The diet ofMyotragus balearicusBate 1909 (Artiodactyla: Caprinae), an extinct bovid from the Balearic Islands: evidence from coprolites

Biological Journal of the Linnean Society (1999), 66: 57–74. With 6 figures Article ID: bijl 1998.0260, available online at http://www.idealibrary.com on

The diet of Myotragus balearicus Bate 1909 (Artiodactyla: Caprinae), an extinct bovid from the Balearic Islands: evidence from coprolites JOSEP ANTONI ALCOVER1∗, RAMON PEREZ-OBIOL2, ERRIKARTA-IMANOL YLL2 AND PERE BOVER1 1

Institut Mediterrani d’Estudis Avanc¸ats (CSIC-UIB), Cta. de Valldemossa km 7,5, 07071 Ciutat de Mallorca, Balears, Spain; 2Departament de Biologia Animal, Biologia Vegetal i Ecologia, Unitat de Bota`nica, Universitat Auto`noma de Barcelona, 08193 Bellaterra, Barcelona, Spain Received 17 March 1998; accepted for publication 20 June 1998

Myotragus balearicus Bate 1909 is an artiodactyl Caprinae endemic to the Balearic Islands which became extinct more than 4000 years ago. Coprolites produced by this species have been collected from the excavation of Holocene cave sediments in Cova Estreta (Serra de Tramuntana, Mallorca). The pollen content of several samples of coprolites has been studied in order to determine the diet of Myotragus. Myotragus balearicus from Cova Estreta was a browser, and consumed huge amounts of box, Buxus balearica, a plant known for its high content of steroidal alkaloids. The coprolites are very fine textured, probably due to the result of a very efficient digestive process.  1999 The Linnean Society of London

ADDITIONAL KEY WORDS:—Holocene – fossil ruminants – cave sediments – diet – Buxus balearica. CONTENTS

Introduction . . . . Material and methods Results . . . . . Discussion . . . . Acknowledgements . References . . . .

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INTRODUCTION

Myotragus balearicus is a fossil ruminant only known from some of the Balearic Islands (Mallorca, Menorca, Cabrera and Sa Dragonera, western Mediterranean) ∗ Corresponding author. E-mail: [email protected] 0024–4066/99/010057+18 $30.00/0

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 1999 The Linnean Society of London

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Figure 1. Myotragus balearicus Bate 1909. Cova C-2, Menorca (Balearic Islands). Collection Museu de la Naturalesa de les Illes Balears, [acronym: MNCM]. A: MNCM 39076, skull in lateral view. B: MNCM 59241, jaw in labial view. Scale bar = 5 cm.

since the beginning of the century (Bate, 1909). It is a very unusual Caprinae (Fig. 1) originating through an insular evolutionary process (Alcover et al., 1981). It is one of the smallest Caprinae known, at least with regard to body height. It reached approximately 45 cm at the shoulder in adult specimens; however, skeletons of adults of only c. 25 cm are known. The weight estimated by different authors for adult specimens varies between 6 kg (minimum estimate provided by Waldren, 1982) and 60 kg (maximum estimate provided by Ko¨hler, 1993). Spoor (1988) calculated that the weight of adults was between 30 and 40 kg for specimens of Wu¨rmian age (last

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ice age), whereas the Holocene specimens weighed between 20 and 30 kg. Our estimates, based on the width of the diaphyses of the larger skeletal elements (Scott, 1983), assign a weight to adult specimens of Myotragus balearicus (for different ages) of between 13 and 20 kg for the smallest adult specimens and between 50 and 70 kg for the larger specimens. The phylogenetic relationships of Myotragus are still not clearly understood. Usually (since the work by Andrews, 1915; see also Gliozzi & Malatesta, 1980) it has been related to Nemorhaedus and Capricornis (and consequently it would be also related to the recently described Pseudoryx; see Thomas, 1994). The first two genera were classically related to Rupicapra and Oreamnos and were included with the former in the Rupicaprini tribe (see Simpson, 1945). Further approaches (Gentry 1978, 1980, 1992; Gliozzi & Malatesta, 1980; Hartl et al., 1990; Thomas, 1994; Groves & Shields, 1996; Gatesy et al., 1997) have questioned the monophyly and recognition of the Rupicaprini and Caprini by Simpson (1945). Therefore, it seems at present prudent to include Myotragus exclusively within the Caprinae subfamily until new studies shed light on the tribal relationships within it. The ancestors of Myotragus balearicus Bate 1909 presumably colonized the Balearic Islands during the Messinian (Alcover et al., 1981), when the western Mediterranean dried up (between 5.7 and 5.35 million years ago; Gautier et al., 1994), and developed under isolated conditions, since the end of Messinian (5.35 million years ago) when the islands became isolated. The first human inhabitants lived alongside Myotragus balearicus for several thousand years, until the latter species became extinct for unknown reasons slightly more than 4000 years ago (Waldren, 1982; Guerrero, 1996). Myotragus balearicus, the terminal species of the lineage, is an atypical animal which presents many apomorphies in its skeleton. It is characterized by, among other features, an extremely modified dentition together with a very peculiar cranial morphology (Bate, 1909; Andrews, 1915). In fact, M. balearicus, unlike any extant ruminant, has a single continuously growing incisor, with an open root, in each lower jaw. The premolar series is very reduced, the dental formula for an adult being 0/1, 0/0, 2/1, 3/3. Its molar teeth are very hypsodont, to such an extent that in younger specimens the M1–2 roots distort the ossification of the base of the ramus. Myotragus balearicus does not share these dental characteristics with any other known Caprinae. This type of dentition suggests an abrasive character for the vegetation which presumably made up the diet of Myotragus balearicus (Alcover et al., 1981, Marcus, in press), although it does not shed light on the actual items consumed. Dental evolution towards the acquisition of extremely hypsodont molar teeth, a shortened premolar series and evergrowing incisors shows its clearest parallelism, although to a lesser extent, with Maremmia (Hurzeler, 1983), which surprisingly is another insular endemic form. On the other hand, it is well known that Nesogoral melonii from the Pliocene-lower Pleistocene of Sardinia had very hypsodont cheek teeth. However, its incisors are unknown (Gliozzi & Malatesta, 1980). The general configuration of the jaw of Nesogoral melonii is similar to that of earlier species of Myotragus and also to that of Maremmia haupti. Nesogoral melonii probably lacked continuously growing incisors, although the incisors were probably hypsodont. The exclusive presence of these taxa with hypsodont molar teeth and incisors in the Mediterranean islands makes one speculate about the existence of a (causal) relationship between insular Mediterranean conditions and the evolution of this peculiar dentition. These features are recognized in insular bovids of the Mediterranean area

