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Why all those spines?: Anachronistic defences in the Didiereoideae against now extinct lemurs

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Plants evolve physical defences, such as spines, against browsing herbivores. However, in some cases, these defences may be anachronistic because the principal consumers of protected parts of the plant are extinct. In such cases, there may be few extant species consuming heavily defended resources. Here we examine the spiny defences of Madagascar's endemic Didiereoideae, and ask whether they may be anachronistic. To accomplish this aim, we reviewed the literature to determine which species consume these plants today, and then used stable isotope biogeochemistry to determine who may have exploited Didiereoideae in the recent past. There are four major groups of browsers that are now extinct in Madagascar: giant lemurs, elephant birds (Aepyornis and Mullerornis: Aepyornithidae), pygmy hippopotamuses (Hippopotamus) and giant tortoises (Aldabrachelys: Testudinidae). Each group was evaluated for isotopic evidence of didiereoid plant consumption. Given the structure of members of this plant clade (especially Alluaudia), we predicted that lemurs would be their most important consumers. Three extant lemur species consume Didiereoideae. Several of the extinct lemurs, particularly Hadropithecus stenognathus, may have relied heavily on these spiny plants. None of the non-lemur megafaunal browsers (elephant birds, hippopotamuses and giant tortoises) were important consumers of Didiereoideae.
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1Volume 109 | Number 1/2
January/February 2013
South African Journal of Science
http://www.sajs.co.za
Research Article Didiereoideae consumption by now extinct lemurs
Page 1 of 7
Why all those spines? Anachronistic defences in
the Didiereoideae against now extinct lemurs
Plants evolve physical defences, such as spines, against browsing herbivores. However, in some cases, these
defences may be anachronistic because the principal consumers of protected parts of the plant are extinct.
In such cases, there may be few extant species consuming heavily defended resources. Here we examine
the spiny defences of Madagascar’s endemic Didiereoideae, and ask whether they may be anachronistic.
To accomplish this aim, we reviewed the literature to determine which species consume these plants today,
and then used stable isotope biogeochemistry to determine who may have exploited Didiereoideae in the
recent past. There are four major groups of browsers that are now extinct in Madagascar: giant lemurs,
elephant birds (Aepyornis and Mullerornis: Aepyornithidae), pygmy hippopotamuses (Hippopotamus) and
giant tortoises (Aldabrachelys: Testudinidae). Each group was evaluated for isotopic evidence of didiereoid
plant consumption. Given the structure of members of this plant clade (especially Alluaudia), we predicted
that lemurs would be their most important consumers. Three extant lemur species consume Didiereoideae.
Several of the extinct lemurs, particularly Hadropithecus stenognathus, may have relied heavily on these
spiny plants. None of the non-lemur megafaunal browsers (elephant birds, hippopotamuses and giant
tortoises) were important consumers of Didiereoideae.
Motivation
Madagascar is renowned for its wealth of endemic flora and fauna. In particular, the arid south and southwest
is famous for its ‘spiny forests’ full of spiny bushes and trees belonging to the Apocynaceae (e.g. Pachypodium
lamerei), Euphorbiaceae (e.g. Euphorbia stenoclada), Fabaceae (e.g. Acacia bellula), Salvadoraceae (e.g. Azima
tetracantha) and Didiereoideae,1 an endemic subfamily of the Didiereaceae.2,3 Indeed, species from the latter
subfamily are limited almost entirely to the Spiny Thicket and Succulent Woodland ecoregions in southern and
southwestern Madagascar, which are characterised by hot temperatures and brief rainy seasons.4
The 12 species of the Didiereoideae belong to four genera: Alluaudia, Alluaudiopsis, Decarya and Didierea. All
members of this subfamily possess sharp, thick spines along their axes which protect their leaves5,6; however,
none of the closely related Didiereaceae from mainland Africa (Calyptrotheca, Ceraria, Portulacaria) possesses
spines.1 Experimental research on plant taxa in mainland Africa has demonstrated that the spines reduce foliage
loss to browsing ungulates.7,8 This protection suggests that the common ancestor of the Madagascan forms
was subjected to intense leaf predation shortly after its arrival. Arakaki and colleagues9 reported a diversification
estimate for Madagascan Didiereoideae of 17 million years ago (mya) based on molecular data. These data imply
an earlier date for the dispersal of the basal didiereoid from continental Africa to Madagascar. According to these
authors, Alluaudia itself began diversifying only 11 mya. Ocampo and Columbus10 suppor t a slightly more recent
radiation of Madagascan didiereoids, with the divergence of the Madagascan lineage from the closest continental
African relative at around 15 mya.
Spines on these tall, emergent plants may be defences against leaf predation by climbing animals such as
lemurs.6 Spines of most Alluaudia spp., for example, are found at heights above the ground (5–9 m) that were
likely prohibitive for terrestrial browsers such as tortoises, hippopotamuses and elephant birds. Whereas it is
conceivable that these taxa browsed juvenile forms or the lower portions of adult plants, widescale herbivory by
tortoises or hippopotamuses seems unlikely. Furthermore, although the ‘wiry’ qualities of Alluaudia humbertii and
Decarya madagascariensis may have provided some defence against elephant bird herbivory,11 their spines are
relatively ineffective against birds and, presumably, other animals with hard beaks that protect their mouths, such
as tortoises.12 Another reason to suspect that the spines on the Didiereoideae evolved to protect leaves against
climbing animals and not against other major groups of herbivores is the timing of arrival of major herbivore groups
to Madagascar. Both hippopotamuses and testudines arrived relatively recently13 – likely after the appearance of
spines and diversification of Madagascan didiereoids. Only lemurs and elephant birds would have been present
when the ancestral didiereoid arrived. If Bond and Silander11 are correct in characterising elephant birds as poorly
suited to exploit the leaves of the Didiereoideae, then lemurs become the most plausible contenders. Additionally,
if few extant lemurs exploit these plants, then the giant extinct lemurs may be implicated.
