Food Resources of Anteaters (Edentata: Myrmecophagidae) I. A Year's Census of Arboreal Nests of and on Barro Colorado Island, Canal Zone Author(s): Yael D. Lubin, G. Gene Montgomery and Orrey P. Young Reviewed work(s): Source: Biotropica, Vol. 9, No. 1 (Mar., 1977), pp. 26-34 Published by: The Association for Tropical Biology and Conservation Stable URL: http://www.jstor.org/stable/2387856 . Accessed: 30/09/2012 22:16

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http://www.jstor.org Food Resources of Anteaters (Edentata: Myrmecophagidae) 1. A Year's Census of Arboreal Nests of Ants and Termites on Barro Colorado Island, Panama Canal Zone

Yael D. Lubin Smithsonian Tropical Research Institute, P. 0. Box 2072, Balboa, Canal Zone

G. Gene Montgomery' National Zoological Park, Smithsonian Institution,Washington, D.C. 20009, U.S.A. and

Orrey P. Young Department of Zoology, Universityof Maryland, College Park, Maryland 20742, U.S.A.

ABSTRACT Arboreal carton nests of four speces of termites( corniger, N. columbicus, N. nigriceps,and Microcero- termes exiguus) and of ants (genus Azteca) were monitoredperiodically for one year on Barro Colorado Island, Pan- ama Canal Zone. The nests were examined for signs of damage, new growth,and nest abandonment.Nest damage was attributableto predation by anteaters (Tamandua tetradactyla),to nestingactivities of birds, or to unknown causes. Nest damage due to anteaterpredation occurred frequently, but rarelyresulted in destructionof the nest. Small nestsof Micro- cerotermestermites were most prone to anteater damage, while large nestsof Nasutitermestermites suffered more dam- age from nestingbirds. Azteca nests were attackedby anteaters,but not by nestingbirds. Fewer Azteca neststhan ter- mite nests showed signs of predation during the year's census, with 37 percent of the ant nests damaged as compared with 91 percentof the termitenests. There were few instancesof multipledamage to ant nests,while 60 percentof ter- mite nests were damaged two or more times. No Azteca ant nestswere abandoned during the census, but 16 percentof termitenests were; most abandonmentsfollowed tree or nest-falls.The significanceof predationon nests by anteaters and of nest damage by nestingbirds is discussedin relation to seasonality,nest longevity,nest defense,and anteaterfeed- ing behavior. The census data and estimatesof the daily attack rates of anteaterson termiteand Azteca ant nests are used to estimate the impact of anteaterson these nests, and population densitiesof anteaters.

SEVERAL of arboreallynesting termites, and griceps (Haldeman), and Microcerotermesexiguus antsof the genusAzteca (Dolichoderinae),may be (Hagen). All fourspecies were utilized as preyby importantfood resources for banded anteaters(Ta- bandedanteaters. Sixteen of thesixty-one nests cen- mranduatetradct-yla) in lowlandmonsoon forest on susedwere not identifiedto speciesbecause samples BarroColorado Island, Panama (BCI). Arborealnests of thetermites were not obtained. of bothtermites and Aztecaants which wild, radio- Nasutitermesnests (table 1) were all arboreal markedanteaters encountered on BCI wereattacked and were medium-to-largesize (over 20 cm diam- infrequently,although in such nests could eter), while those of Mlicroceroternizeswere pre- providean abundantand nutritionallyimportant food dominandysmall (under 20 cm diameter), and were source (Montgomeryand Lubin,in press). When at ground level or relatively low on stumps or attacksoccurred, damage to nestsranged from very branches (fig. 1 ). Both typesof nests are within the slightto severe,but in no instancewas a nestcom- verticalforaging range of banded anteaters.N. corni- pletelydestroyed. The censusreported here was de- ger and AM.exiguus were the most common species in signedto monitordamage to a sampleof Aztecaand the census. Nests of M. exiguus rarely grow larger termitenests in an area of the forestused by ant- than 30-40 cm diameter.Small nests of N. corniger eaters.Other gross morphological changes in nests, must surely exist, but, because nests of this species suchas new growthand repairsor abandonmentof are generallyfound higher in the trees,small nests nests,were also monitored. may have been overlooked.All nests were composed of "carton,"a substance derived from chewed wood THE NESTS mixed with fecal material. Microcerotermes nests, to include some clay TERMITES: We censusednests of fourspecies of ter- however,sometimes appeared mitesof thefamily : Nasutitermes corniger and were harder and more dense than Nasutitermes (Motschulsky),N. columbicus(Holmgren), N. ni- nests. ANTS (Azteca spp.): All Azteca nestscensused were l Presentaddress: SmithsonianTropical Research Institute, P.O. Box 2072, Balboa, Canal Zone. arboreal, and composed of a papery substance de-