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(both Caprinae and Alcelaphinae), but not Bovinae (genus Bubalus) of the islands of the australo-oriental intercontinental mega-archipelago. The unusual morphology of Myotragus balearicus has aroused speculations concerning its diet. In parallel, there has been speculation on its role within the insular ecosystems of the Balearic Islands ( Juniper, 1984) and in the origin of the Balearic flora (Delvosalle & Duvigneaud, 1968). Several authors have commented on the diet and the functional fitness of the dentition of Myotragus (Freudenberg, 1914; Andrews, 1915; Angel, 1966; Leinders, 1977). For other mammalian orders, increase in the degree of hypsodonty of the molar teeth was related to feeding on grasses (see, for example, Peyer, 1968; Chaline & Mein, 1979). Proposed alternative diets—grasses, lichens, mosses, prickly plants or bulbs—are too speculative to be considered as an indication of what the diet of the Myotragus balearicus actually was. On the other hand, the fact that Myotragus balearicus lived under insular conditions implies that particular adaptations to the isolated environments of the pre-human Balearic Islands were to be expected. It is known that specialized trophic adaptations frequently evolved on the islands, sometimes without stated parallelisms with continental ecosystems. Herbivory on the islands, as is the case with other trophic strategies (e.g. Alcover & McMinn, 1994), frequently does not correspond to that observed on the continent. In different islands of the world there are endemic herbivores, both extant or recently extinct, which present particular trophic adaptations. Analysis of the diet of the insular herbivores has been complicated by the fact that many of these insular herbivore species have become extinct. However, there is abundant documentation that the diet of the insular herbivore species was frequently unusual. Among the numerous known cases could be mentioned the moa-nalos from Hawaii, the dwarf hippopotamus from Cyprus and several lemurs from Madagascar. Moa-nalos (Thambetochen sps.) are flightless Anseriformes of large size, which apparently consumed great amounts of ferns ( James & Burney, 1997). Birds which consume ferns are rare and James & Burney (1997) have recently revised their record, with the result that most species that include ferns in their diet are insular. Phanourios minor, the dwarf hippopotamus from Cyprus, had a rather modified dentition, which reveals that unlike the extant Hipopotamidae and their ancestors it was a browsing rather than a grazing species (Boekschoten & Sondaar, 1972). Lemurs from Madagascar present rather varied trophic adaptations, especially when considering the diet of different extinct species. As a particular case, the diet of several extant lemurs of the Hapalemur genus can be mentioned; these eat cyanogenic plants with a concentration of cyanides up to 12 times the lethal dose for human beings (Glander et al., 1989). Thus, if in addition to the atypical character of the dentition of the Myotragus balearicus we consider that the species developed and lived in isolated conditions, its diet can be expected to be peculiar. The study of the coprolites of Myotragus balearicus provides relevant information on the diet of an extinct species. At the same time it provides first-hand information on the vegetation with which Myotragus interacted. The recent finding of the deposit in Cova Estreta (Encinas & Alcover, 1997) has allowed us to obtain many coprolites of this species found in an excellent state of preservation. Finds of coprolites of Myotragus balearicus have also been reported previously in Abric de Son Matge (at least two levels of coprolites, possible indicators of confined animals; Waldren, 1982) and in a cave in s’Arenal

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(materials possibly from the Wu¨rm; see Cuerda, 1975). During the present study it was observed that the coprolites from Abric de Son Matge were oxidized, whereas those from s’Arenal were totally mineralized, and neither therefore contain determinable organic material.

MATERIAL AND METHODS

Coprolites of Myotragus balearicus were collected during three excavation campaigns carried out between May 1996 and September 1997 from the sediments in Cova Estreta, in the municipal boundary of Pollenc¸a, Mallorca (Encinas & Alcover, 1997). Coprolites are found on the upper levels of the sedimentary deposit, from the surface down to a depth of 70 cm. Up to now, the deposit has produced more than 10 000 bones of Myotragus balearicus which correspond to more than 110 individuals. Remains of the bones of two adult sheep (Ovis aries) have been found on the surface of the deposit, together with those representing not less than four neonate suckling Ovis lambs. The stratigraphic location of the coprolite samples was precisely recorded. Several thousand coprolites were obtained and placed in plastic bags corresponding to the depths of the different grids. The coprolites studied in this work were obtained during May and September 1996. An initial sample corresponded to grid square M4. In this grid, at the surface level, well preserved coprolites were found, mixed with bones of Myotragus balearicus and Hypnomys morpheus. From a morphological point of view, these coprolites differ from those of goat and sheep, the only other medium-size artiodactyls present in the area. It is well known that dung pellets produced by cervids and most bovids present few apparent morphological differences (Mead et al., 1986; Mead & Agenbroad, 1992). Sheep and goat dung pellets are usually smaller than those of Myotragus, and their shape is not usually so cuboid-cylindrical subrectangular, but rather more ovoidal. Inside Cova Estreta, on the superficial layer, mixed with the coprolites of Myotragus balearicus, several dung pellets of Ovis aries have been found, along with bone remains of a few specimens. In order to carry out the present study coprolites which presented no doubt about their origin were selected. The results from the analyses confirm that they do not correspond to either Ovis aries or Capra hircus, since they all contain plants which are not found at present in the area. Two dates for one of the coprolite sets (located in the M4 grid) have been obtained. The first date (Utrecht University, laboratory number: Utc 5171) corresponds to a femur of Myotragus balearicus (Museu de la Naturalesa de les Illes Balears, collection number: MNCM 54422) with a 14C age of 5720±60 BP (1r: cal BC 4676–4640, 4618–4468). This femur was found on top of the coprolites studied. The second date (Laboratory number: Utc 5175) corresponds to a bone of Hypnomys morpheus (collection MNCM, without number), found mixed with the coprolites. It corresponds to a 14C age of 6357±44 BP (1r: cal BC 5322–5260). These data rule out the coprolites belonging to Ovis aries or Capra hircus, and confirm that they belong to Myotragus balearicus, the only artiodactyl present in Mallorca during those times. During the field trip of September 1996 new coprolite samples together with the surrounding sediments were collected. In order to avoid risk of contamination, samples corresponding to squares M, N and O of row 7, section 7/8 of the grid