Ideally, testing the hypothesis that spines served to defend the leaves of the Didiereoideae against giant lemurs
requires more than compiling evidence that certain giant lemurs likely consumed these plants. We would like to
know the degree to which the spines acted as a deterrent to overconsumption of small and vulnerable young leaves
by giant lemurs. The latter question is challenging, at best, within the context of palaeobiology. Palaeontological
evidence is often indirect, and arguments may depend on unspoken assumptions. Thus, it is important to make
explicit the questions that can be addressed with the tools we have at our disposal. How, using those tools, can
plant anachronisms in Madagascar be discerned?
As evolutionary biologists we can ascertain, first, whether or not the Didiereoideae are native or endemic to
Madagascar (i.e. not recently introduced). Secondly, we can establish whether the presumed anachronistic spines
are derived. Thirdly, we can determine whether or not the hypothesised consumers (lemurs) were present when
AUTHORS:
Brooke E. Crowley1,2
Laurie R. Godfrey3
AFFILIATIONS:
1Department of Geology,
University of Cincinnati,
Cincinnati, OH, USA
2Department of Anthropology,
University of Cincinnati,
Cincinnati, OH, USA
3Department of Anthropology,
University of Massachusetts,
Amherst, MA, USA
CORRESPONDENCE TO:
Brooke Crowley
EMAIL:
brooke.crowley@uc.edu
POSTAL ADDRESS:
Department of Geology,
University of Cincinnati,
500 Geology Physics Building,
345 Clifton Court, Cincinnati, OH
45221, USA
DATES:
Received: 24 June 2012
Revised: 16 Aug. 2012
Accepted: 25 Aug. 2012
KEYWORDS:
Madagascar; lemur;
crassulacean acid metabolism;
δ13C; δ15N
HOW TO CITE:
Crowley BE, Godfrey LR. Why
all those spines? Anachronistic
defences in the Didiereoideae
against now extinct lemurs. S
Afr J Sci. 2013;109(1/2), Art.
#1346, 7 pages. http://dx.doi.
org/10.1590/sajs.2013/1346
© 2013. The Authors.
Published under a Creative
Commons Attribution Licence.
2Volume 109 | Number 1/2
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Research Article Didiereoideae consumption by now extinct lemurs
Page 2 of 7
these features likely originated. We can probe whether spines can be
understood outside the context of the proposed plant–animal interactions
and we can examine palaeodistribution data to test the plausibility of the
proposed interactions. Finally, we can explore whether spines serve any
apparent purpose today, or were likely used in the past in a manner that
no longer holds.
Our inferences in this paper are based explicitly on the combination of
a literature review and stable isotope biogeochemistry that addresses
these issues. We ask the following specific questions:
1. To what extent do modern lemurs feed in southern and southwestern
Madagascar on C3, C4 and crassulacean acid metabolism (CAM)-
based plants? How much do they feed on Didiereoideae?
2. Can we distinguish Didiereoideae from other CAM plants using
stable isotopes? Such discrimination is needed if we are to
use stable isotope data to successfully test the hypothesis that
Didiereoideae spines are anachronistic.
3. To what extent were lemurs feeding on CAM plants in the past?
4. Do stable isotopes suggest that any of the extinct non-lemur
herbivores were major consumers of Didiereoideae?
Background on stable isotope biogeochemistry
Stable isotopes can be used to reconstruct the diets of living and extinct
animals. The relative proportion of heavy and light isotopes (e.g. 13C/12C
or 15N/14N) in a substance is reported using a standardised ’δ’ notation
(e.g. δ13C, δ15N). These values are measured as parts per thousand (‰)
higher or lower than an international standard.
Carbon isotope (δ13C) values can, in some cases, be used to
distinguish plants that fix carbon via C3 photosynthesis (most trees
and herbs), C4 photosynthesis (many grasses) and CAM (stem and
leaf succulents).14 Many succulents have the ability to switch between
full CAM photosynthesis and C3 photosynthesis, which can result in
highly variable δ13C values.14 However, in arid environments, such as
those in southwestern Madagascar, carbon fixation is strongly biased
towards CAM photosynthesis.15 Nitrogen isotope (δ15N) values in
plants are affected by environmental conditions, plant physiology,
nutrient availability and microbial associations.14,16 Nitrogen isotope
values clearly distinguish plants growing in different habitats. Plants
from moist, cool localities have lower δ15N values than plants from dry,
warm localities.16,17 Coastal localities can evince exceptionally high δ15N
values.18 Most plants obtain their nitrogen directly from soil nitrate and
ammonium, and their δ15N values are greater than that of air (~0‰).
Plants with symbiotic nitrogen-fixing bacteria can have δ15N values close
to 0‰.16,18 No consistent differences in δ15N have been reported among
the three photosynthetic groups, but CAM plants can have significantly
higher δ15N values than sympatric C3 or C4 plants.18,19 Differences in
plant physiology or differential use of water sources may result in δ15N
differences between the Didiereoideae and non-spiny leaf succulents.20
Isotopic patterns in plants are reflected in animal consumers with some
isotopic enrichment. Carbon and nitrogen isotope values in herbivore
bone collagen tend to be, respectively, ca. 5‰ and 3‰ higher than
those in plants.21 Once we have accounted for isotopic enrichment
between collagen and diet, we may be able to use carbon isotope values
in consumer tissues to estimate the relative ingestion of C3, C4 and CAM
plants. As with plants, nitrogen isotope values in animals can be used
to distinguish habitat types.17,22 Within a particular habitat, δ15N values
increase with increasing consumption of animal matter.21,22 However,
because most of the lemur species included in our analyses are, or
were, predominantly herbivorous, we do not believe our results are
confounded by the effects of faunivory on nitrogen isotope values.23-32
The two possible exceptions are Archaeolemur majori (whose diet
likely included some animal matter) and Daubentonia robusta. Extant D.
madagascariensis consumes more animal matter than any of the other
lemurs included in our study33 and it is likely that the extinct D. robusta,
which lived in the southwest, would have had a similar diet.34 If this
species consumed insects that in turn fed on CAM resources, elevated
δ15N isotope values might falsely suggest CAM consumption, when in
fact they really reflect trophic omnivory. We therefore omitted D. robusta
from our analyses.
