Microsoft Word - 00_indice_BM03 Available online http:/amq.aiqua.it ISSN (print): 2279-7327, ISSN (online): 2279-7335 Alpine and Mediterranean Quaternary, 25 (1), 2012, 67-74 AN APPROACH TO BODY SIZE FLUCTUATIONS IN QUATERNARY CONTINENTAL MAMMALS: THE CASE OF HIPPOPOTAMUSES FROM WESTERN EUROPE Paul P.A. Mazza & Adele Bertini Dipartimento di Scienze della Terra, DST, Università degli Studi di Firenze, Italy Corresponding author: P.P.A. Mazza ABSTRACT: Several paleoenvironmental analyses show that community change over geological time is driven by ecological factors which, in turn, are regulated by climate. To most effectively examine the origin of community change researchers need to single out and track specific paleobiological properties and to see how much they depend on local or more general constraints. A suite of proxies have been used to analyze ecologically based community change. Body size is one of the most sensitive to ecological factors and is therefore deemed to disclose significant information on past environmental conditions. Bergmann’s rule proposes a thermoregulatory explanation to the latitudinal gradient of increasing animal body size. Whereas some animals fit the predictions of Bergmann's rule, others do not, or even correlate negatively. Several critical reviews cast doubts on the “thermal” interpretation of Bergmann’s rule, and proposed alterna- tive hypotheses for geographic variation in body size based on various physiological, biological and ecological constraints. The Ice Age cycling that was set off by the 2.6 Ma Arctic ice cap expansion led gradually to ever increasing environmental patchiness, and the effects of this habitat fragmentation became particularly evident in the Late Pleistocene and Holocene. Megafaunas progressively split up into metapopulations confined into ever smaller and more isolated habitats. This led numerous large mammals to experience endemic evolu- tion in isolation, and body sizes changed in ways similar to those observed in land mammals distributed on true islands. Keywords: Body size, Bergman’s rule, Mammals, Climate change, Quaternary. 1. INTRODUCTION The processes that cause community change over geological time have been one of the most investigated topics in paleoecology. To most effectively examine the- se processes researchers need to single out and track paleobiological properties unaffected by local con- straints. Body size is most sensitive to ecological factors and can disclose significant information on past envi- ronmental conditions. The pattern and extent of body size change in Quaternary land mammals has often been connected to climatic change (Tchernov, 1968; Davis, 1977, 1981; Klein, 1986). Quaternary is actually characterized by particularly unstable conditions, with long-term cooling trends and glacial cycles of ever in- creasing amplitude. There are two major, relatively ab- rupt climate transitions: one just before its onset, around 2.7 Myr ago, of a major northern hemisphere glaciation, the other is the so-called “mid-Pleistocene revolution” (MPR; Berger & Jansen, 1994) when the dominant peri- odicity of glacial response switched from 41 to 100 kyr. An equivalence can be established between the body size change of a specific taxon within a community over geological time, on the one hand, and the change of a phenotypic trait of an organism over geological time, on the other. As phenotypic changes reveal specific adapta- tions, so can body size changes provide information on the environmental modifications that caused them. Bergmann’s rule, pros and contras Many studies have highlighted the coincidence of climate or latitude change with size changes in various mammals. Bergmann (1847) observed a latitudinal in- crease in animal body size and proposed a thermoregu- latory explanation to the phenomenon. Climate/latitude- induced size change is often connected to peculiar al- lometric responses. In 1877 Joel A. Allen gave the fun- damentals of what was from then on known as Allen’s rule observing that land mammals from colder climates usually develop shorter limbs than their counterparts from warmer climates. Subsequently re-examined and reformulated, the so-called Bergmann’s rule (or mecha- nism sensu Meiri, 2011) was found to apply also to poi- kilotherm vertebrates, as well as to a number of inverte- brate taxa (e.g., Ashton, 2002; Makarieva et al., 2005, and references