International Journal of Primatology, Vol. 27, No. 1, February 2006 ( C© 2006)DOI: 10.1007/s10764-005-9008-x

Direct and Indirect Impacts of Raptor Predationon Lemurs in Southeastern Madagascar

Sarah M. Karpanty1,2

Received November 18, 2004; accepted January 17, 2005;

Published Online April 4, 2006

I calculated rates of predation by 2 species of diurnal raptors, Polyboroidesradiatus and Accipiter henstii, on the lemur community of RanomafanaNational Park, Madagascar from 2700 h of observation and 470 preydeliveries at 7 nests of each hawk species. The 2 hawks consumed 7 of 12lemurs found in the park region, with a body mass of 63–3500 g and includ-ing diurnal and nocturnal species of all group sizes. Calculations of preda-tion rates indicate that raptor predation is a significant cause of mortality forlemur populations relative to other causes. Minimum rates of predation byPolyboroides radiatus and Accipiter henstii on Microcebus rufus,Cheirogaleus major, Avahi laniger, Hapalemur griseus, Eulemur fulvus ru-fus, Eulemur rubriventer, and Varecia variegata resulted in the raptors re-moving of 1–21% of the population per yr, similar to other rates of pre-dation on primates documented in the literature. Modeling of lemur pop-ulations under varying levels of raptor predation pressure that I calculatedfound that one may attribute 3–17% of adult, juvenile, and infant mortal-ity for nocturnal lemurs and 2–66% of adult, juvenile, and infant mortalityfor diurnal lemurs to diurnal raptor predation. Raptor predation may signif-icantly depress intrinsic growth rates and carrying capacity of Avahi laniger,Hapalemur griseus, Eulemur fulvus rufus, Eulemur rubriventer, andVarecia variegata owing to their low fecundities, long life spans, and longage to sexual maturation. Nocturnal lemurs may best avoid predation by di-urnal raptors by exhibiting a solitary lifestyle and cryptic antipredator tactics,

1Department of Ecology and Evolution, State University of New York, Stony Brook, NewYork.

2To whom correspondence should be addressed at Department of Fisheries and Wildlife, 106Cheatham Hall, Virginia Tech, Blacksburg, Virginia 24061-0321; e-mail: karpanty@vt.edu.

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0164-0291/06/0200-0239/0 C© 2006 Springer Science+Business Media, Inc.

240 Karpanty

whereas, diurnal lemurs benefit less by increasing group size than by usingspecific antipredator tactics.

KEY WORDS: conservation; lemurs; Madagascar; predation; raptors.

INTRODUCTION

There is little doubt that the interactions between predation, social-ity, and behavior are complex (Janson, 2003). The most direct method toexplore the impact of predation on primate populations is to conduct stud-ies of the predators themselves that would reveal the prey profiles for eachpredator (Janson, 1998). Combining prey profiles with demographic param-eters of predator and prey allows estimation of actual predation rates. Thefew direct predator studies conducted to date have consistently demon-strated that primates are subject to a diverse group of predators (Mitaniet al., 2001; Rasoloarison et al., 1995; Shultz, 2001, 2002a,b; Skorupa, 1989;Struhsaker and Leakey, 1990; Wright et al., 1997).

Though Madagascar may have lost some important aerial predators inthe last 2 millennia (Goodman, 1994a,b; Goodman and Rakotozafy, 1995),observations of predation clearly demonstrate the existence of a diverseextant predator fauna on the island (Brockman, 2002; Goodman et al.,1993; Karpanty and Goodman, 1999; Rasoloarison et al., 1995; Rene deRoland, 2000; Wright, 1998; Wright et al., 1997). A strong debate continueson the role of predation by diurnal raptors in the evolution of the diversesocial structures, activity patterns, and behaviors in the lemur radiation(Kappeler, 1997; van Schaik and Kappeler, 1996; Wright, 1999). We needinformation on the details of the predation process to make progress in thisdebate.

It is also critical to understand the ecological and behavioral interac-tions between lemurs and their predators to accurately establish manage-ment objectives for the rapidly decreasing populations of both predatorand prey. Biodiversity monitoring in Madagascar often incorporatescomponents of lemur communities, but minimal quantitative data exist onthe ecological details of predator-prey interactions between lemurs andthe raptor community despite strong behavioral evidence of an interaction(Fichtel and Kappeler, 2002; Karpanty and Grella, 2001; Overdorff et al.,2002; Sauther, 1989, 2002). Predation by raptors on lemurs may have asignificant impact on lemur communities that population viability assess-ments and reserve planning have previously underestimated. Researchershave conducted high-quality studies examining the influence of factorssuch as human disturbance (Johnson et al., 2003), resource extraction(Merenlender et al., 1998), and natural disasters (Ratsimbazafy, 2002) on

Raptor Predation on Lemurs 241

lemur population dynamics, but no study has quantitatively examined theimpact of natural predators on lemur populations.