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(Fig. 2) were chosen. These squares, since they were located on a side of the passageway, were protected from possible disturbance arising from the movement of excavators inside the cave. The section was cleaned and samples were taken every ten centimeters from bottom to top within each grid (M7, N7, O7) using rubber gloves, which were removed for each sampling in order to avoid possible contamination due to accidentally dropping the materials. Dates for the second set have not yet been obtained. However, according to the deposit’s stratigraphy it is clearly related to the former dated level, and consequently an age of 6000–7000 years BP is assigned. On this occasion, in addition to the coprolite samples, sediment samples from the same levels were taken in order to compare the pollen content in the coprolites with that of the sediment. However, it should be stated that the sediment samples may contain pollen of destroyed coprolites, since several coprolites disintegrated when handled. The collected coprolites were stored in individual plastic bags. In order to minimize contamination risks from the coprolites’ surface a palynological analysis was carried out by the following protocol: (1) whole coprolites were used in the analysis, avoiding broken ones; (2) in a clean environment, coprolites were peeled with a sterilized scalpel (new for each coprolite and thus not contaminated) to remove the external layer; (3) under the same conditions a cube was cut from the inner side of the coprolite for the palynological analysis. The palynological chemical treatments follow the methodology of Goeury & Beaulieu (1979). Samples were dried in an oven at 50°C for at least 48 hours to eliminate water prior to weighing for physico-chemical analysis. Samples in series of four were weighed on a precision balance. Material was placed on sieves of 0.5 mm and of 0.25 mm to obtain the larger particles found between these sizes. A 50% HCl solution was added to the fine part to eliminate carbonates and then a 10% NaOH solution was added to eliminate humic acids. Next, a solution with density equal to 2.1 g/cm3 was added to the sample container to separate pollen by density. A 70% HF solution was then added to eliminate silica. Pure glycerine was added to the final dry residue. Microscopic observation of the isolated and concentrated pollen was done by placing a known volume of the concentrate on a 76×26 mm slide with a precision pipette. The counting of the pollen and spores content was performed at magnifications of 400× or 600×. The internal texture of the peeled coprolites was also analysed in order to avoid the aggregating effect of the mucus that presumably covered the dung pellets when fresh. The inner part of a coprolite sample was dissolved in water. This material was then passed through a set of sieves of 2 mm, 1 mm, 0.5 mm, 0.25 mm, 0.125 mm, 0.063 mm and 0.045 mm. The materials separated by the different sieves were dried for 24 hours in an oven at 60°C. Next, the complete operation was repeated to destroy possible material aggregators. Finally, the fractions separated in each sieve were weighed on a precision balance.

RESULTS

The coprolites of Myotragus balearicus were deposited in the passageway of the Cova Estreta (Fig. 2). Figure 3 shows a superficial heap of coprolites from Myotragus obtained from square M4. The fossil vertebrates from this cave are currently being studied (Encinas & Alcover, 1997; Seguı´, 1997). Preservation of coprolites should

Figure 2. Topography and genesis of Cova Estreta. Vertical (upper and middle part of the figure) and horizontal (lower part of the figure) sections. Arrows show the location of the coprolites of Myotragus balearicus studied in this work. The reference grid for the excavation has been situated between both sections. Upper part, right, evolving outline of Cova Estreta: 1. Formation of the cave, presumably during the Pleistocene. 2. During the Upper Pleistocene and Holocene the Cova Estreta acted as the draining system for a doline. 3. Currently, the drainage through the cave is only residual.

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Figure 3. Heap of coprolites of Myotragus found on the surface of grid square M4.

be related to the presumably dry conditions in the cave during recent millennia. When first explored (February 1996) the cave was closed by several obstructing stalactites (apparently non-active) which were re-activated due to breakage. The surrounding clayish sediment has a very fine grain and is very hydrophobic. A thin layer of this sediment might have served as a barrier, preserving coprolites from disintegration by water and from bacterial decomposition of the organic matter. The mucus covering the coprolites could have also played an important role in the preservation of vegetal microremains. The coprolites possess a cuboid cylindrical subrectangular shape, with a prismatic body and spheroidal ends. However, in many cases the proximal end as the bolus

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was excreted was pyramidal, whereas the distal end can appear flatter. A sample of 65 whole specimens chosen at random belonging to grid M4 range between 10.8 and 25.6 mm in length (mean=17.65 mm). The maximum and minimum diameters are usually very similar, with mean values of 18.01 and 16.32 mm, respectively. The coprolite dry weight was usually between 0.25 and 1.10 g (mean=0.6 g). Several fused coprolites have been found, together with few which were less solid at the moment of deposition (with an appearance similar to cow dung pellets, but quite a bit smaller). These kinds of dung pellets are also known in sheep. Many Caprinae produce large numbers of dung pellets and frequently use caves for resting. Thus, on occasion large quantities of fossil coprolites of several Caprinae have been found (e.g. the extinct Oreamnos harringtoni [Mead et al., 1986, 1987], or those of the still extant Ovis canadiensis [Spaulding, 1974]). The attraction to caves must have been very strong for Myotragus balearicus, according to the large quantity of skeletal remains found in caves. The studied deposit shows that Myotragus balearicus entered Cova Estreta and remained alive long enough to allow defecation. The volume of coprolites found is approximately 1 cubic meter, which corresponds to the accumulation product of many defecations corresponding to many individuals. Fourteen coprolites of Myotragus have been palynologically analysed. Three liberated very small amounts of pollen (less than 425 pollen grains), and were discarded in the analysis of the results. The results for the remaining 11 coprolites are shown in Table 1. In Figure 4 the overall result of the analyses is depicted graphically. The most pertinent finding of the analyses was the high proportion of pollen from Buxus balearica, which comprises 98% of the total. The flowers of Buxus balearica are inconspicuous, without perianth (Ko¨hler, 1994), and their pollinization is basically anemophilous. The d13C analyses of the coprolites of Myotragus balearicus gave a mean value of −26.36‰; (n=20 coprolites analysed, r=0.13). This value supports the fact that Myotragus balearicus only consumed C3 plants, as expected.

