Table Of ContentWilson Bulletin, 116(1), 2004, pp. 17-22
SUNRISE NEST ATTENDANCE AND AGGRESSION BY LEAST
BELL’S VIREOS FAIL TO DETER COWBIRD PARASITISM
BRYAN L. SHARP' ’ AND BARBARA E. KUS^-*
—
ABSTRACT. We video-recorded three, natural, brood-parasitism events by Brown-headed Cowbirds (Mol-
othrus ater) at nests ofLeast Bell’s Vireos (Vireo belliipnsillns). All instances occurred neardawn, during both
egg-laying and incubation stages of the nesting cycle. In each case, an adult vireo was on the nest when the
female cowbird arrived. Both members of each parasitized pair vigorously attacked the intruding cowbird, but
in no encounter did a pair of vireos successfully defend its nest from parasitism. Thus, Least Bell’s Vireos in
our study were unable to prevent a female cowbird from parasitizing their nests once the cowbird had reached
the nest. Received 16 October2003, accepted 1 April 2004.
There are several ways in which potential of this strategy varies (Graham 1988, Hosoi
hosts may protect a nest from the detrimental and Rothstein 2000, Kus 2002).
impacts of brood parasitism. Two strategies Nest-attendance behavior by potential hosts
may prevent a cowbird from laying: nest sit- during times when cowbirds may lay eggs is
ting (rushing to the nest and sitting in it; Hob- an important consideration when examining a
son and Sealy 1989, Gill and Sealy 1996) and host’s defense capability (Neudorf and Sealy
aggression directed at the intruding cowbird 1994, Clotfelter and Yasukawa 1999). Scott
(Robertson and Norman 1977, Briskie et al. (1991) and Neudorf and Sealy (1994) found
1990). The effectiveness of such behaviors in that Brown-headed Cowbirds lay near(usually
deterring parasitism is unclear. The hndings of before) sunrise during the laying stage of the
Sealy et al. (1998) suggest that these behav- nesting cycle. A host that is vigilant near the
iors do not thwart parasitism. However, J. M. nest at these times may be able to defend its
Budnik (pers. comm.) video-recorded a nest better than a host that is not attending its
Brown-headed Cowbird {Molothnis ater) lay- nest (Neudorf and Sealy 1994, Clotfelter and
ing an egg on the back of a midwestern Bell’s Yasukawa 1999). However, Sealy et al. (2000)
Vireo {Vireo bellii bellii) that refused to leave found that sunrise nest attendance was a func-
the nest, and several times observed vireo tion of the onset of incubation rather than a
pairs preventing cowbirds from laying by nest-defense strategy.
physically attacking and driving them away Least Bell’s Vireo {V. b. piisillit.s) is a fed-
(Budnik 1999, Budnik et al. 2001). erally endangered songbird that is heavily par-
After a nest has been parasitized, the most asitized throughout most of its current range
effective anti-parasite responses by the host in California (Franzreb 1989; Kus 1999,
2002). Consequently, extensive coubird-trap-
are to ( I ) eject the egg from the nest (Roth- ping programs have been instituted within the
stein 1976, Sealy and Bazin 1995), or (2) bury
the egg (Clark and Robertson 1981, wSealy geographic range of this \ireo. As Least BelLs
1995). A third strategy is that of abandoning Vireo is a recent host, co-occurring with cow-
the nest and re-nesting, but the effectiveness birds only during the last century (Maylield
1965), it may lack natural defenses against
parasitism. Least Bell’s Vireos only rarely
bury cowbird eggs (BliK unpubl. data), and,
C’a'mDpeapnti,lcofDr.B,iSolaongyD,ieSgao,n (D'iAeg0o21XS2t,aleUSUAn.iv., 5500 like many other small hosts, inclutling the
- U.S. (ieological .Survey, Western Lcological Re- western subspecies ol' Warbling Vireo (\'. g/7-
.search ('enter, 5745 Kearny Villa Rcl., San Diego, ('A vii.\ swain.sonii: ,S. G. .Scaly pets, comm.).