Methods
To explore the extent to which modern lemurs feed on C3, C4 or
CAM plants, we conducted a thorough review of the literature. We
examined 74 manuscripts, books and book chapters that discuss the
feeding behaviour of living lemurs in southwestern Madagascar. All
sources included in our survey are listed in Supplementary table 1 (see
supplementary material online), and all documented observations of
feeding on CAM are provided in Supplementary table 2. We used the
website www.tropicos.org and Petitjean and colleagues35 to identify
scientific names and families for recorded food species. Succulence was
assessed using species-specific isotopic or anatomical data whenever
possible.36-41 If no data were available for particular species, we used
published information at the generic or familial level.42,43
To determine if the spiny Didiereoideae can be isotopically distinguished
from other plants, we compared δ13C and δ15N values from leaves
that we collected in the spiny forest at Beza Mahafaly Special Reserve
(BMSR) in south-central Madagascar (taxa provided in Table 1). We
included previously published isotope values for C3 and CAM plants17
and new isotope values for C4 plants. All plant specimens were collected
between 2006 and 2009. We sampled Alluaudia procera, which is the
only member of the Didiereoidea that occurs in abundance at the reserve.
Alluaudia is both the most speciose and the most widespread didiereoid
genus. Additionally, although carbon isotope values have been measured
for a number of spiny CAM species,10,37,41 nitrogen isotope data have
been published only for Alluaudia procera.17 We used an analysis of
variance (ANOVA) with Tukey’s tests of honestly significant differences
(HSD) and Student’s t-tests to test the significance of isotopic differences
between C3, C4 and CAM plants, and between Alluaudia and other CAM
plants. All statistical tests were performed using JMP (version 7.0).
Significance was set at α = 0.05. We assessed the assumptions of
normality and homoscedasticity of variance for all analyses. We tested
for homogeneity of variances using Levene tests.
To address the extent to which lemurs and non-primate herbivores fed on
CAM plants in the past, we used δ13C and δ15N values from bone collagen.
We analysed 72 bones of extant and extinct lemurs as well as extinct giant
tortoises and pygmy hippopotamuses from subfossil sites in the Spiny
Thicket and Succulent Woodland ecoregions (coastal and inland). Collagen
was prepared following previously published methods.44 Samples were
analysed at the Stable Isotope Laboratory at the University of California,
Santa Cruz. We verified collagen preservation using collagen yield, atomic
C:N ratios, and carbon and nitrogen isotope values. We added these data
to our existing database of previously published isotope data.45-48 Raw
isotope data for all individuals are presented in Supplementary table 3.
Carbon isotope values for subfossil individuals were corrected to account
for δ13C shifts in atmospheric CO2 following the industrial revolution (The
Suess Effect).45 Carbon isotope values for individuals younger than 150
years BP were corrected using an age-dependent correction of -0.004‰
per year between 1860 and 1965 AD and -0.02‰ per year between 1965
and 2005 (modern). All individuals older than 150 years were corrected by
-1.2‰. In order to avoid sampling bias, we used nonparametric Wilcoxon
signed ranks tests to compare mean δ13C values for subfossil extant and
extinct lemur species.
We calculated mean %CAM consumption using mixing models in
ISSOERROR version 1.04.49 We used mean δ13C values for C3 and CAM
plants from the spiny forest at BMSR as end members, correcting for
the +5‰ difference in δ13C values between collagen and plants. We
did not include C4 plants in these models because they are relatively rare
in southern Madagascar and no modern lemurs are known to consume
them. If δ15N values do, indeed, differentiate spiny Didiereoideae from
sympatric non-spiny CAM plants, then we may be able to use mean
δ15N values in addition to δ13C values to distinguish consumption of
Didiereoideae. We corrected plant values by +3‰ to account for
the difference in δ15N values between collagen and plants.21 We also
3Volume 109 | Number 1/2
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Research Article Didiereoideae consumption by now extinct lemurs
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corrected for the small 1.6‰ difference in δ15N between coastal and
inland animals (Supplementary table 4).
Results
What do modern lemurs eat in southwestern Madagascar?
Six lemur species have been observed to feed on endemic and introduced
CAM plants in southern and southwestern Madagascar: Eulemur rufifrons
(the red-fronted brown lemur), Lemur catta (the ring-tailed lemur), Lepilemur
leucopus (the white-footed sportive lemur), L. petteri (Jean-Jaques Petter’s
sportive lemur), Microcebus griseorufus (the reddish-grey mouse lemur)
and Propithecus verreauxi (Verreaux’s sifaka) (Supplementary table 2).
Historically, behavioural studies have tended to concentrate on individuals
living in gallery forest habitats. However, recent research has documented
significant CAM consumption by individuals living in dry or spiny forest at
Berenty, Beza Mahafaly, Cap Sainte Marie and Tsimanampetsotsa.24,28,32,50
Loudon et al.50 and Gould et al.32 estimate 15% CAM consumption for
L. catta living in spiny forest at Tsimanampetsotsa and Berenty Reserve,
respectively. Consumption of CAM resources by L. catta at Cap Sainte
Marie can be >75% during some months.28 Although the vast majority
of the CAM plants consumed by members of the latter population are
introduced, including Opuntia (prickly pears), native CAM species such as
Aloe and Kalanchoe can each comprise >10% of the diet of L. catta during
some months of the year.
Only Lemur catta, Lepilemur leucopus and Propithecus verreauxi have
been observed to consume Didiereoideae (Table 2). All but one of these
published observations have involved Alluaudia spp. The exception was
Didierea trolli which is consumed by L. catta.27 Some modern lemurs
have been reported to feed heavily on Alluaudia. For example, during
certain months at Cap Sainte Marie nearly 14% of the diet of L. catta is
Alluaudia procera.28 Lepilemur leucopus was observed to rely entirely on
leaves and flowers of Alluaudia spp. during the dry season at Berenty.24,25
Table 2: Observations of lemurs feeding on Didiereoideae taxa in southwestern Madagascar
Lemur species Genus and species Parts consumed Locality Source on feeding Source on CAM
Lemur catta Alluaudia dumosa Leaves, fruit, flowers Berenty Gallery Forest, Cap
Sainte Marie 28, 52 37, 41
Lemur catta Alluaudia humbertii Mature leaves Berenty Gallery Forest 27, 52 10, 37, 41
Lemur catta Alluaudia procera Young leaves, mature
leaves, flowers Berenty Gallery Forest
and Spiny Forest; Cap
Sainte Marie
27, 28, 32, 52, 53 17, 37, 41
Lemur catta Didierea trollii Young leaves, flowers Berenty Gallery Forest 27, 52 10, 37, 41
Lepilemur leucopus Alluaudia ascendens Buds, leaves, flowers Berenty Dry Forest 2, 24, 25 10, 37, 41
Lepilemur leucopus Alluaudia procera Buds, leaves, flowers Berenty Dry Forest 2, 24, 25 17, 37, 41
Propithecus verreauxi Alluaudia ascendens Flowers Hazofotsy 54 10, 37, 41
Propithecus verreauxi Alluaudia procera Flowers Hazofotsy 54 17, 37, 41
Table 1: Plant taxa included in this study
Family Genus Species NPhotosynthetic
pathway
Spiny?
