AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 147:201–216 (2012)
Spatial and Temporal Ecological Diversity Amongst Eocene Primates of France: Evidence From Teeth Anusha Ramdarshan,1* Gildas Merceron,2 and Laurent Marivaux1 1
Laboratoire de Pale´ontologie, Institut des Sciences de l’Evolution de Montpellier (ISE-M, UMR-CNRS 5554), c.c. 64, Universite´ Montpellier 2, Place Euge`ne Bataillon, F-34095 Montpellier Cedex 05, France 2 UMR 5276 (CNRS, ENS, Universite´ Lyon 1), Laboratoire de Ge´ologie de Lyon, Terre, Plane`tes, Environnement; Campus de la Doua, 2 Rue Raphae¨l Dubois, F-69622 Villeurbanne, France KEY WORDS
Eocene; Europe; paleoecology; diet; microwear
ABSTRACT Diet is of paramount importance in the life of a primate. It is also highly variable, as potential food sources vary in spatial distribution and availability over time. The fossil record, due to its fragmentary nature, offers few possibilities to assess the dietary range of a given primate across its spatial and temporal distribution. Here we focus on three taxa, Leptadapis magnus (Adapidae, Adapiformes), Necrolemur cf. antiquus (Microchoeridae, Omomyiformes), and Pseudoloris parvulus (Microchoeridae, Omomyiformes). These taxa occur at different localities of the Late Eocene in the south of France ranging from MP16 (Robiac, Lavergne; 39 Ma), MP17a (La Bouffie, Euzet, Fons 4; 38 Ma) to MP17b (Perrie`re; 37 Ma). Diets of fossil taxa are assessed here by dental microwear analysis using a comparative database of 11 species of living strep-
sirhines. On the whole, leaves were a preferred food for the large-bodied Leptadapis (4–5 kg). However, the diet of this taxon varied from a mix of leaves and fruit at La Bouffie, a closed tropical rain forest environment, to a strictly leafeating one in the more open environment of Perrie`re. Based on body mass (200–350 g) and dental microwear patterns, Necrolemur had a mainly fruit-based diet, perhaps supplemented by insects. However, the comparison of the different localities reveals the dietary range of this smallbodied omomyiform which seems to vary between insects and a much softer diet. Pseudoloris had a diet strictly based on insects. Contrary to Leptadapis or Necrolemur, its diet seems to have been confined to insects whatever the locality considered. Am J Phys Anthropol 147:201–216, 2012. V 2011 Wiley Periodicals, Inc.
Diet correlates with many different aspects of a primate’s life, from foraging strategies to ranging patterns or even social groupings (Fleagle, 1999). As such, it is an important factor when considering a primate’s ecology. Diet in itself is influenced by the size of the taxon, its tooth morphology, and the physiology of its digestive system (e.g., Chivers et al., 1984; Marshall and Wrangham, 2007). Primate diets are generally divided into three main categories: fruit, leaves, and insects (Chivers et al., 1984; Fleagle, 1999). But this categorization oversimplifies the true diversity of a primate’s diet, which can include a wide array of components. For example, Cebusapella is known to eat fruit, leaves, seeds, pith, nectar, insects, birds, eggs, small reptiles, and even small mammals up to 900 g (Izawa, 1978; Eisenberg, 1989; Janson and Boinski, 1992). Food availability is highly variable, as food distribution can fluctuate from year to year, season to season, or even day to day. Spatial and temporal variability in the distribution of primate foods can have far-reaching effects on primate ecology (Lee et al., 1991; Lee, 1996; Power, 1999). For example, in Malagasy primate communities weaning and maximum fruit availability coincide (Wright et al., 2005). As a response to variation in food availability, diet can also be highly variable. In fact, some primates can shift from a mainly fruit-based diet to a leaf-based one, such as in the case of the Central American Alouatta pigra (Pavelka and Knopff, 2004). Diet variability in extant primates has already been described in numerous taxa. Extensive studies can be carried out for extant primates simply by observation in the wild, or by analysis of their stomach content. Such studies are not possible for fossil primates however, and
the fossil record offers few opportunities to assess the full scope of a primate’s diet, i.e., over its spatial and temporal distribution. Because of the fragmentary nature of fossils, dietary estimates for extinct primates merely represent either an overall approximation or a snapshot in time. The collections representing the European primate fossil record of the Eocene have been built up over decades of fieldwork and now offer the possibility of an extensive dietary study in a spatial and temporal framework. Two groups of fossil primates are abundant in the Eocene fossil record in Europe: Adapiformes and Omomyiformes. Both taxa radiated during the Eocene. They are thought to have colonized a wide range of ecological niches. However, each group displays very distinct morphologies that may reflect different adaptations between the two taxa. By the late Eocene, Adapiformes were
C 2011 V
WILEY PERIODICALS, INC.
C
Grant sponsor: Agence Nationale de la Recherche; Grant numbers: ANR-08-JCJC-0017—ANR-ERC PALASIAFRICA. *Correspondence to: Anusha Ramdarshan, Laboratoire de Pale´ontologie, Institut des Sciences de l’Evolution de Montpellier (ISE-M, UMR-CNRS 5554), c.c. 064, Universite´ Montpellier 2, Place Euge`ne Bataillon, F-34095 Montpellier Cedex 05, France. E-mail:
[email protected] Received 8 June 2011; accepted 11 October 2011 DOI 10.1002/ajpa.21638 Published online 19 November 2011 in Wiley Online Library (wileyonlinelibrary.com).
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mostly medium- to large-bodied and most likely diurnal, fruit- and leaf-eaters. By contrast, Omomyiformes were small (up to 500 g), and most likely nocturnal and fruitand insect-eaters. They occupied very distinct ecological niches, although the two groups overlapped slightly (in term of body mass range) in the Late Eocene with the appearance of small-bodied adapiforms such as Anchomomys, and larger omomyiforms such as Microchoerus (Fleagle, 1999). In this study, we focus on different Late Eocene localities, from the European reference levels [MP, Mammal Paleogene (BiochroM’97, 1997)] MP 16 to MP 17b in the south of France, i.e., from 39 to 37 Ma (Escarguel et al., 1997). The study here is conducted on the primate communities of three localities from the Quercy phosphorites (Lavergne [MP 16], La Bouffie [MP 17a] and Perrie`re [MP 17b]) and three from the region of Gard (Robiac [MP 16], Euzet [MP 17a] and Fons 4 [MP 17a]). The analyses are carried out on all the primate taxa known from these localities. As the focus of this study is dietary variability, special attention is given to Leptadapis magnus (Adapidae, Adapiformes), Necrolemur cf. antiquus (Microchoeridae, Omomyiformes), and Pseudoloris parvulus (Microchoeridae, Omomyiformes), as these three taxa cooccur at numerous localities. They most probably occupied very different ecological niches in these primate communities. Indeed, based on dental morphology Leptadapis has previously been depicted as a large-bodied leafeater, most probably diurnal. These hypotheses have been based on overall dental and cranial morphology (e.g., Gingerich, 1972; Szalay and Delson, 1979; Gingerich, 1981; Gingerich and Martin, 1981; Covert, 1985; Covert, 1986; White, 2006), and shearing quotients (Kay et al., 2004; Perry, 2008). Necrolemur, on the other hand, has been described as a small nocturnal fruit-eater (Fleagle, 1999; Kay and Kirk, 2000; Ross et al., 2007). Previous dietary reconstructions are based on shearing quotients (Strait, 2001). Pseudoloris, based on its small size and well-developed molar shear, has been presumed to eat insects (Covert, 1986; Strait, 2001). Dental microwear analysis has never been studied for these taxa. Indeed, this is the first study to apply dental microwear analysis to European Eocene primates. The aim of this study is to highlight potential intraspecific differences in the diet of Leptadapis, Necrolemur, and Pseudoloris. Dietary reconstruction is based on dental microwear analysis. This method examines traces left by food on the surface of the dental enamel. This abrasion carries a specific signature that depends on the physical nature of the food consumed. Several major sources have been identified. Although some plant foods may seem too soft to damage the enamel surface, most contain microscopic opal amorphous silica bodies (i.e., phytoliths). Such bodies have been found on fossil primate teeth (Ciochon et al., 1990), and numerous studies consider phytoliths to be a major source of dental microwear (e.g., Walker et al., 1978; Covert and Kay, 1981; Kay and Covert, 1983; Ciochon et al., 1990). However, a recent study has suggested phytoliths do not possess the physical properties necessary to scar enamel (Sanson et al., 2007). Even if phytoliths are indeed too soft to scar enamel, there are still numerous other potential sources of dental microwear. For example, exogenous quartz particles can scar dental enamel in mammals, whether they are terrestrial or arboreal (Ungar et al., 1995). Although the extent of its influence is still unknown, geophagy (i.e., the practice of eating soils and clays) is not rare among primates American Journal of Physical Anthropology
(e.g., Krishnamani and Mahaney, 2000), and must also be considered as a potential source of abrasion. Yet more factors can include woody tissues, which may cause tooth wear in the case of exudates and gum-eaters as they have to gouge through tree bark to get to their preferred food source, or fruit which have tough rinds and/or seeds. Additionally insect-eaters have to contend with both the unsclerotized (e.g., moths) and the sclerotized cuticles (e.g., beetles) of their prey. From soft-bodied caterpillars to hard-bodied beetles, insects have very different physical properties, which can cause different types of wear (Strait, 1993a). Consequently, dental microwear patterns are most often the result of a combination of factors. By comparing microwear patterns between modern and fossil primates, this method allows the reconstruction of the diet of fossil species. Several studies have focused on the analysis of this microwear to predict the diet of fossil taxa, particularly primates (e.g., Teaford and Walker, 1984; Grine and Kay, 1988; Ungar, 1996; King et al., 1999; Merceron et al., 2009). Dental microwear records traces of food from only the last weeks or even days in the life of the animal, depending on the nature of its diet (Teaford and Oyen, 1989; Merceron et al., 2010). Thus, dental microwear patterns are a direct record of the last meals before death and not necessarily an indication of the overall diet of an animal. With such a fine scale it therefore becomes possible, at least in principle, to highlight potential intraspecific and interpopulation variation in the diet of Leptadapis and Necrolemur. Although scanning electron microscopy has been the instrument of choice for a number of microwear studies [see Ungar et al. (2008) for a complete review of dental microwear methodology], this approach is expensive and time consuming. Low-magnification light microscopy has been proposed as an alternative (Solounias and Semprebon, 2002). However, the method consists of counting microwear features directly from the cast; repeatability is therefore not guaranteed. Further studies developed a more repeatable approach, based on analyzing digitalized images (e.g., Merceron et al., 2004, 2005). This last approach minimizes inter- and intraobserver error since it can be done several times by one or several observers on the same location on the dental facet and with the very same light and contrast conditions. It therefore offers a cost effective way of analyzing dental microwear. This study will use low magnification light microscopy for dental microwear analysis, following a strict casting protocol, designed to maximize image quality.
