Animals share their living space with many other species. Evolutionary conflicts arise when species compete over the same resource such as food or shelter, and such conflicts may not only influence the composition of mammal assemblages but also may be the driving force for evolutionary specialization, speciation and radiation. We investigate ecological and physiological adaptations in mammals to delineate the factors that make species ecologically and evolutionarily successful in assemblages and ecosystems which are increasingly affected by humans.

Phylogeography of wildlife

Speciation is both driven by genetic drift (key innovations by chance) and selection pressures leading to different evolutionary adaptations of diverging populations. In this context we investigate how extrinsic factors such as climate changes (e.g. during pleistocenic ice ages), catastrophic events (e.g. volcanic eruptions) or anthropogenic selection (e.g. domestication) as well as intrinsic factors (genetic basis for life history traits) influenced population differentiation and speciation. Our studies are carried out in different areas and time horizons and on a variety of species.

For instance, the biodiversity hotspot of the Sunda Shelf in Southeast Asia provides a unique opportunity to investigate the formation of the current species distribution pattern, as falling and rising sea levels periodically either connected or separated the larger islands of the shelf. Recent studies on several carnivore species revealed deep historical splits between populations of these species, not solely explainable by oscillating climatic conditions. As a consequence, we have incorporated the eruption of the Toba volcano on Sumatra ~74.000 years ago into scenarios which explain current species distribution.

Another example is the evolution of genetically distinct clades in European mammals (e.g. European brown hare, red deer), caused by pleistocenic ice ages during which populations of many species were forced to retreat to different, spatially very distant refugia. These refugia caused the inhibition of gene flow between refugial populations and the remainder of the species, thus allowing for independent genetic evolution of enclosed populations.

Niche separation and adaptive diversification: Using bats as a model

Bats (order Chiroptera) are one of the largest groups of mammals and important providers of ecosystem services; therefore bats are a most relevant model group to study questions of niche separation and adaptive radiation. Bats of the New World family Phyllostomidae are particularly interesting because they are an extremely diverse family with respect to their ecology in general and their feeding habits in particular. Radiation within this group was most likely initiated by the evolution of a specific skull morphology that enabled ancestral phyllostomids to use a variety of novel resources and to enter a new adaptive zone. Nowadays, phyllostomid bats contribute with the largest number of species to mammalian assemblages in the Neotropics. Recently, IZW researchers have highlighted that one of the global biodiversity hotspots, the Ecuadorian Yasuní Biosphere Reserve, harbors more than 120 bat species, ten times more than in forests of the temperate zone. The large majority of the Yasuní bat assemblage consists of phyllostomid bats. But how do bats cope with so many other bats in the same habitat? First, species are spatially separated, for example by living in different forest strata such as understorey and canopy. Second, their diets are quite flexible so that they can easily switch to alternative food sources once a given food resource becomes scarce. Current research looks into the functional mechanisms that preclude or facilitate co-existence within such species rich tropical assemblages.

Energetic costs of locomotion

In animals, finding food or finding a partner usually requires some form of movement. However, movement involves energetic costs that may define if it is efficient for an animal to travel a given distance or to make use of a certain habitat. Powered flight is the key innovation for Chiropteran evolution, because it enables bats to travel in a cost efficient mode over long distances (low costs of transport). Yet, mass-specific metabolic rates of flying bats are drastically higher than those of mammals with quadrupedal locomotino. Consequently, bats have to be particularly efficient in balancing the potential gain obtained by exploring novel habitats against the involved metabolic costs. We currently study two questions with respect to the movement ecology of bats: First, what are the metabolic costs of bat flight? Second, what is the fuel of bat flight?

