Abstract
Field and laboratory studies of the iconic nectarivorous and ‘pollenivorous’ honey possum, Tarsipes rostratus, are reviewed with the aim of identifying aspects of its physiology that are as yet poorly understood and needed to implement management strategies for its long-term conservation. Dietary specialisations include the loss of teeth, a modified gut with a high rate of passage, exceptionally low minimum nitrogen requirements, an apparently high basal metabolic rate and a permanently polyuric kidney. In contrast, its reproductive physiology is plesiomorphic, combining aspects such as a post-partum oestrus, embryonic diapause, photoperiodicity and extended maternal care that are usually separate characteristics of other marsupial groups. In common with a number of other marsupials, the honey possum has the potential for trichromatic colour vision and has been the subject of several studies attempting to correlate visual quality with ecological realities. Field physiological studies have established its high rates of nectar and pollen intake needed to maintain energy balance and highlight the need for a constant intake from floral sources. Early allometric studies suggesting that the honey possum’s relatively low reproductive rate may be linked to a diet limited in protein have not been supported and nitrogen intakes in the field exceed by a factor of 10 the animal’s basic requirements for balance. Measurements of rates of protein turnover in field-caught lactating females suggest that they divert nitrogen from the protein pool to milk production by reducing rates of degradation, rather than by increasing rates of synthesis of protein. Although not yet an endangered species, the honey possum’s habitat has been drastically reduced since European occupation of Australia and future-targeted research on the animal’s unique physiology and habitat linkage is needed that can be translated into effective management practices. Only then will its long-term survival be assured.
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Abbreviations
- BMR:
-
Basal metabolic rate
- SMR:
-
Standard metabolic rate
- FMR:
-
Field metabolic rate
- T b min :
-
Minimal body temperature in torpor
- k b :
-
Biological elimination rate
- DLW:
-
Doubly labelled water method
- CCK:
-
Cholecystokinin
- BPP:
-
Bovine pancreatic polypeptide
- MRT:
-
Mean retention time
- SNP:
-
Scott National Park
- FRNP:
-
Fitzgerald River National Park
- OPR:
-
Offspring production rate
- N:
-
Nitrogen
- MNR:
-
Maintenance nitrogen requirements
- MFN:
-
Metabolic faecal nitrogen
- EUN:
-
Endogenous urinary nitrogen excretion
- BV:
-
Biological value
- MWP:
-
Metabolic water production
- TDN:
-
Truly digestible nitrogen intake
- PM :
-
Progesterone metabolites (progestagens)
- E2 :
-
Oestradiol-17β
- C urea :
-
Clearance of urea
- C IN :
-
Clearance of inulin (=GFR)
- C urea/C IN :
-
Clearance ratio of urea
- RMT:
-
Relative medullary thickness
- RMA:
-
Relative medullary area
- JMN:
-
Juxtaglomerular nephrons
- GFR:
-
Glomerular filtration rate
- SWS:
-
Short-wavelength sensitive
- MWS:
-
Middle-wavelength sensitive
- LWS:
-
Long-wavelength sensitive
- UVS:
-
Ultraviolet sensitive
- MSP:
-
Microspectrophotometry
- VMN:
-
Vomeronasal organ
References
Aplin KP, Archer M (1987) Recent advances in marsupial systematics with a new syncretic classification. In: Archer M (ed) Possums and opossums: studies in evolution. Surrey Beatty and Sons Pty Ltd, Sydney, pp xv–lxxii
Archer M, Kirsch JAW (2006) The evolution and classification of marsupials. In: Armati P, Dickman CR, Hume ID (eds) Marsupials. Cambridge University Press, New York, pp 1–21
Arrese C, Archer M, Beazley LD (2002a) Visual capabilities in a crepuscular marsupial, the honey possum (Tarsipes rostratus): a visual approach to ecology. J Zool (Lond) 256:151–158
Arrese CA, Hart NS, Thomas N, Beazley LD, Shand J (2002b) Trichromacy in Australian marsupials. Curr Biol 12:657–660
Arrese C, Oddy AY, Runham PB, Hart NS, Shand J, Hunt DM, Beazley LD (2005) Cone topography and spectral sensitivity in two potentially trichromatic marsupials, the quokka (Setonix brachyurus) and quenda (Isoodon obesulus). Proc Roy Soc B 272:791–796
Arrese C, Beazley LD, Neumeyer C (2006) Behavioural evidence for marsupial trichomacy. Curr Biol 16:R193–R194
Austad SN, Fischer KE (1991) Mammalian aging, metabolism and ecology—evidence from the bats and marsupials. J Gerontol 46:847–853
Baggett HA (1978) The tongue of Tarsipes. Bull Aust Mamm Soc 5:44
Bakker HR, Bradshaw SD (1983) Renal function in the spectacled Hare Wallaby (Lagorchestes conspicillatus): effects of dehydration and protein deficiency. Aust J Zool 31:101–108
Bankir L, de Rouffignac C (1985) Urinary concentrating ability: insights from comparative anatomy. Am J Physiol 249:R643–R666