MATERIAL Localities Robiac, Euzet, and Fons 4. These localities (Fig. 1) are situated in the south of France (Gard). Since their discovery in the early 20th century (Depe´ret, 1917), and notably after the further excavations of the 1960s, 1970s, and 1980s, Robiac, Euzet, and Fons 4 have yielded rich and diverse mammalian faunas (Sudre, 1969). Paleoenvironments for each locality have been inferred by Legendre (1987, 1988) using cenograms. Cenograms highlight the relationship between the mass distribution of a mammalian community and the environment in which they live. The use of this method in numerous extant communities has shown that the structure of the graph is closely linked to the type of environment. Paleoenvironment can thus be inferred by analogy
ECOLOGICAL DIVERSITY OF EOCENE PRIMATES OF FRANCE
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Fig. 1. Geographic location of the studied localities and corresponding cenograms (from Legendre, 1989).
with extant communities from different environments. The primate fauna of Robiac (MP 16, 39 Ma) includes two taxa, Adapis sudrei and Necrolemur cf. antiquus (Table 1). The cenogram for this locality points to a closed tropical rainforest environment (Legendre, 1987, 1988; Fig. 1). Two taxa are also present in the locality of Euzet (MP 17a, 38 Ma) (Escarguel et al., 1997), Leptadapis magnus and Necrolemur cf. antiquus. Cenograms for this locality are similar to those of extant warm and humid environments, most probably more open than at Robiac (Legendre, 1989). Fons 4 is a MP 17a locality (38 Ma; Escarguel et al., 1997) situated only a few kilometers from Robiac and Euzet (Fig. 1). Leptadapis and Necrolemur occur in this locality (Table 1). The paleoenvironment of Fons 4 would have been similar to Euzet, a warm and humid secondary or gallery forest, again more open than at Robiac (Legendre, 1988). Lavergne, La Bouffie, and Perrie`re. These three localities are fissure fillings in the Quercy region of southern France (Lot). All the specimens studied here are from well-known and dated localities (Re´my et al., 1987). Lavergne is a locality assigned to the reference level MP 16 (39 Ma) and corresponds most probably to a tropical rainforest environment (Legendre, 1988; Escarguel et al., 1997). Two taxa are present there: Necrolemur cf. antiquus and Pseudoloris parvulus. The primate fauna at La Bouffie (MP 17a, 38 Ma) consists of four taxa, Leptadapis magnus, Necrolemur cf. antiquus, Anchomomys quercyi, and Pseudoloris parvulus. The cenogram for this locality indicates a tropical rainforest (Legendre, 1987, 1988). Three taxa occur at Perrie`re (MP 17b; 37 Ma): Leptadapis magnus, Microchoerus erinaceus, and Pseudoloris parvulus. The cenogram compares to extant
wooded savannas, indicating a more open and more arid environment than La Bouffie, or may be the presence of a dry season (Legendre, 1988).
Studied specimens Fossil taxa. The specimens figured in this study are housed in the paleontological collections of the ‘‘Universite´ Montpellier 2’’ (France), in the ‘‘Collections de Ge´ologie de l’Universite´ Claude Bernard Lyon 1’’ (France), or in the Basel Natural History Museum (Switzerland). A list of taxa and specimens is presented in Table 1. Dental microwear analysis was applied to all the primates present in each locality, with special attention given to the taxa which occur in more than two localities: Necrolemur cf. antiquus, Pseudoloris parvulus, and Leptadapismagnus. Body mass estimates are provided in Table 2. Godinot and Couette (2008) propose several new species, splitting Leptadapis magnus into two new genera (Leptadapis and Magnadapis) and several species. Their study focuses on 12 well preserved skulls from the ‘‘Phosporites du Quercy’’. The descriptions of the new taxa are mainly based on cranial characters and are difficult to apply in this study as our material is mostly comprised of isolated teeth. Furthermore, Godinot and Couette (2008) focus on material from the Old Quercy collections for which the provenance is unfortunately unknown. For these reasons, our study refers to Leptadapis magnus sensu lato. Extant taxa. The comparative database includes 11 extant species of strepsirrhine primates, consisting of 7 lemuriforms and 4 lorisiforms. The specimens are housed in the Zurich Anthropological Institute (Switzerland) and/or the Muse´um National d’Histoire Naturelle American Journal of Physical Anthropology
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A. RAMDARSHAN ET AL. TABLE 1. List of taxa at each locality and number of specimens studied Systematics
Perrie`re (Quercy, MP17b) Leptadapis magnus Adapidae, Adapiformes Pseudoloris parvulus Microchoeridae, Omomyiformes Microchoerus erinaceus Microchoeridae, Omomyiformes La Bouffie (Quercy, MP17a) Leptadapis magnus Adapidae, Adapiformes Necrolemur cf. antiquus Microchoeridae, Omomyiformes
N
Specimen no.
9 4 5
PRR 1044–45, 1047; 1048; 1050; 1451, 1850, 1965; 1966 PRR 55, 150, 1930–31 PRR 1011, 1023–24; 1027, 1439
7 35
BFI 50–56 BFI 2; 4; 8; 110; 113; 119; 127–8; 132–3; 137; 141; 145; 164–5; 178–9; 635; 637–8; 643; 645; 650–1; 655; 658; 662; 672; 678; 719; 721; 723; 729; 731; 750–1 BFI 2018; 2021; 2023; 2550; 2553 BFI 2549
Pseudoloris parvulus Anchomomys aff quercyi Fons 4 (Gard, MP17a) Leptadapis magnus Microchoerus erinaceus Euzet (Gard, MP 17a) Leptadapis magnus
Microchoeridae, Omomyiformes Notharctidae, Adapiformes
5 1
Adapidae, Adapiformes Microchoeridae, Omomyiformes
10 8
F4 289; 290–2; 334–5; 337; 340–342 F4 236; 239; 240; 250; 259; 261; 308; 333
Adapidae, Adapiformes
12
Necrolemur cf. antiquus Robiac (Gard, MP 16) Adapis sudrei
Microchoeridae, Omomyiformes
FSL 634; 6491–93; 6542; 6495–96; STH 318–19; 1634–1636 EUZ 110; 144; STH 1636; 2511
Adapidae, Adapiformes
15
Necrolemur cf. antiquus
Microchoeridae, Omomyiformes
12
Lavergne (Quercy, MP 16) Necrolemur cf. antiquus Microchoeridae, Omomyiformes Pseudoloris parvulus Microchoeridae, Omomyiformes
6 2
(MNHN) in Paris (France). Details are presented in Table 3. Dietary categories were assigned following the literature cited in Table 3. Diet is split into four categories: leaf-, insect-, fruit-, and gum-dominated diets. Although gum-dominated diets are generally categorized within ‘‘fruit-eating,’’ gums present different physical properties. Moreover, gum-eaters have different foraging strategies and morphological adaptations compared to fruit-eaters (Nash, 1986). Their importance in primate ecology has recently been highlighted (Nash and Burrows, 2010). Therefore, ‘‘gum-eating’’ has been included as a fourth dietary category. Each taxon was attributed to a category based on their known diets. These categories are generated from the available data for extant strepsirhines, which is principally composed of studies based on percent feeding times. These percentages correspond to the time spent foraging and feeding on a given food type. However, these types of study can be imprecise. For example, animal prey can be sparse and rather evasive. The time spent foraging for them will produce a smaller yield than primate foraging for fruit or leaves (Kurland and Gaulin, 1987). Using studies characterizing the physical properties of foods for each taxon would indeed be more relevant to dental microwear analysis, but unfortunately this type of data is not widespread.
