North African Sirenia (Mammalia)

    The disappearance of the European/North African Sirenia (Mammalia) Gonc¸alo Prista, M´ario Estevens, Rui Agostinho, M´ario Cach˜ao PII: DOI: Reference:

S0031-0182(13)00334-9 doi: 10.1016/j.palaeo.2013.07.013 PALAEO 6570

To appear in:

Palaeogeography, Palaeoclimatology, Palaeoecology

Received date: Revised date: Accepted date:

8 March 2013 7 July 2013 11 July 2013

Please cite this article as: Prista, Gon¸calo, Estevens, M´ario, Agostinho, Rui, Cach˜ ao, M´ ario, The disappearance of the European/North African Sirenia (Mammalia), Palaeogeography, Palaeoclimatology, Palaeoecology (2013), doi: 10.1016/j.palaeo.2013.07.013

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ACCEPTED MANUSCRIPT The disappearance of the European/North African Sirenia (Mammalia).

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Gonçalo Prista1

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Mário Estevens3

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Rui Agostinho4

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Mário Cachão1, 2

Centre of Geology of the University of Lisbon, Campo Grande, 1749-016 Lisbon, Portugal

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Faculty of Sciences of the University of Lisbon, Geology Department, Campo Grande,

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1749-016 Lisbon, Portugal

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Almada City Council, Departamento de Estratégia e Gestão Ambiental Sustentável

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Ecoteca de Almada - Casa Municipal do Ambiente R. Bernardo Francisco da Costa, nº 40 e nº

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42 2800-029 Almada, Portugal

Faculty of Sciences of the University of Lisbon, Physics Department, Campo Grande,

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1749-016 Lisbon, Portugal

Corresponding Author: Gonçalo Prista (Campo Grande, 1749-016 Lisbon, Portugal; phone: 967825069; e-mail: [email protected])

ABSTRACT Sirenia inhabited the coastal waters of Europe and North Africa from the Eocene until the end of the Pliocene. They are the only herbivorous marine mammals, and their presence in the European/North African realm is supported by almost 400 fossil records. Their dependence on seagrass, as well as their ecological needs, limited their

ACCEPTED MANUSCRIPT capability to adapt to the climate changes that occurred during the Cenozoic. Their disappearance from European and Mediterranean shores occurred in two different

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steps: 1) the European Atlantic extinction, related to global cooling and fragmentation

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of the seagrass meadows, which greatly reduced sirenia habitats and resources; 2) their

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disappearance from the Mediterranean, linked not to declining resources but to the

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onset of continental glaciations in the northern hemisphere.

1. Introduction

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Sirenia, an Order (Sirenia Illiger, 1811) of placental mammals that, along with cetaceans, represent the only mammals that evolved for a fully aquatic life (Clementz et al., 2009),

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have the particularity of being the only herbivorous marine mammals (Domning, 2002),

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commonly named Seacow . They feed mainly on seagrass, although there are some

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differences between the two extant families, the trichechids and the dugongids. The Trichechidae family is not highly specialized when it comes to food and habitat. They

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live in fresh and sea-water, feeding on more than 60 species of marine plants, and can be considered, as suggested by Anderson (2002), opportunistic feeders on seagrass. The Dugongidae family is more specialized, feeding mainly on seagrass and is almost exclusively found in salt water. These characteristics are not exclusive of the four actual species, as shown by MacFadden et al. (2004), and can be traced back to the extinct species of both families. They first appeared after the Early Eocene Climatic Optimum (53-49 Ma (Höntzsch et al., 2011)), with the oldest record of Pezosiren portelli from Jamaica (Domning 2001a). The coastal shores of Europe and North Africa have records dating from the Lutetian (Caria, 1957; Crusafont-Pairó, 1973; Savage, 1976; Batik and Fejfar, 1990; Zalmout and

ACCEPTED MANUSCRIPT Gingerich, 2012), showing that the Tethys Sea was colonized by these marine mammals in both its north and south margins.

