On Ratites and Their Interactions with Plants*

Home , Cassowary, Casuariidae, Dromaius, Dromornis, Dromornithidae, Duboisia hopwoodii

Revista Chilena de Historia Natural 64: 85-118, 1991 On ratites and their interactions with plants*

Las rátidas y su interacci6n con las plantas

JAMES C. NOBLE

CSIRO, Division of Wildlife and Ecology, National Rangelands Program, P.O. Box 84, Lyneham, A.C.T. 2602, Australia

RESUMEN

Se revisan las historias de los fosiles, patrones de distribucion y preferencias de medio ambiente natural-nabitat, tanto de miembros extintos como sobrevivientes de las ratidas. Se pone especial enfasis en aquellas caracterlsticas f{sicas y anatomicas de las rátidas que tienen aparente significacion desde el punto de vista de Ia dinamica vegetal, especialmente aquellos aspectos relacionados con Ia germinacion de las semillas y establecimiento de los brotes. Aparte de los kiwis de Nueva Zelanda (Apteryx spp.), Ia caracteristica principal que distingue a las ratidas de otras aves es su gran tamafio. En tanto que las consecuencias evolutivas del gigantismo han resultado en Ia extincion comparativamente reciente de algunas especies, tales como, las moas (las Dinornidas y Emeidas) de Nueva Zelanda y los pajaros elefantes (Aeporní- tidas) de Madagascar, el gran tamaño de las rátidas contemporáneas les confiere Ia capacidad de ingerior considerables cantidades de alimentos, como as{ tambien {temes particulares como frutas y piedras demasiado grandes para otras aves, sin sufrir ningún menoscabo en el vuelo. Muchos de estos alimentos vegetates, especialmente frutas como las de los Lauranceae, pueden ser altamente nutritivos, pero las ratidas son omnivoras y pueden utilizar una gama de alternativas cuando es necesario. Es aún incierto si Ia seleccion de alimentos está relaeionada directamente con Ia recompensa nutritiva; sin embargo, Ia estacion de reproduccion del casuario australiano (Casuarius casuarius johnsonii) está estrecha- mente ligada al per{odo de máxima produccion frutal de los árboles y arbustos en sus habitat de selvas tropicales lluviosas. Algunas rátidas extintas, tales como: las moas y los mihirungs (Dromornitidas) pueden haber tambien influenciado Ia seleccion de plantas y sucesion vegetal mediante su ingestion diferencial de especies y organos fitogenos particulares. Existe un aparente mutualismo en lo que respecta a los beneficios sobre Ia poblacion vegetal, consiguientes a Ia inges- tión de los propágulos por parte de las ratidas. En ciertas situaciones, las semillas de las plantas germinan satisfactoria- mente solamente despues que Ia semilla ha pasado a traves de los intestinos de las ratidas. Se postula que muchas de las diásporas de frutos grandes que comen las ratidas s6Io germinan rapidamente en micrositos fecales, confiriendo por lo tanto considerables beneficios ecologicos al promover una importante, y dispersa, ca{da de semillas. En suelos de textura pasada, el arbusto semiárido Nitraria billardieri solamente se establece en abundancia una vez que el fruto suculento que madura durante el verano ha sido comido por los emus (Dromaius novaehollandiae). En sustratos areno- sos de las áreas costeras donde Ia fruta ca{da es cubierta rapidamente por Ia arena llevada por el viento, Ia especie germina prontamente en ausencia de Ia ingestion aviaria.

ABSTRACT

The fossil histories, distribution patterns and habitat preferences of both extinct and extant members of the Ratitae are reviewed. Particular emphasis is directed towards those physical and anatomical features of ratites which have apparent significance in terms of vegetation dynamics, especially those aspects relating to seed germination and seedling establishment. Apart from the New Zealands kiwis (Apteryx spp.), the principal feature distinguishing the ratites from other birds is their large size. Whilst the evolutionary consequences of gigantism have resulted in the comparatively recent extinction of some speeies such as the moas (the Dinornithidae and Emeidae) of New Zealand and the elephant birds (Aepyornithidae) of Madagascar, the large size of contemporary ratites confers an ability to ingest considerable quantities of food, as well as particular items such as fruits and stones too large for other birds, without having to suffer any impairment of flight. Many of these plant foods, especially fruits such as those of the Lauraceae, can be highly nutritious, but ratites are omnivorous and can utilize a range of alternatives when necessary. Whether prey selection is directly related to nutritional reward is uncertain however the breeding season of the. Australian cassowary (Casuarius casuarius john. sonii) is closely linked to the period of maximum fruit production by trees and shrubs in their tropical rainforest habitatats. Some ratites such as the moas and the mihirungs (Dromornithidae) may also have influenced plant selection and vegetation succession through their differential browsing of particular species and plant organs. There is some apparent mutualism in terms of benefits conferred on plant populations following propagule ingestion by ratites. In certain situations, seeds of plants germinate satisfactorily only after the seed has passed through the ratite gut. It is postulated that many of the large-fruited diaspores eaten by ratites will only germinate rapidly in faecal microsites thereby con- ferring considerable ecological benefits by promoting substantial, and dispersed, seedling recruitment. On heavy textured soils, the semi-arid shrub Nitraria billardieri, only establishes in abundance once the succulent fruit, which ripens during the summer, has been eaten by emus (Dromaius novaehollandiea). In the sandy substrates of coastal areas where fallen fruit is readily covered by windblown sand, the species germinates readily in the absence of avian ingestion.

(Received 25 July 1989.) * Invited paper. 86 NOBLE

INTRODUCTION The term ratite, derived from the latin ratis or raft, refers to those flightless birds, some now extinct, whose skeletal structure is characterised by a raft-like breast-bone or sternum. To taxonomists and evolutionists however, they are a "truly confusing, vexacious group" (Rich & Balouet 1984). Much of the complexity inherent in their taxonomy and phylogeny results from the hypothesis that they are closely related to the "fowl-like" tinamous (Tinamiformes) of the South American Neotropics, both groups possessing a distinctive palate Fig. 1.: A phylogenetic scheme for ratites based on (Houde 1988) while differing in sternum DNA x DNA hybridization data of Sibley and structure. This relatively primitive, reptilian Ahlquist (1981 ). palate, described as palaeognathous or Un esquema filogenético para las ratidas basado en los dromaeognathous, is a strong and rigid datos de hibridizaci6n DNA x DNA de Sibley y Ahlquist structure with individual parts either ar- (1981). ticulated along extended sutures or actually fused, in contrast with other birds (ne- ognaths) whose palates are lighter and more flexible in construction (Bock 1963). Accordingly modern birds (subclass Ne- (o.trtcha) ornithes) have been divided into two superorders. the Palaeognathae and Neognathae. An alternative classification \ divides the Neornithes into the Ratitae and Carinatae. Here the Carinates are distinguished by possessing keeled breastbones or carinate sterna to which are attached the powerful breast muscles required for flight (Houde 1988). Many extinct taxa such as the New Zealand moas (Dinornithidae and Emeidae), the mihirungs (Dromornithidae) of Australia, the elephant birds (Aepyor- nithidae) of Madagascar and the Ere- mopezidae of North Africa, have been tentatively included in the Ratitae pending conclusive palatal and other anatomical and biochemical evidence (Rich & Balouet 1984). Phylogenetic relationships of ratites, as shown in Figs. 1 and 2, whilst understood at some levels and for some groups, are not clear for all. Together with other palaeontologists (e.g. de Beer 1956), Rich & Balouet ( 1984) claim that ratites evolved from flying ancestors and not independently from reptiles. With remarkable percep- Fig. 2: Three phylogenetic trees for both extant tion, Charles Darwin postulated that the and extinct ratites proposed by Rich (1979). wingless birds of New Zealand and other Tres arboles filogeneticos, tanto para ratidas sobrevivien- islands arrived by flight but their wings tes como extintas propuesto por Rich (1979). ON RATITES AND THEIR INTERACIONS WITH PLANTS 87 subsequently became atrophied from disuse ing. These birds are highly cursorial with in habitats devoid of predators. Studies by the inside digit of the foot markedly reduced Houde ( 1986) conclude that the kiwis and the lengthened distal elements of the (Apteryx spp.) envolved directly from a limbs enabling them to reach speeds up Northern Hemisphere palaeognath that to 50 km/hr. flew to New Zealand before losing its In terms of energy expenditure, flight is power of flight independently of other the most costly of all modes of locomotion ratites. "In ostriches which inhabit con- and as size increases, so does the energetic tinents and great islands, as we see that cost (Carlquist 1974). As the weight of a they can escape danger by their fleetness, bird is squared, the wing area must be and in close quarters by their dangerous cubed to support the increased weight kicks, quite as well as any quadruped, di- (Davies 1976). The cursorial habit of suse together with the increasing weight of continental ratites is not only economical their bodies may well have rendered them of energy but also enables them to remain incapable of flight" (Darwin in Stauffer in close contact with their food crops on 1975, p. 290). the ground, some of which are located The ratites generally have strong in widely separated regions (Davies 1976). Gondwanan affinities even though ostriches Consequently, there will be positive selec- were once present in Europe and Asia tion pressures for flightlessness whenever (Rich 1975). There may well have been flight is unnecessary, and only small strong coevolutionary links between the changes will push a bird over the threshold ratites and the primitive angiosperms, between flying and non-flying. Selection conifers and cycads of Gondwana (White would be unlikely to eliminate wings 1986) however the precise details of such entirely but rather to induce a reduction linkages remain in the realms of specula- to small vestigial wings (Carlquist 1965). tion. The moas are unique in this sense having This paper examines various aspects ot lost all wing structures during their evolu- the ecology of extant members of the tion (Oliver 1949). Ratitae, excluding the tinamous, with The increasing cursoriality in continental reference to extinct ratites where ap- ratites may have been a selection response propriate. After describing distribution pat- to greater openness of the habitat as the terns, habitat, preferences, fossil histories, temperate rainforests of the Tertiary and the interactions between ratites and decreased with drying of the climate man, the anatomical features of ratites in around the Middle Miocene (15 m.y. BP) relation to their dietary preferences and (Frakes et al. 1987). Many of the features subsequent influence on vegetation dy- of the extinct ratite Emuarius gidju (Boles namics will be discussed in regard to plant- 1991) indicate such an increase in cur- ratite mutualism. soriality as the Nothofagus-dominant rainforests across much of the temperate Australia retreated. Nonetheless the cas- SIZE CHARACTERISTICS sowary is also cursorial despite its tropical rainforest habitat. The continental ratites (ostriches, emus The large size of the continental ratites is and rheas) have effectively substituted a correlated also with increased longevity rapid running (cursorial) capability for (c. 15 years for emus in the wild), rapid flight, decreasing wing size being inversely growth rate and early maturity. Rheas related to leg size. Not only is this an may grow to one third their adult size in expedient defence mechanism from pre- just two months (Bruning 1973), and all dators, but it also enables these birds to the large ratites lay eggs before they are travel large distances seeking food during two years old (Davies 1976). The incuba- drought. Davies (1976) recorded tagged tion period though is quite long ranging emus (Dromaius novaehollandiae) travelling from eight weeks to three months (Carlquist as far as 500 km within 9 months of band- 1965). TABLE 1

Physical dimensions of selected ratite species. Dimensiones físicas de especies seleccionadas de ratidas.