26 BIOTROPICA 9(1): 26-34 1977 rived fromchewed wood. The cartonmaterial of of Azteca rangedfrom 1-20 metersabove ground Azteca nestsis lightcolored, soft on the outsideof (mean 7.9 m, n 19). The nestswere from 30 thenest, and morecompact toward the center. Nests cm to 2 meterslong, eitherconical in shape and hangingfrom a limbor trunk(fig. 2), or flattened 8I againstthe side of a verticaltree-trunk. Nests were oftenclumped, and bothconical and flattenednests 6 Nosutitermescorniger could be foundwithin a singleclump. Azteca are 16nests. 'I 7.4 meters difficultto identifyto species,so specimensfrom eachnest are deposited with the senior author (Y. L.) for futureidentification. 0t METHODS 0- 3- 6- 9- 12- 15- CENSUSING TECHNIQUES: Thirty-fivetermite nests 3 6 9 12 15 18 and fifteennests of Aztecaants were mapped on 31 March 1974 on BCI, and examinedapproximately everytwo weeksuntil 23 April 1975. A finalcheck of the nestswas made in July1975. New nests,or that notbeen noticed previously, were later w nests had z 14- included.Other nests that became obscured by vege- tationor thatfell and were abandonedduring the 0 12 6 Microcerotermesexzguus courseof thecensus were omitted, so thatthe num- ber of nestsmonitored varied from census to census. 61O 22 nests. : 2.2 meters The nestswere located along a 1.8 km circularroute throuighthe forest,and were generallywithin 20 z metersof thepath. Not all nestsalong this route were includedin the census,because many were obsctured 6- by treesand lianas.The nestswere checked for signs of recentdamage (holes, scrapes,or missingsec- 4- tions),and forpatches of new growthor rep-airsto 82 3 6 5 1 the nest. nests that fell duringthe census 2 periodwere monitoreduntil the occupantsdied or vacated the nest. All termitenests were checked 0- occasionallyto determineif thenests were still active, 0- 3- 6- 9- 12- 15- usuallyby breakingtrails which led to thenest. Ac- tivityof Aztecanests was gaugedby the numbersof 3 6 9 12 15 18 ants movingup and down the tree-trunks. The censusmethod was non-destructive,and pro- METERS ABOVE GROUND vided informationon major morphologicalchanges FIGURE 1. Frequencydistribution of heights of censused occurringin a sampleof nestsduring one year.The nests of Nasutitermescorniger and Microcero- accuracyof censusingdiffered for ant and termite termesexigmus. nests.Damage to Aztecanests was conspicuous,and

TABLE 1. List of termitespecies censused and some characteristicsof theirnests. Nests sizes are: S = small (less than 20 cm diameter); M medium (20-50 cm diameter); and, L = large (greater than 50 cm diameter).

No. Species nests S M L Nest type Nasutitermescorniger 16 0 37.5 62.5 arboreal, carton,hard surface N. columbicus 3 0 66.6 33.3 arboreal, carton,hard surface N. nigriceps 2 0 0 100 arboreal, carton, thin papery surface,hard inside Nasutitermessp. 1 0 0 100 arboreal, carton Microcerotermesexiguus 23 78.3 21.7 0 tree bases or arboreal,carton (+ clay), surface with papillae-like extensions