METHODS High resolution replicas were made following the protocol laid out by Merceron et al. (2005). They were made using a transparent polyester-based resin (EBALTA MG 709-120). Photographs were taken at 1003 using an optical stereomicroscope (LEICA M 205 C) connected to a camera (Leica DFC 420C). The resulting grayscale images had a resolution of 3.5 pixels per lm. Image analysis was conducted with the open source software ImageJ (Abramoff et al., 2004), and the plug-in ObjectJ (Vischer et al., 1994). This plug-in allows the user to superimpose graphical markers onto an image American Journal of Physical Anthropology
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RBN 5095, 5100, 5107, 5160–63, 5166, 5187, 5260–61, 5346, 8624, 8627–28 RBN 8539, 8542; 8546; 8569; 8571; 8592; 8594, 8596, 8598; 8602; 8614; 8651 LAV 24–5; 27; 191–92; 210 LAV 225; 227
TABLE 2. Body mass estimates for fossil taxa M1 area
Body mass (g)
Taxon and locality
N
M
S.D.
M
S.D.
Necrolemur antiquus La Bouffie Robiac Lavergne Euzet Microchoerus erinaceus Fons 4 Perrie`re Pseudoloris parvulus La Bouffie Perrie`re Lavergne Leptadapis magnus La Bouffie Euzet Perrie`re Adapis sudrei (Robiac) Anchomomys quercyi (La Bouffie)
59 46 5 6 2 13 5 4 18 1 9 2 12 2 7 3 6 1
6.33 6.48 5.71 5.40 7.15 9.96 9.26 11.53 1.73 1.64 1.85 1.52 35.43 28.92 40.07 28.96 15.91 3.85
0.64 0.53 0.37 0.35 0.75 1.65 0.86 2.05 0.25 – 0.22 0.13 7.79 0.28 6.35 5.67 1.36 –
285 296 241 220 346 597 527 756 35 32 39 28 4674 3295 5639 3344 1260 127
47 39 25 23 58 167 79 215 8 – 7 4 1658 51 1432 1076 178 –
Body mass estimates calculated using the prosimian least squares regression of M1 area (A) against body mass (B) among living primates, LnB 5 1.614LnA 1 2.67 established by Conroy (1987).
(in this case scratches and pits).The plug-in can then compile different variables (such as total number and length) for each type of marker. In this study, ObjectJ is configured so that the observer can mark four different types of characters: scratches, wide scratches, pits, and large pits (for further details, contact first author). Pits have a length to width ratio exceeding ¼ whereas for scratches the same ratio is less than ¼ (Grine, 1986). In addition, pits are categorized as large if their maximum diameter exceeds 15 lm. Similarly, scratches are consid-
205
ECOLOGICAL DIVERSITY OF EOCENE PRIMATES OF FRANCE TABLE 3. Mean (M) and standard deviation (SD) for dental microwear variables for each taxon included in this study Ns Taxon Leaf-dominated diet Lepilemur ruficaudatus Propithecus verreauxi Fruit-dominated diet Microcebus murinus Cheirogaleus major Cheirogaleus medius Eulemur fulvus Perodicticus potto Insect dominated diet Arctocebus calabarensis Loris tardigradus Gum-dominated diet Otolemur crassicaudatus Euoticus elegantulus
N 32 17 15 74 20 10 10 15 19 24 16 8 23 8 15
Perrie`re (Quercy, MP 17b) Leptadapis magnus 9 Microchoerus erinaceus 6 Pseudoloris parvulus 12 La Bouffie (Quercy, MP 17a) Leptadapis magnus 7 Necrolemur cf. antiquus 36 Pseudoloris parvulus 5 Anchomomys quercyi 1 Euzet (Gard, MP 17a) Leptadapis magnus 12 Necrolemur cf. antiquus 4 Fons 4 (Gard, MP 17a) Leptadapis magnus 10 Microchoerus erinaceus 8 Lavergne (Quercy, MP 16) Necrolemur cf. antiquus 5 Pseudoloris parvulus 2 Robiac (Gard, MP 16) Adapis sudrei 17 Necrolemur cf. antiquus 11
M
Ls SD
M
Np SD
M
Nws SD
M
SD
Nlp
Pp
Tot
M
SD
M
SD
M
SD
33.0 32.3 33.6 29.5 37.6 20.6 31.6 35.3 19.2 29.4 29.1 30.7 18.4 19.0 18.1
Extant taxa organized by dietary category 3.9 81.4 16.6 22.7 5.1 0.2 0.5 3.6 73.6 12.0 24.8 5.8 0.4 0.6 4.3 90.3 16.9 20.2 2.4 0.1 0.3 8.6 63.5 12.3 36.2 9.0 0.8 0.9 5.2 60.6 11.9 44.1 6.1 1.3 0.9 1.2 63.8 3.9 38.0 3.1 1.3 0.7 1.7 71.9 15.7 40.7 1.4 0.0 0.0 3.1 70.5 10.0 21.7 3.0 0.4 0.6 2.4 56.3 9.7 36.3 3.5 0.6 0.8 3.1 74.5 13.4 33.2 4.5 2.5 1.7 3.2 74.7 13.9 33.9 4.2 3.0 1.5 2.1 73.5 13.1 30.5 4.8 0.5 0.6 4.6 36.1 9.9 29.2 4.7 2.2 1.4 3.9 36.9 11.0 26.9 2.0 2.1 1.1 5.1 35.7 9.6 30.5 5.2 2.2 1.6 Fossil taxa split according to locality
0.4 0.8 0.1 2.0 2.8 1.1 1.8 0.4 3.0 3.1 3.5 1.5 2.0 2.0 2.1
0.9 1.1 0.3 1.6 1.5 0.8 1.0 0.6 1.5 1.6 1.5 0.6 1.1 1.3 1.0
40.5 43.0 37.6 55.2 53.9 64.8 56.3 38.1 65.4 52.9 53.8 49.6 61.6 58.9 63.0
5.3 5.2 3.8 10.3 2.4 1.8 1.5 3.8 3.2 4.2 3.8 4.5 6.7 4.2 7.4
55.6 57.2 53.9 65.8 81.7 58.6 72.3 57.0 55.5 62.6 62.9 61.3 47.7 45.9 48.6
6.8 7.7 5.2 13.0 10.6 3.7 2.3 4.4 4.6 5.5 5.7 5.1 6.7 5.3 7.3
33.6 19.8 27.1
3.1 3.0 3.8
80.9 86.3 53.7
14.2 10.8 9.5
15.2 31.3 34.3
3.2 4.1 3.3
0.1 0.2 1.9
0.3 0.4 1.1
0.2 0.3 2.3
0.7 0.5 1.4
31.0 61.2 55.9
3.4 4.1 4.1
48.8 51.2 61.3
5.7 5.6 5.1
20.6 18.0 36.8 24.0
2.3 2.9 6.1 –
60.2 73.7 58.3 61.1
6.5 17.8 8.8 –
24.7 36.4 39.6 45.0
2.1 3.3 3.1 –
0.7 1.2 2.4 0.0
0.8 1.9 1.3 –
1.4 0.4 3.0 3.0
1.0 0.8 1.2 –
54.6 67.0 52.0 65.2
2.8 4.4 5.0 –
45.3 54.4 76.4 69.0
3.5 3.8 5.7 –
26.1 24.0
3.5 0.8
101.1 61.6
24.9 12.3
26.8 24.5
3.0 0.6
0.1 0.5
0.3 1.0
0.5 1.3
0.9 0.5
50.8 50.5
4.3 1.3
52.9 48.5
4.6 0.6
26.2 16.1
3.2 3.6
92.6 68.5
27.6 13.1
19.0 38.9
4.5 1.8
0.3 0.0
0.7 0.0
0.4 0.9
0.7 1.5
41.6 70.9
6.3 4.4
45.2 55.0
6.2 4.2
19.7 35.5
7.0 0.7
66.1 62.3
14.6 5.0
37.2 37.5
3.4 0.7
0.0 0.0
0.0 0.0
0.0 1.0
0.0 1.4
69.4 64.5
3.9 1.2
54.0 72.9
3.3 2.1
33.4 28.0
3.9 1.8
79.4 60.9
15.6 14.4
18.4 30.1
2.6 2.6
0.4 3.0
0.7 1.3
0.4 3.3
0.9 1.3
35.5 51.8
4.4 2.9
51.7 58.1
4.5 3.0
Abbreviations are as follows: a : Lemurifomes; b : Lorisiformes; N: number of specimens; M: mean; SD: standard deviation; Ns: number of scratches; Ls: length of scratches; Np: number of pits; Nws: number of wide scratches; Nlp: number of large pits; Pp: percentage of pits; Tot: total number of microwear scars. Taxa are assigned to dietary categories based on greater than 50% consumption of a food type (based on feeding observations). Dietary categories for extant taxa were determined from the literature: Ganzhorn (2002) ; Ganzhorn et al (2004) ; Hilgartner et al (2008); Simmen et al (2003) ; Norscia (2006); Radespiel (2006) ; Dammahn and Kappeler (2008); Lahann (2007a ; b); Fietz (1999) ; Overdorff (1993) ; Vasey (2002); Nekaris and Rasmussen (2003); Oates 1984; Ravosa, (2007); Burrows and Nash (2010).