Barboza PS, Hume ID, Nolan JV (1993) Nitrogen metabolism and requirements of nitrogen and energy in wombats (Marsupialia: Vombatidae). Physiol Zool 66:807–828
Barker S (1968) Nitrogen balance and water intake in the Kangaroo Island wallaby, Protemnodon eugenii (Desmarest). Aust J Exp Biol Med Sci 46:17–32
Barret G (1995) Pollen loads of vertebrates in heath vegetation during autumn at Eneabba. West Aust Nat 20:155–158
Beattie AJ (1971) A technique for the study of insect-borne pollen. Pan Pac Entomol 47:82
Berger PJ (1966) Eleven-month ‘embryonic diapause’ in a marsupial. Nature 211:435–436
Berger PJ, Sharman GB (1969) Progesterone-induced development of dormant blastocysts in the tammar wallaby, Macropus eugenii Desmarest: Marsupialia. J Reprod Fert 20:201–210
Beuchat CA (1990) Body size, medullary thickness, and urine concentrating ability in mammals. Am J Physiol 258:R298–R308
Bradshaw SD (2003) Vertebrate ecophysiology: an introduction to its principles and applications. Cambridge University Press, Cambridge
Bradshaw SD, Bradshaw FJ (1999) Field energetics and the estimation of pollen and nectar intake in the marsupial honey possum, Tarsipes rostratus, in heathland habitats of south-western Australia. J Comp Physiol B 169:569–580
Bradshaw FJ, Bradshaw SD (2001) Maintenance nitrogen requirement of an obligate nectarivore, the Honey possum, Tarsipes rostratus. J Comp Physiol B 171:59–67
Bradshaw SD, Bradshaw FJ (2002) Short-term movements and habitat utilisation of the marsupial Honey possum, Tarsipes rostratus. J Zool (Lond) 258:343–348
Bradshaw SD, Bradshaw FJ (2007) Isotopic measurements of field metabolic rate (FMR) in the marsupial Honey possum, Tarsipes rostratus. J Mammal 88:401–407
Bradshaw SD, Bradshaw FJ (2009) Measurement of the rate of protein turnover and synthesis in the marsupial Honey possum (Tarsipes rostratus). J Comp Physiol B 179:183–192
Bradshaw FJ, Bradshaw D (2011) Progesterone and reproduction in marsupials: a review. Gen Comp Endocrinol 170:18–40
Bradshaw SD, Cohen D, Katsaros A, Tom J, Owen FJ (1987) Determination of 18O by prompt nuclear reaction analysis: application for measurement of microsamples. J App Physiol 63:1296–1302
Bradshaw FJ, Everett L, Bradshaw SD (2000) On the rearing of Honey possums. West Aust Nat 22:281–288
Bradshaw FJ, Stead-Richardson EJ, Reeder AJ, Oates JE, Bradshaw SD (2004) Reproductive activity in captive female Honey possums, Tarsipes rostratus—assessed by faecal steroid analysis. Gen Comp Endocrinol 138:20–31
Bradshaw SD, Phillips R, Tomlinson S, Holley R, Jennings S, Bradshaw FJ (2007) Ecology of the Honey possum, Tarsipes rostratus, in Scott National Park, Western Australia. Aust Mammal 29:25–38
Brody S (1945) Bioenergetics and growth. Reinhold, New York
Brooker B, Withers PC (1994) Kidney structure and renal indices of dasyurid marsupials. Aust J Zool 42:163–176
Brooker BM, O’Shea JE, Stewart T (1995) Renal vasculature of two Dasyurid Marsupials, Sminthopsis dolichura and S. crassicaudata. Aust J Zool 43:259–270
Brown GD (1968) The nitrogen and energy requirements of the euro (Macropus robustus) and other species of macropod marsupials. Proc Ecol Soc Aust 3:106–112
Brown GD, Main AR (1967) Studies on marsupial nutrition. V. The nitrogen requitrements of the euro, Macropus robustus. Aust J Zool 15:7–27
Brownfield MS, Wunder BA (1976) Relative medullary area: a new structural index for estimating urinary concentrating capacity of mammals. Comp Biochem Physiol 55A:69–75
Bryant KA (2004) The mating system and reproduction in the Honey possum, Tarsipes rostsratus: a life history and genetic perspective. PhD thesis, Murdoch University, Perth
Bryant KA, Spencer PB, Bradley S, Wooller RD (2000) Variation within and between populations of the Honey possum Tarsipes rostratus using both morphological and molecular approaches. Aust Mamm Soc Newsl Nov 2000:23
Carthew SM, Goldingay RL (1997) Non-flying mammals as pollinators. TREE 12:104–108
Chester Jones I (1957) The adrenal cortex. Cambridge University Press, Cambridge
Chilcott MJ, Hume ID (1984) Nitrogen and urea metabolism and nitrogen requirements of the common ringtail possum Pseudocheirus peregrinus fed Eucalyptus andrewsii foliage. Aust J Zool 32:615–622
Christensen P, Maisey K, Perry DH (1984) Radiotracking the numbat, Myrmecobius fasciatus, in the perup forest of Western Australia. Aust Wildl Res 11:275–288
Collins BG, Newland C (1986) Honeyeater population changes in relation to food availability in the jarrah forest of Western Australia. Aust J Ecol 11:63–76
Collins BG, Wooller RD, Richardson KC (1987) Torpor by the honey possum, Tarsipes rostratus (Marsupialia: Tarsipedidae), in response to food shortage and low environmental temperature. Aust Mammal 11:51–57
