Deadwood Structural Properties May Influence Aye-Aye (Daubentonia madagascariensis) Extractive Foraging Behavior

Int J Primatol DOI 10.1007/s10764-016-9901-5

Deadwood Structural Properties May Influence Aye-Aye (Daubentonia madagascariensis) Extractive Foraging Behavior Katharine E. T. Thompson 1 & Richard J. Bankoff 1 & Edward E. Louis Jr. 2 & George H. Perry 1,3

Received: 30 June 2015 / Accepted: 19 February 2016 # Springer Science+Business Media New York 2016

Abstract The identification of critical, limited natural resources for different primate species is important for advancing our understanding of behavioral ecology and toward future conservation efforts. The aye-aye (Daubentonia madagascariensis) is an Endangered nocturnal lemur with adaptations for accessing structurally defended foods: continuously growing incisors; an elongated, flexible middle finger; and a specialized auditory system. In some seasons, ca. 90% of the aye-aye’s diet consists of two structurally defended resources: 1) the larvae of wood boring insects, extracted after the aye-aye gnaws through decomposing bark (deadwood), and 2) the seeds of Canarium trees. Aye-ayes have very large individual home ranges relative to most other lemurs, possibly owing to limited resource availability. Identification of limiting dietary factor(s) is critical for our understanding of aye-aye behavioral ecology and future conservation efforts. To investigate whether aye-ayes equally access all deadwood resources within their range, we surveyed two 100 × 100 m forest plots within the territories of two aye-ayes at Sangasanga, Kianjavato, Madagascar. Only 2 of 150 deadwood specimens within the plots (1.3%) appeared to have been accessed by the aye-ayes. To test whether any external or internal deadwood properties explain aye-aye foraging preferences we recorded species, height and diameter, and quantified the internal tree density using a 3D acoustic tomograph for each foraged and nonforaged

Electronic supplementary material The online version of this article (doi:10.1007/s10764-016-9901-5) contains supplementary material, which is available to authorized users.

* George H. Perry [email protected]

1

Department of Anthropology, Pennsylvania State University, University Park, PA 16802, USA

2

Center for Conservation and Research, Omaha’s Henry Doorly Zoo and Aquarium, Omaha, NE 68107, USA

3

Department of Biology, Pennsylvania State University, University Park, PA 16802, USA

K. E. T. Thompson et al.

deadwood resource within the plots, plus 13 specimens (5 foraged and 8 nonforaged) outside the plots. We did not detect any statistically significant preferences for species, diameter, or height. However, results from the acoustic analysis tentatively indicated that aye-ayes are more likely to forage in trees with greater internal (≥6 cm from the bark) densities. This interior region may function as a sounding board in the tap-foraging process to help aye-ayes accurately identify potential grub-containing cavities in the outer 1–4 cm of deadwood. Keywords Food resource limitation . Home range . Percussive foraging . Structurally defended food resources

Introduction Resource availability can be a major predictor of home range size for primate species (Di Bitetti 2001). For example, among lemurs in Madagascar, MilneEdwards’ sifakas (Propithecus edwardsi) have relatively larger home ranges in environmentally disturbed, patchy habitats than conspecifics in primary habitats (Gerber et al. 2012). Similarly, ring-tailed lemurs (Lemur catta) in Beza Mahafaly expand their home ranges during the dry season, likely to accommodate seasonal resource scarcity (Sussman 1991). In addition to expanded home range sizes, low forest productivity and patchy resource distribution may lead to decreased population densities (Hanya and Chapman 2012). Therefore, instances of solitary foraging behavior over large home ranges may be a consequence of food limitation. For example, it is hypothesized that the large, solitary home ranges of Bornean orangutans (Pongo pygmaeus) are an adaptive response to satisfying large nutrient requirements in the face of scarce food resources (Galdikas 1988; Mackinnon 1974; Singleton and van Schaik 2001). We here investigated potential food resource limitations in the wild habitat of a solitary foraging primate with extensive home range sizes, the aye-aye (Daubentonia madagascariensis). The aye-aye is an Endangered nocturnal lemur endemic to Madagascar with an adult body mass of ca. 2.5 kg and the largest relative brain size of any extant strepsirrhine primate (Kaufman et al. 2005; Schwitzer et al. 2013; Smith and Jungers 1997; Sterling 1993). Aye-ayes are able to access structurally defended foods with the aid of number of morphological adaptations, including continuously growing incisors; an elongated, thin, and highly flexible middle finger; and a specialized auditory system (Cartmill 1974; Simons 1995; Sterling 1993). The longest aye-aye behavioral study to date was conducted from 1989 to 1991 on Nosy Mangabe, an island to which nine aye-ayes were introduced in the 1960s (Sterling 1993, 1994). At this site, up to ca. 90% of the aye-aye's diet during hot-dry seasons consisted of two structurally defended resources: the larvae of wood-boring insects (extracted from decomposing bark and wood, i.e., deadwood) and the seeds of Canarium trees (Sterling 1993, 1994). On Nosy Mangabe and at other sites, smaller components of the aye-aye diet include tree