ered wide if their width exceeds 15 lm (e.g., Merceron et al., 2004, 2005). These characters are most often easily recognizable and measurements are made only in borderline cases. For each specimen, a 100 lm 3 100 lm surface was analyzed: a standardized square of 0.01 mm2 is placed in the center of the studied crushing facet. All microwear scars that at least intersect with the defined surface were quantified as a pit or a scratch. Phase II crushing facets (9, 3 or 10n) were chosen as they correspond to the surface against which food is crushed. Thus, they are very informative as to dietary habits (Gordon, 1984; King et al., 1999). The power stroke in primates can be divided into two distinct phases: Phase I which is associated with a shearing motion, and Phase II which is associated with grinding (e.g., Kay, 1977). On the basis of the study of the jaw during Phase I and II activity, Wall et al. (2006) indicate Phase II movements may not be as significant for food breakdown as Phase I. Indeed, adductors experience lit-
tle activity during Phase II of chewing in primates. In this context, the legitimacy of microwear patterns on Phase II facets has to be reconsidered. Food breakdown on Phase II facets occurs principally at the end of Phase I movement (i.e., crushing during Phase I movement; Wall et al., 2006). Microwear patterns can therefore still reflect diet, as scratches and pits can still form on Phase II facets as a result of activity during Phase I. The comparison of microwear textures from three different primate taxa (Alouatta palliata, Cebus apella, and Lophocebus albigena) reaffirms initial findings about Phase II microwear patterns (Krueger et al., 2008). Despite the little activity during Phase II, microwear patterns on Phase II facets better distinguish taxa with differing diets than do those on Phase I facets (Krueger et al., 2008). Phase II crushing facets are therefore chosen in this study. Seven different variables were analyzed; the number of scratches (Ns), the length of scratches (Ls), the number of pits (Np), the number of wide scratches American Journal of Physical Anthropology
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(Nws), the number of large pits (Nlp), the percentage of pits (Pp), and the total number of scars including scratches and pits (Tot). The data were then analyzed with the software STATISTICA (version 8.0, StatSoft) and PAST (Paleontological Statistics; Hammer et al., 2001). Statistical analyses were applied to highlight potential intergroup differences in dental microwear patterns. As the conditions for using parametric tests were not fulfilled (i.e., normality and equality of variances), the data were rank transTABLE 4. Statistical tests carried out on extant taxa
Ns
Ls
Np
Nws
Nlp
Pp
Tot
Diet Taxon Error Total Diet Taxon Error Total Diet Taxon Error Total Diet Taxon Error Total Diet Taxon Error Total Diet Taxon Error Total Diet Taxon Error Total
(diet)
(diet)
(diet)
(diet)
(diet)
(diet)
(diet)
df
SS
MC
F
P
3 7 140 150 3 7 140 150 3 7 140 150 3 7 140 150 3 7 140 150 3 7 140 150 3 7 140 150
74424.9 139703.5 63200.9 286175.0 130593.1 28736.0 116408.3 286900.0 108431.9 117064.7 61864.6 286460.5 76043.6 45704.3 123697.3 255069.0 59785.0 69112.8 134116.8 273144.0 111312.1 127399.9 46769.8 286890.5 98287.7 98020.0 86497.8 286536.0
24808.3 19957.6 451.4
54.954 44.209
\0.05 \0.05
43531.0 4105.1 831.5
52.3532 \0.05 4.9371 \0.05
36144.0 16723.5 441.9
81.794 37.845
25347.9 6529.2 883.6
28.6886 \0.05 7.3897 \0.05
19928.3 9873.3 958.0
20.8025 \0.05 10.3064 \0.05
37104.0 18200.0 334.1
111.067 54.480
32762.6 14002.9 617.8
\0.05 \0.05
\0.05 \0.05
formed before each analysis (Sokal and Rolf, 1995). Three sets of analyses were performed. First, a nested analysis of variance was undertaken to compare extant taxa with differing diets (Tables 4 and 5). The nesting scheme included diet (i.e., four categories: leaf-, fruit-, insect-, and gum-dominated diet), and species at a subordinate level. Tukey’s honest significant difference (HSD) test was then performed to track sources of variation between dietary categories and species within dietary categories if needed (Tables 4 and 5). The second step consisted of comparing fossil populations (e.g., the Necrolemur population at La Bouffie, the Leptadapis population at Perrie`re, and so on)to extant species clustered by dietary category, using only the pertinent microwear variables (as shown by the first set of analyses). Single classification ANOVAs coupled with Tukey’s Honest Significant Difference (HSD) multicomparison test were used to pinpoint sources of significant variation (Tables 6 and 7). Observable inter-and intrapopulation differences in microwear patterns, reflecting potential variations in feeding habits, were explored through supplementary analyses. First, special attention was paid to betweenpopulation variations for three taxa: Leptadapis, Necrolemur, and Pseudoloris. Then, special attention was given to the Necrolemur population of La Bouffie (N 5 36), with the intention of investigating within-population variability. Indeed, in extant primates, diet can vary between and within populations, according to different factors such as resource availability, seasonal variation or even sex (Gautier-Hion, 1980; Teaford and Robinson, 1989). A simple plot representing the number of pits and scratches is used to explore dietary variability within the La Bouffie population of Necrolemur (Fig. 2).
RESULTS Extant taxa
53.0274 \0.05 22.6642 \0.05
Nested ANOVAs on extant species with different diets. The nesting scheme included four dietary categories: leaves, fruit, insects, and gums. Abbreviations: df: degrees of freedom; SS: Sum of Square; MS Mean Square; F: Fisher value; P: P-value. Abbreviations for microwear variables are as in Table 2.
The nested ANOVAs show that all microwear variables vary significantly between dietary categories (Tables 4 and 5). Leaf-eaters have a higher number of scratches (Ns) than fruit-eaters (Tables 3–5). These scratches are also longer than in fruit-eaters. Fruit-eaters have a higher number of pits (Np) than gum- and leaf-eaters. However, fruit-eaters display the most variability in
TABLE 5. Statistical tests carried out on extant taxa Leaf-dominated Leaf-dominated Fruit-dominated Insect-dominated Gum-dominated
Ns, Ls, Np, Nws, Nlp, Pp, Tot Ns, Np, Nws, Nlp, Pp, Tot Ns, Ls, Np, Nws, Nlp, Pp, Tot
Fruit-dominated
Insect-dominated
Gum-dominated
Ls, Nws, Pp, Nlp Ns, Np, Nws, Pp, Tot
Ns, Ls, Pp, Tot
Fruit-eaters
Microcebus murinus
Cheirogaleus major
Cheirogaleus medius
Eulemur fulvus
Microcebus murinus Cheirogaleus major Cheirogaleus medius Eulemur fulvus Perodicticus potto
Ns, Nlp, Pp, Tot Ns, Nws Np, Nws, Nlp, Pp, Tot Ns, Np, Pp, Tot
Ns, Nws, Pp, Tot Ns, Np, Pp Nlp
Ns, Np, Pp, Tot Ns, Ls, Np, Pp, Tot
Ns, Ls, Np, Nlp, Pp
Perodicticus potto
Tukey’s Honest Significant Difference multicomparison tests between dietary categories and between the taxa which have a fruitdominated diet. Abbreviations: df: degrees of freedom; SS: Sum of Square; MS Mean Square; F: Fisher value; P: P-value. Abbreviations for microwear variables are as in Table 2.