DISCUSSION

Given the palynological spectra for the coprolites and the surounding sediments, it should be determined whether these data reflect the diet of Myotragus balearicus. The dietary analysis of coprolites is complex (Mead et al., 1986; James & Burney, 1997). The anemophilous pollen grain can be introduced into the coprolites when pollen grains of non-consumed species fall onto the leaves of plants which comprise the actual diet of a species. The possibility of contamination by anemophilous pollen can therefore be high. The methodology used in this work allowed us to avoid postdepositional contamination risks for the coprolites, since the palynological analyses were performed on the interior parts of the coprolites. A way of evaluating the palynological analyses of coprolites of extinct species involves the study of pollen content for extant related species which have a controlled diet (see, for example, James & Burney, 1977). In the case of Myotragus this was not possible. Firstly, because its nearest relatives are unknown. Secondly, those candidates considered closest extant relatives of Myotragus do not live on the Balearic Islands. Thirdly, two of the possible candidates, Rupicapra and Nemorhaedus, basically have grazing and not browsing diets (Garcı´a Gonza´lez, 1984; Mead, 1989; Mishra & Johnsing, 1996). The artiodactyl species currently present near Cova Estreta are the

M7/ M8 350

%

M7/ M8 360 (2)

%

M7/ M8 370 (2)

%

N7/ N8 360

%

N7/ N8 370

%

O7/ O8 360

%

O7/ 08 380

%

Total MEAN RATE

TOTAL Indetermin.

18389 1

25587

8432

28437

701 19

698 6

646 12

757 6

444 26

2290 16

1114 3

87495 89

Abies 0.0 0.0 0.0 1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1 0.00 Pinus 101 0.5 52 0.2 86 1.0 54 0.2 12 1.7 2 0.3 0.0 3 0.4 2 0.5 3 0.1 4 0.4 319 0.48 Juniperus 1 0.0 17 0.1 6 0.1 6 0.0 1 0.1 0.0 0.0 0.0 0.0 0.0 0.0 31 0.03 Quercus t.c. 1 0.0 4 0.0 1 0.0 2 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 8 0.00 Quercus t.p. 2 0.0 2 0.0 0.0 3 0.0 1 0.1 4 0.6 0.0 0.0 0.0 0.0 1 0.1 13 0.08 Alnus 2 0.0 2 0.0 9 0.1 4 0.0 1 0.1 0.0 1 0.2 0.0 0.0 0.0 2 0.2 21 0.06 Acer 0.0 0.0 0.0 0.0 0.0 3 0.4 0.0 0.0 0.0 0.0 0.0 3 0.04 Corylus 8 0.0 1 0.0 12 0.1 12 0.0 2 0.3 2 0.3 3 0.5 0.0 0.0 1 0.0 2 0.2 43 0.14 Betula 0.0 0.0 0.0 1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1 0.00 Tilia 2 0.0 0.0 1 0.0 1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 4 0.00 Olea 5 0.0 1 0.0 1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 7 0.00 Buxus 18243 99.2 25496 99.6 8264 98.0 28328 99.6 679 96.9 683 97.9 608 94.1 751 99.2 432 97.3 2282 99.7 1096 98.4 86862 98.17 Pistacia 0.0 0.0 1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1 0.00 Ericaceae 4 0.0 1 0.0 5 0.1 3 0.0 2 0.3 0.0 3 0.5 1 0.1 0.0 0.0 0.0 19 0.09 Ephedra 2 0.0 1 0.0 2 0.0 2 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 7 0.00 Artemisia 0.0 2 0.0 1 0.0 3 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 6 0.00 Chenopodiaceae 2 0.0 0.0 1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 3 0.00 Poaceae 7 0.0 5 0.0 6 0.1 10 0.0 3 0.4 3 0.4 26 4.0 2 0.3 5 1.1 0.0 4 0.4 71 0.62 Asteraceae 1 0.0 0.0 2 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 2 0.00 Asteraceae t. 2 0.0 1 0.0 0.0 0.0 0.0 1 0.1 2 0.3 0.0 2 0.5 0.0 1 0.1 9 0.09 Plantago 2 0.0 0.0 2 0.0 3 0.0 0.0 0.0 1 0.2 0.0 2 0.5 4 0.2 3 0.3 17 0.10 Lamiaceae 4 0.0 1 0.0 15 0.2 4 0.0 0.0 0.0 1 0.2 0.0 0.0 0.0 0.0 25 0.03 Fabaceae 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1 0.1 1 0.01 Convolvolus 0.0 0.0 0.0 0.0 0.0 0.0 1 0.2 0.0 0.0 0.0 0.0 1 0.01 Thymelaea 0.0 1 0.0 16 0.2 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 17 0.02 Polygonum 0.0 0.0 1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1 0.00 Dipsacaeae 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1 0.2 0.0 0.0 1 0.02 Cyperaceae 1 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 1 0.00 Espora mono. 2 0.0 1 0.0 1 0.0 0.0 1 0.1 0.0 0.0 0.0 0.0 0.0 0.0 5 0.02 Espora trilet. 0.0 0.0 0.0 1 0.0 0.0 1 0.1 0.0 0.0 0.0 0.0 0.0 2 0.01