02123, USA. Least Bell's Vireos are probably unable to
'('urrent atkiress: Dept, of Itiological and I’hysical grasp- or puncture-eject cowbird eggs (Roth-
SScpireinncgesS,t.,('(o'loulmubmubsusS,taOleH(4’3o2m1m5u.niItkySA(.'ollege, 550 I'.. stein 1975a, .Spaw and Rohwer 1987, Rohwer
'('orrespoiuling author: e-mail: and .Spaw 1988). I.east l^ell's Vireos abtuulon
barbaiii_kus(«4isgs.gov parasitized nests, but they do so at a mueh
17
18 THE WILSON BULLETIN • Vol. 116, No. !, March 2004
lower rate (mean = 29%, n = 207; Kus 1999) time-lapse mode (20 frames/sec) until either
than the nominate subspecies, V. h. hellii the young fledged, or the nest was depredated
[74%, n = 43 (Parker 1999); 51%, n = 63, or abandoned for other reasons, at which time
(Budnik et al. 2001)], and nest desertion and we moved the camera to another nest.
re-nesting by Least Bell’s Vireos is not cur- We reviewed video recordings to determine
rently an effective defense against the impacts whether an adult vireo was on or near the nest
of parasitism (Kus 2002). Nothing is known prior to parasitism, whether vireos defended
about the ability ofLeast Bell’s Vireos to deter the nest during parasitism attempts, and
parasitism through nest defense. whether vireos accepted or rejected cowbird
We video-recorded natural parasitism eggs after being parasitized. We noted the du-
events of Least Bell’s Vireos by Brown-head- ration of each encounter between a female
ed Cowbirds to examine this host’s ability to cowbird and the pairofvireos (sensu the “lay-
defend its nest and to analyze host responses ing bout’’ described in Sealy et al. 1995) as
after being parasitized. The specific questions well as the actual time each cowbird spent
we addressed were (1) when do Brown-head- poised in a laying posture on the nest. We re-
ed Cowbirds lay their eggs in Least Bell’s Vir- viewed 2-hr segments (from 1 hr before sun-
eo nests with regard to time of day and stage rise to 1 hr after sunrise) for each day a cam-
in the nesting cycle, (2) are Least Bell’s Vir- era was located at a nest, up to the midpoint
eos attending the nest when cowbirds arrive of incubation, targeting the time of day (Scott
to lay an egg, (3) how do Least Bell’s Vireos 1991, Neudorf and Sealy 1994) and stage of
interact with cowbirds at the nest, and (4) do the nesting cycle (Lowther 1993, Sealy 1995)
Least Bell’s Vireos accept or reject a parasitic when cowbirds typically parasitize nests. We
egg? We addressed these questions to evaluate also noted whether an adult vireo roosted on
whether Least Bell’s Vireo may be able to its nest overnight. If an adult was not on the
adapt to the pressure of brood parasitism. nest within 1 hr before sunrise, we assumed
no adult roosted on the nest, and we recorded
METHODS
the time an adult first visited the nest in the
We monitored 129 Least Bell’s Vireo nests morning relative to time of sunrise. We ob-
along the San Luis Rey River in northern San tained sunrise times from the U.S. Naval Ob-
Diego County, California, during the 2000 servatory website.
breeding season as part of a larger, long-term We considered incubation to begin the day
study of vireo demographics. Cowbirds were after the last egg was laid, although incubation
not trapped within our study site during this begins with the penultimate egg (BEK pers.
season. We placed cameras at 19 nests of 13 obs.). We chose this chronology to allow us
different vireo pairs between 28 April and 7 to designate days as either laying days or in-
July. These nests were in early stages of the cubation days. Eor nests parasitized during
nesting cycle when Brown-headed Cowbirds laying, we left cowbird eggs in place until
typically parasitize nests (Lowther 1993, Sca- clutches were complete (6-10 days after par-
ly 1995). Videotapings were made from 1 day asitism), and then removed them as authorized
before clutch initiation through the midpoint by federal and state permits. Means are re-
(day 6) of incubation. We extended videotap- ported ± SE.