Aye-Aye Extractive Foraging on Deadwood

sap, nectar, fruits, and adult insects (Iwano and Iwakawa 1988; Pollock et al. 1985; Sterling 1993, 1994). Aye-ayes extract insect larvae from a variety of locations, including trunks and branches of dead trees, fallen deadwood, dead branches on living trees, bamboo, and —very rarely— living trees (Sefczek et al. 2012; Sterling 1994). The middle phalanx is used to tap on the bark of decaying trees to facilitate the detection of tree cavities that may contain grubs, in a process referred to as percussive foraging (Erickson 1994). Aye-ayes rely on the auditory interpretation of signals that are produced by rapidly tapping the outer surface of the tree to identify larval mines beneath the bark (Coleman and Ross 2004; Erickson 1994; Kaufman et al. 2005; Ramsier and Dominy 2012). The continuously growing incisors are then used to gouge holes in the trees, from which the insect larvae are skewered with the flexible middle digit (Erickson 1994; Sterling 1994). Although insect larvae are often envisioned as the most important aye-aye food, researchers have alternatively suggested the nutrient-rich seeds of Canarium as a primary dietary resource (Iwano and Iwakawa 1988; Sterling 1993). Important Canarium species for aye-ayes include C. boivinii and C. madagascariensis (Iwano and Iwakawa 1988; Pollock et al. 1985; Simons 1995; Sterling 1993, 1994). To access the nut-like seeds of Canarium, aye-ayes use their superior incisors to chew through the mid-endocarp and their inferior incisors to pierce the endocarp before scraping out the interior with their middle finger (Sterling 1994). The aye-aye has the largest geographical species distribution of any extant lemur, with populations observed in both the tropical rainforests along the east coast and the relatively dry forests of the west coast and northernmost regions of Madagascar (Sterling 2003). Aye-ayes also have among the largest individual home range (the core area of land within which an animal forages) sizes of any lemur: 120–215 ha for males and 30–40 ha for females on Nosy Mangabe (Sterling 1993). These home range sizes are extensive given that aye-ayes are solitary foragers with a ca. 2.5-kg body size (Smith and Jungers 1997; Sterling 1993). Although aye-ayes have smaller body sizes than orangutans, like orangutans they have relatively large, minimally overlapping (at least for aye-aye females) home ranges and solitary foraging behaviors that could reflect dependence on one or more limited food resources. Studying potential food resource limitation is important for our understanding of aye-aye behavioral ecology and for future conservation efforts. With deforestation and the further loss of deadwood resources or live Canarium trees (the densities of which may vary across habitats), aye-ayes may be forced to range farther to satisfy dietary needs to avoid local extirpation (Farris et al. 2011; Sefczek et al. 2012). In this study, we performed an initial investigation into potentially limiting factors of the aye-aye diet, focusing especially on deadwood. Specifically, to test whether deadwood in general is a limited resource we first assessed whether aye-ayes exploited all or a smaller portion of the available deadwood within their home ranges in order. Second, we investigated whether particular external or internal properties of deadwood or the proximity to living Canarium trees may affect aye-aye resource selection.