My objectives are to 1) report predation rates by diurnal raptorson the lemur community of Ranomafana National Park; 2) describe thedirect impact of raptor predation on lemur population dynamics andimplications for conservation of lemur communities; and 3) discuss ratesof predation in reference to lemur body size, group size, activity patterns,and existing antipredator tactics. Raptors in Ranomafana National Parkthat kill both large and small lemurs include Polyboroides radiatus, theMadagascar Harrier-Hawk, and Accipiter henstii, the Henst’s Goshawk.Polyboroides radiatus averages 68 cm in adult body length and is endemic,nonthreatened, and fairly common throughout Madagascar in woodlandfrom sea level to 2000 m (Langrand, 1990). Accipiter henstii averages57 cm in adult length and is a near-threatened species (Collar et al., 1994),endemic, and though rare throughout its range, is found in forested areasfrom sea level to 1800 m. Both raptors nest annually in the Ranomafanaregion between August and January, coincident with lemur birth seasons,and hunt in a variety of habitats ranging from village agriculture to primaryforest (Karpanty, 2003).

MATERIALS AND METHODS

Study Site

I conducted the study in and around Ranomafana National Park(RNP), Madagascar. RNP is 43,500 ha of continuous montane rain for-est in southeastern Madagascar at 21◦16′S latitude and 47◦20′E longi-tude. Temperatures range from lows in June–September (4–12◦C) to highsin December–February (36–40◦C). Elevations range from 500 to 1500 mwithin the park, and annual rainfall ranges from 2300 to 4300 mm. The fau-nal diversity in RNP is high, with 112 species of birds, 6 species of viverrids,and 12 species of lemurs (Wright, 1998; Wright and Andriamihaja, 2002).

Predation Rate and Mortality Calculations

I quantified lemur predation rates from direct observations of prey de-liveries to active nests of Polyboroides radiatus and of Accipiter henstii fromAugust through January of 1999, 2000, 2001, and 2002. Young birds fledgeand disperse from the nest area in January and it becomes difficult to locateboth fledglings and adults (Karpanty, 2003). Over the 4 seasons, I observed7 nests of Polyboroides radiatus for a total of 1007 h with 186 observed preydeliveries. I observed 7 nests of Accipiter henstii for a total of 1703 h with

242 Karpanty

284 observed prey deliveries. I always identified prey deliveries to the nestto the most precise taxonomic level possible. I conducted focal nest obser-vations from sunrise to sunset for 1–2 d per nest per wk. I made observationsfrom a distance of ≥ 150 m to minimize nest disturbance and collected boneremains of prey species from under and within nests of the raptors. I sum-marized predation rates from direct observations of prey deliveries to thenests of the raptors and do not include bone remains from under and withinthe nests as I could not be certain that I had not already counted remains asa prey delivery and did not want to overestimate lemur predation rates.

The following equation describes the details needed to quantify preda-tion rates during a nesting season of duration D days from direct studies ofraptor predators.

No. of lemurs killedNest×D × No. of nests

km2

No. of lemurs available= No. of lemurs killed

(No. of lemurs available) × D

= Proportion of lemurs killedD

(1)

The result of the equation is a predation rate that one can interpret as theproportion of a lemur population killed by a raptor species in a given timeperiod. Collecting the information needed to complete the measurement ofpredation rates requires the concurrent collection of data on 1) prey profilesof the raptor predators, 2) densities of the predators, and 3) densities of theprey. Interpretation of the data in terms of lemur life histories and popu-lation dynamics also requires the collection of data on lemur birth rates,survivorship, and causes and rates of mortality. Important characteristics oflemur prey species in my study are in Table I, summarized from the pub-lished literature. There is an extensive history of research in and aroundRanomafana National Park (Wright and Andriamihaja, 2002). I used onlydata from peer-reviewed journals (n = 268) or Ph.D. dissertations (n =21). I calculated breeding densities of Accipiter henstii (1 pair/24.1 km2) andPolyboroides radiatus (1 pair/13.4 km2) from all known nests (Karpanty,2003).

For each lemur species that Accipiter henstii, Polyboroides radiatus, orboth delivered to the nest, I calculated a minimum, medium, and maximumrate of predation. First, for each raptor nest, I divided the total numberof individuals of a lemur species killed by the total number of h of obser-vation at that nest to give the number of lemurs killed/h, then simplifiedto the number of lemurs killed per 12-h d. Given a lack of significant dif-ferences between nests and yrs of a raptor species in terms of lemur preydeliveries (Karpanty, 2003), I then summarized the information at the levelof lemur and raptor species to give the total number of lemurs killed per

Raptor Predation on Lemurs 243T

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244 Karpanty

d per raptor species (no. of lemur species X killed/d/raptor species Y). Forthe calculation of the maximum possible yearly predation rate, I assumedthe observed daily delivery rate to be constant across the yr (D = 365). Theassumption of equal predation pressure across the yr places an upper boundon my predation rate calculations from my study by assuming that the di-etary requirements of the raptors and the vulnerability of lemurs do notchange over the yr. For calculation of a minimum predation rate, I assumedthe observed daily lemur delivery rate applied for the nestling and fledglingstage of the raptor nesting cycle but that no lemur prey captures occurredoutside of this nesting period (D = mean length of the nestling-fledglingperiod for each raptor species; Karpanty, 2003). Finally, for calculation of amedium estimate of predation rate, I assumed the observed lemur deliveryrate applied during the nestling-fledgling periods of the nesting cycle, but tobe one-half of that rate for the nonnesting portion of the yr.