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Sirenians were abundant in Tethyan coastal waters, and also in the Paratethys and the

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Mediterranean, which evolved from it. The Sirenia that inhabited the European/North

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African shores are almost exclusively of the Dugongidae family (more than 95% of the European and North African fossil record belong to dugongids), meaning that they fed

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mainly on seagrass. Seagrasses are marine phanerogams that colonized the coastal waters around 100 Ma ago (Hemminga & Duarte, 2000). They show few changes in

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their evolutionary process and many of the genera found today can be traced back to

2001b; Bianucci et al., 2008).

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the Eocene (like Cymodocea nodosa and Posidonia sp. from the Eocene of Paris) (Domning,

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The extinction of the Sirenia in the European/North African realm hasn't been totally

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understood. The climate cooling of the Cenozoic seems insufficient to explain their disappearance from the Mediterranean and Northeast Atlantic shores. In the North

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Pacific, Sirenia adapted to the cold environment, and the largest sirenians known, Hydrodamalis gigas, up to 9 metres in length, colonized the Bering Sea (Domning, 1978). It became extinct after 30 years of overkill, during the eighteenth century. Since the Hydrodamalinae family in the North Pacific (Aranda-Manteca et al., 1994) originated from the Metaxytherium genus, abundant in Europe, the question remains: why the same adaptation/evolution did not occur in the Old Continent?

2. Brief History of the Late Miocene and Pliocene European/North African Sirenia fossil record

ACCEPTED MANUSCRIPT After the Miocene Climatic Optimum (MCO) around 14 Ma ago (Böhme, 2003; Domingo et al., 2012), European and North African sirenia declined in biodiversity.

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Only one genus is known from the Late Miocene and Pliocene, the Metaxytherium, and

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only three species have been classified for this time interval, M. medium, M. serresii and

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M. subapenninum.

The Tortonian is the last age with sirenia fossil records in the Northeast Atlantic shores,

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north of Portugal. In the Faluns Sea, northeastern France, the record is abundant until the Tortonian (Cottreau, 1928; Lécuyer et al., 1996).

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For the Messinian age, Portugal appears to be the only place with a fossil record on this side of the Atlantic, with two records from Santa Margarida do Sado (Ferreira do

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Alentejo, Beja) and Vale de Zebro (Alvalade, Setúbal) (Estevens, 2000). The

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Mediterranean has a slightly richer fossil record, with fossils from Libya (Zalmout and

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Gingerich, 2012) and probably Italy (Zei and Moncharmont, 1987) and Spain (Sendra Saez et al., 1998). This scenario is not totally understood, because it was during the

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Messinian that the Messinian Salinity Crises (MSC) occurred, a period of closure of the Mediterranean and great ecological disturbance (see Fig. 1 for the sirenia distribution area according to the fossil record). The Pliocene shows an increase in the fossil record for the Mediterranean Sea, and only one occurrence in the Atlantic, belonging to the Gulf of Cadiz on the Morocco shore (Ennouchi, 1954). A rib fragment of sirenia has been recovered from Pliocene deposits of Algarve, Portugal . However, it shows signs of transportation and may belong to older sediments, probably from the Middle Miocene (Cachão & Silva, 2000; Estevens, 2000, 2006) (see Fig. 2 for the sirenia distribution area according to the fossil record).

ACCEPTED MANUSCRIPT The Zanclean age has records of M. serresii, which first appeared during the Late Miocene of Libya (Zalmout and Gingerich, 2012), from Montpellier, France (Domning

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and Thomas, 1987; Pilleri, 1987), Sahabi Formation, Libya (Domning and Thomas, 1987)

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and Alicante, Spain (Sendra et al., 1999; Bianucci et al., 2008). During this age appeared

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the last European/North African sirenia species, the M. subapenninum, with the oldest records from the Early Zanclean of Italy (Sorbi and Vaiani, 2007; Tinelli et al., 2012) and

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the last known records dated to the Early Piacenzian (Bianucci et al., 2008). M. serresii

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ceases its appearance in the fossil record during the Zanclean age.