M4 % M4 % M4 % M4 % Surf. 1 Surf.2 Surf.3 Surf.4

T 1. Pollen content recorded inside coprolites of Myotragus balearicus

66 J. A. ALCOVER ET AL.

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Poaceae Pinus

Other 1.8%

Buxus 98.2%

Corylus Plantago Other

A

0.0

2.0

4.0

6.0 8.0 10.0 12.0 Rate

2.0

4.0

6.0 8.0 10.0 12.0 Rate

Poaceae Fem spores

Other 12.9%

Pistacia 87.1%

Lamiaceae Pinus Quercus t. p. Ericaceae Other

B

0.0

Figure 4. A, pollen content of the coprolites of Myotragus balearicus from Cova Estreta. B, pollen content of two recent dung pellets of Capra hircus from the surroundings of Cova Estreta.

introduced species Capra hircus, living in a totally wild state in the area, and Ovis aries, which is subjected to little handling. Several recent goat dung pellets from the area surrounding Cova Estreta have been palynologically analysed. The spectrum obtained (Fig. 4) is of great interest since there appears to be a rather high proportion of pollen from Pistacia lentiscus, a species which is a poor pollen producer. Pistacia lentiscus is consumed by goats from the Serra de Tramuntana of Mallorca ( J.Llop, pers. comm.), and is found in the surroundings of Cova Estreta in the form of small bushes irregularly distributed and of low density. This result appears to corroborate the view that the most abundant vegetable microfossils within the goat dung pellets can provide some information on its diet (see also James & Burney, 1997). Buxus balearica, an important plant within the palynological spectrum obtained from the coprolites of Myotragus balearicus, is not currently present in the Cova Estreta area. Abies, deciduous species of Quercus, Alnus, Acer, Corylus, Betula, and Tilia also currently do not exist in Mallorca or are noticeably scarcer than in the upper Pleistocene flora, according to the palynological analysis. This change has been related to the evolution of the landscape due to climate (Yll et al., 1994, 1997; Pe´rezObiol et al., 1996). In spite of this climatic explanation, involvement of humans in the drastic reduction of box in the Balearic Islands cannot be discounted. The abundance within the coprolites of Myotragus of a taxon which has both a relatively low pollen production and dispersion capacity (Pe´rez-Obiol & Roure, 1985) allows us to propose that the coprolites’ pollen content originates from ingestion and that Buxus balearica was probably a very important part of the diet of Myotragus

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Figure 5. Pollen of Buxus balearica found in the inside of coprolites of Myotragus balearicus.

balearicus, at least in the Cova Estreta area (Fig. 5). Additional support for such consumption can be derived from the cranial functional morphology and the dentition of Myotragus. While up to now only the abrasive character of the diet of Myotragus has been inferred (Alcover et al., 1981, Marcus, in press), in recent years a number of workers have established a series of criteria to evaluate the palaeodiets of ruminant extinct species (Solounias & Dawson-Saunders, 1988; Solounias et al., 1995; Dompierre & Churcher, 1996). Analysis of the cranial morphology of Myotragus balearicus, including the morphology of the premaxillaries and the location and depth of the masseteric muscle, suggest an essentially browsing habit. Furthermore, a species which lived in environments in which Buxus balearica was preponderant (Burjachs et al., 1994; Pe´rez-Obiol et al., 1996) was a good candidate for consuming box, in spite of the necessity for Myotragus having to acquire a capacity to detoxify the alkaloids of its leaves and bark. Buxus balearica is known to be a species with a very high toxicity. Its leaves and trunk contain different steroidal alkaloids (buxines, cyclobuxines, parabuxines and others; see, for example, Khuong-Huu et al., 1966). Ingestion by sheep, goats or calves of leaves or bark of Buxus sempervirens, a species very close to Buxus balearica, leads to gastroenteritis, with colic and diarrhoea. The ingestion of large amounts

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causes nausea, vomiting, diarrhoea, vertigo and convulsions. Finally, death occurs due to respiratory paralysis (Bastien et al., 1973; Fowler, 1983; Camy et al., 1986). Probably the effects of the ingestion of leaves or bark of Buxus balearica are identical. In fact, according to the literature no population of extant artiodactyl has been found to feed on Buxus. Due to the toxicity of box it can be suggested as an alternative explanation that the Myotragus population from the Cova Estreta was forced to consume box owing to the non-existence or scarcity of other species of plants, and that box consumption was the cause of death of the individuals. For us this explanation is not tenable if the morphology of the coprolites is taken into consideration. They are unlikely to belong to sick animals (coprolites revealing either diarrhoeas or abnormal forms are not present). On the other hand, if box consumption represented the last ingestion, a greater diversity of plant microfossils within the coprolites would be expected if the remains of former meals were present. Finally, the analysed coprolites would have had to be produced by different individuals (except perhaps for those corresponding to the grid square M4, found in a well delimited small area). It is not likely that a whole population, comprised of individuals which did not have bone pathologies indicating either rachitism or any other symptomatic condition related to food scarcity, would consume a plant which is not part of its habitual diet. We therefore believe that the pollen analyses suggest that Buxus balearica was part of the habitual diet of Myotragus balearicus, being a source of great importance, at least in the Cova Estreta area. Additional information on diet variability can be obtained from the analysis of stable isotopes (e.g. Ostrom et al., 1994; Bocherens et al., 1994). The negligible variation registered in the d13C analysis of the coprolites of Myotragus balearicus shows that the diet was very uniform. Consequently, it can be inferred that, at least in the Cova Estreta deposit, Buxus balearica was probably the only or almost the only food consumed. The relatively high percentages of other plants found in three coprolites have to be interpreted as pollen depositions on the Buxus balearica material consumed by Myotragus. We are not aware whether Myotragus balearicus depended on box for survival. How Myotragus avoided its toxic effects is a question which we are currently working on. Several extant herbivores feed on plants of very low digestibility, either with nondigestive compounds originated from their secondary metabolism (lignin, tannins, silica particles) or toxins (alkaloids, terpenoids, cyanogenic components and others) (Howe & Westley, 1988; Rosenthal & Berenbaum, 1991). A paradigmatic example is that of the koala, Phascolarctos cinereus, a completely folivorous species exclusively feeding on leaves of Eucalyptus ssp. (Eberhard, 1978). Eucalyptus leaves contain high concentrations of tannins which reduce their digestibility. Recently, an enterobacterium capable of degrading tannin-protein complexes has been isolated from koala dung pellets (Osawa, 1992). Another case, previously mentioned, is that of several extant lemurs of the genus Hapalemur, which consume cyanogenic plants with a much higher concentration of cyanides than a human lethal dose (Glander et al., 1989). The size of the coprolites of Myotragus, relatively large for an animal of its height, is difficult to interpret. The extinct Harrington’s mountain goat Oreamnos harringtoni produced larger coprolites than those of the largest living goat from the Rocky Mountains, Oreamnos americanus. This anomaly seems to be related to the dryness and roughness of its diet (Mead et al., 1986). The fine texture of the Myotragus coprolites, which do not contain macroscopic