K. E. T. Thompson et al.

Methods Study Site We collected data from June to August 2013 in the Sangasanga forest near the village of Kianjavato. Kianjavato (Fig. 1a) is located in the Vatovavy–Fitovinany Region of the Fianarantsoa Province in southeastern Madagascar (latitude: –21.37 and longitude: 47.87) (Schwitzer et al. 2013). The elevation at Sangasanga ranges from 52 to 571 m (Manjaribe et al. 2013). At its lowest elevation the forest borders the village of Kianjavato and is thus frequently used by local people. This area is less densely forested than areas of higher elevation as it is intersected by informal pathways, bamboo-lined streams, and coffee plantations managed by Foibe Fihofanana momba ny Fambolena (FOFIFA; The Plantation Management Headquarters) (Schwitzer et al. 2013). Above this area (at higher elevation) there is a denser band of forest composed of a thick understory that experiences less human disturbance. Toward the area’s highest peaks the forest consists predominantly of the traveler’s palm, Ravenala madagascariensis. The Madagascar Biodiversity Partnership at the Kianjavato Ahmanson Field Station actively monitors and collects behavioral data on GPS- and radio-collared aye-ayes at Sangasanga. Our specific study plots (Fig. 1b) were located within the active home ranges of two collared adult aye-aye individuals (one adult male and one adult female; the female had a single offspring during the time of the study), in a zone of humid

a

Location of study in Madagascar

b

Spatial distribution of foraged and non-foraged deadwood trees Foraged within Plot 2 -21.372

Non-foraged within Plot 2 Foraged within Plot 1 Non-foraged within Plot 1 Foraged outside plots

Latitude

-21.373

Non-foraged outside plots

-21.374

-21.375 100

Kianjavato

50 -21.376

North 100

50

9 .8 6 47

68 .8 47

67 .8 47

66 .8 47

47

.8 6

5

meters

Longitude

Fig. 1 Study plots and site in Kianjavato, Madagascar (June–August 2013). (A) Location of Kianjavato, Madagascar. (B) Spatial distribution of aye-aye-foraged and nonforaged trees. GPS locations of all deadwood standing or fallen tree resources (including stumps and logs) that we analyzed in this study within the Sangasanga forest in Kianjavato. Red denotes the presence of feeding traces on a specimen, while blue indicates the tree was not foraged upon. Circles and triangles indicate specimens found with 100 × 100 m plots; squares indicate supplementary specimens from nearby the plots included to increase sample size (five additional foraged trees and eight nonforaged trees). For the figure, a small number of points that we recorded improperly on the GPS unit were positioned manually based on field notes; these data are used for visualization purposes only and do not affect any analyses. Plots were 0.1528 km apart at the midpoint, and points outside the plot were on average 0.0919 km from the midpoint of plot 2.

Aye-Aye Extractive Foraging on Deadwood

secondary lowland rainforest ca. 0.69 km from the village, the periphery of which is adjacent to the forest boundary. The collared aye-ayes range across all of the aforementioned forest regions (Manjaribe et al. 2013; Solofondranohatra 2014). The welldocumented ranging patterns and foraging habits of aye-ayes within this area, along with Sangasanga’s topographic, botanical, and level of anthropogenic disturbance variation made it an ideal site for this study. Inventory of Tree Distribution Our goal was to perform an initial test of potentially limiting food resources in the ayeaye home range, including of deadwood in general, particular external or internal properties of deadwood, and the proximity of deadwood to live Canarium trees. Densities of Canarium are largely unquantified in southeastern Madagascar rainforests, with the limited available data suggesting a patchy pattern of distribution (Farris et al. 2011; Sefczek et al. 2012). Therefore, we chose to survey two relatively large plots (100 × 100 m each) rather than a greater number of smaller plots or transects, hoping that the plots would each encompass multiple specimens of Canarium. We established one 100 × 100 m plot in the low-elevation, disturbed forest zone and a second 100 × 100 m plot in the medium to high-elevation, dense forest zone. We placed plots within areas of frequent use in the home ranges of the two radiocollared individuals, and far from any of the ranges’ boundaries. We recorded the diameter (specifically diameter at breast height [DBH]), height, vernacular name, and GPS location (using a Garmin GPSmap 62) of each deadwood resource and living Canarium tree specimen. We measured DBH using two observers of identical stature (160 cm with DBH measured at ca. 119 cm). At breast height, the researchers took measurements using a DBH forestry measuring tape (which displays both the circumference and diameter). In the event that deadwood resources were 15.6 m. In contrast, 18 of 153 nonforaged trees (11.8%) were taller than 15.6 m. Similarly, even though the DBH difference was not statistically significant, the mean diameter for foraged specimens (18.81 cm) was 29% smaller than that of nonforaged specimens (26.62 cm). There were also no observations of foraging on trees with

94

Diameter measured specifically at breast height (ca. 119 cm)

