Antpittas and Worm-Feeders: a Match Made by Evolution? Evidence for a Possible Commensal Foraging Relationship Between Antpittas (Grallariidae) and Mammals

COMMENT

Antpittas and worm-feeders: a match made by evolution? Evidence for a possible commensal foraging relationship between antpittas (Grallariidae) and mammals

Grallariidae e mamíferos: evidências de uma possível relação de comensalismo

Harold F. Greeney1 Commensal foraging relationships er, 1993), and primates (Boinski and [email protected] between two groups of animals fre- Scott, 1988; Heymann, 1992; Stott, quently involve one following another 1947; Zang and Wang, 2000). Similar- and capitalizing on the prey flushed ly, the types of birds involved in such by the movement of the other (Al- bird-mammal feeding relationships cock, 1997; Weins, 1989). In broad cover a broad taxonomic spectrum, terms, three of the best documented and include Accipitridae (Robinson, associations involving vertebrates are 1994), Laridae (Harrison, 1979), Pro- birds and mammals following ants cellariidae (Obst and Hunt, 1990), (Elliot, 1950; Júnior and Zara, 2007; Ardaeidae (Rice, 1954), Trogonidae Martins, 2000; Rylands et al., 1989; (Stott and Selsor, 1961), Bucerotidae Willis and Oniki, 1978, 1992), birds (Chapin, 1939), Cuculidae (Siegel et following birds (Baker, 1980; Ben- al., 1989; Smith, 1971), and several nett and Smithson, 2001; Hino, 1998; families of Passeriformes (Di Gia- Robbins, 1981), and birds following como and Di Giacomo, 2006; Komar mammals (see below). Such rela- and Hanks, 2002; Levey, 1999; Stott, tionships between birds and mam- 1947). Unlike the well studied rela- mals have been reported from many tionships between birds and ants in regions of the globe (Wiens, 1989), the lowland Neotropics (Willis, 1969; and documented mammalian “beater” Willis and Oniki, 1978, 1992; Will- species include a wide array of taxo- son, 2004), little is known about the nomic groups including elephants commensal foraging associations of (Ruggiero and Eves, 1998), deer (Her- Andean birds. Largely anecdotal ac- ring and Herring, 2007), coatis (Sick, counts of many species of passerines 1984), peccaries, wolves (Silveira et associated with highland army ants al., 1997), armadillos (Di Giacomo (Labidus spp., Ecitoninae), however, and Di Giacomo, 2006; Komar and are scattered throughout the litera- Hanks, 2002), manatees (Scott and ture (Dobbs and Martin, 1998; Hilty, Powell, 1982), whales (Harrison, 1974; Nieto-R. and Ramírez, 2006; 1979; Obst and Hunt, 1990), dolphins Rios et al., 2008; Vallely 2001), in- (Evans, 1982; Monteiro-Filho, 1992), cluding several species of antpittas domestic cattle (Burger and Goch- (Grallariidae) (Greeney and Gelis, 1 Yanayacu Biological Station & Center for Creative Studies. Km 5, Via Las Caucheras, Cosanga, Napo, Ecuador. field, 1982; Heatwole, 1965; Källand- 2005; Kofoed and Auer, 2004; Nieto- Antpittas and worm-feeders: a match made by evolution?