Food Resources of Anteaters 27 could not distinguishholes made by trogonsfrom thosemade by puffbirdsand parakeets.In the analy- sis theseare groupedtogether under the categoryof bird damage.The birdsmay begin several holes and abandonthem before settling in a good nestingsite. Because of this habit,more termitenests may be dcamagedthan are used for nests.It is sometimes possibleto distinguishbird nest-holesfrom anteater damageto a nest,since completed holes are circular, 8-12 cm in diameter,and extenddeep intothe nest. Smallcavities or scrapemarks, however, could be due to eitherexploratory digging by birdsor small-scale attacksby anteaters. All damageto Azteca nests,ranging from small scrapesto destructionof one-thirdof the nest,was includedin the categoryof anteaterdamage. Only thoseincidents of damageto termitenests that were dearlydue to anteaters,such as visibleclaw marks or large irregularpieces of the nestremoved, were includedin thiscategory. Thus, nest damage by ant- eatersmay have been underestimatedfor term,ite nests. Euglossinebees (Apidae) also burrowin termite nests (Zucchi,et al. 1969), makingholes which are characteristically1-2 cm in diameterbut which prob- ablycause littledisturbance to thetermites. Holes of FIGURE 2. Hangingnest of Aztecasp. euglossinebees wereobserved in threenests of Mi- crocerotermesexiguus on 30 September(2 nests), and on 22 July(one nest), but were not recorded the causes were generallyobvious. New growth,how- as incidentsof nestdamage. ever, was much more difficultto observe in Azteca nests, because the color of the new portion of the RESULTS nest surfacedid not differmarkedly from the over- all color of the nest. Patches of new growth on ter- TERMITE NEST CENSUS: Some evidence of new mite nests were of lightercolor than the remaining growthin termitenests could be discernedat any nest surface,and thus easy to distinguish.Signs of time of the year (fig. 3). The largestnumbers of damage to termite nests and the causes were less nestswith new growthwere observed in mid-rainy obvious. Many termitenests had lumpy,irregular sur- season during July and August (table 2). New faces, whereon small scrapes or marks were difficult growthusually occurred in patchesover the surface to discern.It is likely that small scrapes made by ant- of the nest,most often on the upper side. Scraped eatersin the processof testingor feedingbriefly from placesand holeswere sometimes repaired or covered a nest passed unnoticed in the census. In virtually over with new extensionsof the nest.Large holes all instances,damage to Azteca nests was attributable weregenerally not filledin; instead,new extensions to predation by anteaters.The signs of damage con- werebuilt above theold, tornportion (fig. 4). The sisted of rips in a nest near its attachmentto the old portionsof the nestwere sometimes invaded by trunkor limb, sectionsbroken off the tip of the nest, antssuch as Dolichoderusspp. and Aztecaspp. (Do- or both, and daw marks were often visible on the lichcderinae). surface. Damagesto termitenests were seen in all months Damage to termitenests was attributableto nest- (fig. 5a). Heaviestnest damage, exceeding 1.0 per- ing birds as well as to anteaters. ( centof the nests per day, occurred during April 1974, massena,T. violaceus,T. viridis,and T. melanurus), in theearly wet season;during July-August, in mid- the ,Notharcus pectoralis, and the Tovi wet season;and in January1975, in earlydry season parakeet (Brotogerisjugularis) excavate nestingholes (table 2). Monthswhen little damage was seenwere in termitenests (Eisenmann 1952; Willis. ms.). We February-March1975, in the dryseason, and May-

28 Lubin, Montgomery, and Young 2.5

l) I 22.0 0

Lii t 1.5

I-

7-

19.0 ~17 z~~~~ l

D RY SEASON

FIGURE 3. Termite nests with new growth,expressed as percent nests per day with new growth.

June1974, in earlywet season. Nest damagein April 1975 was also low. Tamanzduaattacks were heaviest,exceeding, 0.5 percentof the nests per day, in April 1974, and AuguLstand January1975 (fig. 5b). Smallerpeaks of damageoccurred in Julyand October 1974. Bird- relateddamage exceeded 0.5 percentof nestsper day onlyin AuguLstand September1974 (fig. 5c). Iow- level nest damage by birds occulrredsporadically throughoutthe year,with the exceptionof May- June1974, in earlywet season. Most termitenests censusedwere damaged at leastonce duringthe year.Thirty-five termite nests werecensused for a fullyear, 91.4 percentof which weredamaged at leastonce (fig. 6). Manyof these nestswere only damaged once (40.6 percentof the damagednests), while some nestsincurred up to 8 incidentsof damage duringthe census.About 10 percentof thetotal 1140 observationsof nestswere of damagedones (table 3), or 0.7 percentof the nestsper day. Individuallarge termitenests (greaterthan 50 cm in diameter)were damaged more often than small(less than20 cm diameter)or medium(20- 50 cm diameter)nests (table 4), and a higherpro- IvA portionof large nests were damaged.Large nests FIGURE 4. Nest of Nasutitermes corniger showing new weremore prone to damage by birds than small growth.