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ECOLOGICAL DIVERSITY OF EOCENE PRIMATES OF FRANCE their dental microwear patterns (Table 3). This is emphasized by the significant between-species differences within the fruit-dominated dietary category (Table 3). Insect-eaters are more difficult to distinguish from other dietary categories although on average they have a higher number of large pits and wide scratches than leaf and fruit-eaters. Leaf-eaters also tend to have lower numbers of large pits and wide scratches than other dietary categories. Gum-eaters have a small total number of microwear scars. The results of the analyses on extant strepsirrhines allow the inference of possible diets for fossil taxa. A low percentage of pits (Pp) discriminates leaf-dominated diets from other dietary categories. A high total number of microwear scars would then rule out the inference of a gum-dominated diet. A fruit-dominated diet will tend to correspond to a high Np. Discrimination between insect and fruit dominated diets can also be based on the Nws and the Nlp, which is higher in insect-dominated
diets. By contrast, a low Pp, confirmed by a high number of scratches, would point toward a leaf-dominated diet.
Fossil vs. extant taxa Statistical results show significant differences between extant and extinct taxa for all microwear variables (Table 6). Perrie`re. Leptadapis shows a significantly lower Pp and Np than extant fruit-, insect-, and gum-eaters (Table 7). This suggests that this primate did not belong to any of these dietary categories, which is confirmed by further differences (e.g., a higher Ns). Leptadapis from this locality was most probably a strict leaf-eater. Microchoerus has a significantly higher Pp than extant leaf-eaters.
TABLE 6. Statistical tests carried out to compare fossils to extant dietary clusters ANOVA Ns Ls Np Nws Nlp Pp Tot
Effect Error Effect Error Effect Error Effect Error Effect Error Effect Error Effect Error
df
SS
MS
F
P
19 281 19 281 19 281 19 281 19 281 19 281 19 281
1227100 1041717 1130797 1141739 1359189 910489 767519 1161017 901217 1166603 1465691 806771 1233408 1035510
64584 3707 59516 4063 71536 3240 40396 4132 47432 4152 77142 2871 64916 3685
17.4214
\0.05
14.6477
\0.05
22.0779
\0.05
9.7769
\0.05
11.4251
\0.05
26.8686
\0.05
17.6159
\0.05
Single ANOVAs on extant and fossil taxa. Fossil specimens, grouped by taxon and locality, are directly compared to extant taxa, which are clustered according to dietary categories (i.e., leaf-, fruit-, insect-, and gum-dominated diets).
Fig. 2. Plot of the number of scratches and pits for extant taxa, grouped by dietary category: leaves (green), fruit (red), gums (yellow), and insects (blue). La Bouffie fossil specimens (circles) were plotted after the polygons had been drawn.
TABLE 7. Statistical tests carried out to compare fossils to extant dietary clusters Leaf-dominated diet Perrie`re (Quercy, MP 17b) Leptadapis Microchoerus Ns, Pp Pseudoloris Ls, Np, Nws, Nlp, Pp La Bouffie (Quercy, MP 17a) Leptadapis Ns, Pp, Tot Necrolemur Ns, Np, Pp Pseudoloris Np, Nws, Nlp, Pp Tot Anchomomys Np, Pp Euzet (Gard, MP 17a) Leptadapis Ns, Pp Necrolemur Pp Fons 4 (Gard, MP 17a) Leptadapis Ns, Tot Microchoerus Ns, Np, Pp Lavergne (Quercy, MP 16) Necrolemur Ns, Np, Pp Pseudoloris Pp Robiac (Gard, MP 16) Adapis Necrolemur Ls, Nws, Nlp, Pp
Fruit-dominated diet
Insect-dominated diet
Gum-dominated diet
Np, Nlp, Pp, Tot Ns, Ls, tot Nws
Np, Nws, Nlp, Pp, Tot Ns, Nws, Nlp, tot Ls
Ns, Ls, Np, Nws, Nlp, Pp Ls, Nws, Nlp Ns, Tot
Ns, Np, Tot Ns, Nlp, Pp, Tot
Ns, Np, Nws, Tot Ns, Nws, Nlp, Pp, Tot
Ls, Np, Pp, Nlp, Tot Np, Tot
Np, Nws, Nlp, Tot Nws, Tot
Ns, Ls, Nws, Nlp, Pp Pp
Ls, Np, Nlp, Pp, Tot Ns, Tot
Np, Nws, Nlp, Pp, Tot Ns, Nws, Nlp, Tot
Ns, Ls, Np, Nws, Nlp, Pp Nws
Ns, Nlp, Pp
Ns, Nws, Nlp, Pp
Nws, Nlp
Ls, Np, Nlp, Pp, Tot Nws
Np, Nws, Nlp, Pp, Tot
Ns, Ls, Np, Nws, Nlp, Pp Ns, Pp, Tot
Nlp Ns, Tot
Tukey’s honest significant difference multicomparison test. Fossil specimens, grouped by taxon and locality, are directly compared to extant taxa, which are clustered according to dietary categories (i.e., leaf-, fruit-, insect-, and gum-dominated diets).
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Furthermore, Nlp and Nws are significantly lower than values seen in extant insect-eaters. Indeed, this taxon is too large to have been a strict insect-eater (760 g; Table 2). A diet based on fruit and maybe on gums can therefore be inferred for this primate. Pseudoloris, on the other hand, clearly distinguishes itself from leafeating taxa by its higher Pp. This primate also has a higher Tot than extant gum-eaters. Microwear results for this taxon are consistent with a diet based on insects and fruit, which is reasonable for a primate of such a small size (65 g; Table 2). La Bouffie. Leptadapis has a higher Pp and lower Ns than extant leaf-eaters, which would seem to argue against a leaf-dominated diet. Furthermore, this taxon has fewer pits than fruit-eaters (Tables 3, 6, and 7). Leptadapis also displays a lower Nws than seen in insectdominated diets, and is too large-bodied (3,200 g; Table 2) to depend on insects or gums alone. Hence, a mixed fruit and leaf diet can be inferred for this taxon. Necrolemur has a significantly higher Pp than leaf-eaters (Tables 3, 6, and 7), suggesting this taxon was not a leaf-eater. With the exception of its Nlp, Necrolemur does not significantly differ from present-day gum-eaters. Thus, this taxon most probably had a diet based primarily on gums, and perhaps supplemented by soft fruits. Results for Pseudoloris show a higher Pp than leaf-eaters, arguing against the hypothesis of a leaf-dominated diet. Its Tot is significantly higher than that of extant gum-eaters (Tables 3, 6, and 7). However, microwear results do not allow us to distinguish between a fruit- or insect-dominated diet. A mixed diet of insects and fruit can therefore be inferred for this primate. Only one specimen of Anchomomys showed any microwear. This specimen, however, presents a high Pp, Np, and total number of microwear scars, thus ruling out a diet based on gums or leaves (Table 3). This specimen may have had a mixed fruit- and insect-based diet. Euzet. Leptadapis has a lower Pp than fruit-eaters and gum-eaters but it is higher than the one found for present-day leaf-eaters (Tables 3, 6, and 7). Results point toward a mixed diet based on fruits and leaves, further confirmed by the low Nws and Nlp. For Necrolemur, Pp is significantly higher than values seen in extant leafeaters, arguing against the inference of a leaf-dominated diet. This taxon does not havea Pp that is significantly different to extant fruit or insect-eaters. However, this taxon also shows a lower Tot than extant insect-eaters. A diet based on fruits and supplemented by insects can thus be inferred for this taxon. Fons 4. The Pp and Np of Leptadapis are not significantly different from those of extant leaf-eaters. Therefore a leaf-dominated diet can be proposed for this species. However, this population of Leptadapis differentiates itself from leaf-eaters by its lower Ns and microwear results support a mixed diet based mainly on leaves and supplemented by soft fruit. Microchoerus shows a significantly lower Pp than extant leaf-eaters, suggesting it did not have a leaf-dominated diet. A low Nws and Nlp seem to rule out the possibility. Microwear results suggest a fruit- and gum-based diet. Lavergne. Necrolemur has a significantly higher Pp than extant leaf-eaters. This suggests it did not have a leaf-dominated diet, which is confirmed by a lower number of scratches than most extant leaf-eaters. It is distinguished from extant insect-eaters by a low Nws and Nlp. American Journal of Physical Anthropology
The diet of this taxon can thus be inferred as having been based on fruit and supplemented by gums. Pseudoloris has a higher Pp than most leaf-eaters, suggesting it was not a strict leaf-eater. This was actually to be expected due to its small size. Microwear results do not allow us to discriminate any further, as there are relatively few specimens. Robiac. Adapis exhibits a lower Pp than fruit, gum, and insect-eaters, thus suggesting these diets are extremely unlikely. Furthermore, the Ns is higher than values seen in fruit- gum-, and insect-dominated diets. Microwear patterns are more comparable to those of extant leaf-eaters, suggesting a leaf-based diet for this taxon. Necrolemur has a significantly higher Pp and Np than those of leaf-eaters (Tables 6 and 7). Microwear patterns display more scars than seen in gum-eaters, placing this taxon outside this category. Necrolemur is also significantly different from fruit-eaters in that it has fewer pits or wide scratches. An insect-dominated diet, possibly supplemented by fruit, can therefore be inferred for this taxon.