R. and Ramírez, 2006). Here, I pres- al., 2008), comes as no surprise. What bamboo at Yanayacu in 2001. During ent observations of Andean antpittas, seems more surprising, however, is a brief pause, I noticed a single adult which suggest that they may, at least how readily they respond to the stim- perched several meters away on a on a facultative basis, partake in com- ulus of human presence, vocalization, low branch. Apart from an occasional mensal foraging associations with and movement at feeding stations. flicking of its wings, it appeared un- mammals. This putative association, Many other wild birds are commonly perturbed by my presence. After mov- in turn, may help explain the success brought in by feeding stations of vari- ing another 20 m, I paused again. of recently implemented antpitta feed- ous types. The common static feeders, Within moments an adult antpitta ap- ing stations which have reached wide- however, are not accompanied by ob- peared and observed me as before. spread use in the tourist industry. vious (to birds) presence of humans. This continued for more than 30 min., My observations of antpitta behavior The following observations of behav- covering perhaps 100 m of dense bam- were made during the course of field ior exhibited by Andean antpittas sug- boo. I was not followed after emerg- work throughout Ecuador over the past gest a possible explanation. ing from the bamboo. In subsequent 12 years. I made most observations at Though allied with obligate follow- years I have had similar experiences Cabañas San Isidro and the adjacent ers of army ants (i.e., some species of with Chestnut-naped Antpitta (n = 1), Yanayacu Biological Station (00°36’S, Thamnophilidae; sensu Remsen et al., White-bellied Antpitta (n = 1), Rufous 77°53’W) in the northeastern Andes, 2011), antpittas are thought to only op- Antpitta (n = 2), Watkins’s Antitta (G. and at the Tapichalaca Biological Re- portunistically join mixed-species for- watkinsi; n = 4), Jocotoco Antpitta (n serve (04º30’S, 79º10’W) in Ecua- aging assemblages at ant swarms. Rel- = 6), and twice more with Chestnut- dor’s extreme southeastern Andes. I atively few species have been reported crowned Antpitta. To the best of my also include unpublished observations foraging at ant swarms (Greeney and knowledge, in all cases, I was not provided by several other field work- Gelis, 2005; Kofoed and Auer, 2004; near their nest at the time. Given the ers in Ecuador and Colombia. Nieto-R. and Ramírez, 2006). These natural ability of antpittas to remain Antpittas are among the most elusive records, along with my own observa- hidden, in concert with my own focus of neotropical passerines, and their tions and those kindly provided by on making a hole through the vegeta- scarcity and retiring manner make Eliot T. Miller, however, suggest that tion, it seems likely that I have been them a daunting challenge for the stu- most species of antpittas will opportu- followed through the undergrowth dent of birds. Predominantly, haunt- nistically follow montane ant swarms. more often than I am aware. Jose Ma- ing montane forests, antpittas occur Between Miller and myself we have ria Loaiza B. related a similar experi- through the Neotropics and reach recorded Chestnut-crowned Antpitta ence whereby he has been followed by their peak diversity in the Andes of (n = 2), White-bellied Antpitta (n = 2), Scaled Antpitta (G. guatimalensis) and South America. Antpittas forage pre- Chestnut-naped Antpitta (n = 5), and Ochre-breasted Antpitta. He observed dominantly on (Grallaria, Hylopezus, Jocotoco Antpitta (n = 4) in attendance both species coming to forage at leaf Myrmothera), or near (Grallaricula), at army ant swarms. I have also ob- litter he had disturbed, following him the ground (Krabbe and Schulenberg, served several species of Grallaricula for some distance to repeatedly cap- 2003). In recent years, due to the prize antpittas associating with ants, includ- ture prey from the areas of overturned that a sighting of these birds represents ing Slate-crowned Antpitta (G. nana; n soil and leaves. Though this is the in the tourist industry, the practice of = 6) and Ochre-breasted Antpitta (G. only other report of such behavior in calling-in and feeding antpittas via flavirostris; n = 2). The frequency of antpittas that I am aware of, it seems the creation of “worm-feeders” has these observations, especially given likely that it may often go unnoticed become wide-spread in Ecuador and the difficulty with which antpittas are or unreported. In addition to my ob- Colombia (Woods et al., 2011). This observed in the wild, suggests that ant- servations above, I have had similar involves establishing a location where pittas may associate with ant swarms experiences of being followed by two worms are regularly provided to ant- more frequently than is reported in Grallaricula antpittas, Slate-crowned pittas and/or may be foraged for in the literature, and that the behavior is (n = 4) and Peruvian (G. peruviana; n enriched compost. At most localities wide-spread within the family. = 2). In addition to these observations where I have witnessed this phenom- Perhaps, surprisingly, other than in under natural conditions, during the enon, antpittas are called in through situations as described above, I have construction of trails near Yanayacu, I whistles, calls, or other coaxing and, had my best looks at antpittas while frequently witness Chestnut-crowned, with time, are frequently tame enough crashing through dense understory White-bellied, and Giant Antpittas to take food from human hands. That vegetation in search of their nests. spending long periods of time foraging these largely terrestrial birds frequent- I first noticed “following behavior” in in the recently disturbed earth, often ly forage on worms, often feeding a Chestnut-crowned Antpitta while I only a few meters from those working them to their nestlings (Greeney et was moving noisily through Chusquea on the trail.