Cooper CE, Cruz-Neto AP (2009) Metabolic, hygric and ventilatory physiology of a hypermetabolic marsupial, the honey possum (Tarsipes rostratus). J Comp Physiol B 179:773–781
Cork SJ (1986) Foliage of Eucalyptus punctata and the maintenance of nitrogen requirements of koalas, Phascolarctos cinereus. Aust J Zool 34:17–23
Cowling JA, Arrese C, Davies WL, Beazley LD, Hunt DM (2008) Cone visual pigments in two marsupial species: the fat-tailed dunnart Sminthopsis crassicaudata) and the Honey possum (Tarsipes rostratus). Proc Roy Soc Biol Sci B 275:1491–1499
Croft DB, Eisenberg JF (2006) Behaviour. In: Armati P, Dickman CR, Hume ID (eds) Marsupials. Cambridge University Press, Cambridge, pp 229–298
Cummins JM, Temple-Smith PD, Renfree MB (1986) Reproduction in the male Honey possum (Tarsipes rostratus: Marsupialia): the epididymis. Am J Anat 177:385–401
Daniel JC (2004) Growth of the preimplantation embryo of the northern fur seal and its correlation with changes in uterine protein. Dev Biol 26:316–322
Davenport MD, Tiefenbacher S, Lutz CK, Novak MA, Meyer JS (2006) Analysis of endogenous cortisol concentrations in the hair of rhesus macaques. Gen Comp Endocrinol 147:255–261
Dawson TJ, Hulbert AJ (1969) Standard energy metabolism of marsupials. Nature 221:383
Dawson TJ, Hulbert AJ (1970) Standard metabolism, body temperature and surface areas of Australian marsupials. Am J Physiol 218:1233–1238
Denny MJ, Dawson TJ (1977) Kidney structure and function in desert kangaroos. J App Physiol 42:636–642
Dey SK, Lim H, Das SK, Reese J, Paria BC, Daikoku T, Wang H (2004) Molecular cues to implantation. Endocr Rev 25:341–373
Dickman CR (1985) Effects of photoperiod and endogenous control of reproduction in the marsupial genus Antechinus. J Zool (Lond) 206:509–524
Du Toit BA, Smuts DB (1941) The endogenous nitrogen metabolism of pigs with special references to the maintenance requirement of protein. Onderstepoort J Vet Res 16:169–179
Dunlop SD, Ross WM, Beazley LD (1994) The retinal ganglion cell layer and optic nerve in a marsupial, the Honey possum (Tarsipes rostratus). Brain Behav Evol 44:307–323
Endler JA (1993) The color of light in forests and its implications. Ecol Monogr 63:1–27
Fisher DO, Owens IPF, Johnson CN (2001) The ecological basis of life history variation in marsupials. Ecology 82:3531–3540
Fleming TH (1971) Artibeus jamaicensis: delayed embryonic development in a neotropical bat. Science 171:401–402
Foley WJ, Hume ID (1987) Nitrogen requirements and urea metabolism in two arboreal marsupials, the greater glider (Petaroides volans) and brushtail possum (Trichosurus vulpecula), fed Eucalyptus foliage. Physiol Zool 60:103–113
Foley WJ, Hume ID, Taylor R (1980) Protein intake and requirements of the eastern walleroo and the eastern grey kangaroo. Bull Aust Mamm Soc 6:34–35
Foley WJ, Charles-Dominique P, Julien-Laferriere D (2000) Nitrogen requirements of the didelphid marsupial Caluromys philander. J Comp Physiol B 170:345–350
Freudenberger D, Nolan J (1993) Protein turnover in two kangaroo sub-species (Macropus robustus robustus and M. r. erubescens) from divergent habitats and the sympatric feral goat (Capra hircus). Comp Biochem Physiol 105A:443–448
Garavanta CAM, Wooller RD, Richardson KC (2000) Movement patterns of honey possums, Tarsipes rostratus, in the Fitzgerald River National Park, Western Australia. Wildl Res 27:179–183
Geiser F (1994) Hibernation and daily torpor in marsupials: a review. Aust J Zool 42:1–16
Geiser F (2004) Metabolic rate and body temperature reduction during hibernation and daily torpor. Ann Rev Physiol 66:239–274
Geiser F, Pavey CR (2007) Basking and torpor in a rock-dwelling marsupial: survival strategies in a resource-poor environment. J Comp Physiol B 177:885–892
Geiser F, Ruf T (1995) Hibernation versus daily torpor in mammals and birds: physiological variables and classification of torpor patterns. Physiol Zool 68:935–966
Geiser F, Hulbert AJ, Nicol SC (eds) (1996) Adaptations to the cold. University of New England Press, Armidale
Gemmell RT (1988) The oestrous cycle length of the bandicoot, Isoodon macrourus. Aust Wildl Res 15:633–635
Glauert L (1928) Notes on the habits of Tarsipes spenserae. J Proc Roy Soc West Aust 15:10
Glauert L (1958) The honey mouse. Aust Mus Mag 12:284–285
Golden MHN, Jackson AA (1981) Assumption and errors in the use of 15N-excretion data to estimate whole body protein turnover. In: Waterlow JC, Stephen JML (eds) Nitrogen metabolism in man. Applied Science Publishers, London, pp 323–324
Goldingay RL (1990) The foraging behaviour of a nectar feeding marsupial, Petaurus australis. Oecologia 85:191–199
Goldstein DL, Bradshaw SD (1998) Renal function in Red wattlebirds in response to varying fluid intake. J Comp Physiol B 168:265–272
Goldstein DL, Newland S (2004) Water balance and kidney function in the least shrew (Cryptotis parva). Comp Biochem Physiol 139A:71–76