Food Resources of Anteaters 29 nests,for damageby birds to small and medium- nests,24.0 percentof that to medium-sizednests, sized nestswas minimal,equal to about 5 percent and only17.0 percentof damage to largenests. Much of all damage,while 35 percentof all damageinci- of the damageto largetermite nests was thusattrib- dentsto largetermite nests were by birds.Anteater utable to bird-nestingactivities, while damage to attacksaccounted for 50.0 percentof damageto small smalland medium-sizednests was largelydue to ant- eaterpredation or unknowncauses. TABLE 2. Numbers of termiteand Azteca nests damaged, On the whole fewerMicrocerotermes nests were abandoned, and with new growth or repairs, duringa year's census on Barro Colorado Island, damagedthan those of Nasutitermesspp. (table 5), Panama. NR indicates that observations were and the numberof damagesper nestwas lower in not made. Microcerotermes(0.9 damagesper nest) than in Termite nests Azteca nests Nasutitermes (2.5 damagesper nest). Nasutitermes - nests were predominantlylarge and sufferedmore V. bird damagethan did Microcerotermesnests which werepredominantly small. Tamandua damagesto Mi- 28 380 1 v crocerotermesnests were greaterthan to those of Nasutitermesspp. (1974) 29 37 7 NR 0 15 0 0 Ten of the 61 termitenests censused (16.4 per- cent) wereabandoned during the period April 1974- May 14 39 1 NR 0 15 0 0 28 38 4 1 0 15 0 0 July1975 (16 months),or an averageof 1 percent per month(table 7). Most abandonmentswere me- June 11 39 1 1 0 16 1 0 dium 24 40 0 1 0 16 0 0 or large nestsand the resultof tree or nest- falls.Colony abandonment did not necessarilyfollow July 8 37 6 13 0 15 0 1 22 40 4 11 0 16 0 0 a tree-fallor nest-fall;some colonies persisted in the fallennest for manymonths and constructednew Aug. 3 44 8 8 0 13 1 0 18 47 4 12 1 15 0 1 foragingtrails into surroundingtrees. In one in- Sept. 3 42 3 1 0 22 0 0 16 38 4 5 0 19 0 1 2.5 - 30 45 4 6 0 22 0 0 2.0 Oct. 14 39 4 3 0 27 0 0 A 28 50 7 5 1 29 2 0 o .5 Nov. 11 54 6 2 0 28 9 0 Dec. 5 55 5 1 2 28 1 7 l.0 16 50 6 2 0 30 0 1 30 50 2 3 0 32 4 0 < 0.5 Jan. 14 50 5 0 1 35 1 4 (1975) 26 51 10 8 0 35 2 0 A M IJ IJ A S 0 N D J F M A Feb. 9 55 1 8 0 35 2 0 z 1974 1975 24 56 3 1 0 36 0 0 Mar. 11 55 1 2 0 36 0 1 z - Apr. 23 54 7 4 3 37 1 0 US 05

A M J J A S 0 N D J F M A TABLE 3. Summary of damages to all termite nests in- curred during the census, expressed as percent of total nest observationsand percent nests per 1.0- C day. - Average percent 0.5 No. nests damaged observations % per day M A J J A 5 0 N D J F N A No. nest observations 1140 No. observationsof DRY SEASON damaged nests 113 (9.9) 0.71 Anteaterdamage 28 (2.5) 0.17 FIGURE 5. Damage to termitenests, expressed as percent nestsdamaged per day. A) Total damage,B) Bird damage 25 (2.2) 0.16 damageby anteaters, C) damageby nesting birds.