Apocynaceae Landolphia sp. 2 C3No
Apocynaceae Pentopetia androsaemifolia 1 C3No
Burseraceae Commiphora sp. 11 C3No
Celastraceae Reissantia angustipetala 1 C3No
Combretaceae Grewia grevei 5 C3No
Combretaceae Terminalia spp. 9 C3No
Euphorbiaceae Croton geayi 4 C3No
Meliaceae Cedrelopsis grevei 5 C3No
Phyllanthaceae Phyllanthus decaryanus 5 C3No
Rhamnaceae Gouania glandulosa 2 C3No
Salvadoraceae Salvadora angustifolia 3 C3No
Mimosaceae Dichrostachys humbertii 6 C3Yes
Asclepiadaceae Cynanchum mahafalense 1 CAM No
Cucurbitaceae Seyrigia sp. 2 CAM No
Cucurbitaceae Xerosicyos perrieri 9 CAM No
Euphorbiaceae Euphorbia tirucalli 21 CAM No
Didieraceae Alluaudia procera 17 CAM Yes
Cyperaceae Cyperus sp. 1 C4No
Poaceae Panicum spp. 7 C4No
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Research Article Didiereoideae consumption by now extinct lemurs
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On the other hand, Lepilemur living in the gallery forest at BMSR does
not consume any Didiereoideae but relies to some degree on non-spiny
Euphorbia tirucalli.51 These differences underscore the potential site
specificity of variation in feeding observations.
Do Alluaudia differ isotopically from sympatric CAM plants?
Carbon isotope values differ significantly for CAM, C3 and C4 plants from
BMSR (Figure 1; F2,111=714.9, p<0.0001). Post-hoc HSD tests indicate
that all three are distinct. Carbon isotopes cannot distinguish Alluaudia
procera from sympatric CAM plants (p>0.05). However, nitrogen isotope
values do clearly separate these two plant groups (t=5.38, df=40,
p<0.0001). Alluaudia has distinctly elevated δ15N values (Figure 1).
Figure 1: Box-and-whisker plots of (a) δ13C values for C3, CAM and C4
plants and (b) δ15N values for spiny Didiereoideae and non-
spiny CAM from the spiny forest at Beza Mahafaly Special
Reserve, Madagascar.
To what extent were lemurs feeding on CAM plants in the past?
We found no differences in mean δ13C values between subfossil
extant and extinct lemur species (Wilcoxon signed ranks, S =17, z
=0, p=1.0), although our subfossil sample showed greater variance.
Mixing models based on δ13C values suggest that subfossil individuals
belonging to each of the three extant species consumed mostly C3
resources (Table 3). CAM consumption was negligible for subfossil
Lepilemur, but modest CAM consumption is indicated for subfossil
Lemur catta (8.5%) and Propithecus verreauxi (5%). These values
are slightly higher than CAM consumption estimates for P. verreauxi
and L. catta living today in gallery forest,27 but they are not as high as
values for L. catta in dry forest at coastal localities in the south.28,32,50
Importantly, substantial CAM consumption by modern lemurs, even at
coastal localities, is a seasonal phenomenon.28 Because isotope values
in bone collagen integrate several years of dietary input,21 modest %CAM
estimates for subfossil individuals may reflect seasonal fluxes in CAM
consumption. Among the extinct taxa living in the south and southwest,
Megaladapis edwardsi, M. madagascariensis, Pachylemur insignis and
Palaeopropithecus ingens show no evidence of CAM consumption
(Table 3; Supplementary table 3). In contrast, our data indicate modest
CAM consumption by Archaeolemur majori (5%) and significant CAM
consumption by Mesopropithecus globiceps (25%) and Hadropithecus
stenognathus (92%). In summary, while it is evident that not all southern
lemurs consume CAM plants today, and it is unlikely that all consumed
them in the past, some CAM consumption can be documented in a wide
variety of lemur species.
Table 3: Descriptive statistics including number of specimens analysed,
and mean δ13C and δ15N values ±1σ for each species
Carbon Nitrogen
Genus and
species NMean
δ13C ±1σ a%CAMbNMean
δ15N±1σd
Lemur catta 25 -20.5±1.4 8.5 25 10.6±2.0
Lepilemur
leucopus 8 -21.9±1.7 0 8 9.5±0.7
Propithecus
verreauxi 29 -20.9±1.0 5 29 9.6±2.1
Archaeolemur
majori 23 -20.9±1.4 5 19 11.3±1.9
Hadropithecus
stenognathus 9-10.8±1.5 92 7 13.8±3.2
Megaladapis
edwardsi 8 -22.0±0.5 0 5 11.5±2.6
Megaladapis
madagascariensis 14 -21.7±1.2 0 12 11.3±1.4
Mesopropithecus
globiceps 4-18.6±2.9 25 3 13.1±1.8
Pachylemur
insignis 18 -22.2±1.4 0 16 11.4±1.9
Palaeopropithecus
ingens 30 -21.7±0.7 0 27 13.5±2.0
Aepyornis spp. 60 -24.4±0.9c 11c
Aldabrachelys
spp. 19 -20.6±3.3 8 16 10.3±1.4
Hippopotamus
lemerlei 14 -21.1±2.0 3 14 9.0±1.8
%CAM values were calculated using ISSOERROR version 1.04.49
aCollagen δ13C values have been corrected to account for δ13C shifts in atmospheric CO2
following the industrial revolution.