Relative egg Species Weight Toe autch Egg Egg weight Reference (kg) Number size size (mm) weight (g) (% bodyweight)

Giant Mihirung 500 3 n.a* 125 X 155 1,300 0.26 Rich & van Tets (1982) (Dromornis stirtoni) Rich & Balouet (1984)

Giant Moa 250 4 1-2 178x253 7,000 2.80 Oliver (1949) (Dinornis giganteus) Grzimek (1972) Elephant Bird 454 3 n.a > 300 long. n.a n.a Carlquist (1965) (Aepyornis maximus) (c. 100 1 Grzimek (1972) in volume). Mahe (1972)

African Ostrich 150 2 16-24 116 X 145 1,200 0.80 Grzimek (1972) (Struthio camelus)

Emu 55 3 15-25 90 X 135 600 1.09 Davies (1967) (Dromaius novaehollandiae) Long (1965) Grzimek (1972) Noble (l975a)

Cassowary 60 3 3-8 90 X 135 650 1.08 Grzimek (1972) (Casuarius casuarius) Crome (1976)

Common Rhea 25 3 15-20 95 X 135 600 2.40 Grzimek (1972) (Rhea americana)

Brown Kiwi 3 4 1 78 X 125 430 14.3 Grzimek (1972) (Apteryx australis) Reid & Williams (1975) Reid (1981) ON RATITES AND THEIR INTERACTIONS WITH PLANTS 89

The egg dimensions for both extant and 3 m in height and weighing more than 150 extinct ratites are shown in Table I. In kg (Grzimek 1972), is the largest of the relative terms the elephant birds and the living ratites. As shown in Fig. 3, there is a kiwis produced the largest eggs per unit linear progression in size from the kiwi, bodyweight. The kiwi, according to Gould through the intermediate-sized rhea, cas- ( 1986), is a phyletic dwarf having evolved sowary and emu to the four largest ratites, from much larger ancestors laying eggs three of which are now extinct. appropriate to their size. Allometric relationships between egg and body weights 1 4 2 (Rahn et al. 197 5) suggest that while the 3 kiwi body decreased greatly in bulk, egg size remained the same or was only slightly E reduced. Carlquist ( 1965) has addres- 7 5 sed the question of what is the largest 6 egg size possible in terms of structural and physical considerations claiming max- 8 imum limits for egg size and body size in birds were attained by the elephant 2 3 4 5 6 7 8 bird (Aepyornis sp.) whose 30 em long Weight (kg egg with a shell several millimetres thick Fig. 3: The relationship between ratite height and was first described in 1832 (Grzimek cubed root of weight for selected species. Size 1972). specifications were obtained from a number of Similar considerations apply to the sources cited in Table I. largest fruit capable of ingestion and I = Giant Mihirung (Dromomis stirtoni) subsequent dispersal by ratites. Whilst the 2 = Giant Moa (Dinomis giganteus) ecological ramifications of body size have 3 = Elephant Bird (Aepyomis maximus) been discussed by Peters (1983), certain 4 = African Ostrich (Struthio camelus) questions relating to ratite size are germane 5 = Emu (Dromaius novaehollandiae) to this paper. Does the large size of con- 6 = Cassowary ( Casuarius casuarius) tinental ratites enable them to eat certain 7 = Common Rhea (Rhea americana) plant foods unavailable to other birds, and 8 = Brown Kiwi (Apteryx australis) has this been important in the evolutionary La relaci6n entre la altura de la ratida y la raíz cubica del success of both predator and prey? Fur- peso de especies seleccionadas. Las especificaciones de thermore, does the gastrointestinal system tamaiio se obtuvieron de diversas fuentes citadas en la of ratites bestow any benefits on dispersed Tabla 1. 1 = Mihirung Gigante (Dromornis stirtoni) plant propagules? 2 = Moa Gigante (Dinornis giganteus) The potential ecological significance of 3 = Pajaro Elefante (Aepyormis maximus) 4 = Avestruz Africana (Struthio came/us) this distinctive group of birds rests pri- 5 = Emu (Dromaius novaehollandiae) marily on two fundamental characteristics; 6 = Casuario (Casuarius casuarius) firstly, the fact that they are essentially 7 = Ñandú Común (Rhea americana) 8 = Kiwi Pardo (Apteryx australis) terrestrial animals and secondly, their disproportionately large size when compared with other birds. It can be postulated that ratites have a significant influence on DISTRIBUTION PATTERNS, FOSSIL RECORDS, the seed dispersal and seedling establishment HABITAT of some plant species through their ability to transport large quantities of diaspores Preferences and Sociability and also their capacity to ingest fruit too large for other birds. Being terrestrial, The distributions of contemporary ratites, their large size also implies some potential i.e. the rheas (Rhea americana and Pte- for physically modifying vegetation as they rocnemia pennata), the ostrich (Struthio move through the landscape, particularly in came/us), the kiwis (Apteryx australis, A. groups. The male ostrich, standing up to oweni and A. haasti), the cassowaries 90 NOBLE

( Casuarius unappendiculatus, C. casuarius well established in Africa by the mid- and C. bennetti) and the emu (Dromaius Tertiary and possibly much earlier, with novaehollandiae), are shown in Figure 4. ostrich-like birds found in the fossil records Australia is unique in being the only of Asia, Europe (Kurochkin & Lungu 1970) continent where birds from more than one and Africa (Rich & Balouet 1984). Recent ratite genus can still be found alive in fossil studies (Houde 1986, Howgate 1986) contrasting habitats, i.e. cassowaries in indicate that the ancestors of ostriches tropical rainforest and emus primarily in evolved from a group of North American semi-arid grassland/ shru bland. and European birds, the "Lithornis-cohort", Details of habitat and social behaviour that could fly. amongst ratites are summarised in Table 2. Whilst the Lithornidae may have had a The emu, cassowary and kiwi are dis- capacity for flight, they were found to tinguished by the fact that for most of the possess a palaeognathous palate thereby year they are solitary or form breeding extending the fossil record of pal- pairs. On certain occasions however, aeognathous birds back to the late cassowaries (White 1913), kiwis (Reid Palaeocene (Houde 1988). Palaeotis wigelti et al. 1982) and emus (Noble 1985) may was a crane-sized, flightless, palaeognathous form flocks when feeding around fruiting ostrich from the Middle Eocene of Germany shrubs and trees. The rhea and ostrich in (Houde 1986). One biogeographical feature contrast, may form large loose flocks, of the contemporary ostrich is its trans- particularly during the breeding season. tropical distribution, other ratites being One social feature common to all extant restricted to the Southern Hemisphere. ratites is the degree to which the male bird Ostriches generally inhabit the open is responsible for incubation. The male savannas of Africa although they are kiwi incubates the large, single egg for a extremely adaptable grazers, S. c. molyb- period ranging from 85 to 92 days dephanus frequenting scrubland in (McLennan 1988) and has ample fat re- Somaliland (Leuthold 1970). serves enabling him to survive fasts lasting up to 7 days. Both the rhea and the ostrich Rheas have shorter incubation periods of 35-42 days however while the male rhea incubates Within the ratites, the ostriches have been alone (Bruning 1974), incubation is shared closely allied by taxonomists to the two by both the male and major female ostrich species of South American rheas (Rich & (Bertram 1980). The male emu has con- Balouet 1984). Both are cursorial, inhabiting siderable fasting capacity and may incubate a similar range of habitats in opposing without eating or drinking for 56 days continents. Rhea americana (greater or before leaving the nest with the chicks common rhea) is regarded primarily as an which hatch over a four day period (Davies inhabitant of the Pampas grasslands east 1976). The male cassowary also rears the of the Andes but in Brazil, where it was chicks after an incubation period lasting once common, its abundance has declined from 47-53 days (Crome 1976). markedly (Davies 1976). Pterocnemia pennata is somewhat smaller than R. EXTANT RATITE GENERA americana, occurring from Patagonia to the high plateaux of the Andes (Mayr & Ostriches Cottrell 1979). Like the ostrich, the fossil record of the rhea extends back in the There are currently five subspecies of Cainozoic, and it was present in South ostriches surviving although a sixth, Struthio America by the Pliocene (Brodkorb 1963). came/us syriacus, disappeared only recently in the 1920s from its range in Asia Minor Emus and Arabia (Davies 197 6). Grzimek (1972) refers to eight extinct species, all belonging The Australian emu (JJromaius: Dromaiinae) to the genus Struthio. These birds were has a pan-continental distribution and is 1 unappendiculatus

2 casuarius

A Apteryx mantelli pennata pennata B Apteryx a. Pterocnemia p. tarapacensis p. Apteryx a.

Rhea americana americana D Apteryx oweni, A. haasti Struthio Rhea a. intermedia D Struthio c. Rhea a. Struthio c. 8 Rhea a. araneipes Struthio c. massai

Rhea a. Struthio c. spatzi

Fig. 4.: The world distribution of extant ratites (after Davies 1976}. La distribucion rnundial de las nitidas sobrevivientes (según Davies 1976). TABLE 2 Habitat, social behaviour, diet and anatomical features of extant ratites. Habitat, comportamiento social, dieta y caracteristicas anat6micas de rátidas sobrevivientes.