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Percent dry weight

40 35 30 25 20 15 10 5 0 40 35 30 25 20 15 10 5 0 40 35 30 25 20 15 10 5 0

Myotragus balearicus

<45

46–63

64–125 126–250 251–500 501–999

>1000

Capra hircus

<45

46–63

64–125 126–250 251–500 501–999

>1000

Cervus canadensis

<45

46–63

64–125 126–250 251–500 501–999

Particle size (µm)

>1000

40 35 30 25 20 15 10 5 0 40 35 30 25 20 15 10 5 0 40 35 30 25 20 15 10 5 0

Odocoileus hemionus

<45

46–63

64–125 126–250 251–500 501–999

>1000

64–125 126–250 251–500 501–999

>1000

Ovis aries

<45

46–63

Oreamnos americanus

<45

46–63

64–125 126–250 251–500 501–999

>1000

Particle size (µm)

Figure 6. Percentage distribution of the dried weights of dung for Myotragus balearicus in comparison with other artiodactyls.

fibres, differs substantially from those of goat and sheep dung pellets which we have compared. The latter contain many fibres of more than 1 mm diameter, visible with the naked eye. The coprolites of Myotragus do not contain apparent fibres, but are composed of fine dust. The results obtained from the texture analysis are presented as percentages of the total dry weight in Figure 6. Only two small shell fragments of a small mollusc appear in the fraction larger than 1 mm. It must have been a mollusc on the leaves of Buxus which was accidentally ingested, and not part of the diet of Myotragus. The weight of the two fragments is smaller than 0.005 g. The particle fraction larger than 1 mm does not contain any vegetable remains, and owing to the small size of the mollusc fragments, is considered negligible. The fragments between 0.5 and 1 mm comprise less than 5% of the dry weight of the inside of the coprolites. Within this range are also several mollusc fragments (probably from the same specimen previously found). More than 95% of the dry weight of the coprolites consists of particles less than 500 lm, and almost 50% is less than 125 lm. According to the microscopic analyses, box fibres are relatively thick (Mauset, 1988), and the box wood is particularly hard. Coprolites of herbivores from the Upper Pleistocene frequently contain fibres (e.g. Hansen, 1980, Mead et al., 1986). Consequently, the internal texture of the Myotragus coprolites cannot be explained as a result of a postdepositional degradation. The small particle size inside the Myotragus coprolites suggests more efficient digestive processes than those of other

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bovid species, in which numerous particles of larger size can be observed. For example, Hansen (1980) finds that 10% of the dry weight of sheep dung pellets, Ovis aries, is comprised of particles of more than 1 mm, and 32% by particles of more than 0.05 mm. For other ruminants studied by Hansen (1980), the percentage of dry dung comprising particles of more than 1 mm is between 5% and 28%, whereas for particles of more than 0.5 mm it is between 29% and 48%. For three lagomorph species—Sylvilagus audubonii, Lepus townsendii and Lepus californicus—between 6 and 11% of the dry weight of the dung pellets comprises particles of more than 1 mm, and between 36% and 42% consist of particles of more than 0.5 mm. For two rodents, between 34% and 41% of the dry weight of the dung pellets comprises particles of more than 0.5 mm. To provide comparisons, several recent dung pellets of Capra hircus garnered in the area surrounding Cova Estreta were also analysed. Twenty-five percent, by dry weight, of the pellets consists of particles of more than 0.5 mm, whereas only 14.2% comprised particles of more than 0.125 mm. However, this apparent high digestive efficiency complicates the analysis of the diet of Myotragus, since it involves a greater destruction of the materials consumed. At present it is difficult to determine which parts of box were consumed by Myotragus balearicus. A very few microhistological remains of flowers of Buxus have been found together with several remains of vessels. In all probability Myotragus consumed the leaves, perhaps only tender leaves in addition to the flowers. However, it cannot be determined if consumption of flowers was either accidental or selective. More information on the parts consumed by Myotragus requires further research. The extent to which Myotragus was dependent on box and the degree of euryphagy it had is unknown. Further investigations based on coprolites from other sites of the Balearic Islands are required to provide a more complete picture of the diet of Myotragus. Data presented in this work are restricted to a mountain population of Myotragus balearicus from Mallorca. The diet of Myotragus balearicus in other habitats and on the other islands is currently unknown awaiting further palaeontological discoveries.

ACKNOWLEDGEMENTS

This work has been possible thanks to the projects ‘Excavacio´ i estudi dels materials paleontolo`gics de la Cova Estreta’ supported by the Conselleria de Cultura del Consell Insular de Mallorca and ‘Characterization of the Aridity Processes on Mediterranean Europe. Protection and Management Guidelines (ENV4-Ct95– 0062)’. One of the authors, Pere Bover, has been granted a scholarship from the Conselleria d’Educacio´ Cultura i Esports del Govern de les Illes Balears (Direccio´ General d’Educacio´). The materials studied were obtained through J.A. Encinas. We thank Helen F. James for providing us with a copy of her unpublished manuscript on coprolites of Thambetochen. Jim Mead (Flagstaff ), Anna Traveset (Ciutat de Mallorca) and George Schaller (New York) provided comments, data and bibliographical material of interest. M. Estiarte (Barcelona) analysed the d13C in the coprolites. Leslie Marcus (New York) checked the first English version; we thank him for his stimulating comments. The paper has benefited also from the comments and suggestions of A.W. Gentry (London).