bMean %CAM consumption was estimated using δ13C values from C3 and CAM plants from
the spiny forest at Beza Mahafaly Special Reserve (-21.5‰ and -9.9‰, respectively). Plant
δ13C values were corrected by +5‰ to account for the isotopic difference between collagen
and plants.21
cδ13C values and %CAM estimates are from the organic portion of eggshell.54 Carbon isotope
values were corrected for the isotopic difference between eggshell and plants.57 We corrected
carbon isotope data for eggshells to account for atmospheric changes in δ13C (-1.2‰).
dPlant δ15N values were corrected by +3‰ to account for the isotopic difference between
collagen and plants.21
Because isotope values in plants are reflected in their animal consumers,
we may be able to use differences in δ15N between Alluaudia and
sympatric CAM plants to identify lemurs that consumed Didiereoideae
in the past. Among those species identified as CAM consumers by
their δ13C values, differing δ15N values suggest varying degrees of
Alluaudia consumption (Figure 2). Nitrogen isotope values indicate that
Didiereoideae were not a dominant element of L. catta or P. verreauxi
diets. Among the extinct taxa, A. majori may have consumed small
amounts of Didiereoideae. However, M. globiceps may have consumed
substantial amounts of Didiereoideae, and H. stenognathus, which is
characterised by exceptionally high δ13C and δ15N values, may have
relied heavily on Didiereoideae (Figure 2).
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Research Article Didiereoideae consumption by now extinct lemurs
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Figure 2: Mean δ13C and δ15N values ±1σ for lemur species that likely
consumed varying degrees of non-spiny and spiny CAM plants.
Bubbles represent mean carbon and nitrogen isotope values
±1σ for C3, C4, non-spiny CAM plants and Alluaudia procera.
Subfossil carbon isotope values for subfossils were corrected
for the post-industrial shift in atmospheric δ13C values.
Carbon and nitrogen isotope values in plants were corrected
by +3‰ and +5‰ to account for the isotopic difference
between collagen and plants. Finally, nitrogen isotope values in
plants were shifted +1.6‰ to account for the mean isotopic
difference between inland Beza Mahafaly Special Reserve and
coastal localities (Supplementary table 3) in Madagascar.
The living lemur most reliant on Didiereoideae is likely Lemur catta. This
species may have consumed more Didiereoideae in the past than it
currently does in moist gallery forests.23,45 Goodman and colleagues55
noted the distributional overlap of L. catta and the Didiereoideae. They
suggested that this lemur species may have evolved in dry forests and
subsequently moved into moister riparian forest, where didiereoid taxa
do not exist. In fact, even today, in some arid habitats where L. catta still
thrives and CAM resources abound (e.g. Tsimanampetsotsa, Cap Sainte
Marie), these lemurs consume substantial amounts of Didiereoideae and
other CAM plants.28,50 More research is needed to document the degree
to which L. catta exploits Didiereoideae as opposed to other CAM plants.
The fact that both Alluaudia and Hadropithecus have extreme δ13C and
δ15N values is striking. The geographic overlap of the Didiereoideae and
Hadropithecus stenognathus is also remarkable (Figure 3). With the
exception of Ampasambazimba in Central Madagascar, all subfossil
localities yielding Hadropithecus fall within the modern distributional
range of the Didiereoideae. Compellingly, δ13C values for the two H.
stenognathus individuals sampled from Ampasambazimba suggest
a pure C3-based, rather than a CAM-based, diet (δ13C <-22‰).
This geographic overlap combined with the match for both δ13C and
δ15N between Alluaudia and Hadropithecus, strongly suggests that
Didiereoideae was a staple in the diet of Hadropithecus in the Spiny
Thicket and Succulent Woodland ecoregions of Madagascar.
Our subfossil isotope data do not support the notion that Lepilemur
consumed large quantities of Alluaudia in the past. This finding might be
considered curious, because Lepilemur is the only living lemur that has
been reported to consume large quantities of Alluaudia today. The diet
of Lepilemur has been studied in detail only at two localities in southern
and southwestern Madagascar: the spiny forest at Berenty Private
Reserve where Alluaudia exists, and the gallery forest at BMSR, where
didiereoid taxa do not exist. Alluaudia spp. may comprise close to 100%
of this species’ diet at Berenty Private Reserve at least during the dry
season.2,24,25 Yet δ13C values for Lepilemur from multiple subfossil sites
in the southwest indicate negligible CAM consumption in the past (Table
3; Supplementary table 3).
Source: adapted from www.tropicos.org.
Figure 3: Map of Madagascar including localities where Hadropithecus
stenognathus remains have been found. The distribution of the
Didiereoideae is shaded in grey.
Because our subfossil Lepilemur specimens come from several,
geographically widespread, localities (two inland, one coastal), it is
unlikely that this result reflects sampling bias. Instead it would appear
that modern individuals might have recently shifted their diet at Berenty
to include a resource that was inconsistently exploited (if at all) in the
past. Recent transitions in diet or habitat may be widespread among
modern lemurs living in southwestern Madagascar.45 Isotope values
for subfossil Lepilemur do not differ significantly from those for extinct
Archaeolemur majori, Megaladapis edwardsi, M. madagascariensis,
Palaeopropithecus ingens or Pachylemur insignis. Four of these (all
except Archaeolemur) have a 0% CAM signal, as does subfossil
Lepilemur. Of these four, the two Megaladapis species have dental
topography much like Lepilemur,23 as well as relatively small infraorbital
foramina29 and dental microwear30,56 that suggest dominant foliage
consumption.
Did now extinct non-lemur herbivores consume Didiereoideae?
Estimated CAM consumption for extinct hippopotamuses, tortoises
and elephant birds is minor compared to that for Mesopropithecus and
Hadropithecus. Mixing models suggest that, on average, Hippopotamus
spp. and the giant tortoise Aldabrachelys spp. consumed only 3% and
8% CAM, respectively (Table 3). Clarke et al.57 used δ13C values in
Aepyornis eggshells to estimate that elephant birds consumed ca. 11%
CAM. Nitrogen isotope values are similar in subfossil Hippopotamus,
Aldabrachelys, Lemur catta and Propithecus verreauxi (Table 3;
Supplementary table 3), indicating nominal consumption of Didiereoidea
for these species. Nitrogen isotope values do not exist for Aepyornis.