Species Habitat Sociability Diet Gastro-Intestinal Tract Reference

Rhea Grass steppes of South Loose flocks up to Grasses and herbs Gut and particularly Grzimek (1972) American lowlands and 5O females after (alfalfa, clover, caeca very long. Bruning (1974) plains up to 4,000 m breeding season. senadella), fruit, Urine stored in Davies (197 6) in the Andes. Polygamous. insects and small expansion of cloaca animals. before elimination in liquid form. Ostrich Open savanna in dry Often form Supplement plant Three stomach segments Grzimek (1972) South African peaceful diet of various with gut up to 14m Robinson & Seeley (197 5) "bushveld ", wide aggregations up grasses, bushes long. Rectum Davies (1976) sand plains or desert to 680 birds but and tree forage with especially extended and Bertram (1980) or dense bush. individual flocks invertebrates and caeca about 70 em long. Bakker (1987) Adaptable grazer and remain identifiable. small animals. Urine concentrated in also found in steep Polygamous. large cloaca but unlike rocky mountain country other birds is secreted up to 3000 m in East separately from faeces. Africa. Emu Grassland and savanna Solitary or breeding Grasses and herbs, Gut and caeca shorter Long (1965) woodlands of semi- pairs for much of fruits from shrubs than in rheas. Grzimek (1972) arid Australia year except when and trees and Strongly developed Dawson & Herd (1983) primarily. feeding on specific invertebrates. gizzard musclature. Herd & Dawson (1984) diet when birds may Fermentation contained Noble (1985) form large flocks up within the ileum. to 80 in number. Monogamous. Cassowary Tropical rainforests Solitary and only Fallen fruit. Gut and caeca shorter White (1913) and fringes. Also pair during breeding. even than emus. Crome (1976) woodland up to 3000 m Monogamous. Small Davies (1976) altitude. flocks concentrated Stocker & Irvine (1983) around fruiting trees. Kiwi Primarily subtropical Many form small Mainly invertebrates Proventriculus small Oliver (1955) and temperate rain-forest flocks around but vegetable matter 75 x 55 mm, gizzard Watt (1971) but also shrub, fruiting trees. including tree fruit moderately muscular Reid & Williams (1975) native grassland and Solitary or as commonly found in and 2 well developed Reid et al. (1982) even exotic forest. breeding pair. varying amounts. caeca of equal length, McLennan (1988) Sea level to alpine Monogamous. each 19 em long. meadows. Nests underground. Total length of alimentary canal215-245 em. ON RATITES AND THEIR INTERACTIONS WITH PLANTS 93 traditionally associated with grassland and riinae), the single-wattled cassowary savanna formations where pastoralism (Casuarius unappendiculatus), the double- is the dominant land use (Fig. 5). It can wattled cassowary (C. casuarius) and the also be found in such extreme habitats as mountain or dwarf cassowary (C. bennetti), the Great Dividing Range in the east, even are quite distinct ecologically from the emu. above the snow-line (Davies 1976), and The cassowaries inhabit dense tropical dense mallee (Eucalyptus spp.) scrubland rainforest. In the rainforests of Cape York in southern Australia (Noble, pers. observ.). peninsula in Australia, only one subspecies The word "emu" is derived from the (C. casuarius johnsonii) occurs (Crome Portugese "ema" meaning cranelike which 1976), whereas all three species can be itself is derived from the Arabic "Naa- found in New Guinea (Fig. 3). Diamond mah" ( naema) meaning ostrich (McDonald ( 1972) has referred to one subspecies of 1986). the dwarf cassowary (C. bennetti shaw- There were originally three other species mayerz) resident in the Eastern Highlands living on coastal islands but these disap- of New Guinea. A large number of other peared in the first 150 years following subspecies have been superficially described European settlement. The black emu for many island populations of cassowaries (Dromaius ater, syn. D. minor), which was yet little is known about the influence of darker and smaller than D. novaehollandiae, sexual dimorphism or age changes on was discovered in 1802 on King Island diagnostic characters (Mayr & Cottrell (Grzimek 1972, Boles 1991). Two birds 1979). Any simple geographical discrimina- were shipped to Paris in 1804 and kept in tion of subspecies is dubious because it is a private zoo by the Empress Josephine; known that Melanesians take tame young the last died in 1822. The last known cassowaries with them on canoe voyages Tasmanian emu (D. diemenianus) survived between islands. until 1873 (Dove 1926, Boles 1991), while The birds are solitary in nature and are the species resident on Kangaroo Island quite aggressive, being the only ratites with (D. baudinianus) has only recently been sharp claws (Majnep & Bulmer 1977). They recognised (Parker 1984). develop a casque on the head ( Crome & The fossil record of the emus extends Moor~ 1988) which acts as a "crash helmet" back to the mid-Tertiary in central Australia protecting the eyes and cranium when with one species (D. ocypus) collected moving through dense forest or when used from Pliocene sediments (Rich & Balouet defensively (Carlquist 1974). The fossil 1984). More recently, another species record of the cassowary is sparse with only (D. gidju) has been described from Oli- a late-Pleistocene record of a pygmy gocene/Miocene deposits in central Aus- cassowary (Casuarius lydekkeri) from New tralia (Patterson & Rich 1987). Additional Guinea and an uncertain fossil from Austra- material of this small, gracile emu has been lia (Rich 1975, Rich & van Tets 1982, subsequently found from deposits of Rich et al. 1988). similar age in northwestern Queensland. This material prompted a systematic Kiwis revision by Boles ( 1991) describing the new genus Emuarius, formed by combining The kiwis (Apteryx australis, A. oweni and "Emu" and "Casuarius", because many of A. haasti) pose considerable systematic its features are intermediate between both problems and some workers have suggested taxa. closer relationships to the cosmopolitan rails (Rallidae) and tinamous (see Rich & Cassowaries Balouet 1984) than to the ratites. Based on the dates provided by the Although the emu and the cassowary are DNA-DNA hybridization clock of Sibley taxonomically allied (both belong to the and Ahlquist (1981), Diamond (1983) Casuariidae: Casuariiformes), the three postulated that the kiwi ancestor reached species of cassowary (Casuarius: Casua- New Zealand from Australia via an island 94 NOBLE

0.02 0.02-0.10 0.10-0.20 0.20 '\E) NS Not surveyed Fig. 5a: The distribution of emu-group density in the area surveyed by Grice et al. (1985). La distribuci6n de Ia densidad del grupo del emu en el area estudiada por Grice eta/. (1985).

100

Sheep pastoral] E t . X enSIYe Ca tile pastoral Grain growing ] . Intensive Other uses Not used commercially

--- May to October rainfall (mm) (;.in 8 yrs out of 10) Fig. 5b: land use zones in Australia (adapted from the Atlas of Australian Resources 1973). Zonas de uso del terreno en Australia (adaptado del Atlas de Recursos Australianos 1973). ON RATITES AND THEIR INTERACI'IONS WITH PLANTS 95 archipelago situated along the rises now North Island, four (Mega/apteryx didinus, bearing Norfolk and Lord Howe islands, Emeus crassus, Pachyornis australis and with the three species of kiwis diverging P. elephantopus) were endemic to the within the last 10 Myr. Nevertheless, dates South Island, while five species (Anoma- provided by this molecular clock still lopteryx didiformis, Euryapteryx geranoi- require futher calibration before they can des, Dinornis struthoides, D. novaezealan- be regarded as absolute (Howgate 1986). diae and D. giganteus) were common to The kiwis have been able to utilize a both islands. The moas apparently inhabited wide range of habitats including exotic primarily forests and their margins (Burrows pine forests and farm pasture, as well as et al. 1981, Anderson 1982) although rainforests and their margins. They are evidence suggests they used shrublands and essentially nocturnal feeders. There are subalpine areas as well (Atkinson & Green- three subspecies of the brown kiwi, each wood 1989, Worthy 1990). based on geographical location, viz. North Island brown kiwi (Apteryx australis mantelli), South Island brown kiwi (A. a. Mihirungs australis) and Stewart Island brown kiwi (A. a. lawryi). The little spotted kiwi Accounts of the evolution, and ultimate (A. oweni) was once widespread in both demise, of the Dromornithidae in Australia the North and South Islands but has not provide fascinating reading (e.g. Rich 1979, been recorded from the North Island for Rich & van Tets 1982, Rich & Balouet nearly a century (Reid & Williams 1975). 1984). While palatal evidence is still lacking, The great spotted kiwi (A. haasti) is found these birds may not have been ratites only in the South Island west of the (P. Rich, pers. comm.). These flightless southern Alps. birds were endemic to this country being unique in possessing hoof-like, ungual phalanges. Their most distinctive feature was their size, some being truly gargantuan EXTINCI' RATITE GENERA (Rich 1981) and they are probably the largest birds ever known standing more Moas than 3 metres high and weighing more than 5 00 kilograms. While the two groups of extinct moas (the Taxonomic studies (Rich 1979) have at Dinornithidae and the Emeidae) are closely this point identified four genera and seven related (Rich 1979), their relationship to species present in the Miocene (Bara- the kiwis remains unclear. These rela- wertornis tedfordi; Bullockornis planei and tionships are unlikely to be refined through a second species of Bullockornis not yet more detailed study of the fossil record named; Dromornis australis, D. stirtoni; since the oldest moa (Anomalopteryx Ilbandornis woodburnei, and I. lawsoni) antiquus) is late Pliocene and the oldest with only the Dromornis species surviving kiwi Pleistocene (Rich & Balouet 1984). into the Pliocene (Fig. 6). The only The moas, endemic to both main islands of dromornithid present in the Pleistocene New Zealand, were classified by Oliver was Genyornis newtoni which survived up ( 1949) under the six genera Anomalopte- until at least 26,000 years B.P. (Rich ryx, Dinornis, Emeus, Eurapteryx,Megalap- 1981), thereby overlapping with colonisa- teryx and Pachyornis. Oliver listed twenty- tion by Aborigines. nine species, but this total was later reduced by Cracraft ( 197 6) to thirteen species although neither classification has proved totally Elephant Birds acceptable (e.g. Caughley 1977, Trotter & McCulloch 1984). Worthy (1988, 1990) Until the dromornithids had been adequate- has subsequently described eleven species, ly described, it was generally assumed that two of which (Euryapteryx curtus and the elephant birds (Aepyornithidae) were Pachyornis mappini) were endemic to the the largest birds ever to have existed, some 96 NOBLE

Million years Epoch 0 26,000 , •• Pleistocene ,_..1 l...... _...~-::-:----~--- GENYORNIS ')j'-----1 Pliocene ROMORNIS I------1 e STIRTONI ILBANDORNIS I "' DROMORNIS I 11 BARAWERTORNIS DROMORNITHIDAE,I - EGG • BULLOCKORNIS Miocene SHELL ~ 1' ~ DROMORNITHIDAE. FOOTPRINTS I VARIETY UNKNOWN

