component of the diet was of Kruger R.D. & Burdyn L. 2015. Guía para la identificación de plaga s relatively minor importance, the documentation and del cultivo del Arroz ( ( (Oryza sativa L.) para la provincia de Corrientes. confirmation of the presence of invertebrates in the Corrientes: Instituto Nacional de Tecnología Agropecuaria (INTA). 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Aportes al conocimiento de la Bobolinks included members of the orders Hemiptera ecología del Charlatán y su estado actual en la provincia de Santa Fe, and Coleoptera, both of which include species that Argentina. Buenos Aires: Aves Argentinas/Asociación Ornitológica del Plata. can damage rice crops (Kruger & Burdyn 2015). The López-Lanús B., Roesler I., Blanco D.E., Petracci P.F., Serra M. & opportunistic behavior shown by the Bobolink to capture Zaccagnini M.E. 2007. Bobolink (Dolichonyx oryzivorus s s) numbers their animal prey can be important when these groups of and non breeding ecology in the rice fields of San Javier, Santa Fe insects become abundant. province, Argentina. Ornitología Neotropicall 18: 493–502. Major R.E. 1990. Stomach flushing of an insectivorous bird: an assessment of differential digestibility of prey and the risk to birds. Wildlife Research 17: 647–657. ACKNOW W WLEDGEMENTS Martin S.G. & Gavin T.A. 1995. Bobolink (Dolichonyx oryzivorus s s). In: Poole A. & Gill F. (eds.). The birds of North Americ a. Washington: Th is study was supported by funds from Aves Argentinas, Academy of Natural Sciences. Revista Brasileira de Ornitologia 27(1): 2019 Diet of Bobolink on its wintering grounds Lorenzón et al. Meanley B. & Neff J.A. 1953. Food habits of the Bobolink in Arkansas inferred from feather isotopes. Condor 119: 439–448. rice fiel ds. Auk 70: 211–212. Renfrew R.B. & Saavedra A.M. 2007. Ecology and conservation of Pensiero J.F. & Gutiérrez H.F. 2005. Flora vascular de la provincia Bobolinks (Dolichonyx oryzivorus s s) in rice production regions of de Santa Fe: claves para el reconocimiento de las familias y géneros: Bolivia. Ornitología Neotropical 18: 61–73. catálogo sistemático de las especies. Santa Fe: Universidad Nacional Renfrew R.B., Strong A.M., Perlut N.G., Martin S.G. & Gavin T.A. del Litoral. 2015. Bobolink (Dolichonyx oryzivorus s s). In: Rodewald P.G. (ed.). Pinkas L., Oliphant M.S. & Iverson I.L.K. 1970. Food habits of Th e birds of North America. Ithaca: Cornell Lab of Ornithology. Albacore, Bluefin Tuna, and Bonito in California waters. Fis h h ttp://dune.une.edu/c g i/vie wcontent.c g i?ar ticle=1025 Bulletin 152: 1–105. &context=env_facpubs (Access on 27 July 2017). Poulin B., Lefebvre G. & McNeil R. 1994. Effect and efficiency o f Sauer J.R., Niven D.K., Hines J.E., Ziolkowski D.J., Pardieck-Jr. K.L., tartar emetic in determining the diet of tropical landbirds. Condor Fallon J.E. & Link W.A. 2004. Th e North American breeding bird 96: 98–104. survey: results and analysis 1966–2003. Laurel: Patuxent Wildlife Poulin B. & Lefebvre G. 1995. Additional information on the use of tartar Research Center. emetic in determining the diet of tropical birds. Condor r 97: 897–902. Renfrew R.B., Hill J.M., Kim D.H., Romanek C. & Perlut N.G. 2017. Winter diet of Bobolink, a long-distance migratory grassland bird, Associate Editor: Leandro Bugoni. Revista Brasileira de Ornitologia 27(1): 2019

Journal

Ornithology Research – Springer Journals

Published: Mar 1, 2019

Keywords: agroecosystems; birds; emetic; foraging; pests

References

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