3. Seagrass

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To understand the sirenia disappearance it is necessary to understand their primary food source, the marine phanerogams, commonly known as seagrass. Seagrasses are

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monocotyledon angiosperms that grow in tidal and subtidal marine environments. They represent less than 0.02% of the angiosperm flora and their biodiversity is very

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low, around 50 species and 12 genera (Hemminga and Duarte, 2000). The fossil record doesn't suggest any higher palaeobiodiversity in the past. Although usually associated with tropical waters, these marine phanerogams actually thrive from tropical to temperate environments, being found, for example, in the North Atlantic and New Zealand (Hemminga and Duarte, 2000; Short et al., 2007). Seagrass rhizomes are the more nutritious part of the plant, accumulating reserves in the form of carbohydrates. They can be located just below the sea bottom (around 2 cm deep) or deeply buried in the sediment (up to 14 cm), varying with species and apical system sizes (Duarte et al., 1998; Domning, 2001b).

ACCEPTED MANUSCRIPT These plants are highly dependent on light, which is the reason why they are always found in shallow, clear waters. They are very sensitive to the increase in suspended

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matter in the water column, with prolonged reductions in luminosity always resulting

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in plant death (Kurtz et al., 2003).

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In the Mediterranean Sea, some seagrass species, like Cymodocea nodosa and Posidonia oceanica, are very important for understanding the evolution and extinction of the

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sirenia. C. nodosa is typically a lagoon and estuary species, preferring harsh hydrodynamic conditions (Short et al., 2007) and being very sensitive to low

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hydrodynamic environments, as shown in Binzer et al. (2005). These characteristics limited their presence in the Tethys Sea during the Eocene, when the hydrodynamic

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conditions were very low (Höntzsch et al., 2011).

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P. oceanica is endemic to the Mediterranean Sea and has been present in this region

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since the Cretaceous. Today it is the dominant species in the Mediterranean, colonizing between 25.000 and 50.000 km2 of the coastal areas (Aires et al., 2011). It has a very slow

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growth rate (1 cm/year) and it is highly sensitive to increases in organic matter and nutrients (Jordà et al., 2012). Despite this sensitivity it is known that it survived the MSC in refuge areas (Aires et al., 2011) and that it existed in the Tethys Sea during the Eocene, although it was a time of great organic matter accumulation and eutrophication events in the platform environment (Höntzsch et al., 2011). The present day map of seagrass distribution and abundance reveals differences between the 3 oceanic realms inhabited by sirenia. The Indo-Pacific region is the area with the greatest biodiversity and colonized area (24 species). The temperate North Pacific has a good biodiversity, with 15 species distributed in lagoons, estuaries and coastal shores. In the temperate North Atlantic, we find a low biodiversity, only five

ACCEPTED MANUSCRIPT species, concentrated in lagoons and estuaries, while in the tropical regions of the Atlantic, and the Caribbean area, there are 10 species, similar to the Mediterranean Sea

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with nine species (Short et al., 2007).

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4. Discussion

Since the Eocene, the Sirenia show a gradual increase in size, an expected response of

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animals with low metabolic rates to the cooling of the Cenozoic (Bianucci et al., 2008). A clear example in the Sirenia Order is Hydrodamalis gigas, almost 9 meters long, and

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inhabiting the Bering sea. This gradual size increase was reversed during the Late Miocene. The species M. serresii, apparently the dominant species of the Tortonian-

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Messinian, and the only one that survived the MSC, shows a reduction of total length

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and cranial size, as shown by Bianucci et al. (2008). This is typical with limited space

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and/or resources, and indicates that even during the Tortonian, the conditions for the Sirenia in the Mediterranean Sea were already declining.