Oligocene

25~-L----~------~

Fig. 6: Stratigraphic distribution of the Dromornithidae in Australia (after Rich 1981 ). Distribucion estratigrafica de las Dromornitidas en Australia (seglin Rich 1981). estimated to weigh from 450 kg (Amadon decreasing mesophytic forests covering 1947, Carlquist 1965). These birds were much of Australia in the Tertiary (Martin unusual taxonomically in having no clear 1982, Truswell & Harris 1982, Rich & relationship with any other ratites, some Balouet 1984). Even though Genyornis features being common to ostriches- newtoni overlapped with Aboriginal rheas and others similar to moas-kiwis occupation, it is uncertain whether hunting (Rich & Balouet 1984). The meagre fossil was a significant factor in its ultimate record of both genera (Aepyornis and disappearance (Rich 1981). Mullerornis) suggests that Aepyornis at one Extinction of the New Zealand moas stage inhabited the African continent at the however followed the arrival of Polynesian beginning of the Tertiary (Mahe 1972). man around 1000 A.D. Not only did Like the moas, elephant birds survived the clearing and extensive use of fire result Pleistocene with Aepyornis surviving longer in a dramatic reduction of forests, but than Mullerornis (Carlquist 1965). The first archaeological evidence from middens French governor of Madagascar, Flacourt, points to their use as a major source of initially described these "giant ostriches" food (Simmons 1968, Trotter & McCulloch with . one particular bird called Vouron 1984). Even the term moa, a Polynesian Patra, still frequenting the southern half of word for common fowl, denotes a culinary the island until the mid 17th century connection. Though some, like theDinornis (Grzimek 1972). species, were probably capable of running (Cracraft 1976), the large size and reduced mobility of these graviportal (walking) EXTINCI'ION AND INTERACI'ION WITH MAN species, must have made them easy prey. On the basis of moa-bone collagen and The dromornithids apparently became marine shell dating of moa-hunter sites, extinct following habitat destruction Caughley (1988) has calculated that moas through increasing aridity and the ever and Polynesians coexisted in any single ON RATITES AND THEIR INTERACTIONS WITH PLANTS 97 district for only about one century. In any burrows (Oliver 1955). They prized their event, by 500 B.P. they were so scarce as feathers for making the highly valued to be rarely hunted (Anderson 1984). Kahu-kiwi, a feather cloak. Europeans also The elephant bird was possibly the hunted kiwis extensively last century for most recent ratite to become extinct. Like their feathers which were used for feather the moa, its ultimate demise has been muffs in E1,1rope, one hunter killing more attributed solely to human activities, in- than 2000 birds in one season (Reid & cluding both direct predation and indirect Williams 1975) before they became fully destruction by burning of their forest protected. habitat (Battistini & Verin 1972). Exotic predators introduced by Eu- This lethal response to human activities ropeans have also imposed considerable has continued partially for the ostriches depredations on kiwi populations, high- with their extermination by hunting from lighting the vulnerability of these island North Africa, Egypt, Iran and Arabia. Their species to such predatores as the fox future in southern Africa at least seems (Vulpes vulpes), ferret (Mustela putorius), relatively secure following the establishment cat (Felis catus) and dog (Canis familiaris) of conservation areas and ostrich farms. (Diamond 1989). Taborsky ( 1988) do- The latter were set up initially in South cumented the case where a single dog killed Africa as early as 1838 (Mosenthal & 13 North Island brown kiwis (Apteryx Harting 18 77), and later in Algeria, Sicily, australis mantelli) out of a total of 23 France and Florida (USA), to fill a fashion carrying radio transmitters. The whole demand for hat feathers before later population may therefore have lost 500 out changing to leather production, 42,000 of 900 birds requiring 10-20 years of ostriches being kept for this purpose in rigorous protection from predation for South Africa as recently as 1970 (Grzimek complete population recovery to occur. 1972). The intermediate-sized rheas, cassowaries Ostrich farming was also attempted in and emus have also been significantly af- Australia from the 1860s unti11914 (Rolls fected by human activities. The rheas are 1969). Commercial flocks were run on seve- possibly the most vulnerable of the three at ral properties in western New South Wales the present time due to hunting for sport, including some near Deniliquin (Eastman loss of habitat by fencing, and replacement 195 3) and north of Swan Hill in Victoria of native pastures with exotic species for (Casey 1966), ostriches being fed mainly on cattle fodder (Bruning 1973). Unlike the irrigated alfalfa (Medicago sativa). The rheas, whose meat is relatively unattractive white wing feathers of the male bird, cut and plumage of little value, the cassowaries twice annually ( 1.4 kg/bird/cut), realized are highly valued by Melanesians for eating, c. A$57-79 per kg at that time (The Illus- and their feathers are also utilized for trated Australian News, December 23, headdress. There have been some attempts 1882). Commercial operations ceased in at domestication of cassowaries in the 1914 due to the outbreak of World War I, Highlands of New Guinea because of their France and Germany hitherto being the trading value, a fully grown cassowary in best markets. The price for ostrich feathers 1973 fetching up to A$400, exceeding by that time had fallen to 5 sovereings per the price paid for a pig or cow (Majnep & lb (c. A$30/1 b or A$66/kg at current Bulmer 1977). values). The greatest threat to the Australian Size alone does not predicate the cassowary lies in the destruction of tropical likelihood of extermination although the rainforest habitat for agriculture although larger forms are obviously more vulnerable several conservation areas have been to hunting. Even the smallest ratite has established in Cape York. Management been exploited in the past by humans. The problems in such reserves occur periodical- Maoris did not regard kiwis as an important ly following cyclone damage when much of food source, although they did periodically the cassowaries' food supply, particularly hunt them using dogs and digging up their in small rainforest remnants, is eliminated. 98 NOBLE

Because these have no natural corridors months, emus can consume significant linking them with other less damaged quantities of pasture-eating caterpillars reserves, conservation managers have to (Gooding & Long 1959). Large flocks of resort to supplementary feeding of cas- emus from the drought-stricken inland sowary populations until the rainforest would periodically invade marginal cropping regenerates (McKenzie 1986). Whilst the areas when cereal crops were ripening, conservation status of cassowaries in New resulting in one case in November 1932, of Guinea and other islands is unclear, army personnel being employed with Australian populations are relatively stable machine guns to shoot marauding flocks. at densities of I bird to -every 5 to 15 km2 In 1935, it was estimated that 86,000 had (Crome 1976). been killed in the Northampton district The emu has long been an important alone and as recently as 1970, the Western food source for Aboriginals (McCarthy Australian government paid bounties on 1965) who used narcotics derived from 24,479 emus (Riggert 1975). Landholders plants such as pituri (Duboisia hopwoodii- in Western Australia now have the right to Solanaceae) to drug water used by emus, destroy emus on their own properties but thus enabling the semi-comatose birds to elsewhere they are protected under the be easily trapped (Cunningham et al. Fauna Conservation Act. Since 1975, li- 1981). Europeans arriving in the First cences to farm emus have been granted at Fleet in February 1788 first named the two locations in Western Australia for the emu the New Holland cassowary (Stockdale commercial production of medicinal oil 1789). Hotham provided the first scientific and leather for high fashion clothing. name of Casuarius novaehollandiae (Stan- bury 1987). With the advent of Europeans, DIET, INTERNAL ANATOMY AND significant changes have occurred to emu GIZZARD STONES populations (Grice et a/. 1985). While numbers have undoubtedly declined in the The anatomy and physiology of the more closely settled areas of the continent alimentary canal and digestive system in through loss of habitat, there are probably birds have been described by Worden more emus present today than there were (1964) and Ziswiler and Farner (1972). prior to European colonisation in 1788 The gastric system in birds comprises two (Davies 1976). distinct chambers, an anterior glandular This increase can be primarily attributed stomach or proventriculus and a posterior to the additional watering facilities provid- muscular stomach or gizzard. The pro- ed for sheep and cattle in the pastoral areas ventriculus not only functions mainly as following closer settlement (Noble & a site for the secretion of gastric juices but Tongway 1986, Davies 1986). Emus require also as a storage area where limited peptide water daily, even in the winter except when digestion occurs. The gizzard remains the the males are incubating. When transient primary site of digestion, both for me- water-holes in the desert dry out, the birds chanical digestion and also digestion by may migrate en masse towards permanent acid proteolysis whereby proteins are re- waters in settled areas. Protection from duced to their constituent amino acids. canine predators following wild-dog The emu and the ostrich differ from trapping and the construction of dingo other ratites by having almost no crop, (Canis familiaris dingo )-proof fencing, also with only a slight swelling noticeable in the contributed to increasing emu abundance oesophagus (Davies 1978). The gizzard in in protected areas (Arnold 1941, Caughley these ratites is positioned so that the an- et al. 1980). terior entry in the left side and the poste- The emu is now a protected species in rior exit on the right side are both dorsal eastern Australia. In the 1930s, it was (Fig. 7). The dimensions of the gastro- regarded as a major pest in the wheatgrowing intestinal tract of the adult emu, and areas of Western Australia (Long 1965), characteristics of gut contents after despite the fact that, during the winter eating herbage, are shown in Table 3. ON RATITES AND THEIR INTERACTIONS WITH PLANTS 99

(a) Oesophagus any specialised chambers in the gut for fermentative digestion because of its large body size and low metabolic rate (Calder & Dawson 1978, Dawson & Herd 1983). The one internal organ likely to have the greatest impact in terms of plant-animal interactions, especially in relation to seed dispersal and germination, is the gizzard. In many birds, the muscular gizzard is

Ventriculus (gizzard) regarded as the analogue of mammalian teeth. Mechanical grinding of food particles in ratite gizzards is often aided by stones 0 Scm collectively held as an accesory grinding device at certain times. Such gastroliths can be extremely useful in the field to palaeontologists searching for the remains of extinct forms (see Table 4). Rich ( 1981) described the piles of small, rounded stones on the otherwise featureless surface of salt lakes in arid Australia which commonly overlaid the remains of mihirungs trapped in unstable sediments around 35,000 years ago. Gastroliths have also been conspicuous in preserved moa gizzards, individual stones measuring up to 9.6 em in length with an entire stone collection from a single Di- 0 Scm nornis weighing over five kilograms Fig. 7: Diagramas illustrating the gizzard region of (Burrows et al. 1981). Rounded quartz (a) an emu chick about 2 weeks old and (b) an stones, reputably moa gizzard stones, have ostrich chick about 4 weeks old. Both organs are been found overlying totally different shown as if the birds were standing upright with the front of the bird facing the right hand margin parent rock material at altitudes up to (after Davies 1978). 1700 min the Westland of the South Island (Atkinson & Greenwood 1989). Widespread Diagramas que ilustran Ia region de Ia molleja (a) un polluelo de emu de mas o menos 2 semanas y (b) un moa gastroliths were recorded last century polluelo de avestruz de mas o menos 4 semanas. Se in the scrublands of the North Island by muestran ambos organos como si las aves estuvieran pa- pioneer farmers and gumdiggers searching radas derechas con el frente del ave hacia el margen dere- cho (segun Davies 1978). for kauri (Agathis australis) gum. The ability to carry such stone loads internally was obviously enhanced by the A sophisticated digestive tract, based on size of these birds and the fact that they fermentation in extremely long intestines, were not required to fly. Other extinct can provide processing systems that ef- flightless birds including the dodo (Raphus ficiently and rapidly reduce plant cellulose cucullatus) and the solitaire (Pezophaps material. "Giant ground birds -rheas and solitarius) of the Mascarene Islands also ostriches- have tiny heads and no teeth possessed gizzard stones, one solitaire's whatever, yet these birds successfully gizzard containing a stone of "the size of employ rearward fermentation on a large a hen's egg" (Hachisuka 1953, p. 97). The scale" (Bakker 1987). The emu digests and dietary significance of gizzard stones is metabolises plant fibre through fermenta- uncertain and the presence of stones does tion within the ileum, the distal segment not necessarily imply, as Owen thought in of the small intestine (Herd & Dawson the case of the dodo (Hachisuka 1953), 1984). It can compensate for the lack of that a bird is granivorous. The gizzards of 100 NOBLE