I calculated the contribution of raptor-caused mortality to overallmortality by dividing the proportion of the population removed by rap-tor species by the overall proportion of the lemur population assumed todie each yr as summarized from the literature in Table I (raptor mortal-ity/overall mortality). I based mortality calculations on the combined maxi-mum, medium, and minimum estimates of predation by both Accipiter andPolyboroides. I applied observed raptor predation rates equally to adult, ju-venile, and infant lemurs as I observed all 3 age classes in the bone remainsunderneath nests. We need further studies to determine if predation ratesare unequal across age classes for these species.

Lemur Population Dynamics

I used the RAMAS (Akcakaya and Root, 2002; Akcakaya et al., 2002;Salia, 1997; Waller, 1998) age-structured modeling program to calculate theimpact of the maximum, medium, and minimum observed predation rateson lemur intrinsic growth rates and population carrying capacity. The ageof sexual maturity, fecundity, and mortality values summarized from fieldobservations of each lemur species used in the modeling exercises are inTable I. Future studies will undoubtedly improve the quality and depthof these lemur datasets, and I caution that the results of the modeling ex-ercises I describe rely only on the information currently available. Fieldmortality data from all causes including predation were unavailable forMicrocebus rufus, Cheirogaleus major, and Varecia variegata. Given thesimilarity in activity patterns and social structures, I assumed mortalityvalues for Microcebus and Cheirogaleus to be identical to Avahi lanigerand values for Varecia to be identical to Propithecus edwardsi. In reality,Microcebus and Cheirogaleus may have higher mortality rates than Avahi,

Raptor Predation on Lemurs 245

and Varecia may have higher mortalities than Propithecus, because thebody sizes of the unknown species are smaller than for the known speciesfrom which I extrapolated their mortality rate. Given this directionality inthe assumptions, the conclusions of the model may overestimate the impactof raptor predation on overall rates of mortality for Cheirogaleus, Microce-bus, and Varecia.

In the model, I calculated the intrinsic rate of increase (r) by quanti-fying the finite rate of increase (λ), or the eigenvalue, of the age-structuredmatrix of the wild population of lemurs. Calculations of the finite rate ofincrease, which measures the proportional change in population size fromone yr to the next, ignore density dependence and model population in-crease under exponential growth conditions. I calculated the population in-trinsic growth rate by approximating r = ln λ when generation time is 1 andthen adjusted observed field mortality and survivorship data under calcu-lated maximum, medium, and minimum rates of raptor predation to calcu-late intrinsic growth rate with and without the presence of raptor predation.Specifically, I assumed the observed rates of mortality include predator-related mortality and thus subtracted the maximum, medium, and minimumrates of predation from the observed field mortality rates to calculate whatthe intrinsic growth rate of the population would be if there were no raptor-related deaths. Therefore, the 4 conditions modeled were: 1) field observedrates of mortality and survivorship, i.e., the population is experiencing pre-dation; 2) the population experiencing no predation using the maximumestimate of predation, i.e., mortality rates are decreased, and survivorshipvalues increased, by the maximum estimate of raptor predation; 3) the pop-ulation experiencing no predation using the medium estimate of raptor pre-dation; and 4) the population experiencing no predation using the minimumestimate of raptor predation. I compared the intrinsic growth rate of lemurpopulations under predation pressure (1) and under situations in which thepopulation is released from predation pressure (2–4).

Next, I modeled the population trajectory of each lemur species undera harvest model in which the harvest rate is first 0 and then equal to themaximum, medium, and minimum raptor predation rates observed viasimulations of 50 time steps in RAMAS. For each simulation, I set themaximum growth rate to that calculated from the stage matrix, assumedharvest to be constant across all age classes, and the population experiencesdemographic stochasticity and contest density dependence. I assumedpredation rate is constant throughout the simulation; thus I did not modelthe response of the raptors to decreasing lemur population sizes, orimmigration or emigration by the lemur population. The purpose of thissimulation is to determine if the varying level of predation rates may de-press the carrying capacity of stable lemur populations and future modeling

246 Karpanty

exercises should explore the interactions of predation and lemur dispersal. Icalculated carrying capacity from the simulation for each harvest conditionand compared the percentage change in population size under simulationsof no harvest vs. harvest at different levels.