ing through day 6 of incubation to find ifpar-
RESULTS
asitism might occur later in the cycle. Cam-
eras were of two types: Fuhrman Microcams We videotaped three parasitism events by
and Christensen Sentinel Systems. Lenses Brown-headed Cowbirds (Table 1). Two
were placed within 1 m ofnests, camouflaged events occurred before sunrise, and one took
by surrounding vegetation. The camera was place shortly after sunrise, yielding a mean
connected by cable to the recorder, which was parasitism-event time of sunrise — 1 1.0 ± 6.4
hidden 10-20 m away from the nest. The field min (Table 1). One nest was parasitized on
of view for cameras included the nest and 5— day 4 of incubation, whereas the others were
50 cm radii around the nest, depending on parasitized during laying (Table 1). No nest
where we were able to locate the camera lens. was abandoned.
We videotaped nest activity continuously in In each parasitism event, an adult vireo was
Sharp and Kiis • VIREO-COWBIRD INTERACTIONS AT NESTS 19
TABLE 1. Characteristics of the nesting stage of videotaped parasitism events at Least Bell’s Vireo nests,
San Luis Rey River, San Diego County, California, 28 April-7 July 2000.^*
Timecowbird Clutch Completedclutch
Dateof Timeof Durationof innest, Nestingstagewhen sizewhen size(vireoeggs
parasitism parasitism encounter laying parasitized parasitized only)
6 May SR'’ - 21 min 42 sec 23 sec Day 2 of laying 1 4
15 May SR - 13 min 35 sec 33 sec Day 3 of laying 2 4
12 June SR + 1 min 43 sec 23 sec Day 4 of incubation 2 2
^Parasitismeventatafourthnestwasnotrecordedontapeduetotechnicaldifficulties.
^SR = sunrise.
Still on the nest from the nocturnal roosting/ after the cowbird left, and resumed normal
incubation period. Because birds were not nest attendance 21-146 sec after parasitism.
marked, we were unable to identify the gender Upon returning to the nest to brood, the adult
of individuals. Attendant vireos remained on inspected the contents prior to sitting in the
the nest, but were forced off the nest after be- nest. Pairs parasitized during laying continued
ing pecked repeatedly by the female cowbird. laying until completing the typical clutch of
Once ousted from the nest, the vireo attacked four vireo eggs (Brown 1993, Kus 1999).
the cowbird and wasjoined by its mate within Egg-laying continued at a normal rate of one
a few seconds, suggesting the mate was near- egg per day, with the exception ofone female
by. Although we could not record sound in that did not lay her fourth egg until 5-7 days
time-lapse mode, we could see that the vireos after her third egg (6-8 days after parasitism).
were scolding, and we presume that this vo- None of the vireo pairs removed the parasitic
calization is what attracted the second adult egg. In the 1 14 “nest-days” of tapes we re-
vireo. Both vireos scolded, jumped on the viewed (n = 19 nests), there were no encoun-
cowbird, struck the cowbird while flying by ters with cowbirds other than the three that
it, tried to pull the cowbird away from the resulted in parasitism. Thus, we found no in-
nest, and repeatedly pecked the intruder. One stances in which Least Bell’s Vireos prevented
cowbird left the nest on its first attempt, but a cowbird from parasitizing a nest once the
returned within 6 sec and successfully laid an cowbird had reached the nest.
egg. Encounters between female cowbirds and Of the 14 nest-days of tapes, there were
1
hosts averaged 40.0 ± 2.5 sec (Table 1). The only 1 1 instances in which an adult \ireo was
mean time each cowbird spent on the nest not on the nest overnight. Of these cases,
1 1
poised in a laying posture was 26.3 ± 3.3 sec 4 occurred before laying began, 6 were during
(Table 1). No host eggs were removed by laying, and 1 occurred on day 2 of incubation
cowbirds. (Table 2). There were no instances in which
After parasitism, one member ofeach vireo an adult did not roost on a nest overnight from
pair returned to its nest 7-18 sec (/? = 3 pairs) day 3 of incubation forward. Linear regression
TABLE 2. Frequency ofovernight roosting on the nest and arrival times of non-roosting adult Least Bell's
Vireos over the nesting cycle, San Luis Rey River, San Diego County, California. 28 April-7 July 2()()().