TABLE 3

Dimensions of the gastrointestinal tract of the emu and characteristics of gut contents (after Herd & Dawson 1984) Dimensiones del conducto gastrointestinal del emu y caracterlsticas del contenido del intestino (segun Herd & Dawson 1984)

Dimensiona Gut Contentsb Total Relative Dry Length Length Weight Weight Matter Osmolality pHd Region (m) ('to) (g) ('to) ('to) (mosm. Icg-')

Oesophagous 0.76 17.1 23 0.7 6.0 340 6.8 Proventriculus 0.14 3.1 86 2.6 16.6 328 2.8 Gizzard 0.11 2.5 1,306 39.7 27.3 290 2.5 Duodenum 0.50 11.2 446 13.6 14.8 681 6.7 Jejunum 1.23 27.6 446 13.6 14.8 681 6.7 Ileum 1.42 31.9 1,260 38.3 12.4 367 8.2 Caecum 0.12e 5 0.2 30.6 Rectum 0.29 6.5 165 5.0 16.8 323 7.2

TOTAL 4.45f 3,291 a Body weight, b Body weight, c Plasma osmolality dpH values, eOne caecum f Excluding caeca 38.3 ± 2.2 kg 35.3 ± 2.1 kg 309 mosm. kg-' after Davies (n = 3) (n =3) (Skadhauge 1974) (1978)

Adelie penguins (Pygoscelis adeliae), whose the stone content increased suggesting diet is primarily marine, also contain stones replacement of ''vegetative stones" by (Emison 1968). Mineral grit can also be a "mineral stones". significant component of gizzard contents A similar replacement phenomenon has in waterfowl (Norman & Brown 1985, been reported for the digestive system of Norman & Mumford 1985). the North Island brown kiwi. After examin- The ostrich, when eating coarse ve- ing the gizzard contents of 50 brown getable matter, may carry up to 907 g of kiwis, Reid et al. (1982) found an inverse pebbles in its stomach, some 2.5 em in relationship between the number of seeds diameter (Thompson 1964). Stones have from drupes of the hinau tree (Elaeocarpus also been found in the proventriculus of dentatus-Elaeocarpaceae) and the quantity emus (Noble 1975)a) intimating that some or mineral grit (Figure 8). mechanical digestion may be occuring in this organ, although they may have been Temporal variation in mineral matter regurgitated from the gizzard when the content of emu gizzards in Western Austra- birds were shot. Proventriculus samples lia has been studied over 12 months by were obtained from emus feeding in two Davies ( 1978). He found a trend for the contrasting habitats on the Riverine Plain stone and gravel content to be low in the of southeastern Australia (Leigh & Noble cooler months and high in the warmer 1972), one a ripening wheat crop and the months (Fig. 9). The increase in gizzard other a low shrubland dominated by mineral content in the summer period fruiting nitre bush (Nitraria billardieri- indicated a major shift in diet composition. Zygophyllaceae). Emus feeding on the Since seeds were more commonly eaten wheat contained stones comprising up to during this period, a positive correlation 52.,. by weight of the total proventriculus may exist between seed and mineral gizzard contents whereas those feeding exclusively contents. Regression analysis however found on drupes of the nitre bush contained no only 41.,. of the variation in both variables stones in December and January (Table 5). could be attributed to this relationship As the nitre bush component declined, so (Fig. 10). TABLE 4

Mineral matter recorded in either the ventriculus (gizzard) or proventriculus of different ratites. Materia mineral registrada ya sea en el ventrfculo (molleja) o proventrfculo de diferentes nitidas.

0 Max. stone "fo stone "fo stone Largest Maximum z weight per (weight) per (weight) per stone stone := gizzard (g) gizzard proventriculus weight (g) Ratite length Geology Reference >>-l contents contents (mm) ::i tr1 fl' z> t::l Emu 98 n.a.* 52 n.a n.a Qaystone Noble (1975a) >-l :z: (Drorruzius novaehollandiae) 76.3 n.a 45.8 36.4 Davies (1978) tr1 30.0 Herd & Dawson (1984) ;;;

North Island Brown Kiwi 20.2 n.a n.a 8.8 n.a n.a Reid et al. (1982) z>-l (Apteryx australis rruzntelli) :=tr1 > Mihirung 400 n.a n.a n.a n.a Jasper, siliceous Rich & Van Tets ~ (Genyornis newtoni) sandstone, (1982) 0 claystone and fl'z quartz ~ Moa > 5,000 1.9 n.a 56 96 Quartz Oliver (1949) :z: (Dinornis, Emeus & Euryapteryx spp.) 4,380 "D Gregg (1972) t'"' Burrows et al. (1981) ~ Trotter & McCulloch (1984) >-l fl' 24.2 4.81 n.a n.a 15 Quartz Eastman (1953) Ostrich Thompson (1964) (Struthio came/us) 907 25 Robinson & Seely (197 50

Mountain Cassowary n.a n.a n.a n.a n.a Quartz Majnep & Bulmer (1977) ( Casuarius bennett!)

* Not available. -0 102 NOBLE

TABLE 5

Emu diets (Of. dry weight of proventriculus contents) on two contrasting vegetation types (after Noble 1975a). Dietas del emu (Of. de peso seco del contenido del proventr{culo) en dos tipos contrastantes de vegetaci6n (segiln Noble 1975a).

(a) Nitre bush

December January February (n = 5) (n = 5) (n = 4)

Nitre bush fruit (seed & pericarp ± S.E.) 96.4 ± 1.5 94.8 ± 1.3 58.6 ± 20.5 Stones 0 0 3.1 Other 3.6 5.2 38.3

(b) Wheat crop

December January Mean (n = 6) (n = 5) (:t S.E.)

Wheat grain 15.2 16.8 16.2±7.0 Wheat rachis 2.0 5.8 4.4 ± 2.0 Charcoal 7.4 15.5 12.6 ± 4.2 Stones 46.2 52.3 50.1 ± 8.0 Other 29.2 9.6 16.5 ± 4.0

~ 25 The nature of the diet may also influence the distribution of food residues throughout the gastrointestinal tract. More than half the mass of gut contents resided in the gizzards of emus feeding primarily on Nitraria fruit (Table 6), even in February when Nitraria comprised only 59% of the diet (Noble 1975a), unlike those feeding § 5 solely on herbage when less than half the .§ .." contents was held in this organ (Table 3). :::E Unfortunately there is a dearth of information detailing the internal anatomy 0 5 10 15 20 25 30 35 Number of Elaeocarp.!!§ dentatus seeds per gizzard of the rhea. There are few published reports, if any, of any rhea x plant interac- Fig. 8: The relationship between seed content of tions. Rheas apparently are not very hinau (Elaeocarpus dentatus) and weight of grit efficient at digesting either grasses or seeds in gizzards of the North Island brown kiwi (D. Bruning, pers. comm.). (Apteryx australis mantelli). The exponential curve was fitted from data of Reid et a/. (1982) and is defmedas y = 19.58e- 0.11 x (r2 = 0.99). SEED GERMINATION FOLLOWING DISPERSAL La relaci6n entre el contenido de semilla de hinau (Elaeo- carpus dentatus) y el peso de granos de arena en las BYRATITES mollejas de Kiwi Pardo de la Isla Norte (Apteryx australis mantelll). La curva exponencial fue ajustada segiln los datos de Reid et a/. (1982) y se define como In any plant's life history, the germination 0 11 Y = 19.58e- • x (r2 = 0.99). and seedling establishment phase (ecesis) ON RATITES AND THEIR INTERACIIONS WITH PLANTS 103

220

200

180 70

160 60 ' % I 140 50 .....• § ~ :0 i 120 0 = ~ ..E ci 100 30 ~ ..c:: :i 80 ~0

60 10

40 0 J F A J J A s 0 N D Month Fig. 9: Mean monthly weight of organic fraction(± S.E.) and percentage mineral fraction in gizzards of emus (Dromaius novaehollandiae) (after Davies 1978).

Peso mensual medio de Ia fracci6n organica ( ± S.E.) y el porcentaje de fracci6n mineral en mollejas de emus (Dromaius novaehollandiae) (seg(ln Davies 1978).

70 studied before valid conclusions can be ...... • ~ 60 • drawn about any "adaptive" significance 'E • of plant x animal interactions (Howe & 50 • 'E.. • 0 Smallwood 1982). (.) • • .. 40 Ratites, like many granivorous and 'E 30 frugivorous birds, are important seed ::::E 20 dispersal agents (Table 7). Unlike many ~.. c:: 10 other birds however, they add a further ':i dimension to seed dispersal. Not only can 0 0 1 0 20 30 40 50 60 70 they carry large internal seed loads over

Seed Content (%) considerable distances but they may also confer some selective advantage on the Fig. 10: The relationship between seed and mi- diaspore that is dispersed by enhancing neral contents of emu gizzards. The logarithmic curve was derived from data of Davies (1978) germination in "safe sites" (Harper 1965). and defmed as: y = 39.92 + 4.58 1nx (r 2 = A series of germination experiments 0.41). conducted with both emu-ingested and La relaci6n entre el contenido de semilla y el mineral non-ingested seed of nitre bush indicated en mollejas de emu. La curva logaritmica fue derivada de such selective advantege through emu datos de Davies (1978) y defmida como: y = 39.92 + 2 dispersal (Noble 1975b, Noble & Whalley 4.58 1nx (r = 0.41). 1978b). Germination was significantly increased by emu ingestion (67"fo compared is critical. The most hazardous period of with only 17"fo of hand-collected seed after seedling life occurs at this transition 24 days) while germination was also much between dependence on seed reserves and quicker (50-. vs. 3"fo in four days). This independent assimilation (Harper 1977). improved germination was attributed pri- Seed development and dispersal, and the marily to removal of the epicarp and establishment of seedlings, must all be mesocarp of the nitre bush drupe during 104 NOBLE

TABLE 6

Internal partitioning of Nitraria fruit and endocarp in emu guts (n = 6) over one fruiting season (after Noble 1975a) Division interna del fruto y endocarpio del Nitraria en los intestinos del emu (n = 6) durante una estaci6n frutal (segun Noble 1975a).