14

16

14

13

12

11

27

at 5 cm (measured at 80–120 cm)

at 6 cm (measured at 80–120 cm)

at 7 cm (measured at 80–120 cm)

at 8 cm (measured at 80–120 cm)

at 1 cm (one average value per deadwood specimen)

11

at 2 cm (measured at 80–120 cm)

at 3 cm (measured at 80–120 cm)

11

at 1 cm (measured at 80–120 cm)

at 4 cm (measured at 80–120 cm)

35

at 8 cm (all scan values)

43

at 5 cm (all scan values)

41

44

at 4 cm (all scan values)

38

41

at 3 cm (all scan values)

at 6 cm (all scan values)

27

at 2 cm (all scan values)

at 7 cm (all scan values)

27

at 1 cm (all scan values)

Velocity

153

150

Diameter (of all specimens)

153

27

168

184

204

188

188

144

112

112

624

708

764

788

812

672

480

480

94

150

7

4

1

2

2

2

2

3

2

2

2

3

3

3

3

5

4

4

7

7

4

20

40

40

40

40

64

44

44

36

60

60

60

60

100

80

80

7

7

7

N values tested

N trees

N trees

N values tested

Foraged trees

Nonforaged trees

Height

Variable

Table I Means and test parameters for foraged vs. nonforaged deadwood comparisons

1515.7 (±92.3) [±479.3]

835.5 (±25.8) [±333.7]

942.6 (±34.2) [±463]

1128.9 (±48.5) [±692.3]

1213.6 (±51) [±699]

1355.5 (±49.3) [±675.3]

1500.9 (±56.6) [±678.8]

1594 (±67.7) [±715.9]

1547.9 (±65.5) [±692.7]

1026.1 (±18.9) [±470]

1116 (±19.7) [±522.5]

1223.4 (±22.4) [±618.5]

1298 (±22.3) [±623.6]

1372 (±21.4) [±607.9]

1491.9 (±23.2) [±600.3]

1598.8 (±28.6) [±625.5]

1544.4 (±28.1) [±614.3]

26.7 (±1.9) [±17.6]

23 (±1.3) [±15.5]

5.5 (±0.6) [±7.3]

Nonforaged mean (±SE) [±SD]

1217.4 (±174.5) [±349]

1581.6 (±161.3) [±721]

1567.5 (±81.8) [±517.3]

1575.7 (±84.6) [±535]

1567.3 (±89.2) [±563.9]

1530.1 (±94.4) [±597]

1598.2 (±76.7) [±612.9]

1817.6 (±105.7) [±700.8]

1498.3 (±85.6) [±567.4]

1440.6 (±98.2) [±589.3]

1433.3 (±64.7) [±500.5]

1433.3 (±66.9) [±518.2]

1414.4 (±70.5) [±545.8]

1370.4 (±74.3) [±574.8]

1326.1 (±56.8) [±567.2]

1366.3 (±74.5) [±665.9]

1217.4 (±58.5) [±522.6]

18.9 (±4.1) [±4.1]

18.9 (±4.1) [±10.7]

6.9 (±2.2) [±5.8]

Foraged mean (±SE) [±SD]

7

135 70

–2.8 –0.1 3.0

73

1.1

134

20 5

–1.6

54

68

68

63

4.6

7.1

4.6

3.5

1.7

81

96 1.8

38 –0.5

71 4.2

4.7

72

104

1.6

119 –3

9

–5.1

1.8

8

–0.6 1.0

df

t

t-test results

0.2

1.86E–04

3.58E–09

2.03E–05

9.91E–04

0.11

0.31

0.08

0.65

0.0002

1.26E–05

0.004

0.12

0.99

0.01

0.004

1.65E–06

0.11

0.36

0.57

P

350.5

–809.8

405.6

447.2

252.4

213.2

1086.8

802.6

641.5

558.7

285.7 387.4

–91.1 –38.3 148.8

164.2 473.3

–26.1

617.1

452 –263.5

212.1

182.7

69.3

152.4 263.8

–30.9

–44.7

–74.5 –155.7

–287

–390.7

–198.7

14.1 17.9

–2.3

–455.4

4 –5.8

Upper

–6.7

Lower

95% CI of the differencea

K. E. T. Thompson et al.

11

11

14

16

14

13

12

at 1 cm (measured at 80–120 cm, one average value per deadwood specimen)

at 2 cm (measured at 80–120 cm, one average value per deadwood specimen)

at 3 cm (measured at 80–120 cm, one average value per deadwood specimen)

at 4 cm (measured at 80–120 cm, one average value per deadwood specimen)

at 5 cm (measured at 80–120 cm, one average value per deadwood specimen)

at 6 cm (measured at 80–120 cm, one average value per deadwood specimen)

at 7 cm (measured at 80–120 cm, one average value per deadwood specimen)