30 Lubin, Montgomery,and Young stanceY. L. observedthe wholecolony vacating the tacked(table 2). Damagesat thelevel of 0.5 percent old fallennest and swarmingup a tree8 metersaway. of thenests per dayor moreoccurred in Augustand We could notdetermine if the colonyre-established December as well as in November.Fewer Azteca successfullyin the new tree.Two of the smallnests neststhan termitenests showed signs of predation thatwere abandoned duringthe censusappeared to duringthe year's census (table 7). The averagenum- havebeen torn apart, perhaps by an anteater.A third ber of attackson Azteca nestswas 0.6 per nest,or smallnest was vacatedfor unknown reasons, as the nestwas completelyintact and undamaged. 0.26 percentper day on an annualbasis. A totalof 594 observationsof Aztecanests were made, 3.9 per- AZTECANEST CENSUS: Damagesto Azteca nestswere cent of whichwere of damagednests, or less than sporadic(fig. 7). Theyoccurred in 9 monthsof the halfthe numberof damagesto termitenests (see 13-monthcensus, but only on 11 of the 25 census table3). Therewere few instances of multipledam- dates(44 percent).A largeburst of nestdamage was age to ant nests,and onlytwo nestswere damaged recordedin November,when 9 of 28 nestswere at- morethan twice during the census.

TABLE 4. Compaorisonof nest damage to small, medium, and large termitenests. N = numberof nestscensused. No. damages No. nests Total no. % total damages per nest Nest size N damaged % damages Anteater Bird ? 1 sd.

Small 25 15 (60.0) 20 50.0 5.0 0.8 ? 0.82 Medium 17 12 (71.0) 21 24.0 5.0 1.24 ? 1.20 Large 19 18 (94.7) 60 17.0 35.0 3.16 + 2.34** Total 61 45 (74.0) 101 25.0 23.0 * * significantat 0.01 > p > 0.001

TABLE 5. Damages to nests of Nasutitermesspp. and Microcerotermesexiguus. N = number of nests censused. Total No. % of total damages No. nests Species N damages Anteater Bird damaged % Nasutitermescorniger 16 48 20.8 33.3 15 (93.75) N. columbicus 3 2 0 0 2 (66.6) N. nigriceps 2 2 100.0 0 2 (100.0) Nasutitermessp. 1 5 0 60.0 1 (100.0) Nasutitermes,total 22 57 21.1 31.6 20 (90.9) Microcerotermesexigf1us 23 23 39.1 4.3 15 (65.2) Unidentified 16 21 19.0 19.0 10 (51-3) Total 61 101 24.8 22.8 45 (74.0)

TABLE 6. Termite nests that were abandoned during the census,aznd approximate number months from tree-fall to death of nest. T = tree-fall,N -nest-fall, D = destroyed,A = abandoned. Approximate Tree-fallto Nest date of tree-fall abandonment No. Size Species or nest-fall Last date active Abandoned (months) 22a. L N. corniger ll.XI.1974 T 23.VII.1975 No 22b. L N. corniger ll.XI.1974 T 11.III.1975 23.IV.1975 5 lOa(2). M N. corniger 16.IX.1974 T 23.IV.1975 23.VII.1975 10 9b.* L N. nigriceps 28.X.1974 T 5.XII.1974 A 5.XII.1974 2 13. L N. nigriceps ? T 23.IV.1975 23.VII.1975 17a. S M. exiguus ? D 30.XII.1974 14.1.1975 25a. M M. exiguus ? T 23.IV.1975 23.VII.1975 4. S unidentified 22.VII.1974 D 16.IX.1974 28.X.1974 6 3(1) a M unidentified 16.XII.1974 T 11III.1975 23.IV.1975 4 lOa(l). S unidentified - 3.VII.1974 A 18.VIII.1974 1 la. M unidentified - - ll.XI.1974 5.XII.1974 17. L unidentified 23.IV.1975 T 23.IV.1975 23.VII.1975 3 43b. M unidentified ? N 11.III.1975 23.IV.1975 * not included in census data

Food Resources of Anteaters 31 40 Damagedant nests were generally repaired within twoweeks of theattack. The scars,however, remained visiblefor one monthor more.Thus, the occurrence Li30- of nestrepairs followed that of nestdamage with a z slightlag. New growthon undamagednests was dif-

Cr) ficultto distinguish,and was omittedfrom the analy- La: 20 sis. All of the censusnests were intactand viable 0 after16 months.Nest-falls, tree-falls. or abandonment of Azteca nestswere not observed. z U DISCUSSION LiJ Q. SEASONALITY OF NEST DAMAGE: Seasonal factors could influencenest damage in severalways. Large concentrationsof termitereproductive stages (pre- alates and alates) in termitenests occur seasonally. NUMBER OF TIMES DAMAGED Anteatersmay monitor nests for the presenceof re- productives(Montgomery and Lubin,in press) and FIGURE 6. Frequency of incidents of damage of termite feed preferentiallyfrom termite nests that contain Li) 105- nests, expressed as percentof total nests. U- IO- alates and pre-alates.Alates are an orderof magni- tude heavier,and have a higherper gram caloric value than workeror soldier termites(Weigert 1970), thusit could be advantageousto feedfrom nestscontaining them.