Oesophagous and Proventriculus Gizzard Intestine Total

Weight Weight Weight Weight (g) (g) (g) (g)

December 87.9 32.3 173.4 63.6 11.2 4.1 272.5

January 102.1 28.0 169.0 46.4 93.1 25.6 364.2

February 11.0 21.2 39.1 75.2 1.9 3.7 52.0

Mean 67.0 29.2 127.2 55.4 35.4 15.4 229.6

digestion by the emu, chemical analysis of 2.5-3.2) whereas the intestine and colon this tissue indicating high concentrations of were neutral to alkaline (pH 6.7-7.2). Such both sodium (0.4"1o) and chloride (3.5"1o). variations in acidity/alkalinity cannot be The osmotic potential created by pericarp easily related to any changes in germination residues on non-ingested seed creates major behaviour. The marked improvement in germination problems, demonstrated by nitre bush seed germination following soaking hand-collected seed in distilled defaecation by the emu also was partly water and then using the leachate as a attributed to the removal of autotoxic moisture source for seed germinating in residues, as yet unidentified, in the en- petri dishes. This leachate contained 416 docarp following diurnal variations of ppm sodium and 7 56 ppm chloride and temperature and moisture content in the severely depressed germination of emu- emu dropping (Noble 1975b). ingested seed (Figure II). Numerous, often subtle, factors interact Improved germination may also result to determine whether a site is suitable for from grinding of the nitre bush endocarp germination. The potential values to plants in the gizzard, thereby increasing per- of having only few seed dispersers depend meability and subsequent imbibition by the on both the treatment of the seeds and embryo. To determine whether such how they are deposited (Wheelwright & scarification occurred only in the gizzard, Orians 1982). Faecal deposition of seeds by the germination of nitre bush propagules ratite dispersers such as the emu and the collected from different organs in the cassowary enhances germination by provid- emu's alimentary tract was compared ing a relatively large and homogeneous with faecal and hand-collected controls. microenvironment. When large seeds are After 21 days, there was no significant not dispersed by suitable agents, they may difference in germination of seed col- have difficulty imbibing sufficient water for lected from either the proventriculus germination due to the low ratio of seed (5.00fo), gizzard (4.5"1o) or intestine (0.5"1o); surface to volume (Harper et al. 1970). in fact, there was a decline in germination The quantity of material voided by a ratite of seed taken from the emu gut, though in one dropping is sufficient to provide an non-significant, when compared with the organic matrix enveloping the dispersed hand-collected seed ( 13.50fo). seed thereby optimising seed imbibition, Davies ( 1978) found the proventriculus particularly in exposed sites, once this ma- and gizzard of the emu to be acid (pH trix has been saturated by rainfall. TABLE 7

Plant species whose propagules are dispersed by ratites. Especies de plantas cuyos reproductores son dispersados por las ratidas.

0z ~ >o-j Content weight ::j Fruit of fully trl rn Ratite Plant species Family Life Fruit diam. Seed distended Form type (mm) weight (g) gizzard (g) Reference >z 0 o-j ::I: Cassowary BeilschmiediJJ sp. Lauraceae Tree Berry 60 52 n.a* Stocker & Irvine (1983) trl Ekleocarpus angustifoluis Elaeocarpaceae Tree Drupe 45 n.a. n.a. Stocker & lrvine (1983) -~ E. bancroftii Elaeocarpaceae Tree Drupe 45 n.a. n.a. Stocker & lrvine (1983) zo-j t'l1 Emu Nitraria bilklrdieri Zygophyllaceae Shrub Drupe 5 0.05 280 Noble (1975b) ~ Santalum acuminatum Santalaceae Ttee Drupe 25 2.3 n.a. Noble (unpubl. data) S. spicatum Santalaceae Tree Drupe 25 2.3 n.a. Davies (1978) ~ EremophikllongifoliJJ Myoporaceae Shrub Drupe 8 n.a. n.a. Cunningham et al. (1981) -0z Petalostigma pubescens Euphorbiaceae Shrub Drupe 25 5.0 n.a. Qifford & Monteith (1989) rn !l Kiwi Ekleocarpus dentatus Elaeocarpaceae Tree Drupe 15 1 49 Reid et at. (1982) o-j E. hookerianus ::I: Elaeocarpaceae Tree Drupe n.a. n.a. n.a. Reid et al. (1982) '"d Podocarpus dacrydioides Podocarpaceae Tree Nut n.a. n.a. n.a. Reid et al. (1982) t"' P. totara Podocarpaceae Tree Nut n.a. n.a. n.a. Reid et al. (1982) > Dacrydium cupressinum Podocarpaceae Tree Nut n.a. n.a. n.a. Colbourne & Powesland (1988) rn?i Pentachondra pumikl Epacridaceae Shrub Nut n.a. n.a. n.a. Colbourne & Powesland (1988)

Moa Podocarpus spicatus Podocarpaceae Tree Nut n.a. n.a. n.a. Burrows eta/. (1981) P. dacrydioides Podocarpaceae Tree Nut n.a. n.a. n.a. Burrows et al. (1981) Ekleocarpus hookeriJJnus Elaeocarpaceae Tree Drupe n.a. n.a. n.a. Burrows eta/. (1981)

* Not available. -~ 106 NOBLE

cassowary dropping contained 13 fruit of a Beilschmiedia species, each with a dia- /e···-·-·-·---·-·-· meter of c. 5 em and weighing 52 g (Stocker •• & Irvine 1983). Another enclosed several seeds of Elaeocarpus bancroftii whose fruit ~ had a diameter of 4.5 em. c 0 A feature of the studies by both Crome ~ -~ 10 ( 1976) and Stocker and Irvine ( 1983) was

Cl the preponderance of drupaceous fruit in 5 the cassowary diet. Whilst the fruit of some species such as Abrophyllum ornans (Saxifragaceae) and Apodytes brachystilis (lcacinaceae) are technically not classified ,.....-o-o--o--o--o as drupes, they nonetheless have many of 0 their characteristics (FHJ Crome, pers. 0 5 10 15 20 25 30 35 Time (days) comm.). One of these is the ability of the diaspore to pass through the digestive Fig. 11: The influence of distilled water (solid symbols) and fruit leachate (hollow symbols) on tract of the cassowary relatively undama- the germination of hand-picked (squares) and ged. The large-fruitedBeilschmiedia "berry" emu-ingested seed (circles) of nitre bush (Nitra- described by Stocker and Irvine ( 1983) ria bil/ardieri) (after Noble 197Sb ). Lines were passes through the cassowary more or less only fitted for the distilled water treatments and intact. are defmed as follows: The fruit of two New Zealand species of Beilschmiedia, viz. tawa (B. tawa) and emu-ingested (solid circles): taraire (B. tarairi), are both classified as 10-0.4182 drupes (Allan 1961), those of taraire log y 73.0 x (r2 0.96) = (x-.1 2 ) = having mean dimensions of 31 x 16 mm. Seeds of both these lauraceous species hand-picked (solid squares): require high humidity, moderate tem- 10-2.14 perature and passage through the digestive log y = 21.7 x ---(r2 = 0.96) system of the New Zealand pigeon (Hemi- (x-3) phaga novaeseelandiae) for maximal germination to occur (Myers 1984, West La influencia del agua destilada (sim bolos solidos) y lixiviadores frutales (simbolos huecos) sobre Ia germina- 1986). Myers (1984) found that seed ci6n de Ia semilla del arbusto nitre (Nitraria billardieri) ingested by captive pigeons gave signi- recogida a mano (cuadrados) y Ia ingerida por los emus ficantly higher germination than intact (circulos) (segun Noble 1975b). Las Hneas se ajustaron solamente para los tratamientos de agua destilada y se seed collected from the forest floor ( 86% vs. defmen de Ia manera siguiente: 13% in 1982 and 95% vs. 58% in 1983). While rate of germination of pigeon- ingerida por emus (circulos s6lidos): ingested seed was significantly higher than ..0.41112 logy = 73.0 x 10-- (r2 = 0.96) that of other seed, higher germination (x-L') resulted when fruit was collected directly recogida a mano (cuadrados s6lidos): from the tree instead of from the ground. -2.14 2 In tropical ecosystems, dispersal of tree logy = 21.7 x 10-- (r = 0.96) (x-3) seeds by the terrestrial cassowaries occurs through a combination of gravichory when Germination of extremely latge seeds ripe fruit first falls to the ground, and has been observed in cassowary droppings endozoochory, when the fallen fruit is (M~nep & Bulmer 1977, Stocker & Irvine later ingested by the disperser. The reverse 1983). Cassowaries are the only extant applies to smaller, non-ratite frugivores like frugivores with sufficient capacity, and gape the New Zealand pigeon which first ingest width, to effectively disperse many of the the fruit directly from the tree canopy fruits of tropical rainforest species. One before gravichory then occurs as seed is ON RATITES AND THEIR INTERACTIONS WITH PLANTS 107 voided directly on to the ground beneath 150° favoured roosting trees. •1 0°~-==-==-==-==-=-=-----+-1 0° Cassowaries probably play a similar role to the New Zealand pigeon in enhancing the germination of seed from large-fruited species of Australian rainforests. Such species are prominent in the Lauraceae, a family of particular importance in the cassowary diet. Crome ( 1976) found that fifteen species of this family accounted for 19"fo of all dietary items recorded. Cas- sowaries also facilitate short-distance dispersal of large diaspores such as those of Beilschmiedia spp. (Fig. 12), to either higher ground or ecotonal forest fringes. Longer Tropic of Capricorn distance dispersal is likely to be infrequent if, as with Beilschmiedia fruit eaten by the New Zealand pigeon, the time taken from ingestion to defaecation is only 2-3 hours, sufficient time nonetheless for the fleshy mesocarp to be stripped from the fruit. 20/570 (3.5%) Short passage times suggest that it is unlikely that enhanced germination can be attributed to increased permeability of the endocarp because little time would be available for grinding within the gizzard. Several factors, including the presence and 1/160 absence of stones, may dictate the duration of the diaspore passage through the bird's (0.6%) gut. In their digestibility trials with captive emus fed diets differing in fibre content, Herd and Dawson ( 1984) found that mean 150% retention time was 4.1 h for the liquid fraction and 5.5 h for the particulate frac- Frg. 12: Estimates of the number (and percentages) tion. Grain can also pass through the emu's of large-fruited species in the woody rainforest gut in 3 hours although most food appears flora of eastern Australia (after Stocker & Irvine to take from 6-26 hours (Davies 1978). 1983). Cassowaries (Casuarius casuarius johnsonii) When surrogate stones in the form of glass are now only found in the two northernmost marbles were fed to emus, 84-100 days regions. elapsed . before several were evacuated in a Oilculos estirnativos del numero (y porcentajes) de espe· heavily abraded condition having lost up cies de frutos grandes en Ia flora maderera de Ia selva de Australia oriental (segun Stocker e Irvine 1983). Los to 28"fo of their original weight. casuarios (Casuarius casuarius johnsonii) se encuentran This abrasion within the gizzard may be ahora solamente en las dos regiones extremas del norte. biologically significant for seeds ingested by emus during the summer when gizzard mineral content is high. Many of the seeds large quantity of seeds and pods of Acacia eaten by emus at this time are leguminous, albida (17.4-t. by weight) and stones (31.2%) such as Acacia species (Davies 1978), and (Robinson & Seely 1975). The gizzard may germinate more readily following contents of another ostrich however abrasion and weakening of the strophiolar contained no legume seeds despite a large region of the seed's testa (Ballard & Grant quantity of stones being present. Seeds of Lipp 1965). The gizzard contents of one hinau (Elaeocarpus dentatus) have been ostrich in South West Africa comprised a taken from kiwi gizzards where the nor- 108 NOBLE mally rough endocarp has been worn plant, providing it occupies a suitable "gap" smooth (Reid et al. 1982). These ap- amongst established plants. parently had been retained as grinding aids Interspecific competition from cool- for extensive periods and germination of season annuals, especially annual medics viable seed may have been significantly (Medicago spp.) as shown in Plate 2, was improved following defaecation. also a major regulatory influence four to six months after the onset of germination (Noble & Whalley 197 8b ). Hand weeding IMPLICATIONS FOR SEEDLING ESTABLISHMENT of all annuals within individual plots resulted in 8% of the original seedling Dense seedling populations in a faecal population of Nitraria surviving for eight dropping of an emu or cassowary rapidly years. After four years, even the weeded induce self-thinning through intraspecific populations showed a marked decline in competition for "biological space" (Ross density as shown by the hazard functions & Harper 1972). Because individual Ni- calculated as -loge (1 - p) in Fig. 13. traria hummocks may attain dimensions up Hazard functions are derived by to 3 x 13 m in horizontal plan (Noble & computing the probability of death of a Whalley 1978a), substantial mortality must seedling of Nitraria billardieri in either occur. Up to 1000 Nitraria seeds have been treatment in a given time interval. For found in a single faecal deposit of c. 15 em each treatment, there is a pair (n, r) of diameter (see Plate I) so that even if only recorded numbers: n being the number 50% of germinated, seedling density of shoots alive at the beginning of the time would be at least 15 cm-2 (Noble 1985). interval and r being the number of these Only the earliest, and most vigorous, shoots that die during that time interval. seedlings will ultimately assume dominance The probability p of death in that time and develop into a mature, reproductive interval is estimated by p = r/n and the