Harder JD, Fleming MW (1981) Estradiol and progesterone profiles indicate a lack of endocrine recognition of pregnancy in the opossum. Science 212:1400–1402
Harding HR, Carrick FN, Shorey CD (1981) Marsupial phylogeny: new indications from sperm ultrastructure and development in Tarsipes spenserae. Search 12:45–47
Harding HR, Carrick FN, Shorey CD (1984) Sperm ultrastructure and development in the Honey possum, Tarsipes rostratus. In: Smith AP, Hume ID (eds) Possums and gliders. Australian Mammal Society, Sydney, pp 451–461
Harman AM, Coleman LA, Beazley LD (1990) Retinofugal projections in a marsupial, Tarsipes rostratus (honey possum). Brain Behav Evol 36:30–38
Hartman CG (1923) The estrous cycle in the opossum. Am J Anat 32:353–421
Hayman DL, Sharp PJ (1982) The chromosomes of Tarsipes spenserae, Gray (Marsupialia). Aust J Zool 30:799–803
Heinrich B (1975) Energetics of pollination. Ann Rev Ecol Syst 6:139–170
Hemmi JM (1999) Dichromatic colour vision in an Australian marsupial, the tammar wallaby. J Comp Physiol A 185:509–515
Heslop-Harrison J (1973) Pollen: development and physiology. Butterworth, London
Hewitt S, Wheldrake JF, Baudinette RV (1981) Water balance and renal function in the Australian desert rodent Notomys alexis: the effect of diet on water turnover rate, glomerular filtration rate, renal plasma flow and renal blood flow. Comp Biochem Physiol 68A:405–410
Hill JP (1910) The early development of the Marsupialia, with special reference to the native cat (Dasyurus viverrinus). Contributions to the embryology of the Marsupialia, IV. Q J Microsc Sci 56:1–134
Hinds LA, Smith MJ (1992) Evidence from plasma progesterone concentrations for male-induced ovulation in the brush-tailed bettong, Bettongia pencillata. J Reprod Fert 95:291–302
Hopper SD (1980) Bird and mammal pollen vectors in Banksia communites at Cheyne Beach, Western Australia. Aust J Bot 28:61–75
Hopper SD, Burbidge AA (1982) Feeding behaviour of birds and mammals on flowers of Banksia grandis and Eucalyptus angulosa. In: Armstrong JA, Powell JA, Richards AJ (eds) Pollination and evolution. Royal Botanic Gardens, Sydney, pp 67–75
Hulbert AJ, Dawson TJ (1974) Water metabolism in perameloid marsupials from different environments. Comp Biochem Physiol 47A:617–633
Hume ID (1977) Maintenance nitrogen requirements of the macropod marsupials Thylogale thetis, red-necked pademelon, and Macropus eugenii, tammar wallaby. Aust J Zool 25:407–417
Hume ID (1982) Digestive physiology and nutrition of marsupials. Cambridge University Press, Cambridge
Hume ID (1999) Marsupial nutrition. Cambridge University Press, Cambridge
Hume ID, Rübsamen K, Engelhardt WV (1980) Nitrogen metabolism and urea kinetics in the rock hyrax (Procavia habessinica). J Comp Physiol B 138:307–314
Hutchinson JCD, Morris S (1936) The digestibility of dietary protein in the ruminant. I. Endogenous nitrogen excretion on a low nitrogen diet in starvation. Biochem J 30:1682–1694
Jacobs GH (1993) The distribution and nature of colour vision among mammals. Biol Rev 68:413–471
Jacobs GH (2009) Evolution of colour vision in mammals. Philos Trans R Soc B 364:2957–2967
Johnson SD, Burgoyne PM et al (2011) Mammal pollinators lured by the scent of a parasitic plant. Proc Roy Soc B 278:2303–2310
Karasov WH (1982) Energy assimilation, nitrogen requirement and diet in free living antelope ground squirrels Ammospermophilus leucurus. Physiol Zool 55:378–392
Kavanagh JR, Burk-Herrick A, Westerman M, Springer M (2004) Relationships among Families of Diprotodontia (Marsupialia) and the phylogenetic position of the autapomorphic Honey possum (Tarsipes rostratus). J Mamm Evol 11:207–222
Kirsch JAW (1968) Prodromus of the comparative serology of Marsupialia. Nature 217:418–420
Kirsch JAW (1977a) The classification of marsupials. In: Hunsaker D (ed) The biology of marsupials. Academic press, New York, pp 1–50
Kirsch JAW (1977b) The comparative serology of Marsupialia, and a classification of marsupials. Aust J Zool Supp. 52
Knox RB (1979) Pollen and allergy. Edward Arnold, London
Kratzing JE (1982) The anatomy of the rostral nasal cavity and vomeronasal organ in Tarsipes rostratus (Marsupialia: Tarsipedidae). Aust Mammal 5:211–219
Krause WJ, Cutts JH, Leeson CR (1979) Morphological observations on the metanephros in the postnatal opossum, Didelphis virginiana. J Anat 129:459–477
Krause WJ, Yamada J, Cutts JH (1985) Quantitative distribution of enteroendocrine cells in the gastrointestinal tract of the adult opossum, Didelphis virginiana. J Anat 144:591–605
Krockenberger AK (2006) Lactation. In: Armati P, Dickman CR (eds) Marsupials. Cambridge University Press, Cambridge, pp 108–136
Landwehr GO, Richardson KC, Wooller RD (1990) Sugar preferences of honey possums, Tarsipes rostratus (Marsupiala: Tarsipedidae) and western pygmy possums, Cercartetus concinnus (Marsupialia: Burramyidae). Aust Mammal 13:5–10