However, their δ13C values suggest that elephant birds did not exploit
large amounts of Didiereoideae.
6Volume 109 | Number 1/2
January/February 2013
South African Journal of Science
http://www.sajs.co.za
Research Article Didiereoideae consumption by now extinct lemurs
Page 6 of 7
Conclusions
Stable isotope data do not support significant CAM consumption by
non-climbing extinct herbivores such as elephant birds, giant tortoises
or pygmy hippopotamuses, but they do support significant CAM
consumption in several extinct lemur lineages. It seems likely that
spines evolved in the ancestral didiereoid as a defence against lemur
folivory. At the very least, as didiereoids diversified to include relatively
large spiny trees in southern and western Madagascar, they must have
been exploited by climbing herbivores of some kind. Because so many
herbivores in the south and southwest have become extinct, one might
hypothesise that the spines on these plants are today anachronistic. The
unusual isotopic signal of these plants allows us to test the plausibility
of this hypothesis, and to offer new insights into likely past consumers.
Our data support the conclusions that the herbivores exploiting the
leaves of Alluaudia were largely climbing lemurs, and that the loss of
giant climbing lemurs has rendered the spines of didiereoid plants,
such as Alluaudia, increasingly anachronistic. With the exceptions of
Lepilemur and Lemur catta in some locations, lemur species today
consume little CAM. However, carbon isotope values indicate that both
extant and now-extinct lemurs may have consumed more CAM plants
in the past, including didiereoid taxa such as Alluaudia. In particular,
Lemur catta, Mesopropithecus globiceps, and especially Hadropithecus
stenognathus, may have relied heavily on Didiereoideae in the recent
past. If indeed the dominant consumers of Alluaudia leaves are now
extinct, these plants may no longer require formidable defence.
Acknowledgements
We thank Dyke Andreasen, Lalao Andriamahefarivo, Anne Axel,
Zachary Rogers, Wendy Applequist, the Madagascar Institut pour la
Conservation des Ecosystèmes Tropicaux, the Missouri Botanical
Garden and the BMSR staff for technical and logistical assistance; the
Université d’Antananarivo Ecole Supériure des Sciences Agronomiques
Département des Eaux et Forêts for permission to collect plants at
BMSR; Margaret Schoeninger and Leanne Nash for providing Lepilemur
isotope data from BMSR; and Stephen Nash/Conservation International
for permission to reproduce illustrations of lemurs. Subfossils were
sampled under collaborative agreements between LRG, D.A. Burney,
W.L. Jungers and the Département de Paléontologie et d’Anthropologie
Biologique, Université d’Antananarivo. Funding was provided by a
Guggenheim fellowship to L.R.G. and the UC Lab Fee Research Program
(09-LR-07-115818-DOMIN to BEC).
Authors’ contributions
Both authors participated in the planning and design of the research.
L.R.G. conceived of the project and B.E.C. conducted analyses. Both
authors wrote the manuscript.
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... We also analyzed two subfossil C. ferox bones from Taolambiby that are currently housed at the Australian National University (ANU). To augment these datasets, we compiled previously published data from five dogs (includes two modern bones, Crowley, 2010;Douglass et al., 2019), nine subfossil C. ferox (Crowley, 2010;Crowley and Godfrey, 2013;Crowley et al., 2017;Anderson et al., 2018), and three subfossil C. spelea (Crowley, 2010). Note that all subfossil Cryptoprocta spp. ...
... Butchered extant taxa in the histogram include only P. verreauxi. Note that the range within each group includes both spatial and temporal variability (Figures 6, 7), and the δ 13 C values for the six modern dogs were corrected for the Suess Effect (following Crowley and Godfrey, 2013) so that they are comparable with subfossil collagen values. ...
... Island-wide, average calibrated dates for C. spelea specimens (n = 3) range from 3,280 to 1,760 cal BP, those for C. ferox (n = 10) range from 2,900 to 1,010 cal BP, and those for dogs (n = 23) span from 890 cal BP to the present. The six modern dogs have δ 13 C values that are corrected for the Suess Effect (following Crowley and Godfrey, 2013) so that they are comparable with subfossil collagen values. ...
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Introduced predators currently threaten endemic animals on Madagascar through predation, facilitation of human-led hunts, competition, and disease transmission, but the antiquity and past consequences of these introductions are poorly known. We use directly radiocarbon dated bones of introduced dogs (Canis familiaris) to test whether dogs could have aided human-led hunts of the island’s extinct megafauna. We compare carbon and nitrogen isotope data from the bone collagen of dogs and endemic “fosa” (Cryptoprocta spp.) in central and southwestern Madagascar to test for competition between introduced and endemic predators. The distinct isotopic niches of dogs and fosa suggest that any past antagonistic relationship between these predators did not follow from predation or competition for shared prey. Radiocarbon dates confirm that dogs have been present on Madagascar for over a millennium and suggest that they at least briefly co-occurred with the island’s extinct megafauna, which included giant lemurs, elephant birds, and pygmy hippopotamuses. Today, dogs share a mutualism with pastoralists who also occasionally hunt endemic vertebrates, and similar behavior is reflected in deposits at several Malagasy paleontological sites that contain dog and livestock bones along with butchered bones of extinct megafauna and extant lemurs. Dogs on Madagascar have had a wide range of diets during the past millennium, but relatively high stable carbon isotope values suggest few individuals relied primarily on forest bushmeat. Our newly generated data suggest that dogs were part of a suite of animal introductions beginning over a millennium ago that coincided with widespread landscape transformation and megafaunal extinction.
... (a) Study area/regional overview Southwest Madagascar experiences a prolonged dry season and receives only a brief rainy season during the austral winter. Regional vegetation is dominated by deciduous C 3 trees and CAM succulents, as well as some C 4 grasses [26]. Riparian forests dissect this otherwise dry landscape, but relatively high δ 15 N values in subfossil lemur collagen suggest that these animals did not prefer wet corridors [27]. ...