41

12

13

14

16

14

11

11

38

2

2

2

2

3

2

2

3

3

3

3

5

4

2

2

2

2

3

2

2

3

3

3

3

5

4

999.8 (±137.8) [±477.1]

1140.2 (±182.4) [±657.5]

1207 (±177.4) [±663.6]

1334.3 (±152.1) [±608.3]

1426.8 (±159.2) [±595.7]

1517.9 (±186.2) [±617.5]

1471.1 (±165) [±547.1]

1141.8 (±81.5) [±505.7]

1241.4 (±91.4) [±584.7]

1293.4 (±87.4) [±573]

1358.3 (±82.7) [±548.1]

1426 (±82.7) [±529.5]

1565.4 (±100.3) [±521.2]

Nonforaged mean (±SE) [±SD]

1567.5 (±31.8) [±45]

1575.7 (±56.7) [±80.1]

1567.3 (±103.8) [±146.8]

1530.1 (±175.8) [±248.6]

1582.9 (±194.2) [±336.3]

1808.4 (±101.2) [±143.2]

1506.8 (±93.6) [±132.3]

1433.3 (±135.5) [±234.7]

1433.3 (±146.2) [±253.2]

1414.4 (±164.3) [±284.5]

1370.4 (±189.2) [±327.7]

1326.1 (±167.1) [±373.6]

1366.3 (±239.5) [±478.9]

Foraged mean (±SE) [±SD]

10 13 12

–2.3 –4.1

3

6

9

1.8

0.9

0.7

1.4

9

4 4

–1.2 –1.9 0.2

4

0.7

3

5 7

–0.8 –0.6 0.1

df

t

t-test results

0.002

0.05

0.12

0.47

0.56

0.21

0.86

0.15

0.34

0.56

0.96

0.62

0.49

P

770.1 793.1 943 823.1

–189.2 –480.7 –551.5 –102.5

–876.1

–259.3

–23

467.8

–396.5

–848.1

162.8

–745.7

294.7

691.9 685.4

–667.7 –443.4 –678.6

353.4

512.7

Upper

–553

–911

Lower

95% CI of the differencea

a 95% CI = the confidence interval for the difference between the nonforaged means and foraged means, i.e., nonforaged – foraged, such that a negative value represents a greater foraged than nonforaged value.

41

38

at 6 cm (one average value per deadwood specimen)

43

at 7 cm (one average value per deadwood specimen)

44

44

at 4 cm (one average value per deadwood specimen)

at 5 cm (one average value per deadwood specimen)

43

41

41

27

27

at 2 cm (one average value per deadwood specimen)

N values tested

N trees

N trees

N values tested

Foraged trees

Nonforaged trees

at 3 cm (one average value per deadwood specimen)

Variable

Table I (continued)

Aye-Aye Extractive Foraging on Deadwood

K. E. T. Thompson et al. Foraging events on deadwood specimens by genera

Number of trees

25 20 Foraged Non-foraged

15 10 5 0

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28

Genera of deadwood

Genera of deadwood 1) Albizia 2) Ampalis 3) Anthocleista 4) Anthostema 5) Bathiorhamnus 6) Beilschmiedia 7) Bivinia 8) Bridelia 9) Campylospermum 10) Canarium 11) Chrysophyllum 12) Diospyros 13) Dracaena 14) Dypsis

15) Ficus 16) Hibisous 17) Lauraceae 18) Noronhia 19) Ocotea 20) Polyscias 21) Protium 22) Raloto 23) Ravenala 24) Sideroxylon 25) Sterculiaceae 26) Suregada 27) Tambourissa 28) Uapaca

Fig. 2 Aye-aye foraging events on deadwood specimens (by genera) in Kianjavato, Madagascar (June– August 2013). The vertical bars represent the number of deadwood resources identified to each observed tree genus; genera are indicated in the figure key. The numbers of nonforaged and foraged trees are represented by dark gray and light gray bars, respectively. Of the total foraged N = 7 and nonforaged N = 156 trees, 1 and 26 trees, respectively, could not be identified to genus. As a result, the sample size for this analysis is N = 6 foraged and N = 130 nonforaged trees.