Lentle RG, Potter MA J, Stafford KJ, Springett BP, Haslett S (1998) The temporal characteristics of feeding activity in free-ranging tammar wallabies (Macropus eugenii Desmarest). Aust J Zool 46:601–615
Lopes FL, Desmarais JA, Murphy BD (2004) Embryonic diapause and its regulation. Reproduction 128:669–678
Lyne AG (1976) Observations on oestrus and the oestrous cycle in the marsupials Isodon macrourus and Perameles nasuta. Aust J Zool 24:513–521
Lyne AG, Pilton PE, Sharman GB (1959) Oestrous cycle, gestation period and parturition in the marsupial Trichosurus vulpecula. Nature 183:622–623
Manatt MW, Garcia PA (1992) Nitrogen balance: concepts and techniques. In: Nissen S (ed) Modern methods in protein nutrition and metabolism. Academic Press, New York, pp 9–66
Mark R (1997) Hugh Tyndale-Biscoe and the developmental neurobiology of vision at the Australian National University. In: Saunders N, Hinds L (eds) Marsupial biology: recent research, new perspectives. University of New South Wales Press, Sydney, pp 311–326
McAllan BM, Dickman CR (1986) The role of photoperiod in the timing of reproduction in the dasyurid marsupial Antechinus stuartii (Marsupialia). Oecologia (Berlin) 68:259–264
McAllan BM, Geiser F (2006) Photoperiod and the timing of reproduction in Antechinus flavipes (Dasyuridae: Marsupialia). Mamm Biol 71:129–138
McAllan BM, Roberts JR, O’Shea TO (1996) Seasonal changes in the renal morphometry of Antechinus stuartii (Marsupialia: Dasyuridae). Aust J Zool 44:337–354
McAllan BM, Roberts JR, O’Shea T (1998a) The effects of cortisol and testosterone on renal function in male Antechinus stuartii (Marsupialia). J Comp Physiol B 168(4):248–256
McAllan BM, Roberts JR, O’Shea T (1998b) Seasonal changes in glomerular filtration rate in Antechinus stuartii (Marsupialia: Dasyuridae). J Comp Physiol B 168:41–49
McCracken HE (1986) Observations on the oestrous cycle and gestation period of the Greater bilby, Mactotis lagotis, (Reid) (Marsupialia:Thylacomyidae). Aust Mammal 9:5–16
McDonald IR (1977) Adrenocortical function in marsupials. In: Stonehouse B, Gilmore D (eds) The biology of marsupials. The Macmillan Press Ltd, London, pp 345–377
McNab BK (2005) Uniformity in the basal metabolic rate of marsupials: its causes and consequences. Rev Chil Hist Nat 78:183–298
McNab BK (2008) An analysis of the factors that influence the level and scaling of mammalian BMR. Comp Biochem Physiol 151:5–28
Moir RJ, Williams VJ (1950) Ruminal flora studies in sheep. II. The effect of the levels of nitrogen intake upon the total number of free micro-organisms in the rumen. Aust J Sci Res B3:381–392
Murphy BD, Concannon PW, Travis HF, Hansel W (1981) Prolactin: the hypophyseal factor that terminates embryonic diapause in mink. Biol Reprod 25:487–491
Nagy KA (1980) CO2 production in animals: analysis of potential errors in the doubly labeled water method. Am J Physiol 238:R466–R473
Nagy KA (1987) Field metabolic rate and food requirement scaling in mammals and birds. Ecol Monogr 57:111–128
Nagy KA (1994) Field bioenergetics of mammals: what determines field metabolic rates? Aust J Zool 42:43–53
Nagy KA, Girad IA, Brown TK (1999) Energetics of free-ranging mammals, reptiles and birds. Ann Rev Nutr 19:247–277
Nagy KA (2005) Field metabolic rate and body size. J Exp Biol 208:1621–1625
Nagy KA, Seymour RS, Lee AK, Braithwaite R (1978) Energy and water budgets in free-living Antechinus stuartii (Marsupialia: Dasyuridae). J Mammal 59:60–68
Nagy KA, Lee AK, Martin RW, Fleming MR (1988) Field metabolic rate and food requirement of a small dasyurid marsupial, Sminthopsis crassicaudata. Aust J Zool 36:293–299
Nagy KA, Meienberger C, Bradshaw SD, Wooller RD (1995) Field metabolic rate of a small marsupial mammal, the Honey Possum (Tarsipes rostratus). J Mammal 76:862–866
Nilsson MA, Arnason U, Spencer PB, Janke A (2004) Marsupial relationships and a timeline for marsupial radiation in south Gondwana. Gene 340:189–196
Oates JE (2005) The reproductive endocrinology of the Honey possum (Tarsipes rostratus) and Western pygmy possum (Cercartetus concinnus). PhD thesis, The University of Western Australia
Oates JE, Bradshaw FJ, Bradshaw SD (2004) The influence of photoperiod on the reproductive activity of female Honey possums, Tarsipes rostratus (Marsupialia: Tarsipedidae): assessed by faecal progestagens and oestradiol-17β. Gen Comp Endocrinol 139:103–112
Oates J, Bradshaw FJ, Bradshaw SD, Stead-Richardson EJ, Philippe D (2007) Reproduction and embryonic diapause in a marsupial: insights from captive female Honey possums, Tarsipes rostratus, (Tarsipedidae). Gen Comp Endocrinol 150:445–461
Pak Poy RKF (1957) Electron microscopy of the marsupial renal glomerulus. Aust J Exp Biol 35:448