therein), which however are not subject to the heat-conservation mechanisms underlying Berg- mann’s rule. McLean (1991) believes that large mam- mals store more heat than smaller mammals, but cannot release it as much easily owing to their relatively small surface/volume ratios. The rapid warming at the transi- tion to an interglacial/interstadial phase causes greater embryogenesis dysfunction in larger mammals than in smaller ones (McLean, 1991). In these periods large mammals may therefore either disappear, experience dwarfing if they are given sufficient time to adapt to the new conditions, or otherwise reduce in size before be- coming extinct (Kurtén, 1972; Guthrie, 1984). Meiri & Dayan (2003) reviewed the occurrence of Bergmann’s rule in statistical samples of birds and mammals, ob- serving that over 72% of the birds and 65% of the mammals they examined conform to it. Meiri et al. (2007) revised these results finding that the mean varia- tion explained by latitude is 35% for birds and 37% for Mazza P.P.A., Bertini A. 68 mammals. Meiri & Dayan (2003) had also found that birds tend to adhere to Bergmann’s rule whatever their size, while smaller mammals (<500 g) conform signifi- cantly less than larger ones. The latter observation is consistent with the conclusions drawn by McDonald (1984), Martin (1984), Merilees (1984), and Ashton et al. (2000), who found that large land mammals had been more sensitive to the climatic oscillations than smaller ones. Meiri et al. (2004) obtained a significantly positive correlation between skull length and latitude in 50% of 44 carnivore species they examined, and a significantly negative correlation in 11% of those species. Diniz-Filho Fig. 1 - Curve through estimated average weights of Western European hippopotamuses, obtained from odontometric and osteometric data, as well as by using allometric scaling techniques (analysis in progress by the writers). Stratigraphic scheme modified from Bertini et al. (2010). Body size fluctuations in Quaternary hippopotamuses 69 et al. (2007) have also analyzed patterns of body size geographic variation in European carnivores. Rodríguez et al. (2006) observed nonlinear relationships between body size and temperature, finding a strong association in northern Europe, and virtually none in the south. Kur- tén (1968) and Huston & Wolverton (2011) propose the idea that mammal size is primarily connected with the amount and nature of food resources. Barnosky (2005) actually showed that most body-size reductions at the last glacial/interglacial transition were ecophenotypic rather than genotypic changes. Teplitsky et al. (2008) reached similar conclusions. In the light of these results, many authors have cast doubt on the “thermal” interpre- tation of Bergmann’s rule, finding that body size is con- trolled by many other factors rather than just tempera- ture. Some authors advocate various physiological, bio- logical and ecological constraints [(1) vascular control and fur insulation (Scholander 1955; Steudel et al., 1994); (2) food availability (Huston & Wolverton, 2011); (3) basal metabolic rate (Steudel et al., 1994); (4) ener- gy costs (Thompson, 1942); (5) size and nature of food (Teplitsky et al., 2008); (6) dominance in a community (Hansson & Jaarola, 1989); (7) competition (Simberloff & Boecklen, 1981); (8) mating success (Lande & Arnold, 1983)]. Others suggest additional climatic factors, such as moisture levels, demonstrating that small body size is associated with hot and humid conditions while larger size is connected to cooler and drier circumstances (Rosenzweig, 1968; James, 1970). Yom-Tov & Nix (1986) and Yom-Tov & Geffen (2006) observed that body size correlates with moisture and precipitation, and thus with primary production, better than with tempera- ture. Blois & Hadly (2009) linked body sizes to climate- change-related responses of vegetation and primary productivity. During the last decade, a wealth of studies analyzed the empirical validity of ecogeographic rules (Blackburn & Gaston, 1998; Blackburn et al., 1999; Angilletta & Dunham, 2003; Cruz et al., 2005; Millien et Species and specimens Ortona Colle Lepre Valdarno Colle Curti Untermaßfeld H. gr. H. an- tiquus (= H. tiberinus) Incarcal I H. amphibius (Barrington included) upper M2 (Janis, 1990) length x breadth (cm) 28.75 30.66 log 1.46 1.48 min length x breadth (cm) 22.56 25.3 23.04 18.49 log 1.35 1.4 1.36 1.26 max