Daybeforelay*' Day I lay Day 2 lay Day .t lay Dalayy4 Dma\e'I Da> 2 me
Adult on nest over- 0/4 3/5 11/13 0/10 5/6 1.5/15 LV14
night/total nests
observed
Mean arrival time of +26.0 13.1 +30.0 5.0 +16.5 * 0.5 +26 *4 0
non-roosting adult
relative to SR'’ 1.
SI: (min)
"lay laying,ine ineubalion
'’SR sunrise.
20 THE WILSON BULLETIN • VoL 116, No. /. March 2004
of arrival time (relative to sunrise) versus day Vireos responded aggressively to the fe-
of nesting cycle demonstrated that adults that male cowbird in each instance of parasitism.
did not roost on the nest overnight arrived at However, sitting in the nest and attacking the
the nest earlier in the day as the nesting cycle cowbird did not prevent parasitism, contrary
progressed {t = -3.859, P = 0.018; Table 2). to observations that midwestern Bell’s Vireos
escaped parasitism with similar behavior
DISCUSSION (Budnik 1999, Budnik et al. 2001). We are
Our recordings represent the first video uncertain as to why defense tactics that were
documentation of parasitism by Brown-head- effective in the midwestern subspecies failed
ed Cowbirds of Least Bell’s Vireos. Two of to deter parasitism in Least Bell’s Vireos.
the recorded instances of parasitism occurred Least Bell’s Vireos quickly accepted cow-
during the laying stage of the nesting cycle, bird eggs. Possible reasons for acceptance
as is most often reported in the literature may be (1) lack of recognition of the cowbird
(Lowther 1993, Sealy 1995). The third nest egg (Rothstein 1975b, 1990; Sealy 1996; Tak-
was not parasitized until midway through the asu 1998), or (2) vireos may recognize cow-
incubation stage. Although most parasitism bird eggs as foreign but are unable to eject
occurs during the laying stage, instances of them. If the latter is the case, nest abandon-
parasitism during the incubation stage are not ment is the only response to parasitism avail-
uncommon (Lowther 1993, Sealy 1995). able to Least Bell’s Vireos. Although nest
As reported elsewhere (Scott 1991, Neudorf abandonment was not observed in our sample
and Sealy 1994), Brown-headed Cowbirds of videotaped nests. Least Bell’s Vireos are
laid their eggs around sunrise. This timing of known to abandon parasitized nests (Kus
laying is believed to be an adaptation for lay- 1999), albeit it at a low rate (Kus 2002).
ing when host adults do not typically attend When Least Bell’s Vireos accept cowbird
nests (Scott 1991); however, Neudorfand Sea- eggs, the end result, without human interven-
ly (1994) and Sealy et al. (2()()0) found that tion (i.e., removal of cowbird eggs from
some hosts do attend their nests at sunrise. nests), is the failure to produce vireo young
Clotfelter and Yasukawa (1999) suggested (Kus 1999, 2002). Least Bell’s Vireos have
that onset of nocturnal incubation early in the never been observed to fledge vireo and cow-
nesting cycle may be a strategy by which Red- " bird young from the same nest (BEK unpubl.
winged Blackbirds (Agelaiusphoeniceus) pre- data). We recognize that our sample size is
vent parasitism. Birds roosting or incubating small (such data are extremely difficult to ob-
overnight will be on the nest at dawn, when tain); however, all of the vireos in our study
cowbirds lay and, thus, will be able to defend failed to deter parasitism. Given the apparent
the nest better than if they were away from inability to avert parasitism even when attend-
the nest during a cowbird visit (Neudorf and ing the nest at sunrise, and the ineffectiveness
Sealy 1994, Clotfelter and Yasukawa 1999). of nest abandonment and re-nesting in re-
An adult vireo was roosting at the nest or sponse to parasitism (Kus 2002), Least Bell’s
incubating before each parasitism event we Vireos may lack behavioral defenses sufficient
videotaped and an adult roosted overnight on to prevent parasitism or its negative impacts
nearly every nest-day we observed. All 1 1 in- once a female cowbird has reached a vireo
stances in which an adult did not roost on the nest.