RESULTS

Predation Rates

Seven of 12 lemur species present in the region of RNP ex-perience predation by Accipiter henstii and 4 of 12 lemur speciesface predation by both Accipiter henstii and Polyboroides radiatus(Table II; Fig. 1). Lemur bone remains included infant, juvenile, andadult individuals of all species observed delivered to the nests exceptEulemur and Varecia (Karpanty, 2003). The lack of bone remains ofEulemur and Varecia prey may likely be due to the low number of actual

Table II. Predation rates (maximum, medium, minimum) and nest delivery data (mean no.of lemurs killed/d during the nest season) by Accipiter henstii and Polyboroides radiatus as

calculated from direct nest observations

Predation rate from Number oflemurs

Lemur speciesAccipiter

henstiiPolyboroides

radiatus Combinedkilled/dcombined

Microcebus rufus Maximum 2.77 4.94 7.72 0.44Medium 1.55 2.78 4.33Minimum 0.33 0.61 0.94

Cheirogaleus major Maximum 3.85 2.17 6.02 0.22Medium 2.16 1.22 3.38Minimum 0.46 0.27 0.73

Avahi laniger Maximum 5.82 14.84 20.66 0.51Medium 3.26 8.34 11.59Minimum 0.70 1.83 2.53

Hapalemur griseus Maximum 75.51 48.84 100 0.37Medium 42.31 27.43 69.74Minimum 9.10 6.02 15.12

Eulemur fulvus rufus Maximum 10.35 0 10.35 0.08Medium 5.80 0 5.80Minimum 1.25 0 1.25

Eulemur rubriventer Maximum 12.80 0 12.80 0.07Medium 7.17 0 7.17Minimum 1.54 0 1.54

Varecia variegata Maximum 6.22 0 6.22 0.02Medium 3.48 0 3.48Minimum 0.75 0 0.75

Note. Predation rate equals the percentage of the lemur population each raptor species killedper yr, or the combination of the 2 hawk species.

Raptor Predation on Lemurs 247

Fig. 1. Combined rates of predation by Accipiter henstii and Polyboroides radiatus on thelemur community of RNP as calculated from direct nest observations in this study. Bars con-nect the minimum, medium (shown as point), and maximum estimates of predation rates ascalculated in this study.

prey deliveries observed of these species (Eulemur sp., 6 prey deliveries;Varecia variegate variegate, 1 prey delivery). I did not find the following5 species of lemurs in either prey remains or in deliveries to the nests:Daubentonia madagascariensis, Lepilemur microdon, Hapalemur aureus,Hapalemur simus, and Propithecus edwardsi.

Though more than 1 lemur prey delivery/d to the raptor nests was rare(Table II), annual combined predation rates ranged from 0.94% to 20.66%for nocturnal lemurs and 0.75–12.80% for the largest 3 diurnal lemurs.Hapalemur griseus experienced the highest predation rates with a minimumof 15.12% of the population removed annually by these 2 hawks (Table II;Fig. 2).

Relative Contribution of Raptor Predation to Overall Mortality

Diurnal raptor predation accounts for between 4% and 100% of to-tal adult (Fig. 2), 3–83% of total juvenile (Fig. 3), and 3–60% (Fig. 4) oftotal infant mortality for nocturnal lemur species. Similarly, raptor pre-dation accounts for 2 to >100% of total adult (Fig. 2), 4–100% of to-tal juvenile (Fig. 3), and 2–100% (Fig. 4) of total infant mortality in

248 Karpanty

Fig. 2. Percentage of total adult mortality caused by predation by Accipiter henstii and Poly-boroides radiatus on the lemur community of RNP. Bars connect the minimum, medium(shown as point), and maximum estimates of percentage mortality caused by raptors for eachlemur species.

diurnal lemur species. Predation by diurnal raptors most significantly im-pacted Avahi laniger and Hapalemur griseus in the context of overall mor-tality rates.

Effect of Diurnal Raptor Predation on Lemur Population Dynamics

The intrinsic growth rate of each of the lemur prey species increasedsignificantly after release of modeled wild populations from diurnal raptorpredation pressure (Fig. 5). Growth rates <0 indicate a decreasing popula-tion and are not unexpected, as long-term studies of Propithecus edwardsiin the study area indicate that it is a shrinking population (Pochron et al.,2004). The depression of intrinsic growth rates by raptor predation is mostevident in the large-bodied, diurnal lemur species (Eulemur and Varecia) inwhich growth rates reverse from negative to positive when raptor predationpressure is released from its maximum level (Fig. 5).