Plate 1. Seedlings of Nitraria billardieri emerging from an emu dropping on a clay soil in southwestern Australia. (Reference: approx. 5 em wide). Brotes de Nitraria billardieri emergiendo de una defecaci6n de emu sobre suelo de arcilla en Australia suroccidental. (Referencia: aprox. 5 em de ancho). ON RATITES AND THEIR INTERACTIONS WITH PLANTS 109

Plate 2: Seedlings of Nitraria billardieri struggling to survive strong competition from annual herbage composed mainly of annual medics (Medicago polymorpha and M. truncatula). The scale is shown in 2.5 em intervals. Brotes de Nitraria billardieri luchando por sobrevivir Ia fuerte competencia del herbaje anual compues- to principalmente de medicagos anuales (Medicago polymorpha y M. truncatula). La escala se muestra en intervalos de 2.5 em.

50 model used (Bartlett & Noble 1985) has the form: loge [-loge (1 - p)] = time component+ treatment component. These functions, together with seedling survivorship data (Noble 1985), illustrate that established plants of Nitraria billardieri are close to maximum carrying capacity (K). Suc- cessful recruitment of seedlings can therefore only occur on a one-for-one basis following the death of an established individual (Harper 1977). Gut retention times obviously have a significant influence on the post-dispersal seed shadow generated by dispersal agents on the simple prediction that the longer the seed is retained in the gut, the higher the 0 01 · o 40 80 120 160 200 240 280 probability that long-distance dispersal will Time (weeks) prevail. However, once frugivores have Fig. 13: Hazard functions or age specific failure stripped seed of their nutritious pericarp, rates for weeded (hollow circles) and non-weeded there is no further advantage in carrying (solid circles) seedlings (1973 cohorts) of nitre "ballast" which is heavy and space con- bush (Nitraria billardieri) in southeastern Austra- suming (Snow 1971). Emus feeding on fruit lia. of Nitraria billardieri concentrate faecal Tasas de funciones por azar o falla espedfica debida a Ia deposits around female fruit-bearing plants edad para brotes desmalezados ( clrculos huecos) y no- desmalezados (circulos s6lidos). (197 3 conjuntos) de with minimal dispersal of seed. The fluid arbustos nitre (Nitraria billardieri) en Australia suroriental. nature of the faeces suggests low gut reten- 110 NOBLE tion times probably induced by the high Examination of preserved moa gizzards water content of the fruit (see Plate 3 ). has revealed that seeds from a wide range Undoubtedly some seeds are periodically of plant species were also an important deposited in favourable sites some distance component of the moa's diet including away from mature plants but seed dispersal those from drupes of Elaeocarpus hooke- curves would be highly skewed. rianus (Burrows 1980). Moas, particularly Where ratites are selectively eating Dinornis spp., specialized by feeding on flowers, browsing may influence fruit twigs of shrubs, vines and trees to a much production. Robinson and Seely (1975) greater degree than extant ratites (Burrows reported large quantities of Acacia giraffae eta!. 1981, Atkinson & Greenwood 1989), flowers in ostrich gizzards. Greenwood grouse (Lagopus and Tetrao spp.) being and Atkinson (1977) claimed that browsing the only other birds habitually feeding on of shrubs by moas in New Zealand had a twigs. Different species of moa may have strong selective influence on their mor- utilised distinct niches distinguished by phology with divaricate shrubs (Tomlinson differences in feeding height, bill shape 1978) now comprising nearly 10% of that and gizzard development. Moas could country's woody flora. The relative evo- digest this woody material because of the lutionary significances of moa browsing strong musculature of the massive gizzard and climate in this respect are open though and enclosed gastroliths (Atkinson & to speculation (McGlone & Webb 1981, Greenwood 1989). In this context, the Wardle 1985). Compared with other ratites, large gizzard stones associated with mihi- the moas were unique in having the ca- rungs suggests that these birds may have pacity to browse twigs and leaves of such also browsed woody plants. shrubs, presumably selecting buds and Atkinson and Greenwood (1989) have young leaves because they were both more recently completed a comprehensive digestible and more nutritious than those analysis of the evidence for the co-evolu- on older twigs (Lowry 1980, Atkinson & tion of certain moa traits such as increased Greenwood 1980). cutting power of the bill, increased gizzard

Plate 3: Emu faeces composed almost entirely of seeds of Nitraria billardieri. The pur- gative action of the fruit is clearly evident. Heces de emu compuestas casi totalmente de semillas de Nitraria billardieri. La acci6n purgante de Ia fruta es c1aramente evidente. ON RATITES AND THEIR INTERACTIONS WITH PLANTS 111

:levelopment, and increased height inter zlia, and the evolution of at least 11 :lifferent growth habits in native plants. fhe main benefit possibly to be derived by tree seedlings from ratite browsing is the suppression of rapidly growing understorey species which would otherwise interfere with their regeneration. Wardle (1985) has discussed the possible role of mea- browsing in promoting the regeneration of podocarp-dominant forests. Any evidence for co-evolution between fruit ingestion by moas and subsequent seed dispersal and seedling development traits is, however, likely to be less compelling. The fruit of one podocarp species, Podocarpus spicatus, was found to occur frequently in the gizzard contents examin- Trampling & ed by Burrows et al. ( 1981) indicating that selective browsing they may also have acted as dispersal agents for these conifers. The mihirungs may have had a similar dispersal role within the Ter- tiary rainforests which covered most of what is now arid Australia (Martin 1982). Fig. 14: A simple model illustrating the various The pollen record includes such conifers influences of ratite activities on seed germination as Podocarpus, Dacrydium and Phyllocla- and seedling establishment. dus (Truswell & Harris 1982). It appears Un modelo simple que ilustra las diversas influencias de unlikely that contemporary forest ratites las actividades de las nitidas en Ia germinaci6n de las se- have a critical role in the establishment of millas y establecimiento de los brotes. coniferous seedlings, only a single seed of Podocarpus dispermus being found in germination sites. Similarly, trampling by Australian cassowary dung (Stocker & ratites appears to be of little significance in Irvine 1983). determining the fate of seedlings although the larger extinct ratites such as the moas, elephant birds and mihirungs, may have EVIDENCE FOR MUTUALISM created "light gaps" in forests because of their sheer size, but only if they fed in flocks Putative relationships between plants and which is uncertain. Moas were more likely ratites are portrayed in Fig. 14. Whilst to forage singly or in small groups (Atkinson simplistic, this model highlights the eco- & Greenwood 1989), possibly to avoid logical significance of the ratite faecal predation by the enormous forest eagle microsite in promoting rapid germination Harpagornis moorei (Braithwaite & and seedling establishment of woody plants Holdaway 1987). in habitats ranging from xeric shrublands Despite the limitations imposed by a and grasslands to humid rainforests. worldwide paucity of contemporary plant Indirect influences such as the predation and ratite data, ecological studies of the of insects and trampling are relatively two Australian ratites, the emu and the unimportant in terms of seedling establish- cassowary, suggest that both birds have ment. Whilst all extant ratites are omni- had a significant influence on vegetation vorous, there is no reliable evidence indicat- history in certain habitats. Wheter or not ing that predation of insects has any they have had an even longer influence significant bearing on the establishment of over geological time is uncertain but seedlings, either within or without faecal Truswell and Harris (1982) refer to fruits 112 NOBLE