nest overnight occurred before or during lay-
ACKNOWLEDGMENTS
ing, with the exception of one instance that
occurred on day 2 of incubation (Table 2). We thank P. Beck, B. Peterson, and D. Kisner for
This pattern, the earlier arrival times of non- monitoring nests of Least Bell’s Vireos. B. Peterson
roosting adults as the nesting cycle progressed and M. Wellik assisted with camera set up and the
(Table 2), and the vireos’ inability to defend changing ofbatteries to run the cameras. K. Burns, D.
their nest when present at the time of a cow- Deutschman, P Pryde, B. Peterson, P Beck, J. Wells,
bird visit, support the conclusion of Sealy et K. Lerree, D. Kisner, and J. Rourke assisted in devel-
al. (2000): nest attentiveness is more a func- oMpesmteanst-Roofmethreo,prSo.jeScutl.liJv.anG,uaRr.dedreals,RioR,. ML.iguGeiroomae,ttiV,.
tion of the onset of incubation than an anti- and J. Mascarin provided additional field assistance.
parasite strategy. Much gratitude is extended to R. Veillette for review-
Sharp and Kus • VIREO-COWBIRD INTERACTIONS AT NESTS 21
ing hours of videotapes. Earlier versions of this man- Lowther, P. E. 1993. Brown-headed Cowbird {Mol-
uscript were greatly improved by comments fromJ. V. othnis ater). The Birds ofNorth America, no. 47.
Briskie, S. I. Rothstein, S. G. Sealy, and two anony- Mayfield, H. E 1965. The Brown-headed Cowbird,
mous referees. We thank the Bureau of Reclamation with old and new hosts. Living Bird 4:13-29.
and Arizona Game and Fish Department for the loan Neudorf, D. L. and S. G. Sealy. 1994. Sunrise nest
of five camera systems used in this study. This work attentiveness in cowbird hosts. Condor 96:162-
was funded by the California Department ofTranspor- 169.
tation, District 11, and by grants to the senior author Parker, T. H. 1999. Response of Bell’s Vireos to
from the Garden Club of America (c/o Cornell Labo- brood parasitism by the Brown-headed Cowbird
ratory of Ornithology), the Frank M. Chapman Fund in Kansas. Wilson Bulletin 1 1 1:499-504.
of the American Museum of Natural History, Sigma Robertson, R. J. and R. F. Norman. 1977. The func-
Xi, Los Angeles Audubon Society, and the San Diego tion and evolution ofaggressive behaviortowards
State University Evolutionary Biology Program Area. the Brown-headed Cowbird (Molotlirusater). Ca-
nadian Journal ofZoology 55:508-518.
LITERATURE CITED Rohwer, S. and C. D. Spaw. 1988. Evolutionary lag
Briskie, J. V., S. G. Sealy, and K. A. Hobson. 1990. versusbill-sizeconstraints: acomparativestudyof
Differential parasitism of Least Flycatchers and the acceptance ofcowbird eggs by old hosts. Evo-
Yellow Warblers by the Brown-headed Cowbird. lutionary Ecology 2:27-36.
Behavioral Ecology and Sociobiology 27:403- Rothstein, S. I. 1975a. An experimental and teleo-
nomic investigation of avian brood parasitism.
410.
Condor 77:250-271.
Brown, B. T. 1993. Bell’s Vireo (Vireo bellii). The
Birds ofNorth America, no. 35. Rothstein, S. I. 1975b. Evolutionary rates and host
Budnik, J. M. 1999. Demography and factors influ- defensesagainstavianbroodparasitism. American
Naturalist 109:161-176.
encing nesting success of Bell’s Vireo in grass-
land-shrub habitat. M.Sc. thesis. University of Rothstein, S. I. 1976. Experiments on defensesCedar
Missouri, Columbia. Waxwings use against cowbird parasitism. Auk
BudnTikh,omJp.sMo.n,,D.111.E.20B0u1r.haNness,t Mde.seRr.tiRoynaann,daanpdpaFr.enR.t Roths9t3e:i6n7,5-S6.91I.. 1990. A model system for coevolu-
nest protection by Bell’s Vireos in response to tion: avian brood parasitism. Annual Review of
cowbird parasitism. Condor 103:639-643. Ecology and Systematics 21:481-508.