diameters >35.6 cm, whereas 21 of 150 nonforaged trees (14%) had greater diameters than the largest foraged deadwood resource. Deadwood Internal Structural Properties The aforementioned results suggest that a different major aye-aye food resource, such as Canarium, may be the critical limiting resource in the aye-aye diet, or that the internal structural rather than external properties of deadwood might impact net nutritional gain from extractive foraging, or both. Unfortunately, as there were only two total foraged trees within our two 100 × 100 m plots and only five Canarium specimens (ESM Fig. S1), we were unable to statistically evaluate the Canarium proximity hypothesis in the present study. However, we were able to study variation in the internal properties of the deadwood resources by using the Fakopp Arborsonic 3D Acoustic Tomograph to estimate the velocity of sound traveling through the trees, a proxy for true density. The exterior bark surfaces of 2 of the 7 (29%) foraged and 109 of the 156 (70%) nonforaged deadwood tree resources in our sample were too decayed to hold the Fakopp Acoustic Tomograph sensors tightly in place, which is necessary to obtain accurate sound velocity data. For each of the remaining deadwood trees in the sample, we conducted up to five cross-sectional Acoustic Tomograph scans spaced at heights

Aye-aye foraging behavior vs. tree height

b

40

Aye-aye foraging behavior vs. tree DBH 100

Tree DBH (cm)

Tree height (m)

a 30 20 10 0

Non-foraged

Foraged

Deadwood tree resources

80 60 40 20 0

Non-foraged

Foraged

Deadwood tree resources

Fig. 3 Boxplots of diameter and tree height for aye-aye-foraged vs. nonforaged deadwood resources in Kianjavato, Madagascar (June–August 2013). (A) Tree heights of foraged vs. nonforaged deadwood specimens. (B) Similar comparison for specimen diameter. For this study, we measured diameter at ca. 119 cm on all standing deadwood specimens and at the next closest available location for truncated or fragmented deadwood segments.

Aye-Aye Extractive Foraging on Deadwood

ca. 5 cm apart and compiled velocity estimates at 1-cm intervals from the outer surface to the origin of the tree on four linear paths for each scan. Our final database for internal structure analysis included 224 scans from 47 nonforaged deadwood resources and 25 scans from 5 foraged resources (Fig. 4a).

a

Representative acoustic tomograph results (one scan per tree)

b

Foraged vs. non-foraged deadwood comparison of acoustic velocity, as a function of trunk depth

1800

Foraged trees

1600

Non-foraged trees

Velocity (cm/s)

1400 1200 1000 800

Foraged Non-foraged

600 400 200 0 1

2

3

4

5

6

7

8

9

10

Distance in from deadwood surface (cm)

c

Fakkop Arborsonic 3D Acoustic Tomograph

17 00

00 15

00 13

11 00

90 0

Velocity in cm/s

Fig. 4 Internal structural properties of aye-aye foraged vs. nonforaged deadwood resources in Kianjavato, Madagascar (June–August 2013). (A) 2D renderings (acoustic tomographs) of nonforaged and foraged deadwood tree resources, as generated by the Fakopp Arborsonic Program. The renderings depict predicted specimen density based on the velocity (centimeters per second) readings of the scan. A representative rendering from one scan per nonforaged deadwood resource is shown. (B) Sound velocity (in cm/s) based on four values per scan for each 1-cm interval from depths of 1–10 cm, with the number of intervals for each scan dependent on the radius of the tree at the scanning location. The velocity estimates at discrete tree depths are compared here between foraged (in red) vs. nonforaged (in blue) deadwood tree specimens. (C) The Fakopp Arborsonic hardware. Thin, elongated probes are hammered into a deadwood specimen around its circumference at equivalent spacing intervals (the version of the machine shown has 8 probes; the version used in our study had 10 probes). At the tip of each probe is a sensor that detects sound waves traveling across the interior of the specimen. The external, flat surface of a probe is tapped with a hammer a minimum of three times. Sound propagates across the tree from tapping one probe. The other nine sensors measure the velocity of the sound waves as they reach each sensor tip. This process is repeated for each of the different probes. These velocity data are communicated to a laptop computer running the Fakopp Arborsonic Program via BlueTooth wireless software or a wired connection.