Figure 6 summarizes the percentage change in carrying capacity (K)for each lemur species from the condition of no harvest to that of harvestat different raptor predation levels. There are large decreases in carryingcapacities for all lemurs experiencing medium and maximum estimates of

Raptor Predation on Lemurs 249

Fig. 3. Percentage of total juvenile mortality caused by predation by Accipiter henstii andPolyboroides radiatus on the lemur community of RNP. Bars connect the minimum, medium(shown as point), and maximum estimates of percentage mortality caused by raptors for eachlemur species.

raptor predation compared to lemur populations without predation, e.g.,no harvest. Even under minimum estimates of raptor predation, all lemursexcept the 2 smallest nocturnal species, Microcebus and Cheirogaleus, havegreatly reduced carrying capacities compared to populations without pre-dation pressure.

DISCUSSION

Raptor Predation Rates

For Microcebus rufus, Cheirogaleus major, Avahi laniger, Eulemur ful-vus rufus, Eulemur rubriventer, and Varecia variegata, the calculated preda-tion rates varied from 1% to 21% of the lemur population removed per yrby raptor predation, in accordance with values for other primate species, in-cluding lemurs, reported elsewhere (Cheney and Wrangham, 1987; Clutton-Brock and Harvey, 1977; Goodman et al., 1993). For Hapalemur griseus, themost frequently killed lemur species in this study, the minimum combinedpredation rate of 15% is in the range of values reported for other primate

250 Karpanty

Fig. 4. Percentage of total infant mortality caused by predation by Accipiter henstii and Poly-boroides radiatus on the lemur community of RNP. Bars connect the minimum, medium(shown as point), and maximum estimates of percentage mortality caused by raptors for eachlemur species.

species; however, the medium and maximum extrapolations of 69% and100% of the Hapalemur griseus population killed per yr by diurnal raptorsseem unrealistic. For Hapalemur griseus and other lemur species, preda-tion pressure by these raptors may be reduced outside of the nesting seasonif other prey items become easier to catch, are more available in differentseasons, or if the activity patterns of the lemurs make them more difficultto catch at different times of the yr (Newton, 1998). Curtis et al. (1999) hy-pothesize that the seasonal cathemeral behavior of the mongoose lemur,Eulemur mongoz, may be an adaptation to reduce raptor predation riskduring dry seasons with little protective vegetative cover. Evidence frommy study does suggest that raptor predation on lemurs varies across the an-nual cycle, with no lemur predation observed during the incubation periodof the nesting season or during 1280 h of searching for 4 radio-tagged Accip-iter henstii (Karpanty, 2003). Similarly, Sauther (2002) found that monthlypredator encounters by groups of ring-tailed lemurs, Lemur catta, andVerreaux’s sifaka, Propithecus verreauxi, peaked annually during the birthand weaning seasons of the lemurs.

The absence of 5 species of lemurs present in the region of RNP fromthe diet of the 2 raptor species likely has 2 explanations. 1) Analyses of the

Raptor Predation on Lemurs 251

Fig. 5. Depression of intrinsic growth rate by raptor predation on the lemur community ofRNP. The black bar illustrates the intrinsic growth rate of the wild lemur population experi-encing predation. The bars labeled max, med, and min predation correspond to the intrinsicgrowth rate of the population released from predation pressure, using the varying levels ofcalculated predation rates.

prey profiles of these raptors indicate that they are foraging on prey to someextent according to prey abundance (Karpanty, 2003). Thus, the absence ofLepilemur microdon (970 g, 0.82 ind/km2) and Daubentonia madagascarien-sis (3500 g, 2 ind/km2) may be the result of their patchiness and rarity in theregion of RNP, given that their body sizes and antipredator tactics do notdiffer from those of other lemur prey species in my study (Wright, 1998).However, densities of Hapalemur aureus (1600 g, 6 ind/ km2, 2–4 ind/group)and Hapalemur simus (2600 g, 4.6 ind/ km2, 4–12 ind/group) are similar tothose of the other lemur prey species and the frequently killed Hapalemurgriseus (1000 g, 4.99 ind/ km2, 2–11 ind/group). The lack of the 2 speciesof Hapalemur from the hawks’ diets does not clearly relate to overall den-sity, body mass, or group size. However, detailed studies of all 3 speciesof Hapalemur indicate that though all species are bamboo specialists,Hapalemur griseus is the most flexible in diet, activity, and ranging patterns(Grassi, 2001; Tan, 2000). The reason for the lack of Hapalemur aureus andHapalemur simus from the diets of the raptors may be that these lemurs arehabitat specialists and the raptors are likely central-place foragers (Shultzand Noe, 2002). The patchy distribution of bamboo and Hapalemur aureus

252 Karpanty

Fig. 6. Percentage change in the carrying capacity of each lemur species caused by raptor pre-dation under minimum, medium, and maximum estimates of predation rates. Only the effectsof harvest on lemur population abundance are modeled in this simulation. Error bars are 1standard deviation around the mean change in K and represent the effect of demographicstochasticity on the estimates of K.

and Hapalemur simus (Arrigo-Nelson and Wright, 2004) may not coincidewith the focused ranging patterns of the hawks in a region near the nest site.Further, the dense large bamboo stands that Hapalemur aureus and Hapale-mur simus use do not offer a good structure for the sit-and-wait huntingtactics of the raptors (Karpanty, 2003). The absence of adult Propithecusedwardsi is likely a result of their large body mass (5800 g, 21.55 ind/ km2,Wright, 1998); however, the absence of infant and juvenile Propithecus de-serves further explanation and may be related to antipredator tactics as dis-cussed later.