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Alcover JA, McMinn M. 1994. Predators of vertebrates on islands. BioScience 44: 12–18. Alcover JA, Moya`-Sola` S, Pons J. 1981. Les Quimeres del Passat. Els Vertebrats Fo`ssils del Plio-Quaternari de les Balears i Pitiu¨ses. Ciutat de Mallorca: Monografies Cientı´fiques, Editorial Moll 1: 1–260. Andrews C. 1915. A description of the skull and skeleton of a peculiarly modified rupicaprine antelope (Myotragus balearicus Bate) with a notice on a new variety, Myotragus balearicus var. major. Philosophical Transactions of the Royal Society of London B206: 281–305 Angel B. 1966. Myotragus balearicus Bate considerado como vertebrado mamı´fero troglo´filo. Bolletı´ de la Societat d’Histo`ria Natural de les Balears 12: 35–38. Bastien A, Grisuard M, Jeanblain C, Roux M. 1973. Poisoning of young cattle by box (Buxus sempervirens L.). Bulletin de la Socie´te´ des Sciences Veterinaires et de Me´decine Compare´e, Lyon 75: 289–290. Bate DMA. 1909. A new Artiodactyle from Majorca. Geological Magazine N.S., Dec 5 6: 385–388. Bocherens H, Fizet M, Mariotti A. 1994. Diet, physiology and ecology of fossil mammals as inferred from stable carbon and nitrogen isotope biogeochemistry: implications for Pleistocene bears. Palaeogeography, Palaeoclimate, Palaeoecology 107: 213–225. Boekschotten GJ, Sondaar PY. 1972. On the fossil mammals of Cyprus. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, ser. B 75: 306–338. Amsterdam. Burjachs F, Pe´rez-Obiol R, Roure JM, Julia` R. 1994. Dina´mica de la vegetacio´n durante el Holoceno en la Isla de Mallorca. Trabajos de Palı´nologı´a Ba´sica y Aplicada: 199–210. Camy G, Leveille JL, Nevers B. 1986. Case report: box (Buxus sempervirens) poisoning in cattle. Point Veterinaire 18: 203–204. Chaline J, Mein P. 1979. Les Rongeurs et l’Evolution. Paris: Doin Editeurs. Cuerda J. 1975. Los Tiempos Cuaternarios en Baleares. Ciutat de Mallorca: Edit. Institut d’Estudis Balea`rics, 304 pp. Delvosalle L, Duvigneaud J. 1967. Voyage a` Majorque. Compte rendue botanique des excursions. Les Naturalistes Belges 48: 365–388. Dompierre H, Churcher CS. 1996. Premaxillary shape as an indicator of the diet of seven extinct late Cenozoic new world camels. Journal of Vertebrate Paleontology 16: 141–148. Eberhard IH. 1978. Ecology of the Koala, Phacolarctos cinereus (Goldfuss) (Marsupialia: Phascolarctidae) in Australia. In: Montgomery GG, ed. The Ecology of Arboreal Herbivores. Washington: Smithsonian, 315–327. Encinas JA, Alcover JA. 1997. El jaciment fossilifer de la Cova Estreta (Pollenc¸a, Mallorca). Endins 21: 83–92. Fowler ME. 1983. Plant poisoning in free-living wild animals: A review. Journal of Wildlife Diseases 19: 34–43. Freudenberg W. 1914. Die Sa¨ugetiere des Alteren Quartas von Mitteleuropa. Geologischen und Paleontologischen Abhandlungen 12: 455–670. Garcı´a-Gonza´lez R. 1984. Comparacio´n de la dieta estival entre sarrios jo´venes y adultos. Acta biologica montana 4: 333–340. Gatesy J, Amato G, Vrba E, Schaller G, Desalle R. 1997. A cladistic analysis of mitochondrial ribosomal DNA from the Bovidae. Molecular Phylogenetics and Evolution 7: 303–319. Gautier F, Clauzon G, Suc JP, Cravatte J, Violanti D. 1994. Age et dure´e de la crise de salinite´ Me´ssinienne. Comptes Rendus l’Academie Sciences, Paris, ser. II, 318: 1103–1109. Gentry AW. 1978. Bovidae. In: Cooke HBS, Maglio VJ, eds. Evolution of African Mammals: 540–572. Harvard University Press. Gentry AW. 1980. Fossil Bovidae (Mammalia) from Langeboanweg, South Africa. Annals of South African Museum 79: 213–337. Gentry AW. 1992. The subfamilies and Tribes of the Family Bovidae. Mammal Review 22: 1–32. Glander KE, Wright PC, Seiger DS, Randrianasolo V, Randrianasolo B. 1989. Consumption of cyanogenic bamboo by a newly discovered species of bamboo lemur. American Journal of Primatology. 18: 1–7. Gliozzi E, Malatesta A. 1980. The Quaternary Goat of Capo Figari (Notheastern Sardinia). Geologica Romana 19: 295–347. Goeury CI, Beaulieu JL. 1979. A propos de la concentration du pollen a` l’aide de la liqueur de Thoulet dans les se´diments mine´raux. Pollen et Spores 21: 239–251. Groves P., Shields G. 1996. Phylogenetics of the Caprinae based on cytochrome b sequence. Molecular Phylogenetics and Evolution 5: 467–476.