Fossil vs. fossil The final series of tests compares fossil groups (i.e., Leptadapis magnus, Necrolemur antiquus, Pseudoloris parvulus) from different localities. For the three groups, microwear variables vary significantly from one locality to another (Table 8). Such results are to be expected as similar between-population variation is well known and documented in extant mammals (e.g., Teaford and Robinson, 1989; Merceron et al., 2010). Leptadapis magnus. Microwear results underline dietary plasticity, with Leptadapis showing microwear patterns similar to those of extant folivores. Further analysis showed significant differences between localities in all microwear variables except the Nws (Table 8). As highlighted in the previous analysis, Leptadapis shifts from a mixed fruit- and leaf-based diet (La Bouffie, Euzet) to a strictly leaf-based one (Perrie`re). Ns is significantly higher at Perrie`re than the other localities, indicating the most heavy leaf-based diet of all the localities. On the other end of the spectrum, at La Bouffie, microwear patterns would correspond better to a fruit-based diet. Pp is significantly higher at this locality than at the others, suggesting that fruit was a larger part of the diet at La Bouffie. Fons 4 and Euzet correspond to intermediate microwear patterns. In these localities, Leptadapis would have integrated varying quantities of fruit and leaves, as suggested by the supplementary microwear results (Table 8). Necrolemur cf. antiquus. The previous analysis (i.e., fossil vs. extant taxa) pointed toward a diet shifting from soft fruit and gums to a more abrasive one based on insects. For Necrolemur, further results (Table 8) showed significant differences between localities in Np, Ns, Nws, and Nlp. No differences in scratch length were found. At La Bouffie, Necrolemur showed a higher Np and Pp than at Euzet and Fons 4, suggesting it incorporated more fruit at La Bouffie than at the two other localities. The Lavergne population of Necrolemur most likely had similar feeding habits to the population at La Bouffie. At Robiac, high Nws and Nlp could indicate a more abrasive diet than at any of the other localities. Indeed, this locality is the only one in which Necrolemur most probably had an insect-dominated diet. At Euzet, results
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209
TABLE 8. Statistical tests comparing the different localities df Nsa Ls Np Nws Nlp Pp Tot
Locality Error Total Locality Error Total Locality Error Total Locality Error Total Locality Error Total Locality Error Total Locality Error Total
3 34 37 3 34 37 3 34 37 3 34 37 3 34 37 3 34 37 3 34 37
Perrie`re La Bouffie Euzet Fons 4
Ns, Ls, Np, Nlp, Pp Ns, Np, Pp Ns, Pp df
Nsb Ls Np Nws Nlp Pp Tot
Locality Error Total Locality Error Total Locality Error Total Locality Error Total Locality Error Total Locality Error Total Locality Error Total
La Bouffie Euzet Robiac Lavergne
3 46 49 3 46 49 3 46 49 3 46 49 3 46 49 3 46 49 3 46 49
Ls Np Nws
SS 5903.47 4449.53 10353.00 1199.44 9210.56 10410.00 6073.93 4263.57 10337.50 3410.83 5636.17 9047.00 5512.03 3187.97 8700.00 6786.57 3618.43 10405.00 3620.42 6675.58 10296.00 La Bouffie
Ns, Np, Nlp, Pp, Tot Ns, Np, Nws, Nlp, Pp, Tot df
Nsc
SS 3046.00 1496.50 4542.50 2201.15 2368.35 4569.50 3390.33 1137.17 4527.50 440.14 1863.86 2304.00 826.35 2405.15 3231.50 3496.83 1071.17 4568.00 1524.61 3020.39 4545.00 Perrie`re
Locality Error Total Locality Error Total Locality Error Total Locality Error Total
2 16 18 2 16 18 2 16 18 2 16 18
SS 308.550 257.950 566.500 60.550 509.450 570.000 205.938 359.063 565.000 156.1375 386.3625 542.5000
F
P
1015.33 44.01
SC
23.0681
\0.05
733.72 69.66
10.5332
\0.05
1130.11 33.45
33.7890
\0.05
146.71 54.82
2.6763
[0.05
275.45 70.74
3.8939
\0.05
1165.61 31.51
36.9975
\0.05
508.20 88.84
5.7207
\0.05
La Bouffie
Euzet
Fons 4
Ns, Ls, Pp, Tot Ns, Ls, Np, Pp
Np, Pp, Tot
SC
F
P
20.3437
\0.05
1967.82 96.73 399.81 200.23
1.99677
[0.05
2024.64 92.69
21.8440
\0.05
1136.94 122.53
9.2793
\0.05
1837.34 69.30
26.5114
\0.05
2262.19 78.66
28.7586
\0.05
1206.81 145.12
8.3159
\0.05
Euzet
Robiac
Lavergne
Nws, Tot Np, Nlp, Pp SC
Ns, Np, Nws, Nlp, Pp F
P
154.275 16.122
9.56930
\0.05
30.275 31.841
0.95083
[0.05
102.969 22.441
4.58834
\0.05
3.23297
[0.05
78.0688 24.1477
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A. RAMDARSHAN ET AL. TABLE 8. (Continued)
Nlp Pp Tot
Locality Error Total Locality Error Total Locality Error Total
df
SS
SC
F
P
2 16 18 2 16 18 2 16 18
79.3458 466.1542 545.5000 176.071 393.429 569.500 382.2375 183.2625 565.5000
39.6729 29.1346
1.36171
[0.05
88.035 24.589
3.58023
[0.05
191.1188 11.4539
16.68590
\0.05
La Bouffie
Lavergne
Perrie`re Perrie`re La Bouffie Lavergne
Ns, Tot Pp
Single ANOVAs coupled with Tukey’s honest significant difference multicomparison test for: a Leptadapis (La Bouffie, Euzet, Fons 4, and Perrie`re). b Necrolemur (La Bouffie, Euzet, Robiac, and Lavergne). c Pseudoloris (Lavergne, La Bouffie, and Perrie`re).
point toward an intermediate diet, which was not as soft as at La Bouffie, but not as abrasive as at Robiac. Although microwear results indicate an overall fruitand gum-based diet at La Bouffie, there seems to be a wide dietary spectrum within the Necrolemur population there (Fig. 2). Indeed, the microwear variables overlap different dietary categories, underlining the dietary plasticity for this population. Rather than being confined to a mainly fruit-based diet, Necrolemur may have incorporated other elements into its diet, such as gums or, to a smaller extent, insects. Pseudoloris parvulus. Extant vs. fossil statistical results indicate a fruit- and insect-based diet for each locality. For this small primate, further tests highlighted few significant differences (Table 8). The La Bouffie population presents a higher Np than at Perrie`re, suggesting fruit could have possibly played a larger part in its diet at La Bouffie than at Perrie`re. However, the differences found are very small in magnitude. Furthermore, interpretations at Lavergne are based on a small number of specimens (N 5 2) and should therefore remain extremely cautious.