PREDATION, MORTALITY RATES, AND LEMURPOPULATION DYNAMICS

Analyses of the impact of predation by Accipiter henstii and Poly-boroides radiatus on the overall rate of mortality, intrinsic growth rate, and

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population carrying capacity of the lemur populations provide importantfindings for both the debate on lemur life history and social evolution andconservation of endangered species such as Varecia variegata. First, utilizingjust the minimum observed annual predation rates and assuming no raptorpredation occurs outside of the nesting season, diurnal raptor predation ac-counts for between 4% and 15% of total adult, 3–10% of total juvenile,and 3–17% of total infant mortality for nocturnal lemur species. Similarly,the minimum levels of predation account for 2 to >66% of total adult,4–66% of total juvenile, and 2–46% of total infant mortality in diurnallemur species. Second, again utilizing the minimum estimates of predationrates, it is evident that raptor predation may significantly depress intrinsicgrowth rates and population carrying capacity of populations of Avahi, Ha-palemur, Eulemur, and Varecia. Though the raptors frequently kill Micro-cebus and Cheirogaleus, their high fecundity and early age to sexual mat-uration limit the negative effects of predation on their population growthtrajectories, even given that one may have overestimated the contributionof predation to overall mortality for the species (see earlier). However,the lower fecundities and later age to maturation of Avahi and the diurnalspecies result in a significant impact of raptor predation, suggesting that forthe diurnal species, raptor predation should be a strong selective pressureon the evolution of life history parameters and the social systems in whichthe lemur life histories are engaged. By contrast, diurnal raptor predationis less likely an important selective factor on the highly fecund, nocturnallemurs. As more information becomes available on field mortality rates oflemurs, researchers should reassess these models. We also need more infor-mation on raptor diets and lemur disappearance data to determine if lemurmortalities and predation rates vary across infant, juvenile, and adult ageclasses.

The findings are especially relevant in discussions of conservation andmanagement of endangered lemur species. Raptor populations may be ca-pable of depressing diurnal lemur populations below levels that the envi-ronment may otherwise support. The impact of raptor predation on lemurscould lead to local extinctions of lemurs in the fragmented habitats socommon throughout Madagascar assuming that fragmentation does notadversely affect raptor predation rates (Crooks, 2002; Mikkelson, 1993).My findings suggest that some species, such as Polyboroides, may actu-ally increase in fragmented habitats and that Accipiter henstii individualswill forage in a matrix of primary and fragmented forest, making frag-mentation potentially more dangerous for the lemurs than it is to the rap-tor predators (Karpanty, 2003). Long-term studies in other systems havereliably demonstrated that raptors can 1) depress breeding numbers ofprey species below what the habitat would support (red grouse, Jenkins

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et al., 1964; Redpath, 1991), 2) cause oscillation of prey numbers (grouse,Watson and Moss, 1979), or 3) promote the extinction of prey species(seabirds, Newton, 1993). Population viability analyses of endangered andthreatened lemur species have previously not considered the effect of dy-namic predator communities on lemur populations, a factor that is impor-tant to take into account given this new evidence of their potential impact.

Effects of Body Size, Group Size, and Activity Pattern on Predation Rates

Lemurs that Accipiter henstii killed ranged from the smallest to thesecond largest lemur in this region and excluded only the 5.8-kg Propithe-cus edwardsi. Polyboroides radiatus predation was more size limited as thelargest lemur the raptor captured was the 700-g Hapalemur griseus. Sur-prisingly, I found no infant or juvenile Propithecus in the diet of the raptorsdespite strong behavioral reactions of the lemurs to encounters with anyButeo brachypterus, Accipiter, or Polyboroides individuals (Wright, 1998).My study, along with previous investigations of the diurnal raptor species,identified that Accipiter henstii and Polyboroides radiatus are capable ofcapturing and returning to the nest with lemur prey up to 4 kg (Karpantyand Goodman, 1999; Rene de Roland, 2000; present study). It is importantto emphasize that though the large size of adult Propithecus edwardsi mayfree them from predation pressure by the diurnal raptors, the lemurs stillexperience significant predation risk from the terrestrial carnivore fossa,Cryptoprocta ferox (Wright, 1998; Wright et al., 1997).

Overall predation rates did not differ across activity patterns or socialstructure. Both solitary and large-group lemurs experienced predation bythe 2 raptors. Further, both nocturnal and diurnal lemurs suffered similarpredation rates in this study, and Eulemur fulvus rufus, which sometimes iscathemeral, did not escape predation.