Picou D, Taylor-Roberts T (1969) The measurement of total protein synthesis and catabolism and nitrogen turnover in infants in different nutritional states and receiving different amounts of dietary protein. Clin Sci 36:283–296
Purohit KG (1974) Observations on size and relative medullary thickness in kidneys of some Australian mammals and their ecophysiological appraisal. Zeit Angew Zool 61:495–505
Raven PH, Evert RE, Eichorn SE (1986) Biology of plants. Worth, New York
Reid IR, McDonald IR (1967) Renal function in the marsupial Trichosurus vulpecula. Comp Biochem Physiol 25:1071–1079
Renfree MB (1978) Embryonic diapause in mammals—a developmental strategy. In: Clutter ME (ed) Dormancy and developmental arrest: experimental analysis in plants and animals. Academic Press Inc., New York, pp 1–46
Renfree MB (1980) Embryonic diapause in the Honey Possum, Tarsipes spencerae. Search 11:81
Renfree MB (1981) Embryonic diapause in marsupials. J Reprod Fertil Suppl 29:67–78
Renfree MB, Shaw G (2000) Diapause. Ann Rev Physiol 62:353–375
Renfree MB, Russell EM, Wooller RD (1984) Reproduction and life history of the Honey Possum, Tarsipes rostratus. In: Smith AP, Hume ID (eds) Possums and gliders. Australian Mammal Society, Sydney, pp 427–437
Richardson KC, Wooller RD, Collins BG (1986) Adaptations to a diet of nectar and pollen in the marsupial Tarsipes rostratus (Marsupialia: Tarsipedidae). J Zool (Lond) 208:285–297
Ridley M (1983) The explanation of organic diversity. Oxford University Press, New York
Riek A (2008) Relationship between field metabolic rate and body weight in mammals: effect of the study. J Zool (Lond) 276:187–194
Robbins CT (1993) Wildlife feeding and nutrition. Academic Press, New York
Rose RW (1987) Reproductive biology of the Tasmanian bettong (Bettongia gaimardi: Macropodidae). J Zool (Lond) 212:59–67
Rose RW (1989) Reproductive biology of rat-kangaroos. In: Grigg G, Jarman P, Hume I (eds) Kangaroos, wallabies and rat kangaroos. Surrey Beatty and Sons, New South Wales, pp 307–315
Rosenberg HI, Richardson KC (1995) Cephalic morphology of the Honey possum, Tarsipes rostratus (Marsupialia: Tarsipedidae): an obligate nectarivore. J Morphol 223:303–323
Rotenberg D (1928) Notes on the male generative apparatus of Tarsipes spenserae. J Roy Soc WA 15:9–14
Russell EM (1982) Patterns of parental care and parental investment in marsupials. Biol Rev 57:423–486
Russell EM (1986) Observations on the behaviour of the Honey Possum, Tarsipes rostratus (Marsupialia: Tarsipedidae) in captivtiy. Aust J Zool 121:1–63
Russell EM, Renfree MB (1989) Tarsipedidae. In: Walton DW, Richardson BJ (eds) Fauna of Australia: mammalia. AGPS, Canberra, pp 769–782
Sadlier RMFS, Tyndale-Biscoe CH (1977) Photoperiod and the termination of embryonic diapause in the marsupial Macropus eugenii. Biol Reprod 16:605–608
Sandell M (1990) The evolution of seasonal delayed implantation. Quart Rev Biol 65:23–42
Sanderson KJ, Nelson JE, Crewther DP, Crewther SG, Hammond VE (1987) Retino-geniculate patterns in diprotodont marsupials. Brain Behav Evol 30:22–42
Scarlett G, Woolley PA (1980) The Honey Possum Tarsipes spenserae) Marsupialia: Tarsipedidae): a non-seasonal breeder? Aust Mammal 3:97–103
Schmidt-Nielsen B, Schmidt-Nielsen K, Houpt TR, Jarnum SA (1957) Urea excretion in the camel. Am J Physiol 212:341–346
Schultz W (1976) Magen-Darm-Kanal der Monotremen und Marsupialier. Hand Zool 8:1–177
Schwarzenberger F, Palme R, Bamberg E, Mostl E (1997) A review of faecal progesterone metabolite analysis for non-invasive monitoring of reproductive function in mammals. Int J Mamm Biol 62(Suppl II):214–221
Selwood L (1980) A timetable of embryonic development of the dasyurid marsupial Antechinus stuartii (Macleay). Aust J Zool 28:649–668
Sharman GB (1955a) Studies on marsupial reproduction 3. Normal and delayed pregnancy in Setonix brachyurus. Aust J Zool 3:56–70
Sharman GB (1955b) Studies on marsupial reproduction. IV. Delayed birth in Protemnodon eugenii. Aust J Zool 3:156–161
Shaw G, Rose RW (1979) Delayed gestation in the potoroo Potorous tridactylus (Kerr). Aust J Zool 27:901–912
Slaven MR, Richardson KC (1988) Aspects of the form and function of the kidney of the Honey Possum, Tarsipes rostratus. Aust J Zool 36:465–471
Smith MJ (1981) Morphological observations on the diapausing blastocyst of some macropodid marsupials. J Reprod Fert 64:83–486
Smith AP (1982) Diet and feeding strategies of the marsupial sugar glider in temperate Australia. J Anim Ecol 51:149–166
Smith MJ (1994) Male-induced oestrus and ovulation in female brush-tailed bettongs (Bettongia penicillata) suckling a young in the pouch. Reprod Fertil Dev 6:445–449
Smith AP, Green SW (1987) Nitrogen requirements of the sugar glider (Petaurus breviceps), an omnivorous marsupial, on a honey-pollen diet. Physiol Zool 60:82–92