length x breadth (cm) 30.24 30.36 34.16 32.48 lower M2 (Janis, 1990) length (cm) 5,48 log 0.74 6.32 min length (cm) 5 6.6 5.2 0.8 log 0.7 0.82 0.71 max length (cm) 6.4 7 5.9 log 0.8 0.84 0.77 Femur (allometric scaling: Schmidt- Nielsen, 1984; Reitz and Quitmyer, 1988; Prange et al., 1979) DC (cm) 9.5 11.7 log 0.98 1.07 DC min (cm) 9.5 9.5 8.7 7.4 log 0.98 0.98 0.94 0.87 DC max (cm) 10.8 10.2 9.3 8.6 log 1.03 1.01 0.97 0.93 Fifth metatarsal (allometric scaling: Schmidt-Nielsen, 1984; Reitz and Quitmyer, 1988; Prange et al., 1979) length (cm) 9.92 9.3 log 0.99 0.97 min length (cm) 9.5 10 9.9 10.3 log 0.98 1.00 0.99 1.01 max length (cm) 11 10.7 10.8 10.9 log 1.04 1.03 1.03 1.04 estimated weights (kg) 1000- 2100 2200 2100-2750 2100- 2600 2200-3200 1700-2750 2000 1260-3000 Tab. 1 - Body weight estimates Mazza P.P.A., Bertini A. 70 al., 2006; Rodríguez et al., 2006, 2007; Gaston et al., 2007; Meiri & Gavin, 2007; Meiri et al., 2007; Aragón et al., 2010; Gardner et al., 2011). Many of these factors suggested as alternatives to Bergmann’s rule could be more or less directly correlated, or at least influenced, by the environmental and climatic changes that oc- curred over the last 2 million years. Quaternary climate instability caused changes in the vegetation (e.g., Lang, 1994; Bertini, 2003, 2010; Tzedakis, 2003, 2007; Gon- zález-Sampériz et al., 2010; Rodriguez-Sanchez et al., 2010; Joannin et al., 2011; Magri & Palombo, 2012), as well as the progressive fragmentation of the ecosys- tems, with consequences on the fauna that are de- scribed further on. 2. BODY SIZE CHANGE IN QUATERNARY HIPPO- POTAMUSES: A WESTERN EUROPEAN EXAMPLE In Western Europe, the significant changes in temperature and precipitation ensuing from the maxi- mum expansion of the Arctic ice cap that set off the Ice Age cycling caused the progressive demise of tropical and subtropical forest taxa, while altitudinal arboreal taxa and herbs spread, with the creation of new compe- tition patterns (e.g., Suc et al., 1995; Bertini, 2010, Ber- tini et al., 2010; Fig. 1). Vegetational modifications clear- ly reflect substantial paleoecological and paleoclimatic reorganizations. Most commonly, but not exclusively (e.g., Bertini, 2010), Artemisia and Ephedra-dominated open vegetation alternated with interglacial forests characterized by deciduous taxa, such as Quercus, Carya, Carpinus, Pterocarya, Ulmus and Zelkova in re- sponse to the Early Pleistocene 41 kyr climatic cycling. A ca. 100 kyr (eccentricity) cycling, which started since the transition to the Middle Pleistocene, intensified the glacial phenomena, but also seasonality and aridity. This had disrupting consequences on both flora and fauna. Many resident animal taxa became extinct, whereas others were replaced by new incomers from eastern Europe, central Asia, and Africa. Some of the Western European inhabitants seem to have changed size in coincidence with climatic variations. Hippopota- muses might represent a good example (Fig.1). If the body sizes of European Quaternary hippopotamus are estimated from stratigraphically controlled remains, it seems that these pachyderms grew smaller from the Jaramillo subchron onwards (Table 1). During the se- cond half of the Middle Pleistocene these suiforms turned progressively rarer, especially during the coldest phases of this interval (MIS 8, 6). At the beginning of the Late Pleistocene, during the very warm MIS 5e, large to very large hippopotamuses dispersed as far north as the British Isles. It is worth noting that Western European hippopotamuses grew smaller in coincidence with the MPR (~1.2÷0.5 Ma) and just after the disappearance of the subtropical vegetal ecosystems from the Mediterra- nean area, around 1.2 Ma (e.g. Combourieu-Nebout & Vergnaud-Grazzini, 1991; Bertini, 2010). The great modifications in the structure and composition of vegetal formations induced by the long lasting glacial phases (up to 85 ka) and short interglacial phases (up to 15 ka) of this time period had significant consequences on the type and availability of food for the fauna. In a working hypothesis in preparation by the writers, hippopotamus- es turned smaller under the prevalently cooler Middle Pleistocene conditions, in contrast to Bergmann’s predict- ed pattern, as an indirect response to climatic change, owing to the unsteadiness in food availability. This would fully agree with Kurtén’s (1968) and Huston & Wolverton’s (2011) idea that mammal size is primarily connected with the amount and nature of food resources. 