The metabolic costs of bat flight depends on various factors, including extrinsic (e.g. environmental conditions and habitat complexity) and intrinsic factors (e.g. wing morphology and flight behavior). Recently, we confirmed that echolocation does not add additional energy costs to the power requirements of flight, suggesting that bats benefit from coupling echolocation pulses to their wing beat cycle while flying. Further studies highlighted that species with long and slender wings that are particularly well adapted for fast flight (members of the Molossidae) are excluded from foraging in more confined spaces (e.g. forest gaps) because of the high energetic costs caused by balancing the centrifugal forces during quick turns. Thus, wing morphology seems to define largely what kind of habitat a bat may use and also how it may use it. For example, two ecologically similar species within the genus Rhinolophus experience contrasting metabolic rates because of their different wing morphology, defining their foraging mode either as a flycatcher type or as an aerial forager.

Aerial locomotion is energetically expensive, and thus bats seem to work as endurance athletes on a daily basis. What kind of oxidative fuel do bats use to power flight? Nectar-feeding and fruit-eating bats, for example, are able to supply their metabolism solely by oxidation of dietary sugars from nectar or fruits. Our studies also suggest that insectivorous bats use ingesta to power their flight rather than relying on endogenous energy reserves on a regular basis. This contrasts with terrestrial mammals that are limited in the use of exogenous nutrients for maintaining their metabolic rates; humans, for example, are only able to power only about 30% of their metabolism with ingesta. But how about endurance fliers like migratory bats? Recently, we documented that migratory Nathusius pipistrelle use a mixed fuel to power their migratory flights from Northeastern to Southwestern Europe, i.e. as an oxidative fuel they use a combination of consumed insects and fatty acids derived from their body reserves. Current research focuses on the biochemical and cellular adaptations of bats to perform such long-distance migrations.

Spatial and temporal habitat use

Knowing what an animal is doing where and when is crucial for understanding habitat use, ecosystem dynamics and the detection of unusual behaviours or responses such as responses to disturbances or predators. Studies on wild animals equipped with GPS-collars provide valuable information on the locations used by individuals over longer periods and these can be related to local habitat availability, food availability, and ideally even to specific behaviours expressed in different habitats and at different times. Of great importance is the idea that animals do not just search for food (or at specific times for mates) but also move through a ‘landscape of fear’ characterised by varying probabilities of being either disturbed or predated upon by people or by natural enemies. Our focus is therefore on the movement ecology of both ungulates and carnivores in temperate and tropical and subtropical environments, such as roe deer, black bear or leopard, where we study the trade-off between searching for food and avoiding risks. The detailed analysis of movements also permits an assessment of the ecosystem services / roles provided by these species, particularly their impact on their habitats and ecosystems in relation to their seasonal adaptations and interspecific interactions.

GPS on its own provides only limited information on the habitat use of animals. We therefore develop methods to distinguish between different behavioural categories based on activity values generated by acceleration sensors embedded in GPS-collars. Such acceleration sensors provide a unique way to document behaviour of wildlife under free-ranging conditions in high resolution and are part of a revolution currently under way within the field of movement ecology. By carefully testing acceleration sensors within collars attached to real animals but under controlled conditions it is possible to classify acceleration values as being an expression of a specific behaviour, particularly if such behaviours have also a specific spatial point of reference. We have successfully tested this on ungulates and carnivores. For instance, the successful differentiation between feeding and non-feeding activity in leopards provided a useful tool to detect kill sites in rugged and largely inaccessible regions where direct observations and scat collections may be challenging.

Feeding ecology and digestive strategies of wildlife

Larger mammals evolved a variety of behavioral and physiological strategies to adapt to their specific nutritional environment, to cope with seasonal and spatial variation in food resources, with competitors and predators. Especially herbivores found numerous morphological and physiological solutions to process food differing in both nutrient and antifeedant (secondary plant compounds) content, such as foregut or hindgut fermentation, rumination and coprophagy. In cooperation with several international zoos and research institutes the IZW conducts and participates in feeding experiments to understanding the evolution of physiological and morphological adaptations, to characterize the effect of secondary plant compounds such as tannin, to develop husbandry recommendations and to develop and improve non-invasive methods for estimating digestion patterns and energy budgets of free ranging populations.