Smith AP, Lee AK (1984) The evolution of strategies for survival and reproduction in possums and gliders. In: Smith AP, Hume ID (eds) Possums and gliders. Surrey Beatty and Sons, Sydney, pp 17–33
Smuts DB (1935) The relationship between the basal metabolism and the endogenous nitrogen metabolism, with particular reference to the estimation of the maintenance requirement of protein. J Nutr 9:403–433
Smuts DB, Marais JSC (1938) The endogenous nitrogen excretion of sheep with special reference to the maintenance requirement of protein. Onderstepoort J Vet Res 11:131–139
Speakman JR (1997) Doubly labelled water: theory and practice. Chapman & Hall, London
Speakman JR (2005a) Body size, energy metabolism and lifespan. J Exp Biol 208:1717–1730
Speakman JR (2005b) Correlations between physiology and lifespan—two widely ignored problems with comparative studies. Aging Cell 4:167–175
Spencer PBS, Bryant KA (2000) Characterization of highly polymorphic microsatellite markers in the marsupial honey possum (Tarsipes rostratus). Mol Ecol 9:492–494
Sperber I (1944) Studies on the mammalian kidney. Zool Bidr Upps 22:249–432
Stead-Richardson EJ, Bradshaw SD, Bradshaw FJ, Gaikhorst G (2001) Monitoring the oestrous cycle of the chuditch (Dasyurus geoffroii: Marsupialia, Dasyuridae): non-invasive analysis of faecal oestradiol-17β. Aust J Zool 49:183–193
Stead-Richardson EJ, Bradshaw SD, Friend AJ, Fletcher T (2010) Monitoring reproduction in the critically endangered marsupial, Gilbert’s potoroo (Potorous gilbertii): preliminary analysis of faecal oestradiol-17β, cortisol and progestagens. Gen Comp Endocrinol 165:155–162
Stein TP (1981) 15N-glycine as a tracer to study protein metabolism in vivo. In: Waterlow JC, Stephen ML (eds) Nitrogen metabolism in man. App Sci (Lond), pp 345–356
Strachan J, Chang L-Y E, Wakefield MJ, Marshall Graves JA, Deeb SS (2004) Cone visual pigments of the Australian marsupials, the stripe-faced and fat-tailed dunnarts: sequence and inferred spectral properties. Vis Neurosc 21:223–229
Studier EH, Wisniewski SJ, Feldman AT, Dapson RW, Boyd BC, Wilson DE (1983) Kidney structure in neotropical bats. J Mammal 64:445–452
Sumner P, Arrese C, Partridge JC (2005) The ecology of visual pigment tuning in an Australian marupial: the Honey possum Tarsipes rostratus. J Exp Biol 208:1803–1815
Turner V (1984) Banksia pollen as a source of protein in the diet of two Australian marsupials Cercartetus nanus and Tarsipes rostratus. Oikos 43:53–61
Tyndale-Biscoe CH (1979) Hormonal control of embryonic diapause and re-activation in the tammar wallaby. In: Maternal recognition of pregnancy ciba foundation symposium 64 (new series). Excerpta Medica, Amsterdam, pp 173–190
Tyndale-Biscoe CH (1986) Embryonic diapuase in a marsupial: roles of the corpus luteum and pituitary in its control. In: Liss AR (ed) Comparative endocrinology: developments and directions, pp 137–155
Tyndale-Biscoe CH, Hawkins J (1977) The corpora lutea of marsupials: aspects of function and control. In: Calaby JH, Tyndale-Biscoe CH (eds) Reproduction and evolution. Australian Academy of Science, Canberra, pp 245–252
van Tets IG, Hulbert AJ (1999) A comparison of the nitrogen requirements of the eastern pygmy possum, Cercartetus nanus, on a pollen and on a mealworm diet. Physiol Biochem Zool 72:127–137
Van Tets IG, Whelan RJ (1997) Banksia pollen in the diet of Australian marsupials. Ecography 20:499–505
Voigt CC, Kelm DH, Visser GH (2006) Field metabolic rates of phytophagous bats: do pollination strategies of plants make life of nectar-feeders spin faster? J Comp Physiol B 176:213–222
Vose HM (1972) Some observations of a Honey Possum (Tasipes spenserae) in captivity. WA Nat 12:61–67
Vose HM (1973) Feeding habits of the Western Australian Honey Possum, Tarsipes spenserae. J Mammal 54:245–247
Walker MT, Rose RW (1981) Prenatal development after diapause in the marsupial Macropus rufogriseus. Aust J Zool 29:167–187
Ward SJ (1990) Reproduction in the Western Pygmy-possum, Cercartetus concinnus (Marsupialia: Burramyidae), with notes on reproduction of some other small possum species. Aust J Zool 38:423–438
Ward SJ, Renfree MB (1988) Reproduction in females of the feathertail glider Acrobates pygmaeus (Marsupialia). J Zool (Lond) 216:225–239
Wasser SK, Monfort SL, Southers J, Wildt DE (1994) Excretion rates and metabolites of oestradiol and progesterone in baboon (Papio cynocephalus cynocephalus) faeces. J Reprod Fert 101:213–220
Waterlow JC, Garlick PJ, Millward DJ (1978) General principles of the body measurement of whole-body protein turnover. In: Waterlow JC, Garlick PJ, Millward DJ (eds) Protein turnover in mammalian tissues and in the whole body. Elsevier/North-Holland Biomedical Press, Amsterdam, pp 249–255