... Six general linear models based on multiple approaches to grouping data according to collection site suggest that taxon, age, location and interactions among all variables typically best explain variability in faunal δ 13 C and δ 15 N values Sites marked in green include bones of only endemic animals, those in yellow include only introduced animal bone, and those in red include both. We used sites grouped along the Morombe coast [1][2][3][4][5][6][7][8][9][10], Tulear coast [11][12][13][14][15][16][17][18][19][20][21][22], Mangoky drainage [23][24][25][26], and Onilahy drainage [27,28] and sometimes the Far South [29][30][31][32][33][34][35][36][37][38][39][40][41][42][43] Capra hircus and Ovis/Capra Figure 3. Taxon-specific 14 C date histograms (unsaturated colour) and confidence/credible intervals (saturated colour) for extinction and introduction event estimation. Bayesian posterior probability distributions with 95% brackets give the probability that a species is not present at a certain time given that it was not sampled. ...
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... We propose two nonmutually exclusive explanations for the past phylogenetic inference discrepancies. First, based on patterns of dental microwear (42)(43)(44), dental topography (45), craniodental features (12,29), infraorbital foramen size (IOF) (63), and isotopic data (64)(65)(66) with further support from our evolutionary genomic results, Megaladapis was likely a specialized folivore. Meanwhile, the diets of sportive lemurs (Lepilemur spp.) are also highly folivorous (67)(68)(69). ...
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Significance Based on “subfossil” skeletal remains it is known that multiple now-extinct giant lemur (primate) species with estimated body masses of up to ∼160 kg survived on Madagascar into the past millennium. In this study, we used ancient DNA methods to sequence the nuclear genome of one of these megafaunal lemurs, Megaladapis edwardsi (∼85 kg). With the power of the nuclear genome, we robustly resolved the phylogenetic relationship between Megaladapis and other lemurs, which had been a lingering uncertainty. We also identified multiple signatures of past positive natural selection across the M. edwardsi genome that support reconstructions of this taxon as a large-bodied, specialized folivore.
... We propose two non-mutually exclusive explanations for the past phylogenetic inference discrepancies. First, based on patterns of dental microwear 38,40,58 , dental topography 41 , craniodental features 9,25 , infraorbital foramen size 59 and isotopic data [60][61][62] with further support from our evolutionary genomic results (see below), Megaladapis was likely a specialized folivore. Meanwhile, the diets of sportive lemurs (Lepilemur spp.) are also highly folivorous [63][64][65] . ...
... Stable isotope data are also consistent with the reconstruction of a folivorous diet for Megaladapis. Specifically, carbon isotope ratios can help differentiate the relative contributions of C3 plants, C4 plants and stem/leaf succulents, as well as non-photosynthetic plant tissues (e.g., fruits, flowers) in the diets of extinct species 60,61 . The spiny thicket habitat in southern and southwest Madagascar is dominated by succulents with patches of C4 grasslands and C3 trees, yet M. edwardsi carbon isotope ratios ubiquitously suggest a C3-based, herbivorous leafy diet 60 . ...
Preprint
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No endemic Madagascar animal with body mass >10 kg survived a relatively recent wave of extinction on the island. From morphological and isotopic analyses of skeletal ‘subfossil’ remains we can reconstruct some of the biology and behavioral ecology of giant lemurs (primates; up to ~160 kg), elephant birds (up to ~860 kg), and other extraordinary Malagasy megafauna that survived well into the past millennium. Yet much about the evolutionary biology of these now extinct species remains unknown, along with persistent phylogenetic uncertainty in some cases. Thankfully, despite the challenges of DNA preservation in tropical and sub-tropical environments, technical advances have enabled the recovery of ancient DNA from some Malagasy subfossil specimens. Here we present a nuclear genome sequence (~2X coverage) for one of the largest extinct lemurs, the koala lemur Megaladapis edwardsi (~85kg). To support the testing of key phylogenetic and evolutionary hypotheses we also generated new high-coverage complete nuclear genomes for two extant lemur species, Eulemur rufifrons and Lepilemur mustelinus , and we aligned these sequences with previously published genomes for three other extant lemur species and 47 non-lemur vertebrates. Our phylogenetic results confirm that Megaladapis is most closely related to the extant Lemuridae (typified in our analysis by E. rufifrons ) to the exclusion of L. mustelinus , which contradicts morphology-based phylogenies. Our evolutionary analyses identified significant convergent evolution between M. edwardsi and extant folivorous primates (colobine monkeys) and ungulate herbivores (horses) in genes encoding protein products that function in the biodegradation of plant toxins and nutrient absorption. These results suggest that koala lemurs were highly adapted to a leaf-based diet, which may also explain their convergent craniodental morphology with the small-bodied folivore Lepilemur .
... While δ 13 C data are now available for a broad variety of plants from various environments across Madagascar, minimal data exist for the island's grasses. These are limited to a handful of unidentified Poaceae specimens from southwestern Madagascar (Crowley & Godfrey, 2013;Hixon et al., 2021) and herbarium specimens from several Panicum species (Osborne et al., 2014). These are hardly enough data to be able to determine expected carbon isotope values for C 3 and C 4 grasses from particular regions in Madagascar, possible isotopic differences among different grass lineages, or species with different distributions or adaptations. ...