2.5 I 74 3 1956 7 Some indicationof whenreproductives are pres- <2.5 entin termitenests can be inferredfrom when alates emergefrom the nests.Based on insectcaptures at lighttraps on BCI near the studyarea, winged ter- o .5 mites(all speciescombined) swarmed mainly during theperiod mid- or lateMay through June (H. Wolda, o.0 2 pers. comm.;Smythe 1973). Swarmingwas inter- mittentand correlatedwith periodsof heavyrain- 0.5ti a~~~~~~~~~~~ fall. Some winged termitescontinued to emierge throughSeptember or October,but duringseven or JoA J A S 0 N D J F M A eightmonths of theyear, from October-November to 1974 1975 May, therewere virtually no mass emergences.The DRY SEASON timerequired for alates of Nastititermesand Micro- cerotermesto develop,and theperiod they remain in the nestprior to emergence,is notknown. Alates of FIGURE 7. Damages to Azteca nests,expressed as percent nests damaged per day. otherspecies may be presentin the nestfrom a few daysto severalmonths before swarming, depending TABLE 7. Summaryof damages to 38 nests of Azteca spp. on the speciesand on weatherconditions (Nutting incur~reddur~ing the census. 1970). One bandedanteater was observedattacking neststhat contained reproductives on 17 March1974 Number Percent (N. corniger),22 March(N. corniger),8 April (N. Nests damaged, total 14 36.8 nigriceps), and 19 April (M. exiguus). The same once 8 21.1 twice 4 10.5 bandedanteater fed primarily on antsuntil the mid- three times 1 2.6 dle of March,when she switchedto feedingprimarily four times 1 2.6 on termites.In May she againswitched back to feed- Ave. no. damnages per nest ?+ 1 s.d. 0.605 ? 0.974 ingmainly on ants. Total nest observations 594 Observationsof Anteaterattacks on termitenests, as monitored damaged nests 23 3.9 in the census,did not necessarilycorrespond to per- Ave. percentnests iodswhen reproductive termites were present in nests. 0.26 damaged per day Some of the anteaterattacks, particularly in April,