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The aggravation of the ecological conditions during the Tortonian may have been influenced by factors other than the cooling that was taking place. The two washhouse periods (Böhme et al., 2008; Böhme et al, 2011) of this age may have promoted eutrophication in coastal areas due to the increase of organic matter and nutrients, through soil leaching induced by abundant precipitation. The increase in the rivers volume also could have transported more suspended matter (Köhler et al., 2010), which would have had a negative impact in the marine phanerogams. The Tortonian fossil record shows a Sirenia distribution in Southern Italy, Crete, Libya and possibly in the South of Spain and Northwest France, in the Faluns Sea. The shores of Northwest Italy, Catalonia and Southern France have no fossil record, contrary to

ACCEPTED MANUSCRIPT what it's found before (Catalonia and Southern France) and after (Northwest Italy). The fossil record suggests that Sirenia were dislocated to central areas of the Mediterranean,

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supporting the eutrophication hypothesis of coastal areas, with its negative impact on

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seagrass.

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Sirenia’s decline intensified during the Messinian with the MSC. This event reduced seagrass availability even more, and species like P. oceanica were reduced to small

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refuges. During this event, all seagrass species were affected and were limited to small areas, what we could characterize as small islands of seagrass. The seagrass meadows

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were dominated by C. nodosa, Z. marina and Z. noltii, species more resistant to salinity variations. The first one has medium size rhizomes, while the other two have small

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ones, according to the classification of Domning (2001b). Rhizomes, being the more

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nutritive part of these plants, played an important role in sirenia evolution and

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adaptation, particularly during extended periods of environmental stress. Parallel to the reduction in M. serresii length, tusk size increased. The presence of tusks

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in Sirenia is known since the Oligocene (Domning and Beatty, 2007) and this has been attributed to feeding habits, because it is an anatomical characteristic of both genders. The increase in tooth size during the Messinian reveals a new need: to dig up the more nutritive rhizomes of seagrasses, essential in a low resource period (Bianucci et al., 2008; Sorbi et al., 2012). The use of these teeth from the perspective of reproduction or competition for space, as suggested by Sorbi et al. (2012), is also probable, however, because there is no differentiation between the tusks of males and females, it seems that a reproductive reason is not very likely. Nevertheless, an attack/defence mechanism in competition for space is highly probable, as it would be something needed by both genders.

ACCEPTED MANUSCRIPT The Pliocene brings a new species, M. subapenninum. A new increase in tusks size is observed in this new species, probably associated with the recolonization of the

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Mediterranean by P. oceanica, a seagrass with large rhizomes. An adaptation to feed on

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these rhizomes would be more favourable than returning to a diet of smaller species

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(Sorbi et al., 2012). However, in M. subapenninum, tusks may have been a sexual

4.1. Tusks and reproductive behaviour

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characteristic as well, as will be discussed in the next point (4.1).

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The variations in tusk size have been one of the great challenges in studies of Sirenia evolution. The extant dugong species are particularly relevant to our understanding of

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these dental structures. In Dugong dugon, territorial dispute and defence are only

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observed during mating season, when males use territories that they defend against

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any intruder. The territories are no more than combat arenas, since usually they are small sheltered bays, without any food resources. Females enter the territories

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probably following the male's vocalizations, which are frequent during this season (Anderson, 2002). The other dugongid that lived until historical times, H. gigas, was probably the only monogamous sirenian, judging by George Steller's observations. Manatees have a different reproductive behaviour. There is no territorial dispute and a single female is pursued by several males (up to 22 during a period that can last up to 30 days), ending by copulating with those (usually more than one) that keep closer. These groups are called mating herds (Anderson, 2002). Similar herds have been observed in dugongs, but because these observations occurred during aerial surveys it wasn't possible to distinguish between females and males (Anderson, 2002), making any interpretation unreliable.

ACCEPTED MANUSCRIPT In the past, tusks were not characteristics of sexual dimorphism, strengthening the hypothesis that they were related to feeding activity, or territorial defence during

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lower resource periods (like the MSC). They first appear in the Oligocene, precisely

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when a decrease in Sirenia biodiversity was observed, most probably due to an

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increase in climate seasonality, also related to the onset of the Antarctic continental glaciations (Zachos et al., 2008; Costa et al., 2011). These two aspects could have had an

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impact on marine phanerogams at medium and high latitudes, suggesting that tusk development could have been a way of maximizing food resources.