K. E. T. Thompson et al.

We observed that for the first 1–3 cm from the outer tree surfaces, the estimated velocity values were slightly but statistically significantly lower for foraged deadwood resources compared to nonforaged specimens (Fig. 4b). However, from 6 cm inward toward the center of the tree this pattern is reversed, with statistically significantly higher velocities for the foraged deadwood specimens. For example, at 6 cm, 7 cm, and 8 cm from the outer surface of the tree the average velocity estimates for foraged trees were 17%, 28%, and 40% greater, respectively, than those for nonforaged specimens (Welch two-sample t-tests: df = 73, P < 0.01; df = 71, P < 0.0001, and df = 38, P < 0.001; Fig. 4b). Because we scanned foraged trees at the locations where traces occurred rather than strictly at DBH, the scanned heights were different for some of the foraged vs. nonforaged trees. However, when we restricted our comparison of foraged vs. nonforaged trees to only those scans that were taken from 80–120 cm heights (N = 3 foraged trees; N = 17 nonforaged trees), we observed similar results (ESM Fig. S2; ttests for 6 cm, 7 cm, and 8 cm from tree outer surface: df = 68, P < 0.0001; df = 54, P < 0.0001; df = 20, P < 0.0001 respectively). Thus, while nonforaged trees have similar or slightly higher velocities on the 1- to 3-cm intervals compared to foraged trees, the deadwood resources selected by aye-ayes for insect larvae foraging tend to have relatively more intact interior cores compared to the overall sample of available deadwood. The aforementioned t-tests of similarity for foraged vs. nonforaged velocity estimates likely violate the test’s assumption of independence among values. The density values from a given region of one deadwood specimen are likely related to the density values of different region within that same tree. Using a reduced dataset with a single mean velocity value for each cm interval per tree (see Methods) to repeat the analysis, only comparisons from the subset of 80–120 cm height scans remained statistically significant (all scans at 6 cm t-test: df = 4, P = 0.34; all scans at 7 cm t-test: df = 4, P = 0.15; subset of 80–120 cm scans at 6 cm t-test: df = 13, P = 0.05; subset of 80–120 cm scans at 7 cm t-test: df = 12, P < 0.01). Thus, our results should be considered tentative and preliminary until they can be replicated with a larger sample of foraged trees and, ideally, across additional aye-aye sites.

Discussion We here investigated the distribution and properties of deadwood, a potentially important resource for the aye-aye diet that —if limited in some manner— could explain why aye-ayes maintain such large individual home ranges. However, we found that only a small fraction of all deadwood resources within aye-aye home ranges are accessed for insect larvae. Thus, either deadwood itself is not a limiting resource for aye-ayes, or particular properties of the deadwood are important, such that only subsets of all deadwood resources are limiting dietary factors for aye-ayes. If deadwood alone was a limiting resource, then a higher rate of deadwood foraging would likely have been observed, as aye-ayes would be expected to attempt to maximize nutrient gain relative to travel distance by foraging at all available dead trees. Alternatively, aye-ayes might attempt to maximize nutrient gain by repeatedly foraging on a singular resource with high larval content, once such a resource is discovered. Although we did observe