Neotropical Biology and Conservation 141 Harold F. Greeney

Most species of antpittas occur sym- ing strategy. Their apparent scarcity at http://dx.doi.org/10.1163/156853982X00265 patrically with a range of large mam- feeding stations is likely a reflection of CHAPIN, J.P. 1939. The birds of the Belgian mals. Other than large cats, montane a difference in prey choice, and their Congo, part 2. New York, The American Mu- seum of Natural History, 632 p. (Bulletin of the mammalian predators (which might relatively reduced experience with American Museum of Natural History 75). pose a threat if followed) are gener- worms as food. DOBBS, R.C.; MARTIN, P.R. 1998. Migrant bird ally small (e.g., Mustellidae) and Commensal foraging relationships participation at an army ant swarm in montane would not likely be profitable “beat- involving birds as “follower” species Jalisco, Mexico. Wilson Bulletin, 110:293-295. are common and wide-spread geo- EISENBERG, J.E.; REDFORD, K.H.; REID, ers.” Large herbivores, however, are F.A. 1999. Mammals of the Neotropics, Volume diverse, and include agoutis, pacas, graphically and taxonomically (see 3. Chicago, Illinois, Chicago University Press, deer, tapirs, and bears (Eisenberg et al., introduction). Reports of birds fol- 644 p. 1999; Jarrín-V., 2001; Tirira, 1999), lowing humans, potentially for the ELLIOTT, H.F.I. 1950. Driver-ants and the of which the latter two often create same reasons, however, are few (e.g., breeding seasons of birds. Ibis, 92:320-321. Skutch, 1969); though some species EMMONS, L.H.; FEER, F. 1997. Neotropical considerable noise and physical dis- rainforest mammals, a field guide. Chicago, turbance to their surroundings (pers. are known to follow gorillas (Rug- University of Chicago Press, 281 p. obs.). Thus, the attraction of antpit- giero and Eves, 1998). The array of EVANS, P.G.H. 1982. Associations between tas to large, noisy mammals may not taxonomic associations found to date, seabirds and cetaceansa: review. Mammalogy be maladaptive. In fact, given their however, suggest that many species Review, 12:187-206. may, at least opportunistically, follow http://dx.doi.org/10.1111/j.1365-2907.1982.tb00015.x potential phylogenetic predisposition DI GIACOMO, A.S.; DI GIACOMO, A.G. to following army ant swarms, along any organism which is flushing prey 2006. Observations of Strange-tailed Tyrants with their apparent curiosity and oc- within its natural habitat. The dearth (Alectrurus risora) and other grassland birds casional boldness around humans, I of information on the natural history following army ants and armadillos. Journal of suggest that a natural foraging tech- of antpittas in general is a reflection of Field Ornithology, 77:266-268. their shy and elusive habits (Greeney http://dx.doi.org/10.1111/j.1557-9263.2006.00052.x nique of antpittas is to follow in the GREENEY, H.F.; DOBBS, R.C.; MARTIN, wake of large mammals and capital- et al., 2008), and I suggest that the as- P.R.; GELIS, R.A. 2008. The breeding biology ize on prey items exposed by their sociation between antpittas and large of Grallaria and Grallaricula antpittas. Journal foraging. In my experience, bears are mammals has not been previously of Field Ornithology, 79:113-129. particularly destructive as they tear documented only due to the difficulty http://dx.doi.org/10.1111/j.1557-9263.2008.00153.x of observing both antpittas and large GREENEY, H.F.; GELIS, R.A. 2005. Juvenile apart bromeliads and logs, but most plumage