32 Lubin, Montgomery,and Young however,may have been on nests containingrepro- nestssystematically while following an anteater,but ductives. Factors other than presence of alates may rathernoted their presence when the anteater passed influenceanteater attacks on termitenests. For ex- nearthem. ample, nests that contain dolichoderineants may be Averagerates of nestdamage by an anteatercan attacked more frequentlythan nests containingonly be estimatedfrom observed encounter and feeding Nasutitermes.Predation on such nests may not be rates.One radio-markedanimal fed on 17 of the 51 seasonal. timesit encounteredtermite nests, and on 10 of the Bird-nestingis also seasonal. Eisenmann (1952) 13 encounterswith Azteca nests on 25 datesduring and Willis (unpublished ms.) recordedtrogon, puff- whichwe followedand observedit. Thus, the ant- bird,and parakeetnesting in termitenests during the eaterattacked 17/51 = 33 percentof the termite period of March to July; much of the nest-digging nestsand 10/13 = 77 percentof the Aztecanests activityoccurs between March and May. During the whichit encountered.Our observationperiods lasted census we observed a male trogon (sp?) digging in 3.7 ? 1.6 hoursper day,while the anteater'stotal a termitenest on 15 and 29 April,and a male Trogon activityperiod was 7.4 ? 1.6 hoursper day.Thus, massena calling next to a termitenest with a new our observationperiods covered,on the average, hole on 26 January.Trogon damage to nestsrecorded 3.7/7.4 0.5 of the daily activityperiod, or the in the census covered a broader seasonal spectrum equivalentof 25/2 12.5days of observation. than reported in Eisenmann (1952). If theanteater attacked 33 percentof thetermite Damages to Azteca nestsshowed more seasonality nestsit encounteredin 12.5 days,then the average than did damages to termitenests, with a large peak daily attackrate is 33/12.5 2.6 percentof the of nest damage during the late wet season. It is not nests.Likewise, 77/12.5 6.2 percentof theAzteca known if this is correlatedwith changes in colony nestsencountered were attacked daily. By comparison, composition. dailyattack rates based on a year'scensus of nests were 0.17 percentfor termitenests (table 3) and NEST DAMAGE AND PREDATION BY ANTEATERS: The 0.26 percentfor Azteca nests (table 7). The dis- impact of anteaterpredation on nestsand the density crep,ancybetween these figures may be dtie to the of anteatersresponsible for the amount of nest dam- factthat anteaters do notmove randomly through the age observedcan be estimatedbased on (1) the cen- forest,but may select their paths in sucha wayas to sus data, (2) observeddensities of termiteand Azteca encounterparticular nests (Montgomeryand Lubin, nests, and (3) estimated rates of attack on nests in press). Thus,the sampleof nestsencountered by by an individual anteater. an anteateris not a randomsample of the nestsin Densities of termiteand Azteca nests were ob- the forest,and a large proportionof the nestsen- tained by searching carefully through three plots counteredare approachedand testedor attackedby 1000 m2 in surface area (100 meters long by 10 the anteater.This circumstancewould resultin a meters wide) randomlyselected within the census higherattack rate based on directobservation of an area, and recordingall nestsvisible in the trees.These anteaterthan on a censusof a randomsample of nests. are uindoubtedlyunderestimates, as some nests were The numbersof nestsattacked by an individual probably obscured by canopy vegetation.We found anteater,using the above attackrates, are 2.6/100 an average of 4.3 ? 1.5 (mean ? 1 s.d.) termite X 43 1.12 termitenests per hectareand 6.2/100 nests and 2.0 ? 2.0 Azteca nests per 1000 m2 of X 20 1.24 Azteca nestsper hectare(assuming groundsurface, or approximately43 termitenests and densitiesof 43 termitenests and 20 Aztecanests per 20 Azteca nestsper hectareof forest. hectare).By comparison,the numberof nestsdam- By comparison, one radio-markedanteater en- aged daily,based on the censusdata, are 0.17/100 couLntered51 termitenests and 13 Azteca nests in X 43 = 0.07 termitenests and 0.26/100 X 20 1184 trees on 25 observationdates, or 0.04 termite 0.05 Aztecanests per hectare. nests and 0.01 Azteca nests per tree. In our census The estimateddensities of anteatersresponsible of three 1000 m2 plots we counted 76.7 ? 18.1 trees forthe level of nestdamage observed in the censtus greater than 10 cm diameter per 1000 m2 surface are 0.07/1.12 0.06 and 0.05/1.24 0.04 ant- area, or approximately767 trees per hectare. Thus, eatersper hectare. We haveestimated the home range the anteater encounteredan equivalent of 0.04 X of two radio-markedbanded anteaters at 25-30 hec- 767 - 31 termitenests and 0.01 X 767 - 8 Azteca tares(Montgomery and Lubin,in press), and since nestsper hectarewhile foraging.These, too, are prob- some overlapof home rangesspaces does occtur,the ably underestimatesof the total nests present in the above estimateof 4-6 anteatersper 100 hectaresis treesused by the anteatersince we did not search for reasonable.