Aye-Aye Extractive Foraging on Deadwood

indirect evidence of this behavior, with one heavily foraged specimen, this was a novel occurrence and does not change our overall conclusions. We next compared external variables of foraged vs. nonforaged deadwood resources, beginning with taxonomy. We did not observe a preference toward any given deadwood genus. In her previous work at Nosy Mangabe, Sterling observed aye-ayes foraging on at least 6 families of insect larvae inhabiting a minimum of 29 different tree genera (Sterling 1993, 1994). Our observation that aye-ayes do not exhibit a strong preference for specific deadwood taxa is consistent with Sterling’s original result. Besides taxonomy, we also considered tree height and diameter as potential limiting factors. Within our sample, height and diameter were not statistically significantly different between foraged and nonforaged deadwood trees. However, it appears that there could be some preference for foraging on trees with smaller diameters, which in turn could be related to the ability to grip the tree properly during percussive and extractive foraging. Still, aye-ayes foraged on only a fraction of all available shorter and smaller diameter deadwood resources, suggesting that deadwood tree height and diameter alone are not major limiting factors for the aye-aye diet. Finally, we compared the internal structures of foraged vs. nonforaged deadwood resources. We found that beyond 5 cm inward from the outer tree surface, foraged trees propagate sound more efficiently, i.e., have higher densities. Although this result is based on a limited number of observations and should thus be considered preliminary, it at least sparks an intriguing hypothesis related to aye-aye deadwood foraging ecology. Specifically, a previous study of aye-aye percussive foraging behavior reported that most larval excavation events occur within the first 1–3 cm from the outer surface of trees (Erickson 1994). Following our results, we tentatively hypothesize that the area behind the larval mines toward the tree center may have an important function in the aye-aye percussive foraging process. Specifically, this region could serve as a reflective Bsounding board,^ with denser wood in this region facilitating more precise acoustic reconstruction of the tree’s outer 1–3 cm, leading to more efficient foraging for insect larvae. Another factor that may contribute to deadwood resource selection could be independent of the tree structural properties required for aye-aye percussive foraging perceptual capability; namely, whether larval location varies by resource density. It may be that larvae preferentially occupy certain trees or particular regions therein based on deadwood interior or exterior structural properties. This will be an interesting topic for future research. As only 10% or less of Madagascar remains forested, species with large home ranges are increasingly vulnerable to extinction (Mittermeier et al. 2010). Given their large and minimally overlapping (for females) home ranges, it is likely that aye-aye population densities are naturally very low (Mittermeier et al. 2010; Sterling 1993). Such factors, in conjunction with the aye-aye’s slow life history and relatively low genetic diversity, may make aye-ayes especially vulnerable to extinction (Catlett et al. 2010; Perry et al. 2012a, b, 2013; Schwitzer et al. 2013). An understanding of the role that limited food resources play in determining home range size may be crucial to our efforts of preserving this unique and Endangered primate (Schwitzer et al. 2013). Home range sizes and minimum conservation areas needed to maintain healthy populations of aye-ayes may vary as functions of the densities of deadwood, bamboo, Canarium, or other food items that comprise a smaller proportion of the aye-aye diet but may be seasonally or nutritionally critical, if those critical food resources are variable among

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different forest types within the species range, e.g., wet tropical rainforest vs. dry deciduous forest. Therefore, in addition to larger sample sizes of foraged trees, expanded analyses of Canarium resource locations, and the inclusion of other dietary resources and potential larval foraging from bamboo, future studies should include deadwood specimens measured at different times of the year, as rainfall, humidity, and temperature may all alter the decay process. Future studies could also investigate the relationship between deadwood density and the abundance of wood-boring insect larvae. As insect and tree species may also vary from region to region, this study should also be conducted in several different known aye-aye habitats to provide a more comprehensive view of the foraging preferences of this Endangered species. Acknowledgments We thank the Government of Madagascar for the permission to conduct research and the Madagascar Biodiversity Project (MBP) and its staff at the Kianjavato Ahmanson Field Station for facilitating this study, especially Razafindrahasy Alexander Théofrico (Frico), Kotozafy Gilbert André (Abanky), Randriambololona Stéphan Justin (Tofa), Fanoharanomenjanahary Hubert El-Phanger (Dadah), and Razafindrazefa Elysé Fortinand (Dagah). We also thank John Wickes, Peter Divos, and Akos Smuck of Fakopp Enterprise for their help and expertise regarding the ArborSonic 3D Acoustic Tomograph machinery and analysis program; James S. Solofondranohatra of the University of Antananarivo for his insight into ayeaye behavior and assistance in the field; and Zach Farris and Tim Sefzeck for contributing their compiled databases on the vernacular to scientific name translations for Malagasy tree species. We thank Steig Johnson and Nate Dominy for comments and discussion that helped shape this study; Logan Kistler, Martin Welker, Jeoren Smaers, Andrew Zamora, Rosemary Miller, and Annie Lin for insights or assistance with data analysis; Tim Ryan, Logan Kistler, Becki Coleman, and Stephen Johnson for comments on an earlier draft of this manuscript; and the constructive comments from two anonymous reviewers, the associate editor, and the editor of the journal that helped us to improve the paper. Funding was provided by the American Society of Primatologists, the Pennsylvania State University College of the Liberal Arts, The Pennsylvania State University Huck Institutes of the Life Sciences, and the benefactors of Pennsylvania State University Schreyer Honors College.

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