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Grasses are significant drivers of fires and are the primary food source for cattle in Madagascar's Central Highlands. However, their extent and importance to animals and people in the past remain poorly understood. Clarifying the history of Malagasy grasslands is necessary for building climate resilient food systems and supporting carbon stores that also conserve biodiversity. We generated chemical data for grasses that grow in open habitats in central Madagascar, which will help improve our understanding of the ecological and economic importance of modern grassy ecosystems, reconstruct the regional history of grasses, and anticipate how vegetation may respond to changing climate and rising atmospheric carbon dioxide levels. Stable carbon isotope (δ13C) data for Malagasy grasses are needed to establish expected values for C3 and C4 grasses from particular regions in Madagascar, and possible differences among different grass lineages, or species with different distributions or adaptations. These data, in turn, may help inform how widespread grasses were in the past, and the importance of grasses to endemic and domesticated animals as well as people over time. We analysed both δ13C and weight %C:N from 63 Poaceae species that grow in open grassy biomes in Madagascar's Central Highlands and explored how these values relate to multiple variables, including encounter frequency, distribution, lineage, adaptations to grazing and fire and the typical floral assemblage in which each species occurs. Of the species sampled, 56 are C4 and seven are C3. There are no differences in δ13C or weight %C:N among either C3 or C4 species with different distributions or adaptations, from different assemblages, or that are frequently or infrequently encountered. However, there are differences in both δ13C and weight %C:N among C4 lineages, and the single C3 arundinoid (Styppeiochloa hitchcockii) has larger weight %C:N than C3 Paniceae. Our results provide a foundation for evaluating reliance on C4 resources by people, as well as domesticated and endemic animals both today and in the past. We encourage gathering additional comparative data for co‐occurring individual plants from the same open grassy biome localities, as well as other species, habitats and regions in Madagascar. Les graminées sont d'importants facteurs de feux de brousse mais en même temps elles constituent aussi les principales sources de nourritures des troupeaux de bétail dans les Hauts Plateaux du centre de Madagascar. Cependant, leur étendue et leur importance pour les animaux et les êtres humains dans le passé restent encore mal connues. Elucider ou clarifier l'histoire des prairies Malagasy est nécessaire pour créer des systèmes alimentaires résilients au changement de climat et pour supporter la séquestration de carbone en terme de la conservation de la biodiversité. Nous avons créé des données chimiques pour les graminées qui poussent dans des habitats ouverts dans le centre de Madagascar, données qui permettront d'améliorer notre compréhension sur l'importance écologique et économique des écosystèmes herbeux actuels, de reconstruire l'histoire des graminées de la région, et d'anticiper les réponses de la végétation au changement climatique et à l'augmentation des niveaux de dioxyde de carbone dans l'atmosphère. Ny rohivoaharim‐bozaka aman'ahitra no tena mahatonga sy miteraka ny afo na ny doro ala, kanefa izy ireo ihany koa no loharanon‐tsakafon'ny omby ompiana ao amin'ny faritra avo ao afovoan'I Madagasikara. Eo antrehan'izany anefa dia tena mbola tsy mazava na fantatra tsara hatramin'izao ny hoe hatraiza ny naha zava‐dehibe ny bozaka aman'ahitra teo amin'ny fiainan'ny biby sy ny olombelona tany aloha be tany. Tena ilaina ny manazava ny tantaran'ny bozaka aman'ahitra Malagasy mba hahafahana manangana rafitra ara‐tsakafo mahazaka ny fiovaovan'ny toetr'andro sy mba ho fanohanana ny fitehirizana karbaona izay manampy koa amin'ny fikajiana ny harena voajanahary. Namorona angona na antontan‐kevitra simika momba ny bozaka aman'ahitra maniry an‐kijana malalaka ao amin'ny faritra afovoan'ny Madagasikara izahay, entina hanampy sy hanatsarana ny fahalalantsika ny maha‐zava‐dehibe ara‐ekolojika sy ara‐toekarena ny rohivoaharim‐bozaka misy ankehitriny, entina koa hanorenana ny tantaran'ny bozaka aman'ahitra any amin'ny faritra ary haminavinana ny mety ho fihetsiky ny vondron‐javamaniry amin'ny fiovan'ny toetr'andro sy ny fiakatran'ny habetsahan'ny entona karbonika eny amin'ny habakabaka. Grasses are significant drivers of fires and are the primary food source for cattle in Madagascar's Central Highlands. However, their extent and importance to animals and people in the past remain poorly understood. Clarifying the history of Malagasy grasslands is necessary for building climate resilient food systems and supporting carbon stores that also conserve biodiversity. We generated chemical data for grasses that grow in open habitats in central Madagascar, which will help improve our understanding of the ecological and economic importance of modern grassy ecosystems, reconstruct the regional history of grasses and anticipate how vegetation may respond to changing climate and rising atmospheric carbon dioxide levels.
... This suggests significant predation was experienced by the Madagascan clade (Cooper and Owen-Smith, 1986), even if today they experience only light predation by Lemur catta and Propithecus verreauxi (Norscia and Palagi, 2011;LaFleur and Sauther, 2015). In fact, Hadropithecus is the only species we know that presumably had the capacity and stable isotope compositions to have predated upon these CAM plants regularly (Crowley and Godfrey, 2013). ...
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Carbon isotopic analysis has been challenging our ideas about hominin diet for nearly 30 years. The first study in 1994 revealed that Paranthropus robustus from South Africa consumed principally C3 foods (e.g., tree fruits and leaves) but also about 25% C4/CAM resources (e.g., tropical grasses and sedges). This result was largely consistent with morphological and dental microwear evidence suggesting P. robustus had a diet which included hard objects like nuts and seeds. Decades later, however, P. boisei from eastern Africa was shown to have eaten nearly 80% C4/CAM plants like the contemporaneous grass-eating primate Theropithecus. Moreover, dental microwear revealed no evidence of hard object consumption in P. boisei, suggesting a diet of tough foods such as grass or sedge leaf and stem. So Paranthropus presents us with two central problems: 1) Why do dietary proxies suggest different diets for the two robust australopiths despite their morphological congruity; and 2) How could P. boisei have consumed tough foods with teeth that seem unsuited to the task. Here we review these questions and more with a particular focus on new isotopic data from the Omo and insights that can be gleaned from mammals outside the haplorrhine primates. We argue that extant Primates do not capture the ecomorphological diversity of P. boisei and other extinct primates and should not narrowly circumscribe the behaviors we ascribe to extinct taxa. We also discuss possible digestive strategies for P. boisei in light of its morphology, dietary proxy data, food mechanical properties, and comparative data on mammalian digestive kinetics.
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Linnaeus' original scientific description of Lemur catta, the ringtailed lemur, was based on a living animal brought to England in 1749. Although there were many brief descriptions of wild ringtailed lemurs, it was not until Jolly wrote her now classic book, Lemur Behavior, that we had our first detailed description of the natural history of these beautiful animals (Fig. 1). Since then, long-term field studies, mainly from two study sites in Madagascar, Berenty and Beza Mahafaly (Fig. 2), as well as studies on forest-living groups in captivity at the Duke University Primate Center in Durham, North Carolina, have greatly expanded our knowledge of the ecology and behavior of this species (Table 1, Box 1). Thirty-five years of research on this species at these various sites indicates that Lemur catta is proving to be every bit as complex in its behavior as are many anthropoid primates. This very complexity has been reflected in the current controversies and questions concerning the ecology and behavior of this species.