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After the end of the MSC, during the Early Zanclean, M. subapenninum appears, and in the Late Zanclean, M. serresii became extinct. As described by Bianucci et al. (2008), the

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increase in total body size in M. subapenninum was very rapid, and it was accompanied

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by an increase in tusk size. This species became the largest Sirenia ever to inhabit

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European shores. The same authors suggest the feeding habits, rich in P. oceanica rhizomes, as the main reason for such a rapid size increase. However, the cooling that

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marks the beginning of the Pliocene (Kovar-Eder et al., 2006; Micheels et al., 2009), started before, with the beginning of the Arctic glaciations during the Tortonian (Bruch et al., 2011; Utescher et al., 2011), and should also be taken into account as a generator of this size change. In M. subapeninum, there are some indicators that suggest that for the first time tusks could be a characteristic of sexual dimorphism, being larger in males than females. However, new data are required to prove this hypothesis (Sorbi et al., 2012). The Pliocene is marked by an increase in seagrass in the Mediterranean, with P. oceanica recovering from the MSC. This could have helped the beginning of this gender separation, by reducing the pressure on resources. The sexual dimorphism may reveal

ACCEPTED MANUSCRIPT changes leading to reproductive behaviour similar to that seen in Dugong dugon, although one must not exclude the possibility that this behaviour was already present

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in previous species. However, despite the fact that Metaxytherium belongs to the

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Dugongidae family, it is of a different subfamily than the present dugong, so some

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precaution is necessary when extrapolating interpretations based on present day

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behaviour (Sorbi et al., 2012).

4.2. The End of European/North African sirenians

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By the end of the Pliocene, after the Middle Piacenzian Warm Period (MPWP) (Dowsett et al., 2011; Robinson et al., 2011), Sirenia disappeared from the

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Mediterranean, with its last European/North African record dating from the late

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Piacenzian (Sorbi et al., 2012). Around 12 Ma, Metaxytherium gave rise in the North

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Pacific to the Hydrodamalinae subfamily, adapted to cold waters (Aranda-Manteca et al., 1994). This did not happened in the North Atlantic, most probably because the

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North Atlantic shores may have had a different seagrass biodiversity, distribution and abundance. Since these marine plants have shown almost no variations since the Eocene (Domning, 1981; 2001b), it is likely that during the Late Miocene their biodiversity was similar to the one we encounter nowadays. This means that the North Atlantic had low seagrass biodiversity, contrary to the North Pacific that would have had, as it does today, high levels of marine phanerogams biodiversity. Because the distribution of seagrass in the Northeast Atlantic region was fragmented, Sirenia was confronted with a reduced food supply, and that may have prevented Metaxytherium from being able to adapt to the cooling trend and to cold environments in the North Atlantic realm. Instead, Sirenia took refuge in the Mediterranean Sea.

ACCEPTED MANUSCRIPT Ultimately, we need to understand why there are no sirenians in the Mediterranean today, even though extensive meadows of seagrass are present. The Metaxytherium

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genus, with a cosmopolitan distribution, became more restricted worldwide during the

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Late Miocene, except on the European and Mediterranean shores (Sorbi et al., 2012),

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where it became the only genus present. It gave origin to the species M. subapenninum, exclusive to the Mediterranean basin, with the latest record dating from the Piacenzian

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(Sorbi et al., 2012). With the Mediterranean full of seagrass, it seems that the beginning of the continental glaciations of the northern hemisphere is intimately linked to the

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Sirenia extinction. According to Böse et al. (2012), glaciations in the North of Europe started in 2.7 Ma, with recurrent glaciations in the highlands. This had effects on the

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Mediterranean biodiversity, with extinction events between 3.1 Ma and 2.7 Ma due to

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the cooling of deep waters at the beginning of the glacier growth of the northern

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hemisphere (Hayward et al., 2009). This is precisely the time period when Sirenia

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disappeared from the Mediterranean shores.