Limited behavioral observations of the hunting strategies of the rap-tors in this study indicate that both predators hunt primarily at dawn andin the late afternoon, with most prey deliveries to the nest just after sunriseand just before sunset (Karpanty, 2003). Both birds are capable of removingnocturnal species from tree nests or cavities as evidenced by the large num-bers of Microcebus and Cheirogaleus in the birds’ diets. Further, the raptorsmay exploit early morning or late afternoon movements by both diurnal andnocturnal species to and from their sleeping sites. My team and I observed1 unsuccessful hunting attempt by 2 fledgling Accipiter henstii chicks on anadult Avahi laniger. The predation attempt took place near dusk and wefirst became aware of the event by the Avahi jumping between tree trunksat 2 m above the ground, <10 m from us. Following 5 m behind the Avahi

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Table III. Potential predator-specific and predator nonspecific antipredation tacticsof primates

Predator-specific and non-specific tactics to avoid predation

1) A distinct aerial predator mobbing and alarm call. Immediately after the alarm,members drop low in the canopy

2) A distinct terrestrial predator mobbing and alarm call. Alarm call initiates a responseof downward vigilance and flight by group members

3) Daytime resting sites are lower in the canopy (avoid raptors) than nighttime sleepingsites (avoid nocturnal carnivores)

4) Small sleeping parties to prevent detection at night by vision and olfaction (avoidterrestrial carnivores)

5) Large group size. More eyes and ears to detect predators more efficiently and thedilution effect, which reduces an individual’s chances of being targeted in an attack

6) Small group size and slow, quiet group movement to decrease detection7) Polyspecific associations to increase group size8) Sentinels in feeding trees to prevent surprise attack by a predator9) Travel progression places subordinate adults in most dangerous positions—end of

line—and infants and juveniles in central, safe position10) Multiple sleep sites to prevent predators from predicting routes and sleep sites11) Cryptic coloration12) Protected sleep or nest sites—tree holes, leaf nests13) Extra adult males for predator defense and mobbing14) Generalized alarm calls

Note. Some behaviors taken from Wright (1998), Mittermeier et al. (1994), and Overdorff(1995).

was 1 fledgling goshawk silently flying and landing on small branches at thesame level as the Avahi. As the predator and prey moved toward us, a sec-ond fledgling goshawk surprised both us and the lemur by flying in from theside and grabbing the Avahi, which immediately screamed. As soon as thesecond goshawk grabbed the lemur, the first fledgling flew into the scream-ing melee. Several seconds later, we saw both birds struggling on the groundand the Avahi jumped away from them and immediately moved quicklyaway from the birds at our eye level. This appears to be an unsuccessfulattempt by 2 inexperienced fledglings to capture an Avahi as it left its sleepsite for evening foraging.

Predation Rates and Antipredator Tactics

A brief summary of antipredator tactics of the lemurs I observed asprey species is in Tables I and III. Again, I observed all ranges of antipreda-tor tactics in the lemur prey species, including 1) crypsis, small group sizes,and protected sleeping sites in the nocturnal species, 2) large group sizes,predator-specific vigilance and alarm tactics in some diurnal species, and3) small sleeping and traveling group sizes in some other diurnal species.

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One can make an interesting comparison across the diurnal lemurspecies that the raptors killed. Hapalemur griseus, a species that in a preda-tor encounter becomes cryptic and huddles into a sleeping, yet vigilant,group (Grassi, 2001), suffered a much higher predation rate than Eule-mur and Varecia species, which respond very specifically and aggressively inpredator encounters (Karpanty, 2003; Karpanty and Grella, 2001). ThoughEulemur and Varecia have larger body masses than Hapalemur, their densi-ties are also greater and both are within the size range of catchable prey forthese hawks. A similar comparison within the nocturnal lemur prey of mystudy is valuable as Avahi laniger suffered much higher rates of predationthan either Cheirogaleus or Microcebus despite the higher densities of thelatter species. Microcebus and Cheirogaleus are solitary foragers and sleepin protected tree cavities while Avahi appear to range as a family (2–3 indi-viduals) and sleep in dense huddles in open vegetation. The findings suggestthat for the Malagasy lemurs, day-active species best avoid diurnal raptorpredation by not being cryptic, but rather utilizing specific antipredator tac-tics and aggressively responding to predator encounters. On the contrary,nocturnal Malagasy lemurs best avoid predation by diurnal raptors by em-ploying crypsis and sleeping and foraging in a solitary fashion.