of Santalum spp. being found in Miocene content of endosperm and embryo tu sup- deposits in arid South Australia. They port subsequent seedling growth. Seed pre- suggested that the genus Santalum was dators act as a dependent variable by select- therefore a late migrant into arid regions ing instead for increased thickness of endo- originating from stocks in coastal rainforests. carp (Smith 1975). If this is so for ratite Whether this migration was facilitated by predators, gut retention time may need to emu or other ratite dispersal is unknown increase to compensate if gizzard scarifica- although there is no doubt about the tion of the endocarp is important for pro- modern emu's predilection for ripe fruit moting postdispersal germination. As men- of Santalum species. tioned earlier, experimental evidence tends Many of the fruits eaten by ratites have to refute this hypothesis. evolved traits characteristic of ornithochory Extensive recruitment of seedlings of (van der Pijl 1972). Such features as an Nitraria billardieri cannot occur on heavy attractive edible part, signalling colours soils such as those found on the Riverine when mature, and inner protection of seed Plain of south-eastern Australia in the against digestion, can be applied to most of absence of emus. Prior avian ingestion of the fruit consumed by Australian cas- fruit is however not obligatory for suc- sowaries (Stocker & Irvine 1983) and emus cessful germination to occur in sandy (Noble & Whalley 1978a). Here dispersal is substrates. It has also been alleged (Sargent endozoochorous when whole fruits are 1928) that seeds of the zamia palm (Ma- ingested by the disperser and the seed crozamia fraseri) in Western Australia, eventually regurgitated or defaecated un- often larger in size than a walnut, will only damaged (van der Pijl 1972). Whilst the germinate after they had been eaten by dispersal "syndrome" of bird-dispersed the emu however this has since been found propagules includes several attributes, not to be obligatory. Herrera ( 1981) has also pointed to the What is critical in the case of Riverine importance of matching external fruit size, Plain Nitraria billardieri is that speed of particularly of tropical species, to the gape germination is significantly increased enabl- widths of avian dispersal agents. Snow ing seedlings to rapidly establish them- (1973) has described the disproportionate- selves while moisture conditions remain ly wide gape of some tropical frugivores favourable within the faecal microsite and such as some Cotingidae, a family of small surface soil. Similar constraints must also South American passerines, as constituting apply to cassowary-dispersed seeds which an adaptation to feeding on large-seeded require quite specific moisture, and fruits. probably light, conditions for successful Whether there has been coevolution by seedling recruitment. Some Beilschmiedia emus and Nitraria with both acting as species for example, not only require the selective forces on each other, is uncertain. removal of the fruit's mesocarp by appro- In his study of coevolution between plants priate dispersal agents but also the main- and avian dispersers in Mediterranean tenance of high moisture, either within a Spain, Herrera ( 1982) found definite large faecal dropping of a cassowary, or support for the hypothesis that fruit alternatively, burial beneath forest leaf quality traits evolved to meet disperser litter (Knowles & Beveridge 1982, Wright demands. He found that fruit that ripen 1984 ). Such seedlings are unable to tolerate during the dry Mediterranean summer, like the effects of direct sunlight unless very Nitraria billardieri, when water demands of high moisture conditions are maintained. dispersers were highest, also had the There is no evidence available suggesting highest water content. that any plant-ratite mutualism exists si- Selective forces are distinguished accord- milar to that proposed by Temple (1977) ing to whether they act either as dependent for the near-extinct tree Calvaria major of or independent variables. The physical en- Mauritius and the extinct dodo (Raphus vironment generally acts as an independent cucullatus) although recent observations variable by selecting for optimum energy suggest that these seeds can germinate ON RATITES AND THEIR INTERACTIONS WITH PLANTS 113 without ingestion (1. Atkinson, pers. shown to enhance winter reproduction of comm.). Nonetheless, the semantics of the introduced Australian possum (Tri- mutualism are complex. The term itself is chosurus vulpecula) in broadleaf-podocarp often applied to obligatory associations forests in New Zealand (Belll981 ). Whether while protocooperative associations are the fruit has similar demographic signifi- facultative (Hallam 1980). Although there cance for kiwi populations is unknown may be exceptions, symbiotic mutualisms although the preponderance of hinau fruit tend to be coevolved and obligate whereas in some kiwi gizzards suggests that there facultative mutualisms are frequently non- could be considerable nutritional benefit symbiotic and not coevolved (Bourcher for these birds when fruit is abundant et al. 1982). In his scheme for classifying (Reid et al. 1982). biological associations, Starr (197 5) de- Observations of large emu flocks (up to fined mutualism as a "mutually beneficial 80 birds) feeding on fruit of Nitraria billar- symbiosis", a definition which would apply dieri (Noble 1975a) demonstrated that the to those ratite and plant relationships emu is an apostatic generalist feeder or where there was a positive gain at both feeder that concentrates on the source of trophic levels. food in greatest supply at any point in Absolute dependence in mu tualistic as- time, leaving this when the supply becomes sociations of temperate zone systems can limiting (Harper 1969). Data on the food be often too costly, due to prolonged quality of native drupes is limited but the winter breaks. Bristow in May (1982) nutritional value of both N. billardieri and claimed that " ... temperate zone mutualisms Elaeocarpus dentatus fruit is not insignifi- are rarely obligate, but rather than by rely- cant (Table 8). N. billardieri fruit particular- ing on simple environmental cues and beha- ly, in terms of both its nutrient and water vioural mechanisms a high degree of fine tun- contents, provides a valuable source of ing may be achieved with almost no loss of fresh food during summer (December- flexibility". The ratio of energetic reward of February). When fruit production of the fruit pulp, or mesocarp in the case of N. billardieri has been reduced following drupes, to the indigestible seed is equivalent poor insect pollination in wet springs in temperate and tropical fruit (Herrera (Noble 1985), the catholic tastes of emus 1981 ). The real difference is that many (Davies 1978) enable them to find al- tropical fruits have large seeds and corre- ternative summer food sources. spondingly rich pulp while most temperate In the tropical rainforests of northern fruits have small seeds and smaller nutri- Australia, the cassowary breeding season tional rewards (Howe & Smallwood 1982). coincides with the period of maximum It is the quality, as well as the quantity, fruit production from July through to of the fruit as a food source which determi- October (Crome 1976) (Fig. 15). Fruits nes the demographic significance of any produced by species from the Lauraceae frugivore -or omnivore- plant association. are particularly important in this respect, Nevertheless, studies indicate that the rich not only because they produce most of mesocarp pulps commonly found in tro- their fruit during this period but also pical fruits are not necessarily related to because the fruit itself is highly nutritious close coevolution between large-seeded (Crome 1976, Stocker & Irvine 1983). The plants and their "specialised" dispersers mesocarps of some lauraceous species (Snow 1971, McKey 197 5, Howe & contain 8-14% protein and 19-44% fat, Estabrook 1977). Data on the composition with water contents ranging from 54-75% of Elaeocarpus dentatus drupes in New (Snow 1962). Crome (1976) found protein Zealand are shown in Table 8a. This tree contents (% fresh meso carp) of two lau- produces heavy fruit crops which may last raceous species, Endiandra montana and for several months through the autumn E. muelleri, to be 0.77 and 2.89% respective- and winter (Fitzgerald 1976). Because of ly. Elaeocarpaceae is another important its high nutrient status, and especially as a family in the cassowary diet and the source of available energy, it has been protein content of the mesocarp of Elaeo- 114 NOBLE

TABLE 8(a)

Composition (dry weight basis) of the mesocarp of hinau (Elaeocarpus dentatus) fruit in New Zealand (after Williams 1982) Composici6n (en base al peso seco) del mesocarpio del fruto del hinau (Elaeocarpus dentatus) en Nueva Zelanda (seg(m Williams 1982).

Available Water Methanol Crude Crude fibre carbohydrate soluble -soluble Gross protein Lipid Ash (acid detergent) (N.F.E.*) sugars sugars energy % % % % % % "'o kJg-1 3.4 1.7 3.2 21.8 69.9 10.0 2.9 18.0

* Nitrogen-free extract

TABLE 8 (b) Comparative composition of entire nitre bush (Nitraria billardieri) fruit at different stages of maturity in southeastern Australia (after Noble & Whalley 1978a). Composici6n comparada del fruto entero del arbusto nitre (Nitraria billardien), en diferentes etapas de maduraci6n en Australia suroriental (segun Noble y Whalley 1978a).

Soluble solids Titratable acid Vitamin C Maturity %sucrose (% w/v as citric) pH (mg/100 ml)

Immature (green-yellow) 15.5 1.73 3.9 Near-ripe (bright red) 16.7 0.96 4.3 8 Fully ripe (red-purple) 18.5 0.78 4.6

KEYWORDS: Ratites = nitidas. size = tamafio distribution = distribuci6n habitat = habitat. Exactly the same as in English but it is not a widely known word. For this reason I put "medio ambiente natural" (natural environment)- habitat" the first time the word appears in the abstract. seed dispersal = dispersion de las semillas. seedling establishment = establecimiento del brote (1 seedling), establecimiento de los brotes (more than 1 seedling).

OJ FMAMJ JASONDJ FM J J J F M A 1971 1972 Fig. 15: The relationship between breeding seasons of the Australian cassowary ( Casuarius casuarius johnsonii) and fruit production in tropical rainforest (after Crome 1976). The stippled area represents the amount of fruit available and bars represent breeding season. Arrows represent known hatching dates while the broken arrow indicates the suspected hatching date of one chick. La relaci6n entre las estaciones de reproducci6n de los casuarios (Casuarius casuarius johnsonii) y Ia producci6n frutal en Ia selva tropical lluviosa (segun las barras representan Ia estaci6n de reproducci6n). Las flechas representan las fechas conocidas de incubacion, mientras que Ia flecha quebrada indica Ia fecha sospechada de incubacion de un polluelo. ON RATITES AND THEIR INTERACTIONS WITH PLANTS 115

:arpus grandis (1.64%) recorded by Crome BALLARD LAT & AE GRANT LIPP (1965) Germina- tion of subterranean clover seed in relation to 1976) is not dissimilar to that recorded for some softening procedures. Proceedings of the S'. dentatus (Table 6a) given differences in International Seed Testing Association 30: 893- noisture content. 904. Because all the extant ratites are essential- BARTLETT NR & JC NOBLE (1985) The population biology of plants with clonal growth. III. Analysis ly omnivorous, it is unlikely that their of tiller mortality in Carex arenaria. Journal of 1ssociations with plants, particularly those Ecology 73: 1-10. producing drupaceous fruit, are obligatory BATTISTINI R & P VERIN (1972) Man and the environment in Madagascar. In: Battistini R & G Richard- ;ymbioses. They do nonetheless, have the Vindard (eds) Biogeography and evolution in ~apability to exploit periodic abundances Madagascar. Dr. W. Junk, The Hague: 311-337. BEER G de (1956) The evolution of ratites. Bulletin Jf such food sources, either for reproductive of the British Museum (Natural History) 4: 1-63. Jr simply maintenance purposes. BELL BD (1981) Breeding and conditioning of possum Few studies of plant dispersal systems Trichosurus vulpecula in the Orongorongo Valley near Wellington, New Zealand. In: Bell BD (ed) ilave actually demonstrated increases in Proceedings of the first symposium on marsupials ~ither fitness or population growth rate in New Zealand. Zoology Publication N° 74. )y organisms at either trophic level (Boucher Victoria University of Wellington: 87-139. BERTRAM BCR (1980) Breeding system and strategies ?t al. 1982, Wheelwright & Orians 1982). of ostriches. Proceedings of 17th International fhis general lack of specificity in seed Ornithological Congress: 890-894. :lispersal conforms to the hypothesis BOCK WJ (1963) The cranial evidence of ratite affinities. Proceedings of the 13th International Ornithological :Howe & Smallwood 1982) that coevolu- Congress: 39-54. tion reflects adaptation to arrays of similar BOLES W (1991) Revision of Dromaius gidju Patterson & Jrganisms rather than to particular species. Rich 1987 from Riversleigh, northwest Queens- land, Australia, with a reassessment of its generic position. Contributions to the Los Angeles County ACKNOWLEDGMENTS Museum of Natural History (in press). BOUCHER DH, S JAMES & KH KEELER (1982) The Several colleagues have read previous drafts of this paper ecology of mutualism. Annual Review of Ecology md their assistance is gratefully acknowledged. Particular and Systematics 13: 315-347. BRAITHWAITE DH & RN HOLDAWAY (1987) A preli- thanks however are extended to Drs Graeme Caughley, minary reconstruction of Harpagornis moorei: Ian Atkinson, Wal Whalley and Pat Rich for their detailed md constructive comments. Dr. Walter Boles kindly top predator in the moa's world. 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