4.3. Present Mediterranean conditions Today the Mediterranean has a mean sea surface temperature (SST) of ≈22°C in the east and southeast regions and ≈19°C in west/southwest (Marullo et al., 2007). Marullo et al. (2007) also present Mediterranean temperatures for the 29 of December, in the year 2000, which were ≈22°C in the east, southeast and Gulf of Sirte, and 15-16°C in the west and southwest regions. This means that today the Mediterranean has conditions for Sirenia to exist. Temperatures are similar to the ones seen during the Early Miocene, when mean SST of the Central and Western Paratethys was ≈14-28°C (Kocsis et al., 2009) or during the MCO, when the mean SST of the North Paratethys was ≈17-19°C

ACCEPTED MANUSCRIPT during the cold season and ≈28°C during the warm season (Kroh, 2007; Harzhauser et al., 2011).

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The absence of Sirenia from present Mediterranean shores has two reasons: (1) the

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Dugongidae family only exists in the Indo-Pacific region which is not connected today

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to the Mediterranean, preventing the dugongs that inhabit the Red Sea, which was separated from the Mediterranean during the Early Serravallian (Rögl, 1999), from

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recolonizing the shores of southern Europe and the north of Africa; (2) the Trichechidae family has only one species that would be able to reach the

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Mediterranean, the African manatee, but this would require individuals of this species to go through the upwelling zone of northwestern Africa (coast of Morocco and West

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of Sahara), which is almost as equally impossible as passing through land, since this

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region has cold waters (McGregor et al., 2007) and practically no seagrass (Short et al.,

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2007).

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5. Conclusions

Observing the evolution of Sirenia in the European/North African realm, we can conclude that there were regional extinction events at two different moments. The first moment is related to the North Atlantic extinction. Sirenia first disappeared from these coastal shores, strongly affected by the lowering temperature and the reduced food supply. The second moment occurs with the Mediterranean extinction. In this case, temperature must have been the primordial factor. The main events are summarized as follows:

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The Northeast Atlantic has a low biodiversity of seagrasses, characterized by fragmented meadows. This means that Sirenia food resources were present in

Dugongids are highly dependent on seagrass, and the low biodiversity and

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

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small disperse areas;

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fragmented meadows of the North Atlantic, together with the cooling of the Northern Hemisphere, pushed the European dugongids towards the south; In the North Pacific region, the slow cooling of the Late Miocene, along with the

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

great biodiversity and low fragmentation of the seagrass meadows, allow

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Metaxytherium to adapt to the changing environment, evolving to Hydrodamalinae and inhabiting the cold waters of the Bering Sea; The North Atlantic disappearance is related to temperature changes and

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

Finding refuge in the Mediterranean, Sirenia remained present on the European

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

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pressure on food resources;

shores, and the Metaxytherium genus remained in existence, although already



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extinct in the rest of the world; Seagrass meadows are abundant today in the Mediterranean Sea and are not believed to have been different during the Pliocene. As such, there was no pressure on food resources in the Mediterranean Sea; 

The onset of the Northern Hemisphere continental glaciations was preceded by a rapid cooling and extinction events in the Mediterranean around 3.1 Ma. This is very close to the youngest records of Sirenia in the Mediterranean basin;

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The fact that the cooling of the Piacenzian was very rapid, in contrast to the one seen during the Late Miocene, is the reason why Mediterranean sirenians were unable to adapt to a colder environment. Sirenia are mammals with a low

ACCEPTED MANUSCRIPT metabolic rate, which means that adaptations to rapid temperature changes are unlikely to occur; So it seems that the European continental glaciations were determinant in the

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

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disappearance of European dugongids and the end of the Metaxytherium genus.

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The rapid cooling of the Northern Hemisphere prevented Sirenia from adapting to colder environments and they disappeared by the end of the Middle

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Piacenzian Warm Period.

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Acknowledgements

The authors thank Daryl P. Domning and Iyad Zalmout for all their help and

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constructive critics, which significantly improved the initial manuscript, as well as the

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6. References

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We studied the evolution of Sirenia in the Euro-North African realm

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We studied Sirenia food resources in this region between Upper Miocene and

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Pliocene We studied climate evolution during this interval

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Sirenia were primarily affected by changes in food resources, leading to refugee

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Northern Hemisphere Glaciations was the final event for Sirenia disappearance

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