Recent studies showed that ruminating and non-ruminating foregut fermenters differ in their excretion pattern of particles and fluid, which might be a prerequisite for the sorting process of rumination. And even among ruminants in the family Bovidae different digestion types are found such as the moose-type and the cattle-type, which was unexpected and thought to be limited to non-bovids. Studies on digestion physiology of captive animals allow distinct, controlled experimental set-ups and are an extremely valuable complement to field studies. For instance, in bonobos in captive facilities energy consumption and nutritional stress was monitored by using isotopic and elemental analyses of urine, and since urine is relatively easy to sample from free-ranging habituated apes it should be possible to calculate energy budgets from undisturbed populations as well.

Free-ranging animals in temperate and even in tropic habitats often have to cope with seasonal changes in food availability and food quality resulting in fluctuations of body mass and body condition. Gorillas as well as chimpanzees are able to optimize individual energy and protein gain by choosing an appropriate diet of food plants (abundant, rich in macronutrients such as sugar and protein, and low in secondary plant components) and by behavioral adjustments such as reducing daily journey length and increasing feeding time.

Morphological adaptations: Production mechanism of elephant rumbles

A typical vocalization of elephant communication is the rumble, a low-frequent “rumbling” sound below 20 Hz. It has been speculated that this type of infrasonic vocalization might be produced either by a “purring” mechanism, i.e. individually nerve-controlled muscle twitching (intermittent activation of intrinsic laryngeal muscles by stereotyped nerve discharges) as in cat purring, or by sustained oscillations of the vocal folds requiring coordinated lasting intrinsic laryngeal muscle contractions and the expiratory air flow as a driving force. Infrasound vocalization with an average fundamental frequency of 16.38 Hz (range: 5-60 Hz) could be experimentally produced in an excised larynx of an African elephant. Lasting intrinsic muscle contractions were simulated by manipulating the arytenoids, thereby tensing and adducting the roughly 10 cm long elephant vocal folds towards a vocalizing position. As there cannot be any nervous input in an excised larynx experiment, successful production of rumble-like vocalizations in this set-up strongly suggests that the second mechanism can account for the production of rumbles in the live animal. The frequent occurrence of nonlinear phenomena (period doubling, biphonation, bifurcation) might in part result from the large dimensions of the elephant vocal folds, facilitating higher-order modes of oscillation. Calculation of fundamental frequency on the basis of the piano-string model and a measured vocal fold length of 10.4 cm in the investigated specimen predict a fundamental frequency of 18.43 Hz, which is remarkably close to the mean fundamental frequency measured in the excised larynx experiments. It appears that the low fundamental frequency of the elephant rumble is directly related to the dimensions and tension of the oscillating vocal folds. Thus, the elephant larynx and vocal folds function in a similar way as those of other mammals and humans. The flow-induced vocal fold oscillations inside the larynx are capable of producing the very intense low-frequency rumbles that elephants use in their long-distance communication.

Selected publications

Deschner T, Fuller BT, Oelze VM, Boesch C, Hublin JJ, Mundry R, Richards MP, Ortmann S, Hohmann G (2012) Identification of energy consumption and nutritional stress by isotopic and elemental analysis of urine in bonobos (Pan paniscus). Rapid Commun Mass Spectrom 26: 69-77.

Dumont ER, Dávalos LM, Goldberg A, Santana SE, Rex K, Voigt CC (2012) Morphological innovation, diversification and invasion of a new adaptive zone. Proc R Soc Lond B 279: 1797-1805.

Herbst CT, Stoeger AS, Frey R, Lohscheller J, Titze IR, Gumpenberger M, Fitch WT (2012) How low can you go? Physical production mechanism of elephant infrasonic vocalizations. Science 337: 595-599.