DISCUSSION Extant taxa According to statistical tests, the four dietary categories used in this study are significantly different from one another. The main differences include a higher Ns in leaf-eaters and a low Tot in gum-eaters. Pp can also be indicative of a fruit- or of a leaf-dominated diet (a high vs. low Pp). The differences between leaf- and fruit-eating primates have been abundantly recorded for extant primates (e.g., Teaford and Walker, 1984; Teaford and Runestad, 1992; Merceron et al., 2005). Results from this study are consistent with previous studies, underlining the pertinence of this method for distinguishing between dietary categories. Leaf-eaters are easily characterized by a low Pp and high Ns. Insect-eaters show a high Tot, and further indications can include a high Nws and Nlp. Such results are consistent with previous studies (Strait, 1993a). Gum-dominated diets were considered separately, as the physical properties of gums are very different from those of fruits. For the first time, differences between gum-eatAmerican Journal of Physical Anthropology
ers and fruit-eaters can be detected based on the molar microwear patterns. The total number of microwear scars is much lower in extant gum-eaters than in extant fruit or insect-eaters. Although no studies have considered the physical properties of gums, it seems reasonable to infer that soft gums are much too soft to scar enamel. This could explain the low values. However, the amount of large pits and wide scratches seems intriguing. Soft gums are most probably too soft to scar enamel, but some primates also feed on dried, hardened gums that have had enough time to incorporate extraneous particles such as dust and grit. Such elements could explain the microwear patterns seen in extant gum-eaters. Otolemur and Euoticus, the two gum-eaters of the database, use similar harvesting method to obtain their preferred food source. They are both ‘‘scrapers’’, i.e., they harvest the gum produced in reaction to insect infestations in trees (Burrows and Nash, 2010). As such, they do occasionally feed on hardened gums (Ravosa et al., 2010). They scrape the gum off the tree bark in contrast to gum-gougers, which actively puncture the tree bark with their lower jaw to activate the flow of exudates. However, Euoticus does also engage in gum gouging (Burrows and Nash, 2010). Euoticus elegantulus accomplishes this with the help of its caniniform premolars (Charles-Dominique and Petter, 1980; Stephenson et al., 2010). As such, some harder exogenous particles can be expected to end up at the level of the molars during mastication. Another point to consider is that, although some primates feed extensively on gums, it does not provide all the necessary nutrients for a complete diet (Power, 2010). Gum-eating primates need to complete their diet with other resources, like insects or fruit, which would have the physical properties necessary to scar enamel. A more extensive study on the dental microwear of gum-eating primates needs to be carried out. It would be of great interest to look for a signature wear pattern on the anterior teeth, which are instrumental for gouging into wood (Nash and Burrows, 2010; Rosenberger, 2010). This study has highlighted an important disparity among the results for fruit-dominated diets. Some variables, such as Ns or Np, yield wide ranges of data and provide overlapping dietary signals. The formation of microwear scars depends directly on the physical properties of the food consumed. Some fruit-eaters will prefer
211
ECOLOGICAL DIVERSITY OF EOCENE PRIMATES OF FRANCE
Fig. 3. Paleoenvironment and summary of the proposed diets for each locality. Paleoenvironment is inferred from the cenograms of each locality (Fig. 1, Legendre, 1989).
soft mature fruits, which might not possess the physical characteristics necessary to scar enamel. Moreover, fruiteaters supplement their diet with other foods, such as leaves or insects. Dental microwear patterns will then reflect the physical properties of these secondary components, rather than a mainly fruit-based diet. For example, Eulemur does prefer fruit but heavily supplements its diet with mature leaves throughout the year (Overdorff, 1993). This could explain the high number of scratches seen in this taxon. Microcebus has a very diverse fruit-based diet, which is supplemented by eating insects (Lahann, 2007) depending on the season and resource availability. A certain amount of insects in Microcebus’ diet could then explain the high number of large pits, wide scratches and total number of microwear scars highlighted by this study. Another example is Perodicticus. This species prefers soft fruit and supplements its diet with gums, exudates and insect secretions (Oates, 1984). These foods are not hard enough to scar enamel, explaining the low number of microwear scars for this taxon. This study emphasizes the dietary diversity among extant strepsirhine fruit-eaters.
Fossil taxa A summary of the inferred diets for each taxon at each locality is presented in Figure 3. Comparisons between previous dietary reconstructions and the results provided by this study are summarized in Table 9. Necrolemur cf. antiquus. We can consider two main sources of dietary variability: (i) Interpopulation difference which can be due to spatial heterogeneity in food resources and competition with sympatric species. (ii) Intrapopulation variations which can be due to sex and seasonal factors influencing resource availability. Fossils
TABLE 9. Inferred diets for fossil taxa: previous dietary assessment compared to results provided by this study Taxon
Previous dietary reconstructions a
This study
Adapis sudrei Anchomomys quercyi Leptadapis magnus
Leaves Insectsa
Robiac La Bouffie
Leaves Fruit/Insects
Leavesb
Microchoerus erinaceus Necrolemur cf. antiquus
Fruitc
La Bouffie Fons 4 Euzet Perrie`re Fons 4 Perrie`re Robiac Lavergne Euzet La Bouffie Lavergne La Bouffie Perrie`re
Fruit/Leaves Leaves (Fruit) Leaves (Fruit) Leaves Gums/Fruit Gums/Fruit Insects (Fruit) Gums/Fruit Fruit (Insects) Gums/Fruit Fruit/Insects Fruit/Insects Fruit/Insects
Pseudoloris parvulus
Fruitc
Insectsc
Previous dietary assessments are from: a Fleagle, 1999; Szalay and Delson, 1979. b Gingerich, 1972, Gingerich, 1981; Gingerich and Martin, 1981; Szalay and Delson, 1979; Covert, 1985, Covert, 1986; White, 2006. c Strait, 2001.
at each locality certainly represent multiple seasons, as these primates are supposed to have died at different moments of the year, over a number of years (e.g., Behrensmeyer, 1982; Vianey-Liaud and Legendre, 1986). As such, the fossil sample at each locality could reflect the effects of seasonality. However, samples at most of the localities are too small (N 10) to properly interpret intrapopulation variation. American Journal of Physical Anthropology
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Microwear patterns at Robiac are characterized by a high pitting that may reflect insect predation, a diet which may have been supplemented by fruit. This hypothesis is coherent for such a small primate (285 g; Table 2). These results contrast with shearing quotients (Strait, 2001), which seem to point toward fruit-eating. Necrolemur does not present the long, sharp crests that are usually associated with extant insect-eating species. These crests help perforate and reduce the chitinous tissues of insects, which are otherwise difficult to cut. As such, Necrolemur’s teeth do not share such morphology. However, tooth morphology might reflect the physical properties of food (Strait, 1997) and different insects have different physical properties. For example, caterpillars may be described as ‘‘soft-bodied’’ insects as opposed to ‘‘hard-bodied’’ insects such as beetles. Based on the study of extant species, short molar blades allow the load to be concentrated, thus facilitating the fracture of brittle foods such as a beetle (Strait, 1997). Long blades will slice through ductile soft foods with ease. As such, shearing crests will not be as well developed in eaters of hard-bodied insects as they are in eaters of soft-bodied ones (Strait, 1993b; Lucas, 2004). This could explain slightly low shearing values (Strait, 2001), especially as insects do not seem to be the only component of Necrolemur’s diet. Although a previous microwear study has been able to separate hard-bodied insectivores from softbodied ones (Strait, 1993a), the sample used in this study did not allow us to distinguish between the two categories. In the other localities, Necrolemur has a diet based mainly on fruit. This illustrates a degree of plasticity in the diet of this small-bodied primate. Both Robiac and La Bouffie were closed tropical rainforests (Legendre, 1987, 1988) (Fig. 2), so this shift in diet does not seem related to major differences in the environment in which these primates lived. At Robiac, the insect- and fruit-eating Necrolemur is the only small-bodied primate. At other localities, fruit-eating Necrolemur occurs with other primates such as Pseudoloris and Anchomomys. The small size of both these primates indicates they would have at least supplemented their diet with insects, and microwear results support a mixed fruit and insect diet for both Pseudoloris and Anchomomys. In extant taxa, competition between taxa can influence diet (Janson and van Schaik, 1988). Each primate occupies a specific niche in the primate community. As resources are inevitably limited, sympatric taxa cannot occupy identical ecological niches (Ganzhorn, 1988). In this case, Necrolemur would seem to avoid further competition with other small-bodied primates by slightly shifting its diet toward fruit, and gums as in the case of La Bouffie. Insects seem only to be the main constituent of Necrolemur’s diet when there are no other insect-eating primates at the same locality. At La Bouffie, the only locality with a large sample of Necrolemur there is evidence of a broad dietary spectrum. As such, these primates might have relied on different food sources, possibly exudates and fruit (Fig. 2). Fruit can have a patchy distribution throughout rainforest environments, and can also be available only at certain moments of the year (Terborgh and Schaik, 1987; van Schaik et al., 1993; Fleagle, 1999). Exudates and gums constitute a more constant resource, which is less susceptible to seasonal variations than other foods (Nash, 1986; Power, 2010). Although often grouped within ‘‘fruit-eating,’’ eating gums or other American Journal of Physical Anthropology