Clark, K. L. and R. J. Robertson. 1981. Cowbird Scott, D. M. 1991. The time ofday ofegg-laying by
parasitism and evolution ofanti-parasite strategies the Brown-headed Cowbird and other icterines.
in the Yellow Warbler. Wilson Bulletin 93:249- Canadian Journal ofZoology 69:2093-2099.
258. Sealy, S. G. 1995. Burial ofcowbird eggs by parasit-
Clotfelter, E. D. and K. Yasukawa. 1999. Thefunc- ized Yellow Warblers: an empirical and experi-
tion ofearly onset ofnocturnal incubation in Red- mental study. Animal Behaviour 49:877-889.
winged Blackbirds. Auk 116:417-426. Sealy, S. G. 1996. Evolution of host defenses against
Franzreb, K. E. 1989. Ecology and conservation of brood parasitism: implications of puncture-ejec-
the endangered Least Bell’s Vireo. Biological Re- tion by a small passerine. Auk I 13:346-355.
port 89(1), U.S. Fish and Wildlife vService, Wash- Sealy, S. G. and R. C. Bazin. 1995. Low freciuency
ington, D.C. ofobserved cowbird parasitism on Eastern King-
Gill, S. A. and S. G. Sealy. 1996. Nest defense by birds: host rejection, effective nest defense,orpar-
Yellow Warblers: recognition of a brood parasite asite avoidance? Behavioral Ecology 6:140-145.
and an avian nest predator. Behaviour 133:263- Se:aly, S. G., D. G. McMa.sti;r. S. A. Ciii.i., and D.
282. L. Neudorf. 2000. Yellow Warbler nest attentive-
Graham, D. S. 1988. Responses of five host species ness: antiparasite strategy or onset of incubation?
to cowbird parasitism. Condor 90:588-591. Pages 169-177 in Ecology and management ol
Hob.son, K. a. and S. G. Sealy. 1989. Responses of cowbirds and their hosts: studies in the conser-
Yellow Warblers to the threat ofcowbird parasit- vation of North American passerine birds (J. N.
ism. Animal Behaviour 38:510-519. M. Smith, r. L. C'ook, ,S. I. Rothstein, S. K. Rob-
Hosoi, S. A. AND S. I. R()THsri:iN. 2000. Nest desertion inson, and S. G. Sealy, FaIs.). Uni\ersity ol fexas
and cowbird parasitism: evidence for evolved re- Press, Austin.
sponses and evolutionary lag. Animal Behaviour Si;ai.y, S. G., I). L. Ni iidori, and D. P. Hiil. 1005.
59:823-840. Rapitl laying by Brown-hcatIctI ('owbinls Molot/i-
Kus, B. H,. 1999. Impacts ol Brown-headed Cowbird rn.s ater aiul other parasitic birtls. Ibis 137:76 84.
parasitism on the productivity ot the endangered SiAi.Y, S. (i.. I). L. Ni i DORi, K. A. Hobson, and S.
Least Bell’s Vireo. Studies in Avian Biology 18: A. Gii I . 1008. Nest tlelense by potential hosts of
160-166. the Browii-heaileil Cowbinl: methoilologieal ap
Kus, B. F2 2002. Fitness consec|uences of nest ilcser- proaches, benelits of ilefense, aiul coe\olutit>n.
tit)ii in an endangercti host, the Least Bell's Vireo. Pages 104 21 I in Parasitic birds and their hosts:
C’ondor 104:795 802. stiulies in coevolution tS. I. Rothstein aiul ,S. K.
22 THE WILSON BULLETIN • Vol. 116, No. I, March 2004
Robinson, Eds.). Oxford University Press, New Takasu, E 1998. Why do all hosts not show defense
York. against avian brood parasitism: evolutionary lag
Spaw, C. D. and S. Rohwer. 1987. A comparative or equilibrium? American Naturalist 151:193-
study ofeggshell thickness in cowbirds and other 205.
passerines. Condor 89:307-318.