Weibel ER (1979) Stereological methods: practical methods for biological morphometry. Academic Press, London
Weichert CK (1940) The experimental shortening of prolonged pregnancy in the albino rat. Anat Rec 77:31
Wellard GA, Hume ID (1981) Nitrogen metabolism and nitrogen requirements of the brushtail possum Trichosurus vulpecula (Kerr). Aust J Zool 29:157–166
Welle S, Nair KS (1990) Relationship of resting metabolic rate to body composition and protein turnover. Am J Physiol 258:E 990–E 998
White RG, Hume ID, Nolan JV (1988) Energy expenditure and protein turnover in three species of wallabies (Marsupialia: Macropodidae). J Comp Physiol B 158:237–246
Whitten WK (1958) Endocrine studies on delayed implantation in lactating mice. Role of the pituitary in implantation. J Endocrinol 16:435
Wiens D, Renfree M, Wooller RD (1979) Pollen loads of Honey possums (Tarsipes spenserae) and nonflying mammals in southwestern Australia. Ann Miss Bot Gard 66:830–838
Withers PC, Richardson KC, Wooller RD (1990) Metabolic physiology of euthermic and torpid honey possums, Tarsipes rostratus. Aust J Zool 37:685–693
Woodd C, Czarny NA, Gunn IMG, Sturrock W (2006) Faecal steroid analysis and urinary cytology of the squirrel glider (Petaurus norfolcensis). Aust J Zool 54:277–285
Wooller RD, Richardson KC (1992) Reduction in the number of young during pouch-life in a small marsupial. J Zool (Lond) 226:445–454
Wooller RD, Renfree MB, Russell EM, Dunning A, Green SW, Duncan P (1981) Seasonal changes in a population of the nectar feeding marsupial Tarsipes spenserae Marsupialia: Tarsipedidae). J Zool (Lond) 195:267–279
Wooller RD, Russell EM, Renfree MB (1983a) A technique for sampling pollen carried by vertebrates. Aust Wildl Res 10:433–434
Wooller RD, Russell EM, Renfree MB, Towers PA (1983b) A comparison of seasonal changes in the pollen loads of nectarivorous marsupials and birds. Aust Wildl Res 10:311–317
Wooller RD, Russell EM, Renfree MB (1984) Honey possums and their foodplants. In: Smith AP, Hume ID (eds) Possums and gliders. Surrey Beatty and Sons, Sydney, pp 439–443
Wooller RD, Richardson KC, Collins BG (1993) The relationship between nectar supply and the rate of capture of a nectar-dependent small marsupial Tarsipes rostratus. J Zool (Lond) 229:651–658
Wooller RD, Richardson KC, Garavanta CAM, Saffer VM, Anthony C, Wooller SJ (1998) The influence of annual rainfall upon capture rates of a nectar-dependent marsupial. Wildl Res 25:165–169
Wooller RD, Richardson KC, Bradley GO (1999) Dietary constraints upon reproduction in an obligate pollen- and nectar-feeding marsupial, the Honey possum (Tarsipes rostratus). J Zool (Lond) 248:279–287
Wooller RD, Richardson KC, Garavanta CAM, Saffer VM, KA Bryant (2000) Opportunistic breeding in the polyandrous honey possum, Tarsipes rostratus. Aust J Zool 48:669–680
Woolley PA (1990) Reproduction in Sminthopsis macroura (Marsupialia:Dasyuridae) I. The female. Aust J Zool 38:187–205
Woolley PA, Scarlett G (1984) Observations on the reproductive anatomy of male Tarsipes rostratus (Marsupilaia: Tarsipedidae). In: Smith AP, Hume ID (eds) Possums and gliders. Australian Mammal Society, Sydney, pp 445–450
Yadav M (1979) The kidney types of some Western Australian macropod marsupials. Mammalia 43:225–233
Yamada J, Richardson KC, Wooller RD (1989) An immunohistochemical study of gastrointestinal endocrine cells in a nectarivorous marsupial, the honey possum (Tarsipes rostratus). J Anat 162:157–168
Young VR, Yu Y-M, Krempf M (1991) Protein and amino acid turnover using the stable isotopes 15-N, 13-C and 2-H as probes. In: Whitehead RG, Prentice A (eds) New techniques in nutritional research. Academic Press, New York, pp 17–72
Acknowledgments
Our own research on honey possums has been generously supported by grants from the Australian Research Council (ARC), the Australian Institute for Nuclear Science and Engineering (AINSE), The University of Western Australia and “The Friends of the Honey Possum”. Numerous graduate students contributed to both field and laboratory studies that have increased our understanding of honey possums: in particular Jessica Oates and Ernie Stead-Richardson. Helpful comments and suggestions by two reviewers are gratefully acknowledged and our thanks to Ian Hume for proposing the review. Acknowledgement must also be made to the many researchers who have studied this unique marsupial over the past four decades and made this review possible.
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Bradshaw, D., Bradshaw, F. The physiology of the honey possum, Tarsipes rostratus, a small marsupial with a suite of highly specialised characters: a review. J Comp Physiol B 182, 469–489 (2012). https://doi.org/10.1007/s00360-011-0632-9
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DOI: https://doi.org/10.1007/s00360-011-0632-9