Diurnal raptor predation is only 1 risk to which lemurs might adjusttheir activity, antipredator, and social habits. Predation by nocturnal owls,snakes, and terrestrial carnivores would reinforce the need to live in smallgroups and be cryptic for nocturnal lemurs but would conflict with the di-urnal lemurs’ tactics to avoid diurnal raptor predation. To avoid these noc-turnal and crepuscular predators that rely heavily on smell and sound, itwould favor both diurnal and nocturnal lemurs to be cryptic and minimizegroup size. Overdorff et al. (2002) and Sauther (2002) illustrate predator-sensitive foraging in both rainforest (Eulemur rubriventer, Eulemur fulvusrufus, Propithecus edwardsi) and dry forest (Lemur catta) diurnal lemurs inthat smaller groups and sizes of lemurs will be more cryptic and forage inless risky locations than larger-group or larger-bodied lemurs of the sameand different species. The risk-averse foraging tactics may be adaptationsto avoid terrestrial predation, but may place the lemurs more at risk to di-urnal aerial predators. At least for diurnal lemurs, diurnal and nocturnalpredators may select for contrasting antipredator behaviors and producetrade-offs or suboptimal intermediate behaviors (Karpanty, 2003).

Diurnal Raptor Predation and Lemur Social Systems

Much debate has focused on the contrast of lemurs with anthropoidprimates in several features including female dominance, lack of sexual

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dimorphism regardless of mating system, high infant mortality, cathemer-ality, and seasonal breeding (Kappeler, 1997; Wright, 1999). Researchershave argued 2 different, though not mutually exclusive, hypotheses in theliterature: 1) the energy conservation hypothesis argues that the harsh andunpredictable climate of Madagascar has driven the evolution of most ofthese unique features (Wright, 1999) and 2) the evolutionary disequilib-rium hypothesis proposes that the evolution of diurnality and associatedbehavioral and social system features is very recent owing to the extinctionof at least 3 large raptor predators in the last 2 millennia (van Schaik andKappeler, 1996). In a review of the data relating to these hypotheses, Wright(1999) concludes that it is possible to explain the majority of unique lemurtraits that distinguish them from anthropoids as adaptations to conserveenergy and most efficiently use scarce resources. The results of my studyindicate that both nocturnal and diurnal lemurs of all body and group sizessuffer significant levels of predation by diurnal raptors. Predation pressurefor day-living animals may have been even higher before the megafauna ex-tinctions of the last millenium; however, my data do not suggest that a shiftto diurnality has resulted in markedly low predation pressures compared tonocturnal species. Particularly important are the analyses of the percentageof total mortality that one can attribute to diurnal raptor predation. Usingjust the minimum observed annual predation rates, diurnal raptor predationaccounts for a large proportion of overall mortality for both nocturnal anddiurnal lemurs of all age classes. It is difficult to assess predation rates oflemurs before the extinction of the 3 large eagle species unless one can findsubfossil nest remains, but my study weakens the argument that reduceddiurnal predation risk drives lemur radiation into the diurnal niche.

The lack of any simple relationship between diurnal raptor predationrates on lemur species with different group sizes, body sizes, or activity pat-terns makes it difficult to argue that any one of these features have evolvedas a mechanism to reduce predation pressure from diurnal raptors. Clearly,the ability of diurnal raptor predation to depress the intrinsic growth rate ofdiurnal lemur species and to lower the carrying capacity of the populationsof lemurs below what food limitation alone would predict does suggest thatpredation may select on critical life history parameters such as fecunditythat may influence lemur social system organization.

ACKNOWLEDGMENTS

The National Science Foundation Pre-doctoral Fellowship, UnitedStates Environmental Protection Agency STAR Fellowship (U-91554301),Wildlife Conservation Society Research Fellowship Program, National

258 Karpanty

Science Foundation Dissertation Improvement Grant (Proposal no.0200747), National Geographic Committee for Research and Exploration(Award no.7295-02), International Osprey Foundation, Margot MarshBiodiversity Foundation, Slobodkin Research Award, and Stony BrookUniversity Graduate School provided funding for the project. I thankDrs. Charles Janson, Patricia Wright, Lawrence Slobodkin, and RickWatson for their helpful comments on this manuscript and my entiredissertation. I thank the Association Nationale pour la Gestion desAires Protegees (ANGAP) and the Direction des Eaux et Forets (DEF)in Madagascar for permission to conduct this research in and aroundRanomafana National Park. The project was made possible with theassistance of the Institute for the Conservation of Tropical Environments(ICTE), the Malagasy Institute pour la Conservation des EnvironnementsTropicaux (MICET), and a team of dedicated guides and students:Loret Rasabo, Ramarojoana Perle Mamisoa, Sabo, RafanomezantsoaSedrarimanona Angelo, Rakotomalala Miandrisoa Jeannot, Randrianan-tenaina Johnny, Samuel, Randrianalenarina Mamy, Razafy MahatratraMaurice, Fahatelo Gista, Rakotonirina Telo, Randrianarivo Jeannot,Rakotonjatovo Justin, Filybert, Velotsara Jean Baptiste, DjaizandryBertrin, Sapna Sopori, Cassie Rogge, Anna Scheinzbach, and KimberlyMay. I thank two anonymous reviewers for their helpful comments on thismanuscript.

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