Popa-Lisseanu AG, Soergel K, Luckner A, Wassenaar LI, Ibáñez C, Ciechanowski M, Görföl T, Niermann I, Beuneux G, Myslajek R, Juste J, Fonderflick J, Kramer-Schadt S, Kelm DH, Voigt CC (2012) A triple isotope approach to predict breeding origins of European bats. PLoS ONE 7.

Pruvost M, Bellone R, Benecke N, Sandoval-Castellanos E, Cieslak M, Kuznetsova T, Morales-Muniz A, O'Connor T, Reissmann M, Hofreiter M, Ludwig A (2012) Genotypes of predomestic horses match phenotypes painted in Paleolithic works of cave art. PNAS 108: 18626-18630.

Voigt CC, Sörgel K, Suba J, Keiss O, Petersons G (2012) The insectivorous bat Pipistrellus nathusii uses a mixed-fuel strategy to power autumn migration. Proc R Soc Lond B 279: 3772-3778.

Voigt CC, Lewanzik D (2012) ‘No cost for echolocation in flying bats’ revisited. J Comp Physiol B 182: 831-40.

Voigt CC, Voigt-Heucke SL, Kretzschmar A (2012) Isotopic evidence for seed transfer from successional area into forests by short-tailed fruit bats (genus Carollia; Phyllostomidae). J Trop Ecol 28: 181-186.

Voigt CC, Voigt-Heucke S, Schneeberger K (2012) Isotopic data do not support food sharing within large networks of female vampire bats (Desmodus rotundus). Ethology 118: 260-268.

Voigt CC, Holderied MW (2012) High manoeuvring costs force narrow-winged molossid bats to forage in open space. J Comp Physiol B 182: 415-424.

Wilting A, Fickel J (2012) Phylogenetic relationship of two threatened endemic viverrids from the Sunda Islands, Hose’s civet and Sulawesi civet. J Zool 288: 184-190.

Wilting A, Meijaard E, Helgen K, Fickel J (2012) Mentawai’s endemic, relictual fauna: is it evidence for Pleistocene extinctions on Sumatra? J Biogeography 39: 1608-1620.

Clauss M, Lunt N, Ortmann S, Plowman A, Codron D, Hummel J (2011) Fluid and particle passage in three duiker species. Eur J Wildl Res 57: 143-148.

Erzberger A, Popa-Lisseanu AG, Lehmann GUC, Voigt CC (2011) Potential and limits in detecting altitudinal movements of bats using stable hydrogen isotope ratios of fur keratin. Acta Chiropterol 13: 431-438.

Hambly C, Voigt CC (2011) Measuring energy expenditure in birds using bolus injections of 13C labelled Na-bicarbonate. Comp Biochem Physiol A 158: 323-328.

Hebel C, Ortmann S, Hammer S, Hammer C, Fritz J, Hummel J, Clauss M (2011) Solute and particle retention in the digestive tract of the Phillip's dikdik (Madoqua saltiana phillipsi), a very small browsing ruminant: Biological and methodological implications. Comp Biochem Physiol A 159: 284-290.

Kelm DH, Simon R, Kuhlow D, Voigt CC, Ristow M (2011) High activity enables life on a high sugar diet: blood glucose regulation in nectar-feeding bats. Proc R Soc Lond B 278: 3490-3496.

Meyer CFJ, Aguiar LMS, Aguirre LF, Baumgarten J, Clarke FM, Cosson J-F, Villegas SE, Fahr J, Faria D, Furey N, Henry M, Hodgkison R, Jenkins RKB, Jung KG, Pons J-M, Kunz TH, MacSwiney Gonzalez MC, Moya I, Voigt CC, von Stade, D, Weise CD, Kalko EKV (2011) Estimating species richness and detectability in tropical bat surveys. J Appl Ecol 48: 777-787.