3. THE “INSULARIZATION” OF QUATERNARY CON- TINENTAL MAMMALS The MPR caused increasing habitat fragmentation (Simakova, 2001; Markova et al., 2001; Zazula et al., 2003), whose effects became particularly evident in the Late Pleistocene and Holocene. The mosaic evolution of plant communities, as habitats grew smaller and more isolated, turning into habitat islands (Lister & Bahn, 1994; Ward, 1997; Reumer, 2007), affected the evolu- tionnary relationships between herbivores and the vege- tation (Graham & Lundelius, 1984). Megafaunas pro- gressively broke down into metapopulations. As interbreeding became ever more infrequent, subpopulations were increasingly exposed to the effects of inbreeding, genetic drift as well as morphological change. When the intensity of interbreeding turned ex- cessively low, evolutionary change tended to resemble that of insular settings (Schmidt & Jensen, 2003). Numer- ous mammals grew smaller (e.g., edentates, mastodonts, wild boar, gazelle, goat, aurochs, bison, deer, fox, wildcat, spotted hyena, beech marten, burrowing mole rat, hedgehog, porcupine: Kurtén, 1965; Tchernov, 1968; Frenkel, 1970; Heller, 1970; McDonald, 1981; King & Saunders, 1984; Martin, 1993; Martin & Barnosky 1993; Wilson, 1996; Barnosky et al., 2003; Blackburn & Haw- kins, 2004, Rodríguez et al., 2006, Cooper & Purvis, 2010; Saunders et al., 2010), with results somewhat fitting the predictions of the so-called Island Rule (Foster, 1964; Sondaar, 1977). Insular populations, both in true and eco- logical islands, are in fact under the control of strict genet- ic and ecological constraints (Lomolino et al., 2010). As in true islands, in isolated ecosystems popula- tion densities are bracketed between a maximum number of individuals, determined by the carrying ca- pacity of the environment, and a critical minimum number of individuals to prevent extinction. Large- sized animals seems to be left with no other choice but to decrease their size to lower selective pressure in insular isolation. 4. CONCLUSIONS Because mammal body size is most sensitive to ecological factors, size changes are often considered as a useful proxy indicator to monitor climatic changes, not only in the past. In fact, declining body size has recently been considered the third universal response to climate, together with changes in phenology and distribution of species (Gardner et al., 2011). In his pioneer contribution Bergmann (1847) stirred debate over the relation be- tween temperature and body size. The controversy peaked over the years, with convinced supporters and opponents both with shrill and convincing arguments on the merits or shortcomings of Bergmann’s rule. Many Body size fluctuations in Quaternary hippopotamuses 71 studies have admirably shown that mammalian body size is governed by, and responds to, a number of factors, which include temperature, precipitation and moisture, physiologic constraints, basal metabolic rate and energy costs, environmental carrying capacity (food availability), degrees of environmental stability, interspecific com- petition, predator-prey interaction, just to mention some. A body size that is thought to be diagnostic of a particular environmental situation may actually arise for different reasons, being the result of the interplay of an array of factors which may be, to various degrees, interdependent. Researchers involved with these issues are therefore confronted with a tangled network of related variables, which imposes to inquire each instance individually, on a case-by-case basis: model (“Rule”) generalization is not easy to achieve. Today, researchers could have the un- precedented opportunity to test the effects of global warming on fast-reproducing animals (e.g., Gardner et al., 2011). Paleoclimatological analysis and oxygen isotope curves clearly show that, with the outstanding exceptions of particularly warm episodes (e.g., MIS 47, 37, 11, 9, 5e), Earth’s climate has been progressively deteriorating over time, trending towards increasingly cooler and somewhat drier conditions. The escalating environmental patchiness during the Quaternary translated into habitat fragmenta- tion, and this in turn caused the splitting up of populations into subpopulations or metapopulations. 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