and vocalization of the Jocotoco Ant- other montane herbivores also forage Andean mammals. Though this pres- pitta Grallaria ridgelyi. Cotinga, 23:79-81. by pawing through and disrupting leaf ents a challenge, it is likely that any HARRISON, C.S. 1979. The association of litter (Emmons and Feer, 1997; Jarrín- student of neotropical biology will be Marine birds and feeding Gray Whales. Condor, V., 2001). Given this possibly natural highly rewarded by studying and doc- 81:93-95. http://dx.doi.org/10.2307/1367866 umenting this potential interaction. HEATWOLE, H. 1965. Some aspects of the means of foraging by antpittas, I sug- association of Cattle egrets with cattle. Animal gest that they have an innate propen- Behaviour, 13:79-83. sity to be attracted to human activity References http://dx.doi.org/10.1016/0003-3472(65)90075-8 and are thus easily trained to respond HERRING, G.; HERRING, H.K. 2007. Com- ALCOCK, J. 1997. Animal behavior: an evo- mensal feeding of Great Egrets with Black- to non-subtle cues (i.e. vocalizations, lutionary approach. Sunderland, Maryland, tailed Deer. Western Birds, 38:299-302. movements of tourist groups) indicat- Sinauer Associates, 547 p. HEYMANN, E.W. 1992. Associations of tama- ing sources of food provided by hu- BAKER, B.W. 1980. Commensal foraging of rins (Saguinas mystax and Saguinas fuscicollis) mans. While the effects of worm feed- Scissor-tailed Flycatchers with Rio Grande Tur- and Double-toothed Kites (Harpagus bidenta- ers on antpitta biology are unstudied, key. Wilson Bulletin 92:248. tus) in Peruvian Amazonia. Folia Primatolog- BENNETT, J.; SMITHSON, W.S. 2001. Feed- ica, 59:51-55. it seems that perhaps feeding stations ing associations between Snowy Egrets and http://dx.doi.org/10.1159/000156642 may mesh more naturally with ant- Red-breasted Mergansers. Waterbirds, 24:125- HILTY, S.L.1974. Notes on birds at swarms of pitta natural history than is at first ob- 128. http://dx.doi.org/10.2307/1522252 army ants in the highlands of Colombia. Wilson vious. Thus, despite the fear of some BIRDLIFE INTERNATIONAL. 2009. Jo- Bulletin, 86:479-481. that worm-feeder tourism may have cotoco Antpitta – BirdLife species factsheet. HINO, 1998. Mutualistic and commensal orga- Available at http://www.birdlife.org/datazone/ nization of avian mixed-species forag ing flocks negative impact on the many species species/index.html. Accessed on: 2011/09/22. in a forest of western Madagascar. Journal of of threatened antpittas (BirdLife In- BOINSKI, S.; SCOTT, P.E. 1988. Association Avian Biology, 29:17-24. ternational, 2009), this seems unlikely of birds with monkeys in Costa Rica. Biotro- http://dx.doi.org/10.2307/3677336 to me. While the foraging behavior pica, 20:136-143. JARRÍN-V., P. 2001. Mamíferos en la niebla: and prey selection of the smaller, http://dx.doi.org/10.2307/2388186 Otonga, un bosque nublado del Ecuador. Quito, BURGER, J.; GOCHFIELD, M. 1982. Host Ecuador, Imprenta Mariscal, 244 p. less terrestrial Grallaricula diverges selections as an adaptation to host-dependent JÚNIOR, T.A. de M.; ZARA, F.J. 2007. Black- from that of Grallaria antpittas, I sug- foraging success in the Cattle Egret (Bubulcus tufted-ear Marmoset Callithrix penicillata (Pra- gest they may adopt a similar forag- ibis). Behavior, 79:212-229. mates: Callitrichidae) following the army ant

142 Volume 7 number 2  may - august 2012 Antpittas and worm-feeders: a match made by evolution?

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