Rex K, Michener R, Kunz TH, Voigt CC (2011) Vertical stratification of Neotropical leaf-nosed bats (Phyllostomidae: Chiroptera) revealed by stable carbon isotopes. J Trop Ecol 27: 211-222.

Schwarm A, Albrecht S, Ortmann S, Wolf C, Clauss M (2011) Digesta retention time in roe deer Capreolus capreolus, as measured with cerium-, lanthanum- and chromium-mordanted fibre. Eur J Wildl Res 57: 437-442.

Siemers BM, Greif S, Borissov I, Voigt-Heucke SL, Voigt CC (2011) Divergent trophic levels in two cryptic sibling bat species. Oecologia 166: 69-78.

Voigt CC, Lewanzik D (2011) Trapped in the darkness of the night: Thermal and energetic constraints of daylight flight in bats. Proc R Soc Lond B 278: 2311-2317.

Voigt CC, Akbar Z, Kunz TH, Kingston T (2011) Sources of assimilated proteins in old and new world phytophagous bats. Biotropica 43:108-113.

Voigt CC, Schneeberger K, Voigt-Heucke SL, Lewanzik D (2011) Rain increases the energy cost of bat flight. Biol Lett 7: 793-795.

Wilting A, Christiansen P, Kitchener A, Kemp YJM, Ambu L, Fickel J (2011) Geographical variation in and evolutionary history of the Sunda clouded leopard (Neofelis diardi) (Mammalia: Carnivora: Felidae) with the description of a new subspecies from Borneo. Mol Phyl Evol 58: 317-328.

Amitai O, Amichai E, Holtze S, Barkan S, Korine C, Pinshow B, Voigt CC (2010) Fruit bats (Pteropodidae) fuel their metabolism rapidly and directly with exogenous sugars. J Exp Biol 213: 2693-2699.

Bass M, Finer M, Jenkins CN, Kreft H, Cisneros-Heredia DF, McCracken SF, Pitman NCA, English PA, Swing K, Villa G, DiFiore A, Voigt CC, Kunz TH (2010) Global conservation significance of Ecuador’s Yasuní National Park. PLoS ONE 5.

Meyer CFJ, Aguiar LMS, Aguirre LF Baumgarten J, Clarke FM, Cosson J-F, Villegas SE, Fahr J, Faria D, Furey N, Henry M, Hodgkison R, Jenkins RKB, Jung KG, Pons J-M, Kunz TH, MacSwiney Gonzalez MC, Moya I, Voigt CC, von Staden D, Weise CD, Kalko EKV (2010) Long-term monitoring of tropical bats for anthropogenic impact assessment: Gauging the statistical power to detect population change. Biol Cons 143: 2797-2807.

Hohmann G, Potts K, N'Guessan A, Fowler A, Mundry R, Ganzhorn JU, Ortmann S (2010) Plant foods consumed by Pan: Exploring the variation of nutritional ecology across Africa. Am J Phys Anthropol 141: 476-485.

Patou ML, Wilting A, Gaubert P, Esselstyn JA, Cruaud C, Jennings AP, Fickel J, Veron G (2010) Evolutionary history of the Paradoxurus palm civets – a new model for Asian biogeography. J Biogeography 37: 2077-2097.

Rex K, Czaczkes BI, Michener R, Kunz TH, Voigt CC (2010) Specialisation and omnivory in diverse mammalian assemblages. Ecoscience 17: 37-46.

Schwarm A, Ortmann S, Rietschel W, Kühne R, Wibbelt G, Clauss M (2010) Function, size and form of the gastrointestinal tract of the collared Pecari tajacu (Linnaeus 1758) and white-lipped peccary Tayassu pecari (Link 1795). Eur J Wildl Res 56: 569-576.

Voigt CC (2010) Insights into strata use of forest animals using the ‘canopy effect’. Biotropica 42: 634-637.

Voigt CC, Schuller BM, Greif S, Siemers BM (2010) Perch-hunting in insectivorous Rhinolophus bats is related to the high energy costs of manoeuvring in flight. J CompPhysiol B 180: 1079-1088.