plant exudates implies a different set of adaptations and foraging strategies. It is a resource rarely used by mammals, therefore its exploitation by certain species of primates could confer a competitive advantage (Nash, 1986). Gums and exudates could have constituted a fallback resource for Necrolemur. If Necrolemur had really included gum in its diet then this would have allowed this species to differentiate itself from the other smallbodied primates of La Bouffie. Indeed, none of the others seem to have consumed gums. Necrolemur shows other characteristic anatomical features, notably in its anterior dentition. Wear patterns on microchoerid incisors indicate a combined grooming and feeding function (Schmid, 1983). Gum-eating is also more commonly seen in nocturnal small bodied primates (Burrows and Nash, 2010), a description likely fitting of Necrolemur (Kay and Kirk, 2000; Ross et al., 2007). The other potential source of variation is the effect of seasonal food abundance and quality. The effects of seasonality could explain the existence of two different diets among the Necrolemur specimens at La Bouffie. This karstic locality is one of the many fissure fillings of the Quercy region of France. Over the years, these fillings have provided numerous rich and diverse mammalian faunas which have been studied in great detail (e.g., for a summary, see Legendre et al., 1997). Based on these faunas and their uniformity, previous studies have established that the karsts were probably filled over a relatively short window of time (e.g., Vianey-Liaud and Legendre, 1986; Sige´ and Legendre, 1997). Although the scale of time averaging cannot be determined in this assemblage, it seems reasonable to assume that it could be small enough to enable the detection of short-term variability (i.e., seasons, years). Teaford and Robinson (1989) focus on the effects of seasonality on the diet of different populations of Cebus in South America. The study finds no difference in microwear patterns between seasons in humid tropical environments, only in the drier tropical sites with a more marked seasonality. Although differences in the Necrolemur population at La Bouffie are small in magnitude, they are reliably detected. The environment at La Bouffie might have been seasonal, but no other data collected from this site would suggest the existence of a drier season (Legendre, 1988). In their study, Teaford and Robinson (1989) found differences in microwear patterns according to the amount of rainfall. This could also explain results at La Bouffie. Although gums are less susceptible to seasonal variations, some factors, in particular moisture, can influence patch size and renewal rates (Nash, 1986). Differences in the amount of rainfall from one month to another, or even from one year to another, could then explain the different diets found among the Necrolemur specimens at La Bouffie. Leptadapis magnus. Most previous studies suggest Leptadapis taxa was a leaf-eater (e.g., Gingerich, 1972, 1981; Szalay and Delson, 1979; Gingerich and Martin, 1981; Covert, 1985, 1986; White, 2006) based on cranial and dental morphology and also according to body weight. Our study broadly confirms these previous dietary interpretations, although Leptadapis does not appear here to have been a strict leaf-eater. It shifts from a mixed fruit and leaf diet in La Bouffie and Euzet to a strictly leaf-based one in Perrie`re. In each locality, Leptadapis is the only large-bodied primate. Interspecific competition is therefore much less likely to be the main
ECOLOGICAL DIVERSITY OF EOCENE PRIMATES OF FRANCE cause of the variation between localities. However, paleoenvironmental conditions, as estimated by Legendre (1987, 1988) are not the same in each locality. At La Bouffie, cenograms indicate a primary rainforest environment (Legendre, 1987). Euzet and Fons correspond to more open secondary forest environments (Legendre, 1988). In these localities, Leptadapis most probably had a diet based on leaves and fruit. On the other hand, Perrie`re, in which Leptadapis was most probably a strict leaf-eater, corresponds to an open wooded savannah environment (Legendre, 1988). Furthermore, marked seasonality has also been proposed for the Quercy region during the Late Eocene (Legendre, 1988). In this case, Leptadapis seems to increase the degree of leaf-eating in response to cooler and drier seasons and environments, where fruit becomes less common throughout the year. This taxon shows a degree of plasticity, shifting its diet according to its living conditions. Other dietary habits have been proposed for Leptadapis. Gingerich and Martin (1981) suggest that the dentition of Adapis-Leptadapis resembles the short-tusked morphology of gum-gouging marmosets. However Leptadapisdoes not have any of the usual cranial features characterizing gum-eating (Perry, 2008; Rosenberger, 2010). Furthermore, Leptadapis is too large-bodied to depend on exudates as an energy source. Lane`que (1993) proposes a different hypothesis wherein smaller individuals might have occasionally supplemented their diet with insects. Once again, microwear patterns on Leptadapis disprove the insect predation hypothesis. However, our dental microwear analysis supports Perry’s hypothesis (2008), namely the consumption of tough fruits. Indeed, based on the anatomy of the masticatory process, Perry (2008) concludes Leptadapis has a strong bite force but did not have a wide gape. He then proposes a diet based on tough foods such as mature leaves and small fruit with tough rinds. To sum up, Leptadapis most probably preferred leaves as its main food resource although fruit was a large part of its diet, especially in a tropical rainforest environment where fruit would have been much more common throughout the year. This plasticity, i.e., going from leaf- to fruit-eating habits, makes Leptadapis most likely capable of surviving in more open and drier environments, such as Perrie`re, and shifting its diet according to the different environmental conditions. A last hypothesis that may explain the difference in diet is sexual dimorphism. Indeed, it has been shown in extant mammals (Merceron et al., 2010) that microwear patterns can record differences in feeding preferences between sexes. Differences in morphology among largebodied adapoids have been explained by sexual dimorphism (e.g., Gingerich, 1981). Among extant primates, differences in diet can be observed between males and females of the same species (Gautier-Hion, 1980). These have been associated with their different dietary needs. For example, energy requirements can be higher for a female during lactation than at other times of the year (Lee, 1996). In some extant cercopithecoids, differences in diet between males and females are as important as between different species (Gautier-Hion, 1980). The presence of males and females in the studied populations could explain the significant differences highlighted by the statistical analyses. Sexual dimorphism has however been questioned by Godinot (1992) and Lane`que (1993), who support the view that multiple taxa occur within
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Leptadapis in the Quercy fissure fillings. Analysis of post-cranial remains also supports the existence of multiple large-bodied adapoid taxa (Bacon and Godinot, 1998; Godinot, 1998). If this is the case, each separate taxon may have shown no, or at least a very low level of, sexual dimorphism. In this context, one question arises: how would competition between these species have been limited? These taxa were likely all diurnal and of similar size. Diet may have been a factor limiting ecological overlap, but this question remains unresolved. Pseudoloris parvulus. Results indicate a diet primarily based on insects, which is consistent with previous dietary interpretations (Covert, 1986; Fleagle, 1999; Strait, 2001). Microwear results vary very little, if at all, between the different localities, indicating this taxon was confined to a narrow ecological niche throughout its occurrence at these localities, i.e., from MP 16 to MP 17b. Pseudoloris’s diet does not seem to have varied depending on its environment, as diet remains similar at localities such as La Bouffie and Perrie`re which correspond to a closed tropical rainforest and a more open environment, respectively. Diet does not seem to vary according to the competition that might have occurred within each primate community either. Indeed, Pseudolorisis inferred to have been an insect-eater whether it occurs with Necrolemur, or Anchomomys, or even if it is the only small-bodied primate in the community. Interspecific competition does not then seem to have influenced its diet in any considerable way. In this context, Pseudoloris appears as a very specialized primate, constant throughout an occurrence spanning the longest period of time considered here, i.e., from MP 16 to MP 17b. This taxon is also the only one to occur from MP 16 right up to the Eocene-Oligocene transition, and is the last primate to disappear from the European fossil record at that time. Further investigations need to be carried out to establish whether its diet remained constant right up to the Eocene-Oligocene transition, but also whether or not this ecological specialization had an influence on this taxon’s longevity in the fossil record.
CONCLUSION For the first time, dental microwear analysis has allowed a snapshot of the dietary range of a single species of fossil primates. For example, although Necrolemur can be considered as having had a fruit-dominated diet, this taxon was most capable of shifting its diet according to the strength of the competition for food resources. Indeed, this study revealed a diet shifting from being insect-dominated to being fruit- and gumdominated. Similarly, Leptadapis, considered to have a leaf-dominated diet, appears to have shifted its diet toward fruit-eating depending on the environment and the available resources. On the other hand, Pseudoloris parvulus seems to have had a fairly constant diet (based on insects and fruit) throughout the localities considered in this study. This study highlights the importance of considering the full dietary range of each species. Some taxa show more variability in their diets than others, which could imply a greater capacity to cope with changing environments. For example, such a capacity could theoretically confer an advantage to the Primates of the Late Eocene, in the midst of the climatic variations approaching the Eocene–Oligocene transition. Further studies need to be carried out to determine whether or not the primates American Journal of Physical Anthropology
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occurring in the latest Eocene are the ones showing the greatest plasticity in their diet. Although Leptadapis shows a degree of plasticity in its diet, this taxon does not occur in the later MP 18 and 19 localities. Further lines of research need to compare Leptadapis to other large-bodied adapines such as Adapis or even Cryptadapis.
ACKNOWLEDGMENTS The authors thank C. Zollikofer, M. Ponce de Le´on (Anthropological institute in Zurich) and J. Cuisin (Muse´um National d’Histoire Naturelle) for access to their collections and permission to cast extant specimens. They gratefully acknowledge A. Prieur (Collections de Ge´ologie de l’Universite´ Claude Bernard Lyon 1, UMR 5276 Terre, Plane`tes, Environnement) and L. Costeur (Natural History Museum of Basel) for access to the fossil specimens of Euzet. They express their appreciation to the two anonymous reviewers and the associate editor for their helpful comments. They also thank A.-L. Charruault, B. Marandat, and S. Jiquel for their help with this study. This is publication no. 2011-144 of the ´ volution de Montpellier’’ ‘‘Institut des Sciences de l’E (ISE-M, UMR-CNRS 5554).
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