DIET OF MYOTRAGUS BALEARICUS

73

Guerrero V. 1996. El poblamiento inicial de la Isla de Mallorca. Complutum Extra 6: 83–104. Hansen RM. 1980. Late Pleistocene plant fragments in the dungs of herbivores at Cowboy Cave. Anthropology Papers of the University of Utah 104: 179–189. Hartl G, Burger H, Willing R, Suchentrunk F. 1990. On the biochemical systematics of the Caprini and the Rupicaprini. Biochemical Systematic Ecology 18: 175–182. Howe HF, Westley LC. 1988. Ecological relationships of plants and animals. New York: Oxford University Press. Hu¨rzeler J. 1983. Un Alce´laphine´ Aberrant (Bovidae, Mammalia) des “Lignites de Grosseto” en Toscane. Comptes Rendues de l’Academie Sciences, Paris, ser. II, 296: 497–503. James HF, Burney DA. 1997. The diet and ecology of the Hawaii’s extinct flightless waterfowl: evidence from coprolites. Biological Journal of the Linnean Society 62: 279–297. Juniper BE. 1984. The natural flora of Mallorca. Myotragus and its possible effects on the coming of man to the Balearics. BAR International Series 229: 143–163. Ko¨hler E. 1994. Parallel evolution of pollen characters in the genus Buxus L. (Buxaceae). Acta Botanica Gallica 141: 223–232. Ko¨hler M. 1993. Skeleton and habitat of recent and fossil ruminants. Mu¨ncher Geowissenschaftlichen Abhandlungen, A, 25: 1–88. Khuong-Huu F, Herlem-Gaulier DS, Khuong-Huu MQ, Stalisnas E, Goutarel R. 1996. Alcaloides de Buxus balearica Willd.; Cycloprotobuxine-D, Buxamine-E, Buxaminol-E, N-IsobutrylBaleabuxidine-F, N-Benzoyl-Baleabuxidine-F, Baleabuxoxazine-C, N-Isobutryl-BaleabuxidienineF, N-Benzoyl-Baleabuxodienine-F, N-Isobutyryl-Baleabuxaline-F. Tetrahedron 22: 3321–3327. Leinders J. 1977. Some aspects of the ankle joint of artiodactyls, with special reference to Listriodon (Suina). Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, ser. B, 81: 61–69. Marcus LF. in press. Variation in selected skeletal elements of the fossil remains of Myotragus balearicus, a Pleistocene bovid from Mallorca. Acta Hungarica. Mauset JD. 1988. Plant Anatomy. Menlo Park, California: Benjamin Cummings.. Mead JI. 1989. Nemorhaedus goral. Mammalian Species 335: 1–5. Mead JI, Agenbroad LD. 1992. Isotope dating of Pleistocene dung deposits from the Colorado Plateau, Arizona and Utah. Radiocarbon 34: 1–19. Mead JI, Agenbroad LD, Phillips III AM, Middleton LT. 1987. Extinct Mountain Goat (Oreamnos harringtoni) in Southern Utah. Quaternary Research 27: 323–331. Mead JI, O’Rourke MK, Foppe TM. 1986. Dung and diet of the extinct Harrington’s mountain goat (Oreamnos harringtoni). Journal of Mammalogy 67: 284–293. Mishra C, Johnsing JT. 1996. On habitat selection by the Goral Nemorhaedus goral bedfordi (Bovidae, Artiodactyla). Journal of Zoology, London 240: 573–580. Osawa R. 1992. Tannin-protein complex-degrading enterobacteria isolated from the alimentary tracts of koalas and a selective medium for their enumeration. Applied Environmental Microbiology 58: 1754–1759. Ostrom PH, Zonneveld JP, Robbins LL. 1994. Organic geochemistry of hard parts: assessment of isotopic variability and indigeneity. Palaeogeography, Palaeoclimatology, Palaeoecology 107: 201–212. Pe´rez-Obiol R, Roure JM. 1985. Relaciones entre la vegetacio´n y su espectro polinico en Catalun˜a. Anales de la Asociacio´n de palino´logos de Lengua Espan˜ola 2: 329–338. Pe´rez-Obiol R, Yll EI, Pantaleo´n-Cano J, Roure JM. 1996. Historia de Buxus y Corylus en las Islas Baleares durante el Holoceno. In: Ramil-Rego P, Fernandez-Rodriguez C, Guitia´n M, eds., Biogeografia Pleistocena – Holocena de la Peninsula Ibe´rica. Xunta de Galicia, 87–97. Peyer B. 1968. Comparative Odontology. Chicago: The University of Chicago Press. Rosenthal GA, Berenbaum MR, eds. 1991. Herbivores. Their Interactions with Secondary Plant Metabolites. San Diego: Academic Press. Scott K. 1983. Prediction of body weight of fossil artiodactyla. Zoological Journal of the Linnean Society 77: 199–215. Seguı´ B. 1997. Els ocells fo`ssils del Plistoce` superior i Holoce` de Mallorca i Menorca. Tesina Llicenciatura, Universitat de les Illes Balears. Simpson GG. 1945. The principles of the classification and a classification of mammals. Bull. Amer.Mus.Nat.Hist. 85: 1–350. Solounias N, Dawson-Saunders B. 1988. Dietary adaptations and paleoecology of the Late Miocene ruminants from Pikermi and Samos in Greece. Paleogeography, Paleoclimatology, Paleoecology 65: 149–172. Solounias N, Moelleken SMC, Plavcan JM. 1995. Predicting the diet of extinct bovids using the masseteric morphology. Journal of Vertebrate Paleontology 15: 795–805.

74

J. A. ALCOVER ET AL.

Spaulding WG. 1974. Pollen analysis of fossil dung of Ovis canadensis from southern Nevada. Unpublished M.S Thesis, Univ. Arizona, Tucson. Spoor CF. 1988. The limb bones of Myotragus balearicus Bate 1909. Proceedings of the Koninklijke Nederlandse Akademie van Wetenschappen, ser. B, 91: 295–309. Thomas H. 1994. Anatomie craˆnienne et relations phylogenetiques du nouveau bovide´ (Pseudoryx nghetinhensis) de´couvert dans la Cordille`re Annamitique au Vietnam. Mammalia 58: 453–482. Yll EI, Pe´rez-Obiol R, Julia` R. 1994. Vegetational change in the Balearic Islands (Spain) during the Holocene. Historical Biology 9: 83–89. Yll EI, Pe´rez-Obiol R, Pantaleo´n-Cano J, Roure JM. 1997. Palynological evidence for climatic change and human activity during the Holocene on Minorca (Balearic islands). Quaternary Research 48: 339–347. Waldren WH. 1982. The excavation and study of certain caves, rock shelters and settlements. BAR International Series 149: 1–773.