Food Resources of Anteaters 33 CONCLUSIONS Azteca nestsmay be longer-livedthan termite nests.The censusnests were not subjectto damage A year'scensus of arborealcartorn nests of termites by nestingbirds, and theywere damagedless fre- showedthat these nests were damagedoften. at an quentlythan were termitenests. Although heavy averagerate of 0.71 percentof the nestsper day. damagesof up to one-thirdof the nestwere record- Damageswere generally slight, and we observedonly ed, all of the censusnests survived throughout the two incidentsof total nest destructionthat might year.Survival may be partlyattributable to colony have been direcdycaused by predation.It appears, defenseof Azteca ants,which consists of swarming however,that nests suffered repeated damages, and overthe predator in largenumbers, biting, and secret- largernests were more likelyto be damagedthan ing chemicalswhich may act as repellents(unpub- small ones (particularlyby nestingbirds). Termite lished data). Montgomeryand Lubin (in press) nestswere abandonedat a rate of 1 percentper showedthat this defensebehavior was effectivein month,and themajority of theabandoned nests were repellinganteaters. Another feature of Aztecacolonies over 50 cm in diameter. whichmay contribute to theirlongevity is the tend- Colonydefense in Nasutitermesand Microcero- encyof growingcolonies to formsatellite nests near termesmay be correlatedwith different susceptibili- theparent nest and apparentlyconnected to it. Thus, ties to predators.Microcerotermes colonies defend colonysurvival is ensuredeven if some of the nests themselvesby having a hardnest. If thenest is broken are damaged. open,the termitesavoid contactwith breaks in the We concludethat anteater predation on arboreal nestsurface by escapinginto the dense center of the coloniesof termites and Aztecaspp. does not normally nest (unpublisheddata). Colonydefense of Nasuti- severelydamage or destroythe nest.This situation termesinvolves production of large numbers of nasute maybe due to effectivedefense behaviors employed soldierswhich mobilize rapidly at a breakin thenest by the preyspecies, involving active defense in the and mayrepel predators by meansof a chemicalde- case of Aztecaand Nasutitermesand passivedefense fense (Stuart1970). In the one case, the energetic in the case of Microcerotermes.The year'scensus of costof nestdefense seems to be tiedup in nesthard- a sampleof thesenests demonstrates that they are a ness;in theother, it maygo intocontinuous produc- re-usable,and repeatedlycropped, resource for ant- ticn of largenumbers of dispensablesoldiers. Micro- eatersand nestingbirds. cerotermescolonies may be protectedby theirsmall size and dense nest fromattacks of nestingbirds ACKNOWLEDGEMENTS (but notfrom euglossine bees), and fromsome dam- The studywas supportedby the SmithsonianTropical Re- age by anteaters.The chemicaldefense of Nasuti- searchInstitute's Environmental Sciences Program. We thank termes soldiersdoes not seem to protectthe nest Dr. EgbertLeigh for criticizingan earlier draftof the man- againstnesting birds, but may be more effective uscript, and other members of the Smithsonian Tropical Research Institutefor their helpful comments.Dr. R. L. againstanteaters (Montgomery and Lubin,in press). Araujo of Sao Paulo, , kindly identifiedthe termites.

LITERATURE CITED

EISENMANN, E. 1952. Annotatedlist of birds of Barro Colorado Island, Panama, Canal Zone. Smithson. misc. Collns 117 (5) : 1-62. MONTGOMERY,G. G., AND Y. D. LUBIN. In press. Prey influences on movements of neotropical anteaters. In, R. L. Phillips and C. J. Jonkel (Eds.). Proceedingsof the 1975 PredatorSymposium, Montana Forestand Conservation ExperimentalStation, School of Forestry,University of Montana, Missoula. NUTTING,W. L. 1970. Flight and colony foundation.In, K. Krishna and F. M. Weesner (Eds.). Biology of Termites, Vol. 1. Academic Press, New York. SMYTHE, N. D. 1973. sampling. In R. W. Rubinoff (Ed.). EnvironmentalMonitoring and Baseline Data, SmithsonianInstitution Environmental Sciences Program,Tropical Studies. STUART, A. M. 1970. The role of chemicals in termitecommunication. In J. W. Johnson,Jr., D. G. Moulton, and A. Turks (Eds.). Advances in Chemoreception.Vol. I: Communicationby Chemical Signals. Appleton-Century-Crofts, New York. WEIGERT, R. G. 1970. Energeticsof the nest-buildingtermite, Nasutitermescostalis (Holmgren), in a Puerto Rican forest.In H. T. Odum (Ed.). A Tropical Rainf!orest:A Study of Irradiation and Ecology at El Verde, . Oak Ridge Atomic Energy Commission. WILLIS, E. 0. Ms. A revised list of birds of Barro Colorado Island, Panama, Canal Zone. ZUCCHI, R., S. F. SAKAGAMI, AND J. M. F. DE CAMARGO. 1969. Biological observationson a neotropicalparasocial bee, Eulaema nigrita,with a review on the biology of Euglossinae (,Apidae). A comparative study.J. Fac. Sci. Hokkaido Univ. Ser. 6 (Zool.) 17(2): 271-380.

34 Lubin, Montgomery,and Young