Voigt CC, Sörgel K, Dechmann DKN (2010) Refuelling while flying: Foraging bats combust food rapidly and directly to fuel flight. Ecology 91: 2908-2917.

Ganas J, Ortmann S, Robbins M (2009) Food choices of the mountain gorilla in Bwindi Impenetrable National Park, Uganda: the influence of nutrients, phenolics and availability. J Trop Ecol 25: 123-134

Ludwig A, Pruvost M, Reissmann M, Benecke N, Brockmann GA, Castaños P, Cieslak M, Lippold S, Llorente L, Malaspinas A-S, Slatkin M, Hofreiter M (2009) Coat color variation at the beginning of horse domestication. Science 324: 485.

N’guessan A, Ortmann S, Boesch C (2009) Daily energy balance and protein gain among Pan troglodytes verus in the Tai National Park, Cote d'Ivoire. Int J Primatol 30: 481-496.

Popa-Lisseanu A, Voigt CC (2009) Bats on the move. J Mammal 90: 1283-1290.

Schwarm A, Ortmann S, Wolf C, Streich WJ, Clauss M (2009) More efficient mastication allows increasing intake without compromising digestibility or necessitating a larger gut: Comparative feeding trials in banteng (Bos javanicus) and pygmy hippopotamus (Hexaprotodon liberiensis). Comp Biochem Physiol A 152: 504-512.

Schwarm A, Ortmann S, Wolf C, Streich WJ, Clauss M (2009). Passage marker excretion in red kangaroo (Macropus rufus), collared peccary (Pecari tajacu) and colobine monkeys (Colobus angolensis, C. polykomos, Trachypithecus johnii). J Exp Zool A 311: 647-661.

Voigt CC (2009) Studying animal diets in-situ using portable infra-red stable isotope analyzers. Biotropica 41: 271-274.

Fickel J, Hauffe HC, Pecchioli E, Soriguer R, Vapa L, Pitra C (2008). Cladogenesis of the European brown hare (Lepus europaeus Pallas, 1778). Eur J Wildlife Res 54: 495-510.

Ganas J, Ortmann S, Robbins M (2008) Food preferences of wild mountain gorillas. Am J Primatol 70: 927-938.

Rex K, Kelm DH, Wiesner K, Matt F, Kunz TH, Voigt CC (2008) Species richness and tructure of three Neotropical bat assemblages. Biol J Linn Soc 94: 617-629.

Voigt CC, Baier L, Speakman JR, Siemers BM (2008)Stable carbon isotopes in exhaled breath as tracers for dietary information in birds and mammals. J Exp Biol 211: 2233-2238.

Voigt CC, Rex K, Michener RH, Speakman JR (2008) Nutrient routing in omnivorous animals tracked by stable carbon isotopes in tissue and exhaled breath. Oecologia 157: 31-40.

Voigt CC, Grasse P, Rex K, Hetz SK, Speakman JR (2008) Bat breath reveals metabolic substrate use in free-ranging vampires. J Comp Physiol 178: 9-16.

Voigt CC, Speakman JR (2007) Nectar-feeding bats fuel their high metabolism directly with exogenous carbohydrates. Funct Ecol 21: 913-921.

Clauss M, Castell JC, Kienzle E, Dierenfeld ES, Flach EJ, Behlert O, Ortmann S, Streich WJ, Hummel J, Hatt J-M (2007) The influence of dietary tannin supplementation on digestive performance in captive black rhinoceros (Diceros bicornis). J Anim Physiol Anim Nutr 91: 449-458.

Clauss M, Schwarm A, Ortmann S, Streich WJ, Hummel J (2007) A case of non-scaling in mammalian physiology? Body size, digestive capacity, food intake, and ingesta passage in mammalian herbivores. Comp Biochem Physiol A 148: 249-265.